B

Babesia Bacillus sphaericus

A genus of Protozoa that is transmitted to animals colin berry by ticks. Cardiff University, Cardiff, Wales, United  Babesiosis Kingdom  Piroplasmosis The bacterium Bacillus sphaericus is best-known to entomologists because of the toxicity of some Babesiosis strains to the larval stages of mosquitoes. This tox- icity will be examined below but first, some con- Several related diseases caused by infection sideration of the taxonomic group that is known with Babesia protozoans, and transmitted by as “Bacillus sphaericus” is necessary. ticks.  Piroplasmosis Taxonomy

Identification of a bacterium as aB. sphaericus iso- Bacillary Paralysis late is based on relatively few morphological fea- tures (e.g., the possession of a spherical terminal A disease of silkworm larvae caused by ingestion spore) and a limited number of biochemical tests of spores and parasporal crystals of Bacillus (e.g., inability to ferment sugars). As a result, the thuringiensis. classification contains a heterogeneous collection of strains and it has been shown that, at the DNA level, these can be divided into five major homol- Bacillus larvae (=Paenibacillus ogy groups (groups I-V), each of which could be larvae; Bacteria) considered as a separate species. All of the insecti- cidal strains of B. sphaericus are found within a The bacterium responsible for causing American subdivision of one of these groups – Group IIA; foulbrood in honey bees; it is now known as however, not all strains that fall within this group Paenibacillus larvae. are insecticidal. It is the insecticidal strains of  American Foulbrood B. sphaericus and their properties that will be con-  Paenibacillus sidered further below. 346 B Bacillus sphaericus Target Range The Insecticidal Toxins

Bacillus sphaericus is toxic to a small range of dip- Insecticidal strains of B. sphaericus owe this teran target insects, principally mosquitoes (with property to the fact that they produce protein some possible activity against Chironomus spe- toxins. To date, several different types of toxins cies). Within the mosquitoes, B. sphaericus is often have been identified. The names of these toxins, seen as most active against Culex species with along with notes on their mechanisms of action, lower activity against Anopheles, Mansonia and are given in the table below. Psorophora and lowest activity against Aedes spe- All the toxins except sphaericolysin exert cies. However, these generalizations should be their effects on the gut of the aquatic larval form treated with caution as some Aedes species are as of the mosquito after ingestion of the bacterium. sensitive as Culex species so that susceptibility The binary toxin (Bin) is produced on sporula- must be judged at the species level and not by tion whereupon it is deposited in spore-associ- genus. In addition, activity of a B. sphaericus toxin ated crystal As shown in the figure of B. has been reported against the German cockroach, sphaericus, (Fig. 1) the spore is the round body at Blattela germanica. the top, the crystal is the grey, rhomboid body in the center, and both are contained within the elongated exosporium. Once eaten by a mos- quito larva, the crystal dissolves and its two com- Field Use ponent proteins (BinA -42 kDa and BinB -51 kDa) are able to bind to ­specific receptors in the Bacillus sphaericus strains have been used in gut before lysing the cell by pore formation. control programs worldwide to suppress mos- Note: although the Bin proteins form a spore quito populations that are of nuisance or public associated toxin crystal, they are not related to health importance. For this purpose, only strains the majority of the crystal-associated Cry and showing high-level, spore-associated toxicity Cyt toxins of Bacillus thuringiensis. Most highly are used (e.g., VectoLex® and Spherimos® from toxic B. sphaericus strains produce only the Bin Valent BioSciences, or Sphaerus® from Bthek toxin in association with spores (Mtx toxins are Ltda). For production of maximum toxicity, as produced only in vegetative cells and in very low well as for ease of production and storage, such quantities). The existence of only one toxin in formulations are produced from fully sporu- spores applied in mosquito control programs in lated B. sphaericus ­cultures that can be sprayed the field can lead to resistance in target popula- or applied as blocks or granules that disperse in tions. A few strains of B. sphaericus can over- the aqueous habitats. come this resistance in Culex mosquitoes. These

Bacillus sphaericus, Table 1 Toxins of Bacillus sphaericus Toxin (molecular wt.) Mechanism of action Reference Bin (51 and 42 kDa) Pore formation Oei et al. (1992), Schwartz et al. (2001) Mtx1 (100 kDa) ADP-ribosylation Thanabalu et al. (1993) Mtx2 (31.8 kDa) Pore formation Thanabalu and Porter (1996) Mtx3 (35.8 kDa) Pore formation Liu et al. (1996) Cry48/Cry49 (136 and 53 kDa) Pore formation Jones et al. (2007) Sphaericolysin (53 kDa) Pore formation Nishwaki et al. (2007) Bacillus sphaericus B 347 References

Ahmed I, Yokota A, Yamozoe A, Fujiwara T (2007) Proposal of Lysinibacillus boronitolerans gen. nov. sp. nov., and trans- fer of Bacillus fusiformis to Lysinibacillus fusiformis comb. nov. and Bacillus sphaericus to Lysinibacillus sphaericus com. nov. Int J Syst Evol Microbiol 57:1117–1125 Jones GW, Nielsen-Leroux C, Yang Y, Yuan Z, Dumas VF, Mon- nerat RG, Berry C (2007) A new Cry toxin with a unique two-component dependency from Bacillus sphaeriucs. FASEB J 21:4112–4120 Krych VK, Johnson JL, Yousten AA (1980) Deoxyribonucleic acid homologies among strains of Bacillus sphaericus. Int J Syst Bacteriol 30:476–484 Liu J-W, Porter AG, Wee BY, Thanabalu T (1996) New gene from nine Bacillus sphaericus strains encoding highly conserved 35.8-kilodalton mosquitocidal toxins. Appl Environ Microbiol 62:2174–2176 Nielsen-LeRoux C, Rao DR, Murphy JR, Carron A, Mani TR, Hamon S, Mulla MS (2001) Various levels of cross- resistance to Bacillus sphaericus strains in Culex pipiens (Diptera: Culicidae) colonies resistant to B. sphaericus strain 2362. Appl Environ Microbiol 67:5049–5054 Nishiwaki H, Nakashima K, Ishida C, Kawamura T, Matsuda K (2007) Cloning, functional characterization, and mode of action of a novel insecticidal pore-forming toxin, sphaericolysin, produced by Bacillus sphaericus. Appl Environ Microbiol 73:3404–3411 Oei C, Hindley J, Berry C (1992) Binding of purified Bacillus sphaericus binary toxin and its deletion derivatives to Culex quinquefasciatus gut: elucidation of functional binding domains. J Gen Microbiol 138:1515–1526 Schwartz J-L, Potvin L, Coux F, Charles J-F, Berry C, Bacillus sphaericus, Figure 1 Bacillus sphaericus. ­Humphreys MJ, Jones AF, Bernhart I, Dalla Serra M, Menestrina G (2001) Permeabilization of model lipid (Photo courtesy of Dr. J.F. Charles.) membranes by Bacillus sphaericus mosquitocidal binary toxin and its individual components. J Membr Biol 184:171–183 Silva-Filha MH, Nielsen-LeRoux C, Charles J-F (1999) Iden- strains produce a novel toxin pair, Cry48/Cry49, tification of the receptor for Bacillus sphaericus crystal which are deposited as crystals outside the exo- toxin in the brush border membrane of the mosquito sporium. The Cry48 protein is related to 3-do- Culex pipiens (Diptera: Culicidae). Insect Biochem Mol Biol 29:711–721 main Cry toxins of B. thuringiensis while Cry49 Silva-Filha M-H, Regis L, Nielsen-LeRoux C, Charles JF is related to the Bin proteins. Both components (1995) Low-level resistance to Bacillus sphaericus in a are required for toxicity to Culex larvae and do field-treated population ofCulex quinquefasciatus (Dip- not appear to kill other insects (including Anoph- tera: Culicidae). J Econ Entomol 88:525–530 Thanabalu T, Berry C, Hindley J (1993) Cytotoxicity and eles and Aedes mosquitoes). ADP-ribosylating activity of the mosquitocidal Despite reports of resistance developing in toxin from Bacillus sphaericus SSII-1: Possible roles mosquito populations, careful use of this bacte- of the 27- and 70-kilodalton peptides. J Bacteriol rium is likely to enable the continued favorable 175:2314–2320 Thanabalu T, Porter AG (1996) A Bacillus sphaericus use of this product for integrated control programs gene encoding a novel type of mosquitocidal toxin in the field. of 31.8 kDa. Gene 170:85–89 348 B Bacillus thuringiensis Yuan Z, Zhang YM, Cai QX, Liu EY (2000) High-level field farms. Additional B. thuringiensis isolates have been resistance to Bacillus sphaericus C3–41 in Culex detected in various insectaries, stored product envi- ­quinquefasciatus from Southern China. Biocontrol Sci Technol 10:41–49 ronments, and grain processing facilities. Studies have suggested that B. thuringiensis is a normal inhabitant of the foliage of plants. However, the soil Bacillus thuringiensis habitat has been the primary source for isolating novel B. thuringiensis isolates. Whether or not B. thu- Bacillus thuringiensis was initially described early ringiensis undergoes saprophytic development in in the 1800s as the causal agent of the “sotto bacil- soil is unclear. Many bacilli ­considered to be close lus disease” of the silkworm Bombyx mori. Later relatives of B. thuringiensis are known to inhabit studies by Aoki in 1915 demonstrated that this hypogean environments. Presently, it has been esti- bacterial agent produced a crystalline toxic mate- mated that over 60,000 isolates of B. thuringiensis are rial at sporulation. In 1911, Berliner isolated the being maintained in culture collections worldwide. type species Bacillus thuringiensis var. thuringien- Members of B. thuringiensis are rod-shaped sis from the flour moth in the province of Thurin- (1.0–1.2 by 3–5 microns), gram positive, facultative gia, Germany. Following this report, a series of anaerobes which utilize carbohydrates as preferred papers demonstrated that B. thuringiensis could energy sources. Classification based on 16S rRNA infect and kill a variety of lepidopteran host insects. sequence data clusters B. thuringiensis with B. cereus, Until the 1970s, all B. thuringiensis isolates were B. mycoides, and B. anthraxis within the B. subtilus characterized as being toxic to immature insects group. Bacteriological tests define B. thuringiensis within the order Lepidoptera. However, today var- isolates as being closely related to B. cereus. In fact, the ious B. thuringiensis subspecies have been identi- ability of B. thuringiensis to produce the crystalline fied which are lethal to lepidopterans, dipterans, inclusion is the major feature that separates it from coleopterans, and/or nematodes. B. cereus. Acrystalliferous strains of B. thuringiensis Historically, Bacillus thuringiensis has been iso- generated by plasmid curing are nearly identical to lated from environments associated with insect B. cereus. The growth of B. thuringiensis on relatively

populations and/or plant material. For example, B. simple media (0.1% glucose, 0.2% NH2SO4, 0.2% thuringiensis was discovered initially in silkworm yeast extract) is biphasic and involves both a

Bacillus thuringiensis, Figure 2 Electron micrograph of thin section of sporulating cell of Bacillus thuringiensis. Note the thick-walled endospore and endotoxin-containing crystalline inclusion. Bacillus thuringiensis B 349 ­vegetative cell division phase and a sporulation B. thuringiensis resistance is the same as that phase. During sporulation, B. thuringiensis pro- required for resistance to the neurotoxic ­insectides: duces both the (Fig. 2) endospore and crystalline a multigenerational (continuous) exposure of the inclusions. The endospore, highly resistant to envi- host to the mortality agent. With B. thuringiensis, ronmental stress, provides a mechanism for long- this may be achieved either by a conventional term survival of B. thuringiensis. This mesophilic spray ­program or by a contiguous planting of B.t.- bacterium can be produced easily on solid media or transgenic plants. under submerged fermentation conditions. The Early work on the mode of action of the rapid growth and sporulation of B. thuringiensis in δ-endotoxin addressed the effect of extracted relatively inexpensive media under submerged fer- inclusions on lepidopteran larvae. Initial symp- mentation conditions have been key factors in its toms, occurring within one hour of ingestion of successful development as a biopesticide. Many of inclusions, include a cessation of larval feeding the advances made in the fermentation industry and gut paralysis. The endotoxin-induced gut over the past three decades have improved the paralysis retards passage of ingested plant material quality of B. thuringiensis products. and spores, allowing spores to germinate and Initially, it was presumed that the B. thuringi- undergo vegetative development. At later stages, ensis was an infectious agent and much effort was intoxicated larvae display a general paralysis spent on maximizing the delivery of bacterial ­followed by death within one to two days post- spores to host insects. Early field experiments in challenge. Histological studies demonstrated that the 1960s involving applications of spore-based the toxins released from inclusions and proteolyti- formulations against pest insect populations cally activated in the gut lumen specifically target ­produced erratic results. By the 1970s, it was dem- the midgut columnar cells. Examination of midgut onstrated that the primary insecticidal activity of tissue dissected from treated larvae initially B. thuringiensis against lepidopteran hosts was due revealed that columnar cells are slightly swollen to the δ-endotoxins comprising the crystalline but over time goblet and columnar cells become inclusions. These endotoxins are extremely potent heavily vacuolated. At the late stages, midgut cells and are toxic to target insects at picomole concen- dislodge from the basement membrane and are trations. However, with certain insects such as the sloughed off. At subcellular levels, the δ-endotoxins larvae of the Indian meal moth Plodia interpunc- produce pores in the membrane. The activated tella, the addition of spores synergizes the activity toxin recognizes specific cell membrane receptors of the δ-endotoxins. Potentially, this synergism is and then generates small pores in the cell mem- due either to additional toxins in the spore coat or brane. The subsequent depolarization of the to the outgrowth of vegetative cells from ingested columnar cell stimulates the closure of the gap spores. Many commercial formulations contain- junctions, causing an increase in intracellular pH ing high levels of δ-endotoxin have proven to be as and cell hypertrophy. Without a functional colum- effective as chemical insecticides yet exhibit high nar cell, the K+ pump in goblet cells ceases to func- specificity to target pests without detrimental tion. Intoxicated cells, due to increases in internal effects on beneficial insects and animals. By the pH and loss of ion transport, become osmotically 1990s, B. thuringiensis-based products represented sensitive and lyse. more than 90% of the biopesticides used world- Importantly, the δ-endotoxins are primary wide. Until the 1980s, it was proposed that micro- translation products of bacterial genes and are bial-based products such as B. thuringiensis, unlike amenable to genetic engineering techniques. By their chemical pesticide counterparts, did not the early 1980s, U.S. and European laboratories select for resistance in treated insect populations. had successfully isolated, cloned, and character- The critical element required for the selection of ized genes ­coding for δ-endotoxins. During the 350 B Backswimmers past two decades over 90 different protoxin genes Bacterial Conjugation containing representatives of both Cry and cyt classes have been cloned and sequenced. The A temporary union between two bacteria, during ­technology developed to study the structure and which genetic material is exchanged. All or some function of the δ-endotoxin has provided the of the chromosomes are transferred from the foundation for the genetic engineering of this class donor to the recipient of biopesticides. In several respects, the δ-endotoxin gene has played a pivotal role in agricultural ­biotechnology. The δ-endotoxins derived from Bacterial Wilt of Corn recombinant bacteria represent the first group of genetically engineered products released into agri- This is an important insect-transmitted disease of cultural systems. To date, recombinant microbes corn (maize). expressing δ-endotoxin genes have been field  Transmission of Plant Diseases by Insects tested worldwide in numerous agricultural sys- tems. ­Secondly, the δ-endotoxin genes have been used as models for optimizing the gene expression Bacterial Wilt of Cucumbers in transgenic plants. Over the past decade, researchers have manipulated the δ-endotoxin This is an important insect-transmitted disease of gene and have altered the protoxin profile as well cucurbit crops. as the ­toxicity and ­specificity of individual Cry  Transmission of Plant Diseases by Insects ­toxins. Significantly, Cry gene expression in trans- genic plants has ­provided protection against insect herbivory Bacteremia

The presence of bacteria in the hemolymph or blood References of invertebrates and other animals without produc- tion of harmful toxins or other deleterious effects Aronson A (2002) Sporulation and δ-endotoxin synthesis by Bacillus thuringiensis. Cell Mol Life Sci 59:417–425 Fieltelson JS, Payne J, Kim L (1992) Bacillus thuringiensis and beyond. Bio/Technology 10:271–276 Bacteriophage Knowles BH, Dow JA (1993) The crystal δ endotoxin ofBacil - lus thuringiensis: models for their mechanism of action A virus whose host is a bacterium on the insect gut. Bioassays 15:469–476 Maagt RA, Bravo A, Crickmore N (2001) How Bacillus thur- ingiensis has evolved specific toxins to colonize the insect world. Trends Genet 17:193–199 Whiteley HR, Schnepf HE (1986) The molecular biology of Bacteriophage Wo parasporal crystal body formation in Bacillus thuringi- ensis. Annu Rev Microbiol 40:549–576 jason m. meyer, marjorie a. hoy University of Florida, Gainesville, FL, USA

Backswimmers Bacteriophages are obligate intracellular viruses that infect and kill bacteria. These viruses are ubiq- Members of the family Notonectidae (order uitous and shape aspects of bacterial ­population Hemiptera). ecology in almost every environment on earth.  Bugs Bacteriophage WO infects the alpha-proteobacterium Bacteriophage Wo B 351 Wolbachia, which is commonly associated with appears that both Wolbachia and bacteriophage insects, mites, nematodes, and terrestrial isopods. WO are horizontally transmitted between different Wolbachia is notorious for causing reproductive arthropod species by unknown mechanisms. This is alterations in its hosts such as feminization, male supported by evolutionary studies showing incon- killing, cytoplasmic incompatibility, and parthe- gruence between phylogenetic trees constructed nogenesis. The diversity of Wolbachia strains and using DNA sequences from Wolbachia and bacterio- their influence on host biology has stimulated phage WO. Interestingly, some insects host multiple research encompassing broad topics including strains of Wolbachia that are infected with different genetics, ecology and evolution. In addition, types of bacteriophage WO, and even individual removing obligate Wolbachia infections from strains of Wolbachia can harbor multiple phage types. filarial nematodes has provided a novel treatment Wolbachia has a broad and dynamic host range that for human disease. The significance of both basic may be facilitated by the horizontal transfer of and applied research involving Wolbachia has made ­virulence factors it acquires from ­bacteriophage WO. it one of the most well understood endosymbiont- In 2000, the first bacteriophage WO was host associations. ­completely sequenced using DNA isolated from Virus-like particles (bacteriophage WO) were the Mediterranean flour mothEphestia kuehniella discovered inside Wolbachia cells in the reproduc- Zeller (Lepidoptera: Pyralidae) infected with tive tract of the mosquito Culex pipiens using ­Wolbachia. A total of 33 open reading frames were ­electron microscopy in 1978. Bacteriophage WO detected among a genome of approximately particles are approximately 40 nm in diameter 25,000 base pairs of DNA. The open reading with short tails, contain linear double-stranded frames ­represent the DNA coding information DNA, and are found near the Wolbachia cell mem- that ­dictates the construction and assembly of brane. Since its discovery, researchers have focused proteins. Some of the putative ­proteins identified on characterizing the basic biology, distribution, were related to proteins known from a diverse and evolution of bacteriophage WO. group of other bacteriophages, while others Bacteriophage WO has both a lysogenic phase, showed no significant similarities to known phage where its genetic information is integrated into proteins. Additional bacteriophage WO types the Wolbachia chromosome as a prophage, and a have since been sequenced using DNA isolated lytic phase, where the virion resides in the from ­Wolbachia infecting the almond moth, ­cytoplasm and can lyse Wolbachia cells. Little is Cadra ­cautella Walker (Lepidoptera: Pyralidae), currently known about what triggers the virus to and from Wolbachia infecting Drosophila mela- kill Wolbachia. Bacteriophage WO may prevent nogaster ­Meigen (Diptera: Drosophilidae). excessive proliferation of Wolbachia, and this may Using the polymerase chain reaction (PCR), have evolutionary implications for long-term the putative minor capsid protein gene, orf7, is maintenance of the association with the host. commonly used to detect bacteriophage WO in Bacteriophage WO is transmitted transovarially Wolbachia strains infecting arthropods. More inside arthropod eggs along with its host ­Wolbachia than 100 orf 7 sequences of bacteriophage WO cells. This transmission mechanism ­provides an have been deposited in GenBank as of May 2007. ­efficient and stable means for Wolbachia and its Theorf 7 gene has been detected in many, but not ­associated bacteriophage WO to infect arthropod all, Wolbachia-infected arthropods. Using species populations at a high frequency. This notion is representing multiple orders of arthropod hosts, ­substantiated by the similarity of the G + C content between 70 and 100% of the Wolbachia strains and codon usage of phage and ­Wolbachia genes, tested are PCR-positive for bacteriophage WO. indicating a long-term evolutionary tie between However, multiple Wolbachia-infected species bacteriophage WO and Wolbachia. ­However, it also of parasitoids in the genus Trichogramma 352 B Baculoviridae (Hymenoptera: Trichogrammatidae) and the Baculoviridae parasitoid Diaphorencyrtus aligarhensis Shafee, Alam and Agarwal (Hymenoptera: Encyrtidae) A family of insect pathogenic viruses known as lack bacteriophage WO. In addition, the nema- baculoviruses. todes Dirofilaria immitis, Litosomoides sigmodon-  Baculoviruses tis, Setaria equine and Brugia malayi, and a population of the predatory mite Metaseiulus occidentalis (Nesbitt) all had Wolbachia infec- Baculoviruses tions but lacked bacteriophage WO, based on PCR analysis of the orf7 gene. The insect baculoviruses, the nucleopolyhedrovi- In vitro cultures of Wolbachia must be ruses (NPVs) and the granuloviruses (GVs), are ­maintained using insect cell cultures because the most intensely studied insect viruses. Histori- the endosymbiont is intracellular. Currently, no cally, the first reports of a baculovirus-induced methods have been developed to transform viremia were associated with the silkworm (genetically modify) Wolbachia that would ­Bombyx mori. The spread of sericulture from Asia ­provide a tool to study its interactions with to Europe led to the introduction of the affiliated arthropods in detail. ­Bacteriophage WO has the diseases grasserie or jaundice disease (NPV), as potential to be developed as a vector to geneti- well as flacherie (non-occluded virus, bacteria), cally modify ­Wolbachia because it integrates into the silk-producing regions. In the sixteenth into the Wolbachia genome and its genes are century poem titled “De bombyce,” Marco Vida actively expressed. describes the rupture of tissues and the release of  Sex Ratio Modification by Cytoplasmic Agents fluid from diseased silkworm larvae. It is presumed  Symbionts of Insects he is describing the last stages of B. mori NPV-­ induced jaundice. In 1856, the Italian scientist ­Maestri made the first scientific observation of References the causal agent of jaundice. With the aid of the compound microscope, he described the presence Braquart-Varnier C, Grève P, Fèlix C, Martin G (2005) of polyhedral bodies (Fig. 3) or occlusions in the ­Bacteriophage WO in Wolbachia infecting terrestrial isopods. Biochem Biophys Res Commun 337:580–585 fluid and tissues of diseased silkworm larvae Fujii Y, Kubo T, Ishikawa H, Sasaki T (2004) Isolation and By the late 1890s, J. Bolle reported that the ­characterization of the bacteriophage WO from ­Wolbachia, polyhedral bodies were proteinaceous crystals an arthropod endosymbiont. Biochem ­Biophys Res Commun 317:1183–1188 resistant to various solvents but sensitive to Masui S, Kamoda S, Sasaki T, Ishikawa H (2000) Distribution ­alkaline solutions. Bolle reported that healthy and evolution of bacteriophage WO in Wolbachia, the ­silkworms that fed on the polyhedral bodies con- endosymbiont causing sexual alterations in arthropods. tracted jaundice. The intracellular inclusions J Mol Evol 51:491–497 Masui S, Kuroiwa H, Sasaki T, Inui M, Kuroiwa T, Ishikawa H described initially by Bolle as Microsporidium (2001) Bacteriophage WO and virus-like particles in polydricum were named later by Prell as Crystal- Wolbachia, an endosymbiont of arthropods. Biochem loplasma polyhedricum. Glaser and Chapman, who Biophys Res Commun 283:1099-1104 in 1916 reported that the infectious agent was a Gavotte L, Henri H, Stouthamer R, Charif D, Charlat S, Boulétreau M, Vavre F (2007) A survey of the bacterio- filterable agent of dimensions much smaller phage WO in the endosymbiotic bacteria Wolbachia. than the micron-sized polyhedral bodies, ques- Mol Biol Evol 24:427–435 tioned the infectious nature of the polyhedral ­bodies. Hoy MA, Jeyaprakash A (2005) Microbial diversity in the preda­ tory mite Metaseiulus occidentalis (Acari: Phytoseiidae) They and others proposed that the polyhedral and its prey, Tetranychus urticae (Acari: Tetranychidae). bodies were metabolic by-products and not causal Biol Control 32:427–441 agents of the disease. The nature of the polyhedral Baculoviruses B 353

Baculoviruses, Figure 3 Scanning electron micrograph of occlusion bodies of the nucleopolyhedrovirus depicting their three dimensional shape.

bodies and capsules finally was resolved in the similar disease in the larvae of the variegated cut- 1940s by the German scientist G. Bergold. He and worm, Peridroma margaritosa, the first report of co-workers examined alkali-treated baculovirus this disease outside of France. To date, granulosis inclusions under the newly developed electron viruses have been found to infect only lepidopteran microscope and described the occluded, rod-shaped hosts. These viruses are considered to be among virus particles. the most specific insect viruses, capable of­infecting In the late 1930s, the French scientist A. Paillot a single species or species within the same genus described a new type of viral disease in the Prior to their identification, baculoviruses cabbage butterfly, Pieris brassicae, that, unlike the were recognized as important natural regulators NPVs, produced numerous minute capsules of various lepidopteran defoliators. At the end of ­(granules). Using high-speed centrifugation, Paillot the nineteenth century in central Europe, nun and co-workers determined that the infectious moth (Lymantria monacha) populations were entities were associated with the granules in the decimated periodically by a wilt disease. Prior high-speed pellets. Paillot observed that this viral to death, infected insects migrated to the tops disease, termed pseudo-grasserie, multiplied in (Wipfeln) of the trees, attached by their prolegs, the fat body and caused infected larvae to exhibit and died. Upon death, the body disintegrated and a whitish coloration. In the early 1930s, he released infectious fluid. Initially, the causal agent described a similar disease in the cutworm Euxoa of the disease, known as Wipfelkrankheit, was segetum that caused nuclear hypertrophy of described as a bacterium, then later as a protozoan infected fat body cells followed by the formation within the genus Crystalloplasma. Although it was of the granules. In 1947, Steinhaus discovered a not properly named, a great deal was learned from 354 B Baculoviruses these early studies of this disease agent. Experi- of a baculovirus. In Canada, the European pine ments showed that the infectious material resisted sawfly, Neodiprion sertifer, was introduced and putrification and was stable for 3 years when stored became established as a major forest defoliator. in a dry state. Furthermore, the disease agent In the early 1950s, T. Bird (Canadian Forest Ser- ­persisted in the soil and could be extracted from vice) reported that a sawfly virus imported from washings using differential centrifugation. This Sweden was highly virulent to N. sertifer larvae. agent was transmitted per os; the fluid released The introduction of this virus resulted in wide- from the cadavers was highly infectious to healthy spread epizootics that spread through the sawfly larvae. Finally, it was reported that the infectious population and provided a natural control of agent displayed specificity to certain insect­species. this defoliator. This virus, unlike the lepidopteran For example, the fluid released from diseased nun baculoviruses, was transmitted easily from moth larvae was infectious to the related gypsy infected adults to the egg stage. The combination moth, Lymantria dispar, but was harmless to of its high virulence and ability to be vertically ­silkworm larvae. Throughout the 1920s, a program transmitted were responsible for its ability to in Europe promoted the spread and distribution provide effective long-term control of this pest of the causal agent into disease-free areas. This insect. The natural occurrence of baculovirus involved a variety of tactics, including the use of epizootics and their potential to be manipulated mortars to deliver infectious material into the tree as biological control agents against key pest canopy. The field studies on the nun moth NPV insect defoliators served as the catalysts for bac- suggested that this disease operated as a density- ulovirus research during the past 30 years. Dur- dependent disease agent ing this period more than 4,000 research papers In the United States, a similar scenario was have been published on baculoviruses, of which observed in populations of the gypsy moth, an more than 3,000 have focused on the nucleopo- imported defoliator of deciduous hardwoods. This lyhedrovirus group. In the 1970s and early 1980s, insect, originally imported as an alternative silk the major focus was studying the effects of wild- ­producer, escaped into the oak forests and spread type baculovirus strains on insect population. throughout southern New England. In the early From the mid-1980s to the present, the emphasis 1900s, collapses of gypsy moth populations were has been directed at the biochemistry and molec- attributed to the natural occurrence of wilt or ular biology of these viruses. This work, in addi- flacherie disease. At this time, Glaser and­Chapman tion to providing detailed insight into the initiated a series of key studies on this disease. workings of this complex virus, has provided the Microscopic examination revealed that this virus scientific community with a highly efficient replicated initially in the tracheae then spread to eukaryotic expression vector system that is being virtually all the insect tissues. Infected cells were used commercially to produce various protein recognized by the large number (Fig. 4) of intra- products. Lastly, the basic research has provided nuclear occlusion bodies. In 1913, Glaser and a means to engineer the baculovirus, which in Chapman reported that the filterable agent, the future years may provide highly efficacious causal agent of gypsy moth wilt disease, was recombinant strains for managing insect pest ­sensitive to sunlight and to heat treatment. In 1916, populations (Table 2). it was determined that the occlusions could be Nucleopolyhedroviruses are horizontally ­disrupted readily when placed in alkaline solu- transmitted to susceptible insects per os; larvae tions and could be re-formed by neutralization of become infected by ingesting foliage contami- the alkaline solution. nated with occlusions. In limited cases, chroni- One of the classic examples of biological cally infected adults may disseminate baculovirus control of insects has involved the introduction onto the chorion surface during oviposition, Baculoviruses B 355

Baculoviruses, Figure 4 Transmission electron micrograph of a thin section of the multiply embedded nucleopolyhedrovirus, not the crystalline protein matrix within which are embedded membrane bound rod shaped virus particles. Ingestion of these occlusions by host insects results in the digestion of the matrix protein and release of occluded virus. resulting in a vertical transfer of the pathogen to role in both the initiation and maintenance of progeny caterpillars. Not all baculoviruses cause natural virus epizootics. During the epizootic lethal infections; latent infections can persistently phase the primary route of baculovirus transmis- infect insect colonies in which the virus is trans- sion is per os. Ingested viral occlusions are dis- mitted within the egg stage. At present, very little rupted by the action of alkaline proteases in the is known about the frequency and impact of such midgut lumen. The types and amounts of gut persistent baculovirus infections on natural proteases produced by an insect influence the insect populations. The initiation of ­baculovirus processing of ingested occlusions. Increased epizootics has been attributed mainly to insects feeding rates, as displayed by mature larvae, may contacting and ingesting overwintering virus result in the rapid passage of ingested food con- inocula that are associated with plant and/or soil taining intact or only partially digested occlu- substrates. It is likely that latent infections play a sions, thereby preventing contact with the midgut 356 B Baculoviruses Baculoviruses, Table 2 Examples of baculoviruses production of a well-defined peritrophic mem- isolated from different insect hosts brane. The ODVs do not orientate to the Baculovirus Host microvilli in any particular fashion, suggesting Nucleopolyhedrovirus that the anti- receptors, if present, are distrib- AcNPV Lepidoptera: Autographa uted throughout the ODV envelope. The viral californica membrane fuses to the microvillar membrane AgMNPV Lepidoptera: Anticarsia and the nucleocapsids are released into the cyto- gemmatalis plasm. Nucleocapsids are transported to the LdMNPV Lepidoptera: Lymantria nucleus and attach to the nuclear pores of the dispar columnar epithelial cells. In addition to directly SeMNPV Lepidoptera: Spodoptera infecting the columnar cells, investigators have exigua reported that parental nucleocapsids can tra- CfMNPV Lepidoptera: verse the columnar cells and infect underlying ­Choristonuera fumiferana regenerative cells. Viral development in the TnSNPV Lepidoptera: ­ columnar epithelial cells may be aborted by the Trichoplusia ni preferential sloughing off of infected cells and by BmSNPV Lepidoptera: Bombyx the removal of the midgut layer at larval molt. mori Therefore, the ability of a baculovirus to infect TpSNPV Diptera: Tipula paludosa the regenerative cells may play a key role in CnSNPV Diptera: Culex nigripalpus maintaining a systemic infection. NsSNPV Hymenoptera: The naming of the different viruses includes ­Neodiprion sertifer the initial letter of the host species followed by Granulovirus mnv (multiply embedded nucleopolyhedrovirus), Snpv (singly embedded nucleopolyhedrovirus) or TnGV Lepidoptera: ­ Gv (granulovirus). Trichoplusia ni In the midgut cells, viral particles either PiGV Lepidoptera: Plodia attach to the nuclear pore and uncoat, or enter interpunctella the nucleus and uncoat. The release of the viral CpGV Lepidoptera: Cydia genome into the nuclear region marks the initia- pomonella tion of the primary replication phase. In various lepidopteran hosts the majority of baculoviruses produce only the non-occluded virus; occlusions tissue. Alternatively, the ingestion of plant mate- are not normally synthesized in either virus- rial that either buffers gut alkaline conditions or infected columnar or regenerative cells. Unlike contains endogenous protease inhibitors or anti- other enteric viruses (e.g., Cypoviruses), the viral allelochemicals may reduce the susceptibil- virus released from the infected columnar cells ity of an insect to baculovirus infection. do not horizontally spread to adjacent midgut The released occlusion derived virus (ODVs) cells but can infect adjacent tracheal cells or must bypass the peritrophic membrane in order migrate to the basal face of the midgut. However, to access the initial target midgut cells. The the basement membrane, comprised of exocel- ­peritrophic membrane is a dynamic structure lular matrix proteins, surrounds the basal face of that varies among different species and between the midgut and is believed to act as a barrier to the different developmental stages. As insects prevent the large-scale release of baculoviruses mature they often display a developmental resis- into the hemocoel. The virus that has penetrated tance to infection that is related in part to the the tracheal cells can undergo a complete Baculoviruses B 357 ­replication cycle and may then infect neighbor- massive numbers of the ODV phenotype and ing tracheal cells. Utilizing the host tracheal sys- associated occlusion bodies. The very late stage tem as a conduit, the virus can access and infect of NPV development is characterized by the other susceptible insect tissues. In addition to ­presence of hypertrophied, infected nuclei being disseminated via the tracheal conduit, becoming filled with highly refractile occlu- NPV-infected hemocytes also can spread the sions. Virtually all host tissues become infected virus to healthy tissues and larvae are extremely fragile. Frequently, During baculovirus replication, various NPV infected larvae will disintegrate into a viral proteins are produced which modulate the puddle of occlusion bodies. This “wilting” symp- host at the cellular as well as organism level. tom is believed to result in part from the Baculoviruses may contain genes that code for ­production of virally encoded hydrolases hav- proteins with ­anti-apoptotic activities that block ing either proteolytic or chitinolytic activities. the internal cell suicide program. Premature cell The production of this enzyme, detected in cul- death would abort the production of viral prog- ture supernates at 12 h post-infection, is under eny particles. Baculovirus replication also has the ­regulation of a late gene promoter. This been observed to disrupt the developmental enzyme, stable between pH 3 and 10, is believed program of host insects. For many years it has to be ­partially responsible for the liquefication been known that baculovirus infection retards of baculovirus-infected insects. The disintegra- larval development and prevents the larval-to- tion of infected insects also is aided by the pro- pupal molt. In the late 1980s baculoviruses were duction of various viral proteases. A variety of found to contain a gene (egt) which codes for a viral, host, and environmental factors determine ecdysteroid UDP-glucosyl transferase (egt). The the rate and level of occlusion formation in a egt gene encodes for a 57 kDa polypeptide with baculovirus-infected insect. Regardless, the bio- 506 aa. The egt holoenzyme, an oligomer of 3–5 magnification of baculoviruses in their respec- subunits, catalyzes the transfer of glucose or tive lepidopteran hosts is phenomenal. Neonate galactose from UDP-glucose or UDP-galactose, larvae may be infected by ingesting as few as respectively, to ecdysteroids producing inactive 1–10 occlusions, succumb to viremia within sugar conjugates of this steroidal hormone. 4–12 days, and then release 107 occlusions into Expression of the egt gene inhibits the molting the environment. process and maintains the host in the larval stage. This gene is non-essential, deletion mutants retain their ­ability to infect and to rep- licate both in cell culture and in host insects. References However, egt expression alters host ecdysone titers, results in a massive reprogramming of Clem RJ, Fechheimer M, Miller LK (1991) Prevention of apoptosis by a baculovirus gene during infection on host tissues, and disrupts larval molting and insect cells. Science 254:1388–1390 pupation. The prolongation of the larval stage Granados RR, Federici BA (eds) (1986) Biology of the bacu- results in increased viral yields. Alternatively, loviruses. CRC Press, Boca Raton, Florida the disruption of pupation due to viral infection Maramorosch K, Sherman KE (1985) Viral insecticides for biological control. Academic Press, Orlando, FL, 809 pp reduces the likelihood of viral-infected adult Miller LK (1996) Insect Viruses. In: Fields BN, Knipe DM, insects. Since the initial report in AcMNPV, Howley PM (eds) Fundamentals of virology. Lippincott- homologous genes have been detected in vari- Raven ­Publishers, Philadelphia, PA, pp 401–424 ous NPVs. Miller LK (1984) Exploring the gene organization of baculo- viruses. Methods Virol 7:227–258 In non-midgut tissues, NPVs, in addition to Rohrmann GF (1992) Baculovirus structural proteins. J Gen producing the baculovirus phenotype, produce Virol 73:749–761 358 B Baetidae Baetidae families in the past). The family is part of the superfamily Tineoidea, in the section Tineina, A family of mayflies (order Ephemeroptera). subsection Tineina, of the division Ditrysia. Adults  Mayflies minute to medium size (4–60 mm wingspan), with very rough head scaling; haustellum vestigial and naked; labial palpi reduced, 1 to 2-segmented but fused together (rarely 3-segmented); ­maxillary Baetiscidae palpi; antennae usually bipectinate. Maculation mostly dull colored, but sometimes with clear A family of mayflies (order Ephemeroptera). wings or translucent wing spots; some are spotted;  Mayflies rarely colorful. Adults are mostly diurnal or ­crepuscular. Larvae are mostly leaf feeders or feed on lichens, all making distinctive types of larval Bagworm Moths (Lepidoptera: cases, or bags. Pupation is within the larval case Psychidae) and females often remain there in a wingless or larviform shape, using pheromones to attract the john b. heppner winged males. A number of species are economic Florida State Collection of Arthropods, and many are general plant feeders. Gainesville, FL, USA

Bagworm moths, family Psychidae, total 1,001 References known species, mostly Palearctic and African, with only 88 known for the New World; actual fauna Betrem JG (1952) The genotypes of the Indo-Australian likely (Fig. 5) exceeds 1,200 species. The family is ­Psychidae (Lepidoptera). Tijdschrift voor Entomol now divided into six subfamilies, although vari- 95:331–340 ous tribes are sometimes elevated as additional Dalla Torre KW, von Strand E (1929) Psychidae In: Bryk F subfamilies: Lypusinae, Naryciinae, Taleporiinae, (ed) Lepidopterorum catalogus, vol 34. W. Junk, Berlin, 211 pp ­Penestoglossinae, Psychinae, and Oiketicinae (most Davis DR (1964) Bagworm moths of the Western Hemisphere of the subfamilies have also been treated as separate (Lepidoptera: Psychidae). Bull US Natl Mus 244:1233 Hättenschwiler P (1997) Psychidae – Sachträger. In: Schmet- terlinge und ihre Lebensräume: Arten – Gefährdung – Schutz. Schweiz und angrenzenden Gebiete, 2:165–308, pp 4–7. Pro Natura-Schweizerische Bund fuer Naturschutz., Basel Kozhanchikov IV (1956) Nasekomye Chechuekrulye. Chechlo­ nosye Meschechnitsky (sem. Psychidae). In Fauna USSR. Insects. Lepidoptera 3(3):15–16. Moscow [Engl transl: 1969. 525 pp, Smithsonian Institution, Washington]

Bait

A food or food-like substance that is used to attract Bagworm Moths (Lepidoptera: Psychidae), pests. It often is combined with an insecticide to Figure 5 Example of bagworm moths (Psychidae), poison insects, slugs, snails and rodents. Eumeta pryeri (Leech) from Taiwan.  Food-Based Baits Banana Pests and Their Management B 359 Balanced Mortality Hypothesis so when viewed on a larger scale. Clearly, eco- logical ­stability is scale-dependent, and broad- The belief that the level of reproduction is scaled scale stability (metastability) usually exists only to the probability of survival, with insects living in at the meta-scale. hostile environments having higher levels of reproduction than those occurring in more benign environments References

Egerton FN (1973) Changing concepts of the balance of Balance of Nature nature. Q Rev Biol 48:322–350 Wu J, Loucks OL (1995) From balance of nature to hierarchi- cal patch dynamics: a paradigm shift in ecology. Q Rev This is the idea that in nature there exists an inher- Biol 70:439–466 ent equilibrium founded on the interactions of plants and animals, resulting in a stable, ­continuing system of life on Earth. This belief is fundamental to many cultures, though Carl Linnaeus is often Banana Pests and Their ­credited with popularizing it (“oeconomia Management ­naturae”) in his writings of 1749. Sometimes this natural order was attributed to divine providence, william tinzaara,1 clifford s. gold2 but at other times maintained by nature. Once a 1Bioversity International-Uganda, Kampala­ popular notion, it no longer is popular with ­Uganda ecologists. 2CIAT-Uganda, Kampala Uganda Some elements of “balance” exist, such as the adaptations of different elements in a natural Bananas are among the most important food crops ­ecosystem such that resource production and use in the world. Despite their importance, banana are commonly balanced and optimized. However, yields are continuously declining due to attack by the so-called “balance” is continually upset by insect pests. Insects attack the banana rhizome, ­natural events and by the activities of humans. pseudostem, leaf and fruit. The most serious insect ­Outbreaks of insects are an example of the dis- pest on a global basis is the banana weevil. Other equilibrium that calls into question the notion of pests include the sugarcane weevil, pseudostem ­“balance.” However, the resistance of systems to weevil, banana scab moths, banana skipper, banana perturbation, the ­resiliency (rapidity of return to thrips and banana aphids. Pests of minor or local- equilibrium after perturbation) of both producer ized importance include the spiraling whitefly, and consumer organisms, and the persistence mealybugs, big-headed ant, chinese rose beetle ­(tendency of organisms to persist even when and coconut scale. Thrips cause cosmetic damage faced with catastrophic changes in ­abundance), directly to the fruit, reducing marketability. Most can be construed as supportive of the balance pests do not attack the bunch and cause indirect hypothesis, or at least supportive of the idea of damage. For example, banana weevils attack the ­continuance or constancy. rhizome and pseudostem causing yield reductions Much of the disagreement about the “bal- through plant loss, delayed maturation and bunch ance of nature” is due to differences in scale. weight reduction. Some pests, such as Pentalonia ­Ecosystems are mosaics of patches, and envi- nigronervosa, are vectors of serious diseases. In ronmental stochasticities or biological feed- this article, the pest status, distribution, biology backs that appear to be destabilizing or and control options of major pests of banana are catastrophic on a local scale may be much less discussed. 360 B Banana Pests and Their Management Banana Weevil, Cosmopolites morphological features and all show extreme sordidus (Germar) (Coleoptera: variation in color. The adults are 9–14 mm long Curculionidae) black adults with red or yellow markings. The base of the elytra is one-half to one-third red or yellow The banana weevil is the most important insect on a black background. The pronotum and venter pest of banana and plantain. Its host range is are black to red and black. This species can be restricted to wild and cultivated clones of Musa confused with Metamasius calligsona which (banana, plantain, abaca) and Ensete. The insect infests bromeliads. M. hemipterus adults are active originated in southeast Asia and has spread to all fliers (unlike C. sordidus). important banana and plantain growing areas. It is not normally a pest in its area of origin. Because of its importance, detailed treatment of Biology this insect is provided elsewhere in the Encyclopedia.  Banana Weevil, Cosmopolites sordidus The three subspecies of M. hemipterus have simi- lar biology. The adults are most often found in moist, dark places. They are attracted to, and ovi- Sugarcane Weevil, Metamasius posit in, healthy banana pseudostems, rotting hemipterus sericeus (Coleoptera: banana plants, banana residues, damaged or Curculionidae) stressed sugarcane stalks, ripe fruit (i.e., pineapple, mango, papaya), or palm sheaths or stems. More The sugarcane weevil Metamasius hemipterus is known about the oviposition habits of ­sericeus (Olivier) (Coleoptera: Curculionidae: Dry- M. hemipterus on sugarcane than on banana. The ophthorinae) primarily infests banana, ­plantain, weevil is attracted to stalks damaged by either sugarcane and, less commonly, ornamental palms. mechanical cultivation, harvesting equipment, The insect is endemic to the America tropics. It has rats, borers, disease or natural growth cracks. In been found on plantain in West Africa but has not some cases, Metamasius females prefer to deposit been reported from East Africa. eggs on sugarcane that has been damaged by Dia- The importance of M. hemipterus as a pest of traea (Lepidoptera: Pyralidae). In Colombia, this banana is disputed but it is considered more seri- type of damage is known as the Diatraea-Meta- ous than the banana weevil, Cosmopolites sordidus, masius complex. Metamasius hemipterus has also in the banana growing areas of western Colombia. been observed infesting canes used as seed pieces. In this region, M. hemipterus is known to transmit The females lay their eggs in cracks and Erwinia chrysanthemi pv paradisiaca causing rot- damaged areas of bananas and sugarcane, or in ting of the banana pseudostem. Some authors petioles and crown shafts of certain species of argue that M. hemipterus is unimportant or only a healthy palms. The adult can live up to 60 days secondary pest of banana. during which time the female can deposit 400– There are three recognized subspecies, all of 500 eggs. This contrasts with the biology of which attack banana: M. h. hemipterus (L.) is dis- C. sordidus, which is longer lived but produces tributed from Puerto Rico through the Lesser far fewer eggs. As with C. sordidus, M. hemipterus Antilles and into most of South America; M. h. places single eggs in holes made in the host by sericeus (Olivier) is found in the Greater Antilles, the insect’s rostrum. southern Florida (USA) and from Nicaragua to The oval egg is 1.2–1.5 mm in length and Ecuador; while M. h. carbonarius (Chevrolat) creamy-white. The egg stage is 3–7 days. The cream- occurs from Mexico to El Salvador and Hondu- color, yellowish larvae are typical legless weevil ras. The three subspecies have similar external grubs and similar in most aspects to other members Banana Pests and Their Management B 361 of the Rhynchophorinae. Fully developed larvae are Trapping and Monitoring 1.3–2.0 cm. The larval stage lasts 50–60 days. Metamasius hemipterus larvae can be differ- Trapping of adults is often used to monitor weevil entiated from those of Cosmopolites by color numbers, although interpretation of trap captures (creamier coloration), behavior (more active), is difficult. The use of a “sandwich trap” using and morphological features (stigmata, cranial banana pseudostem as an attractant has been sug- sutures, and structures on the labium and gested. A maximum of ten weevils per trap per clypeum). Mature M. hemipterus larvae construct week have been captured using banana pseu- a fibrous pupal case (similar to that of the giant dostem disc traps, although the number of weevils palm weevil, Rhynchophorus palmarum) and collected at these traps was consistently too low to pupation takes place mostly within the banana accurately assess weevil density. Fermenting sug- pseudostem. The pupal stage is 10–20 days. Thus, arcane has also been used to attract M. hemipterus. depending on temperature, the life cycle is com- An average of 30 weevils per trap using pieces of pleted in 63–86 days. bamboo filled with pieces of fermenting cane have been captured. Tests conducted on different trap designs and the response of adults to semiochemi- Pest Status cals demonstrated that weevil counts increased with combinations of ethyl acetate, sugarcane and/ Damage in banana is caused by the larvae, which or the aggregation pheromone metalure, com- feed in the upper part of the pseudostem. The lar- pared with the use of any compound alone. The vae bore into the stem causing extensive physical major male-produced aggregation pheromones damage and, in heavy infestations, can kill the and host kairomone compounds have identified plant. The first symptoms of M. hemipterus attack the trap designs and protocols that can be used for are yellowing of the lower leaves and consequent enhanced monitoring of weevil populations in the rotting of the pseudostem. In cases of extensive field. In addition, it has been demonstrated that damage to the pseudostem, the plants cannot resist pheromone and host-baited traps can be used to the weight of fruit, increasing the likelihood that mass trap M. hemipterus infesting banana and the plants may double and eventually die. The pest sugarcane in Costa Rica. has also been reported to attack the banana ­rhizome  Control Measures and cause damage similar to that of C. sordidus. Moreover, there are reports that M. hemipterus did not show any preferences between rhizome and Chemical Control pseudostem tissue of the cultivars Gross Michel (AAA) and Bout Rond. Unfortunately, there are no Labeled rates of acephate, carbofuran, chlorpyri- yield loss data for M. hemipterus in banana. fos, cyfluthrin, disulfoton, imidachloprid, isofen- Larvae of M. hemipterus can seriously affect phos, lindane and vydate have been demonstrated the ornamental palms Phoenix canariensis, Pty- to kill adults of M. hemiperus. The data suggest chosperma macarthurii, Ravenia rivularis, and that poisoned sugarcane traps may be adequate for Roystonia. Larval tunneling in palms starts in the control of M. hemipterus, although inadequate petioles, wounds in petioles, crown, stem and then control with chemical insecticides has also been extends into healthy leaf or stem tissue. Affected reported. Moreover, chemically based pest con- palms are often characterized by the production of trols represent short term and questionable strate- an amber-colored, gummy exudate in the stem, gies for resource-poor farmers in developing crown shaft or petioles, and galleries in the leaves, countries, along with accompanying health and petioles and stems. environmental concerns. 362 B Banana Pests and Their Management Cultural Control M. hemipterus larvae, but not adults. However, the authors concluded that chemical insecticides and Sanitation of residues harboring the weevil has entomopathogenic nematodes would need to be been recommended. This procedure is done by applied frequently and over a long period of time cutting up pseudostems and allowing them to dry for effective management because of the weevil’s up. No data are available on efficacy. high reproductive potential and the cryptic ­habitat of the immature stages.

Biological Control Natural Enemies Both entomopathogens and naturally occurring biological control agents affect sugarcane weevil. Reported predators of M. hemipterus include labi- durids, histerids, staphylinids, carabids, cicindelids, formicids and reduviids. Little is known on the con- Entomopathogens trol potential of predators. In Florida, Colombia and Ecuador, surveys for predators and parasitoids of The use of entomopathogens provides a promising, M. hemipterus sericeus have been unsuccessful. yet still expensive means of control of M. h. sericeus. There are reports that trials with the tachinid The entomogenous fungi Beauveria bassiana Microseromasia sphenophori failed. ­However, the ­(Balsamo) Vuillemin and Metarhizium anisopliae tachinid Admontia spp, observed parasitizing (Metchnikoff) Sorokin have gained considerable Metamasius quadrilineatus in Honduras, could be attention as potential control for weevils. For example, tested as a possible parasitoid of M. hemipterus. studies have demonstrated that naturally occurring Thus, to date, very little research has been done on B. bassiana was an important mortality factor to parasitoids of M. hemipterus in the neotropics, so it adults of M. hemipterus in Florida. Beauveria is unclear whether or not effective biological control ­bassiana infection increased up to 70% between will be possible. March and April 1991 when more than ten weevils were captured per trap. In Brazil, B. bassiana and M. anisopliae caused high death rates of adults Banana Pseudostem Weevil, applied under laboratory conditions. Odoiporous longicollis (Coleoptera: Applying fungal formulations to traps made Curculionidae) from banana pseudostems was considered the most effective delivery system, while applica- The banana pseudostem weevil, Odoiporous tions outside traps were deemed impractical. It longicollis­ (Olivier) (Coleoptera: Curculionidae) is was observed that M. hemipterus adults were considered a minor to important pest of banana and more susceptible to infection by both fungi than Manila hemp in parts of India, Nepal, Burma, Sri C. sordidus adults. In Cuba, a strain of B. bassi- Lanka, Thailand, Indonesia, China and elsewhere in ana from the sweet potato weevil, Cylas formi- Asia. The weevil bears a superficial resemblance to carius elegantulus, which is reported to be highly the banana weevil, Cosmopolites sordidus (Germar), pathogenic to M. hemipterus and C. sordidus was but is slightly larger and its elytra do not completely isolated. More information is needed on the cover the abdomen. The color of the adult weevil effect of these fungi before pest management varies with age from reddish-brown to black. Sexing decisions can be made. of adults is based on punctuation of the rostrum. The nematode Steinernema carpocapsae Males also tend to be smaller than females. The sex has been demonstrated to be effective against ratio ranges from as 1:1.2 (male:female) to 1:1.5. Banana Pests and Their Management B 363 Biology The larvae attack the pseudostem and stem of banana plants, although they will occasionally feed The weevil is characterized by long life span, within the rhizome. This contrasts with the banana ­negative phototropism, thigmotropism, gregari- weevil, which attacks the rhizome and uncom- ousness, hydrotropism and death mimicry. Most monly enters the pseudostem. As such, pseudostem adults live 6–10 months, although some can borer damage may be clearly visible, while banana ­survive for more than 2 years. In contrast to the weevil damage can only be observed by dissection banana weevil, the adult readily flies, although it of the rhizome. The pseudostem borer will attack has been described as a poor flyer. Still, it has suf- both living plants and harvested stumps. ficient capability to move between proximal Larval damage can lead to the rotting of banana stands. In spite of being negatively photo- ­pseudostem tissues and breakage in the wind. trophic, diurnal flight occurs. ­Breakage of damaged plants is potentially a serious Oviposition is in the leaf sheaths of living plants problem, although such losses are rarely quantified. or residues. The weevils are especially attracted to, Thus although the weevil has been described as an and readily oviposit in, cuts in banana material. important pest, there are no available data on plant Some authors have suggested that ­ovipositing loss and/or yield reductions. Further work in this females prefer stressed plants, while others observed area is required for the development of any integrated­ greater oviposition in residues than in living pest management program. plants. The greatest oviposition has been found in ­pseudostems with a girth of 25–50 cm, with little oviposition in plants less than 25 cm or more than Control Measures 75 cm in girth. The eggs are placed singly in cham- bers made with the female’s rostrum. The egg stage Cultural Control has been reported as 3–4 days and 5–12 days. The larvae pass through four instars. The first There is limited information available on control instar remains near eclosion sites in the same leaf of banana pseudostem weevil. Selecting new and sheath. Subsequent instars bore into the inner leaf clean sites, use of clean planting material, crop sheaths or pseudostem. The mature larvae may be sanitation (e.g., burying infested residues), rogue- twice the size of those of banana weevil. The larval ing of infested plants, crop rotation (to rid fields of stage has been reported by several authors to be weevils), and trapping by placement of residue 14 days, 3–6 weeks and 26–68 days. slices on the ground has been recommended. The prepupa forms a pupal chamber within Because the weevil flies and its dispersal capacity the host plant. Pupation is within a cocoon formed has not been determined, it is unclear how effec- out of plant fibers. The prepupal stage lasts 3–9 days, tive the use of these cultural methods might be. while the pupal period has been reported as 3–20 One scientist reportedly collected more than 2 days. Following emergence, the adults may pass million weevils in traps over a 4-month period, extended periods and even mate within the host but did not provide information on the effect of plant. The pre-oviposition period lasts 1 month. this trapping program on weevil populations.

Pest Status Chemical Control

The adult weevils feed on living and decompo­sing Swabbing of the pseudostem and weevil holes with banana leaf tissues, but eat little and are not con- insecticides has also been recommended. No data sidered pests. Damage is done by the larval stage. are available on efficacy. 364 B Banana Pests and Their Management Host Plant Resistance Pest Status

Host plant resistance has been suggested to be Banana scab moth females lay eggs on the outside ­effective in reducing weevil infestations. In India, one of the banana flower bracts or on nearby leaves as variety was found to be completely free of the weevil, the flower first emerges. Upon hatching, the larvae while two others appeared resistant. In screened enter the flower and feed on the developing fruits banana germplasm studies, six varieties were found within. Feeding results in irregular dark brown to to be severely infested, three heavily infested, four black corky blotches on the fruit skin. Light dam- moderately infested, and 27 lightly infested. age may be superficial and confined to the upper end and outer side of the curved fingers. Heavier infestations can scar the entire fruit, cause deformed Banana Scab Moth, Nacoleia fingers, or penetrate into the flesh of the fruit. octasema (Lepidoptera: Pyralidae)

Banana scab moth, Nacoleia octasema (Meyrick) Control Measures (Lepidoptera: Pyralidae), is a serious pest of bananas in the Samoan Islands and elsewhere in the south- Uses of biological control, resistant varieties, or western Pacific. The pest also attacks ­Heliconia cultural controls have not proven effective for spp. and Pandanus spp. Other moths that attack managing banana scab moth. banana but are considered of minor importance include Opogona sacchari and Othreis fullonia. Chemical Control

Biology Chemical control works well when used properly. Because the larvae begin damaging the developing Banana scab moth females lay eggs on banana fruits when they are still enclosed inside the flower, flower bracts or leaves as the inflorescence emerges. the best control can be achieved by injecting an Larvae hatch, enter the flower, and feed on the insecticide into the flower after it first becomes developing fruits within. The feeding results in visible, but before it starts bending over from the rough and irregular scars (brownish-black) on vertical position. A single injection at this stage, fruit skin. Large infestations can scar the entire applied about 1/3 of the way down from the flower fruit and cause deformed fingers. tip, will percolate down to protect all the hands Eggs are laid singly or in small, flattened, almost inside. This protection will last until the bracts transparent clusters of a few to over 20 eggs. The eggs begin to fall away and no more egg laying occurs. hatch in 3–4 days and the larvae enter the banana Some growers prefer to lift or remove the lower, where they feed. The larval period is 11–19 flower bracts and dust or spray insecticide onto the days. Pupation is inside a loose silken cocoon, often fruits after the flower has bent over. This method placed between banana ­fingers, in folds of the dead can stop some of the damage, but not all of it, leaves still attached to the pseudostem, or in litter because by this stage feeding has already begun. near the base of the plant. Adult moths emerge in Flowering is more or less continuous in banana 8–10 days and are short-lived, dying after about 3–10 plantations in American Samoa, and the stage at days. Females lay approximately 80–120 eggs during which insecticide must be applied lasts only a few their lifetime. The moths are rarely seen, because they days for each plant. Therefore, it is important to hide among dead leaves and vegetation ­during the check the plantation frequently to ensure that all day and are active only during the early night. emerging inflorescences are treated. Banana Pests and Their Management B 365 Biological Control are more common after a drought and in wind protected areas. Several kinds of natural enemies attack the banana The banana skipper is a large brownHesperiid scab moth, but in general they do not provide with large yellow spots on the forewings above. sufficient control to reduce damage to acceptable Adults are less often seen although the caterpillars levels. Spiders and ants may prey on the immature can be quite common on the host plants. This may stages of banana scab moth. Parasitic wasps may be due to the fact that the butterfly is only active also help reduce banana scab moth numbers. In during the early morning hours and just before the Samoan Islands, the most common parasitoid dusk. It is sometimes attracted to the lights of is Chelonus sp. (Hymenoptera: Braconidae), which dwellings and flies towards the lights in the lays its egg inside the egg of the scab moth. The evenings. Chelonus larva then develops inside the scab moth The caterpillars can be found where the banana egg and larva. It finally emerges from the nearly plants (Musa spp.) are cultivated. Occasionally, an full grown scab moth larva to spin a cocoon nearby infestation is severe enough for the species to be in which it pupates. considered one of the banana farmer’s pests. The characteristic rolled up portions of the banana leaves are a dead giveaway to the presence of the Host Plant Resistance caterpillars. Pupation takes place in a rolled up leaf as well, and the adult butterfly emerges after about Some banana varieties appear to be less suscep- 7 days. The caterpillar swings from side to side tible to scab moth damage. Left untreated, these when disturbed, and exudes a greenish fluid. The varieties may produce a satisfactory product for pupa also wriggles violently when disturbed. markets that can tolerate some damage. Biology The Banana Skipper, Erionota thrax (Lepidoptera: Hesperiidae) The adult butterfly lays bright yellow eggs singly or in groups of up to 25. Oviposition is mostly on the The banana skipper, Erionota thrax (Linnaeus) lower leaf lamina midway between the midrib and (Lepidoptera: Hesperiidae) is a minor to severe the outer edge. Eggs turn bright red and the pale pest of bananas and Musa textilis in Southeast green larvae hatch after about 5–8 days. The larvae Asia and Papua New Guinea. Damage has also move to the outer leaf lamina where they com- been reported from bamboo, coconut and other mence feeding and then produce loose rolls by plants although it has been suggested that other cutting the leaf and rolling the lamina towards the species may be responsible for the records on midrib. Larvae feed and grow within the rolls, palms and bamboo. Banana clumps in isolated commencing a new roll once the midrib is reached. villages in Java had a very patchy damage distri- The second and subsequent three instars are cov- bution, ranging from severe defoliation to nil on ered in a white waxy powder that provides protec- clumps growing within close proximity. Heavy tion from drowning during high rainfall. The rainfall and strong winds are unsuitable for larval stage lasts 20–30 days, depending on tem- banana skipper. Entry of water into the leaf rolls perature. Pupation occurs within the leaf roll and drowns the larva (particularly the first instar) lasts 8–12 days. Adults emerge in the afternoon and wind-torn leaf laminae are unsuitable for and are most active in the evening and early morn- the production of leaf roll shelters. For these ing when they actively fly around banana plants to ­reasons, outbreaks in Malaysia and Indonesia mate and oviposit. 366 B Banana Pests and Their Management Pest Status result in splitting of the peel with subsequent development of secondary rots. Usually only fruit Direct fruit production losses is only significant grown commercially requires treatment with following heavy defoliation since banana plants ­prophylactic pesticides. In Australia, chemical can withstand at least 20% leaf lamina loss before treatments are routinely applied to prevent the production is affected. Nonetheless, bananas in rusty brown discoloration caused by the pantropi- Southeast Asia are grown for aesthetic value and cal banana rust thrips C. signipennis. The closely for culinary purposes where even minor infesta- related C. orchidii (Moulton) causes similar dam- tions would be detrimental. age in Central and South America. The banana flower thrips T. hawaiiensis, a widespread and polyphagous flower feeder in Oriental and Pacific Control Measures regions, damages fruit at flowering as it oviposits and feeds on fruit during and immediately after The banana skipper is adequately controlled by a emergence of the inflorescence. The slightly raised, range of beneficial insects such that other control silvery grey lesions caused by these thrips are measures are seldom required. In Indonesia, egg locally referred to as “corky scab.” parasitoids, including Ooencyrtus erionotae, Agi- In Mexico, Frankliniella parvula prefers to ovi- ommatus sp. and Anastatus sp., can parasitize 50– posit in the epidermis of young banawna fruits and 70% of the eggs. Young larvae are attacked by less frequently in the flower parts. In Yemen,Scirto - Apanteles erionotae while older third instar larvae thrips aurantii and Thrips pusillus cause fruit spot- are preferred by Scenocharops sp. The pupal para- ting on bananas. Small circular spots first appear on sitoids Brachymeria sp., Xanthopimpla sp. and the surface of the fruit, gradually enlarge, blacken, Pediobius sp. also contribute to biological suppres- and develop into oily, water soaked lesions. sion of E. thrax. If unusually heavy outbreaks In Australia, T. hawaiiensis causes a superfi- occur, the collection and destruction of leaf rolls cial skin injury locally referred to as corky scab. may reduce subsequent damage. Adults are attracted to the emerging inflorescence. Female oviposition and subsequent nymphal and adult feeding cause damage on the developing Banana Thrips (Thysanoptera: fruit while the bunch is wrapped closely in the Thripidae) bracts. Oviposition punctures result in localized raised “pimples” which disappear as the fruit Species of thrips that attack and damage banana develops, while the superficial grazing by the include Chaetanaphothrips orchidii (Moulton), C. thrips develops into the slightly raised silvery-grey signipennis, Caliothrips bicinctus, Frankliniella areas of corky scab. This damage is more prevalent ­parvula, Heliothrips haemorrhoidalis (Bouché), during dry periods and is more commonly associ- ­Hercinothrips bicinctus (Bagnall), Thrips hawai- ated with fruit fingers on the lower bunch hands, iensis (Morgan), and Tryphactothrips lineatus. the rachis and attacked cushion. The banana thrips H. bicinctus (Bagnall), C. bicinc- tus, C. orchidii, C. signipennis, T. hawaiiensis and T. lineatuss are the most important peel-blemish- Biology ing insects, producing a range of damage symp- toms on immature fruit. Eggs are inserted into the plant tissues including Thrips cause superficial skin blemishes on fruit, pseudostem and leaf petioles, depending on immature and developing banana fruit. Damage is species. Surfaces that are in close contact are pre- primarily cosmetic although severe attacks may ferred for oviposition and development. The eggs Banana Pests and Their Management B 367 hatch in 1–2 weeks. Nymphs are clear to straw- flowers after the fruits are formed, removal of colored and, like the adults, shun sunlight, quickly alternate host plants, and covering banana bunches dispersing when disturbed from their cryptic hid- with a bag impregnated with insecticides have ing places between adjacent fruit or from under leaf been recommended. There are no known useful bracts on the pseudostem. Pupation takes place on natural enemies of banana thrips. Reportedly there the plant or in the soil near the base of the plants, is a lack of effective predators for C. signipennis in depending on species. Banana rust thrips (C. signi- north Queensland, Australia, although a number pennis) may spend part of their life cycle in the soil, of generalist predatory bugs, coccinellids and while banana flower thrips stages all occur on the chrysopids feed on flower thrips and can reduce host plant. For example, in Australia, the entire life their numbers. cycle of T. hawaiiensis is spent on the fruit or other Chemical control methods consist of enclosing parts of the plant. During summer months, the the bunch inside an insecticide-treated bag. This period from egg to adult for this species is 3 weeks. practice, once widespread, is still recommended in South America. A single pesticide injection into the emerging inflorescence, a treatment ­specifically Pest Status aimed at the banana scab moth, is also efficacious against T. hawaiiensis and helps ­protect from early Thrips can scar, stain, or deform banana fruits by C. signipennis infestation. Attaching a piece of feeding on the fruit skin. Thrips are small, winged ­chlorpyrifos impregnated ­ribbon to the upper bunch insects that feed on banana flowers and/or the ten- stalk also provides extended ­protection against C. der green skin of developing fruits. The two fac- signipennis. Untreated polythene bunch covers sig- tors of feeding site and species determine the type nificantly reduced damage compared to uncovered and extent of fruit damage. Thrips outbreak can fruit, while bunch covers impregnated with 1% chlo- occur during periods of dry weather. Thrips cause rpyrifos provided almost total protection. superficial skin blemishes on immature and devel- oping banana fruit. Damage is primarily cosmetic although severe attacks may result in splitting of The Banana Aphid, Pentalonia the peel with subsequent development of second- nigronervosa (Hemiptera: ary rots. Usually only fruit grown ­commercially Aphididae) requires treatment with prophylactic pesticides. Most of the species are found in the inflores- The banana aphid, Pentalonia nigronervosa cences or between fruits. The skin of severely Coquerel, (Hemiptera: Aphididae) is present world- infested fruit may crack, allowing secondary inva- wide where banana (Musa spp.) is grown. The aphid sion of pathogens. In Brazil, injury by T. lineatus is is a serious problem on banana because it is a vector regularly observed on 30-day old fruits, or fruits of Banana Bunchy Top Virus (BBTV), the most larger than 32 mm in diameter. damaging virus disease of bananas. The preferred host of this aphid is banana but also may infest many tropical and subtropical food and ornamen- Control Measures tal plants, including Alpinia purpurata (floral red and pink ginger), Xanthosoma (“ape or elephant Cultural control methods, such as clean cultiva- ear), cardamom, Heliconia, tomatoes, taro, Calla, tion and removal of trash, promote the exposure Costus, kahili ginger, torch ginger, and Zingiber. of pupae to desiccation, but do not provide effec- The banana aphid is present just about every- tive control. In Brazil, use of chemical control as where banana is grown. It has been reported soon as the flowers are formed, elimination of throughout tropical Africa, Atlantic Islands, 368 B Banana Pests and Their Management Australia, California, Florida and Hawaii (USA), bracts of the ginger stem. The entire inflorescence Central America, Cook Islands, Egypt, Fiji, ­Kiribati, may be infested. Small colonies occasionally occur India, Indonesia, Malaysia, Madagascar, Marshall on the leaf blade. Ants are associated with the banana Islands, Mauritius, Mexico, Micronesia, the Middle aphid. The ants feed on the honeydew secreted by East, Mozambique, New South Wales, Papua New the aphid and, in turn, establish new aphid colonies Guinea, the Philippines, Réunion, Samoa, northern and ward off natural enemies. Winged adults often South America, Taiwan, Tokelau, Tonga, Tuvalu, develop after 7–10 generations of wingless individu- Vanuatu, Wallis Island, and much of the West Indies. als. Dispersing winged adults establish new colonies on other new host plants. Although they are not strong fliers, they may be carried considerable Biology distances by light winds. Flight activity peaks between 9:00–11:00 A.M. and 5:00 P.M. to dusk. Reproduction in the banana aphid is entirely ­parthenogenetic (without mating). Females give birth to live female young. Males are not known Pest Status for this species. The life cycle (nymph to adult) is completed in 9–16 days. The adult life span ranges The banana aphid is a phloem feeder that uses its from 8 to 26 days; there could be as many as 30 long stylets to pierce plant tissues to suck the sap generations produced per year in Hawaii. directly from the vessels. This can cause plants to There is no egg stage. Young are born live. Like become deformed; the leaves become curled and most other aphid species, the banana aphid has shriveled, and in some cases galls are formed on four nymphal stages. Newborn nymphs are oval at the leaves. Young plants may be killed or their first and become slightly elongated. They are red- growth checked if there is sufficient feeding by the dish brown, with four segmented antennae, and banana aphid. However, direct damage by this measure 0.1 mm in length. The second stage aphid is generally negligible. nymphs are similar in appearance and measure The insects do far more harm as vectors of approximately 0.7 mm long. The third nymphal numerous viruses, including bunchy top. The aphid stage individuals are light brown, measuring about picks up the virus while feeding on a sick plant, 0.9 mm in length; the compound eyes are more then spreads it to healthy banana plants in subse- noticeable beginning with this stage, and the quent feedings. Both wingless (apterous) and nymphs have five-segmented antennae. The fourth winged (alate) aphids are able to transmit viruses. stage nymphs have six-segmented antennae, are Transmission is usually in a non-persistent manner light brown in color, and are 1 mm long. The first, where the virus is taken up into the aphids’ second, third, and fourth nymphal stages last 2–4, ­mouthparts while feeding on an infected plant and 3–4, 2–4, and 2–4 days, respectively. transferred to a healthy plant during subsequent Adult banana aphids are small to medium feedings. In non-persistent transmission, the virus sized aphids (1–2 mm), shiny, reddish to dark brown reproduces in the plant, and aphids simply aid in or almost black. They have six-segmented antennae transporting the virus. With these types of virus- that are as long as the body. Alates have prominent, vector associations, the aphid acquires the virus dark (brown or black) wing veins. Adults start pro- and is only able to transmit the virus temporarily. ducing young one day after reaching maturity. They Once all the infective charge is reduced by feeding can give birth to four aphids per day with an aver- or the passing of time, the aphid is unable to trans- age production of 14 offspring per female. mit the virus until it feeds on infected tissue again. Colonies of the banana aphid are commonly Symptoms of banana bunchy top disease found in the upper leaf sheaths and lower flower include bunched, yellow leaves at the top of the Banana Weevil, Cosmopolites sordidus (Germar) (Coleoptera: Curculionidae) B 369 plant, dark green streaks on the leaves and mid- Hippodamia convergens, Scymnodes lividigaster, ribs, progressively smaller leaves, leaf curling, and ­Diomus notescens (Coleoptera: Coccinelidae), and small, distorted fruits. Since the aphid harbors the Nesomicromus navigatorum (Neuroptera: Hemero- virus only temporarily, it needs a regular diet of biidae). The larvae, as well as the adults, of ladybird infected plant tissue to remain infective. beetles and lacewings are very active aphid feeders, and have been found, along with syrphid fly larvae, in floral red ginger in Hawaii. Control Measures An entomopathogenic fungus, Acremonium sp., was also observed on banana aphids. The fungus Farmers typically manage banana bunchy top dis- observed to reduce reproduction, development and ease by destroying infected plants, which serve as a population of banana aphid, Pentalonia nigronervosa, reservoir for the virus, and controlling aphids with a vector of bunchy top virus diseases of banana. insecticides. A wasp that is a known parasitoid of the  Banana Weevil, Cosmopolites Sordidus aphids and ladybird beetles that prey on them was  Tropical Fruit Pests and Their Management introduced in Hawaii as biological control agents. However, none will control banana aphid adequately enough to prevent the transmission of BBTV. References

Botha J, Hardie D, Power G (2000) Banana scab moth (Naco- Chemical Control leia octasema): exotic threat to Western Australia. Fact sheet No. 45/2000. Hortguard TM Initiative AGWEST, Department of Agriculture, Australia Chlorpyrifos and acephate foliar sprays have been Giblin-Davis RM, Peña JE, Oehlschlager AC, Perez AL (1996) effective in reducing aphid populations and the Optimization of semiochemical-based trapping of attending ants. Immersing flowers and foliage in Metamasius hemipterus sericeus (Olivier) (Coleoptera: Curculionidae). J Chem Ecol 22:1389–1410 hot water at 49°C for 10 min kills banana aphids. Gold CS, Pinese B, Peña JE (2002) Pests of banana, pp 13–56 This treatment is safe for many commodities, but In: Peña JE, Sharp JL, Wysoki M (eds) Tropical fruit preconditioning may be required. pests and pollinators. CABI, Oxford, UK, 448 pp Scot C, Nelson R, Ploetz C, Kepler A (2006) Musa species (banana and plantain). Species profiles for Pacific Island Biological Control agroforestry. Traditional tree initiative, Version 2.2. (www.traditionaltree.org) Sosa O, Shine J, Tai P (1997) West Indian cane weevil Introductions of the braconid Lysiphlebius ­testaceipes (Coleoptera: Curculionidae): a new pest of sugarcane in were made in 1923, 1953, and 1965 by the Hawaii Florida. J Econ Entomol 90:634–640 Department of Agriculture to combat aphids. The sources of the introduced wasps include Japan, Cuba, California, and Mexico. This parasitoid is established on all populated Hawaiian Islands and Banana Weevil, Cosmopolites is a known parasitoid of the banana aphid. sordidus (Germar) (Coleoptera: Biological control experts from the Hawaii Curculionidae) Department of Agriculture have introduced ­ladybird beetles to the islands to control insects. Coccinella clifford s. gold1, william tinzaara2 7-punctata var. brucki was brought in from Okinawa 1CIAT, Kampala Uganda in 1958 and is established on the major islands, and 2Bioversity International, Kampala Uganda is listed as a banana aphid predator. Other predators that have been successfully introduced to combat The banana weevil is the most important insect aphids are Coelophora inaequalis, C. pupillata, pest of banana and plantain. Its host range is 370 B Banana Weevil, Cosmopolites sordidus (Germar) (Coleoptera: Curculionidae) restricted to wild and cultivated clones of Musa contribution of M. acuminata and M. balbisiana. (banana, plantain, abaca) and Ensete. The insect Cooking, ­roasting, dessert and brewing types are originated in Southeast Asia and has spread to all grown. Production systems range from kitchen important banana and plantain growing areas. It is gardens and small, low input stands to large-scale not normally a pest in its area of origin. export plantations. Banana weevil larvae bore in the corm, damag- ing the root and vascular system, reducing nutrient and water uptake, and weakening the stability of the Biology and Life Cycle plant. Attack in newly planted banana stands can lead to crop failure. In established fields, weevil Adult Stage damage can result in plant loss (death of suckers, toppling, snapping), reduced bunch weights, mat Adults are uniform black or dark brown and disappearance (following failure to produce suckers), ­average 12.5–13 mm in length. The sex ratio is 1:1. and shortened stand life. Damage and yield losses Males can be distinguished from females on the increase over time. Yield losses may exceed 50% in basis of small pits on the rostrum extending ratoon crops. Stand life can be reduced from more beyond the point of insertion of the antennae and than 30 years to less than five. by greater curvature of the last abdominal sternite. Banana weevil pest status is affected by clone Males are on average 20% smaller than females in selection, ecological conditions, and management size and weight. system. Highland bananas (AAA-East Africa) and The banana weevil displays a classical “K” plantains (AAB) are most susceptible. Other clonal selected life cycle with long life span and low groups, including export dessert bananas (e.g., fecundity. Adults may live 4 years though most live Cavendish, AAA), tend to be moderately to highly less than 1 year. They are free living but closely resistant. Ensete is susceptible, but usually grown associated with banana mats and cut residues. They above the pest’s upper elevation threshold and there- are usually hidden during daylight hours and most fore escapes attack. often observed at traps. The adults feed on rotting banana tissues and can survive months without food. They require moist environments and die The Host Crop within days if maintained on dry ­substrates. Banana weevils are attracted to their hosts by ­volatiles, Banana is an herbaceous perennial that is propa- especially those released from damaged corms. gated through lateral buds giving rise to new plants Males produce an aggregation pheromone attrac- (suckers). The plant consists of an underground tive to both sexes. corm and a pseudostem composed of overlapping Banana weevils are negatively phototrophic leaf sheaths. The true stem emerges from the corm, and most active between 2100 and 0400 h grows through the pseudostem, and bears the ­Temperature thresholds for activity are 15–18°C. inflorescence. The plant dies after the bunch Flight is uncommon. Dispersal by crawling is ­limited; matures. A group of plants sharing a common fewer than half move 50 m in a year. The banana corm comprise a mat. Suckers may be detached weevil’s narrow host range and limited dispersal from the mat and planted elsewhere. capability preclude immigration of adults into Edible bananas are ultimately derived from ­isolated stands. Dissemination is primarily through two wild progenitors, Musa acuminata and M. bal- movement of infested planting material (suckers). bisiana. Banana clones (or cultivars) are assigned Ovipositing weevils prefer flowered plants and to genome groups (e.g., AB, AAA, AAB, ABB, crop residues but accept all plant stages. Females AAAA) based on ploidy and the relative genetic are attracted to freshly cut corms, making suckers Banana Weevil, Cosmopolites sordidus (Germar) (Coleoptera: Curculionidae) B 371 detached from banana mats especially vulnerable; and resistant clones and will accept any clone a single larva can kill a young plant if it damages for oviposition. A male aggregation pheromone the growing point. Oviposition rates are usually ­(sordidin) is attractive to both sexes. This has been 0.5–4 eggs per week, although averages of 14 eggs synthesized and is commercially available as lures. per week have been observed. Low fecundity con- The attraction range of semiochemicals is unlikely tributes to the slow build-up of weevil populations to exceed 10 m and may be much less. over time. Monitoring Immature Stages Accurate assessment of banana weevil population Eggs (0.5 × 2 mm) are cylindrical and laid in the levels and damage are necessary for understanding corm and base of the leaf sheaths. Eggs are depos- pest status, screening germplasm and evaluating ited singly in holes (1–2 mm deep) excavated by the impact of intervention strategies. The insect’s the female with her rostrum. Eclosion rates are biology makes assessment and control difficult. 80–100%. Larvae emerging in leaf sheaths usually move to the corm, although feeding in the true stem and, rarely, the pseudostem also occurs. In Damage Assessment the corm, the larvae prefer cortical tissue to the central cylinder. The larvae pass through 5–8 The reclusive behavior of the adults and the instars. Pupation is in a bare chamber near the ­difficulties in measuring larval damage in the inte- plant surface. rior of the corm has resulted in a multitude of In West Africa, developmental thresholds and scoring and evaluation systems. These include thermal requirements were 12°C and 89 degree- monitoring adult numbers through trapping; days for eggs, 8.8°C and 538 degree-days for larvae, ­measuring damage to the corm periphery; and and 10.1°C and 121 degree-days for pupae. Under measuring internal corm damage through cross ambient tropical conditions, stage duration is 6–8 and longitudinal sections. Some of these methods days for eggs, 21–55 days for larvae, and 6–8 days are subjective, making results hard to interpret or for pupae. In addition to temperature, larval stage compare. Moreover, sites of banana weevil attack duration is affected by clone, plant stage, size of may differ among clones. In Uganda, for example, corm, and weevil density. The data suggest the dessert banana Ndiizi (AAB) had similar levels extended periods of low night-time temperatures of damage to the corm surface as that of highland (e.g., at higher elevations) are bottlenecks for cooking banana (AAA-EA), but only 16% as much immature development and/or adult survival. The internal damage within the corm. banana ­weevil is rarely important at elevations Damage to the corm interior is better related above 1,600 m. to yield loss than damage to the corm periphery, while damage to the central cylinder is more important than damage to the corm cortex. Semiochemicals ­Measuring larval damage in cross sections at the collar (corm-pseudostem­ junction) and 10 cm Both males and females are attracted to hosts by below the collar in recently harvested plants is kairomones containing mono- and sesquiter- ­recommended. A common method is to visually penes. Attraction to corm material is greater than estimate percentage cross section surface area con- to pseudostems. Field observations suggest that sumed by weevil ­larvae in the central cylinder and banana weevils are attracted to both susceptible cortex, respectively. 372 B Banana Weevil, Cosmopolites sordidus (Germar) (Coleoptera: Curculionidae) Yield losses tend to increase over time. In one populations may be as much as 2.5 times higher in trial, yield losses increased from 9% in the plant mulched than in unmulched plots because of more crop to 48% in the third ratoon. In Ghana, weevil favorable soil moisture conditions. damage in plantain stands was often low in spite of susceptible germplasm, favorable temperatures and low management levels. Shifting agricultural systems Pest Status predominated with most plantain abandoned after two crop cycles. As such, short plantation life The pest status of banana weevil was once controver- ­precluded adequate time for weevil populations to sial as many clones are resistant and attack in some build up to damaging levels. Weevil problems (e.g., Cavendish, AAA) is often realized on crop became evident in the few plantations maintained ­residues where damage has no effect on yield. beyond two cycles. ­Meaningful yield losses have now been demonstrated in highland banana (AAA-EA) and plantain (AAB) systems. The banana weevil has also been shown to Population Densities be an important component of yield decline leading to the disappearance of highland bananas in its Adult populations may be monitored using traps ­traditional growing areas in East Africa. made from corm or pseudostem residues. How- Crop establishment may be impeded if plant- ever, interpretation of trap data is difficult as a ing is in an already infested field or if planting multitude of factors (e.g., materials, size, number, material carries eggs and larvae. Plant loss of up location, weather) influence trap catches. There- to 40% has been recorded in newly planted fore mark and recapture studies (using pseu- ­highland banana and plantain stands. In fields dostem traps) are recommended for estimating with minor initial infestations of banana weevils, population densities. Weevils are marked by population build-up is slow and problems may scratching the elytra. In Uganda, densities not appear for several years. In a highland banana among proximal farms ranged from 850 adults/ha trial in Uganda, damage to the central cylinder (1.5 per mat) to 149,000 adults/ha (240/mat), while increased from 4% in the plant crop to 17% in the in Cameroon density estimates for subplots third ratoon. Similarly, in surveys of plantain ranged from 10 to 337 adults/mat. ­systems in Ghana, damage increased from 2% in This within-site variability suggests that man- the plant crop to 7% in the second ratoon. Damage agement plays an important role in regulating will have a greater effect on yield if the same mat weevil populations. Weevil pressure is widely has sustained heavy attack in preceding crop believed to be associated with clonal susceptibility, cycles. Thus, single cycle yield loss trials may management levels, bad drainage, acid or low underestimate weevil importance. For example, ­fertility soils, weedy fields, inadequate sanitation, yield losses in several highland banana trials extended droughts and nematode infestations. went from negligible in the plant crop to 48–60% However, on-farm and on-station studies have within a few years. failed to find strong relationships between weevil Yield loss is reflected in plant loss, reduced damage and management factors or plant stress. bunch weights and dying out of mats. Plant loss Moreover, only a modest relationship (r = 0.22) attributable to banana weevil attack in two high- existed between weevil adult density and damage land banana trials increased from 4% in the plant across 50 farms within one watershed. Population crop to 29% in the third ratoon, while heavily estimates may be a poor indicator of economic damaged plants suffered reductions in bunch status if a high population reflects build-up on weights of 20–45%. In another trial, 35% of residues rather than maturing plants. Also, adult banana mats died out in 5 years in plots infested Banana Weevil, Cosmopolites sordidus (Germar) (Coleoptera: Curculionidae) B 373 with ­weevils, compared to 2% mat loss in con- the time of planting. Once established in the field, trols. This suggests that the weevil can severely it is unclear whether tissue culture plants are reduce stand life. Farmers in central Uganda more or less susceptible to banana weevils than reported that banana weevil had contributed to plants grown from suckers. Paring (removal of reductions in highland banana stand life from >30 the outer corm surface) eliminates most eggs and years to 4 years, while in Colombia the weevil first instar larvae, and exposes weevil galleries, reportedly reduced plantain stand life to two to allowing farmers to reject heavily damaged three crop cycles. ­suckers. Paring cannot remove larvae that have penetrated below the corm surface. Suckers may be dipped in pesticide solutions or pesticides Integrated Pest Management may be applied to the planting hole. Alternatively, Beavueria bassiana formulations can be applied Current research results suggest that no single to planting holes to reduce weevil attack of ­control strategy will provide complete control ­suckers. None of these methods assure elimina- for banana weevil. Therefore, a broad integrated tion of weevils. Adults may already be in the field pest management (IPM) approach, combining a from a previous planting or may invade from range of methods, might offer the best chance nearby plantations. As a result, the benefits of for success in controlling this pest. The compo- clean planting material may be ­limited to a few nents of such a program include cultural control crop cycles. (habitat management), biological control, host Selected cropping systems: Mixed cropping plant resistance, botanicals and (in some cases) systems often result in lower insect pressure by chemical control. reducing immigration rates, interfering with host plant location and increasing emigration rates. However, banana weevils are sedentary insects Cultural Control (Habitat Management) that live in perennial systems with an abundant supply of hosts. Coffee intercrops and residues Cultural controls for banana weevil include clean (e.g., husks) may repel banana weevils but this planting material, selected cropping systems, requires further study. Otherwise there is little improved agronomic practices to promote plant evidence that intercrops or insect-repellent green vigor, crop sanitation (destruction of crop residues) manures (Canavalia, Mucuna, Tephrosia) have and trapping with crop residues. meaningful effects on banana weevil populations. Clean planting material: Infested suckers ­provide the principal entry point of banana ­weevils into newly planted fields. Thus, clean planting Crop Sanitation material eliminates the most important source of infestation in new plantations. The insect’s low Banana residues serve as adult refuges and ovipo- fecundity and slow population growth suggest that sition sites and contribute to population growth. a reduction in initial infestation level can retard In Uganda, 25–32% of adult weevils were associ- pest build-up and damage for at least several ated with prostrate (cut or fallen) residues, while cycles. The use of clean planting has been widely another 10–12% was found in standing stumps. In recognized and promoted. Australia, 60% of adults emerged from residues. Recommended methods include the use of For some clones, banana weevil damage is much tissue culture plantlets, paring and selection of higher on residues than on growing banana plants. weevil-free suckers, pesticides, and entomo- It is widely believed that destruction of crop pathogens. Tissue culture plants are insect-free at ­residues (splitting of harvested pseudostems 374 B Banana Weevil, Cosmopolites sordidus (Germar) (Coleoptera: Curculionidae) and/or removal of corms) lowers overall weevil Biological Control ­populations and reduces damage on standing plants in susceptible clones. In Ugandan field Biological control efforts against banana weevil ­surveys, ­sanitation level had more impact on have included the use of exotic natural enemies ­weevil pest status than any other management (classical biological control), endemic natural practice. In ­on-farm trials, increasing sanitation enemies and microbial control (e.g., entomo- level from low to high for 3 years reduced adult pathogens, entomophagous nematodes). Micro- population density from 52,000 to 13,000 ha−1, bial control agents may require repeated lowered corm damage by 41% and increased applications as biopesticides and entail application yield by 70%. costs on the part of the farmer.

Trapping Classical Biological Control

Traps exploit banana weevil attraction to crop Introduced pests, unimportant in their areas of ­residues. The most common are split pseudostem origin, often reach damaging levels when released traps (30–60 cm lengths split longitudinally and from the control of co-evolved natural enemies. placed flush on the soil surface at the base of The banana weevil appears to fit this pattern. banana mats) and disk-on-stump traps (a piece of Searches in southeast Asia identified histerids cut corm placed on top of a banana stump). Inclu- (Plaesius javanus Erichson and Hololepta spp.), sion of corm material in a trap increases its attrac- staphylinids (Belonuchius ferrugatus Erichson and tivity to weevils. Thus disk-on-stump traps tend Leptochirus unicolor Lepeletier), a hydrophilid to have higher weevil catches than pseudostem (Dactylosternum hydrophiloides MacLeay), a cucu- traps. However, pseudostem trapping is more jid (Canthartus sp.), and a leptid (rhagionid) fly often ­recommended for systematic trapping (Chrysophila ferruginosa (Wied.)) as predators of ­studies because a single harvested plant can only banana weevil. Of these, P. javanus appeared most support one disk-on-stump trap (fixed in space), important. Between 1913 and 1959, 45 attempts while the same plant can provide material for were made to introduce eight natural enemies many pseudostem traps (placed where the farmer from Asia to other banana growing regions in the deems most useful). The effect of trapping on world. P. javanus, for example, was released in weevil ­populations will, in part, reflect trap den- ­Australia, Oceania, Latin America and Africa. sity and trapping frequency. Intensive trapping in In most cases, the predators did not establish and established fields results in a gradual decline in in no case did they provide control. Recent searches weevil numbers with a lag time required before for egg and larval parasitoids in Indonesia came effects are manifested in reduced damage. In a up empty handed. Classical biological control of 1-year study in farmer’s fields in Uganda, weevil banana weevil, therefore, remains an elusive numbers declined by 61% in farms with intensive objective. trapping (1 trap/mat/month), 53% with moderate trapping (0.3–0.6 traps/mat/month) and 38% in farms without trapping. Trapping success was Indigenous Natural Enemies affected by management level and weevil immi- gration from neighboring farms. Although Reported arthropod predators of banana weevil farmers were convinced that trapping was bene­ immatures include nabids, cydnids, capsids, redu- ficial, adoption was low due to resource and viids, mirids, thrips, rhagionids, sarcophagids, labor requirements. ­histerids, carabids, hydrophilids, staphylinids, Banana Weevil, Cosmopolites sordidus (Germar) (Coleoptera: Curculionidae) B 375 ­tenebrionids, labiids, carcinophorids, and formi- penetration through the insect’s cuticle. The fungi cids. Ants appear to be the most promising while can kill the insect through direct attack on the other predators seem of little importance. In insect’s nutrients or through toxic metabolites. Cuba, the myrmecine ants Pheidole megacephala Dead insects kept in moist environment quickly and Tetramorium guineense (Mayr) reduced developed surface growth of mycelia. Beauveria banana weevil populations and damage by bassiana can invade the haemocoel where it 54–69% ­following artificial establishment of ant ­produces a toxin, beauvericin, that reduces colonies in plantain stands. In Uganda, Pheidole ­competition with bacteria and weakens the sp. and Odontomachus troglodytes were most immune system. Strain virulence is often related effective in reducing weevil egg and larval popu- to toxin production. lations in pot experiments. Both species readily Natural rates of infestation are normally entered and removed larvae from galleries in crop low (i.e., <5%). Nevertheless, numerous strains of residues. B. bassiana and M. anisopliae have been demon- strated to kill >90% of banana weevils when applied topically in the laboratory or in pot trials. In Ghana, Microbial Control B. bassiana applications to planting holes reduced damage to suckers, while in Brazil, Colombia, Costa Microbial agents tested against the banana weevil Rica, Cuba and Uganda, applications B. bassiana at include entomopathogenic fungi (e.g., Beauveria the base of established mats in banana or plantain bassiana and Metarhizium anisopliae) and ento- stands reduced weevil populations and/or increased mopathogenic nematodes (e.g., Steinernema spp. yields. In Uganda, transmission from infected to and Heterorhabditis spp.). Entomopathogenic uninfected weevils under field conditions was 13%. fungi and nematodes are most often used to kill While these studies demonstrate field potential, adult weevils. Beauveria bassiana has been estab- cost-effective production and delivery systems still lished as an endophyte, although its potential need to be developed. However, field establishment against banana weevil immatures is not yet clear. of B. bassiana tends to be low, so repeated applica- Although a number of strains of entomo- tions are usually necessary. pathogenic fungi and entomopathogenic nema- Entomopathogenic nematodes in the genera todes have shown promise in the laboratory and in Steinernema and Heterorhabditis have been tested ­preliminary field studies, efficient and economi- against banana weevil, most notably in Australia. cally viable mass production and delivery systems Infective juvenile nematodes enter through ­natural still need to be developed, while the performance orifices (Steinernema) or interskeletal membrane of microbial control agents against banana weevil (Heterorhabditis). After entering the host, the nema- under different agro-ecological conditions is not todes penetrate mechanically into the haemocoel well understood. Only in a few sites have entomo- and release Xenorhabdus bacteria which cause pathogens been reported to establish following ­septicemia and death within 1–2 days. In Brazil, applications in banana fields. Without adequate entomopathogenic nematodes were widespread in establishment, entomopathogens will require plantain stands, but naturally occurring mortality of repeated applications as a biopesticide. This will banana weevils was low and, as with entomo­ entail continued production, distribution and pathogenic fungi, viable delivery systems are an ­storage costs that will be passed on to the farmer. important consideration. The cryptic habitat of The conidia of Beauveria and Metarhizium weevil larvae within living plants makes delivery enter the insect through its spiracles or digestive against these stages difficult; therefore, applications system or by producing extracellular proteolytic, of entomo­pathogenic nematodes should target chitinolytic and lipolytic enzymes which facilitate adult weevils. 376 B Banana Weevil, Cosmopolites sordidus (Germar) (Coleoptera: Curculionidae) The most effective entomopathogenic nema- Antixenosis (nonpreference) is of little impor- tode delivery system, developed in Australia, tance. Laboratory and field studies suggest that ­capitalizes on the weevil’s attraction to cut corms banana weevils (i) appear to be attracted equally and damaged plants. This system employs conical to susceptible and resistant clones, and (ii) will shaped cuts in residual corms, i.e., a cone is cut and accept all clones for oviposition. Clonal attraction removed, and then loosely replaced into the corm. and acceptance (i.e., number of eggs) were not These cuts attracted adult weevils and provided related to damage. In one field trial, oviposition ­thigmotactic stimuli that encouraged them to remain was similar on resistant Pisang awak (ABB) and at the infection sites. The holes also ­buffered the susceptible five highland bananas (AAA-EA), delivery site against temperature extremes and pro- while subsequent damage was 5–25 times higher vided excellent conditions (high humidity, ­moderate on the highland clones. Thus, antibiosis appears to temperatures, protection against ultraviolet light) for be the most important in conferring host plant nematode persistence. The nematodes were released resistance to banana weevil. at a density of 250,000 per hole in a formulation Antibiotic factors are those which negatively including a polyacrylic gel (to reduce water build-up influence larval performance (i.e., poorer survivor- and incidence of nematode drowning) with an adju- ship, slower development rates, reduced fitness). vant of 1% paraffin oil (to encourage the weevils to These factors may be physical (e.g., sticky sap and raise their elytra, exposing the first spiracle for latex, corm hardness), antifeedants, toxic secondary ­nematode entry). However, controls based on plant substances and nutritional deficiencies. To test ­entomopathogenic nematodes are more costly than these factors, banana weevil larvae are ­commonly pesticides in Australian commercial banana systems. reared on potted plants or excised corm material. One difficulty in this system is that resistant factors may quickly break down after harvest or ex situ. Host Plant Resistance For example, Pisang awak (ABB) is highly resis- tant to banana weevil in Indonesia; larvae freely Highland bananas (AAA-EA) and plantains (AAB) feed ­without problems in its residues. Similarly, are most susceptible to banana weevil attack. Some Yangambi- Km5 is highly resistant to banana variability exists among clones within these weevil, often showing no damage in screening­trials, genome groups. Among highland bananas, for yet larvae may be successfully reared on excised example, Atwalira and Kisansa displayed weevil corm material taken from this clone. damage scores two to three times higher than Nevertheless, screenhouse and laboratory those for Mbwazirume and Nakyetengu, while the studies have shown that immature banana weevils degree of penetration into the central cylinder was may have higher mortality, extended develop- greatest for Nakitembe, Namwezi and Musakala. mental periods and lower pupal weights on In screening trials, Ensete appeared to be highly ­resistant clones. Corm extracts from resistant susceptible. However, in Ethiopia where the crop is Pisang awak placed on corm material of suscep- most widely grown, Ensete escapes attack because tible highland banana clones severely inhibited most production is above the weevil’s upper eleva- larval feeding while extracts from other clones did tional threshold. Export Cavendish dessert bananas not. A bioassay-guided separation process of the (AAA) are generally considered resistant, although Pisang awak extract was then undertaken using serious banana weevil problems may occur in some chromatographic techniques. Two of the 16 frac- areas (e.g., southeastern coast of South Africa). A tions obtained were found to be very active against wide range of other banana dessert and brewing weevil larvae. However, the compounds respon- types (AB, AAA, AAB, ABB) are moderately to sible for activity against banana weevil have not highly resistant to banana weevil. been identified. Banana Weevil, Cosmopolites sordidus (Germar) (Coleoptera: Curculionidae) B 377 To date, there have been no attempts to breed Botanical Control bananas or plantains for resistance to banana ­weevil. Conventional breeding of banana is a dif- In Kenya, varying formulations of neem ficult and complicated procedure as the most (Azadirachta indica) seed derivatives (neem widely used clones are triploids and sterile. This seed powder, neem kernel powder, neem cake entails crossing wild diploid and highly fertile and neem oil) applied to banana material greatly males to female triploid clones followed by exten- (i) reduced adult settling on corm pieces, (ii) sive hybrid selection. Nevertheless, there does reduced oviposition rates, (iii) reduced eclosion appear to be useful sources of resistance within the success, (iv) increased larval penetration time, available germplasm. The wild diploid Calcutta-4 (v) extended larval development, (vi) increased (AA), Yangambi-Km5 (AAA) and the hybrid larval mortality, (vii) reduced larval weights, FHIA-03, for example, show high levels of resistance (viii) impeded population build-up in field tri- and might be exploited in breeding programs. Corm als, and (ix) reduced damage in pot and field hardness has been shown to be a key resistance experiments. Neem kernel powder and neem oil mechanism and screening for this trait may assist in appeared toxic to the banana plants and may weevil improvement. Secondary metabolites found have interfered with nutrient and water uptake, in resistant clones also appear to be important. whereas neem seed powder and neem cake dis- Transgenic approaches (i.e., biotechnology) played ­phytotoxic effects only at very high are also being used to develop resistant clones by application rates. Neem applications in farmers’ transforming banana through insertion of foreign fields in ­Tanzania also resulted in reduced dam- genes, in particular cysteine proteinase inhibitors age. In spite of these encouraging results, neem (cystatins) from rice and papaya and toxins derived has not been widely adapted by farmers due to from the bacterium Bacillus thuringensis (Bt). availability and costs. Cysteine proteinases are mid-gut enzymes that many beetles, including banana weevil larvae, use in the digestion of dietary proteins. Cysteine Chemical Control ­proteinase inhibitors are defensive compounds produced by some plants in response to insect Chemical pesticides for control of banana weevil attack or wounding. These inhibitors impede diges- may be applied to protect planting material tion resulting in protein deficiency and stunted (through dipping of suckers or applications in development. Bt has been used as a biopesticide planting holes), periodically applied at the base of in the control of several insect pests. More recently, the mat after crop establishment, and/or applied Bt toxin genes have been inserted into crop plants to pseudostem traps to increase trap catches. to improve resistance. There have been numerous studies on the relative Successful incorporation of cysteine protei- ­efficacy of different insecticides under different nase inhibitors from rice and papaya into banana formulations and application rates, persistence tissue reduced banana weevil larval body weights and the appearance of insecticide resistance in by 60% in 10 d. Current efforts are to insert the banana weevils. At least 45 pesticides have been genes into banana plants. In preliminary bioassays, used at one time or another against banana incorporation of the Cry3A Bt toxin into artificial ­weevil. Insecticide resistance in banana weevil diets resulted in 30% mortality of banana weevil has been documented in ­Australia, Latin America larvae. It is believed that high rates of mortality can and Africa for a range of ­chemicals including ultimately be achieved by pyramiding cysteine cyclodienes, organophosphates, and carbamates. ­proteinase inhibitors and Bt toxins. Research in Cross-­resistance has also been ­demonstrated. this area is on-going. Nevertheless, ­chemicals remain an important part 378 B Band of banana weevil control although costs often Band make them prohi­bitive for subsistence farmers. Pesticides remain the ­fastest action method that A transverse line, usually wide, crossing the body. can be used to bring a weevil outbreak under This term often is confused with “stripe,” a term control. used to designate a longitudinal line running the  Tropical Fruit Pests and Their Management length of the body. The term band is also used to describe an aggregation of insects, usually immature ­grasshoppers or caterpillars, dispersing in the same direction. References

Collins PJ, Treverrow NL, Lambkin TM (1991) Organophos- Band Application phorous insecticide resistance and its management in the banana weevil borer, Cosmopolites sordidus ­(Germar) (Coleoptera:Curculionidae), in Australia. Crop Protect An application in which an insecticide (or other 10:215–221 chemical) is applied in strips, usually to the Gold CS, Peña JE, Karamura EB (2001) Biology and integrated ­planting bed or seed row. pest management for the banana weevil, Cosmopolites sordidus (Germar) (Coleoptera:Curculionidae). Integr Pest Manag Rev 6:79–155 Gold CS, Ragama PE, Coe R, Rukazambuga NDTM (2005) Banded Thrips Selection of assessment methods for evaluating banana weevil Cosmopolites sordidus (Germar) (Coleoptera: Curculionidae) damage on highland cooking banana Members of the family Aeolothripidae (order (Musa spp., genome group AAA-EA). Bull Entomol Res Thysanoptera). 95:115–123  Thrips Kiggundu A, Gold CS, Labauschagne MT, Vuylsteke D, Louw S (2003) Levels of host plant resistance to banana ­w e e v i l , Cosmopolites sordidus (Germar) (Coleoptera: Curculionidae), in Ugandan Musa germplasm. Euphyt- Bandwinged Grasshoppers ica 133:267–277 Kiggundu A, Pillay M, Viljoen A, Gold C, Tushemereirwe W, A subfamily (Oedipodinae) of grasshoppers in the Kunert K (2003) Enhancing banana weevil ­(Cosmopolites sordidus) resistance by genetic modification: a per- order Orthoptera: Acrididae. spective. Afri J Biotechnol 2:563–569  Grasshoppers Nankinga CM, Moore D (2000) Reduction of banana weevil  Katydids and Crickets populations using different formulations of the entomo- pathogenic fungus Beauveria bassiana. Biocontr Sci Technol 10:645–657 Pavis C, Lemaire L (1997) Resistance of Musa germplasm Banks Grass Mite, Oligonychus to the banana weevil borer, Cosmopolites sordidus pratensis (Banks) Germar (Coleoptera: Curculionidae): a review. Info- musa 6:3–9 Tinzaara W (2005) Chemical ecology and integrated mana­ A mite (Acarina: Tetranychidae) pest of grasses, gement of the banana weevil Cosmopolites sordidus including wheat. in Uganda. Ph.D. Thesis, Wageningen University,  Wheat Pests and Their Management ­Wageningen, UR, 184 pp Treverrow NL (1994) Control of the banana weevil borer, ­Cosmopolites sordidus (Germar), with entomopatho- genic nematodes, pp 124–138. In: Valmayor RV, Barb Davide RG, ­Stanton JM, Treverrow NL, Roa VN (eds) Proce­edings of Banana Nematode/Borer Weevil Conference, Kuala ­Lumpur, 18–22 April 1994INIBAP, Any of a number of sharp projections armed with Los Banos, Philippines teeth or hooks. Insects sometimes have spines or Bark Beetles in the Genus Dendroctonus B 379 setae equipped with projections pointed backward Bark Beetles (to the base, or away from the point) that cause them to remain imbedded once contact with them is made. Some members of the subfamily Scolytinae (order Presumably they function in defense, especially Coleoptera, family Curculionidae). against vertebrate predators. Structures bearing such  Beetles projections are said to be barbed, and the occurrence  Bark Beetles in the Genus Dendroctonus of numerous setae is ­sometimes described as barbate. A small barb is called a barbule. Bark Beetles in the Genus Dendroctonus Barber, Herbert Spencer barbara j. bentz Herbert Barber was born in South Dakota on April U.S. Department of Agriculture Forest Service, 12, 1882. His father, an engineer, encouraged his Logan, UT, USA son’s interest in natural history. At the age of 16 he was given employment as an insect preparator at the The genus Dendroctonus (Coleoptera: Curculioni- U.S. National Museum. He worked at such tasks as dae, Scolytinae), originally described by Erichson in arranging the Hubbard and Schwarz ­collection of 1836, currently includes 19 species that are widely Coleoptera, but including a collecting trip with distributed. Seventeen species occur between Arctic Schwarz to Arizona and New Mexico. Although he North America and northwestern Nicaragua, and an was employed continuously at the museum until additional two species are in northern Europe and retirement, his pay was, after some years, and until Asia. Dendroctonus species attack and infest conifer his retirement, provided by the U.S. Department of hosts (Pinaceae) in the ­genera Larix, Picea, Pinus, Agriculture. In time, by association with entomo­ and Pseudotsuga. ­Species within the genus can be logists and through experience, he began to ­publish identified by the host­species they attack, egg gallery results of his own studies. His publications eventually patterns, population behavior, and morphological amounted to some 90 papers. One of the most distinctions. The smallest­species is D. frontalis (male intriguing was on his ­discovery of the strange life his- length 2.0–3.2 mm) and the largest is D. valens (male tory of Micromalthus (Coleoptera: Micromalthidae) length 5.3–8.3 mm). ­Members of the Dendroctonus in which there are several forms of larvae, and that genus, which means “tree killers,” are noted as the some larvae may produce eggs and larvae. He died most economically and ecologically significant spe- in Washington, DC, on June 1, 1950. cies affecting forest ecosystems in western North America. Tree ­mortality resulting from Dendrocto- Reference nus outbreaks can adversely affect timber manage- ment, forest planning, and recreational opportunities. Mallis A (1971) Herbert Spencer Barber, pp 281–283. In: In contrast, disturbance events caused by native bark American entomologists. Rutgers University Press, New beetle species are important drivers of forest succes- Brunswick, NJ, 549 pp sion, foster heterogeneity and biodiversity, promote­ ­biomass recycling, and play a critical role in the fire ecology and overall health of many ecosystems. Barberry Whitefly, Parabemisia Dendroctonus beetles are monogamous, and myricae (Kuwana) spend the majority of their lifecycle in a cryptic habitat beneath the bark of host trees where larvae A whitefly (Hemiptera: Aleyrodidae) pest of citrus. feed within the inner bark or phloem. Relative to  Citrus Pests and Their Management the length of their life cycle, only a short time is 380 B Bark Beetles in the Genus Dendroctonus spent as an adult moving from tree to tree. The commonly used, often with traps, for monitoring majority of the species in this genus is capable of and control of many economically important killing the host tree in one generation. In fact, death ­species in the genus. The complexity of the signal of the host is often a requirement for successful for interruption of aggregation has made it difficult brood production. Although most of the species to identify the chemical makeup of compounds, as are capable of attacking and killing standing, well as, the specific biological action of the ­vigorous trees, recently fallen trees are favored by ­compounds within the population ecology of some species. The female is the colonizing sex in many Dendroctonus species. Consequently, the the majority of Dendroctonus species. After attack current use of synthetic interruptive aggregation of a new host, mating typically occurs in a nuptial chemicals is limited. chamber beneath the bark and an egg gallery is As with most poikilothermic organisms, tem- ­initiated. Adults of a few species, however, mate perature is a strong driving force of Dendroctonus before emerging from the brood host. Eggs are laid population dynamics and an important controller either singly along the sides of the gallery, or in of seasonality. Diapause, which is often tempera- clumps. Egg galleries may be either vertical or ture related, is typically considered the universal ­sinuous, and larvae mine and feed horizontally in adaptation of insects for maintaining seasonality. the phloem, either singly or en mass, depending on However, with the exception of an adult reproduc- the species. Pupation takes place in individual tive diapause in D. rufipennis and D. pseudotsugae, niches within the phloem or in the outer bark of and a prepupal diapause in D. rufipennis, this the host tree. Upon adult emergence, which is usu- physiological timing mechanism appears to be ally ­temperature dependent, beetle dispersal to a absent in the Dendroctonus genus. Instead, new host occurs and the process begins again. ­Dendroctonus seasonality appears to be under Aggregation, which facilitates host selection direct temperature control. Life cycle duration in and mating, is an important life history strategy of the genus is variable depending on the species, most, although not all, Dendroctonus species. latitude, elevation, and microclimate of the popu- Aggregation is often a response to chemicals lation. Species in the south can have as many as ­produced by the host tree, adults from the same or seven ­generations per year, whereas in the north, a different species attacking the host tree, microbes, or at high elevation some species require up to 3 or a combination of these factors. Aggregation on years to ­complete a single generation. Intraspecific a single host tree allows for a mass attack by lati­tudinal differences in many temperature-­ ­conspecific beetles, thereby overcoming the resin associated life history traits exist as well. Global defensives of the conifer hosts. To overcome the climate warming will undoubtedly have significant defenses of healthy, vigorous hosts, many beetles impacts on the distribution and seasonality of the must attack within a short time (1–3 days). Con- Dendroctonus species. versely, trees of poor health may be overcome by Many Dendroctonus species carry spores of fewer beetles (e.g., endemic population levels). symbiotic fungi either passively on the exoskele- Because a single tree is a limited resource, some ton or in specialized structures of the integument Dendroctonus species have evolved a response to a called mycangia. The fungi are disseminated series of chemicals that interrupt aggregation. among host trees via adult Dendroctonus beetles. These chemicals act to space beetle attacks along a Although little research has been conducted on single tree and signal incoming beetles to begin fungal associations of the majority of Dendrocto- attack on another, nearby tree. Synthetic forms of nus species, the work that has been done shows both attractive and interruptive aggregation chem- both a benefit and a detriment to the beetle, icals have been developed for many Dendroctonus depending on the particular fungal associate. species. The attractive aggregant chemical(s) are ­Benefits gained include protecting the beetle brood Bark-Lice, Book-Lice or Psocids (Psocoptera) B 381 from other antagonistic associates, aiding beetles Office, Forest Service, U.S. Department of Agriculture. in overcoming host tree defenses through patho- USDA Forest Service, Rocky Mountain Research ­Station, General Technical Report RMRS-GTR-62 genic action of the fungi, altering the moisture Seybold SJ, Bohlmann J, Raffa KF (2000) Biosynthesis of composition of the phloem, and providing or coniferophagous bark beetle pheromones and conifer ­concentrating nutrients essential for reproduction isoprenoids: evolutionary perspective and synthesis. or development. Can Entomol 132:697–753 Wood SL (1982) The bark and ambrosia beetles of North and Native Dendroctonus bark beetles play signifi- Central America (Coleoptera: Scolytidae), a taxonomic cant roles in long term forest ecosystem function monograph. Great Basin Naturalist Memoirs, Number 6 and structure. However, forest conditions in many Brigham Young University Provo, UT, 1359 pp parts of the Dendroctunus range in North America have changed from conditions that existed prior to pre-European colonization. The result is large Bark-Gnawing Beetles ­landscapes vulnerable to Dendroctonus outbreaks which are often in conflict with current land use Members of the family Togossitidae (order objectives. The formulation of effective manage- Coleoptera). ment strategies for Dendroctonus populations  Beetles requires careful consideration of all aspects of land use including timber production, the urban/wild- land interface, wilderness, watershed, recreation Bark-Lice, Book-Lice or Psocids and wildlife. Synthetic attractive and interruptive (Psocoptera) ­aggregation chemicals and silvicultural options are available for some species to aid in the preven- arturo baz tion and suppression of large scale outbreaks. Any Universidad de Alcalá, MadridSpain action, including no action, should be tightly tied to the management objectives for the landscape The insects of the order Psocoptera (=Copeog- under ­consideration. Restoration of the landscape natha, Corrodentia) are commonly called psocids, to reestablish ecological integrity after an outbreak although outdoor species living on tree trunks and is also important for maintaining long-term branches have been called bark-lice, whereas ­ecosystem health. indoor species, sometimes found in old books,  Mountain Pine Beetle have been called book-lice. The Psocoptera are a  Douglas-Fir Beetle small order of paraneopteran insects (near 4,000  Roundheaded Pine Beetle species have been described around the world) which are found in a wide range of terrestrial eco- systems throughout the world. Most psocids References inhabit trees and shrubs, some others occur in ground litter, others are found on rocks and in the Coulson RN, Witter JA (1984) Forest entomology, ecology nests of birds and mammals. Some live on herbs and management. Wiley, New York, NY, 669 pp and grasses, and a few in moss, whereas others are Mitton JB, Sturgeon KB (1982) Bark beetles in North ­American conifers, a system for the study of evolution- found in caves. Lastly, several species are found in ary biology. University of Texas Press, Austin, TX domestic habitats. The Psocoptera share certain Schowalter TD, Filip GM (1993) Beetle-pathogen interac- morphological features with the lice (orders Mal- tions in conifer forests. Academic Press, London, UK. lophaga and Siphunculata; Phthiraptera of some 252 pp Samman S, Logan J (2000) Assessment and response to bark authors), and these taxa are grouped together in beetle outbreaks in the rocky mountain area. Report to the superorder Psocodea by some authors. Fossil Congress from Forest Health Protection Washington insects identified as psocids have been reported 382 B Bark-Lice, Book-Lice or Psocids (Psocoptera) from as far back as the Permian period in Kansas, epicraneal suture ocelli Russia and Australia. These, together with Jurassic material from Germany and Russia, differ in many antenna ways from more recent forms. So, although these fossils are quite psocid-like, some doubts exist compound about their ordinal placement. The earliest unques- eyes tionable fossil psocids are those from Cretaceous amber. These Cretaceous forms are essentially postclypeus modern and do not show any clear connections anteclypeus with the older fossils of doubtful assignment. labrum

Morphology

maxillary Psocoptera are free-living exopterygote insects palpi ranging in body length from 0.6 to 25 mm, Bark-Lice, Book-Lice or Psocids (Psocoptera), although rarely exceeding 10 mm. ­Figure 6 Head of Stenopsocus stigmaticus in frontal view.

Head cutting edges

The head capsule is large compared to the rest of the body, with a large bulbous postclypeus. The anten- grinding edges nae are long and filiform with 11–50 flagellomeres. The eyes commonly are large and globose, varying from multi-faceted structures down to the complete reduction in a cavernicolous species. Three ocelli Bark-Lice, Book-Lice or Psocids (Psocoptera), are usually present in winged forms, but absent in ­Figure 7 Mandibles of Cerobasis guestfalica. apterous species. The Y-shaped epicraneal suture is prominent. The mouthparts (Figs. 6–10), although The labium has reduced one- or 2-segmented palpi, retaining a chewing function, are specialized. The and the chitinous mentum is divided apically into mandibles are asymmetrical, and each has both lateral halves (paraglossae) by a small protuberance grinding and cutting edges. In the maxillae the (glossa) representing the opening of the salivary cardo is not ­differentiated; the galea is a large, fleshy glands to the exterior. The labrum is simple, with lobe, whereas the lacinia is a narrow, sclerotized rod the distal margin bearing two groups of setae: an (the pick). The lacinia is perhaps the most special- anterior group of 4–10 sensilla, and a posterior ized and characteristic psocid structure. The lacinia group which has some taxonomic value. The palatal may be used to scrape food from the substrate, but lining of the labrum and the anteclypeus is the such has not been directly observed. Some authors ­hypopharynx, which has a characteristic structure. inferred that the lacinae may be used as “picks,” The lingua bears a pair of ventral sclerites (lingual because psocids move laciniae vertically in a man- sclerites) which are connected to the median sitophore ner which suggests this may be so. Also, they appear sclerite by ligaments; these lingual sclerites when to be used to support the head whilst feeding and ­protruding are capable of taking up water from the may act to regulate the depth of feeding on the atmosphere (Fig. 11). The sitophore sclerite is situated ­substrate. The maxillary palpi are 4-segmented. on the ventral surface of the base of the cibarium. On Bark-Lice, Book-Lice or Psocids (Psocoptera) B 383

stipe

maxillary palp

lacinia galea

Bark-Lice, Book-Lice or Psocids (Psocoptera), Figure 8 Left maxilla of Cerobasis guestfalica.

mentum of both winged and apterous psocids is clearly separated from the other thoracic segments. Legs are slender, and hind legs are longer, which allows

paraglosses them to carry out small jumps. The coxae of hind legs are modified in many species by having labial palp ­cuticular projections of various kinds. The most Bark-Lice, Book-Lice or Psocids (Psocoptera), usual are a small blister-like projection on the Figure 9 Labium of Cerobasis guestfalica. inner surface, an ovoid “rasp” bearing rows of small denticles; in some cases near the “rasp,” a rounded lingual sclerites area of similar size can be found. These structures are called “coxal organs” or “Pearman’s organs” (Fig. 12) and the function is unknown, although it has been suggested that they are stridulatory. The small trochanters are articulated with the coxae but their junction with the femora is usually immovable. The femora are simple, but sometimes lingua filament markedly convex on their outer ­surface. Tibiae sitophore may have a row of characteristic ctenidiobothria Bark-Lice, Book-Lice or Psocids (Psocoptera), (setal sockets, having four to ten conspicuous ­Figure 10 Hypopharynx. teeth, with each bearing a simple spine) along the ventral surface. The tarsi are of either two or three the ­dorsal surface of the cibarium wall (opposite the segments (all the immatures possess two segments ­sitophore) is a knoblike process that is believed to and this character remains in some adults); all move against the sclerite in the manner of a mortar and except the apical segment have apical spines, and pestle and facilitate the grinding up food. ctenidiobothria may be present on the basal or all segments. The tarsus terminates in a pair of claws; the base of each claw usually has two ventral Thorax ­projections: the proximal one is setiform and the distal (the pulvillus) is of various forms. Some The thorax unites to the head with a membranous ­pulvilli are greatly expanded, whereas others are and flexible neck. In a general way, the prothorax slender or narrow. Expanded pulvilli can act as a 384 B Bark-Lice, Book-Lice or Psocids (Psocoptera)

filament sitophore labrum

labium

lingual sclerite

hypopharynx Bark-Lice, Book-Lice or Psocids (Psocoptera), Figure 11 Mechanism of absorption of atmospheric water.

coxa

Pearman’s organ

a

trochanter femur

tibiae b rasp

ctenidiobothria

c pulvillus

claw

d claws tarsi Bark-Lice, Book-Lice or Psocids (Psocoptera), Figure 12 Metathoracic leg (a); Pearman’s organ of ­Psococerastis gibbosa (b); ctenidiobothria from a metathoracic tibia (c); detail of a metathoracic tarsus (d). Bark-Lice, Book-Lice or Psocids (Psocoptera) B 385 sucker, enabling the insect to walk on smooth sur- posterior border of pterostigma. The radial sector faces. Most foliage-frequenting psocids have a pul- (Rs) terminates in an apical fork, named the radial villus of this type, whereas most bark-frequenters fork, which is composed of R2 + 3 and R4 + 5, and have a narrow pulvillus. Two pairs of wings contacts the median (M) in the middle of the wing. (Fig. 13) are found in many psocids, although one At this junction, the two veins (Rs and M) may or both pairs may be reduced in size, showing meet in a point, be linked by a short crossvein or ­various states of reduction (brachyptery, microp- be fused for a short length. M usually has three tery) and sometimes absent (aptery). Some species branches (M1, M2, M3). The first cubital vein (CU1) are dimorphic, with macropterous individuals of reaches the posterior border of the wing, sometimes one sex (usually males) and apterous or micropter- simply, but in many psocids it is two-branched, ous individuals of opposite sex (usually females). forming a cell known as “areola postica” (AP),

The anterior wings are larger than the hind pair. At which is bordered by CU1a and CU1b. The presence rest they are held rooflike over the body. The fore and shape of the “areola postica” vary considerably and hind wings are coupled during flight and at in different groups of psocids, and it may be joined rest. Most psocids have simple venation, with few to the median, or fused with it or completely free. crossveins. The second cubital vein (CU2) is morphologically In the forewing, the costa (C) forms the wing distinct from the more anterior veins. It is simple margin. The subcosta (Sc) is often greatly reduced and unbranched. Behind this is one anal vein (1A), to a small vein at the base of the wing (the basal which reaches the wing margin near the same sector) and a short vein closing basally the point as CU2. When the vein 1A reaches the ­margin pterostigma (the distal sector). The radius (R) runs at the same point as CU2 it forms the “nodulus.” In more or less parallel to the costa and forms the a few groups a small second anal vein (2A) is

Bark-Lice, Book-Lice or Psocids (Psocoptera), Figure 13 Wings of Stenopsocus stigmaticus. 386 B Bark-Lice, Book-Lice or Psocids (Psocoptera)

Fore wing Cu2

1A nodulus

stigmapophysis b a Hind wing Bark-Lice, Book-Lice or Psocids (Psocoptera), Figure 14 Stigmapophysis from the ventral surface of the forewing in Cerastipsocus sp (a); joining system of the wings of Lachesilla sp. (b).

­present. The cells take the name of the vein imme- Underside the forewing the distal end of Cu2 pos- diately anterior to them. The one exception is the sess a hook which engages the hind costa in flight. large “discoidal cell” bordered by M and Cu1, and present in the forewing of the family Psocidae and others forms in which AP is joined to M. In the Abdomen hind wing the venation is more reduced. Sc is often

vestigial, R1 reduced and simple, Rs forked in two The abdomen consists of ten segments and the branches as in the forewing, M usually simple but ­terminal region (telson) formed by three lobes: the sometimes having two branches, both cubital veins epiproct which is dorsal and the paraprocts which are simple, and one small anal vein is usually are lateral. In many psocids the last tergite (tg 9 + 10) ­present. As in the forewing, the form of the R-M and the distal half of tergite eight are strongly sclero- junction can be variable. Of particular interest is tized, forming a structure called the clunium. The the fact that in the families Lepidopsocidae and epiproct is, normally, a very simple structure, of Amphientomidae the forewings are typically covered rounded, trapezoidal or triangular shape in both by scales, and give the insect the appearance of a sexes. In some species, the male epiproct bears rows small moth. In this case, the shapes of scales are or fields of hooks or denticles. The paraprocts are sometimes of specific value. Psocids possess two variable in shape. On the dorsal basal region there is independent methods of wing coupling. At rest, often a well-defined area (sensorial field)­containing some species have a protrusion at the base of the long setae each rising from a sunken rosette-like pterostigma on the underside of the forewing, socket. These setae are called “trichobothria” and are, formed from modified trichia and tracheolar rings presumably, involved in the orientation in flight or

of R1; this projection (known as “stigmapophysis”) air currents. Near the apex of the paraprocts of the engages the costal vein of the hind wing in repose Trogiomorpha is a long, thickened spine (anal spur). (Fig. 14). Similar structures for coupling wings in Male genitalia comprise a hypandrium (male repose can be found in the family Lepidopsoci- subgenital plate) and a phallosome (copulatory dae, where it is composed of a row of comb-like apparatus). The hypandrium is an expansion of

teeth on Sc or R1. When they fly, many psocids the 9th sternite, defining a cavity in which lodges have another mechanism for coupling wings. the phallosome. The hypandrium varies from a Bark-Lice, Book-Lice or Psocids (Psocoptera) B 387 broad shield, varying from slightly convex and resembles it in appearance. The external valvulae weakly sclerotized to a strongly convex and heavily are attached to the surface of the base of the dorsal sclerotized, and bearing apophyses of different valvulae, and commonly are broad and setose. The kinds. The phallosome (Figs. 15 and 16) comprises spermapore (female gonopore) opens between the endophallus, the parameres and the aedeagus. the gonapophyses in the 9th sternite. Sometimes The endophallus is a membranous structure which the cuticle around the spermapore is heavily scle- is everted during copula. Its surface is adorned rotized to form a distinct plate (spermapore plate). with small sclerites (radulae). The parameres are The internal structure of psocids resembles symmetrical, sclerotized structures with small that of other insects. The tracheal system usually pores sensilla on the distal end. From each opens to the exterior by means of two pairs of paramere an inner branch often protrudes; these ­thoracic and eight pairs of abdominal spiracles. branches are fused apically, forming a sclerotized Four Malpighian tubules are attached at the posterior arch (the aedeagus). end of the midgut. The nervous system is very simple Female genitalia comprise, in the majority of and comprises the following ganglionar centers: brain, species, a subgenital plate, one pair of gonapophyses subesophageal ganglion, prothoracic ganglion, from the 8th segment (ventral valvulae), two pairs pterothoracic ­ganglion and the abdominal ganglion. of gonapophyses from the 9th segment (dorsal val- The reproductive ­system in females comprises two vulae and external valvulae), the modifications of ovaries, each with three to five polytrophic­ovarioles, the 9th sternite around the spermapore, and the lateral oviducts which open into a larger median spermatheca or “receptaculum seminis” (Fig. 17). duct, and a spermatheca. In the males the testes are The subgenital plate is a extension of the 8th stern- round or three-lobed. ite; commonly it is a large broad plate having the apical margin rounded. However, in many groups a pronounced median posterior lobe is present Systematics which has (Fig. 17) been termed the “egg guide.” The ventral valvulae are shorter than the others, Living Psocoptera are divisible into three well-­ glabrous, and apically pointed. The dorsal valvulae defined suborders: Trogiomorpha, Troctomorpha run parallel to the ventral valvulae, and sometimes and Psocomorpha. The earliest fossils from the

Bark-Lice, Book-Lice or Psocids (Psocoptera), Figure 15 Male terminalia of Mesopsocus unipunctatus. 388 B Bark-Lice, Book-Lice or Psocids (Psocoptera) Lower Permian of Kansas, regarded as Psocoptera by some authors, differ from modern species in wing venation and mouthpart characters. Thus, they have been placed in a distinct suborder, ­Permopsocina. The Trogiomorpha contain the most primitive forms, and the Psocomorpha the most advanced.

Suborder: Trogiomorpha

Diagnostic characters of Trogiomorpha are as ­follows: antennae with more than 20 segments; hypopharyngeal filaments separate, never fused Bark-Lice, Book-Lice or Psocids (Psocoptera), on midline; tarsi of the adults 3-segmented; labial ­Figure 16 Phallosome of Elipsocus sp. palps 2-segmented; pterostigma not thickened

Bark-Lice, Book-Lice or Psocids (Psocoptera), Figure 17 Female terminalia of Metylophorus nebulosus in lateral view (a); detail of the gonaphyses of Metylophorus nebulosus (b); detail of the subgenital plate of Metylophorus nebulosus (c). Bark-Lice, Book-Lice or Psocids (Psocoptera) B 389 or absent; and paraprocts with strong ­posterior (Psyllipsocidae) are exclusively found in domestic spine. situations. Lastly, the Prionoglarididae are a small This suborder (Fig. 18) contains five families family containing three genera (Prionoglaris from into two family groups: Atropetae (Lepidopsocidae, the Palaearctic, Speleketor from the United States Trogiidae and Psoquillidae) and Psocatropetae (Psyl- and Sensitibilla from Namibia) and seven species. lipsocidae and Prionoglarididae). Lepidopsocidae The members of these families live almost exclu- (the major family of the suborder) form a primar- sively in caves or under stones. ily tropical group of bark- and leaf-litter inhabit- ing forms ­recognized by their moth-like appearance caused by the scales that cover their body and Suborder: Troctomorpha wings. Trogiidae comprise species with reduced wings (apterous or brachypterous); this cosmopoli- Characters of Troctomorpha (Fig. 19) are: antennae tan family includes several domestic species, in par- with 14–15 segments, rarely with fewer segments ticular Lepinotus sp., which causes great infestations (the only exception is the Palaearctic genus Nephax in ­granaries and warehouses. Psoquillidae and Psyl- which possess antennae of 13 segments), the flagellar lipsocidae are both small and widely distributed fami- segments beyond the fifth usually with ­secondary lies. Psoquillids are commonly found on bark annulations; hypopharynx with filaments separated whereas Psyllipsocids occur in caves or leaf-litter. only in distal region; tarsi 3-segmented; labial palps Both families include some domestic species; for 2-segmented; forewing, when present, lacking scle- instance, some species of the genus Dorypteryx rotized pterostigma.

Bark-Lice, Book-Lice or Psocids (Psocoptera), Bark-Lice, Book-Lice or Psocids (Psocoptera), Figure 19 Liposcelis bostrychophila ­Figure 18 Trogium pulsatorium (Trogiomorpha). (Troctomorpha). 390 B Bark-Lice, Book-Lice or Psocids (Psocoptera) This suborder contains eight families in two family groups: Amphientometae (Musapsocidae, Troctopsocidae, Manicapsocidae, Compsocidae and Amphientomidae) and Nanopsocetae (Lipos- celididae, Pachytroctidae and Sphaeropsocidae). The largest families in this suborder are the ­Liposcelididae (near 150 species), Amphiento­ midae and Pachytroctidae. The Liposcelididae are a ­cosmo-politan group of apterous psocids (although a few species possess reduced wings) whose mem- bers are recognized by their small size (1–2 mm) and their greatly enlarged hind femora. The family includes a number of common booklice (Liposcelis spp.) found in houses, warehouses and ships holds where they may cause measurable weight loss and quality deterioration in stored grain. Some authors concluded that Liposcelis spp are secondary pests of grain whose diet is supplemented by mold. Outdoor species occur in leaf-litter and under bark. The other families are mainly tropical, occurring in both the Old and the New World. Bark-Lice, Book-Lice or Psocids (Psocoptera), ­Figure 20 Lachesilla pedicularia (Psocomorpha). Suborder: Psocomorpha ­Stenopsocidae and Amphipsocidae. The Caecil- This suborder is characterized by possessing ­ante- iusidae are one of the largest families of Psocop- nnae with 13 or fewer segments, never with ­secondary tera, with nearly 400 known species. It is a family annulations. The labial palpus is 1-segmented, of worldwide distribution, in which most species lacking-basal segment. The hypopharynx has are foliage dwellers. Amphipsocidae (150 species) ­chitinous filaments separated in posterior region. are a large family widely distributed in the Old The forewings usually are present, with­sclerotized World (a few species can be found in the pterostigma. Adults have 2- or 3-segmented tarsi. ­Americas); these psocids are generally found on This very large suborder contains nearly 80% broad-leaved foliage. The group Homilopsocidea of all known species of Psocoptera. It consists of was erected to hold those ­families which could 23 families, in four family groups: Epipsocetae not easily be associated with families in the other (Epipsocidae, Dolabellopsocidae, Ptiloneuridae family groups. The result is a heterogeneous and Cladiopsocidae). Epipsocidae are the largest ­assemblage of 11 families (Lachesillidae, Ectopso- family of this group with 133 described species, cidae, Peripsocidae, Calopsocidae, Pseu-docaeciliidae, mostly tropical and subtropical in distribution. Bryopsocidae, Trichopsocidae, ­Elipsocidae, In some species, females are apterous or brac- Philotarsidae, Mesopsocidae and Archipsocidae). hypterous. Most species live in particularly damp Most of these families are of cosmopolitan situations: under stones, in caves, on dead ­distribution and can be found forming part of the branches in humid forests, or in damp leaf litter. psocid faunas around the world. Lachesillidae The family group Caeciliusetae comprises the consist of more than 250 species (most of them ­following families: Asiopsocidae, Caeciliusidae, living in the Americas), primarily found in dry Bark-Lice, Book-Lice or Psocids (Psocoptera) B 391 foliage. Some species (e.g., Lachesilla pedicularia) Simultaneously, males vibrate the wings or, in are widely distributed, occurring in granaries, apterous species, vibrate the antennae. Courtship warehouses and human habitations, occasionally requires a variable time (2–20 min) and is followed in great numbers. Ectopsocidae and Peripsocidae by mating. The male approaches the female from are two closely related families, and are cosmo- the side or from behind, passes over her in a politan in distribution (although Peripsocidae ­forward direction, then backs underneath, and are more diverse in the Oriental region). Some copulation ensues. The copulation has a variable species of Ectopsocidae (Ectopsocus briggsi) and duration, ranging from the 5–10 s (as observed in Trichopsocidae (Trichopsocus clarus) are commonly Stenopsocus stigmaticus) to 2–4 h in the Trogiidae. found on fruit-bearing trees, and possibly are Copulation length depends on the degree of involved in the transmission of pathogenic fungi. ­complexity of the genitalia, and the sperm trans- Pseudocaeciliidae and Archipsocidae are mainly mission mode. In the species with extremely short tropical groups. Some species of Archipsocidae copulation, the terminalia are very simple and live in massive aggregations under sheets of ­little sclerotized in both sexes. Also, the spermato- webbing that may cover an entire tree. Philotar- phore is directly deposited on the atrium from sidae live on bark or low vegetation. Members which the sperm is transferred to the spermatheca. of this family can be found around the world In other species the coadaptation of the genital but are especially common in the Oriental apparatus is more intense, which explains the long region. Elipsocidae and Mesopsocidae are bark duration of copulation. In the Atropetae and the inhabitants, and also may be found in many Amphientometae, sperm are transferred in a ­liquid types of bushes. Both families are abundant in medium into the spermatheca within a structure temperate regions. called a “sperm packet.” This structure apparently Lastly, the family group Psocetae consists of is formed by glandular secretions of males and four families (Psocidae, Psilopsocidae, Myopsoci- females, a process that lengthens the duration of dae and Hemipsocidae). Psocidae are the largest the copulation. family in the order with near 600 known species. It is a cosmopolitan group of psocids which are, in a general way, darkly colored and live on bark or, Eggs, Oviposition, Hatching, Viviparity, occasionally, on the ground or under stones. Parthenogenesis ­Myopsocidae (near 150 species) are large, tropical Psocoptera living on bark. The members of this Eggs of Psocoptera are often simple, elongate family usually have densely spotted brown wings. ovoids or cylinders without a micropyle, and usually are smooth, lacking any conspicuous sculpture. In the more primitive psocids, however, eggs have Reproductive Biology pronounced areolate folds or a crest on the upper surface. Observations on psocid eggs allow us to Courtship and Mating recognize four categories of egg deposition:

Many observations of courtship in various species 1. Eggs laid bare: (a) webbed, (b) not ­webbed. of psocids show that elaborate behavior patterns 2. Eggs encrusted with material from the ­digestive tract: may be involved, and that behavioral differences (a) webbed, (b) not webbed. may constitute effective isolating mechanisms for closely related species. In a general way, mating it There is a systematic and an ecological basis for is preceded by the male nuptial dance, in which the pattern of egg deposition. Thus, species which the male describes circles around the females. are open bark inhabitants (as Psocidae) lay 392 B Bark-Lice, Book-Lice or Psocids (Psocoptera) unwebbed encrusted eggs, whereas leaf inhabiting dance by the males, which eventually results in species (Caeciliusidae, Pseudocaeciliidae) usually copulation. Meanwhile, the parthenogenetic lay bare, webbed eggs. females remain indifferent. This incompatibility Batch size varies considerably, but egg ­number of the races within the same species could be the is constrained by the fact that two follicles mature rule in all Psocoptera possessing such biologic in each ovariole at once, thus imposing a ­maximum races, driving reproductive isolation of the races. batch size (for example, 12 eggs in Graphopsocus; This ultimately can be responsible for speciation. 16 in Caecilius and Stenopsocus, and 20 in Ectopsocus More recently, in the common domestic psocid briggsi). However, larger batches are occasionally pest Liposcelis bostrychophila dense concentra- laid by such species (32 eggs in the first batch of an tions of small bacterial inclusions have been individual of Graphopsocus cruciatus). This is a found. These bacteria are tentatively identified as rare phenomenon, but occurs because the presence Wolbachia, a genus implicated in changes in of two eggs in an ovariole does not inhibit matura- reproductive function (in which parthenogenetic tion of further follicles. reproduction is included) in many other insect Hatching is accomplished with the aid of a groups. specialized egg burster on the frontal region of the pronymph. This egg burster has the form of a blade or tooth, or a row of several spines. By pushing Postembryonic Development this structure against the egg cuticle, the pro- nymph creates a hatching orifice, and the nymph The juvenile instars of psocids (nymphs) gener- is partially extruded through this orifice. The first ally resemble adults in body form and markings. instar then emerges from the pronymphal cuticle They lack functional ocelli, never have more than attached to the hatching orifice. two tarsomeres, and early instars have fewer Viviparity is an unusual habit in the psocids. flagellomeres than adults of their species. Only a few species are known as viviparous. In the Nymphs of some genera of the families Troctop- best-known viviparous genus of psocids (Archip- socidae, Psocidae and Myopsocidae have gland socopsis), females lack gonapophyses and the hairs, which in some cases retain bits of debris, abdomen may contain more than a dozen embryos thus forming a camouflaging coat over the body in different stages of development. Eggs remain in surface. The usual number of nymphal instars in the ovarian tubules and pass down the common psocids is six for the two sexes, but this can be oviduct to the exterior. reduced to five (micropterous form ofPsyllipsocus Parthenogenesis in psocids is widespread. The ramburii), four (apterous females of Embidopsocus usual form of parthenogenesis is obligatory enderleini) or, more rarely, three (apterous males ­thelytoky, although a few examples of facultative of Embidopsocus enderleini). The reduction of thelytoky are known. This mode of reproduction instars number is frequently associated with alary is known in at least 12 families, representing all polymorphism, in which some species with ­sexual three suborders. However, the situation actually is alary dimorphism differ in instar number between more complex, as demonstrated by Caecilius sexes: the apterous sex having one less instar ­flavidus and Psocus bipunctatus (two European than the macropterous one. Also, the reduction species). These species consist of two races, one of the number of larval stages is generally bisexual and other parthenogenetic. Females of regarded as a case of neoteny, and associated the parthenogenetic race in the presence of males with the reduction of other characters (lack of of the bisexual race provoke no reaction from the ocelli, only two ­tarsomeres and reduction in males, whereas the introduction of a female of the numbers of ctenidiobothria and paraproct bisexual race is immediately followed by a nuptial trichobothria). Bark-Lice, Book-Lice or Psocids (Psocoptera) B 393 Feeding various psocid ­species of the genera Lachesilla, Lepinotus, Liposcelis, Ectopsocus or Rhyopsocus. Psocids are herbivores or detritivores, feeding on Other organisms parasitizing psocids are microflora and organic debris on the surface of nematodes that live in the abdominal cavity, and vegetation and other substrates. They are among fungi of the order Entomophtorales (species of the a relatively small number of insects that actively genus Erynia). exploit these food resources (according to some authors, the psocids together with the Collem- bolans constitute the guild of epiphyte grazers). Parasitoids The primary components of their diet are green algae of the genus Pleurococcus, lichens (espe- The parasitoids of psocids are Hymenoptera cially corticicoles and lapidicoles) and fungal attacking both eggs and nymphs. spores and hyphae. Although it is common to Parasitic Hymenoptera that attack the eggs find pollen grains in their alimentary tract belong to the genus Alaptus (Mymaridae), and (mainly of coniferous trees), detritus of all types include several species. In general, only a few eggs and even remains of dead arthropods (probably of each batch are parasitized, and each egg ­contains already in decomposition) are consumed. A few only a single individual of Alaptus. Some studies psocids are partial predators, taking insect eggs reveal that the proportion of parasitized eggs and possibly scale insects. The differences in the ­varies between 6–10% although in some species of diet depend on the habitat occupied by the Mesopsocus, proportions of 20–70% have been ­species. For example, the bark-inhabiting psocids observed. Parasitic Hymenoptera attacking the feed on pleurococcine algae and lichens. Leaf- nymphs belong to the genus Leiophron (Braconidae: inhabiting psocids feed primarily on small leaf Euphorinae). The proportion of parasitized fungi, and often ingest small amounts of leaf nymphs is sometimes 50–60%, as has been ­tissue with the fungal hyphae. Domestic psocids reported in some populations of Caecilius flavidus feed on mold that develops on the organic matter studied in England. found on furniture in dwellings, and on the rotted wood and the old papers found in basements. Psocids that live in the kitchens of houses become Ectoparasites consumers of stored food (flour, cereals, rice, bags of tea, etc.). The presence of larvae of Acari (genusHauptman - nia) living as ectoparasites on psocids has been mentioned. Some phoretic Acari (Phytoseiidae) Natural Enemies attached to larvae of psocids have also been described. Parasites

The intestine of most species contains gregarines Predators (Protozoa) fixed to the intestinal wall. These ­gregarines are also found in the feces, and can The main predators of psocids are arthropods and infect other individuals. vertebrates. Among the arthropods, numerous spe- Psocids have been mentioned occasionally cies that feed on eggs, nymphs or adult psocids have as intermediary hosts of tapeworms (Cestoda). been reported. For example, several arachnids Cestode larvae of the genera Thysanosoma, (Acari, spiders, Opiliones, pseudoscorpions) and ­Thysaniezia and Avitellina, have been found in numerous representatives of various orders of 394 B Bark-Lice, Book-Lice or Psocids (Psocoptera) insects (Dermaptera, Heteroptera, Neuroptera, Some authors suggest the existence of mim- Hymenoptera [ants], Diptera and Coleoptera) are icry in some species. The best example is the case known. The main vertebrate predators on psocids of Chelyopsocus garganicus, which resembles a are birds. Many bird species include psocids in their beetle, a less consumable species. diet, although they represent only a small fraction of the total insect captures: 1.5% in the diet of swifts (Apus pallidus) that hunt flying insects, or 3.6% in Dispersal the diet of treecreepers ­(Certhia) and nuthatches (Sitta) that hunt on the trunks of trees. Interchange of psocids between different habitats, Occasionally, predation by reptiles has been and extension of habitat or geographical range, mentioned, as in the case of an arboricolous occurs frequently and may result from one or more ­lizard in Chile. of three interrelated forms of dispersal. These are:

1. Aerial dispersal by flight, as revealed by the abundance Defense Mechanisms and frequency of catches in aerial traps (suction traps or Malaise traps). Most psocids possesses features or develop 2. Passive dispersal. Psocids, like many other small behaviors to avoid parasites and predators. These insects, frequently become incorporated in the ae- defense mechanisms can be included in several rial plankton after active take-off, and may be trans- categories: ported over considerable distances. On the other First, defense by hiding is called crypsis. Among hand, phoresy of psocids on vertebrates has been psocids, many examples can be recognized: eggs observed. Psocids have been recovered from the covered with silk and detritus helps reduce detec- plumage of several species of birds, and from rats, tion, nymphs with glandular hairs covering the body chinchillas, puppies and humans. surface to which detritus adheres, and both adults 3. Hitchhiking in vehicles or cargoes. This method is pro- and nymphs with color patterns matching the sub- bably responsible for the broad occurrence of many strate where they live. Protective coloration has been domestic ­species. In fact, most of them are cosmopoli- well studied in ­British populations of the species tan despite being flightless. Mesopsocus ­unipunctatus, providing a case of indus- trial melanism for this species (the darker individu- als are more frequent on trees near industrial areas Ecology as a consequence of differential predation by birds). On the other hand, some cases of mechanical Habitats defenses are known: the ability of the Liposcelidiidae to run backward swiftly, the surprising ­jumping Psocids occupy a wide range of habitats, ­abilities of some species (Dorypteryx, Psocathropos, although the various habitat categories of ­psocids and the females of Cyrtopsochus), or the partial intergrade substantially. The following ecological ­autotomy of the antennal flagellum as have been ­categories hold for a great majority of psocids: observed among some species, such as Prionoglaris stygia. Some species combine two defense methods. For example, Hemineura bigoti blend in well with Trees and Shrubs (Foliage-Frequenting and dried Genista bushes, but H. bigoti also shows a Bark-Frequenting Psocids) ­hiding behavior that consists of revolving around the Genista shoots, thereby keeping out of sight of Most psocids live on trees and bushes, but not all possible predators. occupy the same parts of the plant. So, in a general Bark-Lice, Book-Lice or Psocids (Psocoptera) B 395 way, we can consider two categories of psocids: towards alary polymorphism. The principal ­foliage-frequenting and bark frequenting. ­psocid group of this category is the family The foliage-frequenting habitat has been Liposcelididae. adopted by relatively few species, but some groups use this habitat. Some of them contains species that live on live leaves. The claws of most of these Low Vegetation species lack a preapical tooth, and the pulvillus is broad. With the aid of this pulvillus, psocids moves Some species have a clear preference for low without problems onto flat leaf surfaces. Also, the ­vegetation (herbaceous or woody). This fauna is presence of abdominal vesicles in some species typically found in those ecosystems where low guarantees adherence that is particularly effective ­vegetation predominates (heathers, brooms, gorses, against the action of the wind. Other psocids that thyme, grasses and herbs). Some examples of true can also be considered foliage inhabitants are grass-frequenting psocids are Asiopsocus meridi- those that live on dead leaves, including those that onalis in semi-arid regions of Spain, Peripsocus remain attached to the trees, as well as those that alboguttatus on heaths in southern Britain, or Cae- fall to the ground. This habitat (the dead leaves) cilius antillanus in Brazil. harbors an epiphytic microflora that is attractive to some psocids (members of the families Lache- sillidae and Ectopsocidae). For example, several Litter Brazilian Lachesilla species appear to be closely associated with palm foliage, and their numbers Psocoptera are a small portion of the active are considerably greater on dead foliage than on mesofauna of litter and are encountered in ­litter living fronds. In general, psocid abundance tends habitats in many parts of the world. However, to be greater on dead foliage than on living foliage distribution of litter Psocoptera is extremely vari- if the two types are available together. able. For example, in northern temperate regions Most of the psocids living on trees are bark- only a small part of the total psocid fauna is frequenters. In fact, in some areas, psocids are the found in this habitat, whereas in the southern most abundant animals found feeding on bark temperate zone of South America (Chile), edaphic surface microfloral communities. Some families Psocoptera may be more diverse than arboreal are almost exclusively found on this habitat (Pso- species. Traditionally, the litter psocid fauna has cidae, Myopsocidae, Mesopsocidae, Peripsocidae been included in three ecological categories: and Philotarsidae). In these species, the shape of the claws is different: the claws possess a preapical 1. Primary litter dwellers. These species spend their tooth and the pulvillus is, in general, setiform and entire life in the litter, and do not frequent other with the apex pointed, which favors the attach- ­habitats. Species ­typical of this category are Lepino- ment to a surface more or less rough. Among the tus reticulatus and many species of Liposcelis. psocids living in barks and trunks, an important 2. Secondary litter dwellers. These species have ge- group is the subcortical psocids, which live under nerations in two distinct ­habitats each year, with the bark, where they find food and protection. at least one being in the litter. Some species that They show morphological adaptations for could be included in this category carry out seaso- ­subcortical existence: extreme dorsoventral nal local migrations from the litter onto trees and f­lattening with legs inserted laterally, apterism or vice versa. For example, in a Mediterranean species somewhat thickened forewing held flat on the (Hemineura sclerophallina) the edaphic populations abdomen (rather than in a more vertical position are composed only of nymphs, with a peak during of other arboreal psocid) and a strong tendency July, while the nymphal populations on trees have a 396 B Bark-Lice, Book-Lice or Psocids (Psocoptera) peak during October (adults are found exclusively Bird and Mammal Nests on plants). The edaphic populations are restricted to the dry season when the humidity conditions are, Psocids frequently have been reported from mam- presumably, more suitable for psocids in leaf litter mal and bird nests. For ground-nesting mammals, than in trees. the psocids are primarily leaf-litter species, while 3. Casual litter dwellers. These species do not normally for tree-nesting species the psocids usually are breed in litter, but are ­present intermittently as a re- those occurring on bark. Psocids are common sult of ­falling from trees. inhabitants of bird nests, because psocids find favorable conditions in the bird nests. The associa- Generally, the bulk of primary litter dwellers tion between psocids and the birds in the nest is belong to the more primitive suborders, while not parasitic because the psocids feed on the Psocomorpha are relatively rare in this role. microflorae that grow on the nest material. Most species of psocids living in bird nests are apterous or micropterous and are members of the families Rock Surfaces Trogiidae, Liposcelididae and Ectopsocidae. Less frequently, some psocids species live inside the A few psocids appear to have become specialized nests of other insects. For example, Liposcelis for dwelling on the surface of rocks. This category ­formicaria and Liposcelis myrmecophila occur in includes species that are located under the stones ant nests, Lachesilla pedicularia is found in nests of on soil, as well as species living on the stones of wasps of the genus Polistes, and numerous species walls (for example, on the walls of old houses). In of psocids have been reported in the hives of Europe, members of the families Psocidae, Myo- honey bees. psocidae, and Peripsocidae such as Psocus bipunc- tatus, Neopsocus rhenanus, Myopsocus eatoni and Peripsocus subfasciatus are habitually found in this Domestic Habitats habitat type, although most of such species have broader habitats, either in the litter or on bark with Among the Psocoptera, a considerable number of similar lichen or algal associations. species (predominantly Trogiomorpha and Troc- tomorpha) occur in houses and other buildings, Caves feeding mainly on fungal hyphae, spores of molds, and on green algae. Psocids are common Nymphs and adults of psocids are regularly found ­inhabitants of domestic environments such as in caves. Psyllipsocidae (in Europe the most humid rooms, basements, damp walls and room ­common psocid in caves is Psyllipsocus ramburii) partitions. Psocids are commonly associated with and Prionoglarididae are perhaps particularly char- products in food stores, granaries, warehouses, acteristic of caves. Some authors hypothesize that railway boxcars and ships’ holds. Many species the hypogean fauna (from caves and similar habi- seem to be exclusively domestic, including some tats) had a remote origin in Cretaceous ­tropical for- species of the genus Dorypteryx, Ectopsocus and ests. These forests disappeared during the early Liposcelis (Liposcelis mendax is frequently encoun- Tertiary, as a consequence of climatic change, and tered in rice). Psocids are usually not seriously the fauna moved to colonizing some subterranean unhygienic, causing only minor problems of habitats. In the case of psocids, it has been suggested ­contamination and allergies. Their principal dam- that the Psyllipsocidae (an ancient group) may have age to buildings is their effect on property values: survived by avoiding competition with more recent lawsuits resulting from the presence of psocids forms by inhabiting caves or similar habitats. often prove costly. For example, in a Spanish Bark-Lice, Book-Lice or Psocids (Psocoptera) B 397 coastal town, three ­species of psocids were involved Substrates and Plant "Preferences" in spreading infestation of the alga Pleurococcus on recently constructed buildings, and were the Psocids are not strictly phytophagous because they basis of a legal conflict. feed on the microflora that grows on the plants. However, occasionally they show a certain speci- ficity toward their substrate plant. In a general Ecological Distribution way, this specificity refers to groups of plants. For example, among the foliage-frequenting psocids, a Altitudinal Distribution marked division exists among those that live on conifers and those that live on broad-leaved trees. Although some psocid habitats are distributed Also, they are more frequent on plants with rough over a wide altitudinal range, many of the psocids leaves (Ulmus spp.), or with small leaves that are present are usually limited to a part of this range. easily moved by the wind (Betula spp.). However, In the most comprehensive work concerning alti- among the bark-frequenting species this specific- tudinal distribution of psocids, only two of 53 spe- ity is less marked. The ecological conditions of a cies of psocids found on mango (Mangifera indica) site that favors a type of vegetation can be more in Jamaica were found throughout the plant’s alti- important for psocids than the presence or absence tudinal range of 150–1,200 m. An altitudinal zona- of certain substrate plants. In central Spain, some tion of psocids has also been observed in central well defined psocid communities have been found, Spain between a range of 900–1,700 m. In this in particular those that live in the Spanish juniper case, of the 15 species studied, three showed pref- forests (Juniperus thurifera) and in the Scots pine erences for the low altitude, four were distributed forests (Pinus sylvestris), suggesting that changes mostly at high altitudinal levels, while the remain- in structure and composition of psocid communi- der were distributed throughout the altitudinal ties can be determined by both climate and vege- range. The same has been observed in Swiss tation types. Psocid faunas inhabiting ­different National Park; only 14 of 55 species were taken in plant species are affected by taxonomic related- the upper alpine zone (above 1,900 m) and 24 were ness and by architectural similarities among the not found above the montane level (to 1,500 m). substrate plant species. For example, there are dis- So, from the available data, psocids can be classi- crete faunal communities on ­shrublands ­(Cistus fied into three altitudinal groups: sp., Rosmarinus sp., and Genista sp.), ­junipers (Juniperus thurifera, J. sabina, J. comunis is J. oxyce- 1. eurytopic species, found over most of the range. drus), pines (Pinus pinaster, P. nig ra , P. halepensis, 2. low altitude stenotopes, restricted to ­lower eleva- P. sylvestris) and oaks ­(Quercus faginea, Q. pyrena- tions. ica, Q. rotundifolia). 3. high altitude stenotopes, found at higher elevations only. Humidity Although data are not available from most parts of the world, it seems that individuals at the upper The thinness of the integument of psocids (partic- end of an altitudinal gradient may be larger than ularly in the nymphs) is responsible for the fact those lower down. In Jamaica, there was a linear that most psocids are very susceptible to desicca- increase in the size of females of Pseudocaecilius tion. This means that relative humidity is a limit- citricola and Hemipsocus roseus with increasing ing factor to psocids and that, therefore, high altitude. This tendency is probably due to temper- humidity is desirable. Psocids can ingest water ature gradients. with the food or, exceptionally, as liquid, but it is 398 B Bark-Lice, Book-Lice or Psocids (Psocoptera) generally insufficient to prevent desiccation. How- particularly favorable (namely Lepinotus and Lipo- ever, psocids are able to actively take up water scelis). In general, they have been assumed to cause from the atmosphere. This process (this is not little damage, but the observations on some spe- exclusive of psocids because it is also found in cies of Liposcelis that cause primary damage to some Mallophaga) is carried out with the mouth- stored grain indicate that some species may cause parts. The lingua bears a pair of ventral sclerites) direct economic loss. On the other hand, although which are connected to the median sitophore domestic psocids are generally only contaminants, sclerite by ligaments; these lingual sclerites are the appearance of some species in large numbers capable of taking up water from the atmosphere can cause a direct damage to insect collections, and driving it by means of the tubular filaments herbaria, older books and animal products. Most into the alimentary tract. of these species (genus Liposcelis) are difficult to eliminate because they can survive without food and tolerate unfavorable conditions of tempera- Psocids and Humans ture and relative humidity, recovering their nor- mal activity once the environmental conditions In general, psocids are of little economic and become favorable. Also, as a consequence of the health importance to man. Occasionally they may parthenogenetic mode of reproduction in many of cause human health problems such as skin dis- these species, they are able to multiply in an explo- eases or scalp infestations. The dead bodies of sive way and to expand their population very some domestic psocids in household dust are quickly. Some authors suggest maintenance of rel- responsible for allergies and asthmatic attacks. ative humidity of less than 50% with temperatures Also, several species of psocids serve as intermedi- of 15°C or less, in order to retard development and ate hosts of some cestodes, particularly of the slow the increase in populations. However, though fringed tapeworm of sheep. Psocids also have such measures may be feasible in temperate been revealed to be disease vectors on plants. For regions, they are likely to prove extremely difficult example, Ectopsocus briggsi may occasionally in many tropical areas. Other control measures ­disseminate fungal pathogens on fruit-bearing include the use of insecticides in varied forms; one trees by leaving viable spores in feces deposited on of the most widely used is pyrethrin dust. uninfected sites. As mentioned previously, three species of psocids were involved in spreading infestation of the alga Pleurococcus on recently References constructed buildings. Some species of psocids can be considered to Lienhard C (1998) Psocoptères Euro-méditerranéens. Faune be pests. Among the psocids occurring out-of- de France, 83. Federation Française des Sociétés de doors, the large webs of Archipsocidae have occa- ­Sciences Naturelles (ed) Paris, France, 517 pp, 11 plates Mockford EL (1993) North American Psocoptera (Insecta). sionally required removal due to their unsightliness. Flora and fauna handbook 10. Sandhill Crane Press, Those of Archipsocus nomas in Florida, for exam- Gainesville, FL, 455 pp ple, are sometimes removed by scrubbing larger New TR (1987) Biology of the Psocoptera. Oriental Insects branches and trunks of trees with oil emulsions. In 21:1–109 Smithers CN (1972) The classification and phylogeny of the Europe, the species Lachesilla pedicularia can form Psocoptera. Aust Mus Memoir 14:1–351 dense clouds that are a temporary nuisance. How- Smithers CN (1990) Keys to the families and genera of Pso- ever, most of the psocid species that become pests coptera (Arthropoda: Insecta). Tech Rep Aust Mus are domestic species. Most of the domestic pso- 2:1–82 Smithers CN, Lienhard C (1992) A revised bibliography of cids occur in large numbers in houses or stored the Psocoptera (Arthropoda; Insecta). Tech Rep Aust products when the environmental conditions are Mus 6:1–86 Bates, Henry Walter B 399 Thornton IWB (1985) The geographical and ecological distri- Bat Bugs bution of arboreal Psocoptera. Ann Rev Entomol 30:175–196 Members of the family Polyctenidae (order Hemiptera). Barley Thrips, Limothrips  Bugs cerealium (Haliday)

A thrips (Thysanoptera) pest of some grasses, including wheat. Bates, Henry Walter  Wheat Pests and Their Management  Thrips Henry Bates was born in Leicester, England, on February 8, 1825, and developed an early interest Basal in entomology. At the age of only 17 or 18 he published notes on Coleoptera in the Zoologist. A term used to refer to the base or point of attach- At about the age of 20, he met Alfred Russel Wal- ment, or the portion of the appendage nearest the lace, who was then teaching English in a school main body. in Leicester and had an interest in botany. Through the influence of Bates, Wallace began to collect beetles. In 1847, Wallace proposed a trip Basalare to Pará, Brazil, to collect insects and other natu- ral history objects, having read W.H. Edwards’ A small section above the principal pleuron, anterior “Voyage up the Amazon”. These two explorers, to the wing, to which flight muscles are inserted. together with Bates’ brother, sailed from Liver- pool for Pará in April 1848. They intended to Base Pair (bp) support themselves by the sale in Europe of natu- ral history objects that they expected to collect in Two nucleotides that are in different strands of Brazil. Many ­hardships ­followed. These included nucleic acid and whose bases pair by hydrogen his affliction with yellow fever, the death of Bates’ bonding. In DNA, adenine pairs with thymine and brother, and the loss at sea of Wallace’s first col- guanine pairs with cytosine. lection of natural ­history objects. Nevertheless, he persevered (Wallace traveled separately after Basement Membrane the first 2 years, and departed from Brazil years sooner than Bates), and assembled large collec- tions, including over 14,500 species of insects, of A noncellular layer that separates the epidermal which 8,000 were new to science during the 11 cells from the hemolymph. This membrane is the years that he spent in Brazil. He returned to Eng- innermost layer of the integument. land, worked on the specimens he had collected,  Epidermis and published. In 1861 his paper “Contributions  Cuticle to an insect fauna of the Amazon Valley”; was read before the Linnean Society. It explained Basic Reproductive Rate mimicry (see Batesian mimicry). In 1863, his two-volume book “A naturalist on the river Ama-

(R0) The average number of offspring produced by zons”; was published by John Murray with an a population of individuals over the entire course introduction by Charles ­Darwin, to great acclaim. of their life. These works resulted in his being offered the job 400 B Batesian Mimicry of assistant secretary to the Royal Geographical environmentalism. His books include (1949) “The Society in 1864. This at last freed him from finan- natural history of mosquitoes”, (1950) “The nature cial worry, but reduced the time available for him of natural history”, and (1955) “The prevalence of to work on his Amazonian insects. He later con- people”. He died on April 3, 1974. tributed (1881–1889) volumes to the series ­“Biologia Centrali-Americana”;, ­published numerous other works, and was twice president References of the Entomological Society of London. He died on February 16, 1892. Anon (2002) Marston Bates. Available at http://www.­ netwalk.com/~vireo/bates.html. Accessed Aug 2002 AN Marquis Company (1968) World who’s who in science. AN Marquis Company, Chicago, IL Today in Science History (2002) Marston Bates. Available References at http://www.todayinsci.com/7/7_23.htm. Accessed Aug 2002

Sharp D (1892) Henry Walter Bates, F.R.S. Entomologist 25:7–780 Woodcock G (1969) Henry Walter Bates. Naturalist of the Bat Fleas Amazons. Fader and Fader, London, 269 pp

Members of the family Ischnopsyllidae (order Siphonaptera).  Fleas Batesian Mimicry

Resemblance of a palatable insect to a less palat- able one, a process that benefits the palatable Bat Flies mimic by reducing predation.  Mimicry Members of the families Streblidae and Nycteribi- idae (order Diptera).  Flies Bates, Marston

Marston Bates was born in the state of Michigan, B Chromosomes USA, on July 23, 1906. He graduated from the University of Florida with a B.S. degree in 1927. B chromosomes are non-vital supernumerary He worked for the United Fruit Company in chromosomes found in many organisms. They are 1928–1931. He entered Harvard University and thought to be derived from normal chromosomes, was awarded an A.M. degree in 1933 and Ph.D. in and often transmitted at higher rates than expected, 1934. In 1935–1937 he worked as a research assis- thus exhibiting “drive.” tant at Harvard. In 1937–1952, he worked at vari- ous laboratories of the Rockefeller Foundation, and his studies of mosquitoes in northern South Beach Flies America contributed to an understanding of epi- demics of yellow fever. In 1952–1971 he was a fac- Members of the family Canacidae (order ulty member of the University of Michigan. He Diptera). contributed much to ecology of mosquitoes and to  Flies Beauveria B 401 Beaded Lacewings is the discovery that a 25 million-year-old worker ant embedded in amber was covered with a fun- Members of the family Berothidae (order gus similar to present day B. bassiana isolates. Neuroptera). The infective propagules, the conidia of Beau-  Lacewings, Antlions and Mantidflies veria, are dry, hyaline (colorless), and globose to oval in shape (Figs. 21 and 22). The conidiophores can occur singly or can be grouped in irregular Beak clusters or in whorls; the base of the conidiophore is inflated or flask-shaped, with conidia borne on A prolongation of the head, usually referring to a distinctive apical zigzag extension (rachis). Like the snout of weevils. This term also is used to other entomopathogenic hyphomycetes, B. bassi- describe the jointed piercing-sucking, or sucking, ana conidia initiates infection of host insects at mouthparts of Hemiptera. the outer integument, although invasion through the alimentary tract has been reported in certain ants and termite hosts. Successful infection by B. bassiana by cuticular penetration depends Beauveria upon a number of factors. For example, younger insects are usually more easily infected than older Jacqulyn c. pendland, Drion g. boucias larvae. Specific Beauveria strains are infectious to University of Florida, Gainesville, FL, USA adult insects such as grasshoppers, as well as to insects undergoing a molt. The type of plants that The genus Beauveria (Deuteromycota) includes the target insects consume is also important since several entomopathogenic species, the most some plants produce compounds inhibitory to notable being B. bassiana. Beauveria has a fungal growth. Conidial germination on a suscep- worldwide distribution and has a wider host tible host requires optimal temperature and range than the other Deuteromycetes infect- humidity (>75%). Conidia, for example, will not ing insects from most orders. In addition to infect overwintering adult Colorado potato bee- B. bassiana, three other species, including tles because the soil is too dry and cool; however, B. brongniartii (=tenella), B. relata, and B. amor- ­post-emergent beetles can become infected later pha have been identified. The latter two species in the spring when conditions are more favorable. are South American isolates from Lepidopteran Even if conditions are optimal for the germina- larvae and Coleoptera, respectively. Beauveria tion and penetration processes, B. bassiana brongniartii (B. tenella), found predominantly conidia must first bind to the host cuticle after in soil-inhabiting insects, has been described as contact has been made. Attachment, as in the case a naturally occurring pathogen of mosquito of other fungi that produce dry conidia, is likely larvae. Beauveria bassiana, the white muscar- due to the hydrophobicity of both the conidial dine fungus, was observed around 900 a.d. in and cuticular surfaces. In B. bassiana, conidial silkworms in Japan. Insects mummified by hydrophobicity can be attributed, at least in part, B. bassiana also were used for medicinal pur- to the presence of a hydrophobin-type protein poses, e.g., as an antiseptic for wounds and sore in the outermost rodlet layer. In addition to throats. Importantly, it was through a study of attachment, conidial surface hydrophobicity may this fungus that the germ theory of disease (i.e., prevent desiccation of the propagules and aid the idea that microorganisms could cause infec- in their dispersal. Fungal enzymes may help to tious disease in animals) was postulated by consolidate attachment of B. bassiana conidia A. Bassi in 1834. Also of historical significance to host cuticle. 402 B Beauveria

Beauveria, Figure 21 Adult mole cricket, Scapteriscus­ vicinus, infected with Beauveria bassiana. Note the external conidiospores emerging from the head, thorax, and leg regions.

Beauveria, Figure 22 Scanning electron micrograph of the conidiophore of Beauveria bassiana.

Under the proper conditions, germination of enzymes. There are several classes of enzymes B. bassiana conidia occurs within hours. Studies produced by B. bassiana during germination, have shown that different strains of B. bassiana including proteases, chitinases, and lipases that produce different amounts of cuticle-degrading function in the breakdown of host cuticle. Beauveria B 403 Penetration of insect cuticle (e.g., Helicoverpa tospores show both a reduction in the overall zea) by B. bassiana germ tubes usually does not number of immunocompetent granular hemo- involve the formation of appressoria. Once the cytes and a suppression in their abilities to spread germ tubes penetrate the cuticular and epidermal and form filopodia. regions, the fungus grows towards the hemocoel, In addition to being a ubiquitous soil ento- where blastospores become evident at about 48 h mopathogen, certain strains of B. bassiana have post-infection. In vivo produced blastospores, been reported to be endophytic and colonize unlike in vitro cells, lack a formal cell wall and plant tissue. Unlike most insect mycopathogens, contain a thin fibrillar layer on the plasma mem- B. bassiana has been associated with fatal respi- brane. In Heliocoverpa zea, there is very little tis- ratory infections in some cold-blooded animals, sue damage until 60–70 h post-­infection, when including tortoises, crocodiles and American the fat body may show some signs of deteriora- alligators. One strain causes the rupture and/or tion. The gut and Malphigian tubules can become death of fish embryos due to attachment of the affected at 6–7 days, when death and mummifica- conidia to the chorion with subsequent germi- tion also occur. However, the gut, muscle, silk nation and penetration of the fungus. A second glands, and tracheae can remain intact during the strain tested also caused teratogenic responses, entire infection process. Death is likely due to including abnormalities in embryos. As a result nutrient depletion, dehydration, and/or toxin of these tests, there is some concern that large- production by the fungus. scale applications of B. bassiana conidia could Host response to Beauveria invasion varies, be harmful to aquatic ecosystems. Infections in of course, depending upon the insect and its sus- the lungs and nasal passages of mammals have ceptibility to the particular isolate used. Melanized been reported but are rare since the fungus patches (dark spots) can occur on the cuticle at probably does not grow well at 37°C; however, the penetration site, thus indicating the induc- B. bassiana can cause allergic reactions in some tion of phenoloxidase activity in the insect. In people. grasshoppers injected with B. bassiana conidia, Beauveria conidia from field-collected levels of phenoloxidase in the hemolymph were cadavers can be inoculated onto mycological found to increase by 24 h post-treatment. After media such as SMY agar or broth and main- topical application with conidia and penetration tained in culture by transfer at regular intervals of the cuticle, as the fungus reaches the hemo- to fresh media. Beauveria, less fastidious than coel, host immunoreactive hemocytes may sur- Nomurea rileyi, can be grown on oatmeal agar round the hyphal tip and further melanization or potato dextrose media, and stored at ­ultra-low reactions can occur. If B. bassiana cells become temperatures (-70°C). Isolation of Beauveria surrounded by hemocytes either via phagocytic from a soil environment may require the and/or nodulation or granuloma-type mecha- ­selective media containing antibiotics such as nisms, the fungus can still remain viable as an streptomycin, ­tetracycline, gentamycin and intracellular parasite, and later emerge from the cycloheximide to eliminate bacterial growth insect blood cells to continue growth and replica- and N-dodecylguanidine acetate (dodine) to tion in the hemocoel and tissues. Thus, B. bassi- inhibit growth of other soil fungi. ana can overcome host cellular defense response Due to its broad host range, including mem- even if it has already been initiated, and as bers within the orders Lepidoptera, Coleoptera ­mentioned earlier, some ­toxins produced by the and Hemiptera, and to the fact it is cultured eas- fungus appear able to suppress such responses ily on inexpensive media, B. bassiana has long (phagocytosis, nodulation) entirely. Spodoptera been targeted as a potential biocontrol agent. exigua larvae injected with B. bassiana blas- Insect pests such as the Colorado potato beetle, 404 B Beck, Stanley Dwight Leptinotarsa decemlineata; European corn borer, in a lumber mill for a year to save money to pay Ostrinia nubilalis; codling moth, Laspeyresia for a university education. With those funds, he pomonella; Japanese beetle, Popillia japonica; entered Washington State University to study European cockchafer, Polyphylla fullo; chinch biology, and earned a B.S. degree in 1942. He bug, Blissus leucopterus; and the European cab- then served 3 years in the U.S. navy. From 1945 bageworm, Pieris brassicae, are susceptible to to 1950 he was a graduate student at the University B. bassiana. However, the inability to produce of Wisconsin at Madison, earning an M.S. degree and formulate fungal propagules that are stable in 1947 and a Ph.D. in zoology in 1950. At the and provide consistent mortality rates in con- same university, he was appointed assistant stantly changing biotic and abiotic conditions professor in 1950, a full professor in 1964, and has restrained large-scale development of this a distinguished professor in 1969. He taught a mycopathogen. For example, over the years both course on insect physiology. His research inter- B. bassiana and B. brongniartii have been targeted ests were in host-plant resistance to pests, and to control some soil-inhabiting insects, but due insect nutrition and metabolism. His publica- to this hypogean environment, Beauveria is tions were 138 scientific papers and several placed in direct contact with the antagonistic books including (1963) “Animal photoperiod- soil microfauna that can be lethal or can inhibit ism” and (1968) “Insect photoperiodism”. He its growth. received several awards, was elected to the U.S. National Academy of Sciences in 1988, and served as president of the Entomological Soci- References ety of America. His accomplishments were the more remarkable because by 1952 he was essen- Bing LA, Lewis LC (1992) Endophytic Beauveria bassiana tially paralyzed by poliomyelitis and was con- (Balsamo) Vuillemin in corn: the influence of the plant growth stage and Ostrinia nubilalis (Hübner). Biocontr fined to a wheelchair for the rest of his life. He Sci Technol 2:39–47 died on July 8, 1997, in Madison, Wisconsin, Boucias DG, Pendland JC (1991) Attachment of mycopatho- survived by his wife, Isabel, and three of his four gens to cuticle. In: Cole GT, Hoch MC (eds) The fungal daughters. spore and disease initiation in plants and animals. ­Plenum Press, NY, pp 101–127 Hung S-Y, Boucias DG (1992) Influence of Beauveria bassiana on the cellular defense response of the beet armyworm, Spodoptera exigua. J Invert Pathol Reference 60:152–158 Middaugh DP, Genthner FJ (1994) Infectivity and teratoge- nicity of Beauveria bassiana in Menidia beryllina Wedberg J (1998) Stanley D. Beck. Am Entomol 44:127 embryos. Arch Environ Contamin Toxicol 27:95–102 Pendland JC, Hung S-Y, Boucias DG (1993) Evasion of hose defense by in-vivo produced protoplast-like cells of the insect mycopathogen Beauveria bassiana. J Bacteriol 175:5962–5969 Bed

In modern agriculture, a raised area of soil into which crops are planted (planting bed). Beds are Beck, Stanley Dwight bounded by furrows which sometimes are used to deliver irrigation water to the beds. In tradi- Stanley Beck was born in the state of Oregon on tional agriculture, a bed (seed bed) is also an area October 17, 1919, but grew up in the adjoining used to grow seedlings for later transplant into state of Washington. As a young man he worked fields. Bed Bugs (Hemiptera: Cimicidae: Cimex spp.) B 405 Bed Bugs (Hemiptera: Cimicidae: caves where humans began their cohabitation Cimex spp.) with the ancestral bed bug. As humans began to practice agriculture (8000–5000 b.c.) within the dini miller “fertile crescent” (present day Iraq), people Virginia Tech University, Blacksburg, VA, USA moved from their cave dwellings into villages near their agricultural fields. It has been specu- The Cimicidae are obligate blood feeding ecto- lated that bed bugs were transported into these parasites of humans and other animals. There are newly civilized environments, thus becoming 74 species of cimicids, including the human bed permanently associated with humans and human bugs, bat bugs, chicken bugs, swallow bugs, and dwellings. pigeon bugs. Cimicids are organized into 22 gen- era and 6 subfamilies. Of the 22 genera, 12 have evolved to feed exclusively on bats while another 9 Morphology genera feed exclusively on birds. There is only one genus, Cimex, which contains species that feed on Adult bed bugs are easily identified by their brown- multiple hosts, typically specializing on birds, bats, ish red color and their lack of wings. The body is or humans. Of all the cimicid species only three broadly flattened and ovoid, typically 5–8 mm in feed on humans. These include Leptocimex boueti length and about 4 mm wide. Because the adults Brumpt, a West African species that feeds on only have wing pads, the first 11 dorsal abdominal humans and bats; Cimex hemipterus F. (tropical segments are usually easy to see when the body is bed bug), found in both the new and old world not engorged. tropics feeding on humans and chickens; and The morphology of the bed bug head is very Cimex lectularius L. (common bed bug), which is similar to that of other cimicids. The multifac- found all over the world and feeds on humans, eted eyes of the bed bug look like small knobs chickens and bats. protruding from the sides of the head. The anten- Cimicids that feed on humans get their com- nae of the bed bug are 4-segmented and project mon name “bed bugs” from their long history of forward from a small protuberance between the harboring in human dwellings, particularly in eye and clypeus. The third and forth segments of those locations where the host would come to rest the antennae are thinner than either the basal or at night (bed or bedding). By harboring in the second segment. “bed,” the bugs could feed undisturbed while the The most prominent feature on the head is host was asleep. the labrum. The labrum extends out from the While the origin of the bed bug is unknown, clypeus at the extreme anterior of the head and it is thought that human bed bugs were originally is marked with a labral suture. The labium arises ecto-parasites of bats. When humans moved into just below the labrum, at the anterior margin of caves and either lived with the bats or removed the head, and has three segments. When the them, the bat parasites adapted to the presence of labium is held at rest (under the bed bug head), the new host. Those bat bugs that survived and the ventral side of the labium contains a longi- proliferated on human blood continued to inhabit tudinal groove which holds a fascicle of man- human environments. dibular and maxillary stylets. Between the The exact geographic origin of human bed maxillary ­stylets are a large food canal and a bugs is also unknown, but both Neanderthal smaller salivary canal. The food canal and the man (100,000 years ago) and, later, Cro-Magnon stylet fascicle are connected with the cibarial man (12,000 b.c.) populated caves in the Middle pump inside the head of the bed bug. The 3-seg- East. It is most likely in these Middle Eastern mented labium, including the maxillary and 406 B Bed Bugs (Hemiptera: Cimicidae: Cimex spp.) mandibular stylets and the food and salivary Life Cycle canals, are collectively referred to as the ros- trum (Fig. 23). The rostrum pierces the host’s The bed bug life cycle is unique in that it begins skin and the cibarial pump is used to pump the with an unusual form of copulation known as blood from the host into the head of the traumatic insemination. Unlike other hemipter- bed bug. ans, Cimex males never insert their copulatory The pronotum of the bed bug is very distinct organs into those of the female. Instead the male and the shape or hairiness of the dorsal side is awkwardly mounts the female’s back and wraps often used for species identification. In general his abdomen around the right side of her body. the pronotum is broad, surrounding the base of He then punctures her body wall, wounding the the head within the concave anterior margin. female as he inserts his copulatory organ into her The sides of the pronotum extend up around the paragenital sinus or “Organ of Berlese” to inject base of the head in a wing-like fashion. his sperm. Mating usually lasts for several min- The abdomen of the adult bed bug consists utes but can last up to half an hour in some cases. of 11 segments and is completely sclerotized. Within 2 h of mating the male spermatozoa pass ­However, the sclerotized abdomen is capable of from the female Organ of Berlese into her enormous expansion due to the wide interseg- ­abdominal cavity. Once in the hemocoel, the mental membranes and the “hunger folds” (ven- ­spermatozoa accumulate at the base of the tral ­membranous sections) located within the ­oviducts, moving into the seminal conceptacles second and fifth abdominal segments. The within 12 h. female ­reproductive organs (gonapophyses) are After mating, a female held at 23°C will begin homologous to the ovipositor found in other to produce eggs within 3 days. Several sources species and are located on the ventral side of the have indicated that female bed bugs, when fed reg- 8th and 9th abdominal segments. The female ularly, are able to produce viable eggs for 5–7 weeks spermalege or paragenital sinus appears as a after a single mating. However, mated females will notch located on the ventral side of the abdo- usually cease oviposition after about 11 days with- men between the 5th and 6th segments. The out an additional blood meal. Under laboratory genitalia of the male bed bug also originate on conditions (23°C and 75% RH) a ­typical female the ventral side of the abdomen near the apex. that has been fed and mated regularly can produce The male abdomen is narrower at the apex than 3–4 eggs every day averaging more than 200 eggs that of the female and the 9th segment is longer total over her entire lifespan. Under natural condi- and asymmetrical. The male paramere is tions fecundity can be quite variable, depending strongly curved to the left and lies in a groove not only on the availability of mates but also tem- within the 9th segment. perature and nutrition. Egg production is closely Immature bed bugs differ from adults in their correlated to ambient temperature, the weight of morphology in several ways. First, they lack the the unfed female, and size of the female blood characteristic reddish color of the adults. Nymphs meal. An increase in temperature from 17 to 23°C are typically translucent white, making their inter- has been shown to produce as much as a ten-fold nal structures visible after a blood meal. Nymphs increase in weekly egg production among well fed, also differ from adults in that not all of their mated females. The mean weight of unfed females abdominal segments are sclerotized, particularly also influences egg production. As expected, larger on the ventral surface of the abdomen. Nymphs females produce more eggs. Also, because larger also have a 2-segmented tarsus while the adult females tend to take larger blood meals, the size of ­tarsus is 3-segmented. Finally, immature bed bugs the blood meal has also been shown to result in lack any structures associated with reproduction. increased egg production. Bed Bugs (Hemiptera: Cimicidae: Cimex spp.) B 407

Bed Bugs (Hemiptera: Cimicidae: Cimex spp.), Figure 23 The common bed bug, Cimex lectularius: (a) ­ventral morphology of adult bed bug head showing the rostrum, pronotum, and antennae; (b) adult female bed bug; (c) engorged adult and early instar bed bugs; (d) partially fed first instar bed bug with egg cap on head; (e) first instar bed bug emerging from egg. 408 B Bed Bugs (Hemiptera: Cimicidae: Cimex spp.) Oviposition occurs 3–6 days after mating. extended to 4 months or more depending on the The bed bug eggs are about 1 mm in length, ambient temperature and the availability of white, elongate, and slightly bow shaped. Upon ­regular blood meals. oviposition, eggs are coated with sticky cement that dries quickly causing them to adhere to the substrate on which they were deposited. The eggs Behavior are typically laid in cracks and crevices near a harborage site and take 6–10 days to hatch, Bed bugs are thigmotrophic and seek out har- although temperature variation may alter hatch borages where their bodies can be in direct con- time. As a first instar bed bug emerges from the tact with surrounding surfaces. They are often egg, anti-peristaltic movements of the gut drive found aggregating in cracks and crevices of fluid into the head, deploying hatching spines to homes and other structures, or wedged into dislodge the egg cap. After hatching, most first mattress tufts or staple holes where they can instars will stay near the egg capsule until they remain undisturbed. In hotel rooms they are leave in search of their first blood meal. Several often found behind removable headboards or studies have indicated that bed bug survivorship picture frames hanging on the wall. They can is closely linked to the amount of energy they also be found hiding in the wood frames of the have to expend searching for a host. This is par- box springs or the stuffing. In some heavy infes- ticularly true for first instars. While quite ambu- tations, the best harborages are already filled so latory for their size, first instars are at great risk many bed bugs will take up residence along of dehydration compared to the older life stages. baseboards, behind posters on the wall, or under Therefore, we can assume that many first instars the carpet tacking. Bed bugs will typically avoid are lost before they ever consume their first locations exposed to air movement but may be blood meal simply because they hatched too far seen aggregating in the open on the ceiling or at from a host. the ceiling/wall junction if no other space is Bed bugs have five nymphal instars, each available. The stimulus that prompts bed bugs requiring a blood meal to complete develop- to leave their harborages is not well understood ment. Each nymphal stage can feed within 24 h but ­obviously they have to leave in order to feed. after molting and all bed bugs are typically After feeding, bed bugs will return to these same stimulated to feed at slightly less than weekly ­harborages after their meal and remain there intervals. At higher temperatures (27°C), the while digesting. The digestion period after feed- feeding interval can be reduced to every 3 days, ing results in the accumulation of fecal material and all nymphal instars molt more quickly when (black spots of dried blood) in preferred har- exposed to warmer temperatures. In studies borage locations. conducted on nymphal stages 1–5, it was found Bed bugs are nocturnal, usually avoiding the that the mean number of days between the light. Studies have indicated that bed bugs are most blood meal and molting ranged between 2.1 active after 3:00 a.m., a time when the host would days at 35°C and 26 days at 15°C. Ordinarily, most likely be in a deep sleep. However, bed bugs nymphal bed bugs will feed once per instar, will feed during the daylight hours if they are hun- with each instar lasting 3–5 days at optimal gry and a host is available. The question regarding temperatures (23°C). If insufficient blood meals how these nocturnal insects are able to navigate are taken, secondary blood meals will be neces- between the host and their harborage is quite con- sary before molting can occur. So although the troversial. Little is known about bed bug vision, average time from egg to adult is often reported but it is suspected that they do not see well because as about 1 month, that time period can be of their nocturnal and parasitic lifestyle. Bed bugs Bed Bugs (Hemiptera: Cimicidae: Cimex spp.) B 409 are thought to use pheromone and odor cues for treatment, and may have had some potential for navigation. However, bed bugs have been tested repelling bed bugs away from the sleeping host. repeatedly and have never been observed to detect However, the snap bean (Phaseolus vulgarius) has heat sources or host odors over distances >12 cm. demonstrated true potential for bed bug control. Several researchers have suggested that bed bug In the Balkans, the leaves of this bean plant were searching behavior in the natural environment placed under the beds in infested rooms. Foraging must be completely random. However, others bed bugs would become entangled in the hairs on claim that random searching would be too costly the bean leaves during the night. In the morning, for bed bugs to have achieved their obvious repro- the leaves were simply swept up and burned to ductive success. Regardless of how bed bugs detect destroy the bed bugs. While the practice of sleep- their food source, there is no question that they ing over bean leaves most likely provided at least have evolved to take advantage of the diurnal some bed bug relief, the ancient remedy of hang- nature of the human host. They feed at night when ing the feet of a dead stag or rabbit at the foot of the host is unconscious, thereby increasing their the bed (as host decoy), probably had little effect. chances of feeding to repletion. After feeding they Another folk method of bed bug prevention that is quickly abandon the host and return to their har- still used today is to place the legs of the bed frame borage where they remain during the daylight in pans of water or kerosene. Although this method hours, thus decreasing their chances of being is thought to work, there have been many anec- detected. dotal references to bed bugs circumnavigating these barriers by crawling up the wall and drop- ping onto the sleeping host from the ceiling. Bed Bug History In spite of all of the recorded history of cohab- itation with humans, bed bugs are still “the bug References to the bed bug as the bane of human that nobody knows.” The reason for this “bed bug existence appear in some of the earliest recorded denial” is that there is a social stigma associated history. Aristotle made reference to bed bugs in his with bed bug infestations. Many people believe Historia Animalia (384–322 b.c.), and many other that bed bugs only infest overcrowded or unsani- historical texts document the presence of bed bugs tary housing. Therefore, you can only get bed bugs in Greece in 499 b.c., Italy in 77 a.d., and in China if you visit or live in these poor conditions. This by 600 a.d. Because bed bugs have co-existed with has never been true. Bed bugs do not discriminate humans for centuries, many common names and between human hosts and infest every social class folk remedies have been created regarding them. and nation across the globe. The bed bug’s ability Bed bugs are known by over fifty common names to infest any human environment has been con- in a number of different languages. The English firmed by the resurgence of bed bug infestations language names include wall-louse, red coat, in industrialized nations over the past decade. ­pursuer, crimson rambler, wall flounder, and the During the 1990s, new bug infestations appeared mahogany-flat. In addition to the various com- first in five star hotels and other expensive tourist mon names, there are several folk sayings that are locations within the United States, Australia, related to bed bugs, including “crazy as a bed bug” ­Singapore, and Europe. or “snug as a bug in a rug.” Bed bugs have long been a target of folk rem- edies. Some remedies may have been somewhat Geography of the Bed Bug effective while others, though creative, were prob- ably useless. The plant Actaea cimicifuga or bug- Today, Cimex hemipterus F. (tropical bed bug) and bane has long been regarded as viable bed bug Cimex lectularius L. (common bed bug) are by far 410 B Bed Bugs (Hemiptera: Cimicidae: Cimex spp.) the two most important and widespread cimicid C. lectularius was compromised in the presence of parasites of humans. Both are thought to have C. hemipterus. Specifically, it was found that in originated from the Old World but are now found mixed populations, C. lectularius females laid only all over the globe. Colonies of C. hemipterus sterile eggs when C. hemipterus accounted for have been cultured from such diverse locations as >75% of the individuals. However, the potential ­Vietnam, Taiwan, Panama, Uganda, Venezuela, negative impacts (if any) of C. hemipterus males Cuba, India, and Florida in the United States. on C. lectularius females living in mixed popula- Although C. hemipterus has a worldwide distribu- tions have yet to be fully determined. tion, its range rarely extends beyond the tropics, therefore it has been described as strictly a ­tropico-politan species. Public Health Importance C. lectularius is a truly cosmopolitan bed bug and has expanded its range with humans through- Because bed bugs are blood feeders and have typi- out Europe and into the Americas. Records of cally been associated with poor living conditions, C. lectularius have been collected from all over the they have long been suspected of being potential world with the exception of Antarctica. However, vectors of human disease. In fact, studies prior to Antarctica will no doubt have C. lectularius by the the 1960s identified many diverse disease organ- end of the decade due to the eco-tourist industry isms that were collected from the bed bug gut, that has recently developed on that continent. body and feces. These pathogens included those In many tropical locations, the distribution of responsible for plague, murine typhus, smallpox, C. hemipterus and C. lectularius overlap. Yet, unlike poliomyelitis, yellow fever and at least 20 other C. hemipterus, C. lectularius is able to survive in diseases. However, there has been no conclusive both tropical and temperate climates. Interestingly, evidence that bed bugs transmit any of these C. lectularius does not typically occur where pop- ­diseases to humans. More recently, bed bugs have ulations of C. hemipterus are well established. been evaluated for their ability to become infected Some authors have speculated that the reason with and transmit Human Immunodeficiency for this absence is that C. lectularius is suscepti- Virus (HIV) and Hepatitis B. HIV has been found ble to fungal infection in tropical locations of to survive in bed bugs for several days after ingestion, high humidity while C. hemipterus is not. A more but there has been no epidemiological evidence interesting suggestion is that the distribution of indicating that HIV could be transmitted from an C. lectularius is limited by the fact that interspe- infected bed bug to a host during the feeding pro- cific copulation is common between the two spe- cess. While Hepatitis B cannot be transmitted from cies and yet has a deleterious effect onC. lectularius. bed bugs to humans via the taking of a blood meal, For example, one older study suggested that there is evidence to suggest that the Hepatitis B sperm fluid of C. hemipterus males was toxic to virus may be mechanically transmitted to humans C. lectularius females. Later research indicated that in bed bug feces or when bed bugs are crushed the deleterious effects of interspecific copulation during the feeding process. However, as of this were due to the fact that attempts of C. hemipterus writing there is no medical record of such a trans- males to mate with C. lectularius females resulted mission ever taking place. in female mortality. The reason suggested for Disease transmission is not the only health this mortality was that the paragenital sinus of the issue associated with bed bugs. In many cases, C. lectularius female was not suited to accommo- the number of bed bug bites or reactions to the date the C. hemipterus paramere. The most recent bites has been cause for concern. When a bed study regarding the viability of mixed bed bug bug bites, the mandibles and maxillae form a populations determined that the fecundity of compact bundle (fascicle) that is rapidly injected Bed Bugs (Hemiptera: Cimicidae: Cimex spp.) B 411 into the host’s skin. During the act of piercing, around the bite site and the delayed response the toothed mandibles move in a rapid alternat- may last for longer than a week. Perhaps the worst ing motion slicing their way through the skin scenario for sensitive people who experience the tissues slightly ahead of the maxillae. After the delayed reaction is to inadvertently spend several tissues are breached, the fascicle probes in all nights sleeping in an infested location. Only with directions, backwards and forwards, often cut- the onset of the delayed immune response, do ting across or entering small capillaries and they realize that they have been subjected to larger vessels. The probing can result in numer- ­hundreds of bed bug bites. ous small hemorrhages throughout the tissues. Fortunately, the suffering caused by receiving The bed bug fascicle probes for a vessel of suit- hundreds of bed bug bites typically has no long able size from which to begin feeding. Blood term physiological effects, provided the person is vessels that are too large or too small are ignored. able to leave the infested area or have the bed bugs Once the fascicle finds a suitable vessel, the max- eliminated. Today, the most common medical illae enter the blood vessel and inject the saliva consequences of bed bug bites are secondary bac- (anticoagulant). The pressure in the vessel causes terial infections that can occur from vigorous the host’s blood to rush up the food canal into scratching and excoriation. Yet historical records the bed bug head, allowing for feeding to be indicate that excessive bed bug feeding has been completed in a matter of minutes. However, the known to cause iron deficiencies among infants destructive nature of the probing coupled with in India. the injection of the bed bug saliva can produce a Although bed bug bites do not produce any wide variety of reactions within the host. long-term physiological problems, the psycholog- It has been well documented that many peo- ical aftermath of dealing with a bed bug infesta- ple do not react to bed bug bites; however, some tion may be significant. Many people suffer from people can suffer severe skin reactions that last for stress and anxiety after an encounter with bed several days. There have been many reports of bugs and are fearful that bed bugs may be infest- married couples staying in infested hotel rooms ing their homes or living on their bodies. Most where the wife or husband was made miserable by people who suffer from bed bug anxiety have had hundreds of itching bed bug bites while their an infestation in their home or have been bitten spouse experienced nothing at all. It has also been severely while traveling. Still other sufferers have suspected that hypersensitive individuals living never had an encounter with bed bugs, but have with large populations of bed bugs may actually been told about bed bugs or have had it suggested suffer asthma attacks after being bitten repeatedly that their itching skin may be the result of bed bug by bed bugs. The reactions of people who are sen- bites. Regardless of whether they have encoun- sitive to bed bug bites vary widely in severity and tered real bed bugs or not, people who suffer from may be immediate, delayed or both. bed bug anxiety have great difficulty sleeping for Bed bug saliva contains many proteins that fear that bed bugs are crawling on them. They trigger the body’s immune response. The imme- often get up several times a night to check them- diate immune response usually involves the selves or their children for bed bugs. Some people development of an inflamed reddish weal that have moved several times and discarded most of will start to itch within a couple of hours and their furniture and other belongings. Many have may continue to itch for 1–2 days. People who also paid thousands of dollars for repeated bed experience the delayed response are typically bug exterminations that have not worked to their unaware that they have been bitten for several satisfaction. Another characteristic of these suffer- days. They then begin to experience localized ers is that they often withdraw from family and itching and swelling (sometimes very severe) friends and spend hundreds of hours on the 412 B Bed Bugs (Hemiptera: Cimicidae: Cimex spp.) ­computer researching bed bug cures and partici- Current Pest Status pating in internet-based bed bug support groups. Although not everyone who suffers from In the early 1990s pest management professionals bed bug anxiety has experienced a real infesta- began to receive complaints about new bed bug tion, the potential for bed bug infestation is very infestations within the United States. By 2001, real. Bed bugs have enjoyed a long history of many pest control firms were reporting tenfold infesting human environments and it was only increases in bed bug calls every year. While new within the last century that certain developed infestations were found to be particularly com- nations have enjoyed a brief respite from these mon in hotels, bed bugs were increasingly being noxious pests. reported in homes, apartments, retirement com- munities, health care facilities, college dormito- ries, youth camps and used furniture outlets. The resurgence of the bed bug after its supposed eradi- Control History cation has presented a number of unique chal- lenges to a variety of commercial industries which At the turn of the twentieth century the bed bug in their own way have contributed to the bed bug was a common household pest in the United problem. States and the world. Bed bugs were frequently First, within the pest management industry, encountered in quality hotels and motels, laun- most pest management professionals are too dromats, movie theaters, city buses, and taxis. young to have had any personal experience with Bed bugs were easily transported home via a bed bug control. This lack of experience has traveler’s clothing, vehicle, or luggage. Once resulted in many incomplete and ineffective bed inside the home, bed bugs could find harborage bug treatments since the bed bug resurgence in furniture, cracks and crevices in the floor or began. Second, the medical profession has had walls, behind wallpaper, or under carpeting. The very little experience with bed bugs, so many bite easy transportability of the bed bug coupled with complaints were misdiagnosed, allowing bed bug the war-time movement of people in the United infestations to continue in homes where they States and Europe (1914–1945) led to millions of might have been treated had they been correctly homes and other structures becoming infested. identified. Leaders in the hospitality industry were However, the importance of the bed bug as a also slow to admit that bed bugs were a problem in household pest began to ­diminish in the 1940s hotels. Therefore, the hoteliers did not readily and 1950s with the use of pyrethrum insecticides develop bed bug prevention or treatment plans and DDT. These insecticides were applied liber- because they failed to recognize the potential dam- ally to all walls, floors, mattresses, bed frames, age that bed bugs could cause their industry. For curtains, cupboards, and any other surface that example, when bed bugs were first (re)discovered could be occupied by bed bugs. Complete control in the United States, it was in five-star hotels in was usually obtained within a matter of days, and cosmopolitan locations like Los Angeles and New with the use of DDT, the residual activity was so York City. The hotel industry was immediately long that the sprayed areas remained toxic and faced with million dollar lawsuits initiated by cli- bed bug free for months. Therefore, in the latter ents who had been bitten while staying in their half of the twentieth ­century the bed bug was facilities. These lawsuits received extensive press almost eradicated in the United States and coverage and immediately associated the hotel Europe, with only a few persistent ­populations brand name with bed bug infestations. It was only surviving in locations where ­living conditions after a number of these bed bug cases were reported were exceptionally poor. that the hospitality industry began to address the Bed Bugs (Hemiptera: Cimicidae: Cimex spp.) B 413 expanding bed bug problem. Finally, an unantici- that the increasing population pressure has led to pated source of bed bug proliferation has been the the widespread dissemination of bed bugs rapidly growing organic foods industry in the throughout the world. United States. Organic poultry farms house thou- Historical records indicate that bed bugs sand of chickens that are being raised for either developed resistance to a number of the insecti- meat or eggs. There have been several documented cides used for their control. These chemicals infestations within these organic facilities where included DDT, methoxychlor, dieldrin, aldrin, bed bugs have been found cohabitating with and carbaryl, Malathion and other organophosphates. feeding on the chickens. Because these facilities Many of these older chemistries have been banned are pesticide-free, the bed bugs in these facilities by the US Environmental Protection Agency and number in the millions, causing stress to both the are no longer available for bed bug treatment. chickens and migrant workers. While the trans- However, because bed bugs have not been a prob- port of these bed bugs to other locations has not lem in the USA for over 40 years, few of the exist- been documented, there is the potential for these ing pesticide products are labeled for bed bug bed bugs to be shipped all across the nation via the control and many of these products have the same thousands of delivery trucks that bring eggs and type of active ingredients. The majority of insecti- other poultry products to food distribution ­centers cide products that are labeled for the treatment of every day. bed bugs are either natural pyrethrins, or pyre- While the exact cause of this recent, world- throids. Because these active ingredients have been wide increase in bed bug activity is not known, used for decades all over the world, and because there are several factors that may have contributed they are from the same chemical class, it has been to the resurgence of bed bugs in the USA. It has suspected that the newly emerging bed bug popu- been suggested that international travel from lations might already be resistant to pyrethroids. developing nations has increased the distribution As of 2007, bed bug resistance to a number of of bed bugs throughout the world. However, inter- pyrethroids has been documented. Field popula- national travel has been common for many decades tions of bed bugs have been found to have variable and bed bugs have only recently (1990s) become levels of resistance to permethrin, deltamethrin, recognized as a widespread problem. Another beta-cyfluthrin, and lambda-cyhalothrin. In some possibility for the bed bug increase has been the cases, the resistance of field collected bed bugs reduction in residual insecticide use indoors. exposed to specific active ingredients was found to Because of concerns about human exposure risk, be 1,000 times that of susceptible laboratory strain routine interior applications of spray insecticide bed bugs. Likewise, the time to mortality for bed have been greatly reduced in favor of integrated bugs confined on dried pyrethroid product resi- pest management (IPM), where pesticides are dues was found to be significantly greater than applied only on an “as needed” basis. IPM also that of the laboratory strain bed bugs. For exam- uses insecticide baits as the primary method for ple, the time it took to kill 50% of the laboratory controlling crawling insects. However, pesticide strain bed bugs (LT50) confined on panels treated baits have no effect on blood sucking parasites. with a formulation of deltamethrin (0.06%) was Thus, it is thought that in the absence of the resid- 61 min. However, when testing bed bugs collected ual sprays, bed bug populations have been able to from an infested apartment in Arlington, Virginia, establish unchecked. One final possibility that the LT50 for deltamethrin was 19 days and 2 h. deserves consideration is that bed bug populations Interestingly, in tests evaluating the potential across the world have become resistant to insecti- repellency of pyrethroids to bed bugs, it was docu- cide products used in developing nations and the mented that neither the field nor the laboratory USA. If this is the case, it is reasonable to suggest strain bed bugs found pyrethroids repellent. In 414 B Bed Bugs (Hemiptera: Cimicidae: Cimex spp.) choice tests where bed bugs could aggregate on infested site by a qualified professional. In many either a panel treated with a pyrethroid product or cases, infested rooms will be taken completely a panel treated with water, there was no significant apart and all personal belongings inspected for difference as to where the bed bugs chose to aggre- live bed bugs, bed bug eggs and fecal spots. Per- gate. In fact, many bed bugs remained in contact sonal belongings are then bagged for treatment, with the pyrethroid treated panels until they died, laundering, or disposal. Because clutter provides even though they could leave the panel to aggre- numerous harborages for bed bugs and makes gate somewhere else at any time during the test. insecticide applications very difficult, a “bare In addition to pyrethroid resistance, these walls” approach is generally required to provide resurgent bed bug populations are not readily sus- adequate control. After all clutter and personal ceptible to the non-pyrethroid products labeled for belongings have been removed, the infested room their control. For example, pyrethroid dusts usually and furniture can then be treated. take several days to kill resistant bed bugs. Desic- A back-pack vacuum cleaner with HEPA cant dusts like silica aerogel, diatomaceous earth or ­filter is recommended for the removal of live bed limestone and corn bran dusts can also take days or bugs and their cast skins. The removal of live bed even weeks to kill bed bugs confined on the bugs and their debris will not only reduce the ­material. Because bed bugs do not groom, stomach bed bug numbers but will aid the pest manage- toxicants like boric acid have no effect on bed bugs. ment professional in identifying incipient infes- Even crack and crevice sprays containing pro-­ tations in future inspections. Once vacuuming is insecticides like chlorfenapyr may take longer than completed, the vacuum cleaner bag must be a week to kill bed bugs, thus allowing them to sealed in a plastic bag and removed from the reproduce prior to suffering any toxic effects. The structure immediately. It should be noted that insect growth regulator hydroprene, which has although the ­vacuum cleaner will be able to been a widely used juvenile hormone analogue for remove the majority of live bed bugs it will not cockroach control, has been found to function as a be able to remove the bed bugs eggs which are chitin synthesis inhibitor in bed bugs, disrupting typically cemented to the surfaces on which they the final molt. Yet, although hydroprene kills close are laid. Therefore, additional treatment(s) will to 50% of exposed bed bugs during the final molt, be necessary. the surviving adults are not sterilized and produce A frequently used method of reducing bed a greater number of viable offspring than unex- bug harborage sites is the use of sealants and caulk. posed bed bugs after taking their first adult blood Because early instar bed bugs are capable of occu- meal. Finally, “non-toxic” mattress treatments pying extremely small cracks it is important to ­containing isopropyl alcohol, sodium laurel sulfate inspect the walls and ceilings very carefully for or protein degrading enzymes typically kill over bed bug harborages around switch plates, wallpa- 80% of bed bugs that are directly sprayed with per seams, electrical outlets, inside nail holes and these products. However, these treatments have no screw heads, around window frames, and in sta- residual ­activity once the product is dry, and like ples holes. Caulking and sealing these harborages most insecticides, these non-toxic mattress treat- will force bed bugs to wander in search of new ments have no effect on bed bug eggs. harborage space, causing them physical stress and increasing their chances of exposure to insecticide residues. Current Management Practices Steam cleaning is rapidly becoming a widely used method of bed bug control. Professional Because of their cryptic lifestyle, bed bug manage- steam cleaners can be used to kill bed bugs hiding ment begins with a thorough inspection of the in baseboards, under carpeting, in mattress seams Bed Bugs (Hemiptera: Cimicidae: Cimex spp.) B 415 and in the wooden components of box springs. Because bed bugs are susceptible to high Professional cleaners that produce dry steam at temperatures, heat fumigation is being used to temperatures >60°C (140°F) are preferred because eradicate bed bugs from large commercial they produce enough heat to compensate for the ­facilities. Using the heat fumigation technology insulating properties of mattresses and other developed for the treatment of grain silos, fans upholstered furniture which might otherwise are used to blow air in from the outside to raise ­prevent bed bugs from reaching their thermal the atmospheric pressure inside the facility. The death point. When purchasing a steamer for bed air is then heated and monitored to make sure that bug control, it is important to select a machine all locations inside the building reach the appro- with a steam head large enough to disperse the priate temperature (bed bug thermal death steam at a low velocity. The small steam head of point) and pressure. The heat treatment is then some machines will disperse the steam with such maintained for a period of hours to ensure that force that the bed bugs and eggs are blown off the all bed bugs and bed bug eggs are killed. Although treatment areas into other parts of the room. heat fumigation is an effective bed bug treat- Although steaming bed bugs is a slow and ­laborious ment, the cost, like that of chemical fumigation, task, steam cleaning is one of the most effective is often prohibitively expensive for the average methods for killing both bed bugs and their eggs. consumer. After steaming, the treated mattress and box Exposing bed bugs to cold temperatures will springs should both be placed inside a bite proof, kill bed bugs but the duration of exposure is often escape proof mattress cover. A variety of products too long to be practical. For example, the thermal are available for covering mattresses, however, death point for adult bed bugs exposed to cold most were not designed to function as a bed bug temperatures for 1 h is −18°C (−1°F). Yet, most prevention tool. Many tear easily or have zipper conventional freezers have a minimum tempera- casings that are large enough for bed bugs to crawl ture of 0°C (32°F), thus requiring that the bed bugs through. However, there are mattress covers that be frozen long enough to achieve 100% kill. have been tested to ensure that bed bugs cannot Attempting to kill bed bugs at 0°C will take several get inside the cover and any bed bugs already days at least, and if the bed bugs are insulated in trapped inside the cover cannot escape or bite clothes or bedding it may take several weeks of through the fabric. Although mattress covers exposure to ensure that all bed bugs are killed and ­cannot prevent a future bed bug infestation, they bed bug eggs are no longer viable. do keep the client from having to throw the mat- Although increased sanitation and exclusion tress away. techniques are necessary to remove bed bug har- All bedding and any clothing articles that are borages, these techniques alone will not control an suspected of being infested with bed bugs must be established infestation. Therefore, chemical meth- laundered. Both clothing and bedding should be ods must also be employed as part of a compre- bagged and marked so that they are not mixed with hensive bed bug management program. As stated uninfested articles during the cleaning process. All earlier, most modern pesticides will not control items should be laundered at a temperature >49°C bed bug infestations when used individually. How- (120°F) for more than 10 min with laundry deter- ever, combinations of products with different for- gent. Bed bugs, like all insects, are very susceptible mulations and modes of action have been evaluated to drowning when exposed to soap, so the addition in the field and have been found to produce satis- of laundry detergent will ensure a quick kill. Plac- factory control. These products must be applied ing bed clothes in a dryer at 60°C (140°F) for 20 according to the product label and the treatment min or longer is also recommended to make sure area must be regularly monitored to make sure that no bed bug eggs survive. that the products are working. Field evaluations 416 B Bed Bugs (Hemiptera: Cimicidae: Cimex spp.) have determined that microencapsulated products complete vacuuming of all carpeting and furni- containing pyrethroids are an effective residual ture, steam cleaning of upholstered furniture spray because the micro capsules stick to the bed and mattresses to kill bed bugs and their eggs, bug body allowing for enough exposure time to and treatment of the mattresses and box springs kill resistant bed bugs. These products can be used with a non-toxic ­mattress treatment (preferred) for application into cracks and crevices where bed or a labeled residual insecticide. After treating bugs hide and also along baseboards or ceiling/ the mattress, both the mattress and box springs wall junctions where bed bugs will often harbor should be encased in bite proof, escape proof when the infestation levels are high. In addition to mattress covers. The infested room should be the crack and crevice applications, products treated with a combination of residual insecti- labeled for upholstery treatment can be applied to cide spray and an insect growth regulator. These infested furniture as well as to the mattress and products should be applied according to the box springs. Some mattress products have residual label to cracks and crevices, baseboards, and any activity (pyrethroids) while other “non-toxic” other bed bug harborage locations. The infested products do not. The non-toxic products that room and all adjoining rooms should then be ­contain isopropyl alcohol or sodium laurel sulfate inspected (and/or treated) weekly to determine as the primary killing agent will kill bed bugs on the efficacy of the treatment products and to contact. Yet, these products evaporate almost make sure that the bed bug population is being immediately after application and bed bugs that eliminated. survive the treatment will continue to bite and reproduce. Residual dusts are particularly useful in the frame of the box springs and wood compo- Summary nents of the other furniture because they stay within the application site and have a very long Most entomologists and pest management pro- residual. Residual dusts containing pyrethroids fessionals believe that the resurgence of human also adhere to the bed bug’s body allowing for the bed bugs (both Cimex lectularius and Cimex long exposure period (possibly days) necessary to hemipterus) presents the single greatest indoor kill resistant bed bugs. “Non-toxic” desiccant pest management challenge in decades. Since the dusts will also kill bed bugs but they too may take bed bugs’ widespread reappearance in the 1990s, ­several days to work. Baseboard, and crack and the common bed bug has become a full blown crevice treatments with insect growth regulators ­epidemic with new infestations reported in most are useful in that they will kill many immature European countries and in all 50 states in the bed bugs during the final molt. However, there is United States. Likewise, the tropical bed bug has no evidence that insect growth regulators will spread throughout the tropics in the last 10 years kill or sterilize adult bed bugs. Although aerosols increasing its range to infest Australia and rees- and foggers are frequently used for bed bug tablishing populations in Singapore and other ­elimination, they are not effective control prod- tropical nations where they had been previously ucts because they do not penetrate into bed bug eradicated. Because these insects have never harborages. completely disappeared from developing nations Overall, a complete bed bug treatment they have been continuously treated with many should include the removal of infested items insecticide products over the last 50 years. This for either treatment or disposal, the laundering continuous pesticide pressure has selected for of infested clothes and bedding, the elimination bed bug resistance, particularly to pyrethroids. of clutter, the sealing of all small cracks and These pyrethroid resistant populations present a holes that might provide bed bug harborage, a unique problem in developed nations where Bee Louse, Bee Fly, or Braulid, Braula coeca Nitzsch (Diptera: Braulidae) B 417 public opinion and federal legislation has elimi- Newberry K (1989) The effects on domestic infestations of nated entire classes of insecticides from indoor Cimex lectularius bed bugs of interspecific mating with Cimex hemipterus. Med Vet Entomol 3:407–414 use due to their perceived toxicity. Pyrethroids Potter M (2006) The perfect storm: an extension view on bed have been one of the few chemical classes bugs. Am Entomol 2:102–104 that remain available for indoor use due to Usinger S (1966) Monograph of Cimicidae. Thomas Say their low mammalian toxicity. As a result, pyre- Foundation Vol. VII. Entomological Society of America, Lanham, MD, 585 pp throids are the most frequently used class of Vall Meyers M, Hall A, Inskip H, Lindsay S, Chotard J chemistry for bed bug control in the United (1994) Do bed bugs transmit hepatitis B? Lancet States today. However, with increasing bed bug 343:761–763 Webb P, Happ C, Maupin G, Johnson B, Ou C (1989) Potential resistance these products will gradually become for insect transmission of HIV: experimental exposure less effective at controlling new infestations. of Cimex hemipterus and Toxorhynchites amboinensis Because of the prevalence of bed bug resistance to Human Immunodeficiency Virus. J Infect Dis many researchers believe that the bed bug 160:970–977 ­epidemic will become much more severe in the future. The key to bed bug control in developed Bee Bread nations will ultimately be education. People will have to accept that bed bugs exist and learn how A pollen and honey mixture fed to bee larvae by to avoid transporting bed bugs to their homes worker bees (from hotels, taxis, air planes, camp cabins, movie ­theaters, laundromats, day care centers, multiple unit housing, etc.) during the course of Bee Flies their daily activities. The ability of the average citizen to identify bed bugs and bed bug evi- Members of the family Bombyliidae (order dence will be critical for them to successfully Diptera). protect ­themselves and their home from bed  Flies bug infestations.

Bee Lice References Members of the family Braulidae (order Diptera). Cooper R, Harlan H (2004) Bed bugs and kissing bugs. In:  Flies Hedges S (ed) Mallis handbook of pest control, 9th edn.  Bee louse GIE Publications, Cleveland, OH, pp 494–529 Doggett S, Geary M, Russell R (2004) The resurgence of bed bugs in Australia: with notes on their ecology and con- trol. Environ Health 4:30–38 Bee Louse, Bee Fly, or Braulid, Harlan H (2006) Bed bugs – importance, biology, and control Braula coeca Nitzsch (Diptera: strategies. Armed Forces Management Board Technical Braulidae) Guide No. 44. http//:www.afpmb.org/pubs/tims/TG44/ TG44.htm Johnson CG (1942) The ecology of the bed-bug, Cimex jamie ellis lectularius L in Britain. J Hyg 41:345–361 University of Florida, Gainesville, FL, USA Moore DJ (2006) Evaluation of multiple insecticidal products for control of the common bed bug (Cimex lectularius, (L.)). Unpublished M.S. thesis, Virginia Tech University, The bee louse, Braula coeca Nitzsch (Diptera: Blacksburg, VA, 118 pp Braulidae), is a wingless fly that lives as a 418 B Bee Louse, Bee Fly, or Braulid, Braula coeca Nitzsch (Diptera: Braulidae) ­commensalist in western honey bee (Apis mellif- era L.) ­colonies. Not much is known about the bee louse as its biology has been studied only ­irregularly since the 1920s. The fly is presumed to be harmless to its host, although this point is debatable. It is found in many countries, and because no true ­economic damage can be attributed to the fly, it probably poses a mini- mal threat to bees.

Bee Louse Life Cycle and Behavior Bee Louse, Bee Fly, or Braulid, Braula coeca Nitzsch (Diptera: Braulidae), Figure 24 An adult Adult bee lice (Fig. 24) are small (<1.5 mm long) Braula coeca (photo by James Ellis, University and are covered in spine-like hairs. They are round of Florida), and its worldwide distribution (from in shape and unlike most flies, have neither wings Ellis, Munn (2005) The worldwide health status of nor halteres. They are reddish-brown in color, honey bees. Bee World 86(4):88–101). which often leads to their misdiagnosis as varroa mites, Varroa destructor. Structurally, physically, and their location on the adult bee all are similar While on the head of its host, the fly will or the same for varroa. One noticeable difference steal food from the mouth of its host as the host between the bee louse and varroa is the presence is fed, or is feeding another bee. There is some of six legs on the bee louse while varroa has eight. evidence that bee louse adults can induce regur- Further, the adult bee louse has a raised appear- gitation from the bees. They accomplish this by ance while varroa are flatter and more oval than scratching the upper edge of the bee’s labrum the bee louse. Despite this, both are very small and until the bee extends its tongue, at which time difficult for most people to distinguish with the they will feed on food or other secretions that naked eye. the bee offers. The eyes of adult bee lice are located just Bee louse eggs are white, oval shaped, and above the antennae. They occur as pale spots on have two lateral flanges. The flanges are flat and the surface of the cuticle and are surrounded by extend parallel to each other toward the long axis pigmented chitinous rings. The terminal joint of a of the egg. The eggs range from 0.78–0.81 mm bee louse’s 5-segmented tarsi is divided and modi- long and 0.28–0.33 mm wide without the flanges. fied with comb-like teeth, an adaptation that allows Including flanges, the eggs average 0.84 × 0.42 mm the fly to cling to bees. The thorax is very short. (l x w). Female bee lice can oviposit a number of When viewed dorsally, it is less than half as long as places in the bee nest (empty cells, brood ­cappings, the head, resembling an abdominal segment. The debris on the floor) but only eggs oviposited on scutellum is absent. honey cappings hatch. The incubation period of Presumably, bee louse adults feed on nectar the egg can range from 2–7.4 days, depending on and pollen, as well as food and other excretions the season. passed between adult bees trophallactically. After the incubation period, larvae emerge Regarding the latter, bee louse adults often are from the eggs oviposited on the waxy cappings of found on the heads of workers, drones, and espe- honey comb. Upon emergence, the larvae con- cially queens. More than 180 bee louse adults have struct a tunnel under the cell cappings. This is the been found on a single queen. most noticeable damage attributed to the bee Bees (Hymenoptera: Apoidea: Apiformes) B 419 louse. Larvae tunneling under the cell cappings Bee Mites can visually taint the waxy cappings. Although some consider this damage, it is of minor eco- Some species of mites (Acarina) can be serious nomic importance. Regardless, the intersecting pests of honey bees. tunnels are a common sign of bee louse presence.  Varroa Mites, Tracheal Mite, Mites Many beekeepers have seen this damage but few recognize it for what it is. It is believed that bee lice larvae feed on honey and pollen residues encountered while tunneling under the cell cap- Bees (Hymenoptera: Apoidea: pings. There is a modicum of control suggestions Apiformes) for the bee louse, largely because it is not consid- ered a major pest. However, many of the synthetic james h. cane pesticides used against varroa also demonstrate USDA-ARS Bee Biology and Systematics activity against the bee louse. Laboratory, Utah State University, Logan, Larvae of the bee louse have three larval UT, USA instars, ranging from 7.1–10.8 days. Following this time, the larvae become prepupae, a stage that can Bees essentially are wasps that turned to pollen for last from 1–2.7 days. During this time, the ­prepupa dietary protein. A combination of distinctive fea- has a creamy-white appearance. The developing tures, taken together, make bees unique among pupa is enclosed in the larval skin. The white/yel- insects. (i) Sociality, characterized by overlapping lowish pupae are 1.4–1.7 mm long × 0.5–0.75 mm generations, cooperative brood care and a repro- wide. The life cycle begins again as the adult fly ductive division of labor between fertile queens emerges. and sterile female workers, has evolved multiple times within the bee lineage. Presumptive interme- diate stages of sociality are represented by at least several living species, and thus are available for Reference observation, evolutionary study, and experimental manipulation. (ii) Bees, unlike most other herbivo- Morse RA, Flottum K (eds) (1998) Honey bee pests, preda- rous insects, dine solely on pollen and nectar or tors, and diseases, 3rd edn. A.I. Root Company, Medina, floral oils. This dietary transition from their - car OH, 718 pp nivorous ancestors was accompanied by the evolu- tion of branched body hairs which aid bees in picking up pollen, plus modification of the hind legs or ventral abdominal surface for carrying large Bee Milk loads of pollen. These features typically distinguish bees from wasps. (iii) Unlike most insects, each Also called royal jelly, this is a substance that is adult female of every non-parasitic­ bee species, secreted by Apis nurse bees from a gland on whether social or not, rears her young in a nest. their head (the hypopharangeal gland), mixed Thus, all food and shelter needs of bee larvae are with crop contents, and fed to bee larvae. All provided by their mother, or one or more sisters if bees are fed bee milk for the first 3 days, but lar- the species is social, or the host female if the species vae destined to become queens are fed this is parasitic. (iv) From the central nest, females daily material throughout their larval development venture forth repeatedly on spatially extensive whereas future workers are switched to nectar foraging trips to acquire floral resources for their and pollen. brood. These trips require remarkable navigational 420 B Bees (Hymenoptera: Apoidea: Apiformes) skills equaled by few other insect taxa. (v) As a con- ­Circle. Only social bees achieve maximum diver- sequence of their extensive foraging at flowers, bees sity in lowland tropical rainforests. Non-social (or have become the primary biotic agents of pollina- solitary) species are most diverse in drier, more tion for continental floras worldwide. No other seasonal biomes of the world’ s temperate zones. animal group so dominates this, or the other great These include the Mediterranean Basin and areas plant-animal mutualism, seed dispersal. of similar climate around the world (e.g., western South Africa, southern ­California, central Chile and Argentina, much of Australia) and the more vegetated, warm deserts (e.g., Sonoran, ­Chihuahuan Evolutionary History and Colorado deserts of the southwestern U.S. and adjacent Mexico). Warmer grasslands also can be Bees (Hymenoptera: Apoidea: Apiformes) likely productive, such as the Great Plains of the U.S. In arose in the Cretaceous, perhaps 120 million these regions, several hundred bee species can be years ago, when they diverged from the carnivo- easily expected in any given locality. rous habits of their closest relatives, the sand wasps (Hymenoptera: Apoidea: Spheciformes). Flowering plants (angiosperms) had made their debut by this time. Most paleontological material Development and Life Cycle consists of bees entombed in amber (polymer- ized tree resins) millennia later. Specimens from Like other insects with complete metamorphosis, the Eocene (40 million years ago) are common. bees pass through four discrete life stages (Fig. 25). They are typically workers of the stingless bees Bee eggs are sausage-shaped. Those of the solitary, (Meliponini) that probably became mired while non-parasitic species can be proportionally huge gathering resin to seal their nest cavities. These for an insect; eggs of some large carpenter bees represent highly evolved social genera that (Xylocopa) are 16 mm long. Non-social bee spe- remain extant today, suggesting a much earlier cies are much less fecund than most insects, lay- origin for bees. Tantalizing casts of much earlier ing only 10–25 eggs in their lifetimes, averaging fossil nest cells are also reported, but their identity one to two per day. As with other Hymenoptera, remains controversial. progeny sex is determined by egg fertilization: male eggs remain unfertilized and are thus, hap- loid. Bee ­larvae are gently curved, soft, white, blind, largely immobile and defenseless grubs. Diversity and Distribution Only specialized instars of some cleptoparasitic species are mobile and armed with powerful There are more species of bees today than the sum ­mandibles, adaptations that they use to assassi- total of mammals, reptiles, amphibians and birds; nate host larvae before consuming the host’ s 17,000 species of bees have been described, per- ­provision masses. haps another 10,000 await discovery. They are dis- Larvae of nearly all solitary species and most tributed among only seven families. The largest eusocial species receive an individual cache, or genus (Andrena) has 1,400 described species; mass provision, of pollen moistened with nectar, many have more than 100. Bees are native to all or occasionally, floral oils. Provision shape and continents but Antarctica. Few species are found consistency varies from firm, spherical pellets to a on isolated oceanic islands, but ranges of some soupy gruel on which the larva actually floats. hardy species extend well north of the ­Arctic ­Larvae pass through four molts (so five instars) to Bees (Hymenoptera: Apoidea: Apiformes) B 421

Bees (Hymenoptera: Apoidea: Apiformes), Figure 25 Bee life cycle, illustrated using the alkali bee, Nomia melanderi (Halictidae): (top left) egg atop a completed provision mass. Note the polished waterproof cell lining applied to the soil matrix; (top right) third instar larva feeding on remaining provision; (lower left) prepupa, the post-feeding larval resting stage; (lower right) two pupae (removed from their nest cells) (photos by William Nye). 422 B Bees (Hymenoptera: Apoidea: Apiformes) accommodate their rapid growth, consuming Other bee species nest above ground, excavating their provision mass in a few weeks. Larvae do not pithy stems of plants or adopting abandoned defecate until they are mature. Once the provision ­tunnels chewed by ­wood-boring larvae of beetles mass is consumed, larvae of many (but not all) and some other insects. Some carpenter bees species then spin a cocoon. The final larval stage is (Xylocopa) can chew tunnels directly into sound the prepupa, which is more robust and resistant to wood. The highly social honey bees and stingless desiccation than the earlier instars, but still grub- bees often build their nests in hollow tree cavities. like. This is the typical resting, or diapause, stage Free-standing nests are made by a few paleotropi- for those temperate-zone species whose single cal honey bees (pendant wax combs) and a few adult generation flies later in spring or summer. other bees (mostly orchid bees and some Unlike most other insects, bees do not weather ­megachilids that use clay or resin). inhospitable seasons as pupae. Rather, bee pupae are quite delicate, resembling waxen versions of the adult. If a bee species is one that flies in the Mating Biology early spring (allowing little warmth for further development), then the pupal stage lasts only a few Male bees do not contribute to nesting (excava- weeks, yielding an adult that will remain in the tion, foraging, defense) (Fig. 26). With few excep- cocoon (or nest cell) to overwinter. Some tions, males are not welcome in the nest. They ­halictids (sweat bees), as well as bumble bees, spend their days patrolling for receptive conspe- emerge as adults, mate, and then disperse before cific females, and their nights sleeping on flowers overwintering. or vegetation, or in shallow burrows underground. Males of various species enhance their encounter rates with females using one or more search and/ Nesting or advertisement strategies employing scent and vision. Among non-social species, males are often All larval bees live in a nest selected, constructed, protandrous, emerging some days before females maintained, defended and provisioned by their of the year. Males of floral specialists may patrol mother, sisters (social species) or host (parasitic preferred floral hosts, especially if females of their bee). A genus of bee often can be recognized by its species mate repeatedly during their lifetimes. nesting substrate and nest architecture. Most bee Males also may patrol nesting sites; among species species nest underground, typically exca­vating a whose females mate but once and whose nests are central, cylindrical tunnel that is either partitioned ­aggregated, males may compete intensively to find into nest cells, or from which lateral tunnels branch freshly emerged virgin females, guided by the that terminate in nest cells. Soil cliffs as well as ­virgin female’s scent. Conversely, males may apply more horizontal surfaces are used. Excavated soil scent-marks to attract females to a sort of trapline on horizontal surfaces is often heaped in a small that males patrol. These can sometimes extend for cone or delta of irregularly sized pellets, the hundreds of meters. Honey bees, some bumble “tumulus.” Nest depths differ among species, rang- bees and large carpenter bees maintain aerial ter- ing from a few centimeters to several meters if in ritories. Some orchid bees reportedly form “leks” sandier soils. Cells are often egg- or barrel-shaped, perfumed with scents synthesized from floral oils just large enough for a mother bee to fit with her of orchids. A few recent cases report flightless assembled provision mass. Cell walls are com- males that linger in their natal nests to mate with monly smoothed, even polished, usually with the their sisters. In general, courting and mating are addition of a secreted waxy or membranous brief affairs for bees. Most species are monandrous, waterproof lining, or alternatively, plant resin. each female mating but once in her lifetime. All Bees (Hymenoptera: Apoidea: Apiformes) B 423 Sociality

Bees have lineages representing all degrees and hypothesized evolutionary steps of sociality, includ- ing reversion to solitary habits. Populations of a few species range from solitary to social depending on ecological circumstance. Less social arrange- ments include: communal species, wherein repro- ductive females sometimes share in a single nest’s construction and defense but otherwise act soli- tarily; semisocial colonies founded by a group of (likely) sisters; subsocial species in which mothers actively care for growing daughters, that in turn may linger as adults to aid their mother; and ­several other much rarer arrangements. Many non-social species, especially ground-nesters, will nest ­gregariously (Fig. 27) in populous ­aggregations of hundreds to many thousands of individuals. During adult activity, these bee “cities” can be ­dramatic, with a dense traffic of­foragers and patrol- ling males producing a loud, daylong hum. The hallmarks of higher sociality (“eusocial- ity”) are an overlap of generations (mothers and daughters), cooperative brood care by workers, and reproductive division of labor (queens and workers). Workers are rarely, if ever, mated, and so, if they lay eggs, these are male. For primitively eusocial species (some sweat bees and carpenter bees, nearly all bumble bees), nests are founded in the spring by a single, mated female (gyne), as with solitary species. In rare cases, there are several foundresses. This mother bee builds a nest and prepares cells. Each cell receives a ball (Figs. 28 and 29) Bees (Hymenoptera: Apoidea: Apiformes), Figure 26 of pollen moistened with nectar and a single egg. Mating adults (above), male atop female (photo by The cell is then sealed. Emerging daughters remain William Nye); aggregation of males (center) sleeping with the nest rather than dispersing, helping their together atop plant stem (photo by William Nye); mother construct, provision and defend her nest. female at nest entrance (below). (photo by The original foundress, mother to the nest, then James Cane). becomes the colony’s primary egg-layer (queen). The more eusocial species have morphologically female bees are able to store live sperm to varying distinct queens and workers. Primitively eusocial degrees; at the extreme, queens of social species colonies grow to, at most, a few hundred workers. store live male sperm for months or even years. Late in the summer or early autumn, reproduc- Hence, sperm often outlive the male bees that tives are produced, and mate; only the future ­produce them. queens pass the winter in diapause. 424 B Bees (Hymenoptera: Apoidea: Apiformes)

CORE TUMULUS

SCARAB BURROW

4.0 cm

FILL

5 4 3

FECES

6 8 POLLEN

7 FOOD LOAF

Bees (Hymenoptera: Apoidea: Apiformes), Figure 27 Gregarious nesting (above left) showing dark soil tumuli atop a square meter of soil ­surface (photo by James Cane); core (1 cu. ft.) of nesting soil (above right) from alkali bee nesting ­aggregation, showing numerous white prepupae in their individual nest cells (photo by William Nye); ­schematic (below) of an excavated subterranean nest of the neotropical bee Tapinotaspis tucumana (Apidae). Nests and enlarged views of three nest cells (Reproduced with permis- sion from the American Museum of Natural History. Artwork by Jerome Rozen, Jr.). Bees (Hymenoptera: Apoidea: Apiformes) B 425

Bees (Hymenoptera: Apoidea: Apiformes), Figure 28 Laboratory nest of the bumble bee Bombus morrisoni (Apidae) (above left) showing nest cells and honey pots clustered amid insulative cotton batting; Nest of a Brazilian Melipona sp. (Apidae)(above right). The thin pliable sheets of the involucrum (i) have been peeled back to reveal the topmost tier of horizontal combs (c). Between the involucrum and the wall of the ­cavity are the large pollen pots and honey pots (h). Honey is visible in those pots that remain open (Photo by James Cane); adult ­female of the cleptoparasitic bee, Triepeolus dacotensis (Nomadinae) (lower left). Note paucity of hairs, lack of pollen-transporting structures, and the exserted­ sting; first instar “assassin” larva of Triepeolus ­dacotensis (Nomadinae) (lower right). Note its long recurved mandibles, which are used to grip and kill the host egg or young larva. Subsequent instars resemble normal bee larvae (photos by William Nye).

Only the stingless bees (Meliponini) and ­individuals of cleptoparasitic species, it is only for honey bees (Apis) are highly eusocial. Most reside self-maintenance and sometimes mates. All other in the humid tropics. Their colonies are tightly females seek, gather and transport nutritious integrated and perennial, populated by thousands ­substances (typically pollen and nectar) and of workers headed by long-lived queens that are ­sometimes, nesting materials for their progeny. dependent on worker care. Their colonies repro- Species of honey bee size will regularly fly a kilo- duce by “fissioning,” when swarms of workers meter or more to desirable bloom. Using the sun accompany a queen to found a new colony. and local landmarks for navigation, they can then fly directly home at 15–25 kilometers per hour to find a nest entrance that is often no bigger than Foraging the bee, and, in the case of gregarious species, that is imbedded in an aggregation of hundreds or Except for queens and drones of highly eusocial thousands of like-looking entrances of their species, all bees visit flowers. For males and conspecifics. 426 B Bees (Hymenoptera: Apoidea: Apiformes) toxic. A retractable, complex proboscis allows bees to sip or lap nectar. A bee’s access to nectar is ­constrained by body size, tongue length, and the flower’s dimensions. Some carpenter bees, sting- less bees and bumble bees regularly rob deep, tubular flowers of their nectar by perforating the corolla near its basal nectaries. Perhaps because bees can readily assess nectar volume, sugar ­constitution and its concentration, individuals and species can and will compare nectar yields of ­various flowering species, optimally choosing the most rewarding species at any given time. Some flowers, mostly tropical, secrete calorically rich oils rather than nectar. These are mopped or wiped up by bee ­species that have pads and “squeegees” of hairs specialized for the task, to be incorporated into larval provisions and sometimes, nest cell lin- ings. Some ground-nesting species and many eusocial species synthesize and secrete their own calorically rich substances that they blend into progeny provisions. Bees also seek pollen at flowers, which is their key dietary source of proteins, fats, minerals and sometimes starches, for themselves and their off- spring. Pollen, of course, also contains the male gametes of flowering plants, so it really serves two reproductive purposes, plant ovule fertilization and bee reproduction. No effective dietary substi- tute for pollen has yet been devised for bees. Few animals match the nitrogen assimilation efficiency of bees, despite the indigestibility of the external shell, “exine,” of pollen grains. Pollen, in most cases, dusts the foraging bee as Bees (Hymenoptera: Apoidea: Apiformes), Figure a powder that lodges in the vesture of branched 29 Cast of nest cell of Anthophora (Apidae) (above); hairs that envelop its body. Harvest may be provisioned nest cell of ground-nesting Colletes enhanced by buzzing, biting, scraping and scrab- (Colletidae), showing the thin, translucent membrane bling. Many specialized structures, hairs and made of secreted polyesters (center); larvae of parasitic behaviors of foraging females then work in con- Melittobia wasps (Hymenoptera: Eulophidae) in nest cert to efficiently groom and accumulate pollen cell of an Osmia bee (below) (photos by William Nye). from the body for transport. Pollen is transported in a brush of hairs called a “scopa,” often on the Bees always take nectar at flowers. Nectar hind legs (or under the abdomen of megachilids). powers bees’ flight and contributes carbohydrates A few taxa carry pollen internally in their crop and water to larval diets. Typical nectar sugars are (e.g., Hylaeus). Bumble bees, honey bees, orchid glucose, fructose and sucrose. Few nectars are bees and stingless bees carry pollen in a pollen Bees (Hymenoptera: Apoidea: Apiformes) B 427 basket, or “corbicula,” on the hind leg, a smooth, Pollination slightly concave surface surrounded by guard hairs that holds a damp pollen pellet. Bees are the most important and cosmopolitan Anthers of some flowers (e.g., tomato and biotic pollination agents in most continental ­blueberry) shed their pollen through apical pores ­habitats, and for most prevalent plant families, such or slits like a salt shaker. These require vibration to as the Asteraceae, Fabaceae, Lamiaceae, Orchidaceae, ­dispense their content of pollen. Some bees shake Rosaceae and Solanaceae. Few nocturnal flowers this pollen free by battering or stroking the anthers are pollinated by bees. Reciprocal co-evolution with their legs, while others bite the anthers to between bees and their flowers seems, at best, squeeze out pollen. Species of many genera can ­diffuse in nearly all cases, although adaptations shiver their flight muscles while on the flower, that enhance attraction, resource extraction and ­sonicating these anthers to eject their content of pollination are evident everywhere. Most collected ­pollen. This buzzing is audible. The effect can be pollen ends up in a larval provision, not on a flow- duplicated with a vibrating tuning fork. Bumble er’s stigma, but bees are still vastly more efficient bees frequently use this method of pollen extrac- than wind in moving pollen to receptive flowers. tion, even for flowers with anthers of normal Bees are essential ­pollinators of some vegetable morphology. crops (or their seeds), many prominent fruit and Many bee species are floral generalists seed-oil crops, forage legumes and a few nut or (“polylectic”), taking pollen from many taxa of fiber crops. Crops that contribute the starches and flowers, a necessity for the long-lived colonies of refined sugars to the human diet are typically wind- social bees. Foraging individuals often will display pollinated or vegetatively propagated. Home and floral constancy, selectively visiting sequences of market gardeners benefit from pollination services conspecific flowers on a given foraging trip, despite of wild bees. In large mechanized agriculture, how- the availability of alternatives. Such preferences ever, only hived honey bees can generally supply are labile, perhaps reflecting learning or memory the millions of inexpensive foragers needed for constraints. In contrast, a third or more of the non- ­pollination. In the past half-century, though, a social species in a community may be “oligolectic.” growing minority of tree fruit, forage seed and This is a fixed species-specific predilection to greenhouse crops are benefiting from pollination ­collect pollen from the same small subset of avail- services of managed solitary bees and bumble bees able flowering species, commonly one or several (rather than honey bees), a trend that seems likely related genera within a plant family. Such unwav- to continue, given their often superior ­pollination ering fidelity is particularly common among desert efficiencies and the devastating effects of new pest bee faunas and vernal bees of the temperate zone. problems suffered by honey bees. The reason(s) for oligolecty are not fully under- stood. In some cases, oligoleges seem to accumulate at reliable pollen hosts that produce generous quan- Diseases, Parasites and Predators tities of pollen (e.g., willow, sunflowers, creosote bush, and blueberries). For other species, the associ- Among insects, the superior life expectancies of ation seems to reflect phenological specializations bees result largely from superior maternal care of (e.g., crepuscular flowers, early spring blooms) or offspring. Females actively deter predators and more or less private floral resources eschewed by parasites by biting, stinging and by use of chemical other species (e.g., oil flowers of Lysimachia and repellents. Nest cells are waterproofed and possibly their associated Macropis bees). Unlike insect fumigated with applied glandular secretions or ­herbivory, host chemical defenses rarely, if ever, plant resins. Despite such extensive maternal care ­dictate floral specialization by bees. and defenses, bees are nonetheless plagued by 428 B Bees (Hymenoptera: Apoidea: Apiformes) ­diseases, parasites and predators. Feeding larvae, in ­constructs that are extensive, monotonous and particular, succumb to various viral, bacterial inhospitable (e.g., lawns, parking lots, wheat fields) and fungal diseases. Microorganisms commonly fail to fulfill bees ­nesting and/or foraging needs, spoil provision masses, too. Nematodes and mites although bees can readily fly through a finer patch- (mostly external) are ubiquitous bee parasites. work mosaic of these features if interspersed with Many larval insects devour the contents of bee favorable ­nesting and foraging habitats. Unlike nests, including clerid and meloid beetles. Others accidental or misguided introductions of plants, are internal or external parasitoids, including vertebrates and shellfish, exotic bees have­generally ­chalcidoid wasps, bombyliid flies and strepsipter- been of little ecological consequence, although ans. The elaborate structural defenses of stingless ­ill-guided international trade (or smuggling) of bee nests attest to the intense predation pressures honey bees and bumble bees has been disastrous of ants and social parasites of the tropics. Adult in some recent cases. The greatest risk attending bees are subject to the myriad predators of other ­intercontinental transport of live bees is likely to mobile insects. be the inadvertent transport of diseases and pests, Cleptoparasitic, or cuckoo bees, are analogous such as those that are currently devastating to cowbirds and European cuckoos, surreptitiously ­apiculture, especially Varroa and tracheal mites. inserting their eggs into the provisioned nest cells of their bee hosts. There are thousands of clep- toparasitic species, most associated with specific The Families of Bees genera of host bees. They directly or indirectly exterminate the host larva, ultimately consuming Seven families of bees are currently recognized. its provision. Adult females spend much of the day The Colletidae, Halictidae, Andrenidae,­Melittidae searching for and evaluating host nests. They dis- and Stenotritidae are grouped as short-tongued play numerous subtle adaptations to conceal their bees, while the Megachilidae and Apidae are long- eggs from the host female and repair damage tongued bees. The five more common families are incurred to nest cells during oviposition. Odor considered here. concealment and mimicry may be practiced as well. Social bee species (other than Apis) host their own parasitic bees, often evolving from within Family Colletidae: Yellow-Faced, their host’s genus. Psithyrus queens usurp bumble Masked and Plasterer Bees bee nests, enslaving unwitting host workers to produce parasite progeny. Robber genera among Distribution: Worldwide, but Greatest Diversity is the stingless bees (e.g., Lestrimelitta) raid host in the Southern Hemisphere, Including Australia. nests for honey and pollen. This is probably the oldest extant bee family. No studied species nests socially. Pollen is ­transported dry in hair brushes of the hind leg (e.g., Colletes) Conservation or mixed with nectar and carried internally in the crop (e.g., Hylaeus). Their tongue tips are Human activities also can harm bees. Bees tend to ­distinctively bilobed. They nest underground, or be sensitive to broad-spectrum insecticides, which rarely, in mortar and even sandstone (e.g., Colletes), if used indiscriminately or carelessly by farmers or in pithy stems (e.g., Hylaeus), or adopt holes in homeowners during bloom, can ­poison adults, or wood. The plasterer bees are so named for the later, their progeny. No genetic resistance has been peculiar, secreted, transparent, polyester membranes shown. Herbicides, when used to kill wildflowers, used to waterproof their nest cells; those of Hylaeus remove available forage for bees. Habitats and contain silk strands. Hylaeus (=Prosopis) (570 species) Bees (Hymenoptera: Apoidea: Apiformes) B 429 and Colletes (330 species) are the commonly sometimes in dense aggregations. The common, encountered genera in the U.S. and Europe; cosmopolitan cleptoparasite genus in the family is ­Leioproctus has 300+ species in Australia and Sphecodes (250 species). Halictids illustrate an ­temperate South America; Nesoprosopis has radi- unprecedented diversity of social organization, ated in the Hawaiian Islands, where many of its particularly among the 1,000+ species of species appear to be endangered. This subgenus Lasioglossum. contains the only cleptoparasites in the family. The alkali bee, Nomia melanderi, is the world’s Hylaeus may be the most cosmopolitan of all bee only intensively managed ground-nesting bee. In genera, found on all continents but Antarctica as regions of the western U.S., alfalfa (=lucerne) seed well as many oceanic islands, their dispersal growers construct large subirrigated nest sites with facilitated by their stem-nesting habits. salt-crusted surfaces. Densities of 400 nests/m2 over a hectare or more can be obtained with this gregarious bee. Nest sites can remain populous for Family: Andrenidae more than 50 years. Another effective alfalfa pollinator, Rhophitoides canus, is less intensively Distribution: Worldwide, Except Australia, Rare managed in regions of eastern Europe for alfalfa in the Moist Tropics. Species of this family nest seed production. underground. The­family includes two enormous genera: Andrena (1,400 species, ubiquitous in north temperate regions) and Perdita (600 or Family Megachilidae: Leaf-Cutting more species, mostly of the American Southwest Bees, Mason Bees, Carder Bees and and northern Mexico). Perdita are small-bodied, Others including the tiniest bee, Perdita minima (slen- der, 2 mm long, 1/3 mg). A few species of Perdita, Distribution: Worldwide. The common names for Andrena and Panurgus nest communally; no groups in this large ­family refer to the remark- studied andrenid is social. There are no clep- able diversity of exogenous materials that they toparasitic species in this family. Pollen is car- typically use to line or construct their nest cells. ried on the hind legs, and in some ­species, is Many nest above ground in twigs, stems and moistened with nectar. Probably all Perdita are wood, and will readily adopt drilled holes in these ­oligolectic, as are the majority of Andrena and substrates (termed “trap nests”). A few even nest ­species of other genera. in abandoned snail shells. Megachile and others line their nest cells, and partition and cap their nest tunnels, with strips and disks neatly cut from Family Halictidae: Sweat Bees, leaves or petals; other species build with leaf pulp, Alkali Bee, etc resin, nectar, mud, plant hairs, or pebbles. Forag- ing females of non-parasitic species can be easily Distribution: Worldwide. Most halictids are small recognized, as they are unique in (Fig. 30) carry- or medium sized. Some taxa are commonly known ing pollen in a scopa solely beneath the abdomen. as sweat bees because they alight on people’s skin Nearly all species are solitary. There are several to lap up sweat for the salts that it contains. Many cleptoparasitic ­genera (notably Coelioxys, 300 spe- halictids are darkly colored, others are a brassy or cies). Megachile is a cosmopolitan genus (900+ brilliant emerald green. Some Nomia have striking species); Osmia (300 species) are common in the pearly green or orange abdominal bands. Pollen is Northern ­Hemisphere. The world’s longest bee is carried on the hind legs, typically dry. Their nests Megachile pluto at 39 mm. Many megachilids are are burrows in soil, or occasionally, rotting wood, important pollinators, ­especially for plants in the 430 B Bees (Hymenoptera: Apoidea: Apiformes) pea and clover family (Fabaceae). The cavity-­nesting ­species are the most successful stowaways in transoceanic travel. The alfalfa leaf-cutting bee, Megachile rotun- data, came to the U.S. from the Near East as a stow- away before 1937. Burgeoning feral populations of this bee prospered in the semi-arid western U.S. The species’ value as an alfalfa pollinator soon became apparent. A multimillion-dollar industry developed in North America for cheaply mass rear- ing of this species for sale to alfalfa seed growers. Wooden or foam boards, each with several thou- sand nesting holes, are placed in shelters in alfalfa fields. Each shelter receives 50,000 or more females. This bee is versatile, pollinating other crops too, such as hybrid canola and various vegetable seeds. Several species of mason bees in the genus Osmia are more recently being managed in Japan, the U.S. and Europe to pollinate tree crops in the rose family, such as apples, plums, sweet cherries and almonds. One of these species has been dubbed “the blue orchard mason bee.” Only 250–300 blue orchard bees are needed to pollinate as many apple or cherry flowers as two to three hives of honey bees.

Family Apidae: Carpenter Bees, Orchid Bees, Bumble Bees, Stingless Bees, Honey Bees

Distribution: Worldwide. This family is large, eco- Bees (Hymenoptera: Apoidea: Apiformes), logically diverse and continues to be taxonomically Figure 30 Nest of Osmia (Megachilidae) in reed, perplexing. One or more tribes of this family is most split open to reveal partitioned nest cells each closely related to the lineage that evolved into today’s occupied by a single larva with its mass provision of highly eusocial Apinae. Many cleptoparasitic species pollen moistened with nectar (above); three nests are included (1,600 species). This unwieldy group is of a leaf-cutting bee (Megachile: Megachilidae), best recognized by its ­constituent tribes, of which consisting of a linear series of cells each wrapped there are many. Select ones are treated here. with cut leaf pieces (center); female of the alfalfa leaf cutting bee, Megachile rotundata, visiting alfalfa flowers (below). Note the pollen load carried dry in Subfamily Nomadinae: Cuckoo Bees a scopa of hairs beneath her abdomen. To the right is a "tripped" flower, the staminal column pressed Distribution: Worldwide. This is the largest group against the banner petal. Good alfalfa pollinators of cleptoparasitic bees (Nomada alone has 800 trip the flowers frequently (photos by William Nye). species). Most species are glossy, quite hairless Bees (Hymenoptera: Apoidea: Apiformes) B 431 and wasp-like with a rugged exoskeleton. They orchid flowers and, in the process, pollinate the can commonly be seen patrolling low over the orchids. The orchids provide no food, but rather ground for host nests. produce scents which male euglossines collect and place in a glandular pocket of their enlarged hind legs. These perfumes attract mates. Several Subfamily Xylocopinae: Carpenter species have intricate male displays. These large Bees bees are flying jewels, sporting metallic emerald, cobalt, violet and bronze colors as well as red, Distribution: Worldwide. Carpenter bees typically orange and yellow. They are important pollinators excavate nests above ground in pithy stems or even of many endangered tropical orchids and proba- bore into sound wood. Cells are unlined. Most bly the Brazil nut, too. species are solitary, but some are subsocial or even primitively ­eusocial. Females overwinter as mated adults; they can be very long-lived. The large car- Tribe Bombini: Bumble Bees penter bees ­(Xylocopa) are primarily tropical. They can resemble bumble bees, but have a smooth, Distribution: The Americas, Europe, Asia, North glossy dorsal abdomen and transport their pollen Africa. Bumble bees (Bombus) are large, furry, dry. Xylocopa pollinate commercial passion fruit; often black and yellow, orange or red bees. They they are also adept ­nectar robbers. Males of some are common in the world’s cooler climates, follow- Xylocopa hover for hours in aerial territories, pur- ing mountain ranges into the tropics. Few species suing any and all small airborne objects. The small live in deserts or rainforests. They nest shallowly carpenter bees (Ceratina) nest in dead stems of underground, often in abandoned rodent nests, or roses, sumac, elderberry and some grasses. sometimes above ground, either in tree cavities or, less commonly, beneath a leaf heap on the forest floor. They actively brood larvae to warm them, The Corbiculate Apinae: Orchid and fan their wings at the colony entrance to cool Bees, Bumble Bees, Stingless Bees, its contents. Few other bees can fly in cooler Honey Bees weather. Bombus consists of primitively eusocial species and a lesser number of social parasites. Distribution: Worldwide. This quartet of tribes They are important pollinators in alpine, boreal contains all of the highly eusocial bees, as well as and subarctic habitats. Queens of species such the primitively eusocial bumble bees and the as B. nevadensis and B. dahlbomi are the world’s mostly solitary orchid bees. All secrete wax, which most massive bees, weighing a gram or more (the they incorporate into their nest structures. They weight of a raw almond). carry pollen on a specially adapted, smooth region Bumble bees are important pollinators of of the hind leg referred to as the pollen basket or ­several crops, especially red and crimson clover. “corbicula.” Taxonomists formerly grouped these The honey bee proboscis is too short to probe such four tribes as a separate family. deeply tubular flowers. Bumble bees, having­longer tongues, work these flowers efficiently. Bumble bees have been imported into New Zealand and Tribe Euglossini: Orchid Bees Chile for clover pollination. They aid in the ­pollination of several other crops like alfalfa, and Distribution: New World Tropics, from Central several fruits, especially blueberries, cranberries Mexico into Argentina. The orchid bees are so and kiwi. A multimillion-dollar global business has named because the males collect scents from emerged from Europe for year-round propagation 432 B Bees (Hymenoptera: Apoidea: Apiformes) of disposable bumble bee colonies to pollinate Colony fission is unlikeApis , because for meli- greenhouse vegetables like tomatoes, peppers, egg- ponines, the new home is selected and ­furnished plants and squashes. Introduction of these few before the swarm issues from the parent colony. managed species outside of their native ranges can Workers assemble a complete new nest using mate- lead to feral populations that pose problems for rials transported from the parent ­colony. Only then native Bombus and perhaps other bees. does a group of workers and new queen fly to the new nest. The old queen is too large to fly and remains with the parent colony and its workers. Tribe Meliponini: Stingless Bees Workers of some stingless bees recruit nest- mates to food sources, but in ways different from Distribution: Old and New World Tropics. The Apis. Scouts of some species scentmark trails from stingless bees are highly eusocial, and as a group, productive flowers to the nest, depositing mandib- exhibit a sweeping diversity of adaptations and ular gland secretions on surfaces every few meters. natural history traits. Their permanent colonies Returning to the nest, this scout buzzes loudly; the can be populous, containing between 300 and longer the buzz, the greater the distance of the food 80,000 workers. Although stingless, many can from the colony. The scout’s behavior excites others defend their nests with irritating bites sometimes which follow the odor trail to the resource. This accompanied by caustic secretions. Queens are method of recruitment communicates not only the morphologically distinct from workers, their direction and distance of food from the nest, but ­status sometimes determined genetically, in other can lead other foragers directly to the food at any cases as an individual larva’s reproductive gamble. height by means of the odor trail. This three-di- Of the 260 known species, 70% are found in mensional road map is especially adaptive in tow- ­Central and South America. They are the most ering tropical forests where flowers are frequently common insects in Dominican and Baltic amber. found high in the leafy canopy. Stingless bees usually build nests in tree Stingless bees benefit people in several ways. ­hollows, although some species nest on exposed In the Neotropics, Melipona colonies are cultured surfaces, in underground cavities, or in termite for honey in special wooden hives, although yields or ant nests. Workers fashion a hard shell of are meager (2–5 pounds per year). Stingless bees ­“batumen” for the nest, consisting of wax blended pollinate numerous tropical crops, but their eco- with resin, mud or vegetation. Intricate nest nomic impact has not been widely estimated. entrance platforms and tubes are fashioned from Stingless bees are promising pollinators for green- wax, resin, or even plant latex. Within this shell, house crops. honey and pollen are stored in large irregular waxen pots. These rim the brood chamber, whose exterior is delineated by layers of pliable, delicate sheets of the “involucrum,” made of insulative wax Tribe Apini: True Honey Bees imbued with resin. Within this chamber are the waxen combs dedicated to brood rearing, grouped Distribution: Europe, Asia, Africa, Now Intro- in horizontal tiers supported by thin pillars, remi- duced to all Continents Except Antarctica. There niscent of nests of hornets or yellow-jacket wasps. are 11 currently accepted species of true honey Cells are typically mass provisioned with pollen, bees, all of the genus Apis. These are very different honey, and in some genera, glandular secretions from all other bees, such that their evolutionary (in a few cases, consisting of digested carrion). origins and ancestry remain unresolved. The genus Some genera (e.g., Lestrimellita) rob nests of other is largely restricted to tropical Asia. Taxonomic stingless bees for their honey and pollen stores. diversity is centered in Indonesia, Malaysia and Bees (Hymenoptera: Apoidea: Apiformes) B 433 the Philippines, where new species continue to be food, which together with the uniform comb dimen- discovered. Only the familiar western honey bee sions, yields adults of very consistent size. or “hive” bee, A. mellifera, is also native to Europe, Species of Apis can be assigned to one of three northern Asia, and most of Africa. Its colonization groups, based on body size and nesting habits. Two of cooler regions was facilitated by its honey stor- dwarf honey bees, exemplified by A. florea, have age habits that fuels the workers’ warming of their small colonies of a few thousand small workers brood. Because we value this species for honey, that construct beneath a branch a single exposed wax and pollination, and can manage it in trans- comb the size of a waffle. The top of this comb is portable hives, it has been further introduced broadened horizontally; recruitment dances per- throughout most of the world. formed on this surface are oriented simply in the The western honey bee is among the most direction of the food source. Several giant honey studied animals on the planet. Certainly their hall- bees (e.g., A. dorsata) also build a single exposed mark behavior is the remarkable abstract dance vertical comb, often in conspicuous groups, but language performed by foragers and scouts for beneath a stout branch or cliff. Living curtains of precisely communicating distance, direction and the huge workers envelop the massive comb; when quality for resources, translating the direction of disturbed, they pour off en masse to assail any gravity into celestial bearings. Once thought intruder. They are nonetheless robbed for honey. unique to Apis mellifera, this and other behaviors The remaining species ofApis build nests that con- now have been observed and studied for some of sist of multiple wax combs housed in a hollow tree the lesser-known species of Apis, too. or rock cavity. Cavities enhance defense and insu- Colony activities of Apis require sophisticated lation, but present problems with ventilation for coordination. Much of the information is commu- temperature, humidity and atmospheric control. nicated olfactorily using pheromones. Like the The most familiar representatives of this group are Meliponini, all Apis are highly eusocial, maintain- A. cerana and A. mellifera, which share many simi- ing populous perennial colonies. Queens, drones larities, including their management in hives. and workers are morphologically distinct. Among  Honey Bees bees, only worker Apis have a barbed sting that  Alfalfa Leafcutting Bee lodges in the skin and continues to pump venom  Apiculture even after the worker bee has been killed and  Orchid Bees swept away. Colonies reproduce by fissioning,  Hymenoptera again like stingless bees, but in Apis, it is the old  Carpenter Bees queen that departs with the swarm, whose work-  Pollination by Osmia Bees ers then scout out a suitable nesting site at which  Pollination and Flower Visitation they must construct their combs unassisted by the  African Honey Bees parent colony. This seems a riskier strategy, but it  Cape Honey Bees does allow swarms to disperse more widely. Honey bees thermoregulate their colonies using evapora- tive as well as convective cooling. Some tropical References species undertake mass defecation flights to fur- ther nest cooling. Only Apis produce the familiar Free JB (1993) Insect pollination of crops (2nd ed) Academic waxen vertical combs of uniform hexagonal cells Press, New York, NY that are reused over and over to house pollen, nectar Michener CD (2000) The bees of the world. Johns Hopkins University Press, New York, NY (as honey) or progeny, although the wax itself can- Michener CD, McGinley RJ, Danforth BN (1994) The bee not be recycled. Very unusual for bees, larval honey genera of North and Central America (Hymenoptera: bees are fed progressively rather than with a cache of Apoidea). Smithsonian Institution Press, Washington, DC 434 B Beesoniidae Müller A, Krebs A, Amiet F (1997) Bienen: Mitteleuropäische except for South America. Because it is a tropical Gattungen, Lebensweise, Beobachtung. Weltbild Verlag, insect, and lacks a diapause mechanism, it can Augsburg, Germany O’ Toole C, Raw A (1991) Bees of the world. Facts on file, New overwinter successfully only in warm areas or in York, NY greenhouses. Daytime temperatures below 10°C Prys-Jones OE, Corbet SA (1991) Bumblebees, Revised edi- are deleterious, and it rarely overwinters in areas tion. Cambridge University Press, Cambridge, UK where frost kills its host plants. Despite its inability Roubik DW (1989) Ecology and natural history of tropical bees. Cambridge University Press, Cambridge, UK to overwinter in cold areas, beet armyworm nev- Strickler K, Cane J (eds) (2003) Thomas Say publications in ertheless invades temperate areas annually. Despite entomology: proceedings: for non-native crops, whence this invasive potential, however, it is not normally pollinators of the future? Entomological Society of America, Lanham, MD, 204 pp considered a threat in temperate areas, except Westrich P (1989) Die Wildbienen Baden-Württembergs. sometimes in greenhouses. Allgemeiner Teil: Lebensräume, Verhalten, ökologie und Schutz. Verlag Eugen Ulmer, Stuttgart, Germany Life History Beesoniidae Seasonal activity varies considerably according A family of insects in the superfamily Coccoidae to climate. In warm locations, all stages can be (order Hemiptera). found throughout the year, although develop-  Bugs ment rate and overall abundance are reduced during the winter months. The life cycle can be completed in as few as 24 days, and six genera- Beeswax tions have been reared during 5 months of sum- mer weather in Florida. However, generation Beeswax is produced by Apis bees. It is produced times of 50–126 days have been observed, with a only by young worker bees. Beeswax consists of total of five generations annually, in southern fatty acids, esters, and hydrocarbons, and is secreted California. from glands on the ventral surface of the abdomen. Eggs are laid in clusters of 50–150 eggs per The beeswax is used by the bees to ­construct hon- mass. Females may deposit over 1,200 eggs during eycomb cells, in which their young are raised. After their lifetime, but normal egg production is about removal of honey from the honeycomb,­ the wax is 300–600. Eggs are usually deposited on the lower purified and used for many products, particularly surface of the leaf, and often near blossoms and candles, wood ­furniture polish, shoe polish, lubri- the tip of the branch. The individual eggs are cir- cants, and skin treatments. cular when viewed from above, but when exam- ined from the side the egg is slightly peaked, tapering to a point. The eggs are greenish to white in color, and covered with a layer of whitish scales Beet Armyworm, Spodoptera that gives the egg mass a fuzzy or cottony appear- exigua (Hübner) (Lepidoptera: ance. Eggs hatch in 2–3 days during warm weather, Noctuidae) but the incubation period is extended to about 4 days when it is cool. The developmental threshold john l. capinera for eggs is estimated at 12.4°C. University of Florida Gainesville, FL, USA Normally there are five instars, although addi- tional instars are sometimes reported. Duration Beet armyworm is a tropical insect, native to of the instars under warm (summer) conditions Southeast Asia. It is now found around the world, is reported to be 2.3, 2.2, 1.8, 1.0, and 3.1 days, Beet Armyworm, Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae) B 435 respectively, and at constant 30°C, instar develop- and soil particles held together with an oral ment time was reported to be 2.5, 1.5, 1.2, 1.5, and secretion that hardens when it dries. The pupa is 3.0 days, respectively. Total larval development time light brown in color and measures about 15–20 is also influenced by diet quality. The developmen- mm in length. Duration of the pupal stage is 5–7 tal threshold for larvae is estimated at 13.6°C. Only days during warm weather. 1 mm long at hatching, the larvae attain a mean The moths are moderately sized, the wing length of 2.5, 5.8, 8.9, 13.8, and 22.3 mm during span measuring 25–30 mm. The forewings are instars 1–5, respectively. Head capsule widths aver- mottled gray and brown, and normally with an age 0.25, 0.45, 0.70, 1.12, and 1.80 mm, respectively. irregular banding pattern and a light colored bean- The larvae are pale green or yellow in color shaped spot. The hind wings are a more uniform during the first two instars, but acquire pale stripes gray or white color, and trimmed with a dark line during instar 3. During instar 4, larvae are darker at the margin. Mating occurs soon after emergence dorsally, and possess a dark lateral stripe. Larvae of the moths, and oviposition begins within 2–3 during instar 5 are quite variable in appearance, days. Oviposition extends over a 3–7 day period, tending to be green dorsally with pink or yellow and the moths usually perish within 9–10 days of color ventrally and a white stripe laterally. A series emergence. of dark spots, dashes or triangles (Fig. 31) is often This insect has a wide host range, occurring present dorsally and dorsolaterally. Sometimes as a serious pest of vegetable, field, and flower larvae are very dark in color. The spiracles are crops; even trees are sometimes attacked. Among white with a narrow black border. The body is susceptible vegetable crops are asparagus, bean, practically devoid of hairs and spines. It is easily beet, broccoli, cabbage, cauliflower, celery, chickpea, confused with other caterpillar pests. corn, cowpea, eggplant, lettuce, onion, pea, pepper, Initially the larvae of beet armyworm are gre- potato, radish, spinach, sweet potato, tomato, and garious, feeding as a group and skeletonizing plant turnip. Field crops damaged include alfalfa, corn, foliage. As they mature they become solitary and cotton, peanut, safflower, sorghum, soybean, quite mobile, often traveling from plant to plant. ­sugarbeet, and tobacco. Weeds also are suitable Cannibalism may occur when larvae are at high for larval development, including such common densities or feeding on food low in nitrogen. plants as lamb’s-quarters, Chenopodium album.; Pupation occurs in the soil. The larva gener- mullein, Verbascum sp.; pigweed, ­Amaranthus ally constructs a pupal chamber near the soil spp.; purslane, Portulaca spp.; ­Russian thistle, surface, digging only about one cm beneath the ­Salsola kali; parthenium, ­Parthenium sp.; and surface. The chamber is constructed from sand tidestromia, Tidestromia sp. Although the host range is wide, there are ­significant differences in suitability even among hosts considered to be suitable. Numerous natural enemies have adapted to this pest. Among the most common parasitoids are braconid wasps, and the tachinid Lespsia archippivora (Riley) (Diptera: Tachinidae). Preda- tors frequently attack the eggs and small larvae; among the most important are minute pirate bugs, Orius spp. (Hemiptera: Anthocoridae); bigeye Beet Armyworm, Spodoptera exigua (Hübner) bugs, Geocoris spp. (Hemiptera: Lygaeidae); dam- (Lepidoptera: Noctuidae), Figure 31 Mature larva sel bugs, Nabis spp. (Hemiptera: Nabidae); and a of beet armyworm, Spodoptera exigua (Hübner). predatory shield bug, Podisus maculiventris (Say). 436 B Beet Armyworm, Spodoptera exigua ((Hübner)) (Lepidoptera: Noctuidae) Pupae are subject to attack, especially by ants. the need for crop treatment with insecticides. Fungal diseases, Erynia sp. and Nomurea rileyi, Regular monitoring of crops, probably about and a nuclear polyhedrosis virus also inflict some twice per week, is ­recommended because adults mortality. The important mortality factors vary frequently invade from surrounding crops or among crops, and among geographic regions. weeds. None except the nuclear polyhedrosis virus are The relatively high abundance of beet army- highly specific to beet armyworm, which may worm has stimulated frequent application of explain why they are not especially effective. Virus insecticides. Chemical insecticides and Bacillus is considered to be the most important mortality thuringiensis are commonly applied to foliage to factor in Mexico. protect against defoliation. Insecticide resistance is a major problem in management of this insect, possibly because it attacks crops such as flowers, Damage cotton, and vegetables – crops that are treated ­frequently with insecticides. Beet armyworm Larvae feed on both foliage and fruit. Young lar- abundance is favored by frequent insecticide use, vae feed gregariously and skeletonize foliage. As and it is considered to be a secondary or induced they mature, larvae become solitary and eat large pest in some crops. Also, intensive use of insecti- irregular holes in foliage. They also burrow into cides for beet armyworm control in vegetables the crown or center of the head on lettuce, or on such as celery has stimulated outbreaks of other the buds of cole crops. As a leaf feeder, beet army- pests, principally American serpentine leafminer, worm ­consumes much more cabbage tissue than Liriomyza trifolii (Burgess). diamondback moth, Plutella xylostella (Lin- Host plant resistance in several crops has been naeus), but is less damaging than cabbage looper, studied for its contribution to beet armyworm pest Trichoplusia ni (Hübner). This insect is also management. In tomato, for example, resistance is regarded as a serious pest of celery in California, correlated with total glycoalkaloid concentration and damage is directly correlated with abundance in the fruit tissue. However, leaf tissue does not of late instar larvae late in the season. However, have any effective antibiotic chemistry, so larvae damage to foliage and petioles (stalks) during the are able to develop on plants even if they have first half of the growing season is of little conse- unsuitable tomato fruit. quence because these plant parts are removed at Several insect pathogens may prove to harvest. Tomato fruit is most susceptible to injury, be ­useful for suppression of beet armyworm. especially near fruit maturity, but beet armyworm A nuclear polyhedrosis virus isolated from beet is not considered to be as threatening to tomato armyworm is fairly effective as a bioinsecticide as is corn earworm, Helicoverpa zea (Boddie). under greenhouse conditions, where inactivation Larvae not only damage tomato fruit, but may by ultraviolet light in sunlight is not a severe appear as ­contaminants in processed tomato. ­problem. It is as effective as commonly used insec- ticides, but presently is not commercially available. Entomopathogenic nematodes (Rhabditida: Stein- Management ernematidae and Heterorhabditidae) successfully infect both larvae and adults of beet armyworm, Pheromone traps can be used to detect the pres- and infected adults can fly short distances, helping ence of adult beet armyworm. Visual sampling to spread the pathogens. Use of nematodes is simi- for damage and larvae, combined with an action larly constrained by ­environmental conditions, threshold of 0.3 larvae per plant, was used success- but these biological control agents are available fully on cabbage in south Texas to determine commercially. Beetles (Coleoptera) B 437 References Beetles are holometabolous insects which have the front wings hardened and serving as Ali A, Gaylor MJ (1992) Effects of temperature and larval diet ­protection for the hind wings which are used on development of the beet armyworm (Lepidoptera: exclusively for flying. The front wings, or elytra, are Noctuidae). Environ Entomol 21:780–786 Brown ES, Dewhurst CF (1975) The genus Spodoptera usually raised during flight; at rest, they meet in a ­(Lepidoptera, Noctuidae) in Africa and the Near ­East. straight line along the back. When not in use, the Bull Entomol Res 65:221–262 hind wings are folded longitudinally and trans- Capinera JL (2001) Handbook of vegetable pests. Academic versely and hidden under the elytra. Beetles also Press, San Diego, CA, 729 pp Wilson JW (1932) Notes on the biology of Laphygma exigua possess chewing mouthparts, usually 11-seg- Huebner. Fla Entomologist 16:33–39 mented antennae, and the abdominal sternites are Wilson, JW 1933. The biology of parasites and predators of usually more heavily sclerotized than the tergites. Laphygma exigua Huebner reared during the season of 1932. Fla Entomol 17:1–15 Anatomy

Beetles (Coleoptera) The body of an adult beetle is composed, like all insects, of three regions: head, thorax, and ­abdomen. michael c. thomas What is visible in dorsal view in beetles, though, is Division of Plant Industry, Florida Department of the head, prothorax, and elytra (singular, elytron), Agriculture and Consumer Services Gainesville, which cover the meso- and metathorax, and usually FL, USA all of the abdomen. The head bears the eyes, chewing mouthparts, The present era could with some justification be and usually 11-segmented antennae. The size and called the “Age of the Beetles.” Members of the order placement of the compound eyes varies widely Coleoptera comprise the largest order of life. One within the order, and eyelessness is fairly frequent, out of every five species of living things on Earth is especially in soil and litter inhabiting beetles, and a beetle. No one knows precisely how many beetle those which dwell in caves. The presence of ocelli species have been described, but estimates start at occurs in only a very few small groups. Mouthparts 250,000. Beetles live in almost every habitat where may be borne on the end of a rostrum (most notably insects are found but do not come to the attention in weevils, Curculionidae). Beetles exhibit almost of the layperson as often as members of some other endless modifications of the mouthparts, especially orders which are more conspicuous by virtue of of the mandibles, which may be the most striking their size or habits. The majority of beetles are capa- feature of the individual, as in Lucanidae and some ble of flight and some fly quite well, but none has Cerambycidae. The antennae in beetles range from adopted the truly aerial lifestyle of butterflies and simply threadlike (filiform) or beadlike (monili- dragonflies. Most spend the greater part of their form), to gradually (clavate) or abruptly (capitate) lives in cryptic habitats – under bark and in dead clubbed, or saw-like (serrate), or with the club seg- wood, in soil and leaf litter, in the water of ponds, ments asymmetrically developed and capable of lakes, and streams. Although some beetles are opening and closing like a fan (lamellate), or elbowed among the largest insects, most are quite small; like an ant’s antennae (geniculate), or feathery (pec- indeed, some are among the smallest of insects. tinate or flabellate). Although most beetles have Nevertheless, beetles are unrivaled in their 11-segmented antennae, reduction in the number of diversity of form and color and in the nearly segments (to only one or two ­segments in extreme ­endless ways they have found to live, feed, and examples) is common, while an increase in the num- reproduce. ber of segments is quite uncommon. 438 B Beetles (Coleoptera) The thorax is composed of three parts: the pro- ­Triassic. They were preceded by a group of thorax bears the forelegs; the mesothorax gives rise ­beetle-like insects called the Protocoleoptera to the forewings, or elytra, and the middle legs; the that arose in the Lower Permian. By the Jurassic, metathorax bears the hind wings and hindlegs. The many modern families had arisen, and most of legs are 5-segmented, composed of (from closest to the rest appeared during the Cretaceous, coinci- the body) the coxa, trochanter, femur, tibia, and tar- dent with the rise of the flowering plants. Inter- sus. The tarsus is composed primitively of five tar- estingly, many of the Cenozoic amber fossils can someres, but this is often reduced and the tarsal be attributed to modern genera. formula (the number of tarsomeres on the front, middle, and hind legs) is important in beetle identi- fication. The elytra ­generally completely cover the Classification dorsal part of the metathoraz and abdomen, but are secondarily short in many groups (Staphylinidae, Beetles were recognized as a distinct group of Silphidae, Cerambycidae, etc.). They almost always insects as far back as the ancient Greeks, but the meet in a straight line, one of the very few excep- classification within the group has been in a state tions being the genus Meloe in the Meloidae. of flux up to the present day. The limits of the order The dorsal part of the abdomen is usually soft, are well understood, with the only issue being except in those groups with abbreviated elytra; the whether to include or exclude the twisted-wing ventral surface of the abdomen is almost always parasites (Strepsiptera). Most now treat them as a heavily sclerotized. separate order near Coleoptera, but some have argued that their true affinities lie with the Diptera. Within the Coleoptera, the general classification is Life Cycle fairly well accepted but disagreement persists on the ranking or placement of some family-level Beetles undergo complete metamorphosis. The life groups. The classification presented here is that cycle of the typical beetle includes egg, three to five used in the two-volume ­American Beetles (Arnett larval instars, pupa, and adult. A few beetle families and Thomas 2000, Arnett et al. 2002), the most have more complicated life histories: Micromalthi- recently published, major general work on beetles. dae have multiple larval forms and paedogenesis There are 166 families of beetles in the world; (reproduction by larvae); several families, e.g., Mel- 131 of those occur in America north of Mexico. oidae, Ripiphoridae, Passandridae, undergo hyper- The order is divided very unequally into four metamorphosis, with the first instar larva being ­suborders: Archostemata, Myxophaga, Adephaga, considerably different from­succeeding instars. The and Polyphaga. length of the life cycle varies­ widely within the order, but generation length of most beetles falls within a few weeks to 1 or 2 years. A few beetles, Archostemata notably some Cerambycidae, under extraordinary conditions can spend decades as larvae. Only four families comprise this primitive subor- der. Beetles very similar to present-day Cupedidae are known from the Lower Triassic. Two families, Evolution Cupedidae and Micromalthidae, are known from the Nearctic. Most are found in decaying wood. It is generally agreed the beetles are most closely The sole member of Micromalthidae,Micromalthus related to the neuropteroid orders. The first debilis LeConte, has an unusual and complex life ­fossils of true Coleoptera date back to the history, including paedogenesis. Beetles (Coleoptera) B 439 Myxophaga predominantly predacious and aquatic. The Histeri- dae and Sphaeritidae are terrestrial and predacious. Another four families have been assigned to this, Superfamily: StaphylinoideaThis family contains the most recently recognized suborder. Two fami- six small or moderate-sized families and one huge lies, Microsporidae and Hydroscaphidae, occur in one, the Staphylinidae, which has more than 4,100 the Nearctic. The few minute species are associ- species in the Nearctic and more than 46,000 ated with algae. worldwide. All the families occur in the Nearctic. Staphylinids, or rove beetles, often are found around decaying vegetable material and dead Adephaga ­animals, where they feed on fly larvae and other insects. Many staphylinids live in the nests of social Nine families comprise this suborder, the only one insects, ants and termites primarily, and show that is composed exclusively (except for one small many physical and behavioral adaptations to that family of wood-inhabiting beetles, the Rhysodidae) way of life. Most staphylinids have very short elytra of predacious beetles. Eight families occur in the and flexible abdomens. Nearctic, the Carabidae or ground beetles, being by far the largest family in the suborder, with 2,635 species and subspecies being recorded from the Series: Scarabaeiformia Nearctic and about 40,000 for the world. Carabids often are found on the ground under stones or This series contains only the single superfamily logs, or in leaf litter, but many, especially in the tropics, are arboreal. They are usually small to Superfamily: Scarabaeoidea moderate in size. Most are darkly colored, but This superfamily contains 11 small or moderate- many exhibit brilliant metallic colors. Most ground sized families and one very large one, the Scarabaei- beetles are predacious, feeding on soft-bodied dae. There are more than 27,800 species of scarab insects, but some are specialized predators of snails beetles in the world; about 1,700 occur in the Nearc- and millipeds. A few are seed feeders. Beetles in tic. This superfamily includes the ­relatively small most of the other families spend most of their lives but well-known Lucanidae (stag beetles) and Pas- in fresh water. salidae (bess beetles). The Scarabaeidae include some of the largest known beetles, such as the mem- bers of the genera Dynastes and Megasoma in the Polyphaga New World, and Goliathus in tropical Africa. Males of many scarabs bear spectacular horns on the head All the rest of the beetle families are assigned to and/or pronotum with which they battle each other this suborder. It has been subdivided into several for females. Scarab beetles have extremely diverse series and numerous superfamilies. feeding habits. Many feed on dung of mammals, some being extremely specific on the kind of dung they will accept. Dung beetles provision burrows Series: Staphyliniformia with dung for their larvae, some rolling balls of dung away for burying and sculpting the dung ball This series is composed of two superfamilies. into ­special shapes. Some even tend the dung to ­prevent the growth of mold on it. Many ­others feed Superfamily: Hydrophiloidea in soil, humus, and decaying wood. Some, like the Three families, two moderately sized and one small, ­Japanese beetle Popilia japonica Newman, feed on comprise this superfamily. The Hydrophilidae are living plants and are economic pests of extreme 440 B Beetles (Coleoptera) importance. Many others are found in nests of Superfamily: Elateroidea social insects, primarily ants and termites. Fifteen rather diverse families comprise this superfamily, all but three of which are found in the Nearctic. The largest family is the Elateridae, Series: Elateriformia or click beetles. There are about 10,000 species of click beetles in the world, with 965 recorded This series contains five mostly small superfamilies. from the Nearctic. Click beetles (and a few of the other families) bear a “click” mechanism on Superfamily: Scirtoidea the pro- and mesosternum that allows them to Four families, three of which are found in the fling themselves into the air with some force Nearctic, comprise this superfamily. Two families, if they are placed on their backs. Members of Eucinetidae and Clambidae, contain small to one mostly tropical group of click beetles are ­minute beetles that are found in leaf litter and luminescent. Other large or widely distributed apparently feed on fungus. Scirtidae are aquatic as families include the Lampyridae, Lycidae, Can- larvae and adults generally are found in wet tharidae, and Eucnemidae. habitats.

Superfamily: Dascilloidea Series: Bostrichiformia Only two small families, Dascillidae and Rhipic- eridae (Figs. 32 and 33) comprise this superfam- The series includes two small superfamilies, plus ily. Larvae of Rhipiceridae are hypermetamorphic the Jacobsoniidae, which have not been placed in and parasitic on immature annual cicadas a superfamily. (Heteroptera).

Superfamily: Buprestoidea Superfamily: Derodontoidea Two families, Schizopodidae and Buprestidae, Only the Derodontidae are included in this super- are included in this superfamily. The Schizopodi- family. They are found on slime molds. dae are a small family, confined to the western Nearctic. The Buprestidae are one of the larger Superfamily: Bostrichoidea families of Coleoptera, with 788 species and sub- Four families are included here, Nosodendridae, species recorded from the Nearctic and more Dermestidae, Bostrichidae, and Anobiidae. The than 14,000 in the world. These often brilliantly last three including many economically impor- colored beetles are mostly wood borers as larvae, tant pests of animal products such as wool, leather, although some are leaf miners. A few are of eco- feathers, and silk (Dermestidae) and stored prod- nomic importance. ucts and wood or wood products (Bostrichidae and Anobiidae). Superfamily: Byrrhoidea There are 12 mainly small families assigned here; most of the species are aquatic or subaquatic. All but one of the families are found in the Nearctic. Series: Cucujiformia The water penny beetles, Psephenidae, with their remarkably flattened larvae, are found on rocks This huge series contains the rest of the Coleoptera, in streams. arranged in six superfamilies. Beetles (Coleoptera) B 441

Beetles (Coleoptera), Figure 32 Some representative beetles: top left, drugstore beetle, Stegobium paniceum (Anobiidae); top right, lesser grain borer, Rhyzopertha dominica (Bostrichidae); second row left, cowpea weevil, Callosobruchus maculatus (Bruchidae); second row right, Buprestis lineatus (Bupres- tidae); third row left, Pasimachus sublaevis (Carabidae); third row right, banded hickory borer, Knulli- ana cincta (Cerambycidae); bottom left, Trirhabda bacharidis (Chrysomelidae); bottom right, Cicindela punctulata (Carabidae) (photos by Lyle Buss). 442 B Beetles (Coleoptera)

Beetles (Coleoptera), Figure 33 Some additional representative beetles: top left, Neorthopleura thoracica (Cleridae); top right, Mexican bean beetle, Epilachna varivestis (Coccinellidae); second row left, eyed click beetle, Alaus oculatus (Elateridae); second row right, maize weevil, Sitophilus zeamais (Curculionidae); third row left, striped blister beetle, Epicauta vittata (Meloidae); third row right, a firefly, Photinus tanytox- us (Lampyridae); bottom left, a rove beetle, Platydracus fossator (Staphylinidae); bottom right, Hercules beetle, Dynastes titus (Scarabaeidae) (Dynastes and Epilachna by Jim Castner; other photos by Lyle Buss). Beetles (Coleoptera) B 443 Superfamily: Lymexyloidea plants, although some attack living trees. Many This superfamily contains only the ship-timber are of economic importance. Some very large beetles, Lymexylidae, a small group of soft-bodied, forms occur in the tropics and are among the wood-boring beetles. largest beetles. The leaf beetles, Chrysomeli- dae, include about 35,000 ­species worldwide Superfamily: Cleroidea and about 1,720 in the Nearctic. Chrysomelids Three moderate-sized families of predominantly differ from cerambycids in usually being predacious beetles comprise this superfamily. smaller, less elongate, and with shorter anten- nae. Often they are brightly colored. Leaf bee- Superfamily: Cucujoidea tles are associated predominantly with living This is a large superfamily composed of 31 mostly plants, feeding on the foliage and roots. Many small to moderate-sized families, ten of which do are economically important pests of agricul- not occur in the Nearctic. Members of most of turally important crops. The seed beetles, the families are associated with fungus, but some Bruchidae, often are combined with the leaf are predominantly predacious, such as the largest beetles. Several are important pests of stored and best-known family, Coccinellidae, and a few legume seeds. (Bothrideridae and Passandridae) even contain species which have parasitic larvae. Superfamily: Curculionoidea

Superfamily: Tenebrionoidea The largest family of living organisms is included among the eight families in this superfamily. The This is the second largest superfamily with weevils, Curculionidae, contain more than 60,000 30 families, six of which do not occur in the species worldwide and about 2,400 in the Nearc- Nearctic. Most of the families are small to moder- tic. As presently defined, the Curculionidae are ate in size, but the Tenebrionidae are one of the restr-icted to curculionoids with geniculate largest ­families of Coleoptera, with about 19,000 antennae. They are almost entirely herbivorous, species worldwide and about 1,100 in the Nearc- attacking all parts of all kinds of plants. Many of tic. Although the Tenebrionidae are found in all the worst ­agricultural pests are weevils. The Bren- kinds of habitats, the family is especially well rep- tidae, or primitive weevils, are mostly tropical but resented in deserts. They are usually sombre in one oak pest occurs in the eastern Nearctic. The coloration, hence their common name of darkling Anthribidae, or fungus weevils, are associated beetles, and often are found on the ground under with fungi of various kinds. rocks and logs. Classification of the Order Coleoptera Lin- naeus 1758. Superfamily: Chrysomeloidea Suborder: ARCHOSTEMATA Kolbe 1908 Cupedidae Laporte 1836, The reticulated The superfamily contains five families, two of beetles which are very large. The longhorn beetles, Ommatidae Sharp and Muir 1912 ­Cerambycidae, contains more than 20,000 spe- cies worldwide and more than 900 in the Crowsonellidae Iablokoff-Khnzorian 1983 Nearctic. They are generally elongate, hand- Micromalthidae Barber 1913, The telephone- some beetles with long to very long antennae. pole beetles Most are ­associated with dead or dying woody Suborder: MYXOPHAGA Crowson 1955 444 B Beetles (Coleoptera)

Lepiceridae Hinton 1936 Staphylinidae Latreille 1802, The rove Microsporidae Crotch 1873, The minute bog beetles beetles Series: SCARABAEIFORMIA Crowson 1960 Hydroscaphidae LeConte 1874, The skiff Superfamily: SCARABAEOIDEA Latreille 1802 beetles Lucanidae Latreille 1804, The stag beetles Torridincolidae Steffan 1964 Diphyllostomatidae Holloway 1972, The Suborder: ADEPHAGA Schellenberg 1806 diphyllostomatid beetles Rhysodidae Laporte 1840, The wrinkled bark Passalidae Leach 1815, The bess beetles beetles Glaresidae Semenovrlan-Shanskii and Med- Carabidae Latreille 1802, The ground beetles vedev 1932, The glaresid beetles Gyrinidae Latreille 1810, The whirligig beetles Trogidae MacLeay 1819, The skin beetles Haliplidae Aubé 1836, The crawling water beetles Pleocomidae LeConte 1861, The rain beetles Trachypachidae C. G. Thomson 1857, The false Geotrupidae Latreille 1802, The earth-boring ground beetles dung beetles Noteridae C. G. Thomson 1860, The burrowing Belohinidae Paulian 1959 water beetles Ochodaeidae Mulsant and Rey 1871, The Amphizoidae LeConte 1853, The trout-stream ochodaeid scarab beetles beetles Hybosoridae Erichson 1847, The hybosorid Hygrobiidae Régimbart 1878 scarab beetles Dytiscidae Leach 1815, The predacious diving Ceratocanthidae Cartwright and Gordon beetles 1971, The ceratocanthid scarab beetles Suborder: POLYPHAGA Emery 1886 Glaphyridae MacLeay 1819, The glaphyrid Series: STAPHYLINIFORMIA Lameere 1900 scarab beetles Superfamily: HYDROPHILOIDEA Latreille 1802 Scarabaeidae Latreille 1802, The scarab beetles Hydrophilidae Latreille 1802, The water ­scavenger beetles Series: ELATERIFORMIA Crowson 1960 Sphaeritidae Shuckard 1839, The false clown Podabrocephalidae Pic 1930 beetles Rhinorhipidae Lawrence 1988 Synteliidae Lewis 1882 Superfamily: SCIRTOIDEA Fleming 1821 Histeridae Gyllenhal, The clown beetles Decliniidae Nikitsky et al. 1994 Superfamily STAPHYLINOIDEA Latreille 1802 Eucinetidae Lacordaire 1857, The plate-thigh Hydraenidae Mulsant 1844, The minute beetles moss beetles Clambidae Fischer 1821, The minute beetles Ptiliidae Erichson 1845, The feather-winged Scirtidae Fleming 1821, The marsh beetles beetles Superfamily: DASCILLOIDEA Guérin-Méneville Agyrtidae C. G. Thomson 1859, The primitive 1843 carrion beetles Dascillidae Guérin-Méneville 1843 Leiodidae Fleming 1821, The round fungus Rhipiceridae Latreille 1834, The cicada para- beetles site beetles Scydmaenidae Leach 1815, The antlike stone Superfamily: BUPRESTOIDEA Leach 1815 beetles Schizopodidae LeConte 1861, The schizopo- Silphidae Latreille 1807, The carrion beetles did beetles Beetles (Coleoptera) B 445

Buprestidae Leach 1815, The metallic wood- Lampyridae Latreille 1817, The firefly beetles boring beetles Omethidae LeConte 1861, The false firefly Superfamily: BYRRHOIDEA Latreille 1804 beetles Byrrhidae Latreille 1804, The pill beetles Cantharidae Imhoff 1856, The soldier beetles Elmidae Curtis 1830, The riffle beetles Series: BOSTRICHIFORMIA Forbes 1926 Dryopidae Billberg 1820, The long-toes Jacobsoniidae Heller 1926, The Jacobson’s beetles beetles Lutrochidae Kasap and Crowson 1975, The Superfamily: DERODONTOIDEA LeConte 1861 robust marsh-loving beetles Derodontidae LeConte 1861, The Limnichidae Erichson 1846, The minute ­tooth-necked fungus beetles marsh-loving beetles Superfamily BOSTRICHOIDEA Latreille 1802 Heteroceridae MacLeay 1825, The varie- Nosodendridae Erichson 1846, The gated mod-loving beetles ­wounded-tree beetles Psephenidae Lacordaire 1854, The water Dermestidae Latreille 1804, The skin and penny beetles larder beetles Cneoglossidae Champion 1897 Bostrichidae Latreille 1802, The horned Ptilodactylidae Laporte 1836, The ­powder-post beetles ­toe-winged beetles Anobiidae Fleming 1821, The death-watch Chelonariidae Blanchard 1845, The turtle beetles beetles Series: CUCUJIFORMIA Lameere 1938 Eulichadidae Crowson 1973, The eulichadid Superfamily: LYMEXYLOIDEA Fleming 1821 beetles Lymexylidae Fleming 1821, The ship-timber Callirhipidae Emden 1924, The cedar beetles beetles Superfamily: ELATEROIDEA Leach 1815 Superfamily: CLEROIDEA Latreille 1802 Artematopodidae Lacordaire 1857, The Phloiophilidae Kiesenwetter 1863 ­soft-bodied plant beetles Trogossitidae Latreille 1802, The Brachypsectridae Leconte and Horn 1883, ­bark-­gnawing beetles The Texas beetles Chaetosomatidae Crowson 1952 Cerophytidae Latreille 1834, The rare click Cleridae Latreille 1802, The checkered beetles beetles Eucnemidae Eschscholtz 1829, The false Acanthocnemidae Crowson 1964 click beetles Phycosecidae Crowson 1952 Throscidae Laporte 1840, The false metallic wood-boring beetles Prionoceridae Lacordaire 1857 Elateridae Leach 1815, The click beetles Melyridae Leach 1815, The soft-winged flower beetles Plastoceridae Crowson 1972 Superfamily: CUCUJOIDEA Latreille 1802 Drilidae Blanchard 1845 Omalisidae Lacordaire 1857 Protocucujidae Crowson 1954 Lycidae Laporte 1836, The net-winged Sphindidae Jacquelin du Val 1860, The beetles ­dry-fungus beetles Telegeusidae Leng 1920, The long-lipped Brachypteridae Erichson 1845, The beetles ­short-winged flower beetles Phengodidae LeConte 1861, The glowworm Nitidulidae Latreille 1802, The sap-feeding beetles beetles 446 B Beetles (Coleoptera)

Smicripidae Horn 1879, The palmetto Latridiidae Erichson 1842, The minute brown beetles scavenger beetles Monotomidae Laporte 1840, The root-eating Superfamily: TENEBRIONOIDEA Latreille 1802 beetles Mycetophagidae Leach 1815, The hairy Boganiidae Sen Gupta and Crowson 1966 ­fungus beetles Helotidae Reitter 1876 Archeocrypticidae Kaszab 1964, The Phloeostichidae Reitter 1911 archeocryptic beetles Silvanidae Kirby 1837, The silvanid flat bark Pterogeniidae Crowson 1953 beetles Ciidae Leach 1819, The minute tree-fungus Passandridae Erichson 1845, The parasitic beetles flat bark beetles Tetratomidae Billberg 1820, The polypore Cucujidae Latreille 1802, The flat bark fungus beetles beetles Melandryidae Leach 1815, The false darkling Laemophloeidae Ganglbauer 1899, The beetles lined flat bark beetles Mordellidae Latreille 1802, The tumbling Propalticidae Crowson 1952 flower beetles Phalacridae Leach 1815, The shining flower Rhipiphoridae Gemminger and Harold 1870, beetles The wedge-shaped beetles Hobartiidae Sen Gupta and Crowson 1966 Colydiidae Erichson 1842, The cylindrical bark beetles Cavognathidae Sen Gupta and Crowson 1966 Monommatidae Blanchard 1845, The Cryptophagidae Kirby 1837, The silken ­opossum beetles ­fungus beetles Zopheridae Solier 1834, The ironclad beetles Lamingtoniidae Sen Gupta and Crowson 1969 Ulodidae Pascoe 1869 Languriidae Crotch 1873, The lizard Perimylopidae St. George 1939 beetles Chalcodryidae Watt 1974 Erotylidae Latreille 1802, The pleasing Trachelostenidae Lacordaire 1859 ­fungus beetles Tenebrionidae Latreille 1802, The darkling Byturidae Jacquelin du Val 1858, The beetles ­fruitworm beetles Prostomidae C. G. Thomson 1859, The Biphyllidae LeConte 1861, The false skin ­jugular-horned beetles beetles Synchroidae Lacordaire 1859, The synchroa Bothrideridae Erichson 1845, The dry bark beetles beetles Oedemeridae Latreille 1810, The Cerylonidae Billberg 1820, The minute bark ­pollen-feeding beetles beetles Stenotrachelidae C. G. Thomson 1859, The Alexiidae Imhoff 1856 false long-horned beetles Discolomatidae Horn 1878 Meloidae Gyllenhal 1810, The blister beetles Endomychidae Leach 1815, The handsome Mycteridae Blanchard 1845, The palm and fungus beetles flower beetles Coccinellidae Latreille 1807, The ladybird Boridae C. G. Thomson 1859, The conifer beetles bark beetles Corylophidae LeConte 1852, The minute Trictenotomidae Blanchard 1845 fungus beetles Behavior of Insects: Genetic Analysis by Crossing and Selection B 447

Pythidae Solier 1834, The dead log bark  Leaf Beetles beetles  Longicorn Beetles Pyrochroidae Latreille 1807, The fire-colored  Powderpost Beetles beetles  Riffle Beetles Salpingidae Leach 1815, The narrow-waisted  Rove Beetles bark beetles  Sap Beetles Anthicidae Latreille 1819, The antlike flower  Water Penny Beetles beetles Aderidae Winkler 1927, The antlike leaf beetles References Scraptiidae Mulsant 1856, The false flower beetles Arnett RH Jr, Thomas MC (eds) (2000)American bee- tles, vol 1: Archostemata, Myxophaga, Adephaga, Superfamily: CHRYOMELOIDEA Latreille 1802 Polyphaga: Staphyliniformia. CRC Press, Boca Raton, Cerambycidae Latreille 1802, The FL, 443 pp ­long-horned beetles Arnett RH Jr, Thomas MC, Skelley PE, Frank JH (eds) (2002) Bruchidae Latreille 1802, the pea and bean American beetles, vol 2: Polyphaga: Scarabaeoidea through Curculionoidea. CRC Press Boca Raton, FL, 861 pp weevils Crowson RA (1981) The biology of the Coleoptera. Academic Megalopodidae Latreille 1802, The Press, New York, NY, 802 pp ­megalopodid leaf beetles Lawrence JF (1982) Coleoptera. In: Parker SB (ed) Synopsis Orsodacnidae C. G. Thomson 1859, The and classification of living organisms, vol 2. McGraw- Hill Publishers, New York, NY, pp 482–553 ­orsodacnid leaf beetles Lawrence JF (Co-ordinator). Chapter 34. Coleoptera. In: Stehr F Chrysomelidae Latreille 1802, The leaf beetles (ed) Immature insects, vol 2. Kendall/Hunt Publishing, Superfamily: CURCULIONOIDEA Latreille 1802 Dubuque, IA, pp 144–658 Lawrence JF, Britton EB (1994) Australian beetles. Melbourne Nemonychidae Bedel 1882, The pine-flower University Press, Carlton, Victoria, Australia, 192 pp snout beetles Lawrence JF, Hastings AM, Dallwitz M, Paine TA, Zurcher EJ Anthribidae Billberg 1820, The fungus (1999) Beetle larvae of the world: descriptions, illustrations, weevils and information retrieval for families and ­subfamilies. CD-ROM, Version 1.1 for MS-Windows. CSIRO Pub- Belidae Schönherr 1826, The primitive lishing, Melbourne, Australia weevils Lawrence JF, Newton AF Jr (1995) Families and subfamilies Attelabidae Billberg 1820, The tooth-nosed of Coleoptera (with selected genera, notes, ­references snout beetles and data on family-group names). In: Pakaluk J, Slip- inski SA (eds) Biology, phylogeny, and classification of Brentidae Billberg 1820, The straight- Coleoptera: papers celebrating the 80th birthday of snouted weevils Roy A. Crowson. Muzeum i Institut Zoologii, Polska Caridae Thompson 1992 ­Academia Nauk, Warsaw, Poland, pp 779–1006 Ithyceridae Schönherr 1823, The New York weevils Curculionidae Latreille 1802, The snout Behavior of Insects: Genetic ­beetles and true weevils Analysis by Crossing and  Bark Beetles Selection  Bess Beetles  Blister Beetles marjorie a. hoy  Darkling Beetles University of Florida, Gainesville, FL, USA  Fireflies  Ground Beetles Sometimes, as will be demonstrated in examples  June Beetles below, mutations in a single gene or a few major 448 B Behavior of Insects: Genetic Analysis by Crossing and Selection

genes will alter the behavior of insects. The genetic behavior. The behavior of their progeny (the 1F basis of this behavior can be assessed by tradi- generation) and the progeny produced by crosses

tional techniques. Traditional behavior-genetic between the F1 progeny and one of the original analysis primarily employs one of two experimen- parental types (backcross progeny) is also ­evaluated. tal appro-aches: crossing and selection. A third Ideally, the environment experienced by the paren-

­traditional approach, which is limited to D. mela- tal, F1 and backcross generations is controlled so nogaster, involves analysis of fate maps in genetic that all individuals experience the same conditions. mosaics. This method allows the researcher to It is easiest to interpret the results of crossing locate the ­anatomical site of abnormalities that experiments if the individual insects that are affect ­behavior in D. melanogaster. In addition, crossed differ only with regard to a single behav- molecular genetic methods are becoming impor- ioral attribute. tant in the analysis of insect behavior, but are dis- cussed in a separate entry. Although a specific behavior sometimes can Selection Experiments be altered by the mutation of a single gene in a pathway leading to the behavior, an insect’s behav- Selection experiments provide a second tradi- ior often is influenced by many genes. In such tional method to determine the degree to which a situations, analyses of behavior have traditionally given behavior is determined genetically. Selec- required the use of a statistically based approach tion experiments do not usually allow the called quantitative genetics. researcher to resolve the mode of inheritance. In a selection experiment, individuals with a specific behavioral attribute are allowed to reproduce and Crossing Experiments this process is repeated over succeeding genera- tions until a plateau in the selection response is Crossing experiments are used to assess the mode obtained. The behavior of the selected population of inheritance of a particular behavior. The behavior is altered if genetic variation for the attribute is

(phenotype) of the F1 and backcross progeny present in the initial colony and the selection pro- indicates whether the behavior under study is cedures have been appropriate. The response of determined by a single gene or more than one the population to selection can be ­analyzed to gene. The phenotype indicates whether there is estimate whether the trait is heritable. An example dominance (a single copy of the gene is sufficient of a selection experiment is provided by the anal- to determine the behavior under study), sex link- ysis of migratory behavior in the milkweed bug age (the gene is located on a sex-determining Oncopeltus fasciatus. chromosome) or maternal influences (the behav- Migratory and nonmigratory behaviors of ior is determined by the behavior of the mother, Oncopeltus fasciatus were shown to be under which suggests that the trait may be determined genetic control. Strains of O. fasciatus were selected by factors in the cytoplasm rather than in the for two attributes: wing length and propensity to chromosomes located in the nucleus). If the trait is fly. Bidirectional selection (selection for increased determined by many genes, it is difficult to deter- or decreased wing length) on wing length was mine the number of genes, their relationship to ­performed for 13 generations and the flight behav- each other, or their location on specific chromo- ior of the selected individuals was monitored. somes because most insect species lack sufficient Individuals also were selected for flight duration; genetic markers. those whose flight times totaled 30 min were A crossing experiment involves mating ­considered “fliers,” while those with the shortest ­individual insects that differ in a particular kind of flight times were labeled “nonfliers.” Behavior of Insects: Genetic Analysis by Crossing and Selection B 449 Response to selection on wing length was nonhygienic, indicating that the gene, or genes, rapid, and flight tests of the long- and short- conferring the hygienic behavior are recessive. winged insects indicated there was a positive Progeny produced by backcrosses to the correlation between wing length and flight dura- pure hygienic strain yielded approximately 25% tion. Selection after two generations for flight or hygienic worker progeny, which is consistent with noflight likewise resulted in divergent responses, the hypothesis that hygienic behavior is ­determined indicating a large genetic component to flight by two recessive genes. Under this two-gene model, behavior. hygienic worker bees have two copies of each of two genes, called u and r. Hygienic bees (uurr) both uncap the cells (uu) containing dead brood Behavior Determined by One or a and remove them (rr). Few Genes As expected, worker bees that contain two copies of u but only one copy of the gene for removal (r) will uncap the cells, but not remove How often are insect behaviors determined by one dead brood. The workers that contain only one or a few genes? How often are behaviors­determined copy of the uncapping gene (u) but two copies of by many genes? The following examples provide the removal gene (rr) do not uncap brood, but some examples of behaviors determined by one or will remove them if the cells are uncapped for a very few genes. them. Workers that contain only one copy each of u and r (u+u, r+r) are unhygienic, and will nei- ther uncap nor remove brood. Rothenbuhler’ s Susceptibility to American Foulbrood in research on hygienic behavior became a classic the Honeybee in textbooks of behavior genetics because it was one of the first examples to demonstrate that The genetic basis of susceptibility to foulbrood behavior was inherited. The model has been con- disease caused by the bacterium Bacillus larvae in firmed, although one analysis of the data suggest honeybees (Apis mellifera) originally was analyzed that three genes might be involved in this by Walter Rothenbuhler. Differences in resistance behavior. in different bee strains were attributed to differ- Research on hygienic behavior indicates it ences in “hygienic behavior” in worker (sterile may be a general response to remove pathogens female) bees. To understand the genetic basis of and parasites from the nest. It is clear that the the hygienic behavior, two inbred honeybee strains expression of hygienic behavior also depends on with differing levels of resistance were crossed and colony strength and composition of worker types the behavior of the F1 and backcross progeny was within the colony. Analyses of the olfactory characterized. This research was one of the first to responses of hygienic and non-hygienic bees to show that a specific behavior was determined by a diseased brood indicates that hygienic bees have a few genes. higher sensitivity to low concentrations of the “Hygienic” workers consistently remove dead odor of diseased bee pupae. Such differences are larvae and pupae from the brood nest at a high due to a lower stimulus threshold and not a direct rate, thus slowing the spread of the bacteria result of age or experience of the bee, suggesting through the colony by reducing contamination. that non-hygienic bees may be unable to detect The hygienic behavior has two components: (i) the diseased brood readily. uncapping of infected cells, and (ii) removal of the Understanding hygienic behavior in A. mel- dead bee larvae. Crosses between “hygienic” and lifera has great practical importance in maintain-

“nonhygienic” bees yield F1 worker bees that are ing ­effective colonies of pollinators and honey 450 B Behavior of Insects: Genetic Analysis by Crossing and Selection producers. Studies on hygienic behavior has Domesticity in A. aegypti is a complex phe- resulted in practical recommendations to bee nomenon that includes a variety of behaviors, keepers for selecting colonies resistant to chalk including a preference for ovipositing in man- brood (a fungal ­disease) and the pest bee mite made containers, ability of larvae to develop in Varroa. So far, no negative effects have been asso- drinking water stored in clay pots with a low nutri- ciated with hygienic behavior and such colonies tional content, and preferences for feeding on man produce as much honey as nonhygienic ones. (rather than birds) inside houses, as well as resting and mating indoors. No doubt A. aegypti speciated long before man began to build houses, but A. House-Entering Behavior in Aedes aegypti has adapted rapidly to human habitats, and aegypti the domestic form of A. aegypti is the only one known that is entirely dependent on man. The mosquito Aedes aegypti is an important vector of human disease and understanding its behavior could result in better management of Foraging in Drosophila this pest. House-entering behavior by A. aegypti from East Africa has been analyzed by crossing Drosophila melanogaster larvae feed on yeast grow- different populations that exhibited different ing on fruit. Naturally occurring populations con- behaviors, which were controlled by genes with tain individuals that vary in the distance the larvae additive effects. One population of A. aegypti travel while foraging for food, a difference attrib- commonly enters houses (domesticated or D), uted to a single gene called foraging. Natural popu- while others rarely do so (one is called perido- lations comprise approximately 70% “rovers” (who mestic [P]; and the other is a wild or feral [F]; forage long distances) and 30% “sitters” (short dis- population). tance foragers). The rover behavior is dominant to Three populations ofA. aegypti were collected sitter, indicating a single-gene mode of inheritance. either inside houses (D), near a village (P), or from Sitter larvae grow at a normal rate and are of nor- tree holes in a forest (F). The populations then mal size. Both sitters and rovers are maintained in were bred in insectaries and crossed to produce the field by natural selection. It appears that density- hybrid (DP, PD, DF, FD, PF, FP) populations. The dependent selection can shift gene frequencies so original and hybrid populations were then marked that rovers are selected for in crowded larval envi- with different colored fluorescent powders and ronments and sitters in less crowded ones. released near houses. Marked mosquitoes were The foraging gene codes for a cyclic guanos- captured inside houses and in the village area. Of ine monophosphate (cGMP)-dependent protein the mosquitoes entering houses, 45% were from kinase, and rovers have higher kinase activity than the domestic (D) population, 14% from hybrids sitters. Thus, subtle differences in this kinase can between the domestic and peridomestic popula- lead to naturally occurring variation in behavior. tion (DP and PD), 10% from the peridomestic Another gene, Chaser, also may affect larval population (P), and 6% were hybrids between the ­foraging by increasing foraging path length. domestic and feral populations (DF and FD). Only 1.5 and 0.6% of the PF and FP hybrids were ­collected in the house, and the feral population (F) Other Behaviors Influenced by One or a entered the house with a frequency of only 0.6%. Few Genes The recapture rates in the village area were in the reverse order. These results clearly indicate that Crossing experiments have shown that a specific the behavior is genetically determined. behavior is influenced by one or a few genes in the Behavior of Insects: Genetic Analysis by Crossing and Selection B 451 flour moth Ephestia kuhniella (silk mat spinning Alterations in the brain affect behavior and by larvae prior to pupation), the mosquito Aedes genes involved in the behavior can be analyzed by atropalpus (egg maturation without an exogenous mutagenesis and mosaic analysis. For example, source of protein such as blood), and the parasi- eight different genes affecting walking behavior in toid wasp Habrobracon juglandis (flightlessness). Drosophila melanogaster strains were analyzed by In the silkworm Bombyx mori, females with the chemical mutagenesis, histological analysis, and piled egg gene deposit eggs in a peculiar manner. analysis of genetically mosaic flies. These eight B. mori larvae with the Non-preference gene are genes caused structural defects in the central com- unable to discriminate mulberry leaves from ­others. plex of the brain and affected walking motivation, When two tephritid fly species (Procecidochares) fast response to light, and response to gravity. were crossed that differ in their host preference Because the aberrant behaviors were associated (each having only one host plant), the behavior of with changes in a portion of the insect brain called their progeny segregated in a manner consistent the central complex, the mutant flies confirmed with hypothesis that the control of host preference that the central complex controls behavior. The is determined by a single gene. central complex also regulates other behaviors A variety of mutants determined by major (flight, singing, preening, escape). genes have been identified inD. melanogaster that Pheromone communication in the European affect behavior, including Shaker, Hyperkinetic corn borer Ostrinia nubilalis is genetically determined. and eag, which are expressed when the flies are Females of the E- and Z-strains of O. nubilalis pro- anesthetized with ether. Hyperkinetic (Hk) causes duce different ratios of enantiomeric (molecules a vigorous steady leg shaking, and mutations of that are chemically the same but mirror images of Shaker cause vigorous and erratic shaking and a each other) molecules of their sex pheromone strong scissoring of wings and twitching of the (a substance released by an organism that causes a abdomen. The eag mutant flies ether( a-go-go) reaction by another individual of the same species, are less vigorous in their shaking. The easily in this case it serves as a sexual attractant). Hybrids shocked gene of D. melanogaster is one of the between these two strains produce an intermedi- class of “bang-sensitive” paralytic genes. Flies ate ­pheromone blend. Analysis of the F2 and back- with this mutated gene exhibit a transient cross ­progeny indicated the types of pheromones ­paralysis following a brief mechanical shock. A produced are controlled by a single gene, although ­temperature-sensitive recessive mutant gene one or more modifier genes controls the precise ­( parats) causes D. melanogaster to become ratio of the isomers in hybrid females. immobile above 29°C. The couch potato locus Males of the two O. nubilalis strains are causes flies to be less active and exhibit abnor- attracted to the appropriate pheromone blends in mal responses to gravity and light, resulting in the field, but hybrid males respond preferentially altered flight behavior. The couch potato gene is to the ­pheromone produced by hybrid females unusually complex, spanning more than 100 kb rather than to the pheromones produced by the and encoding three different messenger RNAs. two parental female types. The response of males Many “single gene” mutants that affect the mor- to the pheromone is determined by a single phology of D. melanogaster also affect behavior. ­sex-linked gene. The olfactory sensillae of the two Some mutant flies exhibit abnormal behavior types of males are ­different, which is controlled by because they are unable to perform the reaction to a an autosomal gene. Hybrid males give inter­mediate stimulus due to altered morphology. Other mutants results when their antennae tested for their elec- exhibit altered behavior because perception of cues trophysiological responses, with E- and Z- olfac- is impaired. For example, flies with white eyes may tory cells yielding approximately equal responses, exhibit abnormal courtship behaviors. ­suggesting that ­multiple genes are involved. The 452 B Behavior of Insects: Genetic Analysis by Crossing and Selection genes determining variation in pheromone Morinda. The two species can be crossed and F1 ­production and organization of male olfactory hybrids are produced. The number of genes sensillae are not closely linked and are probably involved in resistance was estimated to be three to on different chromosome. five based on a biometric approach. An analysis using marker genes suggests that all chromosomes, except the Y and the small fourth, carry genes Behaviors Determined by Multiple affecting resistance. Thus, resistance appears to be Genes neither very simple nor highly polygenic. D. sechellia is stimulated by Morinda to Behavior is often controlled by multiple genes with ­produce eggs, but oviposition in D. simulans is small additive effects. With such behaviors, the inhibited by this plant. In hybrid progeny, the

task of teasing apart the respective roles of genes ­inhibition observed in D. simulans is dominant. F1 and environment requires statistical methods of hybrids and backcross progeny exhibit intermediate, analysis. Drosophila behaviors determined by mul- approximately additive, behavior. These­differences tiple genes include locomotor activity, ­chemotaxis result in isolation of the two species in nature, (response to chemicals), duration of copulation, although they overlap geographically. Thus, their geotaxis ­(orientation to gravity), host plant prefer- ecological niches are determined by tolerance to ence, mating speed, phototaxis (response to light), toxic products (including octanoic and hexanoic preening, and the level of sexual isolation within acids) in the ripe Morinda fruit, with D. sechellia and between ­species. Multiple genes may influ- exhibiting a strong preference for Morinda fruits, ence host plant adaptation and host preference in an ability to detect fragrant volatiles from Morinda insects. Learning may affect host preference. Host over a long distance, and a stimulation of egg pro- plant choice usually is a hierarchy of several duction by Morinda. By contrast, egg production components. in D. simulans is inhibited by Morinda and octanoic A particularly interesting example of genetic acid in the fruit is toxic to D. simulans. analysis of host preference in insects is that of ­Drosophila sechellia, which is endemic to the ­Seychelles archipelago in the Indian Ocean and is Other Behaviors Determined by morphologically almost identical to its cosmopol- Multiple Genes itan sister species D. simulans and to the endemic island species D. mauritiana. When crossed to Other insects in which specific behavioral either of these species, D. sechellia produces fertile ­attributes have been shown to be complex hybrid females and sterile hybrid males. D. sechellia include: Musca domestica (number of attempts uses the fruit of Morinda citrifolia as its host, which to mate by males); Phormia regina (high and low may have allowed it to escape competition with ability to learn to extend the proboscis to a other species of Drosophila there. ­stimulus applied to the forelegs); hybrid crickets (call rhythm of males; female response to calling songs); Anopheles albimanus (ability to avoid Host Plant Specialization in Drosophila pesticides); Apis ­mellifera (high and low collec- sechellia tion of alfalfa pollen, and stinging behavior). The propensity for ­cannibalism by larvae of Heliothis Drosophila sechellia breeds only in Morinda virescens is determined by multiple genes. Most ­citrifolia, which is toxic to other Drosophila ­species. of these behaviors were analyzed by selection D. simulans breeds on a variety of plants in the experiments. same geographic area but cannot survive on  Behavior of Insects: Molecular Methods Behavior: Molecular Genetic Analyses B 453 References available, it is easier to isolate specific genes that could be involved in behavior. In addition, Arathi HS, Burns I, Spivak M (2000) Ethology of hygienic the genetic modification of D. melanogaster by behavior in the honey bee Apis mellifera L. ­P-element mediated transformation makes it (Hymenoptera: Apidae): behavioral repertoire of possible to insert genes from one species of hygienic bees. Ethology 106:365–379 de Belle JS, Sokolowski MB (1987) Heredity of rover/sitter: ­Drosophila into the genome of another, and alternative foraging strategies of Drosophila melano- their effect(s) on behavior can be determined. gaster larvae. Heredity 59:73–83 Transgenic D. melanogaster carrying markers Osborne KA, Robichon A, Burgess E, Butland S, Shaw RA, such as green fluorescent protein (GFP) also Coulthard A, Pereira HS, Greenspan RJ, Sokolowski MB (1997) Natural behavior polymorphism due to a cGMP- allow scientists to determine when and where dependent protein kinase of Drosophila. Science specific genes are active. 277:834–836 Molecular genetic analyses of learning and Palmer JO, Dingle H (1989) Responses to selection on flight behavior in a migratory population of milkweed bug memory in Drosophila may provide a means to (Oncopeltus fasciatus). Evolution 43:1805–1808 study one of the most challenging frontiers in Kha R, Capy SP, David JR (1991) Host-plant specialization ­neurobiology. Molecular genetic methods in the Drosophila melanogaster species complex: a may identify some of the individual genes ­physiological, behavioral, and genetical analysis. Proc Natl Acad Sci USA 88:1835–1839 among the “many” involved in determining the Rothenbuhler WC (1964) Behavior genetics of nest cleaning interesting and complex behaviors exhibited

in honey bees. IV. Responses of F1 and backcross gen- by insects. erations to disease-killed brood. Amer Zool 4:111–123 Analyses of insect behavior employ tech- Trpis M, Hausermann W (1978) Genetics of house-entering behavior in East African populations of Aedes aegypti niques from several disciplines, including anatomy, (L.) (Diptera: Culicidae) and its relevance to speciation. ­biochemistry, ecology, ethology (study of animal Bull Entomol Res 68:521–532. behavior in the natural environment), genetics, psychology, physiology and statistics. These Behavior: Molecular Genetic ­disciplines are required because an insect per- Analyses ceives the environment through its sensory ­systems. The external sensory stimuli are trans- duced into ­electrical information, which is then marjorie a. hoy processed and decoded, leading to a behavioral University of Florida, Gainesville, FL, USA response. ­Behavior can be divided into several sequential steps: stimulus recognition, signal Molecular genetic techniques are beginning to transduction, integration, and response or motor provide powerful new methods to analyze insect outputs. behaviors such as olfaction (response to odors), learning, circadian rhythms (daily periodicity), and mating behavior. Prior to the use of molecular The Insect Nervous System methods, genetic analyses of behavior primarily involved crossing and selection experiments to Behavior is based on the structure and function of resolve whether the behavior was genetically the insect central and peripheral nervous systems. determined and the mode of inheritance of the The insect brain contains around 105–106 ­neurons. gene(s) involved (e.g., the genes were dominant or It consists of three main divisions, the protocere- recessive, sex-linked or autosomal, determined by brum, deutocerebrum and tritocerebrum. In each single genes or more than one). of these divisions, different neuropil regions are Now that the complete sequence of the located; a neuropil is a dense network of inter­ genome of the fruitfly Drosophila melanogaster is woven axons and dendrites of neurons and 454 B Behavior: Molecular Genetic Analyses ­neuroglial cells in the central nervous system and genes for many of these neuropeptides have been parts of the peripheral nervous system. identified, cloned and sequenced. In the protocerebrum, higher sensory centers Neuropeptides are released as cotransmitters are present that are associated with vision and and modulate fast transmission at neuromuscular other sensory receptors (the mushroom bodies junctions. A given neuropeptide may occur at and central complex). The superior protocere- ­several different sites, including central nervous brum, with the pars intercerebralis, contains system circuits and peripheral synapses, and at ­different sets of neurosecretory cells that supply peripheral targets (muscles and glands). Neuropep- neurohemal organs in the corpora cardiaca and tides regulate behavior by coordinating temporal corpora allata, which are located in the head or and spatial activity of many neuronal circuits. Each prothorax in insects. The optic lobes flanking the of the circuits controlling behavior employs sets of protocerebrum consist of the most well-organized sensory neurons, interneurons and motor neurons. neuropils in the brain. Thus, multiple neural networks share neural ele- Mushroom bodies in the brain are associated ments. Molecular genetic analysis is ­providing rapid with olfactory pathways, including olfactory progress in understanding ­neuropeptide receptors ­learning. Among the insects, mushroom bodies and second messenger pathways. Research on neu- differ greatly in size and shape, with the number of ropeptides and their receptors indicates that they cells ranging from 2,500 in Drosophila to 50,000 in have roles during embryonic development and as the cricket Acheta, 170,000 in the honey bee and cytokines in the immune systems of insects. 200,000 in the cockroach Periplaneta Molecular genetic analyses are providing The antennal centers are found in the deuto- ­significant advances in our knowledge of behavior. cerebrum; in the tritocerebrum, neurosecretory “Behavior” is a complex phenotype to study neurons and neurons associated with the control because it involves the functioning of the whole of feeding and foregut activity are found. The brain organism, is dynamic, and changes in response to is connected to the subesophageal ganglion via the environment. Molecular genetic methods are connectives and to the thoracic and abdominal unlikely to replace traditional methods of behavior ganglia, or ventral nerve cord. analysis, but the ability to identify, clone, and Information is transmitted in the insect via sequence specific genes in D. melanogaster makes nerves and by neuropeptides that coordinate the it possible to understand several behaviors development and behavior of insects. Both neu- ­(including the periodicity of biological rhythms, rosecretory cells and neurons use neuropeptides mating behavior, locomotion, and learning) that as messengers. Many different types of neuropep- are influenced by single genes. tides have been identified, including proctolin It is now possible to clone a gene from one and ­adipokinetic hormone, that serve as both hor- Drosophila species, insert it into a P-element ­vector, mones and neurotransmitters or neuromodulators. and introduce the exogenous gene into mutant Neuropeptides range in size from three amino acid strains of D. melanogaster to confirm that the residues (thyrotropin-releasing hormone) to more ­putative gene does, in fact, code for the behavior of than 50 (insulin). They are generated from larger interest. Cloned genes from Drosophila can, in precursor proteins, ranging from 90 to 250 amino some cases, be used as probes to identify genes acids in length. A number of genes have been from other arthropods, which then can be sequenced ­identified that code for neuropeptides, including and compared. The availability of the complete bombyxin or ­prothoracicotropic hormone (PTTH), genome of D. melanogaster allows analyses of eclosion hormone (EH), FMRFamide- related behavior that could not be conducted previously, peptides, diapause hormone and pheromone as will be described in the discussion of olfaction ­iosynthesis-activating neuropeptide (PBAN). The in D. melanogaster (see below). Behavior: Molecular Genetic Analyses B 455 The Photoperiodic Clock mammals, and cyanobacteria. In Drosophila, the genes called period, timeless, Clock, cycle, double- The potential that molecular genetics offers is time and cryptochrome are now known to be exemplified by the analyses conducted using the involved in the circadian clock. period, and other clock genes, of D. melanogaster. Most insects exhibit particular behaviors at a ­specific time of the day, which due to the action of The Period (Per) Gene of Drosophila a circadian (approximately 24 h) clock that allows the insect to measure time. Circadian rhythms The period gene of Drosophila is located on the X have a number of characteristics: (i) The clocks chromosome. When the wild type gene (called that regulate such behavior usually are free ­running per+) is mutated, eclosion (emergence of adults in constant environments and are not simple from the pupa), locomotor activity and the length responses to changes in light or temperature. of the interpulse interval of the courtship song are (ii) Although the rhythms are free running, an affected. Eclosion of wild type flies typically occurs ­initial environmental signal is required to start around dawn, when the presence of dew and high the clock. Among the cues that set the clock relative humidity increase their survival rate. are ­alternating light and dark cycles, high and ­Locomotor activity then decreases during midday low temperature cycles, or short pulses of light. and is followed by increased activity in the evening. (iii) The circadian rhythm is relatively insensitive Three classes of per mutants exist; they either to changes in ­temperature (temperature compen- shorten (per mutants have 19-h eclosion rhythms sated). (iv) The clock can be reset by altering the instead of 24-h patterns), lengthen (perL mutants cues that entrain the clock. have 29-h eclosion rhythms), or completely ­abolish Drosophila melanogaster reared in constant circadian eclosion and locomotor activity rhythms darkness exhibit circadian locomotor activity (per0 mutants). Flies with the per0 mutation eclose rhythms as adults. However, the rhythms of the arrhythmically, but periodicity in eclosion can be individual flies composing these populations are restored by P element-mediated transformation of not synchronized with one another. Rhythms can arrhythmic flies using the wild type per+ allele. by synchronized if dark-reared flies are exposed to Theper gene is approximately 7 kb long and the light treatments as first-instar larvae (or as later protein produced has a series of threonine-glycine instars). Light treatments occurring prior to hatching (Thr-Gly) repeats in the middle of the gene. The of the first-instar larvae fail to synchronize adult region encoding the Thr-Gly repeat is polymorphic locomotor activity rhythms, indicating the clock in length within and between Drosophila species functions continuously from the time larvae hatch and plays a role in the thermal stability of the until adulthood. The rhythm can be advanced, ­circadian phenotype. For example, either 17, 20 or delayed, or unchanged, depending on the phase of 23 repeats are found in D. melanogaster populations. the cycle at which the cue is given. A clinal pattern occurs along a north-south axis in Molecular genetic analyses of Drosophila Europe and North Africa, with the shorter sequences clock mutants is providing a fundamental under- in southern Europe, suggesting that the length standing of the mechanisms of the circadian clock. ­polymorphism cline is maintained by natural Rapid advances have been made in the past few ­selection under different temperature conditions. years in understanding the molecular aspects of A large number of tissues express the normal ­circadian clocks in a variety of organisms. Circadian (per+) product, including embryonic, pupal and rhythms are found in all organisms, probably adult nervous systems, as well as the esophagus, evolved early, and common genetic elements are gut and ovaries. The per+ gene product (the PER present in Drosophila, the fungus Neurospora, protein) is predominantly found in cell nuclei in 456 B Behavior: Molecular Genetic Analyses adult Drosophila, and per+ messenger RNA levels ranges from a period of 56 ms in D. melanogaster undergo daily fluctuations, producing a feedback and 35–40 ms in D. simulans. D. melanogaster males loop in which PER affects the oscillations of its with the perS mutation sing with 40-ms periods, own messenger RNA. The fluctuations in per+ perL males sing with 76-ms periods, and per0 males messenger RNA are due to fluctuations in gene are arrhythmic. transcription because the per+ messenger RNA has The genetic basis of species-specific song a relatively short half-life, which is consistent with instructions was confirmed by the transfer of the the hypothesis that PER acts to regulate its own per+ gene from D. simulans into D. melanogaster gene activity. via P element-mediated transformation. The The per+ genes from Drosophila simulans, D. D. simulans per+ gene restored a rhythm in these virilis, D. pseudoobscura and D. yakuba have been transgenic D. melanogaster and the transgenic cloned and sequenced. Parts of the gene are con- D. melanogaster males had mean period lengths in served among them and parts are highly diverged, their song cycles of approximately 35 ms, which is which suggests that conserved regions may characteristic of D. simulans males. Thus, substitu- encode basic functions common to all ­(clock-type tions in four or fewer amino acids in the per+ locus functions), while the variable regions may affect was shown to be responsible for this species-specific species-specific differences influencing love courtship behavior. songs, locomotor activity and eclosion. Two X-linked loci, Clock and Andante, are components of the circadian clock, causing slightly Other Effects of Per shortened and lengthened cycles, respectively. In addition, other mutations on the autosomal The per alleles affect locomotion, cellular rhythms ­chromosomes induce flies to emerge as adults and development time. Flies with perS develop from the pupal stage early in a light-dark cycle; faster than wild type flies and perL flies develop phase-angle flies emerge in the pre-dawn part of more slowly than the wild type. the cycle instead of just after dawn while gate flies It has long been thought that circadian oscil- to fail to eclose during this narrow time window. lations provided the clock for photoperiodically Thecryptochrome (cry) gene is an important clock induced diapause in insects. Diapause is a geneti- component because it encodes a circadian photo- cally determined state of arrested development receptor in Drosophila. The gene product, CRY, that is induced prior to the onset of detrimental belongs to a family of blue light-sensitive proteins, conditions. Hibernal diapause, which allows which includes photolyases and plant blue light insects to survive over winter, is often induced in photoreceptors. Flies over expressing CRY are insects when insects develop during a period of hypersensitive to light. The CRY protein is­probably cool temperatures under a short daylength, which the only dedicated circadian photoreceptor in means they must be able to measure light and dark Drosophila. cycles. However, per+ appears to have no influence on the photoperiodic clock in D. melanogaster. Females of a wild-type strain of D. melano- Song Cycle Behavior in Drosophila gaster (Canton-S) and strains with per mutations were able to discriminate between diapause-in- The courtship song is produced when males vibrate ducing short days and non-inductive daylengths. their wings and consists of two components: D. melanogaster adult females exhibit an ovarian (i) courtship hums, and (ii) a series of pulses with diapause when reared and held under short days interpulse intervals, which can fluctuate between and low temperature (12°C). Females exposed to 15 and 85 ms. The variation in interpulse intervals long days at the same temperature reproduce. Behavior: Molecular Genetic Analyses B 457 The critical daylength (the photoperiod at which curve” to an asymptote. (iii) The change in behavior 50% of the individuals enter diapause) for Canton-S accompanying experience declines in the absence females at 12°C is approximately 14 h of light of continued experience of the same type or as a per 24 h. Photoperiodic response curves for the consequence of a novel experience or trauma. perS, perL and Canton-S strains were almost Insect populations vary in their ability to identical, although per0 flies showed shortened learn. Genetic variability within strains has been critical daylengths. However, per0 females are used to analyze learning in Drosophila, Phormia able to discriminate between a long day and a flies and the honeybee Apis mellifera. Drosophila short day. melanogaster can be sensitized and habituated, Many behaviors, including learning, involve learn associations with positive or negative rein- temporally patterned events. The interval between forcement, and be classically conditioned. Droso- presentation of the conditioned stimulus and phila melanogaster can learn to run away from ­reinforcement is important in associative learn- specific odors that they previously experienced ing. The conditioned stimulus must be presented with electric shock and hungry flies can learn to before the unconditioned stimulus and the uncon- run toward odors previously associated with a ditioned stimulus must follow the conditioned sugar reward. Flies can learn visual, tactile, spatial within a relatively brief interval. It was thought and proprioceptive cues. Analyses of ­memory that the per+ gene could be involved in learning, mutants in Drosophila, including the genes dunce, based on the observation that perL males in one rutabaga, amnesiac, radish, zucchini, cabbage, experiment did not exhibit normal experience- tetanic, turnip, linotte and latheo, indicate that dependent courtship behavior. However, males memory consists of distinct phases: short-term, with the wild type or perS and per0 alleles could be intermediate, long-term and anesthesia-resistant conditioned normally. memory. Genetic analyses of learning in Drosophila ­melanogaster began in the mid-1970s in Sey- Learning in Drosophila mour Benzer’s laboratory when D. melanogaster was trained to avoid an odor associated with an It is difficult to produce a single definition of electric shock. The learned avoidance lasted ­learning. Learning can be defined as a change in only a few hours, but the odor avoidance test behavior with experience, but this definition would was used to screen mutagenized flies for strains not exclude responses such as growth and matura- that had normal olfaction and aversion to shock, tion, or other processes that are triggered by events but an abnormally-low ability to associate odors such as mating or feeding. Another definition is a with shocks. The mutants obtained were poor reversible change in behavior with experience, but learners but each had different phenotypes. One this excludes phenomena in which the modifica- mutant strain, amnesiac, had a nearly normal tion caused by some experience is fixed and resis- learning ability but forgot rapidly. The dunce tant to further change. Another definition is that flies had a shortened memory for several learning is a more or less permanent change in ­different conditioned behaviors due to a defec- behavior that occurs as a result of practice, but this tive gene for cAMP-specific phosphodiesterase, ­definition is ambiguous. an enzyme that regulates levels of cyclic AMP The following properties are characteristic of (cAMP). The dunce flies have elevated cAMP learning in insects: (i) The individual’s behavior levels; cAMP is part of a second messenger sig- changes in a repeatable way as a consequence of naling pathway in nerve cells that help form experience. (ii) Behavior changes gradually with associative memories. dunce flies have impaired continued experience, often following a “learning synaptic transmission because the excess of 458 B Behavior: Molecular Genetic Analyses cAMP leads to hyper polarization of the synap- neurons, it was found that long-term memory tic terminals, resulting in a chronically ­lowered requires the vertical lobes. Short-term memory was availability of neurotransmitter. normal in flies lacking either vertical lobes or the The dunce gene is one of the largest and most two median lobes. complex identified in Drosophila, extending over Learning probably requires other brain 140 kb. It produces, by the use of multiple tran- ­centers, including the antennal lobes, the central scription start sites and alternative splicing of complex and the lateral protocerebrum in insects. exons and differential processing of 3′ sequences, During metamorphosis, the nervous system of at least eight to ten messenger RNAs ranging in holometabolous insects such as Drosophila changes size from 4.2 to 9.5 kb. One unusually large intron significantly. A controversy has existed as to (noncoding sequence inside the coding region) is whether flies retain learned behavior after 79 kb in length and contains at least two other ­metamorphosis from larvae to adults, but there is genes (Sgs-4 and Pig-1) within it. This genes within no evidence that larval conditioning induces a an intron arrangement is uncommon. One of the change in adult olfactory responses. This is not contained genes, Sgs-4, is expressed in larval salivary surprising because larval sense organs undergo glands and provides the glue used by larvae to histolysis during the pupal stage and adult sense attach themselves to the surface for pupation. organs are formed de novo from imaginal discs. Sgs-4 is transcribed in the same direction as dunce. The mushroom bodies of the fly brain are The second gene, pre-intermolt gene, also is ­extensively rewired during metamorphosis. expressed in larval salivary glands but is ­transcribed Drosophila carrying the mutant turnip have in the opposite direction. Genes homologous to difficulty in olfactory discrimination, conditioning dunce have been identified in mice, rats and of leg position, larval, visual and reward learning. humans. The mammalian counterparts of dunce The turnip gene is located on the X chromosome function in regulating mood. The dunce gene is and is associated with reduced protein kinase expressed in the mushroom bodies in the brain of C activity. Specifically, the turnip mutant is defective D. melanogaster. in phosphorylation of pp76, a membrane protein in Mushroom bodies are important for olfactory head tissues. Protein phosphorylations have been learning and memory. In D. melanogaster these implicated repeatedly in changes underlying ­learning structures are paired and consist of about 2,500 and short term memory. neurons that send dendrites into a neuropil just Additional genes, including radish, amnesiac, ventral to the perikarya where inputs arrive from cabbage, latheo and linotte, are involved in the antennal lobes and other centers of the brain. abnormal learning or memory of D. melanogaster. Mushroom bodies receive olfactory information For example, flies with the X-linked radish from the antennal lobes through their dendrites mutation initially learn in olfactory tests, but located in the calyx, a region of the brain just their subsequent memory decays rapidly at ­ventral to the mushroom body. Mushroom bodies both early and late times after learning. The house part of the short-term memory for odors, radish flies show normal locomotor activity are required for courtship conditioning memory and sensitivity to odor cues and electric-shock and are necessary for context generalization in ­reinforcements used in the learning tests. visual learning, as well as regulating the transition ­Anesthesia-resistant memory, or consolidated from walking to rest. By analyzing a Drosophila memory, is strongly reduced in D. melanogaster strain with alpha-lobes-absent, a mutation which with the radish phenotype. causes flies to lack either the two vertical lobes of The rutabaga gene codes for an adenylyl the mushroom body or two of the three median cyclase, is expressed in Drosophila mushroom lobes which contain branches of the vertical lobe ­bodies, and is involved in olfactory short-term Behavior: Molecular Genetic Analyses B 459 memory. Volado, which codes for an α -integrin that receptor gene is expressed in 20 olfactory neurons, mediates cell ­adhesion and signal transduction, is some receptor genes are expressed in only two to expressed in mushroom body cells of Drosophila three neurons. Seven olfactory receptor genes are and mediates short-term memory in olfactory expressed solely in the maxillary palp. learning. Integrins have diverse biological roles, It is thought that there are fewer than 100 types including cell-cycle ­regulation, cell migration and of odor receptors in insects, and perhaps as few as cell death (apoptosis), functioning as mediators of 50 or 60. By contrast, mammals have more than interactions between cells with the extra cellular 10,000 different receptor types. The approximately matrix or with counter receptors displayed by their 50–60 odorant receptor genes in insects encode a cells. They can also transduce information across novel family of proteins with seven predicted cell membranes bi-directionally membrane-spanning domains; these genes are The enlightenment obtained from the unrelated to vertebrate or nematode chemosensory study of these Drosophila learning mutants is receptors, suggesting the genes evolved in an providing an understanding of learning in independent manner throughout evolution. Fur- higher organisms. thermore, the Drosophila genes are poorly grouped into subfamilies of similar sequences because they are only 17–30% similar to each other. Functional Genomics of Odor Behavior in Drosophila Learning in Apis mellifera The ability to respond to odors is essential for ­survival and reproduction, allowing insects to Mushroom bodies in the Hymenoptera are much select mates, find and choose food, and locate larger than those in Drosophila, which may reflect appropriate oviposition sites. A beginning has been the importance of the mushroom bodies for made in understanding the complex genetic basis ­functions underlying social behavior, learning and of odor behavior in insects using D. melanogaster memory in the honey bee. Many Hymenoptera as a model system. (ants, bees, wasps) have complex behaviors that Odors are received by olfactory receptors include caring for their brood either as individual located on the third antennal segments and the females or as a social group of females. Bee species maxillary palps, which send their axons to the such as Apis mellifera feed, protect and nurse antennal lobes in insect brains. Each third antennal ­larvae, store food and respond to adverse environ- segment in D. melanogaster contains about 1,300 mental factors. They search for nectar and pollen olfactory receptor cells and each maxillary palp at unpredictable sites, learn the celestial and carries 120 chemosensory neurons. These ­terrestrial cues that guide their foraging trips over neurons project to 43 glomeruli in the antennal long distances and allow them to find their nest lobe of the brain. From there, processed olfactory sites once again. They learn how to respond to the information is relayed to higher-order brain changing position of the sun, to a pattern of ­centers (the mushroom body and the lateral horn ­polarized light during the day, and to landmarks. of the protocerebrum). Associative learning is an essential component to D. melanogaster has approximately 1,300 foraging behavior and dance communication. olfactory receptor neurons and D. melanogaster is Hive mates attending a dance performance learn able to recognize and discriminate between a large the odor the dancing bee carries and seek out that number of odorants. Each olfactory sensory neuron same odor when they forage for food. responds to several odorants, but respond maxi- The complexity of bee behavior makes it an mally to only one. While the average olfactory ideal organism to analyze to better understand 460 B Behavior: Molecular Genetic Analyses learning, especially in response to odors. Associa- binding proteins) are small, soluble proteins that tive olfactory learning in honey bees has several are concentrated in the sensillum lymph. features similar to higher forms of learning in Genes and complementary DNAs encoding vertebrates. odorant binding proteins of many insects have been cloned. Analysis indicates that the binding proteins of unrelated species have low levels of Pheromones in Insects amino acid sequence similarity, although they do have a conserved region with cysteines that may Insects use chemical cues as signals to find mates, be important for function. It appears that there food, oviposition and hibernation sites. Molecular has been gene duplication and divergence of odor- genetic methods are now being used to study vari- ant binding protein genes, with moth proteins ous aspects of pheromone response behavior. For belonging to one branch and the proteins of other example, genes that code for proteins involved in insects not closely related. the synthesis of pheromones, the perception of The molecular receptors in an olfactory semiochemicals, and the processing of the signals ­system involve G-protein-coupled seven trans- are being cloned and characterized. membrane proteins. Such proteins also are found Pheromone biosynthesis appears to use one or in the mouse and rat, where the number of such a few enzymes that convert the products of ­ normal genes number approximately 1,000 or nearly 1% primary metabolism into compounds that act as of the genome, indicating that odor reception is pheromones. For example, pheromones arise from an important component of the mammalian isoprenoid biosynthesis, or by the transformation genome. Sequencing the Drosophila genome has of amino acids or fatty acids. A number of the genes allowed receptor similar proteins to be identified encoding the enzymes involved in transforming in an insect. The receptors are in large multigene metabolites into pheromones have been cloned ­families and expressed at different times during and sequenced. The production of pheromones by antennal development. The receptor genes were insects is regulated by three hormonal messengers: found by searching the Drosophila genome to juvenile hormone III, ecdysteroids, and a neuro- identify sequences that might encode transmem- peptide called PBAN (pheromone biosynthesis brane domains. activating neuropeptide). Once an odor or pheromone has activated the Perception of the volatile pheromone is olfactory receptors, it needs to be deactivated. ­mediated by olfactory organs (sensillae) located Several enzymes have been found that appear to primarily on the antennae. Receptor neurons on degrade odor stimulants, including esterases, the antennae appear to respond to one particular ­oxidases, and glutathion transferases. Multielec- chemical (specialist neurons) while others appear trode recording of the Manduca sexta antennal to respond to a number of compounds (generalist lobe indicates that the relative timing of action neurons). Pheromones are often perceived in potentials may convey information about odor ­combination with other chemicals, including plant concentration and mixture. A large and diverse volatiles. family of genes coding for taste receptors have The detection of pheromones and other been identified inDrosophila that are expressed in chemicals by insects involves proteins (odorant the proboscis. binding proteins, OBPs) that carry the compounds Rapid advances in understanding olfaction from the surface of the antennal sensilla through and gustation in insects, especially based on the sensillum lymph to the G-protein-coupled ­molecular genetic analyses of D. melanogaster, receptors and the olfactory neurons. The odorant promise to advance our understanding of how binding proteins (which includes pheromone insects perceive chemical cues in their environment. Behavior: Molecular Genetic Analyses B 461 Unfortunately, early evidence suggests an extreme of behavior. Est-6 was used to isolate a homolo- divergence of receptors within D. melanogaster gous gene (Est-5) from D. pseudoobscura. Sur- that make it difficult to use homology to isolate prisingly, Est-5 has a different function in D. odor receptor genes from other insects. pseudoobscura. Approximately 40% of Est-5 is expressed in the eyes of D. pseudoobscura, with the remainder expressed in the hemolymph of Divergent Functions of Est-6 and both sexes. Despite these different patterns of Est-5 in Drosophila Species expression, Est-6 and Est-5 have similar protein products, messenger RNA transcripts, and DNA Evolutionary changes in gene regulation can be a sequences. prerequisite for macro evolutionary change and When Est-5 from D. pseudoobscura was species divergence. One case study involves an cloned into a P element and introduced into D. analysis of the esterase 6 enzyme in Drosophila melanogaster, its activity and pattern of ­expression melanogaster and its homologue (esterase 5) in D. in D. melanogaster matched those of D. pseudoob- pseudoobscura. This gene influences behavior in scura. These results imply that regulatory sequences D. melanogaster but has a very different function in Est-5 have been conserved since the divergence in D. pseudoobscura. of the two species 20–46 million years ago, sug- Esterase-6 (Est-6) in D. melanogaster influences gesting that the enzyme in the ­common ancestor male mating speed and rate of remating by females. of these two species had a more extensive expres- Fast and slow variants of esterase 6 protein, as sion pattern. After the species diverged, regulatory detected by electrophoresis, are produced in natural mutations may have occurred that enhanced Est-5 populations of D. melanogaster. More esterase expression in the eyes of D. pseudoobscura, while 6 ­protein is produced in adult males than in females. mutations in Est-6 led to increased expression in The enzyme is highly concentrated in the anterior the male ejaculatory duct of D. melanogaster. Thus, ejaculatory duct of males and is transferred to the use of homology to identify behavioral (and females during the first 2–3 min of the 20min other) genes can lead to surprises. ­copulation. Enzyme activity in females can be detected up to 2 h after mating and influences the timing of remating by females. Males transfer a Courtship Behavior in Drosophila ­substance in the seminal fluid which is converted in the females’ reproductive tract by esterase 6 into a Mating behavior of D. melanogaster is stereotypi- pheromone that serves as an antiaphrodiasiac. The cal, with a fixed sequence of actions that are under antiaphrodiasiac reduces the sexual attractiveness genetic control. Courtship involves visual stimuli, and receptivity of females, reducing the likelihood acoustic signals, and pheromones. Male courtship she will remate. Because the sperm from the most behavior involves six elements in the following recent male takes precedence in fertilizing a female’s fixed order: orienting® following ® wing vibra- eggs, this behavior appears to encourage monogamy tion ® licking ® attempting to copulate ® in D. melanogaster females. Est-6 also influences the copulation. rate of mating of males in D. melanogaster. Males Sexual differentiation in Drosophila is with the slow variant of the protein require 10.2 min ­controlled by a short cascade of regulatory genes, to achieve copulation with females, while males with the expression of which determines all aspects of the faster-moving protein require only 5.7 min. maleness and femaleness in the body and the cen- Once the Est-6 gene was cloned, it was used tral nervous system, including complex behaviors. as a probe to identify homologous genes in related Such sexual behavior is irreversibly programmed species, which can provide clues to the evolution during a ­critical period as a result of the activity or 462 B Behavior: Molecular Genetic Analyses inactivity of the major control gene tra+. Male the courting male a chance to lick the female’s behavior is replaced by female behavior when tra+ ­genitalia ® allowing males to attempt copulation. is expressed around the time of puparium Nonreceptive females leave the courting male, and formation. if the male pursues her, she may kick him. Non- Other genes indirectly affect courtship behav- receptive virgin females persistently repel male ior in Drosophila, including genes that involve: approaches by lifting their abdomens up to block general behavior (yellow, inactive, couch potato, physically any contacts with males. Nonreceptive cuckold, minibrain, nerd); visual behavior (white, fertilized females lower their abdomen, extrude optomotor-blind, no-receptor-potential-A); olfaction their ovipositors and eggs to repel males. Thus, (smellblind); learning/memory genes (dunce, female receptivity varies with age, diet, hormonal rutabaga, amnesiac, Shaker, ether-a-go-go); regu- condition and mating experience. The spinster lating periodicity of behavior (period), courtship mutation affects female sexual receptivity through- song mutants (cacophony, dissonance, croaker, out their lives, and spinster females continuously fruitless); female receptivity (spinster). leave, kick, or fend off courting males. Thefruitless mutation is involved in both sex Both D. melanogaster and D. simulans females determination and courtship behavior and is produce contact pheromones, which consist of active in the central nervous system. Males with cuticular hydrocarbons that elicit wing displays by the fruitless mutation may court both females males. These chemical signals have a low volatility, and males without copulating. Male flies express- and thus act at a very short distance (a few mm) ing this gene are unable to bend their abdomens and thus are perceived by contact rather than in the presence of females they are courting smell. Flies from a given strain, sex, and age because they lack a male-specific Muscle of Law- ­produce a reproducible pattern of cuticular rence. Some fruitless mutations cause males to be ­hydrocarbons, the biochemical pathway of which homosexual (they do not court females), while is under genetic control. The most important others cause males to be bisexual (they court ­hydrocarbons involved in mate recognition or both males and females). Thefruitless + gene is the stimulation are 7-tricosene and 7-pentacosene. first gene in a branch of the sex-determination One mutation, Ngbo, influences the ratios of 7-tri- hierarchy functioning specifically in the central cosene and 7-pentacosene in D. simulans. Another, nervous system, with mutants of this gene affect- kete, reduces the amount of 7-tricosene and all ing nearly all aspects of male sexual behavior. It is other linear hydrocarbons but does not affect the at least 140 kb long and produces a complex array ratio. Flies homozygous for both kete and Ngbo of transcripts by using four promoters and alter- have reduced viability and fertility, perhaps native splicing; the male-specific transcripts are because they have very little 7-tricosene. only expressed in a small fraction of the central Experiments were conducted to eliminate all nervous system. known cuticular hydrocarbons in D. melanogaster Another mutation, dissatisfaction, is necessary in order to determine how mating behavior would for some aspects of sex-specific courtship behavior be modified. The results were surprising; contrary and neural differentiation in flies of both sexes. to expectation that D. melanogaster females ­lacking Mutant males are bisexual but, unlike fruitless males, cuticular pheromones would induce no courtship attempt to copulate. Males with the dissatisfaction by males, such females remained attractive. phenotype take longer to copulate with females Additional analysis indicated that undetermined while females are unreceptive to male advances pheromone(s), probably also cuticular hydrocarbons, during courtship and do not lay mature eggs. were present on both control and transgenic flies. Mating behavior of females involves the These newly discovered pheromones could represent ­following sequence: stopping moving ® offering ancestral attractive substances in D. melanogaster Behavior: Molecular Genetic Analyses B 463 and its sibling species. An absence of inhibitory A recessive mutant (bubblegum) in D. mela- pheromones leads to high levels of interspecific nogaster exhibits adult neurodegeneration similar mating among Drosophila species, suggesting that to that seen in the human disease adrenoleu- cuticular hydrocarbons are important in main- kodystrophy (ALD), otherwise known as the dis- taining reproductive isolation. ease cured in the movie “Lorenzo’s Oil”;. In ALD, high levels of very long chain fatty acids are pro- duced that can be lowered by dietary treatment Studies of Human with a mixture of unsaturated fatty acids; feeding Neurodegenerative Diseases and the ALD flies one of the components, glyceryl tri- Addictions in Drosophila oleate oil, blocked the accumulation of excess very long chain fatty acids and eliminated the develop- Drosophila is perhaps unique among eukaryotes in ment of pathology. Thus,bubblegum flies provide a the variety and level of sophistication that can be model system for studying mechanisms of disease applied to understand its neurobiology. Drosophila and screening drugs for treatment. is being studied, as well, to gain knowledge about Drosophila also has been proposed as a various neurodegenerative diseases in humans. model organism for studying the genetics of Modeling diseases in simple invertebrate alcohol abuse and drug addiction in humans. ­systems is attractive because genetic interactions Alcohol addiction and many types of drug addic- can be used to define cellular cascades mediating, tions appear to share common mechanisms. For for example, death of neurons in Parkinson ­disease, example, the “dopamine hypothesis” suggests the second most common neurodegenerative that addictive drugs may ­activate certain areas ­disorder in humans. Transgenic Drosophila con- of the human brain leading to an increase in taining a mutant form of the human α -synuclein dopamine neurotransmitter release. Elevation of gene exhibit the essential features of the Parkin- dopamine probably provides a sense of well son’s disease in humans, making it possible to being, pleasure, or elation (positive reinforce- study the function of α -synuclein and determine ment). Dopamine is not the only neurotransmit- the underlying pathogenic mechanisms in a genet- ter acting in alcohol abuse; glutamate, serotonin, ically tractable animal. and GABA also are may be involved. Further- The spongecake mutant of Drosophila shows more, four of the five circadian genes period,( degenerative changes similar to that seen in clock, cycle, ­doubletime) identified in D. melano- humans with Creutzfeld-Jakob disease, while the gaster influence the fly’s responsiveness to eggroll mutant produces changes similar to those cocaine and suggest a ­biochemical regulator of seen in humans with Tay-Sachs disease. The beta- cocaine sensitization. amyloid protein precursor-like (Appl) gene of Dros- Selection of D. melanogaster for resistance to ophila encodes a homolog of the human α -amyloid ethanol was shown to be determined by multiple ­precursor protein which gives rise to α -amyloid, a genetic components. Mutant strains with different major component of the plaques in the patients responses to ethanol and different responses to the suffering from Alzheimer’s disease. Another pro- effects of acute ethanol exposure on locomotor tein associated with human Alzheimer’s disease, behaviors are remarkably similar to those described presenilin, has been found in Drosophila and stud- for mammals. Thus, study of Drosophila could ies ­suggest it may also be involved in the develop- pave the way for an in-depth study of the genes ment of the pathology. A Drosophila homolog was involved in acute and chronic effects of ethanol. In identified for the human gene for copper/zinc Drosophila, as in mammals, dopaminergic pathways superoxide dismutase; mutants of this gene are play a role in modulating specific behavioral implicated in Lou Gehrig’s disease. responses to cocaine, nicotine or ethanol. 464 B Behningiidae Sleep even occurs in Drosophila and may be a but the disciplines of ethology, genetics, physiol- model for understanding sleep in other animals. ogy, and molecular biology promise to revolution- Flies that are “resting” are sleeping, which involves ize the field. the flies choosing a preferred location, becoming immobile for periods of up to 157 min at a particu- lar time in the circadian day, and becoming rela- References tively unresponsive to sensory stimuli. When rest is prevented, the flies tend to rest despite stimulation Bellen HJ (1998) The fruit fly: a model organism to study and then exhibit a rest “rebound.” Drugs that affect the genetics of alcohol abuse and addiction? Cell 93:909–912 sleep in mammals alter “rest” in flies, suggesting Brady JP, Richmond RC (1990) Molecular analysis of conserved neural mechanisms. During sleep, an ­evolutionary changes in the expression of Drosophila animal cannot forage for food, take care of its young, esterases. Proc Natl Acad Sc USA 87:8217–8221 procreate or avoid the dangers of predation, indi- Costa RA, Peixoto A, Barbujani G, Kyriacou CP (1992) A lati- tudinal cline in a Drosophila clock gene. Proc R Soc cating that sleep must serve an important function. London B 250:43–49 Sleep disorders in humans are common, but the Field LM, Pickett JA, Wadhams LJ (2000) Molecular studies in genes underlying these disorders are unknown. insect olfaction. Insect Mol Biol 9:545–551 Fortini ME, Bonini NM (2000) Modeling human neurode- generative diseases in Drosophila. On a wing and a prayer. Trends Genet 16:161–167 Molecular Analyses of Complex Greenspan RJ, Ferveur JF (2000) Courtship in Drosophila. Behaviors Annu Rev Genet 34:205–232 Greenspan RJ, Tononi G, Cirelli C, Shaw PJ (2001) Sleep and the fruit fly. Trends Neurosci 24:142–145 The genetic basis of many behavioral attributes in Vosshall LB (2000) Olfaction in Drosophila. Curr Opin insects is probably determined by many genes. ­Neurobiol 10:498–503 Furthermore, behavior is determined, not only by Waddell S, Quinn WG (2001) Flies, genes and learning. Annu Rev Neurosci 24:1283–1309 genetic composition, but also by the environment Yamamoto D, Jallon JM, Komatsu A (1997) Genetic dissec- and can be influenced by learning. The effects of tion of sexual behavior in Drosophila melanogaster. the environment may mask those of the genotype, Annu Rev Entomol 42:551–585 making genetic analysis imprecise. While elabo- rate statistical techniques have been developed for quantitative genetic analyses, a thorough under- Behningiidae standing of behaviors that are quantitatively deter- mined has been slow to develop. A family of mayflies (order Ephemeroptera). Understanding the mechanisms of behavior  Mayflies determined by single genes is hard work, but ­relatively straight forward. Understanding the mechanisms of behavior determined by many Beklemishev, Vladimir genes requires ingenuity and extensive effort. Nikolayevich However, such research offers many rewards. For example, advances in understanding the molecu- inna ioffe-uspensky, igor uspensky lar genetic basis of social behavior in bees and ants The Hebrew University of Jerusalem, Jerusalem, could allow us to understand the evolution of Israel female choice, kin recognition, reciprocal ­altruism, and the organization of insect societies. V.N. Beklemishev was born on October 5, 1890, Analysis of insect behavior using insect in Hrodna, then a portion of Poland incorpo- molecular genetic approaches is still in its infancy, rated into the Russian Empire. He grew up in a Beklemishev, Vladimir Nikolayevich B 465 large harmonious family with a high level of of different species of Anopheles. These ­culture and education. From the family he ­fundamental works included the detailed study received a good intellectual and moral education of mosquito morphology, mosquito behavior, that strongly influenced him. He studied in the gonotrophic cycles, physiological age, etc. He local grammar school which he left as the top wrote that any finding illuminating unknown pupil. He was interested in natural history and he features in Anopheles biology would be ­important collected insects and read books by Braem, Fabre for the success of malaria control. From mos­ and other ­naturalists. In 1908, he entered the quitoes he moved to the study of other groups of University of St.-Petersburg specializing in arthropods which allowed him to develop a ­zoology. After graduating from the University ­concept of the “life scheme” of species, which is (1913) he was kept there “to prepare for the title considered as the total amount of species adapta- of Professor.” In 1918 he received his Master’s tions to the environment. His concept is rather degree in zoology and comparative anatomy with close to Hutchinson’s concept of a fundamental the right to lecture. However, because of terrible ecological niche, developed later. He liked and famine and collapse after the October Revolution estimated the comparative analysis as the mostly of 1917 he left ­St.-Petersburg (Petrograd) for fruitful approach in biological study. He was the Perm’ (in the Ural Mountains) where he received founder of the comparative parasitology of the position of an associate professor in the bloodsucking arthropods. Comparing the life ­University of Perm’. By 1920 he was approved as a schemes of bloodsucking arthropods, he distin- full professor in the faculty of medicine. He guished main types of their parasitism. He con- ­lectured in many general and special courses and sidered the origins and development of arthropod carried out intensive research on the morphol- parasitism on terrestrial vertebrates. He devel- ogy of invertebrates, biocenology and hydrobiol- oped well-­balanced systems of relationships ogy. The wide range of his interests and his between parasitic arthropods and their hosts and excellent erudition in various fields of biology showed the role of such systems in biocenoses. were of great importance when in 1924 he headed During the 1950s he worked intensively on the an entomological study at the Malarial Station of problem of tick-borne encephalitis in the USSR the Medical and Biological Institute of Perm’. and ­significantly contributed to the understand- Working on the ecology of Anopheles ­larvae, he ing of the structure of ­natural foci and epidemi- studied hydrobiological characteristics of larval ology and epizootiology of this ­infection. All his biotopes and the habitat distribution of mosquito ideas were not only ­theoretical constructions but larvae. He evaluated the significance of water the result of ­laboratory studies and field expedi- ­bodies in different landscapes not only from an tions to different areas of the USSR in which he entomological but also from an epidemiological participated together with his younger fellows. point of view. As a result, he formulated the His main publications include: “Ecology of the ­doctrine of landscape malariology which allowed malarial mosquito (Anopheles maculipennis the planning of control measures based on the Mgn)” (1944); “The planning of settlements and characteristics of a particular landscape. In 1932 the problem of malaria” (1949); “Manual of he was invited to Moscow to head the Depart- ­medical entomology” in two volumes (editor and ment of Medical Entomology in the Tropical the author of many chapters) (1949); “Key to Institute (later the Martsinovsky Institute of arthropods injuring human health” (editor and Medical ­Parasitology and Tropical Medicine). the author of some chapters) (1958). He was also The biology of adult mosquitoes was the main the editor of many proceedings and books. aspect of his interest at that time. Together with Unfortunately, most of his papers were published his followers he studied the population biology only in Russian. He was well known among world 466 B Belidae zoologists as the author of his greatest work State College, M.A. in zoology in 1966 from the “Principles of comparative anatomy of inverte- University of Massachusetts, and Ph.D. in 1969 brates” which had three editions in the USSR from the University­ of Pennsylvania. The subject (1944, 1952, 1964) and was also published in of his Ph.D. research was the role of juvenile Romania, Poland and the ­German Democratic ­hormone in ­vitellogenesis. Then followed a Republic. In 1969 this monograph was published 1-year postdoctoral fellowship at the University in English (Edinburgh). In recognition of his of Texas before he was appointed assistant pro- works he was elected to the Academy of Medical fessor of entomology at the University of Kansas. Sciences of the USSR, and twice he was awarded His career was spent in Kansas, and he was pro- the USSR State Prize. He was elected to the Polish moted to full professor at the age of 33. He taught Academy of Sciences. He was also much revered undergra­duate and graduate classes and, between by his numerous pupils many of whom became 1970 and 1996 had trained 18 Ph.D. and eight well-known specialists. His interests were not M.A. students in his laboratory. His research limited by biology only. He knew history, liked interests, begun with developmental ­biology, and knew Chinese art and ­philosophy, and he expanded to reproductive physiology, chemo- liked poetry, fine art and ­architecture. He wrote perception, and related behaviors, and began to verses himself. He died on September 4, 1962. In include field work. He served as editor of Journal 1970 his pupils published a collection of his most of the Kansas ­Entomological Society (1982– important papers under the title “Biocenological 1984), ­co-editor of Environmental Entomology principles of comparative parasitology.” (1984–1987), and as editorial board member of Journal of Insect Physiology.­ He served as editor of Journal of Insect Behavior, which he and References Tom Payne founded, from 1988 until his death. He published over 100 research papers and Balashov YS (1991) The significance of V.N. Beklemishev’s reviews, edited three books, and wrote two: concepts of parasitic systems and life schemes of the (1981) “The laboratory cockroach,” and (1991) species for the development of parasitology. Parazi- tologiya 25:185–195 (in Russian) “Searching behavior: the behavioral ecology of Smirnov ES (1962) Scientific activity of V.N. Beklemi­ finding resources.” He died on October 17, 1998, shev. In: Problems of general zoology and medical after a long illness, ­survived by his one son and parasitology. Medgiz, Moscow, USSR, pp 7–38 (in former wife. Russian)

References Belidae Greenfield MD (1998) William J Bell 1943–1998. J Kans A family of beetles (order Coleoptera). They ­Entomol Soc 71:1–2 Greenfield MD (1999) William J Bell. Am Entomol 45:59 ­commonly are known as primitive weevils.  Beetles

Bell, William J Belostomatidae

Bill Bell was born in Boston, Massachusetts, on A family of bugs (order Hemiptera). They some- ­January 10, 1943. His B.S. degree in biology and times are called giant water bugs and toe biters. ­education was earned in 1964 from Bridgewater  Bugs Bertha Armyworm, Mamestra configurata Walker (Lepidoptera: Noctuidae) B 467 Beneficials Importance

Organisms that provide a benefit to crop produc- The economic impact of bertha armyworm is tion, especially natural enemies of pests and plant attributed to its importance as a major pest of pollinators such as bees. canola crops. Young larvae consume the leaf foli- age of canola and the plant generally compensates for this damage. The fifth and sixth instars cause Benthic Community the greatest damage because they feed on the developing nutrient rich seedpods, adversely The community of organisms inhabiting the affecting seed quality and lowering seed grade. ­bottom of a body of water. Since 1922, bertha armyworm outbreaks have occurred at intervals of varying length and persist from one to three years. Since 1970, the increase in the incidence of bertha armyworm outbreaks has Bertha Armyworm, Mamestra been associated with the extraordinary increase in configurata Walker (Lepidoptera: the number of hectares planted to canola. Most Noctuidae) outbreaks are local and not synchronized with those of other areas. Widespread outbreaks cost peter g. mason producers $10s of millions in yield losses and Agriculture and Agri-Food Canada, Eastern ­control costs. ­Cereal and Oilseed Research Centre, Ottawa, ON, Canada Biology The bertha armyworm, Mamestra configurata, atta- cks canola (Brassica napus L. and Brassica Bertha armyworm has a univoltine life cycle rapa L.) in the northern great plains of North requiring 6–8 weeks from egg to pupa, which America. Other crops subject to damage by ber- overwinters. Adults emerge from the soil from tha armyworm include flax, Linum usitatissimum early June to early August and are attracted to L., sweet clover, Meliotus officinalis L., and alfalfa, canola fields that are in bloom. The moths are Medigaco sativa L., although development is not ­nocturnal, and females copulate during the 2nd or completed or progeny are undersized. Bertha 3rd night after emergence, remaining in copula for armyworm is a Nearctic species, apparently about 17 h. Females lay single-layered masses of restricted to dry grassland-type habitats in west- 20–200 eggs on the underside of leaves of host ern North America. It prefers the native weed plants, depositing 75% of their egg complement Chenopodium album (lamb’s-quarters) but suc- during the first week after emergence and up to cessfully develops on B. napus and B. rapa variet- 3,500 eggs during their lifetime. ies with low isothiocyanate and glucosinolate Eggs are spherical, slightly flattened on the levels (canola). Mamestra configurata has one ventral surface, about 0.45 mm in diameter and North American relative, Mamestra curialis with a series of longitudinal ridges and depres- (Smith). The larvae of the two species are difficult sions (sculpting) radiating from the upper mitotic to separate but adults are ­distinguished by the pole. The white eggs develop for approximately wing markings and by characters­ of the male gen- one week. As development takes place the eggs italia. The two species also occupy different habi- become almost black. Just before they hatch, the tats, M. curialis occurs primarily in forested areas black headed first instar larvae are visible through while M. configurata is found in grassland areas. the chorion. 468 B Bertha Armyworm, Mamestra configurata Walker (Lepidoptera: Noctuidae) First-instar larvae hatch and immediately and females are distinguished by the structure of the ­disperse from the egg mass to feed on foliage. The terminal abdominal segments. Bertha armyworm larvae feed at night and when disturbed they may pupae are not easily distinguished from other drop off the leaves using a fine silk thread which ­cutworm pupae. The pupae undergo a ­facultative they use to climb back onto the plant. Large larvae diapause, induced by temperature and photo-­ may drop off the plants and curl up when­disturbed, period cues experienced by 4–6 instar ­larvae. If fall behavior typical of cutworms and armyworms. ­conditions are unusually warm some pupae continue The first four instars feed on foliage and, although development and will emerge. Over-wintering­ they prefer foliage, the final two instars feed on the ­mortality of pupae is important and is influenced developing pods, the most nutrient-rich plant part by duration of exposure to temperatures near or during this time of the growing season. The final below freezing. instar larva consumes 70–80% of the total food The adult is large with a wingspan of about consumed by the six larval stages. The dark color 4 cm. The forewing is mostly grey with patches of of the last two larval instars makes them noticeable black, brown, olive and white scales. The distin- in the crop. At summer’s end the mature ­larvae guishing feature of the bertha armyworm moth is drop to the ground and seek shelter in cracks the broad olive band adjacent to the subterminal 5–16 cm below the soil surface where they pupate. line, defined by white markings on the inner side ­Larvae vary greatly in color, particularly the older of the forewing. individuals. Outbreaks of bertha armyworm are sporadic, Newly hatched first instar larvae have a yet consist of huge numbers of larvae infesting ­distinct black head and are about 0.3 cm long and canola crops. Population monitoring is important are covered with sparse but distinct setae. The next for determining the potential for damage. Adult five instars have light brown head capsules and the bertha armyworm can be detected by close inspec- body setae are less evident. The first four instars tion of lamb’s-quarters and canola plants where are green, usually with distinct, narrow, whitish, they roost during the day on the underside of stripes on their back, and a wider but indistinct leaves. Egg masses and early instar larvae are found band on the side of the body. Most fifth instar by inspecting the underside of leaves. The dark late ­larvae are green, others brownish green, or brown instar larvae are readily visible when feeding on with darker markings. The sixth instar, about 4 cm developing seedpods on the tops of canola plants, long, is commonly velvety black or brown with even at a distance. Area-wide pest management conspicuous yellowish-orange stripes along programs use traps baited with a species-specific each side and a green underside which contrasts sex pheromone to monitor bertha armyworm adult with the dark dorsum. Individuals of the velvety numbers. The data are refined and mapped using black form have three narrow, interrupted white geographical information systems (GIS) to provide stripes along their backs. In nature, many variants an early warning of outbreak potential. Producers are found, singly or in homogenous groups, and in areas of high risk are advised to regularly inspect appear to represent different species, increasing the their crops to assess larval densities. ­difficulty of accurate identification. Larvae may exhibit ­limited local migration, typical of armyworms, when their preferred food source is consumed. Management Pupae are reddish, slender, 5.5 mm wide and 18.5 mm long, gradually tapering caudally with Chemical insecticides are registered for use against ­flexible abdominal segments. The terminal spines are bertha armyworm. The decision to apply insecti- stout, about 0.7 mm long, close set but slightly cides is based on the larval densities associated ­divergent, and slightly out-curved at the tip. Males with the value of the crop and the cost of spraying. Bequaert, Joseph Charles B 469 However, insecticides harm natural enemies, Mason PG, Erlandson MA, Youngs BJ (2001) Effects of ­particularly parasitoids of the bertha armyworm. ­parasitism by Banchus flavescens (Hymenoptera: Ich- neumonidae) and Microplitis meditor (Hymenoptera: Cultural control methods for reducing the Braconidae) on the bertha armyworm, Mamestra impact of bertha armyworm include crop rotation ­configurata (Lepidoptera: Noctuidae). J Hymenopt Res and tillage. Crop rotation has limited effectiveness 10:81–90 Mason PG, Turnock WJ, Erlandson MA, Kuhlmann U, because adult bertha armyworm are strong fliers Braun L (2001) Mamestra configurata Walker, bertha and readily invade neighboring crops. Fall tillage armyworm (Lepidoptera: Noctuidae). In: Mason PG, may increase the overwintering mortality of pupae Huber JT (eds) Biological control programmes in and spring cultivation may injure the pupae but ­Canada 1981–2000. CABI Publishers, Wallingford, UK pp 169–176 these methods are not used where minimum Rempel JG (1951) A study of the embryology of Mamestra ­tillage is practiced. configurata (Walker) (Lepidoptera, Phalaenidae). Can Naturally occurring diseases, such as the Entomol 83:1–19 ­fungus Entomophthorales sp., a “nuclear polyhe- drosis virus” (NPV), and the microsporidian Nosema sp., are important larval mortality factors Berytidae at high population densities and NPV infections in up to 95% of local populations have been A family of bugs (order Hemiptera). They some- recorded. Of the native parasitoids, only Banchus times are called stilt bugs. flavescens Cresson (Ichneumonidae) and Athrycia  Bugs cinerea (Coquillett) (Tachinidae) cause significant mortality in bertha armyworm populations. ­During outbreaks, B. flavescens, which attacks early instar larvae, is usually the most abundant parasi- Bequaert, Joseph Charles toid, although A. cinerea occasionally is more abundant. Parasitism significantly reduces food Joseph Bequaert was born in Thourout, Belgium, consumption by bertha armyworm larvae. The on May 24, 1886. He earned a Ph.D. from effect of arthropod predators on bertha ­armyworm ­Universiteit Gent in natural sciences in 1908. In ­populations is unknown. Vertebrates, particularly 1910–1912, he worked for the Belgian sleeping birds, may be important when population sickness commission, and in 1913–1915 in what ­densities are high. How natural enemies regulate was then the Belgian Congo. He emigrated to the bertha armyworm populations between outbreaks USA and became (1917–1922) an associate of the is not known. American Museum of Natural History as ento- mologist, malacologist, and botanist. He became a U.S. citizen in 1921. In 1923–1925 he worked as References an instructor in entomology at ­Harvard Medical School (Massachusetts, USA), in 1925–1945 as Bracken GK (1984) Within plant preferences of larvae of assistant professor, and in 1929–1956 as curator Mamestra configurata(Lepidoptera: Noctuidae) feeding of insects in the Museum of Comparative Zoology on oilseed rape. Can Entomol 116:45–49 at Harvard University and in 1951–1956 as Bracken GK (1987) Relation between pod damage caused by larvae of bertha armyworm, Mamestra configurata ­Agassiz Professor of ­Zoology at the same Walker (Lepidoptera: Noctuidae), and yield loss, ­shelling, institution. Then he moved to the University of and seed quality in canola. Can Entomol 119:365–369 Houston (Texas, USA) as professor of biology, Mason PG, Arthur AP, Olfert OO, Erlandson MA (1998) The moving to the ­University of Arizona in 1960. His bertha armyworm (Mamestra configurata) (Lepidoptera: Noctuidae) in western Canada. Can Entomol final move was to the University of Massachusetts. 130:321–336 He married ­Frances A. Brown in 1927 and they had 470 B Beraeidae two children. His interests were in entomology (especially ­medical entomology) and malacology (especially medical malacology); he published major works in both areas and was president of the American ­Malacologists’ Union in 1954. He died in Amherst, Massachusetts, USA, on May 24, 1982.

References

Abbott RT, Young ME (eds) (1973) American malacologists: a national register of professional and amateur ­malacologists and private shell collectors and biogra- phies of early American mollusk workers born between Berlese, Antonio, Figure 34 Antonio Berlese. 1618 and 1900. Falls Church, Virginia, USA, American Malacologists/ Philadelphia, USA: Consolidated/ Drake Press, 494 pp history and collected insects and mites. His Clench WJ (1982) Joseph Charles Bequaert 1886–1982. Nau- tilus 96:35 studies at ­Università di Padova (the University of Padua) resulted in a degree in 1884 in natural sci- ences. He worked for a few months in a school of human anatomy, but then accepted a post at Stazi- Beraeidae one di Entomologia Agraria in Florence, which Adolfo Targione Tozzetti had founded and then A family of caddisflies (order Trichoptera). directed. Finishing a professional course in 1887,  Caddisflies he worked as Targioni’s assistant until 1890 when he was nominated for a position as professor of general and agrarian zoology at R. Scuola Superi- Bergmann’s Rule ore di Agricoltura di Portici, where he worked until 1903. Then, he was nominated director of the Among mammals and birds, individuals of a ­species R. Stazione di ­Entomologia Agraria in Florence, occurring in colder climates tend to have a larger succeeding Targioni. He built up this station little body mass, and a correspondingly lower surface to by little until it became one of the best-equipped volume ratio, than members of the same species in Italy. From his first publication in 1880, he ­living in warmer climates. This trend results from worked 47 years without interruption, producing the need to conserve heat in cold ­climates but to a total of 275 publications. A large part of his work eliminate excess heat in hot ­climates. A variant of was devoted to the study of mites, in which he this is Allen’s rule. These rules do not apply to built a collection of 12,750 slide-mounted speci- ­ectothermic animals such as insects. mens. Another major endeavor was his work on  Allen’s Rule olive fruit fly, and yet another on the scale Diaspis  Thermoregulation pentagona. His two-volume book “Gl’insetti, loro organizzazione, sviluppo, abitudini e rapporti coll’uomo” with 2,187 figures, was published in Berlese, Antonio parts, from 1904 to 1923. His awards included a prize of 10,000 lire from the R. Accademia di Agri- Antonio Berlese (Fig. 34) was born in Padua on coltura di Torino, a gold medal from the province of June 26, 1863. As a boy, he was interested in natural ­Venezia in 1913, an award of 75,000 lire from the Bernhauer, Max B 471 council of the province of Udine in 1924, and hon- he obtained in 1899 was as doctor juris (“doctor of orary ­membership in the Société Entomologique de law”), not as a biologist. He worked as a notary in France. He died in Florence on October 24, 1927. Austria. It was Ludwig Ganglbauer, in particular, who instructed Max on Coleoptera. His first two References papers were published in 1898. Because of the dearth of people willing to study and identify Paoli G (1928) Antonio Berlese. Memorie della Società Staphylinidae, Max was soon presented with an ­Entomologica Italiana 6:55–84 endless flow of specimens collected from around the world, and asked to identify them (cost free, of course). For Max, this was a seemingly endless Berlese Funnel opportunity to classify and describe the species of the huge family Staphylinidae, and to build his col- An extraction devise used to separate and extract lection. He collaborated with Karl Schubert and small arthropods from leaf litter or similar material. Otto Scheerpeltz in producing a world ­catalog A Berlese funnel normally consists of a funnel with (published by Junk-Schenkling as part of “Coleopter- a wire mesh insert that support the plant material orum Catalogus”;), completed in 1926 and listing above a reservoir containing alcohol or another 12,740 species, but expanded to 19,900 species by preservative. As the arthropods move about, 1932 by Otto Scheepeltz and continuing to grow. ­particularly as they move deeper into the funnel to The world total of Staphylinidae as of the year 2000 escape drying of the plant material, they slip down exceeded 45,000 species, and ­Max Bernhauer had the funnel into the reservoir containing liquid described 5,251 of them, including 342 new genera, where they are retained for identification. This tech- in his 285 publications, a spectacular achievement nique is useful for many arthropods, but not for for an “amateur” coleopterist. Names of the vast those that may fly to escape, or those that are very majority of the species that he described are still fragile and perish from desiccation before they can considered valid, even though he was not in the escape the plant material. A modern variant of the habit of providing illustrations or keys for identifi- Berlese funnel is the Tullgren Funnel, which is cation, so that confirmation of ­identity of the spe- ­simply a Berlese funnel with an incandescent light cies he described is often very ­difficult. He died on suspended above the funnel to provide a source of March 13, 1946, in Horn, ­Austria. His collection was heat and to extract the arthropods faster. Another sold, soon after his death, a­negotiation achieved by variant uses a cover to eliminate escape by insects Rupert Wenzel, to the Field Museum of Natural capable of flight, and to more efficiently direct the History, Chicago, USA. There seems to have been a heat generated by the light bulb. Most “Berlese” teacher-student­ train ­Erichson-Ganglbauer- Bern- ­funnels now used are actually Tullgren funnels, but hauer-Scheerpeltz among the German-speaking the distinction is not generally appreciated. students of Staphylinidae, which, unfortunately, ended with Otto Scheerpeltz.

Bernhauer, Max References

Max Bernhauer was born in Müglitz, Austria Herman LH (2001) Bernhauer, Max. Bull Am Mus Nat ­(otherwise known as Mohelnice, and now in the ­History 265:43–44 Czech Republic) on September 24, 1866. His Puthz V (1980) Bibliographie der Publikationen Max Bern- ­education was in Olomonic (now in the Czech hauers (1866–1946) [a bibliography, not a biography]. Philippia 4:248–261 Republic) and then at Universität Wien (“the Rambousek G (1916) Ein Lebensbild Dr. Max Bernhauer’s. ­University of Vienna,” Austria), but the final degree Coleopterologische Rundschau 5:73–82 472 B Berothidae Berothidae Bess Beetles (Coleoptera: Passalidae) A family of insects in the order Neuroptera. They commonly are known as beaded lacewings. jack schuster  Lacewings, antlions, and mantidflies Universidad del Valle de Guatemala, Guatemala City, Guatemala

Bess, patent-leather, or passalid beetles are Bertram, Douglas Somerville ­common, primarily tropical insects. A few of the approximately 600 species occur in temperate Douglas Bertram was born in Glasgow in 1913. regions (China, Japan, Korea, Canada, U.S., and His Bachelor’s degree was from Glasgow Univer- Tasmania, but not Europe, though the largest sity, after which he did graduate research and ­collection in the world may be that of the Paris was employed as a demonstrator in the Zoology Museum of Natural History). Five species have Department of that university. In 1938 he moved been collected in the U.S. (Compare to Guate- as Lecturer in Entomology to Liverpool School mala, the size of North Carolina, with 84 species!) of Tropical Medicine, began insect cultures, and The most common, Odontotaenius disjunctus ­performed research on fowl malaria. In 1940, he (Illiger), is known from the East Coast to the enlisted in the British army and served in Egypt riparian ­forests of the eastern Great Plains north and Greece, but was captured in Crete and to Manitoba and Ontario, and south to Texas and remained a prisoner in Germany for the dura- Florida. Another species, O. floridanus Schuster tion of the war. In 1946, he returned to Liverpool is known only from sand hills of Florida scrub for two years and worked on cotton rat filariasis ­habitat which used to be islands during previous and on control of warble fly. In 1948, he was interglacial times. Two other species, Passalus appointed as Reader in the Department of Medi- punctiger Lepeletier & Serville and P. punctatos- cal Entomology in the London School of Hygiene triatus Percheron, were collected at the beginning and Tropical Medicine, later becoming head of of the twentieth century in eastern Arizona; they the department. His research was directed to may have been brought from Mexico in wood mosquitoes, ­especially their age-grading, and shipped by train. They haven’t been collected in their transmission of viruses and fowl malaria, the U.S. since that time. A fifth species, Ptichopus but extended to other biting families of biting angulatus (Percheron), was recently collected in flies, and to biological control of triatomine bugs. Arizona. This has been expected; it occurs in He traveled extensively to ­tropical countries to ­leaf-cutter ant nests just south of the Rio Grande further his research. He was consultant in ento- in Texas. mology to the British army, fellow of the Royal Flightless beetles tend to originate on islands Entomological Society, of the Institute of Biol- or (in passalids especially) on isolated mountains, ogy, and of the Royal Society of Tropical Medi- resulting in high levels of endemism (an endemic cine and Hygiene. He died in 1988. organism is one found only in a given area, e.g., endemic to Guatemala, or endemic to Pike’s Peak). The distribution of endemic passalids correlates with the distribution of other endemic organisms. References Because passalids are relatively easy to find, they can be used as indicator organisms for areas of Busvine JR (1989) Obituary. Douglas Somerville Bertram. endemism, especially for cloud forests on tropical Antenna 13:8–9 mountains. For example, eight areas of endemism Bess Beetles (Coleoptera: Passalidae) B 473 have been identified for Guatemala and adjacent Passalids are in the superfamily Scarabaeioidea Chiapas, Mexico, on the basis of passalid distribu- together with the more famous scarab beetles. They tions. This is important for prioritizing areas for are large beetles (length 11 to more than 80 mm) conservation. and are orange or reddish when they hatch from Only one fossil passalid is known, similar, if the pupal case; most change to a shiny black color not identical, to a species known from the lowland as they mature. Most have grooves (striae) in the neotropical forests, today reaching only to north- elytra (wing covers). Many have a horn of some ern Mexico. This fossil, from Oregon, implies the sort in the center of the head. In the Americas, most presence of such forests there in the Oligocene, have three lamellae in the antenna, some four or more than 25 million years ago. five; some Old World species have more lamellae. The classification of the Passalidae is: Certain Old World passalids have an asymmetrical Order: Coleoptera “face”; such asymmetry is rare among animals. Superfamily: Scarabaeioidea Beetles of some other families look remark- Family: Passalidae ably like passalids; indeed, one tenebrionid from Subfamily: Passalinae Africa has the epithet passalioides. Tenebrionids Subfamily: Aulacocyclinae and lucanids which resemble passalids also live in The Aulacocyclinae are restricted to the area from rotting wood; however, certain carabids (e.g., Scarites) India to Oceania and Australia. The Passalinae are are superficially similar to passalids, but live mostly pan-tropical. This subfamily is divided into underground. Some scarabs resemble passalids, two tribes: Proculini, restricted to the Americas, and but live in dung or underground as well. Passalini, which is mostly pan-tropical. Eggs are placed in a specially constructed nest Most passalids live in rotting wood; a few live of masticated wood pieces and feces (frass) and in other habitats, such as leaf-cutter ant detritus are red. As they mature they change to brown, chambers, termite nests or under the roots of then green when ready to hatch. The larvae are ­epiphytic bromeliads – all sites of decaying organic easy to recognize; they look like white grubs matter. Those in wood prefer broadleaf trees; oak though not as curved and they have only four is a favorite. Some occur in palms and a few in ­easily visible legs. Actually, they do have 6; the hind pines, but few in other conifers. They are most pair is reduced to a scraping organ that is rasped common and diverse in tropical lowland and against the base of the second pair of legs. This montane wet forests; up to ten species may be produces a sound, the function of which is found in a single log (in Brazil). Some, flatter unknown. ­species, are specialized for living under the bark; The larvae (and adults) require frass for others bore deep into the logs. They appear to be ­feeding; even adults will die if no feces are included quite important as wood decomposers in forest in their diet. They apparently have an “external ecosystems. rumen,” as do rabbits; they feed on the fungi and An unusual number of species of other organ- bacteria and the products of microorganism isms are associated with passalids, especially mites ­digestion that are in the feces. and certain fungi, perhaps due to their boring in The larvae pupate in a specially constructed wood (other groups with high mite diversity include cocoon of frass that the adults and larvae build scolytid beetles, also wood borers). At least ten together. The fact that young adult siblings of a larva ­species of mites are associated with O. disjunctus in will repair a damaged pupal case implies a high the eastern U.S. Various animals attack passalids, level of subsocial behavior for these beetles. Adults including vertebrates (birds and mammals, and live at least two years in nature and to at least 5 years probably some reptiles and amphibians), nematode in the laboratory. Some species have large “colonies” worms, tachinid flies, and reduviid assassin bugs. with many individuals; others seem restricted to a 474 B Beta Taxonomy pair and perhaps their offspring. Generally, only Bet-Hedging mature individuals migrate. Though adults may be found flying or walking at many times of the year, Variable life history strategies within an insect they appear to be most commonly migrating at the ­population resulting from genetic or phenetic beginning of the rainy season in the tropics. polymorphism. Bet-hedging is manifested by Adults stridulate as well, producing sounds by ­variation in diapause, wing development, rate of rubbing the dorsal surface of the abdomen against development, rate of reproduction and other the hind wings. In species that don’t fly, the wings ­critical life history traits. Bet-hedging equips a are reduced to thin straps, but with the stridulatory population to survive variable and unpredictable area preserved. Passalids are known to produce up environments that may favor certain traits in one to 14 different acoustical signals in one species, season and certain traits in others. more than many vertebrates. Pheromones, ­chemical communication, is also apparently used. Sounds are used when fighting other individuals, usually of Bethylidae the same species. Also, sounds are important in courtship, which involves a “dance” that can last as A family of wasps (order Hymenoptera). long as 12 h in the laboratory. At least in some  Wasps, ants, bees, and sawflies ­species, copulation occurs in the tunnels of a log; however, O. disjunctus has been observed copulating during flight! At least in the laboratory, copulation Bias begins venter to venter, a rare position for insects. In sampling, an unidirectional deviation of an References estimate from the true mean or variance of a population. Reyes-Castillo P (1970) Coleoptera, Passalidae: morfologia y  Sampling Arthropods division en grandes grupos; generos americanos. Folia Entomologica Mexicana 20–22:1–240 Schuster J (1983) Acoustical signals of passalid beetles: ­complex repertoires. Fla Entomol 66:486–496 Bibionidae Schuster J (2002) Passalidae. In: Arnett R Jr, Thomas M (eds) American beetles vol 2. CRC Press, London, UK A family of flies (order Diptera). They commonly Schuster J, Schuster L (1997) The ­evolution of social behavior in Passalidae (Coleoptera). In: Choe J, Crespi B (eds) The are known as March flies. evolution of social behavior in insects and arachnids.  Flies ­Cambridge University Press, Cambridge, UK, pp 260–269 Schuster J, Cano E, Cardona C (2000) Un metodo sencillo para priorizar la conservacion de los bosques nubosos de ­Guatemala, usando Passalidae (Coleoptera) como organ- Bicaudate ismos indicadores. Acta Zoologica Mexicana (n.s.) 80:197–209 Having two cauda, or filamentous tail-like pro- cesses, at the posterior end of the body. Beta Taxonomy Biddies The arrangement of species into higher categories of classification. A family of dragonflies in the order Odonata:  Alpha Taxonomy Cordulegastridae.  Gamma Taxonomy  Dragonflies and Damselflies Biocenology (Biocoenology) B 475 Biennial second is the species, and is not capitalized. Both words are italicized. The author’s name (the person A plant that completes its life cycle in two years who first provided a technical description of the and usually does not flower until the second grow- species) often follows the scientific name. If the ing season. genus name has been changed since the organism was named by the author, then the author’s name is placed in parentheses to indicate that a change Bifid has been made. When several species in the same species are discussed together, then “species” may This refers to a structure that is forked, or divided be abbreviated spp. For example, in discussing the into two parts or lobes. More commonly it is genus Spodoptera, we might refer the members as described as bifurcate. Spodoptera spp. On the other hand, a single ­species is indicated as “sp.”

Bifurcate Binomial Sampling This refers to the division of a structure into two parts, as when it is forked; it is also called bifid. The A sampling method that involves recording only the point where the division occurs is called the presence or absence of members of the population bifurcation. being sampled (such as an insect pest) in a sample unit (such as a leaf), rather than counting the ­numbers of individuals. This is a type of presence- absence sampling. (contrast with enumeration Big-Headed Flies sampling).  Sampling Arthropods Members of the family Pipunculidae (order Diptera).  Flies Biphyllidae

A family of beetles (order Coleoptera). They Bilateral Symmetry ­commonly are known as false skin beetles.  Beetles This refers to symmetry of the body in which one side is a mirror image of the other side. When divided along the main axis, insects are almost Bioassay always bilaterally symmetrical, with the left and right halves being mirror images. The use of a living organism to determine the effect of any chemical (or biological agent), such as a semiochemical, upon the organism. Binomial Nomenclature

A system of naming organisms with two names, Biocenology (Biocoenology) the genus and species. This binomial is also known as the scientific name, and is in Latin. The first of Study of the organization and functioning of the two names is the genus, and is capitalized. The ­communities, particularly a descriptive analysis of 476 B Biocenosis (Biocoenosis) assemblages of interacting populations within a Decreased insecticide use helps preserve natural particular area. This term is most popular in enemies, reduces insecticide residues in crops, Europe; elsewhere it is referred to as synecology or and delays the development of insecticide resis- community ecology. In some respects, it is the tance. Other benefits are the conservation of “opposite” of autecology. petroleum products, increased safety to farm  Biocenosis workers, local residents and the environment. Additionally, models of insect biotic potential and life cycle timing can increase the precision Biocenosis (Biocoenosis) of sampling and monitoring programs, and application of biological control procedures. An association of interacting, living creatures in More complex bioclimatic assessment models an area. The environment or habitat is usually have been designed to predict the potential ­uniform, and the community self-sufficient. This ­establishment and distribution of insect species, term is most popular in Europe; elsewhere it is often to assess the risk of invasion into areas referred to as an “ecological community.” where they are not normally found.  Biocenology Temperature Models Biocides Of all the climate variables that directly affect Chemicals that kill a wide range of living organisms. insects, temperature has the greatest influence.  Insecticides The ­influence of temperature on insect develop-  Acaricides ment rate, growth and fecundity has been quan- tified for many species. The relationship often observed in laboratory ­conditions between Bioclimatic Models in Entomology insect development rate and temperature (see development rate figure, Fig. 35) is well used by susan p. worner applied entomologists to predict ­timing and National Centre for Advanced Bio-Protection phenology of insect life cycle events. The rela- Technologies, Lincoln University, Canterbury, tionship is usually nonlinear throughout the New Zealand range of temperatures in which a species can survive; however, a number of mathematical Because climate has such a profound effect on functions, both linear and ­non-linear, have been the distribution and abundance of invertebrates, used to describe it. Such functions comprise quantification of climatic influences on insects simple models for prediction of timing or pheno­ has been of considerable interest to entomolo- logy of life cycles, or can form the basis of more gists for well over a century. While simple pre- complex bioclimatic models. dictive ­models were developed early on, easier There are three basic approaches to modeling access to ­computers in the 1970s resulted in the insect development in relation to temperature. development of ­computer based models to pre- The oldest and most widely used model is a sim- dict the biotic potential of insects in relation to ple ­linear description of insect development in climate. Simple bioclimatic models are often relation to temperature (see development rate used to predict population events so that control ­figure). The linear model forms the basis to the methods can be more precisely applied, reducing well known thermal summation or degree day costs to the grower as well as insecticide use. (DD) approach to timing prediction. Degree days Bioclimatic Models in Entomology B 477 0.06 of the fly larvae or pupae, and by applying the ­particular relationship between temperature and 0.05 development for the fly species, the forensic 0.04 ­entomologist can often determine the time of death of the ­unfortunate person. Of course, when investi- 0.03 gating a suspicious death, things are not usually 0.02 that easy and many factors that influence the Development rate ­temperature experienced by the flies need to be 0.01 taken into account. For example, whether the body 0.00 is found inside a building, a vehicle, shallow grave 10 20 30 40 Mean temperature (degrees celsius) or other enclosed space, or whether it is found out- doors exposed to the elements is of importance. Bioclimatic Models in Entomology, Figure 35 Even the heat generated by the maggots could Generalized nonlinear (solid line) and linear influence the rate of development of the flies. ­development rate curves. Notice that the linear model is confined to the more linear portion of the development rate curve (see development rate figure). Intrinsic to the use are also called thermal units, heat units, or grow- of the linear model is the assumption that devel- ing degree days. Degree days are simply the num- opment is proportional to temperature. This means ber of degrees above a threshold temperature that the reciprocal of the slope (1/slope) of a required for growth. If temperatures are held con- regression line fitted to the developmental data stant in the laboratory, for example at 20°C, and if obtained at constant temperatures gives the DD the lower threshold, T0, for growth or develop- required for development. The linear regression ment of the insect life stage of interest, is 5°C, then equation can also be used to calculate the lower degree days per day or the amount of influential threshold (T0) for development which is defined heat to which the insect is exposed is 20–5°C = 15 as – a/b, where a, is the intercept and b is the slope DD. Degree days per day are accumulated over of the regression line. The thermal optimum the time it takes the particular life stage to com- (if required) is often estimated by visual inspec- plete development. For example, if that life stage tion of the development rate curve. takes 10 days to ­complete development, that time The linear or degree day model is easy to is converted to physiological time by 15 DD ×10 develop and use. While the linear model is clearly days = 150 DD required for development. To pre- wrong in the sense that the lower and upper dict events in the field, some meaningful point or ­curvilinear portions of the development rate curve biofix from which to start degree day accumula- are ignored, this may not matter when field tion and some method to ­calculate degree days ­temperatures lie within the developmental extremes, from the daily diurnal ­temperature curve are but inaccurate predictions will result when temper- required. There is a large amount of literature on atures stray too often beyond these points. application of this method in applied entomology The second approach to predicting insect and plant growth studies. ­phenology in relation to temperature encom- Of special interest is how the relationship passes the many non-linear mathematical between insect development and temperature is descriptions or functions used to describe non- used in forensic entomology. As gruesome as it linear development of insects. These functions might be, species of blowflies are often the first can range from a simple sine-curve fitted to the to find a dead body, on, or near which, they lay nonlinear data to more complex biophysical their eggs. By judging the age of the life stages models or equations. Non-linear models require 478 B Bioclimatic Models in Entomology rate summation for timing prediction. Rate sum- that is available and that may dictate the level of accu- mation can be described as: racy that is achievable. In many cases when great accuracy is not necessary (or achievable) the simple D = Σr(T(t))dt degree day approach may be all that is required. Obviously, other climate variables have poten- where development D is a function of temperature tial to influence insect population processes, and T which in turn is a ­function of time t, r is the therefore the distribution and abundance of insect development rate and dt is the time increment. For species in any locality. Models that incorporate good precision the time increment should be other climate variables to predict insect distribu- hourly. While these models provide a more accu- tion and abundance range from simple graphical rate description of the developmental relationship approaches called climatographs or climographs to they are more difficult to develop and complicated more complex models that are process ­orientated. to apply in practice. The graphs use a combination of­climatic factors to predict areas that are suitable for establishment of a particular species and allow quick comparisons Distributional Models between sites. The simplest ­climatograph is a plot of the profiles of mean monthly temperatures and The third approach to life stage development in rainfall totals for a locality. A much more useful cli- ­relation to temperature is represented by distribution mate diagram or climatograph, however, can be a models of insect phenology that include tempera- plot of mean monthly temperatures against mean ture dependant development as well as variation in monthly rainfall totals or humidity such that the development rates within the population at any points for the 12 months of the year are joined to ­particular temperature. Such models require consid- create a polygon. At a glance one can see different erable research investment but can give important shaped climate ­diagrams may or may not overlap information about the uncertainty of prediction and indicating times of the year where different regions good estimates of limits to development in regions may or may not have similar climatic ­conditions where the species is not normally found. In general, (see climatograph figure, Fig. 36). however, complexity does not ensure more accuracy, and a comparative approach is often required. Addi- tionally, there are also differences in the performance Multivariate Models of phenological models under variable temperature conditions that need to be taken into account. Other bioclimatic approaches include the use of The biological realism or practicality of each multivariate statistical models to predict insect dis- approach to phenological prediction has been widely tribution and abundance in relation to climatic debated. Unfortunately, that debate is not helped by variables. Multivariate approaches such as ­principal the fact that the appropriateness of a model is often components analysis (PCA) and discriminant judged on how well it fits the observed data rather analysis can overcome the limited dimensions that than on rigorous validation using independent data. ­constrain graphical models. Alternatively, multi­ Rigorous validation requires that a model is vali- variate methods can help reduce large amounts of dated against an ­adequate sample of the real world. environmental data to a few important variables, One or two sites or seasons are clearly not enough. and are often used to pre-process data to reduce the Currently, no model provides an accurate number of input variables to improve subsequent description of development in all circumstances, analysis by other statistical methods or models. especially under fluctuating conditions. Clearly, we Because the relationship between insects and are limited by the accuracy of the temperature data their environment can be complex there have Bioclimatic Models in Entomology B 479 15 Iceland ( ) Macquarie Is.(•) 10

5

Campbell Is.( ) 0 •

−5

−10 Deception Is.( )

−15 Casey station( )

−20 0 20 40 60 80 100 120 140 160 Rainfall (mm)

Bioclimatic Models in Entomology, Figure 36 Climatographs for sites in the Antarctic region compared with Iceland. Graphs were compiled to determine how likely insect species that have invaded and ­established in some areas of the Arctic could survive the climatic conditions in representative sites of the Antarctic and sub-Antarctic regions. been many other attempts to characterize their and rainfall for several thousand sites throughout response to a range of abiotic and biotic factors. the world. Such ­models are called bioclimatic “envelope” At the second level of complexity the ­CLIMEX models and are a type of species distribution program is designed to predict the potential model wherein the current geographical distri­ ­distribution of the species by calibrating its bution of the species is related to local climatic ­biological responses to the climate of its current variables to enable prediction of survival or estab- distribution. The species responses are modeled lishment in new areas or climates. The most well by a series of stress indices that include cold, hot, known and well used model that combines insect dry and wet parameters that define particular species’ response to a number of climate variables environmental limits to the sustained growth and into meaningful, manageable indices, is called development of the population. These indices are CLIMEX. CLIMEX is a computer based system then combined in an “Ecoclimatic index” that that provides two ­levels of analysis. First is a describes the overall favorability of geographic ­simple match function that can be used to find locations for that particular organism. There are climates elsewhere in the world that are analogous many examples of bioclimatic assessments of to, or match, within a specified level of similarity, insect species using CLIMEX particularly for the area of interest. Given further information on quarantine or risk assessment purposes. Despite insect biological parameters, CLIMEX can give being relatively easy to use, CLIMEX, like many estimates in the form of simple indices of the models, should not be used as a black box, it favorability of ­particular geographic region for requires a level of expertise or training to opti- insect population growth and development. mize its use and to ensure correct interpretation CLIMEX includes detailed long term weather of results. data, comprising maximum and minimum There are now many examples of biocli- ­temperatures, evaporation or relative humidity matic models that have been applied to a range 480 B Bioclimatic Models in Entomology of taxa. Some of the most well known are weights of the network connections over many STASH, BIOCLIM, CLIMATE, HABITAT, GARP hundreds or thousands of iterations to minimize, and DOMAIN. In fact, the number of computer- by least squares, the difference between the based models, statistical approaches and machine observed values and its own output values. The learning techniques applied to bioclimatic predic- unique algorithm and structure means an ANN tion continue to increase, apparently driven by can learn to fit extremely complex functions and research interest in the distributional changes of therefore is very useful for predicting species species in response to climate change. presence or absence based on a number of cli- mate variables. Another advantage of machine learning approaches is that correct procedure Computational Intelligence involves training (fitting) but also testing and validation of the models. This procedure assesses More recently, applied computational intelligence how well the model can generalize to new data models such as artificial neural networks (ANN) and as a result, over-fitting, the scourge of more and other machine learning techniques have been conventional approaches, is avoided.Of all the successful for bioclimatic assessment of insects as modeling and statistical methods described well as other species. Such models have the advan- above, none can answer all the questions con- tage that they can model complex nonlinear data cerning insect species biotic processes in rela- and they are not constrained by the distributional tion to climate. The seemingly broad range of characteristics of data as more conventional approaches can complicate the choice of model. ­parametric statistical models may be. In some Interestingly, when different models are com- comparative studies, ANN have been shown to be pared over many re-organizations of the data better than other methods for modeling species used to create them (Fig. 37), some models can distribution in response to climate. The most com- perform better than others on a particular data mon ANN used for prediction is the multi-layer set, but can perform worse than the others when perceptron or MLP. using a different data set. That means it is impor- ANN were first designed to mimic the ver- tant to compare the efficacy of new methods tebrate brain and consist of a network of pro- with more standard approaches. While the bio- cessing elements called neurons in usually three climatic models described here cannot replace layers; the input layer, the hidden layer and the more detailed modeling of individual species output layer. All neurons of each layer are con- Processing of nected to all the neurons of the adjacent layer. As the information in the ­animal nervous system, each processing element in the network receives input from many Dendrite others in the network. Each of the inputs or Soma Axon independent ­variables (U) is multiplied by its associated weight or coefficient and this dictates Inputs from Synapse outside or the strength or size of each input. The modified other neurons Outputs to the u1 w1 exterior or inputs are summed and the result is further u 2 w2 N other neurons x modified by what is called a transfer function, a=( ujwj)-θ x=f(a) u which is usually a sigmoid function, but can be j wj j=1 Gaussian or even a simple ­linear function. The uN wN result is either fed forward to other neurons in the network or becomes the ­network’s output. Bioclimatic Models in Entomology, Figure 37 The complex network algorithm adjusts the Comparison of a biological and artificial neuron. Biogeography B 481 responses to climate, they can provide important ­organized into two sub-disciplines, historical information to guide and inform decisions when biogeography and ecological biogeography, more detailed data are lacking. Additionally, although there is overlap between the two. His- many approaches, if correctly applied, have torical biogeography is “big picture” biogeogra- potential for knowledge discovery that will phy. It is concerned with explaining patterns in increase our ­scientific understanding of how a the distributions of organisms (usually at higher range of abiotic variables can influence the dis- taxonomic levels) using the geological history of tribution and ­abundance of insects. the Earth. Historical biogeo­graphy often involves large, even global, areas, and frequently deals References with extinct taxa. Ecological ­biogeography, on the other hand, examines interactions among organisms and their environment to explain spa- Worner SP (1998) Some problems and approaches to modelling insect phenology. In: Baumgärtner J, tial distribution patterns, usually at species and Brandmayr P, Manly BFJ (eds) Important aspects in sub-specific levels. The spatial and temporal ­population ecology. Proc 20th Int Congr Entomol, scales are generally smaller in scope than is the Florence, Italy, August 25–31, 1997, A. A. Balkema, The Netherlands, pp 89–98 case with historical biogeography. As the above Heikkinen RK, Luoto M, Araújo MB, Virkkala R, Thuiller W, definitions suggest, biogeography is a highly Sykes MT (2006) Methods and uncertainties in biocli- interdisciplinary science, drawing on evolution- matic envelope modelling under climate change. Prog ary biology and systematics, ecology, and the Phys Geog 30:1–27 earth sciences. Biogeography is a young disci- pline, first beginning to coalesce into a distinct science in the mid-1900s. The first scientific peri- Biocontrol odical devoted to the discipline, the Journal of Biogeography, first appeared in 1973. The num- An abbreviation for “biological control.” ber of books and ­journal articles devoted to some aspect of biogeo­graphy has increased dramati- cally in the last few decades. But while it only Biogeographic Realms recently emerged as a distinct science, biogeogra- phy as a field of endeavor has been practiced for centuries, and many of the greatest scientists of Dissimilar distributions of animals (and therefore their time were biogeographers, though they may best called zoogeographic realms). The animals not have referred to ­themselves as such. are usually isolated geographically and defined by Questions about the diversity of life and its continents, but sometimes separated by mountain distribution across the world have been asked ranges or other physiographic features. since the time of the ancient Greek philosophers,  Zoogeographic Realms and probably before. But the flowering of ­eighteenth century exploration greatly expanded knowledge of biological diversity and led to a Biogeography ­corresponding increase in attempts to explain the patterns seen in this diversity. At that time, kenneth w. mccravy explanations were hindered by the prevailing lit- Western Illinois University, Macomb, IL, USA eral acceptance of the Bible, and Carolus Lin- naeus (1707–1778) himself wrestled with the Biogeography is the study of spatial patterns contradictions between present-day patterns of of biological diversity. Biogeography is often global ­biodiversity and biblical literalism. 482 B Biogeography For instance, Linnaeus hypothesized a “paradi- selection developed by Charles Darwin (1809–1882) siacal mountain” to explain the spread of species and Alfred Russel Wallace (1823–1913) was criti- from Noah’s point of landing. This mountain cal in providing an explanation for the adaptation would have all the different­ environments of the and diversification of organisms across time and Earth at different latitudes, which were colonized space. Wallace would devote his life to the study of by the different animals as they left the Ark. biogeography, and would become known as the These animals would then be well-suited to colo- “father of zoogeography.” He wrote three seminal nize their respective habitats as they migrated books, and developed detailed maps of the Earth’s throughout the world. While these ideas may biogeographic regions. He was also the first to note seem naive in hindsight, Linnaeus’ logic was the sharp division between Southeast Asian and astute, and his efforts in recording the type of Australasian faunas in the East Indies, a division environment in which each species was found that is now known as Wallace’s line. Many of the can be considered a precursor of the sub-­ principles proposed by Wallace are still active discipline of ecological biogeography. areas of current research among today’s biogeo­ The French naturalist Georges Buffon graphers. It is difficult to overestimate the contri- (1707–1788) was among the earliest to seriously butions of Alfred Russel Wallace to the science of consider that the earth’s climate, species, and even biogeography. British zoologist Philip Lutley the position of the continents were not fixed, but Sclater (1829–1913) was also an important figure mutable. He observed that environmentally ­similar in early efforts to define the Earth’s biogeographic but separated regions have distinct faunas, an realms. Earlier attempts to define biogeographic insight that became known as Buffon’s Law. regions were based to a great extent on artificial Attempts to explain Buffon’s Law would occupy boundaries, and Sclater felt that these maps were the attention of naturalists for decades, and would too arbitrary. His goal was to develop a system require an acceptance of the dynamic nature of reflecting “the most natural primary ontological the Earth and its species. The German botanists divisions of the Earth’s surface,” based on biotic Johann Reinhold Forster (1729–1798), Karl similarity and dissimilarity. Being an ornithologist, ­Willdenow (1765–1812), and Alexander von he based his system on passerine birds. His system Humboldt (1769–1859) collected innumerable of biogeographic regions, with some ­revisions, is plant specimens from around the globe, and found still in use today (Fig. 38). that Buffon’s Law applied to plants as well as Despite the efforts of these and other early ­animals. Von Humboldt is generally recognized as biogeographers, explanations of the disjunct the “father of phytogeography.” The Swiss botanist ­distributions of many plant and animal groups, Augustin de Candolle (1778–1841) recognized particularly in the southern hemisphere, remained distinct phytogeographic regions, and was the first elusive. This was due in large part to the fact that to coin the word “endemic.” biogeographers were preoccupied with mecha- New discoveries in geology and paleontology nisms by which the organisms themselves might would provide a framework for further advances have dispersed across the continents. But the idea in biogeography. The eminent geologist Charles that continents might move, or drift, relative to Lyell (1797–1875) and others used the fossil record one another over geological time was even more as evidence of the mutability of the Earth’s climate difficult for the scientific community to accept. and sea levels, and asserted the antiquity of the This was despite the fact that much geological, Earth. The biblically based time frame of a paleontological, and biogeographical evidence ­few-thousand-years-old Earth was difficult to supported a dynamic Earth with moving conti- ­reconcile with observed biogeographic patterns. nents. For instance, the disjunct southern distri- The revolutionary theory of evolution by natural butions of groups such as the temperate ground Biogeography B 483 beetle tribe Migadopini were difficult to explain ­dispersalist models, which were considered less using dispersal models or short-lived land bridges, testable than the vicariance models. but fit well with a Gondwanaland scenario. Famed evolutionary biologist Ernst Mayr’s Based on evidence from a variety of fields, the (1904–2005) studies of geographic distributions German meteorologist Alfred Wegener (1880–1930) and speciation were instrumental in fostering a ­developed the theory of continental drift in the synthesis between evolutionary biology and early 1900s. However, his ideas were largely ­biogeography, as was the work of German rejected by scientists initially. There were a variety ­entomologist Willi Hennig (1913–1976). Hennig of reasons for this, the most important being the developed the methods of phylogenetic system- lack of a known mechanism by which continents atics, or cladistics, which provided a rigorous could move. But the overwhelming evidence for framework for testing hypotheses of evolution- seafloor spreading and plate tectonics amassed by ary relatedness. Cladistics adheres strictly to the 1960s vindicated Wegener by providing just ­classifications reflecting natural phylogeny, based such a mechanism. on the sequence of branching as reflected by During the last half-century, the study of shared derived character states. This approach ­historical biogeography has been bolstered by fits well with vicariance-based biogeographical increased methodological rigor in biogeographical methods. Development of molecular-based analysis. Botanist Leon Croizat (1894–1982) approaches and their application to biogeograph- ­developed the method of “panbiogeography” ical problems has also led to significant advances. largely in response to what he believed was an The 1980s saw the development of the field of over-reliance on difficult-to-test dispersal models phylogeography, which has revolutionized bio- of geographic distributions. Croizat connected the geographical analysis. This approach seeks to known distributions of taxa with lines, or “tracks” explain recently occurring evolutionary relation- and then combined corresponding tracks into ships and geographical patterns at the level of “generalized tracks.” Croizat asserted that it would species and species complexes, using molecular be unlikely that several taxa, with different disper- approaches to produce “gene trees” that reflect sal capabilities and ecological requirements, would the spread of lineages. exhibit the same dispersal patterns. He reasoned Probably the most influential work in ecologi- that these distributions were established before cal biogeography in the last half-century was being interrupted by geographic barriers such as ­Robert H. MacArthur (1930–1972) and Edward O. oceans. These explanations required hypothetical Wilson’s theory of island biogeography, unveiled in land bridges and drifting of islands, which most the 1960s. Interestingly (and sadly), an earlier form biogeographers considered unrealistic. Further- of this seminal theory was independently devel- more, Croizat never really accepted Wegener’s oped by lepidopterist Eugene G. Munroe in the theory of plate tectonics, even though it would 1940s but, for a variety of reasons, Munroe’s work have provided reasonable explanations for many in this area has remained virtually unnoticed. The of the patterns Croizat observed. Although theory of island biogeography questioned the ­Croizat’s panbiogeography never gained a wide ­long-held view that species diversity and distribu- following among biogeographers, he was a pioneer tions on islands necessarily changed slowly, over in emphasizing the importance of geographic evolutionary time. MacArthur and Wilson asserted ­isolation, or “vicariance,” in speciation. General that the number of species found on islands was a acceptance of the theory of plate tectonics by the result of more proximal factors – rates of immigra- biogeographical community gave a further boost tion and extinction, which in turn are affected to the importance of vicariant events in explaining by island size and distance from the mainland. geographic distributions, at the expense of These ideas provided a much needed theoretical 484 B Biogeography ­framework for the study of biota not only on oce- Insect Biogeography anic islands, but on isolated terrestrial habitat islands as well. The theory of island biogeography Many important contributions to our biogeo- has also had a profound effect on the field of con- graphical knowledge base have been made by servation biology. David Quammen’s excellent entomologists. Many of these contributions book, Song of the Dodo: Island Biogeography in revolve around applications in pest insect control, an Age of Extinctions, provides insight into the such as studies of the migration patterns of the development of the theory and its implications African migratory locust and range expansions of for conservation ­biology, as well as criticisms of the gypsy moth, Africanized “killer” bees, and fire the theory. For some fascinating ideas in the area ants in the United States. In addition, many of human ­biogeography and the geographical pat- ­dramatic range contractions and extinctions, terns of wealth and power, see Jared Diamond’s involving a variety of plant and animal groups, Guns, Germs, and Steel: The Fates of Human have been caused by introduced insect vectors of ­Societies and Collapse: How Societies Choose to plant and animal diseases, or introductions of the Fail or Succeed. causative agents themselves. The introduction of

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Biogeography, Figure 38 Global biogeographic kingdoms and regions based on modern biogeographic analyses. This is more detailed than the original Sclater-Wallace portrayals and is not yet widely used. Numerical designations: 1–2, Holarctic kingdom (= Laurasia); 1, Nearctic region; 2, Palearctic region; 3–6, Holotropical kingdom (= eastern Gondwana); 3, Neotropical region; 4, Afrotropical region; 5, Oriental region; 6, Australotropical region; 7–12, Austral kingdom (= western Gondwana); 7, Andean region; 8, Cape or Afrotemperate region; 9, Antarctic region; 10, Neoguinean region; 11, Australotemperate region; 12, Neozelandic region (after Morrone 2002, J Biogegr 29:149–152). Biogeography B 485 mosquito-borne avian malaria in Hawaii has not appear to correlate with obvious human impacts ­devastated many species of lower-elevation birds such as habitat alteration. However, surveys of this there. The American elm, once a prominent part of species have shown that local extinctions have taken North American landscapes, has been virtually place primarily at low-­altitude and low-­latitude extirpated by Dutch elm disease. The introduced locations, as would be expected if increased smaller European elm bark beetle is a primary ­temperatures were an important cause. vector of the Dutch elm fungus. As mentioned earlier, some of the most Other studies have a strong insect conserva- important theoretical advances in biogeography tion slant, such as analyses of the range collapse of have involved entomologists and the study of the American burying beetle. This insect was insects. Willi Hennig, the founder of phylogenetic ­distributed over most of the eastern United States systematics or cladistics, was a dipterist who pro- until the mid-1900s, but is now restricted to a few duced many important works in the area of fly sys- widely separated locations in Nebraska and South tematics. Hennig was drafted into the German army Dakota, Oklahoma and Arkansas, and the northeast ­during World War II, and did some of his system- (Fig. 39). Evidence for impacts of global climate atics work while held as a prisoner of war. Another change on biotic distributions has been provided entomologist, Lars Brundin (1907–1993), studied through analyses of insect distributions, such as southern hemisphere chironomid midges. He was that of Edith’s checkerspot butterfly, a species that a pioneer in the use of cladistics in biogeographical ranges along the coast of western North America analysis. Brundin produced a cladogram reflecting from Canada to Mexico. Declines of this species do the evolutionary relationships of his chironomid

Biogeography, Figure 39 Range decline of the American burying beetle, Nicrophorus americanus ­(Coleoptera: Silphidae). The original range is indicated by dark shading, the existing range by the small unshaded areas designated by arrows. 486 B Biogeography species. He then inserted the name of the continent the most isolated island had the fewest species, on which each species is found. This resulted in a and the lowest recolonization rate. However, other “taxon-area cladogram.” The sequence of diver- studies have not supported the theory, and the gence of the chironomid species corresponded well theory has been criticized for a variety of reasons, with the sequence of the separation of Gondwana such as lack of consideration for the biology of the into the southern continents (Africa was the first organisms and their ecological and evolutionary continent to break away, and the ­African species interactions. For instance, it has been suggested were the first to diverge, etc.). Thus, systematic and that very small organisms, such as many insects, biogeographical evidence reinforced each other. would be unlikely to reach saturation population Among other things, this work showed that ­geological levels on any but the smallest of islands. So, for information could be used to suggest which of several most islands within the size range that humans plausible cladograms is likely correct. consider important, the theory may only apply to Ecological biogeography has also benefited organisms of larger size, such as vertebrates. greatly from entomological research. Ecologist As is the case in other sciences, biogeogra- Robert MacArthur and entomologist Edward phers are constantly searching for patterns in O. Wilson developed the groundbreaking theory nature. Many have been discovered, and, often, of island biogeography. The major tenets of the insects play important roles in providing data in ­theory, in highly simplified form, are: (i) an island support of, or as exceptions to, these patterns. It will contain an equilibrium number of species, has been observed in many groups of plants and (ii) this equilibrium number is a function of the animals that species diversity increases as one balance of two processes, immigration and extinc- ­progresses from the higher latitudes to the tropical tion, and (iii) immigration and extinction rates are regions. Several theoretical explanations for this in turn a function of the size of the island, and pattern have been proposed. Many insect groups the distance of the island from the mainland. fit this pattern. However, some do not. These MacArthur and Wilson reasoned that small islands exceptions include two huge families of parasitic will have higher extinction rates than large islands, wasps, the Ichneumonidae and Braconidae, as well because populations of species on smaller as the sawflies and aphids. There are many possible islands will be smaller and thus more likely to reasons for these exceptions. It has been suggested become extinct. Likewise, islands far from the that aphids are more diverse in temperate regions mainland will have lower immigration rates than because many aphid species are specialist feeders islands near the mainland. Therefore, small, far that have difficulty locating suitable host plants islands will have low equilibrium numbers of species, from long distances. Therefore, they should fare and large, near islands will have larger equilibrium better in regions where plant species are clumped, numbers of species. such as the agricultural lands of temperate regions, Wilson, with his student Daniel Simberloff, than in tropical regions where plant assemblages also provided an early rigorous test of the theory consist of many species that are each present at through experimental defaunation studies on low densities. As is often the case, it is the excep- small mangrove islands in the Florida Keys. In this tions to the rule that provide the most interesting study, methyl bromide was used to kill all insects research questions. and other terrestrial arthropods on the islands. Another interesting biogeographical pattern Follow-up surveys were then done to monitor has been termed “geographic parthenogenesis.” recolonization of the islands. Several aspects of ­Parthenogenesis is the production of offspring the theory were supported. After defaunation, the from unfertilized eggs, usually with the asexu- islands did eventually return to roughly their orig- ally produced offspring being female. “Geographic inal numbers of arthropod species. In addition, parthenogenesis” refers to a pattern in which Biological Clock B 487 ­parthenogenetic organisms occupy different geo- Lomolino MV, Riddle BR, Brown JH (2006) Biogeography, graphic ranges than their closely related, sexually 3rd edn. Sinauer Associates, Sunderland, MA, 845 pp Lomolino MV, Sax DF, Brown JH (eds) (2004) Foundations reproducing relatives. The parthenogens are often of biogeography: classic papers with commentaries. associated with what could be considered “marginal” ­University of Chicago Press, Chicago, IL, 1291 pp habitats. These include more northerly latitudes, Quammen D (1996) The song of the dodo: island biogeo­ higher altitudes, disturbed habitats, islands or island- graphy in an age of extinctions. Scribner, New York, 702 pp like patches of habitat, or dry environments. Such patterns have been observed in many insect groups. One interesting example is Pelecinus ­polyturator, a parasitic wasp with a huge latitudinal geographic Bioinformatics range that extends from eastern and central North America, through the southwestern U.S. and Central Researchers in bioinformatics develop computer America, down through South America to Argen- software applications that can store, compare and tina. Pelecinus polyturator exhibits patterns consis- analyze the very large quantities of DNA sequence tent with geographic ­parthenogenesis. In the data generated by the new genome technologies. northern part of its range males are extremely rare, New bioinformatics tools can sift through a mass but in tropical regions males are abundant and of raw data, finding and extracting relevant infor- ­sexual reproduction is apparently common. Insect mation and their relationships. species in other groups, including mayflies, aphids,  Genomics and stick insects, have also been found to exhibit  Functional Genomics ­geographic parthenogenesis.  Structural Genomics For centuries now, biogeographers have ­provided fascinating insights into the patterns and processes of the natural world. As human-caused Biointensive Pest Management changes continue to affect global biodiversity, it will be critical that we increase our knowledge of Biologically based pest management. Pest man- the factors determining the geographic distri­ agement that depends on an understanding of pest butions of organisms. The science of biogeo­graphy biology to prevent pests from causing damage, or will continue to be at the forefront of these efforts. uses biological agents to suppress pests.  Zoogeographic Realms  Integrated Pest Management  Pelecinid Wasps Biological Amplification References The accumulation and increase in concentration Avise JC (2000) Phylogeography: The history and formation of species. Harvard University Press, Cambridge, MA, of chemicals, usually insecticides or their metabo- 447 pp lites, in organisms at higher trophic levels. Cox CB, Moore PD (2005) Biogeography: an ecological and  Biomagnification evolutionary approach, 7th edn. Blackwell, Malden, MA, 428 pp Diamond JM (2005) Collapse: how societies choose to fail or succeed. Viking, New York, 575 pp Biological Clock Diamond JM (1997) Guns, germs, and steel: the fates of human societies. W. W. Norton, New York, 512 pp The biological/physiological timing device inside Lomolino MV, Heaney LR (2004) Frontiers of biogeography: new directions in the geography of nature. Sinauer an organism that allows it to establish regular Associates, Sunderland, MA, 436 pp ­biological rhythms. It is self-sustained, but 488 B Biological Clock of the German Cockroach, Blattella Germanica (L.) ­synchronized by natural biological patterns such self-sustained, endogenous clock is easily entrained as light and dark cycles. (synchronized) by environmental signals such as  Biological Clock of the German Cockroach light-dark cycles, temperature cycles, and other environmental changes, and allows an organism to adapt to its environment properly in time. Such an Biological Clock of the German environmental time signal has been called a “Zeit- Cockroach, Blattella Germanica geber” (from the German for “time-giver”). (L.) There are several lengths of rhythmic period on earth, such as half-day tidal cycles, day-night how-jing lee cycles, semilunar and lunar cycles, annual cycles, National Taiwan University, Taipei, Taiwan and seasonal cycles that are caused by the move- ments of sun, earth and moon. Since these predict- Have you had a terrifying experience of seeing an able environmental changes are consistent events, oily flat creature running for cover when you open organisms depend on their endogenous clocks to a cupboard to look for a midnight snack? Even synchronize with the rhythmic changes of environ- worse, while you are watching TV a cockroach ment. Among various lengthened environmental runs swiftly under your feet to reach the other end cycles, the daily cycle is the most prominent and of sofa! This tiny crawler is no stranger to us. It is universal environmental condition to influence the our unwanted and unavoidable housemate, the survival of organisms. From primitive prokaryotic German cockroach. single-cell cyanobateria to highly evolved eukary- The German cockroach, Blattella germanica otic mammals, virtually all organisms possess an (L.) is a cosmopolitan species and well-adapted to endogenous circadian clock (the term “circadian” is human shelters such as houses, buildings, and fac- derived from the Latin for “about a day”). Therefore, tories, and sometimes it is even found on public many scientists focus their research interests on transportation. They feed on almost any organic ­circadian clocks. matter. Although no life threatening disease is transmitted by them, the existence of the German cockroach poses a health threat to humans (allergy, Characters of Circadian Clocks diarrhea) and represents deteriorating hygiene. Since we live with the German cockroach The most important characteristics of a circadian under the same roof, our daily life coincides with clock are: (i) a self-sustained oscillator with a its activities. We rarely see them during daytime, period close to 24 h, (ii) a free-running rhythm but we encounter them frequently at night. Do under constant environmental conditions (such as they avoid their only natural enemy, humans, constant temperature and continuous light or dark ­during the day, or is their activity schedule condition), and (iii) temperature-compensation. ­controlled by a biological clock? The scientific evi- The first two characters are the essential ones that dence shows that timing of its activity is scheduled should be used as the definition of the circadian according to its endogenous biological clock. clock. When we remove all the environmental time signals from an organism, it should follow its own endogenous circadian clock and express an approx- What Is a Biological Clock? imate, but not exact 24 h rhythm. Only when this free-running rhythm is expressed under an artifi- A biological clock is a timing device inside an cial, constant condition, can we definitely infer a organism to give time signals so that an organism circadian clock in this organism. The third charac- can perform proper behaviors at the right time. This ter is the key feature to allow the clock to run as Biological Clock of the German Cockroach, Blattella Germanica (L.) B 489 accurately as possible in different seasons or and TIMELESS ­proteins in the cytoplasm of cells. ­temperature conditions. Since the speed of all The phosphorylation of PERIOD enables it to bind ­biochemical processes within an organism depends with TIMELESS to form a heterodimer, which in on the temperature, the property of temperature turn translocates into the nucleus to inhibit compensation can keep the molecular biological ­further transcription of period and timeless genes. clock running in a constant pace regardless of When the diminishing concentration of PER-TIM ­environmental temperature fluctuation. This ­heterodimer reaches a certain low level, the period ­character is especially essential in ectothermal and timeless genes will be reactivated and cause ­animals, those which depend on external ­conditions another cycle. This process takes about 24 h lag to maintain their body temperature (Fig. 40). time. Light can degrade the TIMELESS protein. If there is reduced TIMELESS available to bind PERIOD, then there is more delay of inhibition Molecular Clock Mechanisms on the two clock genes, which prolongs the cycle and changes the clock phase. This molecular The biological clock operates in a negative feed mechanism explains the synchronization of cir- back loop composed of various molecules. cadian clock phases with the light-dark cycles of Although no universal scheme of molecular clock the environment(Fig. 41). exists in all organisms, the molecular clock mecha- nisms in the fruitfly Drosophila melanogaster underlie the clockwork of the German cockroach. Ecological Significance The simplified molecular clock scheme includes two clock genes, period and timeless, which are The ecological function of biological clocks is activated and transcribed-translated to PERIOD the main reason these clocks occur in various

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Biological Clock of the German Cockroach, Blattella Germanica (L.), Figure 40 The locomotor ­activities of a male adult German cockroach at 28°C, 12L:12D cycles for 5 days then switched to constant­ darkness conditions. Each horizontal line shows 24 h, with each day attached below the previous­ day. A vertical line indicates the onset of locomotion. The shaded areas of the actogram represent darkness. The superimposed line across the actogram represents the predicted onset time of the locomotion according to its circadian period (τDD = 23.5 h) (modified from Lin and Lee, 1996). 490 B Biological Clock of the German Cockroach, Blattella Germanica (L.)

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3.00.0 0 80 Length of oocytes (mm) Successful mating (%) Biological Clock of the German Cockroach, Blattella Germanica (L.), Figure 41 The locomotor activities of a virgin female adult German cockroach at 28°C, 12L:12D cycles for 5 days then switched to constant darkness conditions. Daily development of ovaries represented by the length of oocytes is shown on the left side of the actogram. The mating window for a virgin female is displayed on the right side of the actogram. Other symbols as above (modified from Lee and Wu, 1994; Lin and Lee, 1996).

­organisms across five kingdoms. We can identify Natural selection has shaped the proper the three most important ecological functions of a behaviors of organisms to act in the right place at ­circadian clock: (i) the timing of each behavior is so the right time. Good timing is certainly involved important that every organism within a species in life and death decision-making processes. An should time each movement very accurately. This is endogenous circadian clock is definitely a key asset the key function an endogenous circadian clock can to survive and prosper for the species. provide. (ii) Although most environmental changes are fairly rhythmic and predictable, some condi- tions (such as continual raining, sudden cold or Biological Clock of the German heat) might cause long lasting interruption on envi- Cockroach ronmental rhythmicity. These unpredictable envi- ronmental changes may last a few days and cause With some background information about organisms to perform behaviors solely depending ­biological clocks, we can turn our attention to the on their circadian clock for good ­timing. (iii) Every circadian clock of the German cockroach. Since it day is a new challenge for an organism. The active would be difficult to actually see the working clock tasks ahead require good preparation in physiologi- in a multi-cellular animal, a circadian rhythmic cal conditions to overcome challenges. In order to behavior or physiological parameter can be be well-prepared for the challenge, organisms selected and monitored as the overt expression of depend on their circadian clock to trigger the whole the endogenous clock. The locomotor circadian cascade of reactions. The physiological preparation rhythm is chosen as the focal point of this article. in organisms occurs in the rest phase of the daily The German cockroach is a nocturnal insect, cycles. A ­circadian clock can provide good timing and its locomotor activities mainly occur during to start preparation and achieve survival in danger- the scotophase (dark phase) of the daily photope- ridden environments. riod condition. Once the light-dark cycles are Biological Clock of the German Cockroach, Blattella Germanica (L.) B 491 ­artificially changed to constant darkness condition, and that the locomotor pattern of female adults a male adult’s free-running rhythm continues to does not display a circadian rhythmicity. regulate locomotion for greater activity during the Since possessing a circadian clock is a genetic time that would represent scotophase in light-dark trait for the species, female adults should also have cycles. The circadian period of the male adult is a circadian clock underlying their arrhythmic approximately 23.5 h. From this activity pattern, locomotion. When the ovaries are surgically we know there is an endogenous clock driving its removed during the last instar, they express a loco- locomotion in circadian rhythmicity. motor circadian rhythm of 23.6 h, the same as When female adults are put into the same con- found in male adults (Fig. 42). This circadian dition, their locomotion does not show a circadian rhythmicity also can be seen in starving female rhythm. Their locomotion is concentrated to the adults whose ovaries do not develop. The locomo- few days before the formation of ootheca (egg tor circadian rhythm of females is masked by the case), and activity is distributed relatively evenly endogenous development of ovaries. This masking across the 24 h period. This locomotor pattern effect is a unique characteristic of the biological coincides with the developmental cycles of ovaries. clock in the German cockroach. When the ovaries reach at certain developmental A critical function of the circadian clock in stage, female adults become active. Their locomo- reproductive behavior is to provide good timing tion even occurs during the day, clearly counter to for bringing potential mates together. However, the nocturnal nature of the species. In addition, why does the timing of mate-finding behavior not this locomotor pattern coincides with the narrow synchronize between the sexes of the German mating-window of the females. When the females cockroach? This question certainly implies that become sexually receptive, their daily locomotion the masked circadian rhythm of female adults increases significantly. Once the females mate, their does not impair the chances of meeting males. It locomotion decreases immediately. We conclude requires a detailed analysis of the reproductive that locomotion represents mate-finding activities strategies of the German cockroach to unveil the

0612 18 24

Age (days)

5

10

15

20

Biological Clock of the German Cockroach, ­Blattella Germanica (L.), Figure 42 The locomotor ­activities of an ovariectomized female adult ­German cockroach at 28°C, 12L:12D cycles for 5 days then switched to constant darkness conditions. The circadian period is calculated as 23.6 h. Other symbols as above (modified from Lin and Lee, 1996). 492 B Biological Clock of the German Cockroach, Blattella Germanica (L.) mystery of endogenous masking effects on the sexually mature females release sex pheromone to locomotor circadian rhythm. attract males. Combining these two mechanisms, Although German cockroaches are not social the female adults try to mate in time. insects, they do live in groups. The groups are These complicated reproductive strategies composed of immature and adult cockroaches of guarantee the survival and propagation of the both sexes, and are maintained by an aggregation species. In fact, the high priority of reproduction pheromone secreted by every individual. This style causes a unique masking effect on the mate-finding of living provides easy opportunity for both sexes locomotion of the female. This arrhythmic ­loco- to meet when they are sexually mature. Thus, the motion is the result of high demand on mate-finding timing of mate-finding locomotion becomes less locomotion during the sexually receptive period critical in comparison with solitary cockroach of female adults. Underneath this arrhythmic species. The masked locomotor circadian rhythm locomotion, however, an endogenous circadian does not handicap the chances of mating pair-­ clock paces daily locomotion. formation. Random (Fig. 43) mate-finding is largely dependant upon group living and is the primary strategy of the species. Conclusion Since female adults produce an ootheca regardless of their mating status, the nutrient-rich The biological clock of the German cockroach runs oothecae is wasted when the females do not mate continuously in both sexes. It drives locomotion during the narrow mating-window. The penalty to express circadian rhythm in male adults, but for losing the mating opportunity is severe enough adult females fail to show circadian rhythmicity. to drive female adults into locomotion to find An endogenous masking factor caused by the mates regardless the time of the day. The masked developing ovaries obscures the overt rhythm of locomotor circadian rhythm, therefore, reflects locomotion in females. Although this desynchro- the high importance of mate-finding. In addition, nizing locomotion does not fit into the mode of

mating

male

mating Increasing

male loc motion male

Calling behavior (releasing sex pheromone) female female

Primary strategy Secondary strategy mating

Biological Clock of the German Cockroach, Blattella Germanica (L.), Figure 43 Mating scheme for the German cockroach (modified from Tsai and Lee, 1997). Biological Control by Neoseiulus Californicus (McGregor) (Acari: Phytoseiidae) B 493 function for a circadian clock, the masked arrhythmic Biological Control by Neoseiulus locomotion becomes part of reproductive strategy californicus (McGregor) (Acari: that ensures a mating opportunity for sexually Phytoseiidae) mature females. norma e. sánchez, nancy, m. greco, claudia v. cédola References Universidad Nacional de La Plata, La Plata ­Argentina Enright JT (1970) Ecological aspects of endogenous rhyth- micity. Ann Rev Ecol Syst 1:221–238 Neoseiulus californicus is a predator mite that pro- Lee HJ (1994) Are pregnant females of the German cockroach too heavy to run? Zool Stud 33:200–204 vides an effective biological control of Tetranychus Lee HJ, Wu YL (1994) Mating effects on the feeding and loco- spp. spider mites in strawberries, corn, grapes, roses, motion of the German cockroach, Blattella germanica. fruit trees and ornamentals. It has a worldwide Physiol Entomol 19:39–45 ­distribution in arid and humid areas, including Lin TM, Lee HJ (1996) The expression of locomotor circadian rhythm in female German cockroach, Blattella german- semi-tropical and temperate South America, and arid ica (L.). Chronobiol Int 13:81–91 areas of southern California and southern Europe. Lin TM, Lee HJ (1998) The parallel control mechanisms This predator is very small in size. The adult underlying locomotor activity and sexual receptivity measures 0.25–0.5 mm in length and is pear of female German cockroach Blattella germanica (L). J Insect Physiol 44:1039–1051 shaped and slightly orange in color. It passes Scully AL, Kay SA (2000) Time flies for Drosophila. Cell through four developmental stages (egg, larvae, 100:297–300 nymph and adult). Eggs are oval and translucent. Tsai CW, Lee HJ (1997) Volatile pheromone detection and calling behavior exhibition: secondary mate-finding At 25°C, the eggs hatch after two days. Larval and strategy of the German cockroach, Blattella germanica nymphal (proto- and deutonymph) stages require (L.). Zool Stud 36:325–332 about three days to complete development. Then, Tsai CW, Lee HJ (2000) Circadian locomotor rhythm masked it takes approximately five days to reach the adult by the female reproduction cycle in cockroaches. Phys- iol Entomol 25:63–73 stage. Adult longevity is approximately 20 days, Tsai CW, Lee HJ (2001) Analysis of specific adaptation to a and the oviposition period is 13.5 days. A female domicile habitat: a comparative study of two closely can lay three eggs a day (Fig. 44). related cockroach species. J Med Entomol 38:245–252 Neoseiulus californicus, as well as other predatory Wen HW, Lee HJ (2000) Unequal coupling between locomo- tor pacemakers of the German cockroach, Blattella mites (e.g., N. fallacis (Garman), Phytoseiulus persimilis ­germanica (L.). J Insect Physiol 46:89–97 Athias-Henriot and Mesoseiulus longipes (Evans)) is commercially produced and used to control the two-spotted spider mite, T. urticae Koch, in North American and European greenhouse horticulture. Biological Control A related species in the same genus, N. fallacis, coexists with N. californicus in the Northern The action of parasites, predators, or pathogens in ­Hemisphere. Both species are morphologically maintaining another organism’s population den- ­similar and have been rated as specialized predators sity at a lower average level than would occur in of spider mites, but N. californicus seems to be their absence. Biological control may occur natu- more generalist than N. fallacis. Pollen of different rally in the field or result from manipulation or plants such as maize, almond, castor bean, introduction of biological control agents. ­avocado, and some grasses, as well as thrips are  Augmentative Biological Control alternative food.  Classical Biological Control In South America, releases of predatory mites  Conservation Biological Control are not commonly used, and regular applications 494 B Biological Control by Neoseiulus Californicus (McGregor) (Acari: Phytoseiidae) This predator seems to be a promising natural enemy for controlling T. urticae through the imple- mentation of conservation techniques. Taking into account that the ability to tolerate acaricides is a serious constraint on successful conservation of phytoseiid predators, the reduction of unnecessary acaricide treatments may enhance persistence of predator mite populations. At present, efforts are being made to reduce the number of chemical applications through monitoring of the prey/predator ratio and pest population trend to avoid both unnecessary ­pesticide applications and economic damage. However, more field studies are needed to help elucidate other factors that contribute to increase, and to effectively preserve the natural populations of this predator in annual as well as perennial ­systems. Among these factors, plant diversity may be a critical feature to increase natural enemy ­persistence through: (i) provision of alternative prey/host at times when the pest is scarce, (ii) pro- Biological Control by Neoseiulus Californicus vision of supplementary food, and (iii) provision (McGregor) (Acari: Phytoseiidae), Figure 44 of refuge (for mating or overwintering). ­Neoseiulus californicus (McGregor). It is also known that physical and chemical characteristics of the food plants of prey can affect of acaricides are made to control pest mites. How- natural enemy potential effectiveness. A good ever, in commercial strawberry greenhouses in example of this is the negative way in which per- Argentina, N. californicus is the main established sistence of N. californicus, plant colonization, and enemy of the two-spotted spider mite. Although consumption of T. urticae are affected by tomato this predator consumes fewer prey than other leaf glandular hairs. This finding reveals the risk of phytoseiid species, it has longer survival under generalizing the effectiveness of N. californicus starvation conditions. Moreover, the ability to feed from one crop to another. on other food sources may contribute to its The implementation of conservation biological ­persistence in the absence of spider mites. This control is still receiving inadequate consideration trait may be of critical importance for the success in developing countries. The potential and utility of conservation biological control. of N. californicus as a biological control agent is Conservation biological control means the worth further investigation. environmental manipulation to protect and enhance natural enemies. This is an ecologically, environ- mentally, and economically sound ­solution to pest References problems for growers of developing countries. Recent studies in La Plata (Buenos Aires, Greco NM, Liljesthröm GG, Sánchez NE (1999) Spatial Argentina) showed that T. urticae and N. californicus ­distribution and coincidence of Neoseiulus californicus populations exhibit a high spatial coincidence and and Tetranychus urticae (Acari: Phytoseiidae, Tetrany- the predator is very efficient in locating the prey. chidae) on strawberry. Exp Appl Acarol 23:567–580 Biological Control of Invasive Plants in Latin America B 495 Ma W, Laing JE (1973) Biology, potential for increase and A frequently cited example of a successful prey consumption of Amblyseiulus chilenensis (Dosse) biological control project is the control of prickly (Acarina: Phytoseiidae). Entomophaga 18:47–60 McMurtry JA, Croft BA (1997) Life styles of phytoseiidae pear cactus, Opuntia stricta Haworth (Cactaceae) mites and their roles as biological control agents. Annu in Australia by the pyralid moth Cactoblastis Rev Entomol 42:291–321 ­cactorum Bergroth (Lepidoptera: Pyralidae) intro- Monetti LM, Croft BA (1997) Neoseiulus californicus (McGregor) and Neoseiulus fallacis (Garman): larval duced from Argentina in the 1920s. However, this responses to prey and humidity, nymphal feeding drive is also a good example of conflicting interests, as and nymphal predation on phytoseiid eggs. ExpAppl the invasive plant (cactus) is harmful in Australia Acarol 21:225–234 and biological control was needed. On the other hand, it is useful as human and animal food, and as an ornamental plant for people in other regions Biological Control of Invasive (Mexico, Caribbean, southern regions of the USA). Plants in Latin America Here, the successful biological control agent in Australia, C. cactorum, threatens the native julio medal1, maricela martínez 2 endemic cactus, so it is not regarded as a “hero” but 1University of Florida, Gainesville, FL, USA as a “pest,” and control measures including the use 2Instituto Mexicano de Tecnología del Agua of natural enemies and the sterile insect ­technique (IMTA), Jiutepec, Morelos, Mexico are being undertaken. Other well-known examples of classical bio- An invasive plant is an exotic that has been logical weed control include the effective control ­introduced, intentionally or by accident, into a new of Klamath weed and alligator weed. Klamath region where it successfully establishes, reproduces, weed or St. Johnswort, Hypericum perforatum L. and spreads, eventually replacing the native vegeta- (Clusiaceae) was controlled in the western USA by tion. Invasive plants or weeds, also called “biological two European leaf-feeding beetles, Chrysolina pollutants,” threaten natural ecosystems and human- quadrigemina (Suffrian) and Chrysolina hyperaci modified habitats by reducing biological diversity (Forster) (Coleoptera: Chrysomelidae), imported and by causing significant reductions in crop yields from Australia in the mid 1940s. In Florida, USA, and other harmful effects on property, humans, and complete biological control of alligator weed, domesticated animals. The success of the exotic Alternanthera philoxeroides (Martius) Grisebach plant to become invasive in a new geographical (Amaranthaceae) in aquatic environments was region can be partially attributed to the fact that the achieved by the introduction of the flea beetle exotic has been ­introduced without the arthropod Agasicles hygrophila Selman and Vogt (Coleoptera: natural enemies and disease-producing pathogens Chrysomelidae) from Argentina. that limit its reproduction in the area of origin. Interest in biological control of invasive plants Manual removal and herbicides are the major using host-specific insects and pathogens has invasive plant management practices currently increased in the last decade due to the public’s used in cultivated crops in Latin America. Biological ­concern about the negative effects of pesticides in control, or the use of natural enemies such as the environment, a greater demand for pesticide- arthropods, pathogens, and fish to reduce the free agricultural products, the reduction in the population and reproduction of the exotic inva- number of pesticide registrations, the development sive, has been traditionally practiced in developed of plant resistance to commonly used herbicides, countries such as the United States, Australia, and the intensified oil crisis which increases the Canada, South Africa, and New Zealand, primar- cost of using herbicides. A recent catalogue of ily in rangeland situations, conservations areas, ­biological control agents and their weeds listed 949 and aquatic systems. releases involving at least 350 organisms against 496 B Biological Control of Invasive Plants in Latin America 133 target weeds as of 1996. Forty-one (31%) of Biological Control Activities these weeds are considered under complete or Against Invasive Plants in Latin ­substantial biological control. America Biological control is not a panacea and is not without an element of risk. The advantages The use of insects and pathogens as biological of classical biological control over other invasive control agents of invasive plants in South America plant control methods are that it is highly spe- has been quite limited. Compared with the cific to the target plant, it has little or no impact advances achieved in biological control of arthro- on non-target organisms, it does not pollute the pod pests for the same region, the use of insects environment, it is relatively inexpensive, and it for control of invasive plants is in its infancy or provides self-sustaining and permanent control initial stages of development. Chile can be consid- of the invasive plant when it works. Among the ered a pioneer in this field, with biological control disadvantages of biological control of invasive activities of invasive plants initiated in 1952 against plants with introduced insects are that it is the non-native invasive Hypericum perforatum L. unpredictable, and even if the insects establish, (Clusiaceae). This project has been a great success, biological control may not suppress the invasive providing highly effective control of this weed. plant population enough to achieve the desired Other biological control projects initiated in Chile level of control. in the 1970s that had only moderate successes or Several factors make biological control with have been ineffective include Galega oficinalis L., insects especially difficult in field crops. First, Ulex europaeus L. (Rosaceae), Rubus constictus ­disturbance from planting, cultivation, and Lepeure & Mueller, and Rubus uifolius (Rosaceae). ­pesticide applications is not conducive to the Research efforts using insects or pathogens for establishment of the biological control agent. Sec- biological control of invasive plants in Chile ond, because several species of invasive plants ­continue, with more intensity in the last decade usually require control simultaneously, multiple due to enhanced funding provided by national biological control agents are needed. Finally, rapid institutions. In Argentina, there is only one case control (usually within one month of planting) is known of biological control, that of the invasive necessary in order to prevent crop damage. Once aquatic plant waterhyacinth, Eichhornia crassipes invasive plant-feeding insects establish, they are (Mart.) Solms (Pontederiaceae) in the province unlikely to build up damaging populations in a of La Rioja located in the west-central part of single field season. Highly specific plant patho- the country. The waterhyacinth-feeding weevil gens may be better suited to control invasive Neochetina bruchi Hustache (Coleoptera: Curcu- plants in field crop situations. Native plant lionidae) was introduced from the province of pathogens can be formulated and applied as Buenos Aires and it was able to reduce the aquatic bioherbicides, or exotic pathogens can provide plant infestation from 50% to 8%. effective control of the invasive plants following Biological control of aquatic invasive plants inoculative releases. Lastly is the conflicting in Mexico has been implemented with more inten- interest issue mentioned previously. A plant sity during the last decade using a combination of that is perceived as a nuisance by one group of insects and pathogens against waterhyacinth. Most people can be considered a ­beneficial plant by of the current aquatic plants have been introduced another group. Beekeepers are a good example by humans from their native habitats, and are free of a special interest group that may object from their natural enemies and diseases. Invasive- strongly to biological control because they may ness is a response to the high level of nutrients in value the ­invasive plant as a source of nectar the urban, industrial and municipal wastewater. and pollen. Aquatic invasive plants causes water loss through Biological Control of Invasive Plants in Latin America B 497 plant evapotranspiration, displacement of native (Orthoptera: Acrididae), and Orthogalumna species, public health risks, obstruction of channels ­terebrantis (Wallwork) (Acari: Galumnidae). and drains in irrigation systems, intakes to hydro- There is no evidence of them being native to electric plants, restriction to tourist, recreational Mexico, and they could have arrived with and fishing activities, and increasing sedimenta- ­waterhyacinth plants introduced in the past. The tion with subsequent shortening of the useful life Brazilian weevil N. bruchi was introduced into of the body of water. In Mexico, more than 62,000 Mexican quarantine from the USDA Aquatic ha have been infested by aquatic invasive plants. Plant Management Laboratory in Fort Lauder- The most important species are waterhyacinth, dale, Florida, USA. Although the Neochetina followed by water fern (Salvinia spp.), pondweed ­species are well established in Mexico, the effec- (Potamogeton sp.), cattail (Typha sp.), hydrilla tiveness of biological control requires the use of (Hydrilla verticillata L. Royle), waterlettuce (Pistia additional agents to complement existing ones. stratiotes L.), and duckweed (Lemma spp.). Several highly virulent waterhyacinth patho- In 1993, the Aquatic Weed Control Program gens have been collected, identified, screened for was initiated in Mexico by presidential mandate in plant host range, mass-produced, and field­evaluated response to the increasing need to control the in Mexico. After selecting two specific and highly overwhelming presence of invasive plants in the virulent fungal pathogens, Cercospora piaropi water sources. As part of this program, a biological Tharp., andAcremonium zonatum (Saw) W. Games, control project was included. In Mexico, waterhya- the combined effects of the plant pathogens and cinth is the most prolific invasive aquatic plant, the Neochetina weevils were evaluated in a seven infesting an estimated 40,000 ha of water. This ha water reservoir in the central part of Mexico plant was probably introduced in Mexico in the in the state of Morelos. A total of 9,800 weevils early 1900s. Chemical and mechanical control were released and two applications of a mixture methods have been used to manage waterhya- of the fungal pathogens were carried out. After cinth, but these methods are expensive and several three months of the combined application of the annual applications are needed. The difficulties in fungi and weevils, the reservoir was free of wate- controlling this aquatic invasive are related to the rhyacinth. The dramatic reduction in waterhya- plant’s rapid growth rate and its ability to reinfest cinth coverage was due to the increasing amount via the seed bank or by flood-borne plants. For of a natural pathogen (C. piaropi) already present these reasons, the only long-term and sustainable in the water reservoir, the introduction at the solution is the application of an integrated same time of another highly virulent pathogen approach to waterhyacinth management in which (A. zonatum) combined with the leaf feeding scars biological agents play a key role. made by the Neochetina adult weevils and stem The host-specific Brazilian weevils Neochet- damage by the Neochetina larvae. Weevil feeding ina eichhorniae Warner and Neochetina bruchi allows the transmission of the pathogens, which ­Hustache have been used in many countries results in increased disease incidence. This approach worldwide to control waterhyacinth with relative of combining insects and pathogens to get a better success. Neochetina eichhorniae was introduced control of an invasive aquatic plant is currently to Mexico from the US in the late 1970s. How- implemented by the Instituto Mexicano de ever, other reports indicated its presence in some ­Tecnología del Agua in different regions of Mexico. Mexican water bodies as early as 1967. Another In Honduras, a limited number of biological three ­waterhyacinth insects that have been control activities against waterhyacinth were observed occurring naturally in Mexican water initiated in the 1990s. The Neochetina weevils ­bodies are ­Sameodes albigutalis (Warren) (Lepi- were introduced and released in a body of water dopera: Pyralidae), Cornops aquaticum (Bruner) at the Pan-American Agricultural University 498 B Biological Control of Invasive Plants in Latin America “El Zamorano” located 20 miles east of Tegucigalpa. world, mainly Australia, Canada, the continental Control of waterhyacinth has been a complete United States and Hawaii, New Zealand, India, and ­success in this body of water through the combined several African counties, principally South Africa. effect of the Neochetina and manual removal of the The three countries from which most of the fewer and smaller plants damaged by the feeding of ­biological control agents have been exported the adult/larvae stages of the weevil. are Mexico (42 species or 33.1% of the total In 2005, some biological control activities exported), Brazil (30 species or 23.6% of the against aquatic invasive plants were initiated in total), and Argentina (20 species or 15.8% of Nicaragua. Aquatic systems have been sampled to the total). This trend has continued into this determine the arthropods fauna associated with ­century and is supported by local personnel and waterhyacinth and waterlettuce, which invades institutions (e.g., USDA-ARS ­Bio­logical Control several lakes and rivers in Nicaragua, preventing Laboratory in Hurlingham, ­Argentina) established fishing, navigation, and running of the hydroelectric by foreign countries that have invasive plants plants that provide electricity to a large part of the native to South America. country. A new species of Cornops sp. (Orthoptera: Acrididae) was found feeding heavily on waterhy- acinth, and host-specificity range studies are being Limitations on the Implementation undertaken. of Biological Control of Invasive The first biological control activity in Brazil Plants in Latin America against a non-native invasive plant, Tecoma stans (Bignoniaceae) was initiated in 2000. This medi- Among the main limitations to carrying out um-size tree is originally from the southern USA, ­biological control projects against invasive plants Mexico and Central America, and it is invasive in in South America is the limited number of uplands and pasture areas in southern ­Brazil (the ­technical personnel with training in this disci- states of Paraná and Rio Grande do Sul) where it pline. Some efforts of training in this field were replaces native vegetation. The rust fungusProspo - initiated by the University of Florida in cooperation dium appendiculatum (G. Winter) Arthur was with the ­Universidad Nacional Agraria of Nicara- found attacking this plant in southern Brazil, and gua, the ­Instituto de Investigaciones Agropecuarias no other potential specific agents has been found of Temuco, Chile, and the USDA-ARS South Ameri- in field explorations conducted in recent years. can Biological Control Laboratory of Hurlingham, Initial foreign exploration in the area of origin Argentina. Three intensive weed biological control (Nicaragua, Costa Rica) of T. stans was conducted courses were given in Nicaragua during June 2002, for several days in June 2006 and ­several potential 2004, and 2006 with 78, 51, and 46 participants, natural enemies were collected on the plant. Addi- respectively. This kind of training is necessary to tional field explorations are planned once funds prepare the personnel required for the implemen- become available. tation of biological control ­programs in the region. Another important factor that limits the imple- Exportation of Latin American mentation of invasive plant biological ­control Biological Control Agents ­projects is the limited availability quarantine ­facilities that exist in the region. However, most of the South Contrary to the limited importation of biological American countries already have quarantine control agents into Central and South American ­facilities for the introduction of parasites/predators countries, as of the late 1900s, 127 insect species had for biological ­control of arthropod pests. These been exported and used in other regions of the installations could be modified and adapted for the Biological Control of Invasive Plants in Latin America B 499 introduction of ­biological control agents of invasive Bidens pilosa L. (Compositae; common name plants. Countries that have quarantines to handle “mozote”); Coniza bonariensis (L.) Cronq., (Aster- natural enemies of invasive plants include Brazil, aceae; common name “varilla,” distribution tropical Argentina, and Chile. America); Cyperus rotundus L. (Cyperaceae; known A third and very important limiting factor is as “coyolillo” in Central America, “coquito” in the lack of funds. Economic resources for any ­Colombia); Desmodium tortosum (Swarts) Dc., type of agricultural research are scarce and (Fabaceae; known in Central America as “pega- ­competition for grants is highly competitive. The pega”);­ ­Echinocloa colona (L.) Link (Poaceae; known funding required to initiate a new project for as “arroz de monte” or “arrocillo,” plant originally ­biological control of invasive plants is relatively from Eurasia and very common in South American high. Nevertheless, the ecological and/or rice fields);Eichhornia crassipes (Pontederiaceae; com- ­economic benefits that will be obtained if agents mon name “jacinto de agua,” “lirio de agua,” or “lirio become established and successful are quite acuático”); Eragrostis plana Nees (Poaceae; common substantial. name in Brazil “capim annoni”); Pistia stratiotes (Araceae; known as “lechuga de agua” in Central America and “alfaça de agua” in Brazil); Portulaca Potential for Biological Control of oleraceae L. (Portulacaceae; known as “verdolaga” in Invasive Plants in Latin America Central America), Richardia scabra L. (Rubiaceae; common name “botoncillo”); Ricinus communis L. The successes with biological control of invasive (Euphorbiaceae; highly toxic plant known in South plants in conservation areas, agricultural situations, America as “castor” or “higuerilla”); Rottboellia and aquatic systems obtained in other countries cochinchinensis (Lour) Chyton (Poaceae; known in could be duplicated in Central and South America. Central America and in the Caribbean as “la camina- The diversity and complexity of the agricultural dora”); Sida acuta Burn. f. (Malvaceae; known as practices by South American farmers suggest that “escobilla negra”); Solanum torvum Swarts (Solanaceae, management of invasive plants should be biologi- a spiny bush common in South America known as cally based (biological control using native or “lava platos” or “huevo de gato,” a name also applied introduced insects and/or pathogens) and inte- to various species of Solanum); Sorghum halepense grated with conventional control methods. For (L.) Pers. (Poaceae; known as “grama Johnson”); example, cultural practices (plant density, non- Taraxacum officinale Weber (Asteraceae; originally tillage, intercropping, crop rotation, organic agri- from Europe and known in South America as culture) that contribute to preservation of natural “lechuguilla”); Tecoma stans (L.) Kunth ex HBK. enemies of the invasive plants should be encour- (Bignoniaceae, known as “guabillo” in Central aged. Invasive plant pathogens can be integrated ­America, it is invasive in southern Brazil); and Ulex with the more disruptive chemical and mechanical europaeus L. (Fabaceae; known in South America by methods most commonly used for high-cash the common name “tojo”). These invasive plants crops, or in situations where the availability of cause significant economic or ecological damage manual labor is limited. in Central and South America and justify the The twenty most important invasive plants in research and implementation costs of biological Central and South America are shown in the control. In some cases, the costs for implementing accompanying table: Amaranthus spinosus L. biological control programs in Central and South (Amaranthaceae; common name “spiny amaranth” America can be reduced by making use of the in the USA, “bledo” in Central America); Ambrosia existing technology that has been successful in artemisiifolia L. (Asteraceae; common name other regions of the world, thus, biological control ­“Amargosa,” distribution North and South America); with insects and/or pathogens could provide 500 B Biological Control of Invasive Plants in Latin America Biological Control of Invasive Plants in Latin America, Table 3 The twenty most important invasive plants in Central and South America Scientific name Common name Family Origin Amaranthus spinosus Bledo Amaranthaceae Tropical America Ambrosia artemisiifolia Amargosa Asteraceae America Bidens pilosa Mozote Compositae America Conyza bonariensis Varilla Asteraceae Tropical America Cyperus rotundus Coyolillo Cyperaceae India Desmodium tortuosum Pega-pega Fabaceae Tropical America Echinocloa colona Arroz de monte Poaceae Eurasia Eichhornia crassipes Lirio acuático Pontederiaceae South America Eragrostis plana Capim annoni Poaceae South Africa Pistia stratiotes Lechuga de agua Araceae South America Portulaca oleraceae Verdolaga Portulacaceae India Richardia scabra Botoncillo Rubiaceae South America Ricinus communis Higuerilla Euphorbiaceae Tropical Africa Rottboellia cochinchinensis La caminadora Poaceae India Sida acuta Escobilla negra Malvaceae Tropical America Solanum torvum Lava platos Solanaceae Africa Sorghum halepense Grama Johnson Poaceae Mediterranian Taraxacum officinale Lechuguilla Asteraceae Europe Tecoma stans Guabillo Bignoniaceae Mexico Ulex europaeus Tojo Fabaceae Europe

­effective, safe, and low-cost solutions to many of In: Charudattan R, Labrada R, Center TD, Nelly-Begazo Central and South America’s most important C (eds) Strategies for water hyacinth control. A report of a panel of experts meeting, Fort Lauderdale, Florida. invasive plant problems. Table 3. Food and Agricultural Organization of the United  Biological Control of Weeds Nations, FAO, Rome, pp 125–135  Classical Biological Control Holm LG, Plucknnett DL, Pancho JV, Herberger JP (1997)  Invasive Species The world’s worst weeds. University Press of Hawaii, Honolulu Julien MH, Griffiths MW (1998) Biological control of Reference weeds. A world catalogue of agents and their target weeds, 4th edn. CAB International, Queensland, Aus- tralia, 223 pp Charudattan R (1996) Pathogens for biological control of Martínez M, Charudattan R (1998) Survey and evaluation of ­waterhyacinth. In: Charudattan R, Labrada R, Center TD, Mexican native fungi for potential biocontrol of water- Kelly-Begazo C (eds) Strategies for water hyacinth hyacinth. J Aquat Plant Manage 36:145–148 ­control. A report of a panel of experts meeting, Fort Martínez M, Gutiérrez E, Huerto R, Ruíz E (2001) Importa- ­Lauderdale, Florida. Food and Agricultural Organization tion, rearing, release and establishment of Neochetina of the United Nations, FAO, Rome, pp 90–97 bruchi (Coleoptera: Curculionidae) for the biological Gutiérrez LE, Arreguín CF, Huerto DR, Saldaña FP (1994) control of waterhyacinth in Mexico. J Aquat Plant Control de Malezas Acuáticas en México. Ingeniería ­Manage 39:140–143 Hidráulica en México 9:15–34 Martínez M, Gómez M (2007) Integrated control of Eichhor- Gutiérrez LE, Huerto R, Martínez M (1996) Waterhyacinth nia crassipes by using insects and plant pathogens in problems in Mexico and practiced methods for control. Mexico. Crop Protection (in press) Biological Control of Weeds B 501 Medal J (2004) Perspectives on biological control of invasive coevolved natural enemies to provide permanent plants in Latin-America. In: Cullen JM et al (eds) Proc XI control of the weed. Thus, classical biological control Int Symp Biol ContWeed. Canberra, Australia, pp 425–427 Medal J (2007) El control biológico de malezas en Latinoa- can be defined as the planned introduction and mérica: situación actual y Perspectivas futuras. Vedalia release of undomesticated target-specific organ- (in press) isms (usually arthropods, nematodes or plant Norambuena H, Ormeño J (1991) Control biológico de malezas: fundamentos y perspectivas en Chile. Agricul- pathogens) from the weed’s native range to reduce tura Técnica (Chile) 51:210–219 the vigor, reproductive capacity, or density of the Norambuena H, Escobar S, Rodriguez F (2000) The bio­ target weed in its adventive range. The term control of gorsse, Ulex europaeus in Chile: a progress “adventive” in this definition acknowledges the report. In: Spencer NR (ed) Proc X Int Symp Biol Cont Weed. Montana State University, Bozeman, MT fact that the arrival of a weed in a new geographical pp 955–961 area can occur by any means (e.g., immigration), Norambuena H (2004) Exploraciones en el Extranjero, and is preferable to the term “introduced,” which is ­Transporte, y Procedimientos de Cuarentena de los restricted to actions taken by people. Biological Agentes de Control Biológico. In: Medal J, Norambuena H, Gandolfo D (eds) Memorias del Segundo Curso weed control as it is defined here specifically ­Latinoamericano de Control Biológico de Malezas. excludes natural regulation (the action of organ- Montelimar, Nicaragua. University of Florida-IFAS, isms without human intervention), cultural control Gainesville, FL, pp 16–21 practices (grazing management, crop rotation, etc.), and plant competition (the deliberate use of one plant species to competitively exclude another). Biological Control of Weeds Although plant competition is not included in the definition of biological weed control, it is an essential james p. cuda component of the overall process that can affect University of Florida, Gainesville, FL, USA the outcome of a biological control project. Plant predation (or herbivory in the case of Weeds are universally recognized as significant weed biological control) and plant competition are pests worldwide because they interfere with entirely different ecological processes. An intro- food and fiber production, and are considered duced natural enemy (arthropod, nematode, or the most important threat to biodiversity after pathogen) damages or consumes portions of the habitat destruction. Weeds cause 90% of weed, which rarely leads to plant death but results ­agricultural losses, and herbicides account for in a loss of biomass or nutrients that weaken and approximately half (47%) of the world’s agro- stress the plant. In plant competition, the weed and chemical sales. The economic effect of weeds on its competitors are interfering with each other for the U.S. economy is staggering. Weed-associated use of a common resource (e.g., light, water, ­nutrients losses and costs in the mid 1990s were estimated or germination sites). It is the subtle interaction to be in excess of $20 billion annually, with between these two distinct ecological processes that ­non-native or invasive weed species accounting can lead to the permanent decline of a weed for $13 billion, or 65%. ­population. An invasive weed is less likely to recover An invasive weed is a non-native plant that from the effects of selective herbivory from biological exhibits rapid population growth following its control agents if competition from desirable native arrival in a new environment where it did not plant species is strong. evolve. The success of the weed in its new habitat Classical biological control offers several is due in part to the absence of the natural enemies advantages over other weed control methods: (i) it that normally limit its reproduction and spread in provides selective, permanent control of the target its native range. Classical biological control seeks weed; (ii) it is relatively inexpensive to develop to reunite an invasive weed with one or more of its and implement compared to other methods of 502B Biological Control of Weeds weed control; (iii) introduced biological control Recent examples of successful biological agents are self-replicating and will spread on their ­control of adventive weeds with introduced own throughout the infested area; and (iv) because ­invertebrate organisms in the last 20 years are they are living organisms, biological control agents shown above. are biodegradable. Some of the strengths of classical biological control also contribute to its shortcomings: (i) once Procedures in a Classical Weed biological control agents are established, they c­ annot Biological Control Project be recalled if desirable species are attacked; (ii) con- trol is not immediate and may require 5–10 years for From the beginning, weed biological control agents to attain damaging ­levels; (iii) ­natural ­enemies ­scientists have continued to develop and refine for controlling every weed may not exist; and procedures for locating, screening, releasing (iv) agent establishment and suppression of the and evaluating biological control agents (Sum- ­target weed are not guaranteed. mary of steps, Table 5). All countries currently

Biological Control of Weeds, Table 4 Recent successes in classical biological control of weeds with invertebrate organisms worldwide since 1980 Weed species Country Aquatic and Wetland Weeds Alligatorweed, Alternanthera philoxeroides (Martius) China, New Zealand, Thailand Grisebach Azolla, Azolla filiculoides (Lamarck) South Africa Purple Loosestrife, Lythrum salicaria L Canada, USA Water Fern, Salvinia molesta (D. S. Mitchell) Australia, Fiji, Ghana, India, Kenya, Malaysia, Namibia, Papua New Guinea (PNG), South Africa, Sri Lanka, Zambia Water Hyacinth, Eichhornia crassipes (Martius) Australia, Benin, India, Indonesia, Nigeria, PNG, ­Solms-Laubach South Africa, Thailand, Uganda, Zimbabwe Water Lettuce, Pistia stratiotes L Australia, Botswana, Ghana, PNG, South Africa, Sri Lanka, Zambia, Zimbabwe Terrestrial Weeds Annual Ragweed, Ambrosia artemisiifolia L Russia Giant Sensitive Plant, Mimosa invisa (Martius) Australia, PNG Leafy Spurge, Euphorbia esula L USA Nodding Thistle, Carduus nutans L Canada, USA Purple Sesban, Sesbania punicea (Cavanille) Bentham South Africa Spinyhead Sida, Sida acuta (Burman) f Australia Tansy Ragwort, Senecio jacobaea L USA, Australia

Sources: Julien MH, Griffiths MW (1998) Biological control of weeds. A world catalogue of agents and their target weeds, 4th edn. CAB International, Queensland, Australia, 223 pp; McFadyen REC (1998) Biological control of weeds. Annu Rev Entomol 43:369–393; Spencer NR (ed) (2000) Proc X Int Symp Biol Cont Weed, Bozeman, Montana, USA, 4–14 July 1999. United States Department of Agriculture, Agricultural Research Service, Sidney, Montana, and Mon- tana State University, Bozeman, MT Biological Control of Weeds B 503 conducting weed biological control projects Because these host-specific natural enemies follow this ­protocol in one form or another to reproduce only in the presence of their host plants, ensure that candidate organisms are safe to they are able to regulate weed abundance by introduce. operating in a self-sustaining, density dependent manner. Selecting organisms as candidates for classi- Importance of Host Specificity cal weed biological control can be a complicated and lengthy process because scientists must iden- Host specificity is fundamental to biological weed tify those natural enemies that have developed a control because it ensures that an introduced agent high degree of specificity with their host plants. will not become a plant pest. Host specific, ­Scientists conduct various types of host range tests coevolved natural enemies are considered good in the field and laboratory (oviposition, adult feed- candidates as they are incapable of reproducing ing, and larval development) depending on the on plants other than their weedy hosts, and have biology of the agent. Several screening tests ­usually proven to be the safest to introduce because they are required to demonstrate with confidence the are least likely to damage nontarget species. estimated host range of the agent. Candidate

Biological Control of Weeds, Table 5 Summary of steps involved in a classical weed biological control project Step Description Target selection Review literature about target weed, related plants and known natural enemies; identify and resolve conflicts of interest; ­conduct cost-benefit analyses; seek approval and funding Overseas and domestic surveys Locate native range of target weed and survey for natural ­enemies; assess biocontrol potential of each organism in ­country of origin; conduct faunal surveys in adventive range Host specificity studies Examine host range of organisms in native range; compile list of test plants and import promising candidates into quarantine of country of introduction for further testing Approval of agents Submit screening report to appropriate regulatory agencies to obtain approval for release; respond to requests for additional host testing or other concerns Rearing and release Obtain release permit; mass rear biocontrol agent; identify and implement most effective release strategy; release biocontrol agent at various sites to increase likelihood of establishment Evaluation Conduct field studies to confirm establishment and spread of biocontrol agent on target and nontarget species; use ­replicated manipulative experiments to determine effect of biocontrol agent on target weed populations Technology transfer Provide training to land managers and extension agents about using biocontrol agents; collaborate with user groups to ­determine best strategies for integrating biocontrol with other control methods

Sources: Julien M, White G (eds) (1997) Biological control of weeds: theory and practical application, ACIAR Monograph No. 49. ACIAR, Camberra, Australia; Luken JO, Thieret JW (eds) (1997) Assessment and management of plant invasions 504 B Biological Control of Weeds organisms that fail the host specificity requirement Biological Control of Weeds, Table 6 Number of are dropped from further consideration. Accord- weed species targeted and agent species released ing to established guidelines, no organism can be in the five most active countries through 1990 introduced into a new environment before its host Country Weed species Agent range is determined. species United States 54 130 Taxa Used in Classical Biological Australia 45 123 Control of Weeds South Africa 28 61 Canada 18 53 Through 1996, there have been at least 1,150 New Zealand 15 15 deliberate releases of invertebrate organisms TOTAL 160 391 against invasive weed species in 75 countries. Five of the countries shown here – the United States, Source: Julien M, White G (eds) (1997) Biological control Australia, South Africa, Canada and New Zealand – of weeds: theory and practical application, ACIAR account for most of the activity, based on the ­Monograph No. 49. ACIAR, Canberra, Australia number of weed species targeted and agents released. Biological Control of Weeds, Table 7 Invertebrate A large number of families and species are taxa deliberately introduced between countries represented in these releases, and they are listed by for classical biological control of adventive weeds the taxonomic groupings shown on p. 307. The Group No. of families No. of species taxa used in biological control projects worldwide INSECTA are predominantly insects, but mites, nematodes, Coleoptera 8 147 and fungi also have played an important role in Lepidoptera 25 106 controlling adventive weeds in some cases. ­Overall, Hemiptera 10 28 25% of all releases made before 1985 contributed to the control of the target weed. Diptera 6 44 Thysanoptera 2 4 Hymenoptera 3 5 Classical Biological Control of Orthoptera 1 1 Weeds in Aquatic Habitats ACARINA 3 5 FUNGI 4 17 Compared to terrestrial weeds, biological control NEMATODA 2 2 of aquatic weeds with insects has been remarkably Total 64 359 successful since it was first attempted in the United States against alligatorweed (Alternanthera philox- Sources: Bellows TS, Fisher TW (eds) 1999 Handbook of eroides (Martius) Grisebach) in 1964. Complete or biological control. Academic Press, San Diego, CA ;Julien substantial biological control of several other MH, Griffiths (eds) (1998) Biological control of weeds: a world catalogue of agents and their target weeds (4th ed) aquatic weed species has been achieved in most CABI Publishing, New York, NY countries where it has been attempted. Although a higher proportion of failures than successes has correlated with the growth form of the weeds, the occurred in the field of weed biological control, taxa used as biological control agents, susceptibil- the overall success rate for the aquatic weeds is ity to disease-causing pathogens, fluid nature of extraordinary. A close examination of the various the aquatic environment, or some combination of projects suggests this high success rate may be these factors. Biological Control of Weeds B 505 The aquatic form of alligatorweed, water agents cannot develop damaging populations ­hyacinth (Eichhornia crassipes (Maritius) Solms- quickly enough to be effective against crop weeds Laubach), water lettuce (Pistia stratiotes L.), ­salvinia because rapid control is needed to prevent the (Salvinia molesta D. S. Mitchell), and water fern weed from overwhelming the crop. Finally, most (Azolla filiculoides Lamarck) have been ­predictably crop weeds are multi-species assemblages of short- controlled using classical biological control. An lived annuals that traditionally were not considered interesting pattern emerges when the weed and amenable to biological control by introduced host- insect attributes associated with these successes are specific organisms with the exception of fungi. considered. (i) All of the aforementioned aquatic Several recent examples, however, have shown weeds are either free-floating, or produce floating that classical biological control is feasible in some mats in the case of alligatorweed. This plant growth intensively managed agricultural environments form is susceptible to wave action and currents that where most of the problems are caused by one are unique to aquatic environments. (ii) Reproduc- or two species of adventive crop weeds. Field tion in these weeds is primarily by rapid vegetative ­bindweed (Convolvulus arvensis L.), which is growth. High genetic uniformity usually associated native to Eastern Europe, is a serious pest of corn, with vegetative reproduction was thought to be a cotton, sorghum, turf and wheat in much of the necessary ­prerequisite for successful biological United States and Canada. An eriophyid mite control. (iii) These floating weeds are highly suscep- (Aceria malherbae Nuzzaci), imported from Greece tible to secondary infection. Aquatic plants that have in 1989, has proven to be effective in controlling ­sustained damage by insects or disease will rot and field bindweed infestations in some parts of disintegrate very rapidly. (iv) Beetles (Insecta: Texas and Oklahoma, and can survive repeated Coleoptera) have been responsible for most of the mowing. The mite attacks the plants by producing control, especially weevils. Coincidentally, most inver- galls on the leaves, petioles, and stems that stunt tebrate organisms released for classical ­biological new growth, deform the leaves, and limit seed control of weeds worldwide have been beetles. production. Puncturevines (Tribulus terrestris L. and T. cistoides L.) are annual and perennial herba- Classical Biological Control of ceous plants, respectively, native to the Mediter- Weeds in Stable and Ephemeral ranean region and Africa. In the 1960s, these two Habitats adventive weeds were serious pests of croplands and pastures primarily in arid regions of the Historically, only perennial weeds of relatively southwestern United States and Hawaii. Punc- ­stable environments (e.g., pastures, rangelands, turevines were not only invasive but produced and aquatic systems) were regarded as appropriate spiny burs, capable of penetrating tires, that were targets for classical biological control with host injurious to livestock. Two weevils imported specific introduced natural enemies. Habitat from Italy, a stem borer [Microlarinus lypriformis ­stability coupled with minimal disturbance were (Wollaston)]; and a seed feeder [M. lareynii thought to be necessary prerequisites for success- ­(Jacquelin du Val)]; gave complete control of ful biological control. Conversely, crop weeds were both puncturevines in Hawaii, and provided deemed inappropriate targets for classical biological substantial control of the annual species in many control with most of these organisms because of areas of the Southwest. their vulnerability to conventional cultivation Three ragweeds that are native to North practices (e.g., soil tillage, mowing) and the same ­America are adventive species in the former Soviet pesticides used against crop pests. Also, there was Union where they have become invasive. One of the belief that invertebrate biological control these ragweeds (Ambrosia artemisiifolia L.) caused 506 B Biological Insecticides serious problems because it was infesting ­croplands Florida from Australia for biological control of and was difficult to control using conventional melaleuca (Melaleuca quinquenervia (Cav.) S. T. ­herbicides and cultural methods. A defoliating leaf Blake) are contributing to the successful integrated beetle [Zygogramma suturalis (Fab.)]; obtained management of this invasive ­wetland tree weed that from Canada and the United States, was released in is threatening the ecology of the Florida­ Everglades the former Soviet Union in 1978. This leaf beetle  Foreign Exploration for Insects That Feed on built up enormous populations and provided Weeds ­complete control of this ragweed under certain con-  Host Specificity of Weed-Feeding Insects ditions. On one farm, yields of alfalfa, sainfoin and  Classical Biological Control corn increased dramatically as the beetles ­completely destroyed all the ragweeds in the infested fields. References More recently, the invasion of natural and conservation areas by immigrant plant species or Bellows TS, Fisher TW (eds) (1999) Handbook of biological introduced ornamental plants that have escaped control. Academic Press, San Diego, CA cultivation has generated considerable interest in Julien M, White G (eds) (1997) Biological control of weeds: classical biological control as a weed management theory and practical application, ACIAR Monograph tool. Invasive weeds of natural areas have been No. 49. ACIAR, Canberra, Australia Julien MH, Griffiths (eds) (1998) Biological control of weeds: called “biological pollutants.” Unlike other forms a world catalogue of agents and their target weeds of environmental pollution whose effects are (4th ed). CABI Publishing, New York, NY reversible once the source of the pollution is Luken JO, Thieret JW (eds) (1997) Assessment and removed, invasive weeds pollute the environment ­management of plant invasions. Springer, New York, NY McFadyen REC (1998) Biological control of weeds. Annu Rev after they become established by continuing to Entomol 43:369–393 proliferate and spread causing potentially irrevers- Spencer NR (ed) (2000) Proc X Int Symp Biol Cont Weed, ible ecosystem damage. Incipient populations of ­Bozeman, Montana, USA, 4–14 July 1999. United States Department of Agriculture, Agricultural Research Ser- adventive weeds often are indistinguishable from vice, Sidney, Montana, and Montana State University, the native flora, and they usually avoid detection Bozeman, MT until severe ecological harm already has occurred. Eventually, these invasive natural area weeds change Biological Insecticides the landscape by displacing more desirable native plant species, altering fire regimes, increasing soil Insecticides made with insect pathogens that are erosion, contributing to the loss of wildlife habitat, formulated to be applied like conventional chemi- causing some plants and animals to become rare or cal insecticides. endangered, and diminishing the aesthetic value of  Insecticides recreational areas. In some cases, invasive natural  Microbial Control of Insects area weeds even cause human health problems. Biological control offers an attractive alterna- tive to conventional chemical and mechanical con- Biology trol methods that are too costly and damaging to the environment, especially on large tracts of public The study of life. This is an “umbrella” term that lands set aside for nature preserves as well as state includes all aspects of the study of life, including and national parks. Some recent examples of suc- ­biochemistry, genetics, and taxonomy. Some cessful biological control ­programs against invasive ­taxonomic texts include a section with heading weeds of agricultural as well as natural areas are “Biology” under which the authors assemble infor- listed on p. 305. Although it has not been confirmed, mation about behavior and natural ­history, as if there is every indication that insects introduced into taxonomy were somehow not part of biology. Biotechnology B 507 Bioluminescence as inundative or augmentative biological control agents. Light produced by living organisms from a chemi- Microbial Control of Insects cal reaction, usually involving the protein luciferin and the enzyme luciferase.  Fireflies Biorational Pesticides  Fireflies: Control of Flashing  Glowworms Pesticides that are considered to be safe to humans or the environment, and based on microbial agents or naturally occurring chemicals (e.g., pheromones, Biomagnification hormones). Because these are based on chemical products rather than on living organisms, they are Increase in the concentration of a persistent classified as chemical control rather than biological ­chemical along a food chain, with the top-level control. predators accruing the highest concentration. Pheromones ­Biomagnification is of special concern with long- Microbial Control of Insects lived pesticides, which can be retained in fat ­tissues Botanical Insecticides rather than being excreted. Biomagnification is also known as biological concentration and food chain concentration. Biosphere  Biological Amplification The ecosystem that includes the entire earth. Biomass

The mass of a living organism of a defined type Biosystematics and from a defined area. Biomass, often expressed as dry weight, is used to estimate abundance and The branch of systematics (classification) in which to ameliorate the differences between a few large the genetic and evolutionary relationships between individuals and many small ones. taxa are investigated.

Biome Biota

A large ecological unit or ecosystem defined by The species of plants and animals occurring within vegetation, climate, and geography, though a biome a defined area. can be found in more than one place. Examples of biomes are salt marshes and steppe regions. Biotechnology

Biopesticide The manipulation of organisms to provide desir- able products. It has broader meanings, as well, A product that consists of biological organisms, including all parts of an industry that creates, ­usually microbial agents or their products, for develops and markets a variety of products through pest suppression. Biopesticides usually are applied the molecular manipulation of organisms or using 508 B Biotic Disease knowledge pertaining to the molecular biology of Bipectinate organisms. In pest management, it is the use of genetically modified organisms in the production The presence of comb-like structures on opposing of crops or animals, including in the production of sides, usually used to refer to a form of antennae. insect-suppressive agents.  Antennae of Hexapods

Biotic Disease Bird and Rodent Fleas

Disease caused by a pathogen, such as a bacterium, Members of the family Ceratopsyllidae (order fungus, or virus. Siphonaptera).  Fleas

Biotic Potential Bird Cherry-Oat Aphid The rate at which a species will increase in the absence of limits.  Wheat Pests and Their Management

Biotic Release Bird Lice

The escape of a population from the regulatory Members of the family Philopteridae (order effects of its natural enemies, resulting in a popu- Phthiraptera). lation increase or outbreak.  Chewing and Sucking Lice

Biotope Bird Malaria  Avian (Bird) Malaria An area of uniform environmental conditions occupied by a similar community. This term is most popular in Europe. It is essentially equivalent to “habitat,” but although habitat is often used in Birnaviruses conjunction with populations, biotope is used to describe a community. The family Birnaviridae contains three genera, the Avibirnavirus (infectious bursal disease of chick- ens), the Aquabirnavirus (infectious pancreatic Biotype necrosis virus of fish), and the Entomobirnavirus (Drosophila X virus). Birnaviruses are icosahedral A race or strain of an organism that differs in viruses and lack a viral membrane. Characterized some way from the principal population, often as medium-sized viruses (60 nm diameter), they in ­susceptibility to a pesticide or in association encapsidate two segments (A, B) of linear dsRNA with a food plant. In the case of host plant asso- (total size 6–7 kbp). Unlike other dsRNA viruses ciations, such biotypes are sometimes called (reoviruses), Birnavirus dsRNAs extracted from “host races.” the viral capsid can serve as m-RNA; under in Bíró, Lajos B 509 vitro conditions, the dsRNA molecules can bind to was then part of Hungary). He was the sixth ribosomes and undergo translation. Segment A is child of a poor cabinetmaker. His father wanted polycistronic and codes for three gene products, him to become a woodworker also, but young whereas segment B is monocistronic and codes for Lajos had a keen interest in natural history. one gene product. Thanks to his teacher, Ferenc Török, he became The Drosophila X virus (DXV), the type quite an expert in insect collecting and various ­species of the Entomobirnavirus, was discovered other zoological preparation techniques. From initially as a contaminant in insect cell lines. an early age he longed for the tropics but com- Sequence analysis of DXV has revealed that ing from a poor family and living in land-locked ­segment A contains two open reading frames Hungary, he could only dream about exotic (ORFs) consisting of a 3096 bp and 711 bp countries and the exploration of their zoologi- sequence. The 3096 bp ORF codes for the 114 kDa cal wonders. To ­satisfy his ambitions in discov- polyprotein which is processed post-translation- ery and research, he built an extensive insect ally by virus-encoded protease to generate VP-2, collection of Hungary and ­adjacent lands. To VP-3, and VP-4. In most birnaviruses, the second become a university student was out of the ORF codes for a small, arginine-rich peptide. question because of the family’s financial ­Segment B encodes for VP-1 putative viron asso- ­circumstances. The only way for him to obtain ciate RNA polymerase. DXV is polytropic and can some sort of a tertiary ­education was to become replicate in the cytoplasm of both the mesoder- a priest. He attended Protestant Theology – but mal and epidermal cells of D. melanogaster. DXV only for two years, as he couldn’t develop a deep ­replication results in extensive lysis of Drosophila religious belief and became a teacher. From his cells within 26 h. Surviving cells maintain DXV in meager earnings he tried to save up for a tropi- a repressed form (they are persistently infected) cal journey. At the same time his reputation as and are immune to a second challenge with DXV. an entomologist grew and ­eventually he gained Laboratory colonies of D. melanogaster infected government employment as grape phylloxera with DXV exhibit anoxia sensitivity and do not inspector/consultant at the Entomological Insti- recover after being anesthetized with CO2 or N2. tute in Budapest. The tragic death of Samuel Fenichel prompted Bíró to take important steps References towards the realization of his childhood dreams: to grasp the emerging opportunity and embark Chung HK, Kordyban S, Cameron L, Dobos P (1996) Sequence on a journey to New Guinea. To obtain the nec- analysis of the bicistronic Drosophila X virus genome essary financial ­support, he sold his collection segment A and its encoded polypeptides.Virology 225:359–368 of over 20,000 specimens to the Hungarian Nagy E, Dobos P (1984) Synthesis of Drosophila X virus National Museum and secured an agreement ­proteins in cultured Drosophila cells.Virology with its management for the purchase of the 134:358–367 material he was to collect during the expedition. He left Hungary on the 7th of November 1895 and arrived to Friedrich-­Wilhelmshafen (today Bíró, Lajos Madang) in Kaiser Wilhelm Land or ­German New Guinea (today Papua New Guinea) on the george hangay 1st of January 1896. During the following Narrabeen, NSW, Australia 6 years, Bíró relentlessly worked towards his goal to explore as much as possible of New Lajos Bíró was born on the 29th of August 1856 Guinea’s insect fauna. He was a very ambitious in Tasnád, Szilágy Shire, in Transylvania, (which and ­prolific collector. His activities were not 510 B Bisexual restricted to insects alone as he also collected Biting Midges, Culicoides spp. other zoological and ethnographical specimens (Diptera: Ceratopogonidae) as well. The total number of his New Guinean zoological collections exceeded 200,000 speci- alison blackwell mens, while the ethnographical objects num- University of Edinburgh, Midlothian, Scotland, bered over 6,000. These collections are still not United Kingdom fully processed yet, although its study by many researchers, including Bíró himself, generated Culicoides is the most important of four genera of over 100 papers, describing 2,000 species new to the family Ceratopogonidae which feed on the science. After his New Guinean years, Bíró con- blood of vertebrate animals. Culicoides includes tinued his work as an entomologist, mainly more than 1,400 named species, and at least 50 focusing on Hymenoptera and Coleoptera. His are thought to be vectors of disease, spreading greatest strength was evident in the field, where pathogens to man and animals. his acute sense of observation and excellent col- lecting methods yielded valuable information and great numbers of specimens. He has con- Classification and Recognition ducted fieldwork in many European ­locations, including Turkey, Bulgaria, Crete, etc., and he Order: Diptera was commissioned by the British Royal Geo- Suborder: Nematocera graphical Society to train young zoologists in Infraorder: Culicomorpha India and Burma. In recognition of his achieve- Superfamily: Chironomoidea ments, in 1926 he was awarded an honorary Family: Ceratopogonidae doctorate by the Ferenc József ­University of Sci- Subfamily: Ceratopogoninae ence in Szeged (Hungary). Fellow workers Tribe: Culicoidini named about 150 newly described species after Genus: Culicoides him. He passed away in 1931 at the age of 75. The Ceratopogonidae as a whole is a family of Bíró is considered today as one of the most small nematocerous flies, 2–4 mm in length with a ­outstanding Hungarian field entomo­logists, wingspan of usually less than 2 mm. Although closely who unselfishly served his nation and his related to the non-biting midges, or ­Chironomidae, science. they are easily distinguished by the female’s biting mouthparts, their short fore legs and characteristic venation on their membranous wings. They are most commonly known as “biting midges” but there Reference are numerous geographical variations, including “sandflies,” “punkies,” “no-see-ums,”­“no-nos,” “moose- Balogh J, Allodiatoris I (1972) In Memoriam Lajos Bíró flies” and “biting gnats.” Some names are particularly and Sámuel Fenichel. Acta Zool 42:1–2, Budapest, expressive, for example, the Gaelic name for the Scot- Hungary tish Highland midge is Meanbh-chuileag (tiny fly) emphasizing its diminutive, 1.4 mm wingspan. Culicoides are some of the smallest cerato­ pogonids, 1–2 mm in length, partly distinguishing Bisexual them from the other blood-feeding genera (Lepto- conops, ­Austroconops and the subgenus ­Lasiohelea The occurrence of males and females in different within the genus Forcipomyia). The small head has members of the species. a large pair of compound eyes in addition to Biting Midges, Culicoides spp. (Diptera: Ceratopogonidae) B 511 ­five-segmented maxillary palps, which are outside The wings of Culicoides are often an immedi- of the short set of sucking and piercing mouth- ate identification feature for the amateur, with parts (in the female), held perpendicular to the the majority (but not all) having a series of dark body axis. There is also a prominent pair of seg- and pale spots covering the wings, which are mented antennae, with long mechanoreceptors on folded, ­scissor-like at rest or when feeding. Other the male antenna, giving it a feathery appearance. genera, such as Austroconops, lack any pattern on The dorsal thorax (mesonotum) is frequently cov- their wings. The wings have been a major taxo- ered in a ­distinctive pattern of dark spots or other nomic ­feature of the Ceratopogonidae, with a markings, accompanied at the proximal end by a number of admirable works detailing the degree pair of small, elongate “humeral pits,” distinguish- and pattern of venation, wing color and mark- ing Culicoides from other genera. The body is ings, and the degree of coverage by macrotrichia, ­generally a variation of brown or black, but some which are fine, short hairs that often cover the species are yellowish-brown/orange (Fig. 45). wing surface (Fig. 46).

Biting Midges, Culicoides Spp. (Diptera: Ceratopogonidae), Figure 45 Female Culicoides nubeculosus. 512 B Biting Midges, Culicoides spp. (Diptera: Ceratopogonidae) In addition to the wing characteristics, ­further been carried out by molecular techniques, partic- identification to species is best carried out from ularly species ­complexes, such as the C. imicola slide-mounted specimens. For example, the third complex, where subspecies differentiation can be segment of the maxillary palp contains a large pit difficult using morphological features alone containing palpal sensilla. Some species have small (Figs. 46 and 47). pits, each bearing individual sensilla. These sen- Culicoides larvae are aquatic/semi-aquatic silla are generally considered to be concerned with and swim with a distinctive eel-like motion. They ­carbon dioxide (and hence host) detection in the are found in a variety of environments, such as female midge, with smaller numbers found in the mud, salt-marsh, compost and leaf litter. Some of non-blood-feeding male. The shape and size of the the most important veterinary species breed in palpal pit, and the numbers of sensilla are often damp ground contaminated to a degree with used as taxonomic tools. Likewise, the antennal ­animal excreta and other organic matter. The sensilla are pivotal to species identification. The ­slender larvae are primarily pale, sometimes with antenna consists of a small, flattened ring with a thoracic markings. The pharyngeal skeleton of the triangular apex (the “scape”), a globular, ­cup-shaped sclerotized head capsule is a key taxonomic feature. pedicel, which is enlarged in the male antenna to accommodate a well-developed Johnston’s organ and the antennal flagellum, having 13 sub-seg- Distribution ments. Culicoides antennae bear approximately 300–350 (male) and 200–250 (female) sensilla. Of Culicoides are the most widespread of the greatest importance to the taxonomist is the num- ­Ceratopogonidae, occurring throughout the world, ber and positions of the sensilla coeloconica and with the exception of the polar regions. The only sensilla trichodea. Further taxonomic detail can large inhabited land masses from which they are also be gained from both the male and female gen- known to be absent are New Zealand and the italia. More recently, species differentiation has southern most areas of South America.

Biting Midges, Culicoides Spp. (Diptera: ­Ceratopogonidae), Figure 46 Female Culicoides ­nubeculosus showing separated compound eyes. Biting Midges, Culicoides spp. (Diptera: Ceratopogonidae) B 513

Biting Midges, Culicoides Spp. (Diptera: ­Ceratopogonidae), Figure 47 Culicoides spp. maxillary palp, 3rd segment, showing different arrangements of the palpal sensilla: upper left, C. insinuatus; upper right, C. nubeculosus; lower left, C. impunctatus; lower right C. pseudodiabolicus.

Ecology and Behavior down into the substrate, where they live as omni- vores/detritivores. The larvae commonly remain Life Cycle and Population Dynamics close to the substrate surface. In Scotland, more The cylindrical or cigar-shaped Culicoides eggs than 50% Culicoides impunctatus larvae have been (30–200 per batch) are laid on the chosen sub- recovered from the top two cm of the soil surface. strate surface, where they hatch (2–10 days C. impunctatus appears to show a weak photo- depending on temperature) and the larvae move negative response, with a greater proportion in 514 B Biting Midges, Culicoides spp. (Diptera: Ceratopogonidae) deeper samples ­during the day than at night. This close to emergence sites, host-seeking females may daily migration is far more marked in Culicoides move several kilometers from a breeding site. One furens larvae, which live in the muddy banks of report suggests that Culicoides mississippiensis mangrove channels. With vegetation often sparse, ­travels more than 3 km in 24 h, without wind predation by birds is a serious threat during the ­assistance. When wind carriage does become daylight hours, perhaps explaining the fact that important, midges can travel considerable ­distances larvae feed on algae at the mud surface during the and increasing evidence suggests that disease night and on nematodes deeper down in the mud ­outbreaks in areas where particular Culicoides- during the day. In addition to a vertical compo- transmitted diseases are not endemic may start in nent, the spatial distribution of Culicoides larvae this way. For example, the outbreaks of bluetongue also appears to have a horizontal component. Even virus in Sardinia in 2000 and 2001 may have been in apparently homogeneous environments such as caused by infected midges carried on the wind from the Scottish Highlands, Culicoides larval distribu- Northern Africa. tion can be directly correlated with soil conditions (water and organic content) and key indicator Mating Behavior plant species. A similar situation is seen with the salt-marsh species Culicoides melleus, with larval Mating in Culicoides spp. has been studied for only distribution related to soil pH and areas of a small number of species, and despite the general ­Distichlis spicata (Gramineae). hypothesis that mating is initiated in male swarms There are four larval instars, and the time (as in many other nematocerans), there are only a required for larval development varies with tem- few records of Culicoides spp. swarms (including perature. Development may be completed in 14 Culicoides nubeculosus and C. impunctatus). Since days in warmer areas, with up to seven generations the conditions required for male swarming (still, produced each year. In more temperate regions, warm and humid) can be rare in some temperate this is reduced to one or two generations with the regions, it has been suggested that for species final larval instar often acting as the­over-wintering ­living in these areas (e.g., C. impunctatus in stage, although some species will aestivate as eggs. ­Scotland), at peak emergence periods it may be In Scotland, the over-wintering period for energetically more profitable for males to wait in ­Culicoides lasts for up to 9 months, followed by two the vegetation for emerging females, i.e., some adult generations during the summer. The pupal species may be facultative swarming species. Male period lasts between 2 and 10 days. swarming can be stenogamic (swarming adjacent Nightly trapping program can reveal signifi- to hosts on which females are feeding) or ­eurygamic cant information on the structure of Culicoides (no host involved), depending on the species. populations, including autogeny (e.g., females ­Distance and contact sex pheromones have been ­laying their first egg batch without taking a blood- implicated in the mating of C. nubeculosus and meal), protandry (e.g., males emerging before C. melleus, respectively. Both of these species have females), in addition to reproductive and survival been the subject of detailed studies of the mating rates, themselves allowing the calculation of a process, including mate “selection” by the female, ­species’ vector competency (e.g., the likelihood of it spermatophore formation and sperm transfer. being able to transmit a disease pathogen). In asso- ciation with climate data, it is possible to construct models of the influence of a range of climatic Host Finding and Feeding Behavior ­conditions on midge flight and biting activity. Records of midge dispersal rates vary enor- In addition to a bloodmeal, which is necessary for mously. Whereas male midges appear to remain female Culicoides to develop their eggs (including all Biting Midges, Culicoides spp. (Diptera: Ceratopogonidae) B 515 egg batches laid after the first batch by autogenous host-seeking, with the production of a volatile species), a carbohydrate source is also important for “recruitment” pheromone by parous, host-seeking most species. Direct evidence of sugar feeding in females, possibly analogous to the invitation the field, however, is rare. The small number of pheromone of some mosquito species. Variations published records include C. mississippiensis feeding in these chemical cues between individuals may from flowers of yaupon holly plants (Ilex vomitoria) account for some degree of intra-species selection in Florida. by Culicoides. The majority of Culicoides show some degree Visual cues are also important in bloodmeal of host preference and this has been investigated host location by a range of blood-feeding insects by a number of different techniques, including including both diurnal and crepuscular species. precipitin tests, fluorescent antibody tests, latex Culicoides spp. appear to be no exception. Field agglutination tests, ELISA tests and most recently, populations of C. impunctatus in Scotland were DNA analysis by PCR. These tests help to refine attracted to solid-outlined, black, rectangular the definition of a particular species such as, for ­targets and this response was enhanced in the example, ornithophilic (bird-feeding) or mam- presence of CO2. malophilic (mammal-feeding). Many species show Culicoides are “pool-feeders,” using their finely further specialization within these broad classes. toothed mandibles and maxillae to pierce the skin, For example, using an ELISA assay, single, working in a scissor-like fashion to create a pool of ­blood-fed C. impunctatus were screened against blood from which the insect feeds. Prior to this nine ­different potential bloodmeal hosts. The behavior, however, some midges display a degree results showed that cattle, deer and sheep were the of choice concerning the area to feed from. This ­primary hosts for this species. appears to be particularly the case with large Culicoides spp. biting midges have a highly hosts, including cattle and horses. The size of sensitive olfactory system, which is used in com- the Culicoides bloodmeal has been estimated at bination with other senses to locate their blood- 4 × 10−2 ml, with a process of rapid diuresis acting meal hosts accurately. The olfactory system is to concentrate the blood. based around the antennae and maxillary palps, the morphology and ultrastructure of which has been fully documented for a number of species. Recent studies have used antennal responses as Biting Behavior: Implications a ­screening tool to identify behaviorally active for Man and Animals compounds. This has involved the development of electrophysiological techniques, in particular Disease Transmission the recording of electroantennograms (EAGs) which, combined with behavioral studies and Culicoides spp. biting midges are most important field trapping ­programs with active compounds, as vectors of a number of serious livestock patho- has led to the ­identification of several semiochem- gens, including African horse sickness virus and icals involved in the host location behavior of bluetongue virus (which cause OIE list “A” Culicoides spp. For mammalophilic species, one ­diseases in their equine or ruminant hosts), ubiquitous host-derived attractant is 1-octen-3- bovine ephemeral fever virus (which significantly -ol, with others including acetone, butanone and reduces milk yields in cows and causes sterility L(+) lactic acid. Responses to each of these can be in bulls), ­Akabane virus (which causes abortions either enhanced or synergized by the addition of and ­congenital deformities in ruminants), Palyam carbon dioxide. For one species, C. impunctatus, viruses (which cause abortion storms in cattle) there is evidence of pheromone involvement in and epizootic hemorrhagic disease of deer virus 516 B Biting Midges, Culicoides spp. (Diptera: Ceratopogonidae) (which kills many species of deer and also causes in tropical and sub-tropical regions (e.g., Mansonella disease in cattle). Each of these diseases has an ozzardie, transmitted by Culicoides phlebotomus in established distribution, intricately linked with coastal North Trinidad) and a small number of that of its vector. There are, however, increasing viruses, including Oropouche, which is strongly examples of disease incursions into areas previ- pathogenic to man in parts of South America and ously unaffected, perhaps as a result of relaxations the West Indies. in international trade barriers, and a trend toward more favorable climatic conditions in these areas. For example, bluetongue virus (BTV) occurs as a Animal Welfare clinical disease in Africa, the Middle East, the Indian subcontinent, China, the USA, and ­Mexico The general irritation caused by midge bites can where Culicoides are active throughout the year. occasionally also lead to serious health and In December 1999, and January 2000, a BTV ­welfare conditions in both animals and man. ­serotype 2 epidemic occurred in Tunisia, close to Deer herds are often forced off low-lying pastures the Algerian border. This was the first time the onto higher, poorer slopes by midge attacks, ­disease had been reported from North Africa. which has been suggested as the reason why Scot- ­Further outbreaks followed in June 2000, matched tish red deer are weaker than their European by outbreaks in contiguous coastal areas of counterparts. The distress caused by midges to ­neighboring Algeria. From there it appears that cattle is also held to be responsible for reductions infected vectors carried bluetongue to Europe, in milk yields. Horses can also suffer from a num- with outbreaks reported by Italy (August: ­Sardinia, ber of allergic reactions to midge bites, including November: Calabria and Sicily), France ­(October: “sweet itch” (also known as “Queensland itch” in Corsica, for the first time) and Spain (October Australia and “kasen” in Japan), which is an and November: Balearic Islands, last infected in acutely irritating dermatitis, primarily confined 1960). Although there are only a small number of to the mane and tail, although it may spread to ­confirmed vectors for BTV (Culicoides variipen- the rest of the body. The horse’s skin becomes nis and possibly Culicoides insignis in the New thickened, weals and pustules form, and much of World, Culicoides imicola and possibly Culicoides the hair of the mane and tail breaks off or is obsoletus in the Mediterranean and Middle East rubbed off, resulting in extensive damage and and C. imicola and members of the Culicoides large sores in addition to financial loss. Causal m­ i l n e i and Culicoides schultzei groups in Africa), agents have been identified asCulicoides pulicaris laboratory infections have demonstrated that (UK), C. obsoletus (Canada), Culicoides robertsi a number of endemic species in officially (Australia), C. imicola (Israel) and Culicoides ­unaffected countries will support virus multi- ­insignis, Culicoides stellifer and Culicoides venus- plication following infection. tus (USA). Present methods of prevention include Culicoides spp. also transmit a number of judicious stabling during the summer months ­protozoans, most of which are avian parasites and a range of antihistamine, cortisone injections (Haemoproteus, Hepatocystis and trypanosomes). and soothing ointments. In addition, they transmit a variety of filarial worms (including Onchocerca spp.), infecting a range of animals, including birds, cattle and Human Annoyance horses. Overall, pathogen transmission to man by It is the biting attacks on humans, however, for biting midges appears to be minimal, although which midges are most noted in a number of they do transmit several species of filarial worms areas, including the Caribbean, California, ­Florida Biting Midges, Culicoides spp. (Diptera: Ceratopogonidae) B 517 and Scotland. The annoyance and discomfort potential for the development of resistant strains they cause can influence outdoor activities from such wide applications of broad-spectrum ­significantly and directly affect the local insecticides, precludes their use. Similar concerns ­economies, particularly when they rely heavily are also associated with the use of pyrethroids, on tourism. When bitten, the skin reaction of investigated for Culicoides larval control in the humans is usually mild, including temporary 1980s with populations of C. varipennis and burning and slight swelling. More sensitive indi- C. ­mississippiensis in the USA. For these reasons, viduals, however, can develop weals, blisters and alternative larvicides based on naturally occurring extreme inflammation of the skin. In a very few products, for example, neem-based products, are cases, extreme allergies can lead to hospitaliza- being investigated following the growing trend tion. Scarring and secondary infection may occur toward integrating botanical products into insect if bites are scratched. pest-control programs. Insecticide treatments of adult Culicoides have met with less success than larvicidal Control ­programs. A number of programs in the 1950s and 60s were based on thermal insecticide fog- Culicoides control programs have often been met ging, but the results were disappointing, most with difficulties, due to a number of factors. These probably because the insects avoided contact with include the fact that their breeding grounds are the insecticide by hiding beneath vegetation. In often widely scattered, difficult to recognize and addition, there is the likelihood that a sprayed often within environmentally sensitive areas, area would be reinvaded as soon as the insecti- thereby limiting the application of control prod- cidal mist had cleared, ­requiring regular (and ucts. The vast populations of adult midges and expensive) re-treatment. their extreme mobility and potential for wind-­ Where Culicoides are responsible for out- carriage also places limits on the use of chemical breaks of livestock disease, direct treatments of control of adults. the animals with insecticides (e.g., pyrethroids and ivermectin) have been partially successful. Under serious virus challenge conditions, ­however, permethrin failed to protect cattle Chemical Control from bluetongue virus infection in a Californian dairy. Culicoides spp. are susceptible to the majority of the major insecticide classes and most have been used at some stage against both adults and larvae, with varying degrees of success. Due to the diffi- Habitat Manipulation culty of targeting adult midges, chemical control programs have concentrated primarily on the Biting midge problems world-wide have been ­larval stages. Early studies (from the 1950s to the partly alleviated through a variety of measures 1970s) involved the broadcast application of a aimed at altering the suitability of areas for both number of persistent and broad-spectrum insecti- adult and larval midges. An example is the cides, including members of the organochlorines impounding or flooding of areas in Florida and (e.g., DDT) and organophosphates (e.g., chlorpy- the Caribbean to eliminate breeding sites of midge rifos). Although partly successful, today’s knowl- larvae which cannot survive in free-water. edge of the significant environmental and health ­Alternative strategies have included draining or risks associated with these products, as well as the land-filling breeding sites in salt marshes in­Florida 518 B Biting Midges, Culicoides spp. (Diptera: Ceratopogonidae) to make them too dry for midges to breed. There concoctions marketed as insect repellents. These are various other environmental manipulations, include oils distilled from a range of plants, includ- such as stream flushing and shade removal, which ing lemon-grass, eucalyptus, cypress, lavender, are in widespread use in the tropics to control pennyroyal and thyme. A common factor for most mosquitoes. Such measures have never been used of these is that they contain a number of terpenoid in more temperate regions. In fact, it has been compounds, such as citronellal and limonene. ­suggested that it is doubtful that any attempt to There are a number of regional “favorites.” For alter the landscape of localized areas would, in the example, in Scotland, the oil derived from the long term, be successful against biting midges in leaves of Myrica gale (bog myrtle, sweet gale – Scotland. Considering the relatively high mobility Myricaceae), a deciduous shrub that grows widely of these insects and the vast areas of potential in the Highlands of Scotland, has repellent prop- breeding grounds, this is probably true. Addition- erties equivalent to DEET against Culicoides spp. ally, these methods are often extremely expensive, In North America, even the US military consider laborious and although they may make the the use of ‘Avon Skin-So-Soft’â, as an alternative ­environment less suitable for Culicoides, they to DEET to protect them from biting insects. ­frequently destroy the habitats of other, non-target organisms. Traps

Repellents Traps are used mainly as population monitoring devices for Culicoides spp., although over limited The use of personal repellents can give a degree of areas, they can offer a degree of control. Traps vary protection against biting midges and indeed, this from basic light-suction traps (with blacklights is generally assumed to be the best line of defense. attracting more than whitelights), to more special- In addition, repellents can be used to treat win- ized, odor-baited traps. The latter resulted in dows and door screens and even clothing. A range increased and more specificCulicoides spp. catches. of chemical repellents, in various formulations Carbon dioxide (often released from a dry ice sold under a number of different trade names, are source) provides the most impressive increase in currently available. The most widely used chemi- catch size, although its attractiveness can be cal in insect repellents is DEET (N,N-diethyl-m- enhanced in combination with some of the toluamide), forming the main active constituent in ­host-related kairomones that are gradually being the majority of over-the-counter preparations, identified for Culicoides spp. For example, some with concentrations varying from 10% to 90%. commercial traps use a combination of carbon Since it was first marketed in 1956, DEET has dioxide and 1-octen-3-ol. remained the most effective repellent against midges, mosquitoes and other biting pests, although there have been a number of concerns Biological Control voiced regarding its safety, including a suggested contribution of DEET usage to the psychological The possibility of employing biological control effects associated with a number of combat situa- techniques for the control of Culicoides spp. has tions. Although DEET toxicity from casual use is been little studied. Predators, parasites and thought to be low and there are no definite reports pathogenic microbes suspected of being natural that these products are not safe if used correctly control agents of Culicoides spp. were recorded and sensibly, for those people preferring “natural” by Bacon in 1970, including viruses, rickettsiae, products, there is no limit to the number of herbal bacteria, fungi, protozoa and nematodes. Few, Black Bean Aphid, Aphis fabae Scopoli (Hemiptera: Aphididae) B 519 however, have been identified and studied in Biting Rate relation to potentially reducing biting midge pop- ulations. Nematodes of the family Mermithidae This is a measure of abundance of biting insects, are known to be fatal parasites of Ceratopogoni- and is expressed as number of bites per person per dae larvae, but have been found in only a few period of time. It is usually used in the assessment species, including C. variipennis in dairy waste- of mosquito abundance, and rather than have water ponds in California. The only report of a the insects actually bite before they are tabulated, fungal pathogen of Culicoides spp. is for the insects are typically captured pre-feeding, ­Culicoides molestus larvae in New South Wales, thereby alleviating stress to the census taker, and Australia, in which infection rates with the alleviating the risk of disease transmission. Under Oomycete Lagenidium giganteum of 1–62% were these conditions, then, it is actually the insect land- recorded. Concerning microbial insecticides, ing rate that is being measured, and used as an Culicoides spp. are virtually unaffected by com- index of the potential biting rate. Biting rate is also mercial applications used frequently against used as a component­ of insect repellent assessment. mosquito larvae, including Bacillus thuringiensis var israelensis and Bacillus sphearicus. Ceratopogonid midge species are regularly Bittacidae infested with a variety of ectoparasitic mite spe- cies. In particular, adult Culicoides have been A family of insects in the order Mecoptera. found carrying phoretic instars of several families They commonly are known as hangingflies. of mesostigmatid mites and ectoparasitic larvae Scorpionflies. of the prostigmatid superfamily Trombidioidea. The trombidioids are of additional interest because, in their free-living adult stage, some Bivoltine ­species have been seen feeding on larval cer- atopogonids. The precise impacts of these mites The occurrence of two generation within a year. on their hosts, however, is unknown. Information is lacking on the basic biology of these mites, their precise trophic relationships and perhaps their Bivouac potential as vehicles and vectors of candidate insect pathogens. Among army ants, the cluster of workers within which the queen and brood are sheltered.

References Blaberidae

Blackwell A (2001) The Scottish biting midge, Culicoides impunctatus. Goetghebuer: current research status and A family of cockroaches (order Blattodea). prospects for future control.Vet Bull 71:2R–8R  Cockroaches Boorman J (1993) Biting midges (Ceratopogonidae). In: Lane P, Crosskey RW (eds) Medical insects and arachnids, 723 pp. Chapman & Hall, New York, NY, pp 288–309 Sebastiani F, Meiswinkel R, Gomulski LM, Guglielmino CR, Black Bean Aphid, Aphis fabae Mellor PS, Malacrida AR, Gasperi G (2001) Molecular Scopoli (Hemiptera: Aphididae) differentiation of the old world Culicoides imicola. spe- cies complex (Diptera, Ceratopogonidae), inferred using random amplified polymorphic DNA markers. Mol Ecol This is an important insect pest of several crops. 10:1773–1786  Aphids 520 B Blackburn, Thomas Blackburn, Thomas Black Cutworm, Agrotis ipsilon (Hufnagel) (Lepidoptera: Thomas Blackburn was born at Islington near Noctuidae) ­Liverpool, England, on March 16, 1844. Ordained a deacon of the Anglican church in 1869, he was trans- john l. capinera ferred to Hawaii in 1870. There, he collected insects University of Florida, Gainesville, FL, USA of all orders. Next, he was transferred to Australia and became rector of a church at Port Lincoln in The origin of black cutworm is uncertain, though 1882, then one at Woodville near Adelaide,­ in 1886, it is now found in many regions of the world, which position he held for the rest of his life. In Eng- being absent principally from some tropical land, he and his brother J. B. Blackburn founded regions and cold areas. It is more widespread, and “The Weekly Entomologist” which, after two years, damaging, in the northern hemisphere than the was renamed “Entomologist’s Monthly Magazine” southern ­hemisphere. It annually reinvades and is published to this day. In Australia, he collected ­temperate areas, overwintering in warmer or beetles intensively, but specialized in Scarabaeidae. ­subtropical regions. It has acquired several other He became the foremost Australian coleopterist, and common names, including greasy cutworm and published descriptions of 3,069 Australian species. dark sword grass cutworm. He died on May 28, 1912, at Woodville. Long distance dispersal of adults has long been suspected in Europe, China, and North Amer- ica. The basic pattern is to move north in the spring, Reference and south in the autumn. Studies in the United States demonstrated northward displacement of Herman LH (2001) Blackburn, Thomas. Bull Am Mus Nat moths during the spring in the range of 1,000 km Hist 265:45–46 in 2–4 days when assisted by northward flowing wind. Similar displacement to the south and south- west has been documented in the autumn. Black Carpet Beetle, Atagenus megatoma (Fabricius) (Coleoptera: Life History Dermestidae) The number of generations occurring annually This is an important pest of stored products, varies with weather conditions. In North America, including stored grain. there are 1–2 generations in Canada but 2–4 in  Stored Grain and Flour Insects the United States. In Tennessee, USA, moths are  Stored Grain and Flour Insects and Their present in March-May, June-July, July-August, and Management September-December. Based on light trap collec- tions, moths are reported to be abundant in Arkansas, USA (a warm climate) during May-June and Sep- Black Citrus Aphid, Toxoptera tember-October, and in New York, USA (a cool aurantii (Boyer climate), they occur mostly in June-July. ­However, De Fonscolombe) light traps are not very effective during the spring (Hemiptera: Aphididae) flight, and underestimate early season. Thus, the phenology of black cutworm remains uncertain, This is an important pest of citrus crops. or perhaps is inherently variable due to the  Citrus Pests and Their Management vagaries associated with long range dispersal. Black Cutworm, Agrotis ipsilon (Hufnagel) (Lepidoptera: Noctuidae) B 521 ­Overwintering has been reported to occur in the reported to be 3.5, 5.3–6.2, 7, 10, 20–30, 30–45, 50, pupal stage in most areas where overwintering and 50 mm for instars 1–8, respectively. Duration occurs, but larvae persist throughout the winter in of the larval stage is normally 20–40 days. Mean Florida, USA, a subtropical environment. Pupae duration of instars 1–6 was reported to be 6.0, 5.0, have been known to overwinter as far north as 4.6, 4.3, 5.6, 4.0 days, respectively, at 22°C. Larval Tennessee, but apparently are incapable of surviv- development is strongly influenced by tempera- ing farther north. Thus, moths collected in the ture, with the optimal temperature about 27°C. central region of USA in March and April are Humidity is less important, but instars 1–5 thrive principally dispersing individuals that are past best at higher humidities. their peak egg production period. Nonetheless, In appearance, the larva is rather uniformly they inoculate the area and allow production of colored on the dorsal and lateral surfaces, ranging additional generations, including moths that from light gray or gray-brown to nearly black ­disperse north into Canada. Duration of the life (Fig. 49). On some individuals, the dorsal region is cycle is normally 35–60 days. slightly lighter or brownish in color, but the larva The egg is white in color initially, but turns lacks a distinct dorsal band. Ventrally, the larva brown with age. It measures 0.43–0.50 mm high and tends to be lighter in color. Close examination of 0.51–0.58 mm wide and is nearly spherical in shape, the larval epidermis reveals that this species bears with a slightly flattened base. The egg bears 35–40 numerous dark, coarse granules over most of its ribs that radiate from the apex; the ribs are alternately body. The head is brownish with numerous dark long and short. The eggs normally are deposited in spots. Larvae usually remain on the plant until the clusters on foliage. Females may deposit 1200–1900 fourth instar, when they become photonegative and eggs. Duration of the egg stage is 3–6 days. hide in the soil during the daylight hours. In these There are 5–9 instars, with a total of 6–7 latter instars they also tend to sever plants at the soil instars most common. Head capsule widths are surface, pulling the plant tissue belowground. about 0.26–0.35, 0.45–0.53, 0.61–0.72, 0.90–1.60, ­Larvae tend to be cannibalistic. 2.1–2.8, 3.2–3.5, 3.6–4.3, and 3.7–4.1 mm for Pupation occurs belowground at a depth of instars 1–8, respectively. Head capsule widths are 3–12 cm. The pupa is 17–22 mm long and 5–6 mm very similar for instars 1–4, but thereafter those wide, and dark brown. Duration of the pupal stage individuals that display 8–9 instars show only is normally 12–20 days. small increments in width at each molt and even- The adult is fairly large in size, with a wingspan tually attain head capsule sizes no larger than those of 40–55 mm. The forewing, especially the proximal displaying only 6–7 instars. Larval body length is two-thirds, is uniformly dark brown (Fig. 48). The distal area is marked with a lighter irregular band, and a small but distinct black dash extends distally from the bean-shaped wing spot. The hind wings are whitish to gray, and the veins marked with

Black Cutworm, Agrotis ipsilon (Hufnagel) Black Cutworm, Agrotis ipsilon (Hufnagel) (Lepi- ­(Lepidoptera: Noctuidae), Figure 48 Adult of doptera: Noctuidae), Figure 49 Mature larva of black cutworm, Agrotis ipsilon (Hufnagel). black cutworm, Agrotis ipsilon (Hufnagel). 522 B Black Cutworm, Agrotis ipsilon (Hufnagel) (Lepidoptera: Noctuidae) darker scales. The adult preoviposition period is Euphorocera claripennis (Macquart), Gonia longipul- about 7–10 days. Moths select low-growing broad- villi Tothill, G. sequax Williston, Lespesia archippiv- leaf plants preferentially for oviposition, but lacking ora (Riley), Madremyia saundersii (Williston), these will deposit eggs on dead plant material. Soil Sisyropa eudryae (Townsend), and Tachinomyia is an unsuitable oviposition site. panaetius (Walker) (all Diptera: Tachinidae). Preda- Black cutworm has a wide host range. Nearly all tory ground-dwelling insects such as ground beetles vegetables can be consumed, and this species also (Coleoptera: Carabidae) apparently consume feeds on alfalfa, clover, cotton, rice, sorghum, straw- numerous larvae. Although studies in Florida, USA, berry, sugarbeet, tobacco, and sometimes grains and indicated that 75–80% of cutworms could be killed grasses. In the midwestern USA it is considered to by a granulosis virus, there is surprisingly little infor- be a serious corn pest. Among the weeds suitable for mation on epidemiology and of natural pathogens. larval development are bluegrass, Poa pratensis; Rather, such pathogens as viruses, fungi, bacteria, curled dock, Rumex crispus; lamb’s-quarters, Cheno­ and protozoa from other insects have been evalu- podium album; yellow rocket, Barbarea vulgaris; ated for black cutworm susceptibility;­ in most cases and redroot pigweed, Amaranthus retroflexus. The only relatively weak pathogens have been identified. ­preference by black cutworm for weeds is sometimes An entomopathogenic nematode, Hexamermis quite pronounced, and crops will be attacked only arvalis (Nematoda: Mermithidae), is known to para- after the weeds are consumed. Adults feed on nectar sitize up to 60% of larvae in the central USA. from flowers. Deciduous trees and shrub such as ­linden, wild plum, crabapple, and lilac are especially attractive to moths. Numerous species of natural enemies have Damage been associated with black cutworm, but data on their relative importance are scarce. However, in This species occurs frequently in many crops, and is Missouri, USA, there are reports of 69% parasitism, one of the best-known cutworms. Despite the fre- so natural enemies probably exact a significant toll quency of occurrence, however, it tends not to appear on cutworm populations. Among the wasps known in great abundance, as is known in some other cut- to attack this cutworm are Apanteles marginiventris worms and armyworms. Black cutworm is not con- (Cresson), Microplitis feltiae Muesebeck, Microplitis sidered to be a climbing cutworm, most of the kewleyi Muesebeck, Meteorus autographae Muese- feeding occurring at soil level. However, ­larvae will beck, Meterorus leviventris (Wesmael) (all feed aboveground until about the fourth instar. Lar- Hymenoptera: Braconidae); Campoletis argentifrons vae can consume over 400 sq cm of ­foliage during (Cresson), Campoletis flavicincta (Ashmead), Hypo- their development, but over 80% occurs during the soter annulipes (Cresson), and Ophion ­flavidus Brulle terminal instar, and about 10% in the instar immedi- (all Hymenoptera: Ichneumonidae). Larvae parasit- ately preceding the last. Thus, little foliage loss occurs ized by Meteorus leviventris (Wesmael) consume during the early stages of development. Once the about 24% less foliage and cut about 36% fewer fourth instar is attained, larvae can do considerable seedlings, so considerable benefit is derived from damage by severing young plants, and a larva may parasitism in addition to the eventual death of the cut several plants in a single night. Plants tend to host larva. Other parasitoids known from black outgrow their susceptibility to injury. Corn at the ­cutworm include flies often associated with other one-leaf stage is very susceptible to damage, but by ground-dwelling ­noctuids, including Archytas the 4- or 5-leaf stage plant yield was not reduced by c­ i r p h i s Curran, ­Bonnetia comta (Fallen), Carcelia larval feeding. Leaf feeding and cutting above the formosa (Aldrich and Webber), Chaetogaedia mon- soil line are less damaging to corn than cutting at the ticola (Bigot), Eucelatoria armigera (Coquillett), soil surface. Subterranean damage is very injurious. Black Cutworm, Agrotis ipsilon (Hufnagel) (Lepidoptera: Noctuidae) B 523 Management weeds also can be beneficial by supporting pro- longed survival of parasitoids. In contrast, reduced Adult populations can be monitored with both tillage cropping practices, which often produce blacklight and sex pheromone traps. However, higher weed populations, seem to result in increased light traps are not consistently efficient. Light traps abundance of black cutworm and higher levels are most effective in the summer and autumn, of cutting in corn. This may be due, in part, to but the late season generations generally pose little the tendency of moths to oviposit on weeds; threat to crops. Pheromone traps are more effective weedy fields tend to have higher cutworm during the spring flight, when larvae present the populations. greatest threat to young plants. Trap color affects Black cutworm populations also tend to be moth capture rate, with white and yellow traps higher in wet areas of fields, and in fields that capturing more than green traps. have been flooded. Black cutworm has been Large larvae burrow in the soil, and are diffi- known, at times, as “overflow worm,” due to its cult to observe. However, larvae can be sampled tendency to be abundant and damaging in with bait traps, and this is most effective prior to fields that have been flooded by over­flowing emergence or planting of seedlings. Various trap rivers. designs have been studied, but many employ a In the home garden, barriers are sometimes container sunk into the soil with the upper lip at useful to prevent damage to seedlings by cut- the soil surface. The container is baited with fresh worms. Metal or waxed paper containers with plant material and/or bran, and with vermiculite both the top and bottom removed can be placed so the larvae can attain shelter. Larvae are effec- around the plant stem to deter consumption. tively captured in baited containers if the vermic- ­Aluminum foil can be wrapped around the stem ulite is not too near the surface, and catches are to achieve a similar effect. Because larvae will bur- enhanced if a screen cylinder, which provides a row and feed below the soil line it is necessary to visual stimulus to the cutworms, is suspended extend to barrier below the soil surface. Because above the baited container. If plants are present in black cutworm moths, which easily circumvent the field they compete with the bait in the traps, such barriers, are active during the growing ­season, and trap efficiency declines markedly. The distri- this procedure alone may have little value. Use of bution of larvae in the spring is random. netting or row covers, in addition to larval barri- Persistent insecticides are commonly applied ers, should prove more effective. to plants and soil for black cutworm suppression, Entomopathogenic nematodes (Nematoda: but surface rather than subsurface soil applications Steinernematidae and Heterorhabditidae) will are desirable. Larvae readily accept insecticide- infect and kill black cutworm larvae, but their treated bran and other baits. Application of systemic populations normally need to be supplemented to insecticides to seeds also provides some protection realize high levels of parasitism. Their effective- against larval injury. Bacillus thuringiensis is not ness is related to soil moisture conditions. usually recommended for cutworm control.  Turfgrass Insects and Their Management Black cutworm larvae feed readily on weeds,  Vegetable Pests and Their Management and destruction of weeds can force larvae to feed exclusively on crop plants, exacerbating damage. References Thus, it is often recommended that weeds not be tilled or treated with herbicide until larvae have matured. Timing is important, however, because Abdel-Gawaad AA, El-Shazli AY (1971) Studies on the ­common cutworm Agrotis ypsilon Rott. I. Life cycle and prolonged competition between crop and weed habits. Zeitschrift fur Angewandte Entomologie plants can reduce crop yield. Presence of flowering 68:409–412 524 B Black Earwigs Archer TL, Musick GL, Murray RL (1980) Influence of legs (Fig. 50). The female possesses a long oviposi- ­temperature and moisture on black cutworm tor with which it deposits its eggs in small groups, ­(Lepidoptera: Noctuidae) development and reproduc- tion. Can Entomol 112:665–673 beneath the scales protecting the ostiole (eye) of Busching MK, Turpin FT (1976) Oviposition preferences of the syconium (fig “fruit”). Oviposition takes place black cutworm moths among various crop plants, weeds, preferably in unripe figs, but ripening ones are also and plant debris. J Econ Entomol 69:587–590 Busching MK, Turpin FT (1977) Survival and development of attacked. The larvae feed on the tissues of the syco- black cutworm (Agrotis ipsilon) larvae on various species nium, destroying the fruit. Infestation of unripe of crop plants and weeds, Environ Entomol 6:63–65 figs usually results in premature fruit drop, which Capinera JL (2001) Handbook of vegetable pests. Academic is frequently mistaken by the growers as due to Press, San Diego, 729 pp Harris CR, Mazurek JH, White GV (1962) The life history of physiological problems of the trees. The fly com- the black cutworm, Agrotis ipsilon (Hufnagel), under pletes 4–5 generations per year and overwinters in controlled conditions. Can Entomol 94:1183–1187 the pupal stage in the soil. McCorcle, Robinson JF, Way MO, Wallendorf MJ, Goode- Observations conducted in Chios island, nough JL (1993) Mechanism of southward migration of a noctuid moth [Agrotis ipsilon (Hufnagel)]: a complete Greece showed that the flies are attracted and feed migrant. Ecology 74:2303–2314 mostly on sweet exudates of ripe figs, and on fresh Schoenbohm RB, Turpin FT (1977) Effect of parasitism by or dry milky fig-tree sap exuded from injured plant Meteorus leviventris on corn foliage consumption and corn seedling cutting by the black cutworm. J Econ parts. As many as 63 pupae were obtained from a Entomol 70:457–459 single infested, unripe fig, indicating multiple Story RN, Keaster AJ (1982) Temporal and spatial distribu- ­oviposition. The parasitoid Pachycrepoideus tion of black cutworms in midwest field crops. Environ ­vindemmiae Rondani (Hymenoptera: Ptero- Entomol 11:1019–1022 malidae) emerged from S. adipata pupae. Males were observed swarming in the afternoon hours, an indication that the ­mating behavior Black Earwigs is related to swarm formations. Hexanol, a ­generally-occurring plant volatile chemical, is Members of the earwig family Chelisochidae very attractive for the fly and selective, especially (order Dermaptera). for females. Use of McPhail traps baited with  Earwigs hexanol is very effective for monitoring and pos- sibly for control of this fly. Addition of 2% ammonium sulphate in the trap water enhances Black Fig Fly (Diptera: trap effectiveness. Proteinaceous bait sprays are Lonchaeidae) recommended when better control is needed.

byron katsoyannos Aristotle University of Thessaloniki, ­Thessaloniki, Greece

The black fig fly, Silba adipata McAlpine, is a pest of wild and cultivated figs, Ficus carica L. (Moraceae), occurring in the Mediterranean coun- tries and Iraq. This insect was studied extensively by Silvestri in Italy at the beginning of the twenti- eth century, although he misidentified it as ­Lonchaea aristella Becker. The adult is glossy black, Black Fig Fly (Diptera: Lonchaeidae), 3.5–4.5 mm in length, with reddish eyes and brown ­Figure 50 Adult black fig fly (after Silvestri, 1917). Black Flies (Diptera: Simuliidae) B 525 References Approximately 260 species are known from North America north of Mexico. Katsoyannos BI (1983) Field observations on the biology and The taxonomy of the family is based primar- behavior of the black fig fly Silba adipata McAlpine ily on features of the genitalia, legs, and wings of (Diptera: Lonchaeidae), and trapping experiments. J Appl Entomol 95:471–476 the adults; the cocoons and gills of the pupae; and Katsoyannos BI, Guerin PM (1984) Hexanol: a potent attrac- the head capsule and pigmentation patterns of the tant for the black fig fly,Silba adipata. Entomol Exp Appl larvae. Many species, however, are structurally 35:71–74 similar, if not identical, and are known as sibling Silvestri F (1917) Sulla Lonchaea aristella Beck. (Lonchaeidae) dannosa alle infiorescenze e fruttescenze del caprifico e species. They are typically revealed by studies of del fico. Bollettino del Laboratorio di Zoologia Agraria the banding patterns in the giant polytene chro- in Portici 12:123–146 mosomes of their larval salivary glands. Nearly a Talhouk AMS (1969) Insects and mites injurious to crops in quarter of the North American species, for exam- middle eastern countries. Monographien zur ange- wandte Entomologie 21:1–239, Paul Parey Verlag, ple, were first discovered chromosomally. ­Hamburg und Berlin, Germany The first three stages (egg, larva, pupa) of the life cycle are completed in running water. All types of flowing freshwater are exploited by black flies, Black Flies (Diptera: Simuliidae) from the smallest trickles to the largest rivers. Only a few species can tolerate polluted waters. peter h. adler The female black fly typically deposits its eggs Clemson University, Clemson, SC, USA either by dipping to the water’s surface during flight to release a few eggs at a time, or by crawling Black flies are small, morphologically homoge- about on wetted vegetation and stones while neous insects in the order Diptera, suborder Nem- releasing masses or strings of eggs. The eggs are atocera, best known for their economic impact as bluntly triangular, and a female can carry from biting and nuisance pests of humans and domestic about 20–800, depending on the species. Larvae animals. Adults are readily recognized by their hatch from the eggs within a few days to more arched thorax, cigar-shaped antennae and strong than half a year. They hold onto objects in the venation at the anterior margin of each wing. Black stream, such as rocks and leaves, by means of tiny flies breed abundantly in flowing freshwater – hooks at the end of the abdomen, which enmesh ­rivers and streams – throughout the world, from with a silken pad spun from the salivary glands 965 km north of the Arctic Circle to the southern- and applied to the substrate. The larval stage, most tip of South America. Within this vast realm, including six or seven instars, lasts from about a they are absent only from deserts and islands with- week to six months, depending on the species and out flowing water. The immature stages often attain water temperature. Mature larvae are 3–15 mm in large populations and play an important role in the length. Pupation occurs in flowing water, with a food web of streams and rivers. silken cocoon anchoring the pupa to the substrate. Worldwide, more than 1,700 species have Some species burrow slightly into the sand and silt been formally named and described, with the of the streambed to pupate. The pupal stage gener- expectation that this number will increase signifi- ally lasts no more than a few weeks. Some species cantly as study of the family continues. The world’s are univoltine, completing only one generation species are arranged in two subfamilies and about per year. Other species are multivoltine, producing 24 genera. The largest genus by far is Simulium, from two to about 15 generations in a year, depend- which occurs worldwide. The greatest number of ing on the latitude and species. species, more than one third of the known fauna, The majority of larval life is spent feeding. inhabits the Palearctic Region, especially Russia. Most species feed primarily by filtering particulate 526 B Black Flies (Diptera: Simuliidae) matter from the water column, using a pair of head bubble of air, buoyed to the surface with enough fans, with one fan projecting from each anterior force to break free of the water. The freshly emerged corner of the head. Food particles of an appropri- adult then flies to a resting spot where it tans and ate size, those less than 350 µm in diameter, often hardens its exoskeleton. include diatoms, bacteria, protozoa, pollen, and Adults (Fig. 51) are active during the day. They organic debris. Most species also can obtain food typically live less than a month, during which time by scraping it from the surface of stones and other they must mate and acquire food; females also objects in the stream. About 1.5% of the world’s must return to a stream or river to oviposit. The species do not have head fans and must obtain all adults of most species probably do not disperse of their food by scraping. These species live in more than 10 km, although some species regularly habitats, such as springs and glacial melt waters, travel more than 50 km in search of hosts. At least where little organic matter is present in the water one species in Africa has been reported to disperse column. Some species, in addition to filter feeding more than 500 km from the natal watercourses. and scraping, also prey on small arthropods in the Mating usually takes place shortly after emer- stream. gence. In many species, the males form aerial Larvae often space themselves in characteris- swarms over or beside landmarks such as trees, tic patterns depending on the species and water rocks, and waterfalls. Females fly into these swarms currents. The larvae of some species space them- and are intercepted by males. The coupled pair selves closely in moss-like clumps, others space quickly leaves the swarm. A small percentage of themselves rather widely, and still others pack so species, about 2% in North America, mate on the densely that they can exceed one million per square ground at their emergence sites. A similarly small meter. For most of their lives, larvae remain percentage of females do not mate. These attached to objects in the stream. When disturbed ­non-mating species consist of all-female, parthe- or relocating they loop short distances, inchworm nogenetic populations, and they occur at northern fashion, or release their hold of the silk pad and latitudes. drift downstream either freely or moored to a silk Both male and female black flies feed on water strand, eventually reattaching to a suitable ­substrate. and a source of carbohydrate, such as floral nectar Drift is particularly frequent at sunset and during and honeydew, that fuel their flight activities. Only the night, and is an important means of avoiding females feed on blood. The mouthparts of males are predation by fish and predacious arthropods. Larvae are susceptible to parasites and pathogens, including mermithid nematodes, protozoa, microsporidia, fungi, and viruses. Only a small percentage, perhaps about 1%, of a population is usually infected, although ­parasitized larvae often live longer than unin- fected individuals and become more apparent as the population ages and the healthy larvae pupate. Most parasites kill the larvae, but some pass through the pupae and into the adults, typically sterilizing the adult. Larvae of most species pupate singly, but those of some species form large clusters of pupae. Black Flies (Diptera: Simuliidae), Figure 51 The adult that has developed within the pupa Female black fly (from Cameron 1922; Canadian ­forcibly splits the pupal cuticle and emerges in a Department of Agriculture Bulletin). Black Flies (Diptera: Simuliidae) B 527 incapable of cutting skin. Females use their mandi- allergic reactions. More typical reactions include bles to snip the skin of warm-blooded animals, itching welts at the site where the person was while injecting various anesthetics and anti-clotting ­bitten. Outdoor industries and recreational activi- factors. As the capillaries are severed, a pool of ties often are severely curtailed by both nuisance blood forms, which is then imbibed. Not all species and biting species. have females that feed on blood. In less than 10% of Black flies transmit numerous blood protozo- the world’s species, the females have mouthparts ans, filarial worms, and perhaps a few viruses to much like those of the males, too feeble to cut ver- mammals and birds. Human-borne pathogens are tebrate flesh. These non-biting females typically transmitted by black flies only in Africa and parts occur in northern environments such as the arctic of Central and South America. The most common and are facultatively autogenous, meaning that by and serious human disease is onchocerciasis, or necessity, they mature their eggs without the benefit river blindness, caused by a filarial worm. Filarial of blood. The nutrient reserves for egg production worms also are transmitted to cattle, deer, moose, are carried over from the larval stage. black bears, and ducks, but apparently cause little Black flies use a wide range of hosts to acquire economic impact. The major avian pathogens a blood meal although many species are quite transmitted by black flies are malaria-like blood host- specific. For example, one species of black fly protozoans that cause a disease called leucocyto- feeds only on loons. Other species feed only on zoonosis. In North America, turkeys, ducks, and raptors, or only on small or large mammals. Still wild birds are affected. The consequences among other species appear to be true generalists. To domestic birds can be grievous and include locate their hosts, females use a series of cues such depressed immune systems, weight loss, decreased as color, shape, size, and odor. Carbon dioxide is reproduction, and even death. especially attractive. Species tend either to feed on Since the 1980s, the primary means of con- birds (ornithophily) or mammals (mammaloph- trolling pest populations of black flies has been ily). The bird feeders have a thumb-like lobe on with the bacterium Bacillus thuringiensis variety their claws, whereas most mammal feeders have israelensis (Bti), which produces a toxin highly simple or slightly toothed talons. specific to black flies and mosquitoes. When By virtue of their requirement for blood, applied to streams and rivers, Bti is an environ- black flies frequently become pests of humans mentally safe means of management, killing only and domestic animals. Only a fraction of the spe- larval black flies. Management programs are cies, about 15% in North America, actually causes ­operating in many parts of the world, including economic problems. The majority of species are Pennsylvania, Quebec, sub-Saharan Africa, and not attracted to humans and domestic animals Brazil. Some of these programs cost millions of but, instead, feed only on wildlife. Some of the dollars to conduct every year. pest species are primarily a nuisance, swarming about the head and entering the facial orifices. Those that take blood represent a more serious References threat, either through exsanguination, injection of toxic saliva (simuliotoxicosis), or the transmis- Adler PH, Currie DC, Wood DM (2004) The black flies ­(Diptera: Simuliidae) of North America. Cornell sion of disease agents. Some of the major cattle ­University Press, Ithaca, NY, 941 pp and poultry pests can cause weight loss, reduced Crosskey RW (1990) The natural history of blackflies. Wiley, egg and milk ­production, malnutrition, stam- Chichester, England, 711 pp pedes, stress-related afflictions, and even death. Kim KC, Merritt RW (eds) (1988) Black flies: ecology, ­population management, and annotated world list. Humans may develop fever, swollen eyes and Pennsylvania State University Press, University Park, glands, headaches, nausea, or even more severe PA, 528 pp 528 B Black Flies Attacking Livestock: Simulium arcticum Malloch and Simulium luggeri Nicholson & Mickel (Diptera: Simuliidae) Laird M (ed) (1981) Blackflies: the future for biological allergic reaction can cause death. While S. lug- methods in integrated control. Academic Press, New geri do not have toxic saliva, they swarm in huge York, NY, 399 pp numbers around the head, causing livestock to panic, often running into fences and being injured. Bacteria that cause “pinkeye” may be Black Flies Attacking Livestock: transmitted as black flies land to feed near the Simulium arcticum Malloch and eyes of several hosts. Simulium luggeri Nicholson & Mickel (Diptera: Simuliidae) Biology peter g. mason Agriculture and Agri-Food Canada Eastern Simulium arcticum has one or two generations per ­Cereal and Oilseed Research Centre, Ottawa, ON, year, and attacks only cattle and related animals. Canada This species prefers clean rocky locations in large, fast-flowing, silt-laden rivers such as the Atha- The livestock-attacking black flies,Simulium arcti- basca River in northern Alberta. Simulium arcti- cum Malloch and Simulium luggeri Nicholson & cum formerly was the dominant species in the Mickel, are important pests of cattle and wild Saskatchewan River but because of hydrological ungulates in the northern great plains of Canada. changes caused by hydroelectric developments it Other black fly species are pests of vertebrates ceased to be abundant including humans in other parts of the world. Simulium luggeri has up to five generations Females of S. arcticum and S. luggeri are greyish or per year and will attack humans as well as cattle. brownish with the dorsum of the thorax uniformly This species prefers somewhat clear, flowing water colored. They differ in appearance (the coloration of near the mouth of middle-sized rivers. The the tibia of the hind leg is entirely dark in S. luggeri, human-induced hydrological changes to the Sas- but the basal half is white in S. arcticum), and fea- katchewan River drastically reduced summertime tures of the genitalia. river volumes, effectively modifying it from a fast- flowing, silt-laden system to a slower-flowing, clear system. The once deep and turbid river became shallow, clear and slow flowing. This Damage encouraged the growth of massive vegetation beds on previously barren sand bars. This plant Economic losses occur due to the massive attacks substrate served as suitable attachment sites by female black flies seeking a bloodmeal needed allowing S. luggeri to replace S. arcticum as the for production of eggs. Dispersal in search of dominant species. Both black fly species have four hosts may be 150 km from the rivers where developmental stage, egg, larva, pupa, and adult. emergence and oviposition take place. In parts The eggs, larvae, and pupae are restricted to rivers of Saskatchewan and Alberta, black flies are lim- and streams. iting to cattle production. Cattle harassed by Eggs are tiny and trapezoid-shaped. They are attacking black flies become frightened and “bombed” on the water surface by gravid females bunch together to escape the blood-seeking flying over the river. The eggs sink to the substrate swarms. The cattle do not feed normally, result- where they become buried and pass the winter. In ing in reduced weight gain and milk production. spring hatching commences about two weeks after The saliva of S. arcticum is toxic to cattle and ice breakup. Black Flies Attacking Livestock: Simulium arcticum Malloch and Simulium luggeri Nicholson & Mickel (Diptera: Simuliidae) B 529 Newly hatched larvae drift downriver and Larvicides are more effective than adulticides attach to substrates such as clean rocks or vege- because larvae are concentrated in a relatively tation in the swiftest flowing water. Larvae go definable location in rivers or streams and less through seven instars or growth stages during insecticide is required to kill a substantial number about three weeks. Larvae of S. arcticum are of pest individuals. Larvicide is only applied when larger (0.9–mm) than those of S. luggeri (0.7–4.3 and where pest populations are detected. Exclusive mm). The brown or greenish-grey larvae feed by use of adulticide is ineffective because of the ­filtering nutrients from the water using head extreme ­difficulty in implementing it; it requires (cephalic) fans or by scraping algae from the sur- repeated (about every 10 days) applications of face of rocks using their mouthparts. When mature, insecticide spray or fog over large areas of ground the larva spins a cocoon and pupates within it. in affected communities. In addition, applying Pupae of S. arcticum have paired respiratory insecticide directly to cattle via backrubbers, filaments and pupation occurs within a boot- sprays, etc. has to be safe to the animals and shaped cocoon. Respiratory filaments of S. luggeri consumers of animal products. Control of pupae are grouped in threes and pupation occurs adults, however, can be ­useful as an additional within a slipper-shaped cocoon. After a few days emergency measure, especially on cattle during the adult escapes from the pupa and floats to the severe outbreaks. Bacillus thuringiensis israel- surface in an air bubble. ensis is an effective biological ­insecticide, with Adult male and female black flies feed on little environmental effect. nectar and other plant juices to sustain their Disease agents are commonly associated with energy requirements. Mating occurs soon after black flies but the life cycles are almost completely emergence, and females of biting species then unknown, so knowledge of agent transmission seek blood, which is required to produce eggs. between hosts is lacking. Mermithid nematodes After locating a host, settling on its skin, and are one of the most promising biological control inserting their blade-like piercing mouthparts, agents for black flies but their commercial devel- the females suck blood until they become fully opment is hindered by a lack of basic ecological engorged. After taking the blood meal they have information. expanded to twice their normal size. Engorged females seek suitable flowing water habitats in which they lay eggs on particular substrates. Black References flies are active during daylight hours but their rate of attack is highest during morning and ­afternoon. Crosskey RW (1990) Natural history of black flies. British On cloudy days or when storms are imminent Museum of Natural History, London, UK, 722 pp black flies may attack viciously at any time of day. Kim KC, Merritt RW (eds) (1987) Black flies: Ecology, pop- Winds can disperse large numbers of adults from ulation management and annotated world list. The Pennsylvania State University Press, University Park, breeding areas to surrounding regions, especially PA, 528 pp open farmland, and shifting winds may ­disperse Laird M (ed) (1981) Blackflies: The future for biological meth- black flies to other districts. Cold or rainy weather ods in integrated control. Academic Press, ­London, UK, temporarily ends an outbreak. 399 pp Mason PG, Shemanchuk JA (1990) Black flies. Agriculture Canada Publication 1499/E, Minister of Supply and Service Canada, Ottawa, Ontario, Canada, 8 pp Management Mason PG, Boisvert M, Boisvert J, Colbo MH (2001) Simulium spp., black flies (Diptera: Simuliidae). In: Mason PG, Huber JT (eds) Biological control pro- Control of black flies attacking livestock is achieved grammes in ­Canada 1981–2000. CABI Publishers, most effectively through use of insecticides. Wallingford, UK, pp 230–237 530 B Blackheaded Fireworm, Rhopobota naevena (Hübner) (Lepidoptera; Tortricidae) Blackheaded Fireworm, Black Pod of Cacao Rhopobota naevena (Hübner) (Lepidoptera; Tortricidae) This is an important insect-vectored disease of cacao. A caterpillar pest of cranberries in North  Transmission of Plant Diseases by Insects ­A m e r i c a .  Small Fruit Pests and Their Management Black Scale, Saissetia spp. (Hemiptera: Coccidae)

Black Grain Stem Sawfly, Several species of soft scale in the genus Sais­ Trachelus tabidus (Fabricius) setia, known as black scales, are pests of citrus (Hymenoptera: Cephidae) crops.  Citrus Pests and Their Management This is a pest of wheat in the northern hemisphere.  Wheat Pests and Their Management Black Scavenger Flies

Blacklegged Tick, Ixodes Members of the family Sepsidae (order Diptera). scapularis Say (Acari: Ixodidae)  Flies

This is a common pest of mammals in North America, and an important vector of Lyme Black Turfgrass Ataenius disease.   Ticks Turfgrass Insects and Their Management

Blackwelder, Richard Elliot Blacklight Trap Richard Blackwelder was born on January 29, An insect trap used for monitoring flying insects, 1909. His doctoral research was performed at particularly moths, that come to the ultraviolet Stanford University, California. That research pro- wavelengths produced by the “black” light source duced a (1936) monograph “Morphology of the associated with the trap. coleopterous family Staphylinidae” in which he  Traps for Capturing Insects acknowledges the help of his advisor, G.F. Ferris, and of R.E. Snodgrass. This work still is the fore- most on its subject. Then he published short works on the systematics of North American Tachypori- Black Parlatoria Scale, Parlatoria nae (1936, 1938) and Paederini (1939). After ziziphi (Lucas) (Hemiptera: ­graduation he became a Bacon Traveling Scholar Diaspididae) for the Smithsonian Institution (1935–1938) ­during which time he completed a 21-month col- This is an important pest of citrus crops. lecting trip to many West Indian islands (June  Citrus Pests and Their Management 1935 through March 1937), returning with 50,000 Blasticotomidae B 531 specimens mostly collected by hand or with a net. and another “Taxonomy” in 1967. He died on This culminated in his (1943) publication of a ­January 20, 2001. “Monograph on the West Indian species of the family Staphylinidae,” this work, which dealt with the 91 genera and 468 species known to him, has Reference not been bettered. In 1938–1940 he was Assistant Curator of the American Museum of Natural His- Herman LH (2001) Blackwelder, Richard Elliot. Bull Am Mus tory, and in 1940–1954 Assistant and Associate Nat Hist 265:46–47 Curator of the Smithsonian Institution. During these years he published short works on Lispinini and Osoriinae (1942) and the staphylinid beetles Blaisdell, Frank Ellsworth of the Cayman Islands (1947), and sundry other Frank Blaisdell was born in New Hampshire on papers including, with the help of his wife three March 13, 1862, and moved with his parents and supplements to the Leng catalog of North siblings to California in 1870. Despite lack of a American Coleoptera. His monumental works high school education, in 1887 he entered Cooper were (1944–1947, 1957) “A checklist of the Medical College in San Francisco, and graduated coleopterous insects of Mexico, Central America, two years later with the degree of Doctor of Medi- the West Indies, and South America” and (1952) cine. He worked in California at first as a medical “The generic names of the beetle family Staphylin- practitioner, and from 1900 as an academic at idae.” The first of these has been cited in just about Cooper College and then at Stanford University every subsequent biogeographic study including (into which Cooper College was absorbed). Ulti- neotropical Coleoptera and was of enormous mately he became Professor of Surgery, from importance. In the mid-1960s he explained to this which post he retired in 1927. His hobby for writer the reason for the much-delayed final part decades had been the collection and study of (1957), the bibliography, of the first work: that his ­Coleoptera, especially the families Tenebrionidae card index of bibliographic materials had and Melyridae. After retirement from medicine he ­disappeared during one of his absences from the worked from the Department of Entomology at Smithsonian Institution, and he had to rebuild it the California Academy of Sciences, to which he from his notes and reconsultation of the literature. deeded his collection of almost 200,000 ­specimens. The second undertaking, generic names, attempted He published 95 papers in entomology. He died on to apply the rules of the International Code of July 6, 1946. Zoological Nomenclature systematically across the mishmash of usage; although it shook up the established usage, it was largely correct and inevi- Reference table. Then he retired from life as a coleopterist and researcher and became a teacher, employed Mallis A (1971) Frank Ellsworth Blaisdell. In American ento- first at St. John Fisher College in New York state mologists. Rutgers University Press, New Brunswick, NJ, (1956–1958) and then at Southern Illinois Univer­ pp 278–279 sity (1958–1977). His tremendous energy as a researcher on Staphylinidae in his early years was directed elsewhere by the late 1950s, although he Blasticotomidae remained an active member of the Society of ­Systematic Zoologists, published works on A family of sawflies (order Hymenoptera, subor- ­systematics in Systematic Zoology and a book der Symphyta). “Classification of the animal kingdom” in 1963  Wasps, Ants, Bees and Sawflies 532 B Blastobasidae Blastobasidae another candidate was elected in 1910 as State Geologist, Blatchley retired, and spent the rest of A family of moths (order Lepidoptera). They com- his life working on subjects that appealed to him. monly are known as scavenger moths. He traveled abroad, within the USA, and fre-  Scavenger Moths quently to Florida where in 1913 he bought a  Butterflies “winter residence” that later he occupied for  Moths months each year. With Charles Leng, he ­published in 1916 “Rhynchophora or weevils of northeastern America”; as sole author he published in 1920 Blastoderm “The Orthoptera of northeastern America,” and in 1926 “Heteroptera or true bugs of eastern North The layer of cells in an insect embryo that sur- America.” His books included several of a less tech- rounds an internal yolk mass. The cellular blasto- nical nature but including observations on insects: derm develops from a syncytium by surrounding (1899) “Gleanings from nature,” (1902) “A nature the cleavage nuclei with membranes derived from wooing at Ormond by the sea,” (1906) “Gleanings the enfolding of the surrounding membrane. from nature,” (1912) “Woodland idylls,” (1931) “My nature nook,” (1932) “In days agone,” and (1934) “South America as I saw it.” He died in Indianapolis Blatchley, Willis Stanley on May 28, 1940, surviving his wife, Clara, by 12 years. His collection of insects, including 470 Willis Blatchley was born on October 6, 1859, in ­holotypes, was given to Purdue­ University. Connecticut, but he grew up on a farm in Indiana that his parents bought in 1860. In 1879, after tak- ing a six-week training course, he became a coun- Reference try school teacher, and it was not until 1883 that he entered Indiana University, majoring in natural A Mallis (1971) Willis Stanley Blatchley. In: American ento- mologists. Rutgers University Press, New Brunswick, NJ, science and graduating four years later. From 1887 pp 272–278 to 1894 he worked as head of a high school science department. In the first four years of that period he conducted thesis research (a thesis entitled Blattaria “The Butterflies of Indiana”) toward an M.A. degree, awarded in 1891, again from Indiana Uni- An order of insects, also known as Blattodea. They versity. His third degree was an honorary LL.D., commonly are known as cockroaches. awarded in 1921 by the same institution. Schools  Cockroaches have long summer vacations, and Willis Blatchley found summer employment with the Indiana State Blattellidae Geological Survey or with the U.S. Fish Commis- sion. The first employment experience may have A family of cockroaches (order Blattodea). helped when in 1894 he won the elected position  Cockroaches of Indiana State Geologist, and held it for 16 years. His duties were not just as geologist, but also to work on natural resources and natural history. The Blattidae years 1906–1910 found him working on “Coleop- tera of Indiana” as Bulletin 1 of the Indiana Depart- A family of cockroaches (order Blattodea). ment of Geology and Natural Resources. When  Cockroaches Blister Beetles (Coleoptera: Meloidae) B 533 Blattodea the pro-, meso-, and metathoracic tarsi, respec- tively. The color is variable; though often somber, An order of insects, also known as Blattaria. They some are metallic. Body hairs often are absent but commonly are known as cockroaches. Cockroaches sometimes dense. The pronotum of blister beetles is narrower than the head and thorax. The legs are long, and the body is unusually soft for a beetle. Blephariceridae The body is often elongate, with the elytra flared at the tips. However, body form varies considerably A family of flies (order Diptera). They commonly and though wings usually are normal, some ­species are known as net-winged midges. have short wings and elytra, and are flightless.  Flies The immature display hypermetamorphosis. Ovi- position takes place on the soil, and young larvae ­(triungulins) disperse to feed on grasshoppers Blind Springtails eggs, or the eggs, larvae and provisions (usually pollen) of ground-nesting Hymenoptera. Once A family of springtails (Onychiuridae) in the order attaining a food supply, the larvae lose their Collembola. ­mobility. When disturbed, the adults display reflex  Springtails bleeding, wherein cantharidin-containing blood is released, principally from the femoral-tibilal joints. Blister Beetles (Coleoptera: Cantharidin is a toxic terpenoid that likely imparts Meloidae) some protection from predation, though it also seems to have a role in communication. The bee- tles also may display death feigning. Cantharidin Blister beetles are an interesting group of insects, is produced by larvae, but in the adult stage only both because of their unusual larval development by the males. It is transferred to females at mating, and because of their toxic effects on humans and and occurs in the eggs. livestock. They are widely distributed, but are absent from New Zealand and Antarctica. They are most abundant in warm, dry climates. They number about 3,000 species. Their classification is Life Cycle as follows: Order: Coleoptera Following is an account of black blister beetle Suborder: Polyphaga development, which is typical of many species. In Superfamily: Tenebrionoidae black blister beetle is a single generation per year, Family: Meloidae with overwintering occurring in one of the larval Subfamily: Eleticinae instars. The eggs are deposited within a cavity in Subfamily: Meloinae the soil, in clusters of 100–200 eggs. Because the Subfamily: Nemognathinae likelihood of surviving is so small, blister beetles Subfamily: Tetraonycinae produce very large numbers of eggs, sometimes up to 10,000. The larval instars of black blister beetle are Characteristics quite varied in appearance, reflecting the unusual biology of the insect, called hypermetamorphosis. These are medium-sized beetles (usually 3–30 Unlike most insects, the ovipositing female does mm, but some up to 70 mm) with 7–11 antennal not locate a food source for her offspring, appar- segments. There are five, five and four segments on ently depositing her eggs randomly. Thus, when 534 B Blister Beetles (Coleoptera: Meloidae) young larvae hatch they must dig to the surface larvae. Undoubtedly starvation of first instars is a and disperse to find a host insect on which to feed. very important factor during most seasons, and The first instar is thus quite mobile, and equipped cannibalism is prevalent among larvae. Antlike with long legs with which to disperse. First instars flower beetles (Coleoptera: Anthicidae), false ant- explore cracks, crevices, and depressions in the soil like flower beetles (Coleoptera: Pedilidae), and as they search to find a host. Usually a single egg is some plant bugs (Hemiptera: Miridae) have been adequate for complete development of the first implicated as mortality agents of blister beetles. The instar. The number of instars is normally 6–7. The larva of the blister beetle Epicauta atrata (Fabricius) larvae are creamy white or yellowish white in color, has also been shown to be predatory on eggs of with brown head capsules. After the first instar the E. pensylvanica, and it is possible that other species larva moves little, and the legs become relatively within the genus are predatory (Fig. 52). shorter and shorter. The sixth instar does not feed, instead digging 2–3 cm into the soil and preparing a cell. The sixth instar may be followed by another Damage Caused by Blister Beetles nonfeeding instar, or by the pupal stage. The sixth and seventh instars bear only minute legs, and the Epicauta spp. and other blister beetles sometimes head capsule is reduced in size and retracted into feed on crops, though few are commonly destruc- the body. Black blister beetle larvae consume 21–27 tive. In North America, black blister beetle, eggs of Melanoplus differentialis Thomas during its ­Epicauta pensylvanica DeGeer, is usually the most larval development. This grasshopper, and some common species, and occurs everywhere in the other Melanoplus spp., produces 100 or more eggs, eastern United States and southern Canada west allowing more than one blister beetle to develop. If to the Rocky Mountains. Immaculate blister bee- blister beetle larvae encounter one another, how- tle, Epicauta immaculata (Say); spotted blister ever, they fight and only one survives. Many grass- beetle, Epicauta maculata (Say); and striped blister hoppers produce small egg pods, with less than 25 beetle, Epicauta vittata (Fabricius), are examples eggs, thereby limiting the ability of blister beetles to of other common crop-feeding blister beetles develop. The pupa resembles the adult beetle in Other genera of Meloidae occasionally affect form, though the legs and wings are folded against crops, but incidents of damage are isolated. Among the underside of the body, and there appears to be such occasional pests are Linsleya sphaericollis no tendency for diapause in this stage. The adult (Say) in the Rocky Mountain region and west to digs to the soil surface after pupation. the Pacific Ocean; Nuttall blister beetle, Lytta Other blister beetles sometimes require more ­nuttalli Say, throughout the west and east to than one year to complete a generation, or are Nebraska; and Meloe niger Kirby, which occurs ­multivoltine, depending on the favorability of the throughout the United States and southern Canada environment. The species feeding on bees differ in except for the southeastern states. that the eggs may also be deposited on foliage, where Blister beetle adults are found on alfalfa, clover, the young larvae are phoretic, attaching to adult bees soybean, and sugarbeet, as well as numerous and are transported back to the nest of the bee. ­vegetable and flower crops, fruit trees, and broad- leaf weeds. Adults often collect on goldenrod flow- ers, Solidago spp., in the autumn. Indeed, flowers are Natural Enemies often a preferred food of many species. Beetles tend to aggregate, apparently in mating swarms, so Surprisingly little is known concerning the natural ­damage can be severe in relatively small areas of a enemies of blister beetles, reflecting their minor crop and absent or trivial elsewhere. consumption ­status as crop pests and the subterranean habits of of foliage, in some instances they prefer blossoms. Blister Beetles (Coleoptera: Meloidae) B 535

Blister Beetles (Coleoptera: Meloidae), Figure 52 Representative blister beetles: upper left, Epicauta immaculata; upper right, Epicauta lemniscata; center left, Epicauta pensylvanica; center right, Epicauta andersoni; lower left, Meloe laevis; lower right, Lytta sp.

Preference of blister beetles for blossoms is the drying and preservation of hay, but also can most noticeable and potentially damaging in result in death of aggregations of ­blister beetles, alfalfa, where beetles congregate mostly during and incorporation of their bodies into the hay. periods of bloom. Aggregations of beetles can be Blister beetles, even dead individuals, contain a incorporated into alfalfa hay when it is baled, ­vesicating substance called cantharidin which, ­particularly if the stems are crushed as part of the when ingested, damages the digestive tract of harvesting ­process. Crushing, or crimping, aids in ­animals. Cantharidin also causes blisters to form 536 B Blister Beetles (Coleoptera: Meloidae) on the skin of ­sensitive humans who come into during, and immediately after, periods of grass- contact with crushed ­beetles, and in formation of hopper abundance. The larvae of many ­blister blisters in the mouths of livestock, ­particularly beetles, however, seem to feed principally on horses. This blistering action is the basis for the ground nesting bees and the bee’s nest provi- common name of the beetles. ­Cantharidin ­content sions. Their abundance fluctuates less, and they varies among species, ­ranging from 5% ­cantharadin provide no known agricultural benefits. There is in Epicauta immaculata to about 1% cantharidin even one instance in Canada where bee-feeding in E. pensylvanica. Despite the relatively low toxin blister ­beetles interfered with alkali bees being content in each beetle, large numbers can be managed for alfalfa pollination. ­incorporated into hay, and horses can ingest enough beetles to cause death. Cantharidin likely serves as a feeding deterrent to most predators, Management thereby protecting blister beetles and their eggs from consumption. However, some insects are Blister beetles are not usually pests, though they attracted to cantharidin, and this compound is may become quite abundant during and following involved in the chemical communication among long-term grasshopper population increases. blister beetles. ­Suppression of grasshoppers indirectly suppresses In times past in Europe the so-called “Spanish blister beetles by eliminating the food supply of fl y,” Lytta vesicatoria, acquired the undeserved the blister beetle larvae. Direct suppression of ­reputation as an aphrodisiac for horses. Likely ­blister beetles usually may not occur in conjunction ingestion of this insect irritated the animals, mak- with chemical treatment of grasshopper popula- ing them seem more restless and “spirited.” Thus, tions because the grasshoppers can occur earlier the beetle was sometimes administered to horses, in the season, when blister beetles are still in the and even sometimes to humans, but the effects can soil. Blister beetles are easily controlled by applica- be quite deleterious. tion of common insecticides to crop ­foliage, and small plantings can be protected with row covers or screening. Because some blister beetle is highly Beneficial Effects of Blister Beetles attracted to alfalfa, especially ­during periods of bloom, large numbers of blister beetles may The damage caused by Epicauta spp. blister bee- ­disperse to nearby crops following alfalfa harvest. tles is offset, at least during periods of relatively  Potato Pests and Their Management low beetle density, by the predatory behavior of  Beetles blister beetle larvae. Epicauta spp. larvae feed on the eggs of grasshoppers, including many crop- damaging Melanoplus spp. During periods of References grasshopper abundance the number of blister beetles tends to increase substantially. Studies of Bologna MA, Pinto JD (2001) Phylogenetic studies of egg pod destruction in western areas of the Meloidae (Coleoptera), with emphasis on the evolu- United States during a period of grasshopper tion of phoresy. Syst Entomol 26:33–72 Pinto JD, Bologna MA (2002) In: Arnett RH Jr, Thomas MC, abundance, for example, documented that 8.8% Skelly PE, Frank JH (eds) The American beetles, vol 2. of pods were damaged by blister beetles. CRC Press, Boca Raton, pp 522–529 Although the blister beetles eventually contrib- Pinto JD, Bologna MA (1999) The new world genera of ­Meloidae (Coleoptera): a key and synopsis. J Nat Hist ute materially to the suppression of grasshopper 33:569–620 population outbreaks, the higher numbers of Selander RB (1991) On the nomenclature and classification of blister beetles often cause greater crop injury the Meloidae (Coleoptera). Insecta Mundi 5:65–94 Blood Gill B 537 Blister Beetle Antennal Twisting around the female’s antennae. The ­sexual behavior Behavior of Meloidae­ has been studied in detail. However, entwining of male and female antennae has not yien-shing chow been reported before. The observed ­frequencies of National Museum of Natural Science, Taiwan, right-handed and left-handed antennal pairs were Republic of China 46.7 ± 13.9% and 44.8 ± 12.5%, respectively.  Blister Beetles The blister beetle,Epicauta hirticornis, has an inter- esting pre-copulating behavior. When a male dor- References sally mounts a female, the male continuously waves its antennae toward the female’s antennae. Eventu- Selander R (1964) Sexual behavior in blister beetles (Coleoptera: ally, the male’s right or left antenna, or sometimes Meloidae). I. The genus Pyrota. Can Entomol 96:1037–1082 both, grasps the corresponding female antennae Pinto JD (1975) Intra-and interspecific courtship behavior in and wraps around the female antennae (Fig. 53). blister beetles of the genus Tegrodera (Meloidae). Ann Entomol Soc Am 68:275–285 In northern Taiwan, blister beetles ­usually are found aggregating on the leaves of blooming ­glorybower tree, Clerodendrum cyrtophyllum Blood Gill Turcz, and a novel sexual behavior was observed. During their courtship, a male beetle mounts a A gill that lacks tracheae. In such gills, oxygen female from behind and the male’s antenna winds passes directly into the blood instead of entering

Blister Beetle Antennal Twisting Behavior, Figure 53 Pre-copulating behavior of the blister beetle ­Epicauta hirticornis. (a) A male mounts a female on the leaves of Clerodendrum cyrtophyllum. Their ­antennae are twisted to the right. (b) Both male antennae are entwined with the female's antennae; right-handed and left-handed structures are seen pointing backwards. 538 B Blow Flies tracheae. Blood gills are found in some aquatic Bluetongue Disease insects.  Tracheal System and Respiratory Gas Exchange walter j. tabachnick University of Florida, Vero Beach, FL, USA Blow Flies Bluetongue disease is an insect transmitted ­disease that occurs primarily in sheep and wild ruminants. Members of the family Calliphoridae (order The bluetongue viruses that cause the disease are Diptera). members of a family of viruses called orbiviruses.  Flies Although cattle in many regions of the world are  Myiasis often infected with bluetongue virus, cattle rarely show clinical signs of this disease. Blueberry Maggot, Rhagoletis mendax (Curran) (Diptera: Tephritidae) Insect Vectors

This is an important pest of blueberry in North Bluetongue viruses can be found in the tropics and America. subtropics throughout the world. The viruses are  Small Fruit Pests and Their Management transmitted by insect species within the genus Culicoides, Family Ceratopogonidae. Various ­species of Culicoides transmit bluetongue virus. Bluebottle Flies Different regions of the world contain different species of Culicoides involved in bluetongue virus Members of the family Calliphoridae (order transmission. In South America, Culicoides insig- Diptera). nis is the primary vector of bluetongue virus. In  Flies Africa, the primary bluetongue vector is Culicoides  Myiasis imicola, while in Australia the primary vectors are Culicoides brevitarsis and Culicoides wadai. The Bluegrass Billbug, Sphenophorus Culicoides vectors of the bluetongue viruses in parvulus Gyllenhall (Coleoptera: parts of Asia include Culicoides imicola. However, Curculionidae) the Culicoides vectors in large parts of Asia have yet to be identified. Bluetongue virus transmission does not occur anywhere in the world in the This is an important pest of turfgrass in North absence of bluetongue-competent Culicoides ­vector America. species. The primary North American­vector of the  Turfgrass Insects of the United States: Biology bluetongue viruses is a member of the Culicoides and Management variipennis complex, Culicoides sonorensis.

Blues The Disease Some members of the family Lycaenidae (order Lepidoptera). The most severe clinical signs of bluetongue  Gossamer-Winged Butterflies ­disease occur in sheep. Sheep with bluetongue  Butterflies ­disease show a rise in temperature lasting 5–days.  Moths There can be swelling of the buccal and nasal Bluetongue Disease B 539 mucosa, swollen tongue, profuse salivation, hem- has been essentially free of bluetongue virus orrhages in the membranes of the mouth, and although there have been a few periodic outbreaks hemorrhages in the bands of the hoof, which often in Spain and Portugal due to Culicoides imicola. leads to lameness. Sheep may vomit because of Bluetongue outbreaks in sheep in Europe occurred lesions in the esophagus and pharynx. This sign for the first time in 2001–2002 in ­Bulgaria, France can lead to their aspirating the contents of their (Corsica), Italy (Sardinia) and Greece. The vectors rumen, in pneumonia and frequently in death. of these outbreaks were not identified, although Sheep mortality to bluetongue infection may range some appear to have involved Culicoides imicola. from 5 to 50% of animals infected with virus. Although clinical signs in cattle are rare, early prenatal infection with bluetongue in cattle may lead Impact and Problems to embryonic death. Cattle develop a very prolonged viremia lasting several weeks where bluetongue The presence of severe bluetongue disease can virus can be detected in blood and is available to have disastrous consequences on sheep popula- infected susceptible Culicoides. As a result cattle tions. Consequently, in an effort to reduce the are considered important reservoirs for the virus potential importation of a bluetongue-infected and play an important role in ­infecting susceptible animal and the possibility of a bluetongue out- Culicoides vectors and therefore in the disease break, many countries impose restrictions on the ­transmission cycle in more susceptible ruminants. movement of livestock to their country from any In the western and southern regions of the United country where bluetongue is prevalent. The Office States where Culicoides sonorensis is present, there of International Epizootics is the international are regions where it is not uncommon to find 50% agency responsible for developing regulations to or more of the cattle to have once been infected with protect animals around the world. This agency bluetongue virus. These ­animals are known to have develops regulations for animal trade between once been infected because they contain antibody countries. In the case of bluetongue, the regula- to one of the United States bluetongue viruses in tions in place provide for the safe movement of their blood. The presence of antibody to a virus is livestock from bluetongue areas to bluetongue free ­evidence of a previous infection. areas. For example, the United States, where one of five bluetongue serotypes may be found in ­cattle, has restrictions imposed on its animal export to The Viruses countries in the European Union that do not have bluetongue virus. United States animal exports There are 24 different serotypes of bluetongue virus must be tested and certified as being free of blue- distributed throughout the world. The viral sero- tongue before they can be approved for shipment. types are numbered 1–24 and, as with the different This results in lost trade opportunities for United species of Culicoides vectors, the serotypes also are States animal exports. The worldwide result is that found in specific regions of the world. There bluetongue is the cause of non-tariff trade barriers appears to be an association with the particular costing millions of dollars in testing and lost Culicoides vector species in a region and the trade opportunities on the international livestock ­specific bluetongue virus serotypes found in the market. geographic region. North America has five blue- The northeastern region of the United States tongue serotypes (2, 10, 11, 13, 17), Australia has does not contain the bluetongue vector species, eight serotypes (1, 3, 9, 15, 16, 20, 21, 23), Africa has Culicoides sonorensis. There is no evidence of 21 (1–19, 22, 24) Central America and the Carib- bluetongue virus transmission to livestock in this bean region has eight (1, 3, 4, 6, 8, 12, 14, 17). Europe region. Such information is essential to declare a 540 B Boat Flies bluetongue free region within a country that could very numerous insects is a daunting control chal- result in improving the livestock trade opportuni- lenge. Outbreaks and problems with bluetongue ties for the specific region despite restrictions on subside due to weather and climatic conditions bluetongue transmission regions within the same that naturally reduce Culicoides populations. country. The economic costs due to bluetongue ­Culicoides control has not been shown to interrupt are considerable due to its impact on the interna- bluetongue transmission. tional livestock market and may approach billions of dollars. Several different types of bluetongue virus References vaccines are available for use in domestic livestock. Unfortunately, each bluetongue serotype requires a Gibbs EPJ, Greiner EC (1989) Bluetongue and epizootic specific vaccine for protection. These vaccines have ­hemorrhagic disease. In Monath TP (ed) The arbovi- ruses: epidemiology and ecology. CRC Press, Boca met with varying degrees of success. Some blue- Raton, FL, pp 39–70 tongue vaccines are attenuated forms of the virus Tabachnick WJ (1996) Culicoides variipennis and that were manufactured using techniques to reduce ­bluetongue-virus epidemiology in the United States. their virulence in animals. Their advantage is that Ann Rev Entomol 41:23–43 Walton TE, Osburn BI (eds) (1992) Bluetongue, African they can provide protection after a single or booster horse sickness and related orbiviruses. CRC Press, Boca injection, but unfortunately some have become Raton, Florida, 1042 pp virulent in the animals or after they have been picked up by blood feeding Culicoides. Killed virus as vaccines has been used and these do not become Boat Flies virulent, but often require more boosters to be effective. Bluetongue vaccines have been perfected Members of the family Notonectidae (order using molecular biology technology. Unfortunately, Hemiptera). the commercial prospects for many bluetongue  Bugs vaccines have not been realized so that there has been little commercial interest in their develop- ment and use. In the United States, lack of interest Bodenheimer, Friedrich in the commercial use of bluetongue vaccines is (Frederick) Simon due to several factors. Use of bluetongue virus vac- cines must face the challenge that naturally infected Friedrich Bodenheimer was born in Cologne on animals must be readily distinguishable from vac- June 6, 1897. He was accepted into medical school cinated animals. Undistinguished vaccinates would in 1914 in Munich, but soon volunteered for not be acceptable for international movement, and ­service in World War I in the German army. He vaccinated animals should not inhibit or mask served on the eastern front, realized the level of ­naturally occurring infection that would prevent anti-semitism that existed, resolved eventually to the early detection of an outbreak. Since only cattle emigrate to Palestine (now Israel), and decided to used for export are impacted by bluetongue, there study entomology as a profession that would be is little economic incentive for using the vaccine on useful in Palestine. He completed his studies at the large numbers of United States cattle used for Universität Bonn by 1922, and with a doctorate in domestic purposes. This reduces the need and philosophy (and specialty in entomology). Before commercial value for any vaccine. he left for Palestine, he visited the natural history Although Culicoides control is an option to museum in Hamburg, and chose to spend time prevent or interrupt a bluetongue virus outbreak in studying Coccoidea. His viewpoint was that every domestic animals, the biology of these small and entomologist should have a thorough taxonomic Bogong Moth, Agrotis diffusa (Boisduval) (Lepidoptera: Noctuidae) B 541 understanding of one group of insects. His choice Body Lice of Coccoidea proved appropriate for his future work in Israel. Next, and still before leaving Europe, Members of the family Pediculidae (order he spent six months at the R. Scuola Superiore di Phthiraptera). Agricoltura di Portici in Italy. There, he was able to  Chewing and Sucking Lice study with Grandi and Silvestri, in an environment  Human Lice similar to that of Palestine. He moved to Palestine in 1922 and took up his appointment as head of the Division of Entomology (in fact the only ento- Bogong Moth, Agrotis diffusa mologist) of an Agricultural Experiment station (Boisduval) (Lepidoptera: (in fact the yard of a high school) in Tel Aviv. Noctuidae) His first task in Palestine was to inventory the pest species. He did this as a book (1931) “Die In most respects, Bogong moth is a typical cutworm, Schädlingsfauna Palästinas.” In 1923 he married and is one of the more important and widespread Rachel Ussishkin, and enlisted her help in review- cutworms in Australia. However, it is distinguished ing pre-Linnean entomological works to produce by its migratory tendencies: dispersal into the his (1928–1029) “Materialen zur Geschichte der ­Australian mountains for a period of aestivation Entomologie bis Linné,” a history of entomology. during the summer, followed by dispersal back to In 1928, he moved to the Hebrew University in the plains in the cooler months. In this respect (as Jerusalem as professor of zoology and was required well as morphology) it is quite similar to an American to lecture to students. A difficulty was that he was species, Euxoa auxiliaris (Grote), also known as required to lecture in Hebrew, that he did not army cutworm. However, bogong moth is an inter- speak Hebrew, and there were no Hebrew texts for esting and well-known element in the culture of the the subjects in which he was required to lecture; aboriginal people of Australia, where historically eventually, he compiled the necessary textbooks, the moths were collected for human consumption, publishing nine of them (and later four in Turkish so there is an unusual element of cultural anthro- and one in French). He continued his interests in pology associated with this moth. agricultural pests and published (1951) “Citrus Bogong moth inhabits principally the pas- ­entomology in the middle east,” and (1957, with E. ture-land west of the Great Dividing Range of Swirski) “The Aphidoidea of the middle east.” His eastern Australia (Victoria, New South Wales, professorship in zoology and acquired knowledge Queensland), but during the summer months the over 25 years in entomology and broader aspects moths migrate to higher country. In particular, of zoology induced him to write (1958) “Animal they aggregate near Mount Bogong in the Alpine ecology to-day,” in which he emphasized the National Park, which serves as the basis of their importance of climate. He published more than common name. During the summer, they congre- 420 works. In 1948, although deemed too old for gate in caves and rock crevices until autumn, military service, he nevertheless served in the when they return to the plains to deposit their Israeli army, and was twice wounded. He died on eggs. They can accumulate in tremendous num- October 4, 1959. He was a legendary figure, the bers on the floors and sides of the caves. The founder of entomology in Palestine (Israel). moths are highly nutritious, and the Aborigines traditionally have taken advantage of this resource Reference and collected them by knocking them into bark, kangaroo skin containers or nets, and then roast- Harpaz I (1984) Frederick Simon Bodenheimer (1897–1959): ing them in the hot ashes of a fire to remove the idealist, scholar, scientist. Ann Rev Entomol 29:1–23 wings and legs. The moth carcasses were mashed 542 B Bohart, Richard M together into “moth meat,” which is said to have a Rocky Mountains. Perhaps the bogong moth also nutty flavor resembling almonds or walnuts. They sustains itself during the summer by nocturnal were formed into cakes, and if smoked, preserved feeding. well for a week or longer. The fat content is 50–60%, and harvest of moths by aborigines early in the twentieth century is estimated at several tons Economic Importance annually. Some tribes harvested the moths for 2–3 months annually, so the moths were a staple of the Although bogong moth is an important food aboriginal diet, not just a minor component. source for wild vertebrate animals and of the indigenous people of Australia, it is also consid- ered to be damaging to some crops. Larvae feed on a variety of wild broad-leaf herbaceous plants such Life Cycle and Description as cape weed, Cryptostemma calendula (Asteraceae), but do not thrive on grasses. Among cultivated Eggs are deposited at the base of plants near the plants damaged are alfalfa, linseed, cereal grains, soil in the autumn after moths have descended cabbage, cauliflower, and English peas. from the mountains. The eggs soon hatch and the These moths also can be a nuisance. Some- winter months are passed in the larval stage. ­Lar- times strong wings carry the moths over the vae initially are cream-colored, but later become mountains to the cities of the eastern seaboard of green with pale and dark stripes, and dark spots. Australia, and great numbers invade cities such as Overall, they are dark dorsally and pale ventrally, Canberra, Melbourne and Sydney. with a dark head and prothoracic plate. They  Army Cutworm attain a length of about 5 cm. They hide in the  Native American Culture and Insects soil during the day, emerging at night to ascend  Entomophagy: Human Consumption of Insects plants and to feed. The larvae mature in spring, pupate in the soil, and after about a month the References adults emerge to feed on nectar at flowers. The adults are variable in color, ranging from brown Common IFB (1952) Migration and gregarious aestivation in to almost black. ­However, they typically bear a the bogong moth Agrotis infusa. Nature 170:981–982 dark streak on each forewing that is interrupted Common IFB (1954) A study of the ecology of the adult by a light circular spot and a light bean-shaped bogong moth Agrotis infusa (Boisd): (Lepidoptera: light-colored spot. The hind wing is light brown ­Noctuidae). Aust J Zool 2:223–263 Flood J (1980) The moth hunters. Aboriginal prehistory of the with a darker border. The wingspan is about 5 cm. Australian Alps. Australian Institute of Aboriginal The adults migrate to the mountains for the ­Studies, Canberra, Australia summer months, returning to the lower pasture- lands in the autumn. In the mountains, the moths are reported to fly but not to feed. Interestingly, Bohart, Richard M the American equivalent of bogong moth, army cutworm moth, was until recently thought to aes- Born on 28 September 1913 in Palo Alto, California, tivate during the summer months in the Rocky USA, Bohart became interested in insects as a young Mountains, where aggregations are fed upon by child, and went on to earn three degrees in entomo­ grizzly bears, but not by the indigenous people of logy at the University of California at Berkeley. He the region. Army cutworm has since been shown taught at the University of California at Los Angeles to feed at night on flowers at high altitudes of the (UCLA) from 1938 to 1941 before enlisting in the Boisduval, Jean-Baptiste Alphonse Dechauffour De B 543 U.S. Navy. He joined the faculty of the University of him to travel and collect insects. In 1841, he was California at Davis in 1946 and retired in 1980. appointed head of the entomological section of Bohart is known for his contributions on the the natural history museum of Stockholm. He gave systematics of wasps and mosquitoes. He authored his collection to the museum, and during the over 200 publications, including six books. ­following 26 years he built the museum’s collec- ­Foremost are “Sphecid Wasps of the World” (with tions considerably. His greatest published works A.S. Menke) and “The Chrysidid Wasps of the were his descriptions of new ­species in eight ­volumes World” (with L.S. Kimsey). Over the years, he of Schönherr’s “Genera et species ­curculionidum” acquired an outstanding collection of Nearctic (1833–1845), his “Insecta Cafrariae” (1838–1857) Hymentoptera. He also acquired a number of and “Monographia cassididarum” (1854–1862). He ­successful graduate students who went on the published about 50 important papers, and was the populate museums, state departments of agriculture, describer of the boll weevil, Anthomonus grandis. and universities. Indeed, his love of students was In 1867 he resigned from his position, but ­continued said to be surpassed only by his affection for wasps. to work at the museum until just a few days before He died on 1 February 2007, but will long be his death in Stockholm on November 2, 1868. remembered as one of the world’s most important hymenopterists. References

Reference Stål C (1869) Notice nécrologique sur C.-H. Boheman. Annales de la Société Entomologique de France 9:105–106 Garvey KK (2007) Richard M. Bohart. Am Entomol 53:58–59.

Bohartillidae Boisduval, Jean-Baptiste Alphonse Dechauffour De A family of insects in the order Strepsiptera.  Stylopids Jean-Baptiste Boisduval (Fig. 54) was born in Normandy, France, on June 17, 1799. He was employed by Dejean as curator of the latter’s Boheman, Carl Heinrich insect collection. With Lacordaire as co-author, he published (1835) “Faune entomologique des Carl Boheman was born in Jönköping, Sweden, on environs de Paris…” which follows the same July 10, 1796. From the age of eight, he showed an theme as Fourcroy’s (1785) work. He became interest in entomology. He asked permission of his one of the most famous lepidopterists of France, father to study Latin, because Latin was necessary was one of the original members of the Société to read publications on natural history, although ­Entomologique de France, and an honorary his father expected him to become a businessman. member in 1866. In 1860 he was awarded In 1812, he became a student at the university of ­honorary membership in the Société Ento- Lund, and began to study law, but abandoned this mologique de Belgique. He collected not only in 1813 to enter the Swedish army. His army career Lepidoptera (acquired not only from Europe gave him spare time for his favorite occupation, but from North America too) but also Coleoptera ­entomology, but he retired from the army in 1844 and Hemiptera, and published about 50 works. with the rank of captain. His army career allowed He died in Normandy on December 30, 1879. 544 B Bokor, Elemér XI., 1913, and Három új vakbogár Magyarország faunájából. Annales Musei Nat. Hung. XI., 1913). He fought on the Russian Front in World War I as a professional officer of the Austro-Hungarian army. He suffered the life of a prisoner of war in Russia for some years. On his return to Hungary in 1921 he researched the arthropod fauna of 102 caves. In 1923 he surveyed the Abaligeti Cave and the result of this work formed the basis for his doctoral disser- tation. He received his doctorate in 1924. Elemér Bokor devoted his life to the research of the Hungarian caves. He has described several new species of cave dwelling coleoptera. He was the president of the Boisduval, Jean-Baptiste Alphonse Dechauffour Hungarian Speleological Society as well as the De, Figure 54 Jean-Baptiste Boisduval. ­Entomological Society, providing great impetus to the work of his colleagues. His collection of Lepidoptera was sold in France, his Elateridae are in the Natural History Museum References (London), and the type specimens of his Curcu- lionidae in Brussels. Balázs D (1993) Magyar utazók lexikona. Panoráma, ­Budapest, Hungary Székely K (1987) 100 éve történt. Karszt és Barlang. Budapest, References Hungary

Anon (1880) Jean-Baptiste Alphonse Dechauffour de Boisduval.­ Entomologist 13:1–19 Bolitophilidae Anon (1880) Dr. Boisduval. Entomologist’s Monthly Maga- zine 16:235–236 A family of flies (order Diptera). Essig EO (1931) In A history of entomology. The Macmillan  Flies Company, New York, NY, pp 559–562

Boll Rot of Cotton Bokor, Elemér This is an insect-transmitted disease of cotton. george hangay  Transmission of Plant Diseases by Insects Narrabeen, NSW, Australia

Elemér Bokor was born on the 19th of January Boll Weevil, Anthonomous grandis 1887, at Sátoraljaújhely, in the North- Eastern Boheman (Coleoptera: ­corner of Hungary. As a young man he was already Curculionidae) interested in entomology and in the beetles which lived in caves. Although he received a military This insect, known also as the cotton boll weevil, is ­education, he carried on with his nature studies, a very serious pest of cotton in the western and in 1913 he published some important works ­hemisphere, and has had a significant effect on the on the blind cave-dwelling beetles (új vakbogarak history of the United States. Little was known about Magyarország faunájából. Annales Musei Nat. Hung. it until about 1892 when it appeared in Texas, Boll Weevil, Anthonomous grandis Boheman (Coleoptera: Curculionidae) B 545 ­having moved northward from Central America or Description and Life History Mexico. Once it reached the United States, it spread rapidly to the north and east, and slowly to the Boll weevil is capable of completing its life cycle west, eventually reaching California in 1982. In the in 25 days, so 8–10 generations are possible early part of the twentieth century, little could be annually. The adult stage overwinters, emerg- done to prevent damage by this insect, and the ing from beneath leaf debris, bark, trash and agricultural economy of the southeastern United other protected places from March to June. It States was seriously disrupted by this insect. begins to feed immediately and as squares Numerous farms, cotton gins and related interests become available they begin production of eggs. such as stores and banks ceased business because Females can produce from 100 to 300 eggs. The the cotton crop was destroyed. On the other hand, white eggs are about 0.5 mm long. The eggs the appearance of boll weevil in the southeast stim- hatch in 3–4 days, and the larva feeds within ulated the diversification of the economy because the square or boll. The larva is white and legless,­ the residents could no longer depend exclusively with a brown head. It matures in about 9 days on cotton for their livelihood. Thus, the commu- and measures about 13 mm in length. There are nity of Enterprise, Alabama erected a statue in rec- three larval instars, which can be distinguished ognition of the beneficial side effects of this by head capsule width measurements (0.4, 0.6, devastating pest (Fig. 55). Much later in the cen- and 09 mm, respectively for instars one to tury boll weevil gained entry to South America. It three). At maturity, it forms a pupa within the now infests cotton growing regions of Argentina, feeding cavity, and then the adult emerges in Brazil, and Paraguay. about 5 days. The adult is gray or brown to black in color, measures about 4 mm in length, and bears a long snout. In the autumn the ­weevils leave the crop for sheltered (Fig. 56) areas and enter diapause. Diapause is a critical period for boll weevils, and survival is enhanced when weather is moister and above average in temperature.).

Boll Weevil, Anthonomous Grandis Boheman Boll Weevil, Anthonomous Grandis Boheman ­(Coleoptera: Curculionidae), Figure 55 Boll weevil (Coleoptera: Curculionidae), Figure 56 Adult statue in Enterprise, Alabama (photo USDA, boll weevil feeding on a cotton boll (photo USDA, ­Agricultural Research Service). ­Agricultural Research Service). 546 B Bombycidae Host Plants insects has eliminated boll weevil over much of its former range. Though initially costly, elimination Boll weevil feeds exclusively on malvaceous host of this key pest brings substantial ­savings to gro- plants, principally cotton but also okra, hollyhock, wers in the long run. and hibiscus.  Area-Wide Insect Pest Management

Damage References

Boll weevils cause injury when the adults chew Hunter WD, Hinds WE (1905) The Mexican cotton boll wee- into the square (blossom) and boll (fruit) where vil. USDA Bur Ent Bull 51:45–46 they feed and deposit eggs. The larvae also feed Hunter WD (1917) The boll weevil problem with special ref- erence to means of reducing damage. USDA Farmers’ within these structures, and little or no fiber is Bull 48:1–40 formed. Hunter WD (1922) The boll-weevil problem: methods of reducing damage. USDA Farmers’ Bull 1262:1–31 Gaines RC (1959) Ecological investigations of the boll weevil, ­Tallulah, Louisiana, 1915–1958. USDA Tech Bull Management 1208:1–20 Palmer JO, Cate JR (1992) Overwintering survival of pre Boll weevils are most effectively managed by a reproductive and post reproductive boll weevils (Coleoptera: Curculionidae) in central Texas. Environ combination of approaches. Some of the approaches Entomol 21:117–120 include:

1. Early destruction of plants in the field. Early har- vest and destruction of crop residue kills many Bombycidae weevils and deprives them of shelter. 2. Use of an early maturing cultivar. Early maturing A family of moths (order Lepidoptera). They com- varieties produce blossoms before many weevils monly are known as silkworm moths. are present, whereas late maturing varieties are  Silkworm Moths attacked by higher numbers of insects, thereby  Butterflies and Moths ­experiencing more damage. Proper agronomic practices also encourage rapid growth and matu- rity of the crop, hastening development before the end of the season when weevils are most abun- Bombyliidae dant. 3. Insecticide. Application of insecticide can allevi- A family of flies (order Diptera). They commonly ate weevil injury. Applications are made early to are known as bee flies. control weevils during blossom set and maturity.  Flies Applications may also be made late in the year to reduce the number of weevils entering diapause, and thereby reducing the number emerging in the spring of the following year. Bonnet, Charles 4. Eradication. An eradication program is currently under way in the United States. A combination of Charles Bonnet was born in Geneva in 1720 and host destruction, insecticide application, trapping remained in Switzerland all his life. He received with pheromone-based traps, and release of sterile training in law, and practiced it while deeply Borgmeier, Thomas B 547 ­committed to biological studies. His sight was said Bootstrapping to have been so damaged by the age of 25 by his ­constant use of microscopes that he could barely A statistical method based on repeated random read or write thereafter. He was an observer and sampling with replacement from an original experimenter rather than a taxonomist. In 1745 he ­sample to provide a collection of new estimates of published “Traité d’ insectologie,” in which his a parameter, from which confidence limits can be “insectes” were all the invertebrate animals except calculated. molluscs, and the work contains results of his observations on subjects such as parthenogenesis in aphids, and respiration in caterpillars. His later books included “Contemplation de la nature” Bootstrap Values (two volumes, 1764–1765) and “Oeuvres d’ histoire naturelle et de philosophie” (8 volumes, 1779– A measure of the reliability of phylogenetic trees 1783). He died in 1793. generated using cladistic methods.

Reference Boreidae

Tuxen SL (1973) Entomology systematizes and describes: A family of scorpionflies (order Mecoptera). They 1700–1815. Smith RF, Mittler TE, Smith CN (ed) commonly are known as snow scorpionflies. ­History of Entomology. Annual Reviews Inc., Palo Alto,  CA, pp 95–117 Scorpionflies

Borgmeier, Thomas Book-Lice Thomas Borgmeier was born in Bielefeld, ­Germany, Members of the insect order Psocoptera. on October 31, 1892. After graduation from the  Bark-Lice, Book-Lice and Psocids Gymnasium [“high school”] of Bielefeld, he ­emigrated to Brazil and became a Franciscan monk. From 1912–1914 he studied philosophy in Curitiba, and from 1915–1918 theology in Petropolis. While Boopidae he was a student, he became interested in entomol- ogy, in 1917 befriending Hermann von Ihering. A A family of chewing lice (order Phthiraptera). wealthy industrialist in Rio de Janeiro donated They sometimes are called marsupial chewing money that allowed Thomas to buy von Ihering’s lice. reprint library and a microscope. He was permitted  Chewing and Sucking Lice by the Franciscans to pursue an entomological career. In 1924 he moved to the Museu Nacional in Rio de Janeiro, and then transferred to the new Instituto Biologico in São Paulo in 1928 as assistant in ento- Boreal mology. In 1933 he retuned to Rio de Janeiro as head of the entomo­logical section of the ­Instituto de Bio- A term used to indicate northern faunal regions, logia Vegetal in the botanical garden. He founded the though boreal regions can extend southward at journal Revista de Entomologia, and edited and pub- higher altitudes. lished it until 1951 when financial difficulties ended 548 B Boric Acid it. Later he founded the journal Studia Entomologica. Normally, boric acid products are active only About 1973 he retired from entomological activities when insects ingest the material (as a stomach to a monastery in Rio de Janeiro. During his life, poison), though this can occur during grooming Thomas published 243 papers on ants and on insects (cleaning the antennae and legs) as well as feeding. associated with ant nests, especially the dipterous It is used in structures to control such urban pests family Phoridae. He died on May 11, 1975. as cockroaches, ants, fleas, termites and silverfish. It may be mixed into bait, particularly for cock- roach and ant control, and is quite effective. It also Reference is sprayed onto, or impregnated into, wood for control of termites and wood boring beetles. Herman LH (2001) Borgmeier, Thomas. Bull Am Mus Nat Application as a dust into wall voids, attics, and Hist 265:48–49 cracks and crevices harboring insects also is popu- lar. Because cockroaches spend most of their time in cracks and crevices, application of boric acid into such harborages is advisable. The product is Boric Acid normally blown in with a bulb duster, but must be finely divided to achieve deep penetration. john l. capinera Research has shown that crack and crevice treat- University of Florida, Gainesville, FL, USA ment is superior to broadcast treatment for cock- roaches. Boric acid is superior to borax for This inorganic compound contains boron and cockroach control. Although it commonly takes many other non-volatile elements, and has many several days for cockroaches to die from boric acid

useful properties. The chemical formula is 3H BO3 poisoning, boric acid is especially useful for sensi-

and its sodium salt, or borax, is Na2 B4 O2·10 H2O. tive areas like schools, pet shops and zoos. The

A more water soluble formulation is Na2 B8 O13 4 slow action can be an advantage for cockroach

H2O, known as disodium octaborate tetrahydrate. suppression because nymphs will feed on the feces Formulations of borax and disodium octoborate of adults, so boric acid can be transported back to tetrahydrate usually are known simply as “borates.” harborages. Similarly, cannibalism of boric acid- Boric acid is used as a fungicide, bactericide, killed roaches can kill the scavengers. ­antiseptic, and as an insecticide, but has several Boric acid is often formulated with diatoma- other useful properties such as a flame retardant. ceous earth or silica gel (as desiccants) or ­tricalcium Normally it is produced from borate minerals by phosphate (to reduce caking). Sometimes other reaction with sulfuric acid. toxicants are included, including pyrethrins or From a toxicological perspective, boric acid is sodium fluoride. Dusts can be repellents, and a relatively nontoxic (to people and pets) insecti- although boric acid dusts tend to have low repel- cide. Its oral toxicity is reported to be 2,660 mg/kg lency, inclusion of additives in boric acid formula- in rats. Borax is even less toxic, with oral toxicity to tions increases the likelihood of the product being rats estimated at 5,600 mg/kg. These chemicals are repellent. Thus, additives should be kept at low not readily absorbed by skin. However, there is levels. Similarly, when incorporated into bait, some risk associated with chronic exposure to boric acid concentrations should be kept low (usu- aerosols, so respiratory protection is advised when ally 1%) so insects will not avoid ingestion. Boric working around high concentrations. Also, acci- acid is sometimes mixed into cleaning solutions dental ingestion of large quantities can be lethal. when floor mopping in cafeterias. Use of goggles and gloves are recommended for Though very persistent and water soluble, boric those applying these chemicals. acid is not readily impregnated deep into wood, so Botanical Insecticides B 549 although the outside of structural timbers may be Botanical protected, termites may burrow through incom- pletely impregnated lumber. Formulations of borates A product derived from plants or plant parts. This and penetrating agents such as ethylene ­glycol are term often is used to describe insecticides derived used to improve wood penetration. The formulation from plants. can be sprayed or painted onto untreated wood  Botanical Insecticides ­surfaces, or applied as a foam. Penetration is affected by a number of factors, including moisture content, and wood protection is best achieved when the Botanical Insecticides wood is freshly harvested, or re-wetted to take advantage of the solubility of the damp wood to murray b. isman borates. Other factors affecting protection include University of British Columbia, Vancouver, BC, thickness of the wood and thoroughness of applica- Canada tion. For deep penetration, injection may be neces- sary. Existing fence posts, mailbox supports, and Botanical insecticides are those products used to other wood in contact with soil can be protected by kill or repel insects that consist of dried, ground drilling a hole and inserting borate gel or rods, then plant material, crude plant extracts, or chemicals sealing the hole. Boric acid products have herbicidal isolated from plants. The recorded use of plant activity, however, so vegetation adjacent to treated material or plant extracts for insect control dates wood can be affected. Overall, boric acid products back at least 200 years. Botanical insecticides were are very useful for urban pest control, but should be important tools for crop protection prior to the dis- used as a component of a broader management plan, covery of the insecticidal action of DDT; the subse- not as the sole component. quent development of inexpensive and highly effective synthetic insecticides rendered botanicals all but obsolete. However, botanicals are enjoying References renewed interest as the popularity of organically- grown food increases because botanicals are among Quarles W (1998) Borates for wood protection. The IPM only a handful of “natural” insect control products Practitioner 20(3):1–12 that can be used in organic agriculture. Quarles W (2001) Boric acid, borates and household pests. The IPM Practitioner 23(3):1–12 Although botanicals are products of nature, they should not be considered absolutely safe or non-toxic unless so demonstrated. The active ingredients in certain botanical preparations used Boridae as insecticides are relatively toxic to animals and humans and several are toxic to fish. However, A family of beetles (order Coleoptera). They com- most are used at very low concentrations of active monly are known as conifer bark beetles. ingredients, minimizing the risk to humans and  Beetles wildlife from exposure. On the other hand, the active principles in virtually all botanicals are ­rapidly degraded in the environment, often by Bostrichidae exposure to sunlight, and thus are considered non- persistent. Apart from this generalization, the few A family of beetles (order Coleoptera). They com- botanical insecticides in commercial use vary monly are known as horned powder-post beetles. greatly in their sources, chemistry, toxicity and  Beetles other properties. 550 B Botanical Insecticides Pyrethrum 1% rotenone at most. Owing to its moderate per- sistence on foliage (3–5 days) and chronic effects Pyrethrum is the most widely used botanical on laboratory animals, there are some concerns insecticide. It is the oleoresin obtained by solvent about it potential health impacts on humans. It is extraction of the fresh-picked flowers of the daisy especially toxic to fish, and in fact, more rotenone Tanacetum cinerariaefolium (Asteraceae), native is used as a commercial fish poison (piscicide) to the Balkan region of eastern Europe. Most of than for insect control. As a fish poison, rotenone the world supply of pyrethrum in recent times has has been used for at least 300 years, and at least come from Kenya, but large scale production is 150 years as an insecticide. In insects, rotenone is a under way in Tasmania (Australia). The oleoresin slow-acting stomach poison particularly ­effective contains six esters with insecticidal properties. against plant-feeding beetles (e.g., the Colorado The most potent, pyrethrins I and II, typically potato beetle), but much less effective against make up 20% of the resin by weight. The­pyrethrins caterpillars. are axonic poisons in insects and are characterized by a fast knockdown time in flying insects. They degrade rapidly in the presence of sunlight. In Neem purity, the pyrethins have appreciable toxicity to mammals, but given their concentration in the Neem is an extract of the seeds of the Indian neem resin and the dosages normally used, pyrethrum tree, Azadirachta indica (Meliaceae). Native to the has minimal toxicity to mammals. Pyrethrum is Indian subcontinent, it has been widely planted a broad spectrum insecticide and has more throughout tropical and subtropical regions of ­registered uses (in the U.S.A.) than any other the world. Dried neem leaves have traditionally insecticide. Most products containing pyrethrum been used in protection against stored product or pyrethrins as active ingredients are formulated pests. Neem has a diverse array of behavioral and with a synergist, piperonyl butoxide, that prevents physiological actions against insects, most of the metabolic degradation of the insecticide within which are attributable to the complex triterpenoid the insect’s body, thus increasing potency. The azadirachtin. This chemical is reputed to be the rapid environmental breakdown of pyrethrum most potent antifeedant to insects (it deters insect created the impetus for the industrial development feeding in nanogram quantities), but is also a of the synthetic pyrethroids, now the dominant potent disruptor of the insect neuroendocrine class of agricultural insecticides. system. The most obvious manifestation of this latter action is that azadirachtin inhibits the molt- ing process in insects. As such, azadirachtin is a Rotenone ­slow-acting insecticide and requires ingestion to be effective. Another interesting property of Rotenone is the ground roots or rhizomes of the azadirachtin is its systemic action in some plants. tropical legumes Derris (southeast Asia) and Of primary importance, neem and azadirachtin ­Lonchocarpus (South America, also known as cube are non-toxic to most non-target organisms, root), or resins extracted from them. The name is including humans. Like pyrethrum, neem is rap- also applied to the major insecticidal constituent, idly degraded in the environment by sunlight. although each plant contains a number of related Neem became commercially available in the isoflavonoids, most of which are insecticidal. U.S.A. in 1990, and is beginning to gain accep- Rotenone is a mitochondrial poison in insects and tance for insect control in some agricultural vertebrates. In purity it is quite toxic to mammals, ­commodities and especially in organic food but most home and garden preparations contain production. Botanical Insecticides B 551 Tobacco Schoenocaulon officinale, containing alkaloids that are axonic poisons. Both are examples of plants Water extracts of tobacco have been used to kill whose active principles, in purity, are relatively insects for over 300 years. Nicotine (from Nico­ toxic to mammals, but for which the actual plant tiana tabacum, Solanaceae), nornicotine (from preparations used have a wide margin of safety to N. sylvestris) and anabasine (from Anabasis humans. aphylla, Chenopodiaceae) are alkaloids that are Essential oils from certain plants have been highly insecticidal. They poison both insects and used traditionally in some regions as insect mammals through a common mode-of-action, by ­repellents. The best known among these is oil of mimicking the ­neurotransmitter acetylcholine citronella, obtained from lemongrass (Cym- and causing over stimulation of nerve synapses. bopogon nardus, Poaceae), used as an alternative to Unlike some other botanical insecticides, nicotine DEET for repelling mosquitoes and biting flies. In is very toxic to humans, and poisoning can result ­addition, monoterpenes and phenols in clove oil, not only from ingestion but from dermal expo- thyme oil, and various mint species have been sure as well. As a consequence, nicotine is rarely recently shown to be insecticidal in a wide range used for insect control at present, although it is of insects. As a result, several home and garden still used as a ­fogging insecticide in some insect control products based on plant essential greenhouses. oils have been developed and these materials may have uses in agriculture (e.g., organic farming) as well. Other Botanicals Numerous other plant extracts have seen regional traditional use, especially in developing Other botanicals have seen some commercial use countries. Insecticides can be made from the seeds in North America. These include ryania, the of chinaberry (Melia azedarach, Meliaceae), a ­relative ground stem wood of the Caribbean tree Ryania of the neem tree, although in some countries the speciosa (Flacourtiaceae), containing alkaloids seeds contain substances that are toxic to animals. In that poison neuromuscular junctions, and saba- the Peoples Republic of China, an insecticide is dilla, the ground seeds of the South American lily made from the bark of M. toosendan, considered by

Botanical Insecticides, Table 8 Properties of some important botanical insecticides Property Pyrethrum Rotenone Neem Essential oils Nicotine Country of origin Kenya, Australia SE Asia, India Worldwide Worldwide Venezuela Active ingredients Pyrethrins (esters) Rotenoids Azadirachtin Monoter- Nicotine (isoflavonoids) (limonoids) penes, simple (alkaloids) phenols Formulations Numerous Dusts, WPs ECs Numerous ECs, Dusts % actives in 6% EC 1% Dust 5% WP 1–4.5% EC 35% EC 6% 40% EC formulation Aerosol Action on pests Contact/knock- Stomach poison/ Stomach Contact/ Contact/ down toxin cytotoxin poison/IGR/ knockdown knockdown antifeedant toxin toxin Persistence Very limited Limited Very limited Very limited Limited Mammalian Minimal Moderate; very Non-toxic Non-toxic Very toxic toxicity toxic to fish 552 B Bot Flies some authorities to be taxonomically synonymous Bot Flies with M. azedarach. The ­product, Toosendanin, is reported to be effective against fruit and vegetable Members of the family Oestridae (order Diptera). pests. The tropical trees ­Quassia amara and Ailan-  Flies thus altissima (Simarubaceae) contain insecticidal  Myiasis terpenoids that can be extracted from the wood and used for insect control. Dried leaves of Haplophyton cimicidum (Apocynaceae) have been used for centu- Bothrideridae ries in Mexico and ­Guatemala to prepare “cockroach powder” owing to a series of alkaloids in the foliage A family of beetles (order Coleoptera). They com- of the plant. Seeds of the custard apple (Annona monly are known as dry bark beetles. reticulata, Annonaceae), sweetsop (A. squamosa)  Beetles and ­soursop (A. muricata) contain potent insecti- cidal acetogenins and have been used for insect con- trol in many tropical countries in the Old and New Boutonneuse Fever World. The dried, powdered flowers of Rhododen- dron molle (Ericaceae) have a long history of use as This is a bacterial disease transmitted by ticks. an insecticide in China.  Ticks Botanical insecticides are unlikely to displace conventional synthetic insecticides in many pest management contexts, but they should gain increas- Bovine Babesiosis ing favor in situations where human ­exposure is unavoidable and safety is of primary concern. This is a protozoon disease of cattle transmitted Botanicals will also see continued use in developing by ticks. countries where many of the plants from which  Piroplasmosis they are obtained can be readily grown and the insecticidal preparations are a safer and less expen- sive alternative to imported synthetic pesticides.  Alleochemicals Bovine Hypodermosis: Phenology  Chinaberry in Europe  Pyrethrum  Persian Insect Powder david reina, javier martínez, eantiago  Neem hernández, ignacio navarrete Universities of Extemadura and Córdoba, ­Madrid, Spain References The life cycle and biology of the warble fly, Arnason JT, Philogene BJR, Morand P (eds) (1989) Insecti- ­Hypoderma bovis, and of Hypoderma lineatum, cides of plant origin. American Chemical Society, exhibit regional and local variation attributable to ­Washington, DC, 213 pp Isman MB (2000) Plant essential oils for pest and disease climatic and weather conditions (Fig. 57). management. Crop Prot 19:603–608 In Andalusia (southern Spain), it is possible Isman MB (1995) Leads and prospects for the development of to find H. lineatum adults from the middle of new botanical insecticides. Rev Pestic Toxicol 3:1–20 ­February to the beginning of May, first instar­larvae Koul O, Dhaliwal GS (eds) (2001) Phytochemical biopesti- cides. Harwood Academic Publishers, Amsterdam, The (L1) in the esophagus from April to November, third Netherlands, 223 pp instar larvae (L3) in the back from the middle of Bovine Hypodermosis: Phenology in Europe B 553 while it is found in the rachis from the beginning of October until the middle of February. Warbles Eggs attached are found during much of the year, from October to hairs in rows to March. In other studies, adults occur between Adult Larvae March and August (the latter ones probably are H. bovis), L1 is observed in the rachis and gullet between July and December, and warbles occur Migration between September and February. WarblePupa on cattle On the other hand, there are significant ­differences in phenology between northern and southern Spain. In northwestern Spain (Galicia), it is not possible to observe the first flies until the Bovine Hypodermosis: Phenology in Europe, middle of May, but after that they can be seen Figure 57 Life cycle of Hypoderma spp. on cattle: until the middle of September. First instar larvae eggs (a) are deposited on the legs of the host; are found from the middle of September to the larvae (b) burrow into the animal and migrate end of January, or from August to December. through the animal, eventually reaching the back Warbles are found from February until May. The where a swelling (warble) is formed (d); the mature phenology of Hypoderma in the north of Spain larva drops to the soil to pupate (e) and an adult is more similar to the countries of central Europe emerges from the pupa. than to the southern areas of the same country. November to the end of March, and the mature In the central and eastern regions of France, larva ready to commence pupation from the ­middle Hypoderma adults and eggs are found between of January to the end of March. Adults of H. bovis the end of May and the middle of August. First occur between May and June, L1 from November instars (the period of greatest risk due to local to ­January, the period of warbles from mid-­ and systemic adverse reactions) occur from the December to May, and the dropping of L3 from middle of August to the end of February. Warbles mid-March to May. It is possible to find third are found in the backs of hosts during March to instar larvae of H. lineatum in the back of bovines May, or possibly from March to July. It is likely from October to early May. Adults are found ­during that the phenology is intermediate between the April or May, although in some years some of them countries of central Europe and the southern can be seen in March. First instar H. lineatum appear in ­Iberian peninsula. In Switzerland, the phenology the gullet of bovines between September and is similar to that in France. December. Hypoderma bovis is scarcer in western In Ireland, there is a delay in the presence of and southwestern Spain, but display the same phe- warbles. Warbles appear in July and August rather nology. In some areas of Portugal, such as the than in February and March. Ireland, together “Alentejo” and “Centro” areas, phenology clearly is with the rest of United Kingdom, and also ­Holland, similar to that of western Spain, which is logical are examples of locations where Hypoderma are due to the ­geographic proximity of these regions. practically eradicated, at least from cattle. The phenology (Table 9) is very similar in In eastern Europe, specifically Czechoslovakia, northern Africa. In Morocco, it is possible to find extensive investigations have been conducted on adults from February to the middle of May, and L3 H. bovis (throughout the country) and H. lineatum in the back of the hosts from December to April. (in Slovakia). Warbles of H. bovis appear in heifers In ­Algeria, adults are found between the end of from the end of March to June, and in cows in May March and July. The L1 stage can be found in the to June. Dropping of larvae and pupation were host’s esophagus between August and December, observed from early April to early July, while flies 554 B Bovine Hypodermosis: Phenology in Europe

Bovine Hypodermosis: Phenology in Europe, Figure 58 Warble being removed from beneath the skin of host.

are present from early June to the beginning of As a general rule, H. lineatum occurs September. For H. lineatum, the period of warbles ­earlier than H. bovis. The occurrence varies from was earlier and shorter, from the second half of year to year, however, due to variation in envi- February to the end of April. Pupation was observed ronmental conditions. They occur earlier when from the end of March to the end of April, and flies it is warmer in the spring, summer or winter. from May until the first days of July. In southwestern Spain, the mean annual ­maximum In countries such as Poland, warbles (Fig. 58) temperatures are 20–21°C, with maximum sum- have been detected in February, though normally mer temperatures averaging 29–30°C, and mean the warbles do not occur until April. When ­occurring annual ­minimum temperatures of 8–9°C. The early, warbles are found in April, but when found cooler temperatures of eastern and central normally, the warbles do not occur until May and Europe slow the biology of these pests. June. It is possible to observe warbles until the end of To avoid damage caused by larvae, knowledge July. In Romania, the period of activity of adults is of phenology is important. Before beginning a May to September for H. lineatum, and between management or eradication effort, climatic varia- August and September for H. bovis. The first­warbles tion in Hypodermas must be considered. produced by the ­second instar larvae appear in the southern part of the country at the end of January or References early February. In the north, they occur from March to April. The third stage larvae leave the host’s body Boulard C, Argenté G, Hillion E (1988) Hypodermis bovine: from late April until the end of July (until August in description et incidence économique. Le Point Véteri- the northern part of Romania). Thus, the phenology naire 20 (111):17–30 in Romania is similar to central Europe. Sometimes Martínez-Moreno FJ (1992) Estudio inmunológico de la hipodermosis bovina. Doctoral thesis. Córdoba, Spain warbles are found in the back and lumbar regions of Minar J (1993) Cattle hypodermosis, its investigations the host in September and as late as December; in and suppression in Czechoslovakia. Academia, these cases the larvae are dead. Praha, 207 pp Brachelytry B 555 Bovine Hypodermosis: Phenology in Europe, Table 9 Comparative phenology (chronobiology) of ­Hypoderma species in some European ecological regions Species Hypoderma lineatum Hypoderma bovis Region Southwest Central East Southwest Central East L1 April–December September–March September– November– January–May October–May April January L3 October–April February–May February– December– May–July March–June April May Mature January–April April–June March–April March–May May–August April–July larvae Adults February–May May–June May–July May–June May–Sep- June–­ tember September

Morrondo P, López C, Panadero R (1995) Ciclo biológico y no such comprehensive study appeared in print epidemiología de Hypoderma. Bovis 65:27–38 until the second volume of F. C. Stehr’s (1991) Reina D, Martínez-Moreno FJ, Martínez-Moreno A, Molina JM, Hernández-Rodríguez S (1994) Present ststus of Immature Insects. Bøving died in Washington on warble fly in Extremadura (South-West of Spain). In: March 16, 1957. Improvement in the control methods for warble fly in cattle and goats. Commission of the European Commu- nities, Brussels, Belgium, pp. 59–64 Reference

Mallis A (1971) Adam Giede Böving. In: American entomol- Bøving, Adam Giede ogists. Rutgers University Press, New Brunswick, NJ, pp 431–433 Born at Saby, Denmark, on July 31, 1869, Adam Bøving graduated from the University of Copen- hagen in 1888. His interests included insect larvae, Brachelytry and those of Donacia (Coleoptera: Chrysomelidae) were the subject of his Ph.D. research. Then he was pierre jolivet appointed Assistant Curator of Entomology at the Paris, France Royal Zoological Museum in Copenhagen, and he continued to study beetle larvae. Two years after Elytra are characteristic of Coleoptera, and the death of his first wife, he moved to the United ­substantial thickening of the first pair of wings States in 1913 and found employment with the U.S. (elytra) is uncommon among other orders of Department of Agriculture. His work still revolved insects. The elytra are modified mesothoracic around beetle larvae, but concentrated on those of wings, normally rigid and fitting over the abdo- economic importance. He took an American wife men. Brachelytry is the possession of abbreviated and citizenship. With F. C. Craighead as coauthor, wing covers or elytra. Brachelytrous insects are he published in 1930–1931 in Entomologica commonly found among the Coleoptera, including ­Americana, the work “An illustrated synopsis of the Carabidae, Staphylinidae, Cerambycidae, His- the principal larval forms of the order Coleoptera.” teridae, Meloidae and Chrysomelidae. It seems This major work has been much-cited by later most common among Galerucinae and is unusual authors for the wealth of its informational content; among Alticinae. Both subfamilies are closely 556 B Brachelytry related, as part of the Trichostomata. Alticinae, where the elytra become truncated, with the Galerucinae (both ­Chrysomelidae) and Bruchidae ­apical part of the abdomen uncovered, includ­ sometimes show only an exposed pygidium, with ing Hydroscaphidae, Histeroidea, Staphylinidae, only a small shortening of the elytra. Some beetle ­Nitidulidae, Inopeplidae, etc. In all these groups, families are exclusively brachelytral, as is the the elytra completely cover the folded wings. In Lymexylidae, but they fly very well, as do most of some others, such as the myrmecomorph Ceram- the myrmecomorphic Cerambycidae. Brachelytry bycidae and the Lymexylidae, the wings are left should not be confused with physogastry (the free without any protection. The adaptive signifi- swelling of the abdomen to an unusual degree due cance of this feature is not well understood. to the hypertrophy of fat bodies, ovaries or both), Among the Staphylinidae, the main adaptive which can result in a similar appearance. In that advantage of abbreviated elytra seems to be a case, the abdomen is so big that it is protruding greater flexibility in the abdominal region, but over the end of the elytra. Physogastry is common that does not explain the truncated elytra of among certain Chrysomelinae (Gastrophysa) and ­Histeridae. Many beetles with truncate elytra and ­Galerucinae (Agelastica) (both Chrysomelidae). with wings completely covered live on the ground, Brachelytry occurs also in Dermaptera and and are saprophagous. But there are always excep- Gryllidae. tions; among the Histeridae, for instance, some Pseudophysogastry (artificial swelling of the genera have the elytra entirely covering the abdo- abdomen) is also common among cavernicolous men. In the Staphylinidae, usually there are at or termitophilous beetles. In many Meloidae least four abdominal segments exposed, some- (Meloe), the elytra appear to fit badly, as among times six. There are, however, some Staphylinidae physogastric beetles. The elytra overlap but the with the elytra not truncate. beetle is apterous already as a pupa, as in ­Timarcha. There are also cases where the elytra are This means a long history of apterism. In certain abbreviated and do not completely cover the cases, brachelytry can be seen as a consequence of folded wings. In Atractocerus (Lymexylonidae), apterism, but many macroelytrous (normal) bee- the elytra are very reduced and don’t cover the tles are alternatively brachypterous or apterous wings. There are also some myrmecomorphic (Chrysolina banksi), or totally and permanently Cerambycidae, some Cantharidae (Malthinus apterous (Timarcha). Often, in that case, the elytra and Malthodes), the male of Stylopidae, and are fused. They are never fused among brache- ­several Rhipiphoridae, which are more-or-less lytrous beetles. brachelytrous, with exposed wings. In male A set of mutations is surely at the origin of ­Stylopidae, the elytra are peculiarly modified to brachelytry, but macroelytrous and brachelytrous form balancing organs, like the halters of ­Diptera. individuals do not occur in the same species. Often those beetles are free-living and flori- Brachyeletry is found mostly among mountain- colous. This elytral reduction is increased among ous or desert frequenting species or genera, but some endogeous Staphylinidae (Leptotyphlinae also among parasitic species. It seems absent and Osoriinae), where the elytra are reduced to from a r­ c t i c species, which would seem to benefit two contiguous scales, covering only the poste- from protection on the abdomen, though apter- rior thoracic segments and the first abdominal ism or brachypterism there remains frequent. segment. A similar situation is found among a Brachelytry is also frequently linked with brachy-or Moroccan Staphylotroglops (Cantharidae). The apterism, though some brachelytrous beetles reduction of the elytra can also be done laterally, maintain ­complete wings and fly very well. revealing the sides of the abdomen (some Cetoni- Brachelytry is a very old, derived character dae) or be disjunct on the back (Oedemeridae). (Fig. 59). There are a number of beetle families There are also cases where only the females are Brachelytry B 557

Brachelytry, Figure 59 Somes cases of brachelytry (a) Nyctiphantus nocturnus (Semenov). Russia. Tran- scaspia; (b) Marseulia dilativentris (Reiche). Israel; (c) Theone octocostata (Weise). Tibet; (d) Parageina andrewesi (Jacoby). India; (e) Galeruca barovskyi Jacobson. Tibet (after Jolivet P (2005) Brachelytry among Chrysomelidae. Lambilionea 105(3):371–384). 558 B Brachelytry apterous and brachelytrous, as with Metacycla in highlands of South America (Metalepta tubercu- Central America (Chrysomelidae: Galerucinae). lata). Between 60 and 100 galerucine species in the Also, the elytra are completely absent in the whole world display brachelytry. Strangely, brache- females of glow-worms (Lampyridae), Drilidae lytrous forms are extremely rare in South Africa and some Scarabeidae (Pachypus ­candidae) and probably absent from Madagascar. Some live (Fig. 60). in India and Malaysia, but generally are linked with Among the parasites, apterism can be linked mountains. The genus Galeruca, which is essen- with shortening of the elytra among the females tially palaearctic, has numerous species (nearly 70 (Silphopsyllus), or even among both sexes taxa) from Western Europe to Siberia, China, and (Platypsyllus) (both Leiodidae). We find also a Japan, and normally is macroelytrous and total disappearance of elytra among females of macropterous. However, it displays brachelytrism, Pachypus (Dynastidae), Thylodrias, and Rhipidius joined with brachypterism or apterism, at higher (Rhipiphoridae). altitudes. It can occur, as Chrysolina, above 5300 m in China, Himalayas and Tibet and many of those highland frequenting species are ­brachelytrous and all apterous. Very few real brachelytrous Alticinae Some Examples Among can be quoted: Hespera brachelytra from the Yun- Chrysomelidae nan mountains, Sjoestedtina fordi, S. montivaga from mountains in eastern African, though there Brachypterism or apterism is common among may be more. Chrysomelidae, whereas brachelytry seems ­limited Flightlessness and brachelytry generally to Galerucinae and a very few Alticinae. As far as occur in both sexes. Metacycla is an exception, we know, macro-brachypterism seems to be with only the female brachelytrous and apterous. ­transmitted in Mendelian fashion, when both Flightlessness is favored in females because it morphologies are present. Brachelytrism is a allows greater allocation of resources to egg pro- derived character, but mixed forms do not exist. duction (physogastry); however, flight seems Brachelytrous leaf beetles, which are gener- retained in males because it increases the proba- ally apterous, are evidently devoid of a subelytral bility of finding a mate. Many brachelytrous cavity, which exists among many apterous Chry- species walk on the ground and are relatively somelinae and Tenebrionidae. Probably, this lack polyphagous, like Arima in Europe, Galeruca in of isolation against cold in mountains or heat and China, Marseulia in Middle East, Metalepta on UV in deserts is compensated by other means, the Peruvian plateau, or Rupilia in Australia. such as stronger sclerotizaton of the upper Metacycla occurs in Mexico on Ambrosia ambro- ­abdomen (tergites). sioides, a small plant (Asteraceae). In this species, Brachelytry among Galerucinae is distributed the beetle does not walk on the ground, but the in the Mediterranean region (Arima marginata, male is flying and active, searching for females. Galeruca monticola, Marseulia dilativentris); in The female, black in the collections, is red and mountains or steppe areas of Siberian, Indian and pink in some species when alive and ­probably it is Chinese mountains (Theone octocostata, Galeruca an aposematic color. barovskyi, Paregeina andrewesi, Geinula antennata); A review of the brachelytrous Chrysomelidae in Australian desert areas, where apterous beetles (Galerucinae and Alticinae) has been made by are common (Rupilia ruficollis); in the Ethiopian Pierre Jolivet, but due to the numerous galerucine and East African mountainous areas (Mahutia genera affected, the list is not complete. The alluaudi); in the Mexican and Central America ­phenomenon is more frequent among mountain, dry tropics (Metacycla caeruleipennis); and in the steppe or desert-inhabiting genera and species, Brachelytry B 559

Brachelytry, Figure 60 Some additional cases of brachelytry (a) Galeruca littoralis (Fabricius). South of France. Pygidium prominent. Winged; (b) Galeruca monticola Kiesenwetter. France: Pyrenean mountains. Apterous; (c) Arima marginata (Fabricius). South of France. Apterous; (d) Metacycla marginata Chapuis. Female. Mexico. Apterous; (after Jolivet P (2005) Brachelytry among Chrysomelidae. Lambilionea 105(3):371–384). 560 B Brachelytry mostly in the tropics, but it also exists in temperate ­different in both families. When the beetles are on areas. Life on the edge has its constraints, but such their back, the staphylinids use their abdomen to mutants not only survived, but have persisted for a recover and attain their footing, whereas histerids very long time. Other families like Staphylinidae use their elytral stump. For Degallier (pers. seem more consistent; only in the Arctic, where comm.), histerid elytra are shortened organs, many apterous or brachypterous species occur, whereas for staphylinids the elytra could be brachelytry is absent. Apparently it can be main- ­vestigial in relation to an elongated abdomen. tained only under hot or relatively temperate There seems not to be any synapomorphy between ­climates. Brachelytry seems ancient and linked to the two groups. harsh environmental conditions. It is known that Often, brachelytry or apterism are connec­ wing atrophy helps the female in producing more ted with a reduced metasternum and various eggs. That must also be the same for brachelytry. ­morphological and anatomical correlations There are many cases where only the female is ­(timarchisation of Rüschkamp, 1927). Among brachelytrous. We must distinguish between ­elytra ground Chrysomelidae and others, reflex bleed- fully developed or truncate (brachelytry), but ing, ­hoemocoelous toxicity, thanatosis, aposema- there are degrees between relictual scales (some tism, extra-sclerotization of the abdominal tergites Staphylinidae) and relative shortening of the elytra. help in protection against predators for those However, very rarely the elytra disappeared com- wingless and relatively unprotected beetles. Most pletely. Often scales persist. Among Bruchidae, of those beetles are black, as in Timarcha, but Alticinae, many Galerucinae, very often the end of some are brilliantly colored. Black for a ground the abdomen is apparent, but it is not a case of insect can be aposematic on grasses. A set of brachelytry. mutations should have produced these condi- Certainly the shortening of elytra helps the tions, and apterism and brachelytry are generally mobility of the abdomen among the Staphylini- associated with the many usual morphological dae. Among the Histeridae, the function for trun- conditions. cated elytra is less clear, but among saprophagous beetles the wings are always covered. This may be a necessity in a dirty and humid environment. In the case of Cerambycidae, mimetism with ants References could be responsible, but among floricolous groups the wings can remain free. In many cases, the rea- Beutel RG, Leschen RAB (eds) (2005) Coleoptera, Beetles. I. son for brachypterism is not clearly understood. morphology and systematics (Archostemata, Adephaga, Myxophaga, Polyphaga partim). Walter de Gruyter. The case of the Metacycla species (Galerucinae) is ­Berlin, New York, 567 pp unique, having physogastric, brachelytrous, apter- Beutel RG, Leschen RAB (2005) Phylogenetic analysis of ous females and, macroelytrous, probably flying Staphyliniformia (Coleoptera) based on characters of larvae and adults. Syst Entomol 30:510–548 males. In some ­species of this genus, the drawings Crowson RA (1981) The biology of the Coleoptera. Academic (yellow bands) of the elytra are printed over the Press, London, 802 pp upper side of the abdomen. In most cases of Jolivet P (2005) Brachelytry among Chrysomelidae. Lambil- brachyletry, the upper abdomen is strongly sclero- ionea 105(3):371–384 Paulian R (1988) Biologie des Coléoptères. Lechevalier, Paris, tized to replace the absence of protection by the 719 pp lost elytra. Rüschkamp F (1927) Der Flugapparat der Käfer. Zoologica. Brachelytry does not seem to be analogous Stuttgart 28(75):1–88 between the various families of beetles. It has Seguy E (1967) Der Flugapparat Käfer. Zoologica. Stuttgart 28(75):1–88 appeared independently, for instance, among Seguy E (1967) Dictionnaire des Termes Techniques Staphylinidae and Histeridae. Wing folding also is d’Entomologie Elémentaire. Lechevalier, Paris, 465 pp Brahmin Moths (Lepidoptera: Brahmaeidae) B 561 Brachodidae Brackish

A family of moths (order Lepidoptera). They also Saline water with a concentration of salt between are known as little bear moths. that of fresh and salt water.  Little Bear Moths  Butterflies and Moths Braconidae

A family of wasps (order Hymenoptera). Brachycentridae  Wasps, Ants, Bees and Sawflies  Natural Enemies Important in Biological A family of caddisflies (order Trichoptera). Control  Caddisflies Bradynobaenidae

Brachypsectridae A family of wasps (order Hymenoptera).  Wasps, Ants, Bees and Sawflies A family of beetles (order Coleoptera). They com- monly are known as Texas beetles.  Beetles Brahmaeidae

A family of moths (order Lepidoptera) also known as brahmin moths. Brachypteridae  Brahmin Moths  Butterflies and Moths A family of beetles (order Coleoptera). They ­commonly are known as short-winged flower beetles.  Beetles Brahmin Moths (Lepidoptera: Brahmaeidae)

john b. heppner Brachypterous Florida State Collection of Arthropods, ­Gainesville, FL, USA Having short wings, that do not cover the abdo- men or nearly so. (contrast with macropterous). Brahmin moths, family Brahmaeidae, are a small  Brachelytry family of 28 species, mostly Palearctic and ­African. There are two subfamilies: Dactyloceratinae and Brahmaeinae. The family is in the superfamily Brachytosis ­Bombycoidea (series Saturniiformes), in the section Cossina, subsection Bombycina, of the division A bacterial disease of certain Malacosoma ­Ditrysia. Adults medium size to very large species (tent caterpillars), caused by Clostridium (50–180 mm wingspan), with head vertex rough- brevifaciens. ened; haustellum average (rarely vestigial); labial 562 B Brain Brain

The brain of insects consists of three fused ­­gang- lionic masses: the protocerebrum, the ­deutocerebrum, and the tritocerebrum (Fig. 62) (Fig. 63).  Nervous System

Brain Hormone

An earlier name for the hormone that activates the prothoracic glands to produce molting Brahmin Moths (Lepidoptera: Brahmaeidae), ­hormone (ecdysone). It also is known as protho- Figure 61 Example of brahmin moths (Brahmaeidae), racicotropic hormone (PTTH). The brain is now Brahmaea wallichii (Gray) from Taiwan. known to produce several hormones with different functions.  Endocrine Regulation of Insect Reproduction palpi upcurved or porrect; maxillary palpi ­vestigial  Diapause or very small (2-segmented); antennae bipectinate; body robust. Wings broadly triangular but mostly rounded (rarely with apex somewhat falcate); Brauer, Friedrich Moritz hindwings rounded (Fig. 61). Maculation mostly dark browns with numerous scalloped and con- Friedrich Brauer was born in Vienna on May 12, centric light lines, plus other markings; rarely more 1832. His professional work began as assistant in ­colorful. Adults nocturnal. Larvae are leaf feeders. the entomological museum of Universität Wien, Host plants recorded in Asclepiadaceae and and he was appointed custodian in 1873. In 1874 Oleaceae. he was appointed professor of zoology in that ­university. He became director of the Naturhisto- risches Hofmuseum and published extensively References on Neuroptera and Diptera. He died on December 29, 1904.

Chu HF, Wang LY (1977) The Brahmaeidae of China ­(Lepidoptera). Acta Entomologicae Sinica 20:83–84 Holloway JD (1987). Family Brahmaeidae. In: The moths of Reference Borneo. Malay Nat J 3:91–93, pl 7 Nässig WA, Pauksstadt U (1990) The Brahmaeidae of­Sumatra. In: Heterocera Sumatrana, 6:117–136 Poulton EB (1905) Professor Friedrich Moritz Brauer. Ento- Nässig WA, Treadaway CG (1998) The Brahmaeidae mologist’s Monthly Magazine 41:73–74 ­(Lepidoptera) of the Philippines. Nachrichten des ­Entomologischen Verein Apollo Suppl 17:425–440 Rougeot PC (1971) Brahmaeidae. In: Les Bombycoides (Lepidoptera-­Bombycoi dea) de l’ Europe et du Bassin Braulidae Méditerranéen. In Faune de l’ Europe et du Bassin Médi- terranéen, 5: 46–59 A family of flies (order Diptera). They commonly Seitz A (1911–1928) Familie: Brahmaeidae. In: Die Gross-Schmetterlinge der Erde, 2:227–228, pl. 35 are known as bee lice. (1911); 10:521–522, pl. 56 (1928); 14:349–351, pl.  Flies 47, 60 (1927)  Bee Louse Braulidae B 563

Brain, Figure 62 Lateral view of the insect brain (adapted from Snodgrass, Insect morphology).

Brain, Figure 63 Cross section of an insect brain (adapted from Snodgrass, Insect morphology). 564 B Brentidae Brentidae biogeography. In: Handbuch der Zoologie. Band IV. Arthropoda: Insecta. Teilband. W. De Gruyter, ­Berlin, 35:217–232 A family of beetles (order Coleoptera). They com- Falkovitsh MI (1978) Schreckensteiniidae. In: Identification monly are known as straight-snouted weevils. keys to the insects of European Russia. 4. Lepidoptera,  Beetles 2:526–529. St. Petersburg: Academie Nauk USSR [in Russian], Russia Heppner JB (2003) Schreckensteiniidae. In: Lepidopterorum Catalogus, (n.s.). Fasc. 29. Association for Tropical Bristle-Legged Moths ­Lepidoptera Gainesville, FL, 8 pp (Lepidoptera: Schreckensteiniidae) Bristletails (Archeognatha) john b. heppner Florida State Collection of Arthropods, This is a primitive order of insects known as ­Gainesville, FL, USA Archeognatha or Microcoryphia. The order name is derived from the Greek words archaios ­(primitive) Bristle-legged moths. family Schreckensteinii- and gnathos (jaw). Because these insects are ­wingless, dae, are a small family of only five known spe- and none of their ancestors appear to be winged, cies (three in North America, one in Central the order is placed (with the order ­Zygentoma) in ­America, and one in Europe). Some place the the subclass Apterygota; in this regard they family in its own monobasic superfamily, ­(apterygotes) differ from all other insects. Schreckensteinoidea. The family is part of the superfamily Tineoidea, in the section Tineina, subsection Tineina, of the ­division Ditrysia. Classification Adults are small (10–12 mm wingspan), with head smooth-scaled and hind tibiae with long There are about 250 species found throughout the bristles; haustellum naked; maxillary palpi world minute, 1-segmented. Maculation is lustrous in Class: Insecta shades of gray or brown, with reduced vena- Apterygota tion and long hindwing fringes. Adults are Order: Archeognatha diurnal. Larvae are leaf skeletonizers on Anac- Family: Machilidae ardiaceae or Rosaceae. The family and nomi- Family: Meinertellidae nate genus­ Schreckensteinia are named after the German ­lepidopterist and coleopterist, Baron Friedrich Roth von Schreckenstein Characteristics (1753–1808). Like other insects (but unlike some similar-ap- References pearing wingless animals such as diplurans, order Entotrophi, and proturans, order Protura), the mouthparts are external (ectognathous). They also Buszko J, Skalski AW (1980) Schreckensteiniidae. In: Klucze do Oznaczania Owadów Polski. 27. Motyle – Lepi- lack metamorphosis; they do not change in form doptera, 23:32–36. Polskie Towardzystwo Entomologic- as they molt, only increase in size. The number of zne [in Polish], Warsaw molts is considerable; 20–70 have been reported. Dugdale JS, Kristensen NP, Robinson GS, Scoble MJ They can live from 1 to 4 years. (1999) The smaller Microlepidoptera-grade super- families. In: Kristensen NP (ed) Lepidoptera, moths Bristletails are small, measuring 10–12 mm in and butterflies. vol 1: Evolution, systematics, and length. The body is cylindrical, but somewhat Bromeliad Fauna B 565 ­flattened. The thorax is strongly arched, resulting in Broadleaf Plant a “hump-backed” appearance. Bristletails have large compound eyes that are almost touching, and also One of the major plant groups, with net-veined, ocelli. They are covered with scales, and their color is broad leaves. Synonymous with dicotyledonous gray, whitish, or brownish. The ­mandibles are long. plants. (contrast with grass). The body segments are well-defined, including the three thoracic segments. The tarsi have three seg- ments, the abdomen 11. The abdomen bears a long Broad Mite, Polyphagotarsonemus median apical filament (a tail-like structure) and latus (Banks) (Acari: two shorter lateral cerci. The antennae are fairly long, Tarsonemidae) and least half the length of the body, and filiform. This mite affects several important crops.  Biology Citrus Pests and Their Management  Vegetable Pests and Their Management

Bristletails are nocturnal, and hide during the day is such cryptic habitats as leaf litter and decaying Broad-Shouldered Water Treaders logs. Some frequent the shorelines water bodies, particularly among rocks near the shore. They are Members of the family Veliidae (order Hemiptera). known for their ability to leap. Bristletails feed on Bugs algae, lichens, and plant debris. Bristletails do not copulate. They transfer their sperm indirectly by suspending droplets of sperm on strands or Broad-Winged Damselflies threads, which are taken up by the female. A family of damselflies in the order Odonata: References Calopterygidae.  Dragonflies and Damselflies Arnett RH Jr (2000) American insects, 2nd edn. CRC Press, Boca Raton, FL, 1003 pp Remington CL (1954) The suprageneric classification of the Broad-Winged Thrips order Thysanura (Insecta). Ann Entomol Soc Am 47:277–286 Wygodzinsky P (1987) Order Microcoryphia. In: Stehr FW Members of the family Aeolothripidae (order (ed) Immature insects, vol 1. Kendall/Hunt Publishing, Thysanoptera). Dubuque, Iowa, pp 68–70  Thrips

Broadcast Application Bromeliad Fauna The application of a material such as an insecticide to the entire surface of a field. j. howard frank University of Florida, Gainesville, FL, USA Broad-Headed Bugs Bromeliads are a family (Bromeliaceae) of mono- Members of the family Aldyidae (order Hemiptera). cotyledonous plants with about 2,500 described  Bugs species assigned to about 60 genera. Almost all of 566 B Bromeliad Fauna them are native to the neotropics, but the range of Some authors define tank bromeliads as those a few extends farther north. Sixteen species are that have a central water-impounding tank, ­perhaps native to southern Florida, three of which attain surrounded by additional water-impounding axils. northern Florida, and one of these reaches Others include any bromeliads that impound water ­southeastern Virginia (USA). Many bromeliad in their axils, even if the water is distributed among species are epiphytic whereas others are terrestrial. many axils. The latter position is adopted here for Roots of those that are epiphytic do not penetrate convenience, not because the concept has greater their tree hosts, and serve as holdfasts rather than merit. nutrient-absorbing structures. Thus, minerals are One bromeliad species, Ananas comosus L. absorbed through the leaves, not the roots, and the (pineapple), is a very important agricultural crop plants are not parasitic. In contrast, roots of in tropical countries worldwide. A few other ­species ground-dwelling bromeliads may absorb ­minerals. are grown locally in the neotropics to ­provide food Some bromeliads that grow on the ground dwell or drink (e.g., Bromelia pinguin L. and Puya on rock surfaces (are saxicolous), some in arid ­raimondii Harms) or fiber (e.g., Aechmea magdale- habitats and others in marshy soils. Some major nae (André) and Neoglaziovia variegata (Arruda genera are Aechmea, Billbergia, Brocchinia, Brome- da Camara)). Bromelain, extracted from pineapple lia, Catopsis, Cryptanthus, Dyckia, Guzmania, fruits, has ­pharmaceutical use as an anti-inflam- Hechtia, Hohenbergia, Neoregelia, ­Nidularium, matory, and is also used as a meat-tenderizer. There ­Pitcairnia, Tillandsia, and Vriesia. is widespread harvesting of bromeliad ­inflorescences A remarkable feature of many bromeliad from the wild as decoration for churches on ­species in many genera is the ability to impound ­religious holidays in neotropical countries. Very water in the leaf axils. Water thus impounded is many ­species and ­cultivars and hybrids are grown rainwater, or rainwater enriched with nutrients as ornamental plants especially in Europe and leached from tree canopies (throughfall). Large North America. specimens of many species may impound sub- Bromeliads are used in four ways by animals. stantial volumes of water, up to many liters. First, the habitat formed by bromeliad ­phytotelmata Depending upon architecture of individual ­species, is exploited by some aquatic ­animals as aquaria. each of many axils may hold a separate small pool ­Second, some small animals live permanently or of water, or the axils may combine to form a ­central almost so in the non-water-holding axils of bro- tank. These pools of plant-impounded water are meliads, the terraria. Third, bromeliads are used called phytotelmata. They serve to provide a as an occasional place of concealment or hunting ­reservoir of water for absorption by the plant. grounds, or the impounded water is used as a ­Bromeliads under tree canopies contain fallen, source of moisture, by some terrestrial animals, decomposing leaves and seeds and twigs of trees. so these animals are visitors. Fourth, the bromeli- These decomposing materials provide nutrients ads are eaten by some terrestrial animals. Insects that can be absorbed by the bromeliad (dendro- exploit the plants in all four ways, and among the philous nutrition). Decomposition is caused by insects using each way are specialist species fungal and bacterial action, and by aquatic which have no other means of existence­ or ­habitat. ­invertebrate animals. Bromeliads not under tree Bromeliads are therefore essential to the existence canopies depend on inputs of wind-blown nutri- of many insect species. Many other invertebrate ents (anemophilous nutrition). Typically, algae use animals and a few vertebrates also play a role. these wind-blown nutrients and a food chain Additionally, there are three ways in which depends upon consumption of algae. Epiphytic ­bromeliads exploit animals: first, as dispersers of bromeliads that lack tanks are said to be “aerobic,” seed; second, as pollinators; and third, as food and have in the USA been labeled as “air plants.” (carnivory). Bromeliad Fauna B 567 Aquatic Animals Using Bromeliad genera Metacypris, Candonopsis, and Elpidium. Phytotelmata as Habitat for their The first to be described was Metacypris Immature Stages ­bromeliarum Müller, from Brazil. Others have been found in Colombia, Costa Rica, Jamaica, The account below is not intended as a catalog, Mexico, Puerto Rica, and Florida. Some are and it omits some groups and mentions few of the known from no habitat other than bromeliad individual species. phytotelmata. Cyclopoid and harpacticoid copepods have Rotifera been found in bromeliad phytotelmata in sev- eral neotropical countries and at least some of them are specialists to that habitat. The finding Rotifers (wheel animalcules) dwell in many fresh- of one of the harpacticoid species (Phyllogna- water habitats, and some of these habitats are bro- thopus viguieri Maupas) in cultured bromeliads meliad phytotelmata. The earliest mention of a in Indonesia and the United Kingdom, and rotifer in bromeliads was in Costa Rica in 1913. another (Attheyella ­aliena (Noodt)) in ­Germany The most thorough study to date was made in suggested that these organisms had been trans- Jamaica in the early 1990s, when 41 of the 211 spe- ported in horticul­tural specimens. A cyclopoid cies reported from Jamaica were documented species, Bryocyclops ­anninae Menzel, also was from bromeliads. They belong to 12 genera includ- found in a botanical ­garden in Indonesia, ing Lecane, Lepadella, and Cephalodella. although its occurrence in Puerto Rico suggests the latter locality or a wider area of the West Annelida Indies is its origin. Cladocera are rare inhabitants of bromeliad An aquatic oligochaete worm, Dero superterrenus phytotelmata; they are represented only by Michaelsen, was first detected and described from ­Daphnia ambigua Scourfield in Jamaica andAlona Costa Rican bromeliads and found to be an bromelicola Smirnov in Nicaragua. Sesarma and ­obligate bromeliad inhabitant. Later, it was found Metopaulias are genera of crabs. Sesarma angusti- to be quite widespread in neotropical countries. pes Dana was described from Brazil (later detected The mystery of how it manages to distribute itself in Trinidad), and Metopaulias depressus Rathbun among epiphytic bromeliads – when it seems from Jamaica, both in the nineteenth century. They ­limited to the aquatic environment of bromeliad reproduce only in the habitat provided by bro- axils – was solved when worms were seen to be meliad axils, and M. depressus provides maternal attracted to bromeliad-dwelling frogs. Quite sim- care to its brood. The crabs are able to climb trees ply, the worm is phoretic on the moist skin of frogs. to distribute themselves from bromeliad to This method – phoresy, or “hitching rides” – has bromeliad. been detected in other aquatic invertebrates ­having limited mobility. In contrast, the aquatic insects present in bromeliad phytotelmata have winged Acari adults, so their ability to disperse is assured. Arrenurus andrewfieldi Orghidan & Gruia is an aquatic mite known from axils of Aechmea ­aquilega Crustacea in Venezuela. Other aquatic mites of the same family (Arrenuridae), and some attributed to the Ostracods (seed shrimps) found in the water in family Anoetidae, have been reported from bromeliad phytotelmata include species of the ­bromeliad phytotelmata in other countries. 568 B Bromeliad Fauna Odonata strictly aquatic larvae (Odonata, Plecoptera, and Trichoptera) are represented in bromeliads in neo- Larvae of dragonflies and damselflies are aquatic tropical countries. and predatory. They have well-developed legs and thereby are able to climb out of the water from one leaf axil and into the water in another. At least 12 Diptera species are now reported to have been detected in bromeliad phytotelmata in neotropical countries, It is the order Diptera (flies) which has the record and some of them appear to be specialists to this for the largest number of families (at least 15) and habitat, having been found nowhere else. These ­species (hundreds) with aquatic larvae reported specialists are all species of damselflies, especially from bromeliad phytotelmata. They include lar- of the genus Leptagrion. vae of Tipulidae, Anisopodidae, Sciaridae, ­Ceci- dodomyiidae, and Psychodidae. They include ­Ceratopogonidae whose adults are important in Hemiptera pollination of cacao, case-making and non-case- making larvae of Chironomidae. They include Aquatic Hemiptera are represented by eight Tabanidae, Stratiomyiidae, Phoridae, Syrphidae, ­species of seemingly obligate bromeliad-dwellers Borboridae, Aulacigastridae, and Muscidae. in the family Veliidae (sometimes called broad The family Culicidae (mosquitoes) is espe- shouldered water striders). Four belong to the cially well represented, with well over 200 species genus Paravelia and four to Microvelia. That reported in the literature. Furthermore, a few of these genera belong to separate subfamilies sug- these mosquitoes are among the best studied gests that ­adaptation to the bromeliad habitat ­denizens of bromeliad phytotelmata. This began occurred independently at least twice. Veliids with the realization that the subgenus Kerteszia of are predators. the genus Anopheles contains several species which develop only in bromeliad phytotelmata, and Kerteszia adults are important vectors of malaria. Coleoptera Studies in Trinidad in the late 1940s were followed by studies in the Brazilian state of Santa Catarina, Larvae of three families of water beetles have been and were aimed at preventing transmission of found in bromeliad phytotelmata in neotropical malaria to workers on cacao plantations and in countries. The families are Dytiscidae and Hydro- urban areas surrounded by forest. Unfortunately, philidae (both with predatory larvae), and Scirtidae the simplest solution appeared to be destruction (once known as Helodidae or Cyphonidae) with of bromeliads, and in southern Brazil this took the larvae believed to be filter-feeding detritivores. form of deforestation of a “cordon sanitaire” around urban areas. Public health workers seem to have adopted a concept that bromeliads are a Trichoptera major source of mosquitoes transmitting diseases. Thus, when Old World forms of dengue fever were Larvae of most caddis flies live in freshwater detected in the Neotropics, beginning in the late streams. One species, Phylloicus bromeliarum Mül- 1970s and with continuing problems, public health ler, has adapted in Brazil to the habitat provided by workers targeted bromeliads as a source of the bromeliad phytotelmata. From Costa Rica there is vector mosquitoes (Aedes aegypti (L.) and, begin- a record of a stonefly (Plecoptera) in bromeliad ning in the late 1980s, Aedes albopictus (Skuse)). phytotelmata. So all three insect orders with That concept is almost wholly erroneous, because Bromeliad Fauna B 569 these species of Aedes mosquitoes rarely develop Thus, the presence of the mosquito larvae is in bromeliad phytotelmata. Likewise, public health ­helpful to the bromeliads, and the bromeliads workers in Florida have erroneously targeted provide a habitat for the mosquito larvae, so this ­bromeliads as a source of the Culex mosquitoes is a symbiosis. These mosquitoes are not known that transmit West Nile virus in the USA, although to transmit any diseases to humans, although they such larvae of such mosquitoes rarely develop in take human blood as well as the blood of other bromeliad phytotelmata. vertebrates such as rabbits. They are viewed by In Florida, larvae of two mosquito species, humans as pests. The most appropriate long-term Wyeomyia mitchellii (Theobald) andW. vanduzeei solution to their population control is biological Dyar & Knab, are highly adapted to existence in control by competition. Such biological control the water in bromeliad leaf axils. Typically, few of would introduce organisms that would compete them survive to adulthood because of food for nutrients with the mosquito larvae. Such ­shortage. Thus, they compete with each other in ­competitors would probably be neotropical species scramble competition, and they are adept at of non-biting midges such as Chironomidae. Use sequestering the small amounts of food available. of predators against the mosquito larvae would They are able to survive weeks of starvation which likely provide no solution at all, because survivors non-specialist mosquito larvae are unable to do. of predation would inherit the food resources and This also allows them to out compete larvae of thus develop faster and produce larger and thus other mosquitoes that from time to time occur in more fecund adults (Fig. 64). bromeliad axils. Females of these mosquitoes have color vision and select light-colored (light green) oviposition sites, in contrast to the dark-colored Anura (frogs) sites (preferably black) typically selected by tree ­hole-inhabiting mosquitoes. Females hover over Tadpoles belonging to at least five frog genera: bromeliad axils while ovipositing. When they are Dendrobates (Dendrobatidae), Anotheca, Hyla, and not ovipositing or blood-feeding, they may be Sphaenorhynchus (Hylidae), Syncope (Microhyli- found perched on the trunks of trees harboring dae), and Eleutherodactylus (Leptodactylidae) bromeliads. Males perform up-and-down flights have been reported from bromeliad phytotelmata. over small areas of tree trunks when searching for Adults of Physalaemus spiniger (Miranda-Ribeiro) females. Eggs of W. vanduzeei are made excep- (Leptodactylidae) may deposit their eggs in foam tionally buoyant by having a wax-like coating of nests in bromeliad axils in Brazil, but the tadpoles minute mushroom-shaped structures that trap a develop elsewhere. In contrast, tadpoles of plastron of air; they float vertically at the water ­Dendrobates pumilio Schmidt in Central America surface and may even be washed out of bromeliad are carried up trees to bromeliads on the backs of axils during heavy rain. In contrast, the eggs of parents, and the tadpoles develop in bromeliad W. mitchellii are coated only with a thin layer of a axils feeding on nutritional eggs provided by the greasy substance, are less buoyant, and they float female. Regrettably, the bright colors of many horizontally. ­Larvae depend upon input of dead ­dendrobatid frogs (“poison-arrow” or “poison-dart” leaves, twigs, and seeds that fall into bromeliad frogs) has made them popular in the pet trade, no axils from tree canopies above and are decom- matter that they are poisonous. To supply the pop- posed by fungal and bacterial action. Further ular demand to keep such frogs in aquaria with breakdown of the organic particles and probably bromeliads, hunters have plundered them from digestion of bacteria and fungi in the guts of mos- their natural environment. Consequently, and quito larvae make the nitrogenous content more because of habitat loss, D. pumilio is listed in the rapidly available for uptake by the bromeliads. IUCN Red Book as a threatened species. Other 570 B Bromeliad Fauna

Bromeliad Fauna, Figure 64 Schematic representation of a mosquito and a bromeliad: (a) Female ­Wyeomyia mosquito hovering over a Tillandsia sp. leaf axil while ovipositing. (b) Male Wyeomyia ­mosquito performing up-and-down flight over a small area of a tree trunk while searching for females. (c) Schematic showing how Wyeomyia vanduzeei eggs may be washed out of Tillandsia bromeliads during heavy rain. (d) Schematic showing how leaves and seeds from tree canopies fall and are trapped in bromeliad leaf axils, forming the basis of a food chain. Drawings by John Stark. Bromeliad Fauna B 571 strange development is exhibited by tadpoles of Ants may nest in bromeliad terraria. Some Syncope antenori Walker, which develop in the leaf belong to species that also nest on the ground. axils of a Guzmania bromeliad in Ecuador. Here, Some belong to species that typically are ­arboreal, the tadpoles are born with yolk-filled gastrointes- nesting in hollow twigs and branches. Some tinal tracts, and are able to complete their develop- ­bromeliad species in the genus Tillandsia ment without feeding. (e.g., T. paucifolia Baker) have inflated leaf bases providing cavities protected from rain, and the cavities thus formed are often occupied by ants. Terrestrial Animals Using The ants may cut a small hole in a leaf base for Bromeliad Terraria as Habitat ease of access to the cavity. Investigation may for their Immature Stages reveal whether such bromeliads and their ant tenants participate in a mutualism in which the Bromeliad terraria are the leaf axils that cannot plants also benefit. impound water because they leak. Instead, they accumulate moist organic materials. Typically, inner axils form phytotelmata whereas outer axils Terrestrial Animals Using form terraria. We may also consider the upper Bromeliads as Occasional Habitat, parts of those water-impounding axils that are the Visitors choked with fallen plant debris as terraria. Brome- liad terraria provide habitat for some specialist These visitors are here defined as animals that organisms and many generalists. ­neither eat nor reproduce in bromeliads. They may Beetles of the genus Platynus (Coleoptera: be hunting for prey, they may be seeking moisture or ­Carabidae) typify this group. Among the several concealment from enemies, or they may be present hundred species of this genus, some have specialized just because their wanderings have taken them there. to existence in leaf axils of epiphytic bromeliads, and In Brazil and elsewhere, adult frogs seek refuge their adults and immature stages occur nowhere ­during the daytime in bromeliads. Such vertebrates else. Although their food has not been investigated, differ from bromeliad specialist frogs found in some they are most likely predatory in concordance parts of the tropics in that their tadpoles develop in with their closest relatives. So bromeliads serve as other kinds of habitats. But perhaps because of the hunting grounds for their adults and larvae. These presence of frogs (potential prey), bromeliads are bromeliad specialists occur in Mexico, Central visited by snakes and other frog-eating vertebrates. America, and the West Indies. Birds may find drinking water there. In tropical areas In eastern Brazil, a scorpion Tityus neglectus with ­pronounced wet and dry ­seasons, more indi- Mello-Leitão (Buthidae) and a tarantula spider viduals and species of insects may be present in ­Pachistopelma rufonigrum Pocock (Therophosidae) ­bromeliad leaf axils in the dry season, when brome- have been found so often in terrestrial water-­ liads provide oases of moisture as well as prey for the impounding bromeliads that their association seems predators among these insects. to be obligate. Both are predatory. In Brazil, the ­spider Psecas chapoda (Peckham and Peckham) (Salticidae) reproduces only on the non-water-impounding­ Bro- Terrestrial Animals Eating melia balansae Mez. In the southern USA, one spider Bromeliads Pelegrina tillandsia Kaston (Salticidae) is constantly associated with the atmospheric epiphytic bromeliad Bromeliads in greenhouse cultivation seem more Tillandsia usneoides (L.) although the growth form of often to be attacked by scale insects than by insects the plant does not provide terraria. of any other group, and this may be an artifact due 572 B Bromeliad Fauna to crowding of plants under unnatural conditions were classified within the family Curculionidae, that exclude organisms which could control these but recently the part of that family containing pests. In Florida, these scale insects belong to the Cactophagus and Metamasius has been considered following six families (numbers of species in a separate family (Dryophthoridae). It is unclear parentheses): Asterolecaniidae (2), Coccidae (1), whether any of them is a substantial pest in its Ortheziidae (1), Pseudococcidae (6), and Diaspi- native ecosystem. However, some of them cause didae (8). They can be controlled by chemical substantial damage to cultivated pineapples in ­pesticides or, perhaps, they may be controlled by agro-ecosystems. One of them, Metamasius calli- opening greenhouse walls to allow ingress of tiny zona Chevrolat, which is native to southern Mex- parasitoid wasps (if the greenhouse is in a tropical ico and Guatemala, also causes enormous damage or subtropical area), or by deliberate release of to Florida’s native bromeliad populations after such wasps purchased from biocontrol supply having arrived as a contaminant in one or more companies (none of the necessary wasp species shipments of ornamental bromeliads. A biologi- seems now to be available commercially, but this cal control project against M. callizona is in prog- could change if there were demand). ress in Florida with intent to reduce its ­populations Among pests of fruits of cultivated pineapple, (not eradicate them as is sometimes misstated by the most widespread miner is the larva of a the news media); the objective of ­biological con- ­b u t t e r fl y , Strymon (=Thecla) basilides (Geyer) trol is not to eradicate. (Lepidoptera: Lycaenidae). Perhaps it also attacks Insects that have specialized to eat the leaves of fruits of wild pineapples and perhaps other bromeliads by chewing the surfaces or by ­mining ­members of the genus Ananas. are surprisingly few. They include a few leaf beetles Insect larvae that mine stems of bromeliads (Coleoptera: Chrysomelidae) such as Acentroptera include Castniidae and Acrolophidae (Lepi- basilica Thomson and A. pulchella Guérin Méneville doptera) and Curculionidae and Dryophthoridae in southern South America, the abovementioned (Coleoptera). The castniid species concerned seem adult weevils (Coleoptera: Dryophthoridae and not to have been identified to species level, but Curculionidae), a few caterpillars such as Napaea have been detected by this writer in bromeliads in eucharilla Bates (Lepidoptera: Riodinidae), and natural areas in Mexico, Honduras, and Panama ­larvae of a leaf-mining fly, Melanagromyza rosales and doubtless are yet more widely distributed in Woodley (Diptera: Agromyzidae), in Costa Rica. the tropics. Fully grown larvae are large (~ 5cm), Generalist insects that chew bromeliad leaves and their mining activities surely result in plant include cockroaches (Blattaria), whose actions are death. They have not been seen to be abundant scarcely noticeable outside a greenhouse environ- and their population sizes may be limited by para- ment, and grasshoppers (Orthoptera: Acrididae). In sitoids, although such parasitoids have not been spring in southern Florida (USA), population detected. Larvae of the one acrolophid species ­explosions of “lubber grasshoppers” (Romalea implicated, Acrolophus vigia Beutelspacher, are ­guttata Houttyn (Acrididae)) attack many mono- parasitized by larvae of at least one unidentified cotyledonous plants, including bromeliads; although wasp (Hymenoptera: Braconidae). The subject is the damage they cause initially appears severe, the of academic interest but currently of no economic plants seem to recover by new growth. In Andean interest because A. vigia has not been detected in countries, the spectacled bear, Tremarctos ornatus the USA Larvae of at least 24 weevil species (Cuvier), is reported to include a substantial ­specialize in mining stems of bromeliads. They ­proportion of bromeliads in its diet. belong to three genera, Cholus, Cactophagus, and Larvae of Epimorius testaceellus Ragonot Metamasius. The life cycle of the weevilDiastethus (Lepidoptera: Pyralidae) develop within the flower bromeliarum Champion seems unrecorded. All pods of the bromeliad Tillandsia fasciculata Swartz, Bromeliad Fauna B 573 causing considerable local damage. A tiny wasp the plants trap insects which are decomposed parasitoid attacks these larvae and may limit by bacterial action in their tanks. Although some ­populations of this moth. writers have deemed this to be “proto-carnivory” because the three bromeliads in question do not produce digestive enzymes, the effect is the same. Animals as Dispersers of Bromeliad The first detected instance was in the bromeliad Seed Catopsis berteroniana (Schultes) in southern ­Florida, although the plant has a wider distribution Dispersal of seed in the bromeliad subfamily in the neotropics. Although it grows epiphytically, it ­Tillandsioidea is by wind. The fleshy seeds of many grows typically above tree canopies, so it accumu- Bromelioidea, however, seem designed to attract lates little or no organic debris from trees. It seems feeding by vertebrate animals, and indeed birds to have evolved a method of confusing winged have been reported to consume the seeds, pass ­terrestrial insects so that they stumble into it, have them through alimentary tracts, and disperse them difficulty escaping, and drown and are decomposed together with feces in new habitats. The subject of in the water-filled leaf axils. The two ­Brocchinia seed-dispersal by animals is not well documented. ­species are terrestrial and grow in nutrient-poor habitats in inland Venezuela. We may only hope that the gluttonous commercial trade in carnivorous Animals as Pollinators plants will not plunder these plants from the wild. of Bromeliads Hobbyists should at least be warned that the two Brocchinia species require cool, humid, breezy Feeding by animals at bromeliad nectar may be ­climatic conditions that are hard to match in cultiva- considered as a special case of phytophagy because tion, that populations of C. berteroniana in southern this does no harm to the plants, unless perhaps the Florida are all in ­protected lands, that the plants are animals should consume nectar without effecting specifically protected by law, and that none of the pollination. There are remarkably few observations plants can withstand freezing temperatures. of nectar feeding. Those that are mentioned most are by hummingbirds at large flowers of some large bromeliads, and these may well be over-empha- Conclusion sized because hummingbirds are ­diurnal and easy to see, and by butterflies and a few beetles. Bats are In pre-Columbian times, bromeliads and their documented as pollinators of the genus Werauhia. denizens were a huge ecosystem extending in the Feeding by moths is nocturnal, hard to observe, and Americas from southeastern Virginia (USA) to may be vastly underrated. There is much scope for Argentina. Bromeliads and their animal denizens collaboration between entomologists who can iden- are being destroyed overwhelmingly by encroach- tify the insects ­effecting pollination and botanists ment by human populations. This has been called who can ­identify the bromeliads specifically and “development.” One of the most species-rich areas demonstrate pollination, especially at night. was Brazil’s Atlantic forest, which has been reduced to less than 7% of its former extent, but a similar story prevails everywhere. Some, especially in Animals as Food for Bromeliads Trinidad and Brazil, were destroyed in the twenti- (Carnivory) eth century because of an oversimplified concept that bromeliads are a source of malaria-carrying In just three bromeliad species (one Catopsis and Anopheles mosquitoes, and so the simplest method two Brocchinia) carnivory has developed, because of controlling malaria is to destroy the forest and 574 B Bronzed Cutworm, Nephelodes minians Guenée (Lepidoptera: Noctuidae) the bromeliads. This concept has spilled over, public educational support to laws of many ­irrationally, to other countries, other bromeliads, ­countries that already prohibit “harvesting” of other mosquitoes, and other diseases (or no ­bromeliads from nature for commercial purposes. ­diseases), to which it does not apply. Lesser constraints on bromeliad populations References and their denizens have made their mark because so much has been destroyed by “development.” Frank JH (1983) Bromeliad phytotelmata and their biota, Widespread and vast harvesting of bromeliad especially mosquitoes. In: Frank JH, Lounibos LP (eds) Phytotelmata: terrestrial plants as hosts for aquatic blooms for church activities is having an affect. insect communities. Plexus Publishing, Marlton, NJ, The harvesting of bromeliads from nature has USA, pp 101–128 unequivocally contributed to the spread of pest Frank JH (1996) Bromeliad Biota. Available at http://Bromeli- insects internationally. Selective harvesting of the adBiota.ifas.ufl.edu. Accessed Oct 2006 Janetzky W (1997) Crustacea in bromeliad phytotelmata. rarest bromeliads for the horticulture trade may Available at http://BromeliadBiota.ifas.ufl.edu/crbrom. be having a negative affect, although a counter- htm. Accessed Oct 2006 argument has been made that they are being Janetzky W, Koste W (1997) Rotifera in bromeliad phytotel- ­propagated and thus will survive in culture. mata. Available at http://BromeliadBiota.ifas.ufl.edu/ robrom.htm. Accessed Oct 2006 Destruction of native bromeliad populations in Picado C (1913) Les broméliacées épiphytes considerées Florida by a pest weevil (which arrived as a comme milieu biologique. Bulletin des Sciences de la ­contaminant of “ornamental” bromeliads from France et de la Belgique 47:215–360 Polhemus JT, Polhemus DA (1991) A review of the veliid Mexico) is having an overwhelming negative affect fauna of bromeliads with a key and description of a new on the bromeliad populations – its affect on the species (Heteroptera Veliidae). J New York Entomol Soc bromeliad fauna in Florida has not yet been 99:204–216 addressed although it surely must likewise be ­negative. We have some idea of the reduction of Bronzed Cutworm, Nephelodes bromeliad populations throughout their former minians Guenée (Lepidoptera: range, but we have no idea of the reduction of Noctuidae) populations of the animals that depend upon bro- meliads; we can only guess that it is at very least as This caterpillar is a pest of turfgrass, and occasion- bad, most likely worse. Harvesting of selected bro- ally other crops. meliad-inhabiting animals from nature, such as  Turfgrass Insects and Their Management Dendrobates frogs, threatens their very existence  Turfgrass Insects of The United States: Biology but fortunately most bromeliad-dwelling organ- and Management isms lack appeal to hobbyists, and so are threatened “merely” by development destroying bromeliads. Involved biologists have four major options. Brood The first is to study the heck out of native brome- liad faunas in numerous neotropical countries In asocial insects, this generally refers to a cohort while there still is a fauna. The second is political of individuals resulting from deposition of a lobbying for the preservation of tracts of land that ­cluster of eggs and developing concurrently. may preserve part of the fauna (some of it will ­However, sometimes it is used to refer to all the inevitably be lost with “development”). The third is offspring of a parent, which may include several to persuade churchgoers of Latin American clusters of eggs produced over the lifespan of the churches not to harvest bromeliads from nature – female. In social insects, this refers to all the imma- to use other sorts of decorations instead of ture offspring of a colony, and may consist of eggs, destroying the environment. The fourth is to­provide larvae, nymphs and pupae. Brown Citrus Aphid, Toxoptera citricida (Kirkaldy) (Hemiptera: Aphididae) B 575 Brood Cell

Among social insects, a cell, chamber or pocket constructed to house the immature stages.

Brooding

A form of parental care wherein the young insects remain near the parent insect (though in some insects surrogate parents are employed). Some- times the parents actively engage in defense of the young, but often they do not. Broun, Thomas, Figure 65 Thomas Broun. Brood Sac

In cockroaches, an internal pouch, usually under the Brown Citrus Aphid, Toxoptera wing covers, where eggs are incubated in females. citricida (Kirkaldy) (Hemiptera: Aphididae)

Broun, Thomas james h. tsai University of Florida, Ft. Lauderdale, FL, USA Thomas Broun was born in Edinburgh on July 15, 1838. His father and an uncle were natural- The brown citrus aphid, Toxoptera citricida, is ists and probably influenced him. At the age of believed to originate from China. Until 1900, this 16, he joined the British army, took part in the insect was confined to southeast Asia, Australia, Crimean war, and then served in Burma and New Zealand, the Pacific Islands including Hawaii, India during the Indian Mutiny. In 1862 he South Africa, and South America. Since then it has married and ­emigrated to New Zealand. At become established in several countries of Central outbreak of the Maori war, he was commis- America and many islands in the Caribbean Basin. sioned as captain, served throughout the war, Brown citrus aphid was first discovered in 1995 in and attained his majority. After that war, he south Florida; in the following two years, this began to work on New Zealand insects. In 1880 insect had expanded into all citrus ­production was published his “Manual of New Zealand areas in Florida. Because of its ability to transmit Coleoptera” which listed 1,140 species. Supple- citrus tristeza virus (CTV) in an ­efficient manner, ments increased this total to 3,979 species. In the combina tion of brown citrus aphid and CTV 1890 he was appointed Government Entomo­ has become an important ­problem of citrus world- logist. His type specimens are mainly in the wide. Disastrous epidemics of ­citrus tristeza virus Natural History Museum, ­London. He died on have occurred in association with brown citrus August 24, 1919 (Fig. 65). aphid in Argentina, Brazil, Colombia, and Peru. CTV is known to cause decline and death of citrus References trees grafted on sour orange (Citrus aurantium L.) rootstock, but some CTV isolates can cause stem Herman LH (2001) Broun, Thomas. Bull Am Mus Nat Hist pitting regardless of rootstock, and can result in 265:49 long-term debilitation that reduces yields of sweet 576 B Brown Citrus Aphid, Toxoptera citricida (Kirkaldy) (Hemiptera: Aphididae) orange and grapefruit from 5 to 45%. Currently, there Nymphs undergo four instars. The developmental are about 185 million citrus trees in Florida grafted times for nymphal stages vary with temperatures on the susceptible sour orange rootstock. Citrus and host plants. Within a ­temperature range of tristeza poses a real threat not only to Florida’s cit- 8–30°C, the length of nymphal development rus industry, but also to other citrus producing decreases as ­temperature increases. The average states in the U.S. Brown citrus aphid feeding causes developmental times for first, second, third and leaf distortion and shortening of terminal growth. fourth instars are 1–12, 1–13, 2–16 and 2–22 Its honeydew ­provides a good medium for growth days, respectively. At 5°C, nymphs fail to develop of sooty mold. More importantly, brown citrus beyond the second instar. At 32°C, the develop- aphid is the most efficient vector of CTV as mental times for all nymphal stages increase com- ­compared with other citrus aphids such as Aphis pared to those at 28–30°C. The adults can survive gossypii, A. spiraecola and Toxoptera aurantii. and reproduce within the temperature range of The overall transmission efficiency of CTV by 10–32°C (Fig.­ 66). T. citricida ranges from 1 to 13% dependent upon The mean longevity of females decline expo- CTV isolates and biotypes of vector. Brown citrus nentially from 60 days to 7 days as temperatures aphid reproduces parthenogenetically. Most females increase from 10 to 32°C. The maximal longevities start to produce nymphs within 24 h after­emergence. of individual females are 90, 62, 47, 30, 19, 15 and

Brown Citrus Aphid, Toxoptera citricida (Kirkaldy) (Hemiptera: Aphididae), Figure 66 Winged and wingless adults of brown citrus aphid, Toxoptera citricida (photo P. Choate, University of Florida). Brown Dog Tick or Kennel Tick, Rhipicephalus sanguineus (Latreille) (Acari: Ixodida: Ixodidae) B 577 9 days at 10, 15, 20, 25, 28, 30 and 32°C. Fecundity is References more affected by temperatures; at 10 and 32°C, the fecundity is adversely affected. The average nymph Bar-Joseph M, Roistacher CN, Garnsey SM, Gumpf DJ (1981) production by adults within 15–30°C increases to a A review on tristeza: an ongoing threat to citriculture. Proc ISC 1:419–422 maximum of 53 nymphs per female at 20°C, then Michaud JP (1998) A review of the literature on the brown decreases sharply as temperature increases. The citrus aphid, Toxoptera citricida (Kirkaldy). Fla Entomol daily rate of nymph production ­varies with adult 81:37–61 age. The peaks of reproduction appear at 4 through Michaud JP, Browning HW (1999) Seasonal abundance of the brown citrus aphid, Toxoptera citricida (Homoptera: 10 days after adult emergence, with an average of Aphididae) and its natural enemies in Puerto Rico. Fla 2–5 nymphs per day. The ­duration of reproduction Entomol 82:424–447 lasts as long as adult ­longevity within the tempera- Rocha-Peña MA, Lee RF, Lastra R, Niblett CL, Ochoa-Co- ture range of 15–30°C. rona FM, Garnsey SM, Yokomi RK (1995) Citrus tristeza virus and its aphid vector, Toxoptera citri- The biology of brown citrus aphid is also cida. Threats to citrus production in the Caribbean affected by host plants on which the populations are and Central and North America. Plant Dis reared. The average nymphal development periods 79:437–445 Tsai JH (1998) Development, survivorship, and reproduc- on rough lemon, sour orange, grapefruit, and key tion of Toxoptera citricida (Kirkaldy) (Homoptera: lime are from 5.9 to 6.2 days. However, longer devel- Aphididae) on eight host plants. Environ Entomol opmental periods (6.5–7.2 days) are required on 27:1190–1195 box orange, calamondin, lime berry and orange Tsai JH, Wang K (1999) Life table study of brown citrus aphid (Homoptera: Aphididae) at different temperatures. ­jassamine. The average number of nymphs­produced Environ Entomol 23:412–419 per female reared on sour orange, grapefruit, key lime, rough lemon, ­calamondin, box orange, lime berry and orange jassamine are 59, 43, 34, 43, 33, 18, 21 and 23 nymphs. Female adults live an average of Brown Dog Tick or Kennel Tick, 23 days on these hosts. Because young citrus flush Rhipicephalus sanguineus occurs only intermittently in commercial groves, it (Latreille) (Acari: Ixodida: is believed that plants other than commercial citrus Ixodidae) play an important role in sustaining brown citrus aphid populations when young citrus shoots are igor uspensky not available. The Hebrew University of Jerusalem, Jerusalem, Brown citrus aphid can be controlled by a Israel ­number of pesticides. Hymenopteran insects play a critical role in pollination and fruit set. Pesticide Rhipicephalus sanguineus is the main vector and application can greatly affect the pollination pro- reservoir of a group of bacteria now called the cess in the blooming season; thus the material and Rickettsia conorii complex. They are causative time of application are of great significance in agents of a number of similar human diseases reducing ­mortality of pollinators. Other biocontrol known earlier as Mediterranean spotted fever, and agents such as parasitoids (Lysiphlebia spp., Apheli- distributed all around the Mediterranean and nus sp. and Lipolexis sp.), syrphid fly (Pseudorus Black Seas as well as in India and some countries clavatus), ladybeetles (Cycloneda sanguinea, Har- of southeastern Asia. According to the current monia ­axyridis and Coelophora inaequalis), lace- data, new varieties of this disease connected with wing (Chrysopa spp.), and entomopathogenic fungi R. sanguineus have been distinguished that are (Beauveria bassiana isolates) show various degrees caused by different subspecies ofR. conorii, namely of effectiveness in control of brown citrus aphid. Mediterranean spotted fever (subsp. conorii) in  Citrus Pests and Their Management the Mediterranean area, including northern Africa 578 B Brown Dog Tick or Kennel Tick, Rhipicephalus sanguineus (Latreille) (Acari: Ixodida: Ixodidae) and southern Europe; Israeli tick typhus (subsp. ungulates. Later, dogs became its main and often israelensis) in Israel; Astrakhan fever (subsp. caspia) only hosts. Spread of the tick worldwide has been in the lower reaches of the Volga River in Russia; ­connected with human transport of dogs over the and Indian tick typhus (subsp. indica) in Asia. In globe. At present, this tick can be found in all addition, the brown dog tick was known as the ­continents between the latitudes of 50°N and vector of Rickettsia rickettsii, the causative agent of 35°S, but sometimes even further in association Rocky Mountain spotted fever in Central America, with dogs living indoors (in houses or kennels). It mainly in Mexico. Recently, a focus of this disease was recorded from all 50 states of the USA, many with R. sanguineus as the only vector was described sites in Canada, as well as from such European and investigated in Arizona, USA. The broad countries as Belgium, Denmark, England, Ger- ­distribution of this tick raises concern about such many, Norway, Poland and some others. Some foci in adjacent states. Several new species of Rick- cases of human infection with R. conorii by ticks ettsia were also isolated from R. sanguineus, and inside human dwellings were documented. Rickettsia massiliae was documented as a human Being ecologically flexible and tolerant of a pathogen. The brown dog tick was shown to­harbor large range of climatic conditions, R. sanguineus Coxiella burnetii (the causative agent of Q-fever) populates various areas, mainly inhabited localities for many years after the death of the tick. Rhipi- including human dwellings, but also uninhabited cephalus sanguineus transmits several agents environments which may be humid tropical, pathogenic for dogs. The causative agent of canine ­subtropical or continental (semi-desert). Unfed ehrlichiosis, Ehrlichia canis, originally described in ticks are active for the whole year in the tropics, the Mediterranean area, was later found in numer- indoors as well as in the field. Under tropical ous areas of the world, and today its distribution ­conditions, ticks may have three generations completely coincides with the tick’s range. ­during the year. Year round activity has also been ­Rhipicephalus sanguineus also transmits ­protozoan observed in ticks living together with dogs in dog pathogens, such as Babesia canis endemic in human dwellings in all regions. Unfed ticks living the USA and Africa, and B. gibsoni in the Far East in the field to the north or south of the tropical and North Africa. Several other pathogens were zone are active from spring until autumn. Here isolated from this tick, but their epidemiological they have two or sometimes only one generation or epizootiological significance is either small or annually. The more temperate the climatic unclear. Transstadial and transovarial passage of ­conditions, the shorter is the period of activity of R. conorii, R. massiliae and B. canis has been unfed R. sanguineus specimens. In Mediterranean proven. ­countries, the season of adult activity lasts for 6–8 The difficulties of species identification in the months, from March-April until October-November, genus Rhipicephalus resulted in subdividing the depending on the environmental conditions of a genus into groups of closely related species. In par- particular area. ticular, the R. sanguineus group includes about ten Host seeking behavior of unfed ticks depends species, with R. turanicus being the most difficult to on the conditions of their habitation. When the distinguish from R. sanguineus. At the same time, dog ticks live in human localities, they are genetic analysis of ticks from different areas of the ­constantly rather close to their main hosts, often world showed that there are distinct patterns for just around the dog’s bedding area. When ticks are R. sanguineus and that the intraspecific variability ready to feed, they migrate a very short distance to of sequences within the species is very low. This their hosts, catch onto them and move over the means that R. sanguineus is a valid species. dog’s body looking for an attachment site. In the The brown dog tick is the only cosmopolitan field, the ticks use an ambush strategy positioning species of ticks. This species originated from on the vegetation, preferably on the tips of low Africa where its hosts were local carnivores and grass, often in clusters. In the adult ticks, the Brown Dog Tick or Kennel Tick, Rhipicephalus sanguineus (Latreille) (Acari: Ixodida: Ixodidae) B 579 ­anterior end of the body usually points towards The brown dog tick (Fig. 67) is a typical exo- the ground. Questing ticks can catch onto a pass- philic three-host tick. The larva feeds for 3–6 days, ing host or, sensing it from a distance, they move the nymph for 4–10 days and an adult female for in its direction, rather quickly over the sandy 6–13 days. Insemination of the adult female takes ground. Rhipicephalus sanguineus in the open field place on the host after 3–4 days of feeding. With- lives under much more inhospitable conditions out insemination, the female stops its engorge- than ticks living in dense forests due to low humid- ment and lives in an attached position until ity and great fluctuations of ambient temperature. insemination, or death from drying. The larvae Under such conditions, the ticks are incapable of increase their weight ­during feeding 10 to 20-fold, prolonged questing activity. To replenish their while nymphs increase their weight 60 to 75-fold water reserves, ticks must regularly migrate down and adult females 70 to 120-fold. The adult males to the litter and soil where temperature is lower feed for 3–5 days, increasing their weight 1.5 to and humidity higher. Dog ticks have eyes and 2-fold. Henceforth, males migrate over the host apparently use them effectively both for choice of body, attaching in different sites. The mass of an optimal illumination and for searching for hosts. unfed larva is 0.02–0.025 mg, whereas the mass of The capacity of R. sanguineus for active a fully engorged female reaches 200–350 mg and it migrations is rather limited. There are no data can lay up to 5,000 eggs. Two main components about tick migrations in tropical areas, but in provide the increase of tick reproductive capacity: semi-desert areas the unfed specimens can move minimizing egg size (and, hence, unfed larval upwards up to 20–40 cm, with the difference mass) and increased capability for interstage between ticks of different stages being undetect- growth during nymphal feeding. able. An interesting phenomenon concerning The minimal weight of engorgement after which engorged nymphs and females in or near human females are capable of laying eggs is about 20 mg. dwellings has been documented many times: after After the female reaches the weight of 170–200 mg, repletion and detachment, they migrate vertically over the walls looking for suitable sites (cracks, crevices) for molting or egg-laying. The height of such migrations may be up to 2.5 m. The season of activity for unfed subadults (larvae and nymphs) depends on the seasonality of adult ticks. In the tropical zone, subadults can be active during the entire year, with periodic and sometimes rather small fluctuations in their abun- dance. Under more temperate climatic conditions, the abundance of unfed subadults increases soon after the decrease in adult abundance, larval activ- ity preceding that of nymphs. The life span of individual adults after molting continues from 3–4 months during summer months, to about 8–9 months if the hibernation followed with behav- ioral diapause takes place. In continental climates, only engorged nymphs and unfed adults can suc- cessfully survive during the winter. Unfed ticks Brown Dog Tick or Kennel Tick, Rhipicephalus that do not find a host and cannot feed during the Sanguineus (Latreille)Acari: Ixodida: Ixodidae), activity season die due to complete expenditure Figure 67 The brown dog tick, Rhipicephalus of their nutritional reserves. sanguineus. 580 B Brown Dog Tick or Kennel Tick, Rhipicephalus sanguineus (Latreille) (Acari: Ixodida: Ixodidae) the dependence of egg number/mg of engorged importance. Experiments on the treatment of tick female becomes linear and equals approximately hosts or tick location sites by preparations based on 15–17 eggs/mg of the female weight. Weight char- fungi and nematodes have shown that some patho- acteristics and fecundity of the cosmopolitan gens have an obvious acaricidal effect. However, it is R. sanguineus are different in populations from too early to estimate their real possibility for practi- different regions. The populations from tropical cal purposes of human protection. conditions have smaller engorged female weights  Ticks and, hence, lower fecundity. The brown dog tick is a host-specific species, References having the dog as its main host, though it can also feed on different vertebrates, such as livestock, Beati L, Keirans JE (2001) Analysis of the systematic relation- some carnivores, lagomorphs, rodents, insecti- ships among ticks of the genera Rhipicephalus and Boo- vores. All three parasitic stages can use dogs philus (Acari: Ixodidae) based on mitochondrial 12S ribosomal DNA sequences and morphological charac- (sometimes the same individual) as hosts. Under ters. Journal of Parasitology 87:32–48 conditions of extreme proximity with the host, Goodman JL, Dennis DT, Sonenshine DE (eds) (2005) there are cases where the tick changed from a Tick-borne diseases of humans. American Society for three-host type of development to a two-host type. Microbiology, Washington, DC Ioffe-Uspensky I, Mumcuoglu KY, Uspensky I, Galun R (1997) Sometimes larvae did not leave the dog after Rhipicephalus sanguineus and R. turanicus (Acari: Ixodi­ engorgement, and molted to nymphs on the host. dae): closely related species with different biological In other observations, these were engorged nymphs characteristics. J Med Entomol 134:74–81 that molted on the host to adults. Adults actively Ioffe-UspenskyI, Uspensky I, Mumcuoglu KY, Galun R (2005) Rhipicephalus sanguineus and R. turanicus (Acari: Ixo- attack people in the Palaearctic and are the main didae): numerical indices for distinguishing between source of human infection by different pathogens. adults of closely related species in Israel. In:5th interna- Until recently, R. sanguineus rarely attacked people tional conference on ticks and tick-borne pathogens, programme, proceedings. Université de Neuchâtel in the Nearctic, particularly in the USA. However, ­Switzerland, pp 171–175 during the last several decades this tendency seems Nicholson WL, Paddock CD, Demma L, Traeger M, Johnson B, to have changed and a number of cases of human Dickson J, McQuiston J, Swerdlow D (2006) Rocky moun- bites by the brown dog tick have been recorded. tain spotted fever in Arizona: documentation of heavy environmental infestations of Rhipicephalus sanguineus The recent outbreak of Rocky Mountain spotted at an endemic site. Ann N Y Acad Sci 1078:338–341 fever in Arizona was connected to heavy infesta- Parola P, Paddock CD, Raoult D (2005) Tick-borne rickettsio- tion of dogs by R. sanguineus and numerous ticks ses around the world: emerging diseases challenging old of this species in the yards of patients’ homesites. concepts. Clin Microbiol Rev 18:719–756 Pegram RG, Keirans JE, Clifford CM, Walker JB (1987) Clari- Because the dog is a principal factor in human fication of the Rhipicephalus sanguineus group (Acari, tick-borne infections, the suppression of ticks on Ixodoidea, Ixodidae). II. R. sanguineus (Latreille, 1806) dogs by using systemic acaricides or plastic collars and related species. Syst Parasitol 10:27–44 Uspensky I, Ioffe-Uspensky I (2002) The dog factor in brown impregnated with acaricides is an effective protec- dog tick Rhipicephalus sanguineus (Acari: Ixodidae) tion of humans from tick attacks and bites. Dogs infestations in and near human dwellings. Int J Med heavily infested by ticks are dipped into water mix- Microbiol 291(Suppl 33): 156–163 tures prepared with acaricidal emulsifiable concen- Uspensky I, Ioffe-Uspensky I, Mumcuoglu KY, Galun R (1999) Body weight characteristics of some ixodid ticks: reflect- trates and wettable or soluble powders. Regular ing adaptations to conditions of their habitats? In Bruin J, cleaning of kennels, changing beddings, and acari- van der Geest LPS, Sabelis MW (eds) Ecology and cidal treatment of sites which dogs frequent are ­evolution of the Acari. Kluwer Academic Publishers, necessary measures for tick suppression. Educa- Dordrecht, The Netherlands, pp 657–665 Walker JB, Keirans JE, Horak IG (2000) The genusRhipiceph - tional programs for dog owners might be useful for alus (Acari, Ixodidae). A guide to the brown ticks of the increasing their knowledge about tick medical world. Cambridge University Press, ­Cambridge, UK Brues, II, Charles Thomas B 581 Brown Lacewings father to Argentina. Later that same year he obtained a job providing photographic and print- Members of the family Hemerobiidae (order ing services to the newly-built Museo de La Plata. Neuroptera). The insect collection that he had formed in  Lacewings, Antlions and Mantidflies ­Germany became the foundation of the entomo- logical section of the museum, and later he became head of that section despite lack of formal training Brown Planthopper, Nilaparvata in entomology. In 1906 he was appointed profes- lugens (Hemiptera: Delphacidae) sor of zoology of Universidad de La Plata. In 1913 the title of “doctor honoris causa” was bestowed upon him, followed by other titles. His research This is a serious pest of rice in Southeast Asia. and some 200 publications were on diverse groups  Area-Wide Insect Pest Management of insects. He died on July 3, 1943. Pages 48–55 of Revista de la Sociedad Entomologica de Argentina (vol. 43), written by several authors as representa- Brown Rot of Fruit tives of several Argentine institutions, laud his accomplishments. These are fungal diseases of fruit that are transmit- ted by insects.  Transmission of Plant Diseases by Insects Reference

Herman LH (2001) Bruch, Carlos. Bull Am Mus Nat Hist 265:49–50 Brown Wheat Mite, Petrobia latens (Müller) (Acari: Tetranychidae) Bruchidae This mite causes injury to wheat.  Wheat Pests and Their Management A family of beetles (order Coleoptera). They com- monly are known as seed beetles.  Beetles Brown-Banded Cockroach, Supella longipalpa (Fabricius) (Blattodea, Blattellidae) Brues, II, Charles Thomas

This common cockroach is one of the more Charles Brues was born on June 20, 1879, in West important pests in cooler climates. Virginia. His high school years were spent in  Cockroaches ­Chicago, but instead of attending the University of Chicago, he went to the University of Texas, persuaded to do so by William Morton Wheeler who had just been appointed head of the zoology Bruch, Carlos department there. A schooldays friendship with A. L. Melander, both of whom had been intro- Carlos Bruch was born in Munich in 1869. He was duced to entomology by H. E. Walter, was contin- interested in natural sciences but at age 14 joined ued in Texas and until the death of Brues many his father’s business, and then in 1887 followed his years later. They coauthored entomological 582 B Brulle, Gaspard Auguste papers while at Texas. After graduation with A.B. French government-sponsored expedition to degree in 1901 and M.S. degree in 1902, Brues Moorea, and enthusiastically studied insects. In went to Columbia University, but then returned 1933–1839 he was an assistant at the Muséum to Texas to work for the U.S. Department of Agri- National d’ Histoire Naturelle in Paris, working culture. In 1905 he moved to the Milwaukee Pub- for the chairman of entomology. In 1832, with lic Museum to work as Curator of Invertebrate other entomologists, he contributed to founding Zoology, but in 1909 relocated to Harvard Uni- the Société Entomologique de France. His (1839) versity to become instructor in economic ento- professional thesis presented to the Faculté des mology, with William Morton Wheeler as his Sciences of Université de Paris was on deposits of supervisor. In 1935 he was promoted to Professor fossil insects. In 1839 he was appointed to a of Entomology and also was Associate Curator of ­professorship of zoology and comparative anat- Insects at the Museum of Comparative Zoology. omy in Dijon. Unfortunately for entomology, his In 1946 he was made Emeritus Professor of Ento- duties in Dijon precluded his further contribu- mology at Harvard. He collected insects through- tions to studies of insects. Nevertheless, from out the United States, and in the Philippines, East 1831 to 1843, he published on taxonomy of Indies, West Indies, and South America. He was Coleoptera and Hymenoptera, mostly in Annales an active member of the Cambridge Entomologi- de la Société Entomologique de France. The cal Club and editor of its publication (Psyche) (1834–1837) book “Histoire naturelle des from 1910 to 1947. Among his publications are “A insectes”; that he ­co-authored with Audouin key to the families of North American insects” (Brullé wrote for it the sections of Coleoptera, (first published in 1915 and coauthored with Orthoptera, and Hemiptera) was not completed. Melander, and later revised), “Insects and human He was awarded France’s ­highest medal, the welfare” (1921, later revised), and “Insect dietary” Légion d’ Honneur. He died on January 21, 1873. (1946). His research was on taxonomy and behav- ior of phorid flies in ant nests, “parasitic” Hymenoptera, food and feeding habits of insects, Reference medical entomology, and tissue staining, and thermophilous insects. He was a stimulating Desmarest E (1873) Note sur la vie et les travaux ento- advisor of his graduate students. He died in Flor- mologiques d’ Auguste Brullé. Annales de la Société ida on July 22, 1955, survived by his wife and a Entomologique de France (5)2:513–516 son and daughter.

Brunner Von Wattenwyl, Carl Reference Carl Brunner was born in Bern on June 13, 1823, a Mallis A (1971) Charles Thomas Brues, II. In American ento- member of a notable Swiss family, but moved at an mologists. Rutgers University Press, New Brunswick, early age to Vienna. His early publications were in NJ, p 434–435 chemistry, physics, geology, glaciology, and meteo- rology. In 1861 he published his first important con- tribution on Orthoptera, then in 1865 the first of a Brulle, Gaspard Auguste series of papers on classification of Blattodea. These were followed in 1878 by a paper on classification of Auguste Brullé was born in Paris on April 7, 1809. Tettigoniidae, then in 1888 on that of Stenopelmati- At school he showed a taste for the natural sci- dae and Gryllacrididae. In 1882 was published his ences. Then, in 1829 he was able to take part in a encyclopedic work of the European Orthoptera Brush-Footed Butterflies (Lepidoptera: Nymphalidae) B 583 “Prodromus der Europäischen Orthopteren.” In all, Subfamily: Apaturinae he published 27 works on Orthoptera and was one Subfamily: Nymphalinae of the most notable of orthopterists. He died on Subfamily: Danainae August 24, 1914, at Kirchdorf, Austria, and his Subfamily: Heliconiinae Orthoptera collection is in Vienna. Subfamily: Biblidinae

References Distinguishing Characteristics and Relationships Burr M (1900) Brunner von Wattenwyl. Ent Rec J Var 12:12 + pl. 1 One distinctive and unambiguous character is Rehn JAG (1915) Carl Brunner von Wattenwyl. Entomol News 26:285–288 unique to the Nymphalidae: the ventromesial ­surface of the antenna has three longitudinal ridges (termed carinae, meaning “keel”; the antenna is hence “tricarinate”), one lying either side and one Brush-Footed Butterflies separating two shallow longitudinal grooves. Two (Lepidoptera: Nymphalidae) further characters may be the ­presence of a distinc- tive structure, von Siebold’s organ, in the female keith r. willmott genitalia, and a filiform seta in the mature larva that The Natural History Museum, London, United is absent in other papilionoid families. Kingdom The sister taxon (most closely related group) to the Nymphalidae is thought to be the Lycaeni- The Nymphalidae is one of five families in the dae plus Riodinidae, which share several thoracic superfamily Papilionoidea (true butterflies) of the and musculature characters with the family. More order Lepidoptera (moths and butterflies). obvious characters are provided by the foreleg, Although a number of lineages within the family which is reduced in adults of most male Lycaeni- are well circumscribed and have been recognized dae plus Riodinidae, and in male and female since the 1800s, the taxonomic rank which such Nymphalidae (only in male Libytheinae). The male lineages should be accorded and how they should foreleg in all three families lacks tarsal claws and be subdivided remains contentious. A number of has the original five tarsal segments (tarsomeres) currently recognized subfamilies, and even some reduced in number through fusion, with the latter tribes, have been considered distinct families by feature also occurring in some female Nymphali- some authors. However, continuing morphological dae. In male Riodinidae, and both sexes of most and especially molecular research now provides Nymphalidae, only four legs are used for walking, real hope of a stable higher classification in the and in male Nymphalidae the forelegs are clothed future. Ten subfamilies are currently recognized, in hair-like scales, inspiring the common familial including: name “brush-footed butterflies.” Order: Lepidoptera All nymphalid subfamilies, except for Superfamily: Papilionoidea ­Libytheinae, are further grouped by the loss of use Family: Nymphalidae of the foreleg in the female. Relationships between Subfamily: Libytheinae other nymphalid subfamilies remain obscure, Subfamily: Calinaginae although certain relationships are often found and Subfamily: Morphinae seem plausible, such as Morphinae plus Satyrinae. Subfamily: Satyrinae While most subfamilies are probably natural Subfamily: Charaxinae (monophyletic) groups, the Nymphalinae, Biblidinae, 584 B Brush-Footed Butterflies (Lepidoptera: Nymphalidae) and Satyrinae have no convincing autapomorphies to giant Caligo (Morphinae), the size of dinner- (uniquely derived characteristics). They will plates. The wings may be rounded, elongate (e.g., almost certainly be subdivided or merged with Heliconiinae, Ithomiini), scalloped (e.g., Cethosia), other subfamilies as our knowledge of nymphalid or with long hindwing tails (e.g., Marpesia). The phylogeny increases. simplest nymphalid wing patterns consist of a series of dark lines and ocelli (eyespots, a common ­feature) on a pale background, which are variably modified through loss, expansion or fusion into a fantastic Morphology array of patterns. These­patterns range from almost entirely transparent and colorless in ithomiine dan- Adult aines to the extremely complex ­patterns of certain Charaxes species (Charaxinae), to the ­brilliant iri- Nymphalid butterflies (Fig. 68) range from tiny descent blue that makes Morpho butterflies visible melitaeines (Nymphalinae), the size of a fingernail, from low-flying aircraft. Many insights into the

Brush-Footed Butterflies (Lepidoptera: Nymphalidae), Figure 68 Representative nymphalid butterflies. A, Coenophlebia archidona (Charaxinae), Ecuador; B, Mycalesis orseis (Satyrinae), Malaysia; C, Cethosia penthesilea (Heliconiinae), Malaysia; D, Marpesia petreus (Biblidinae), Ecuador; E, Caligo ilioneus (Brassolinae), Ecuador; F, Phystis simois (Nymphalinae), Ecuador; G, Idea lynceus (Danainae),­ Malaysia; H, Charaxes castor (Charaxinae), Kenya; I, Consul fabius (Charaxinae), Ecuador; J, Heliconius numata (Heliconiinae), Ecuador; K, Oleria baizana (Danainae), Ecuador. Brush-Footed Butterflies (Lepidoptera: Nymphalidae) B 585 developmental genetics and ­evolution of lepi- coremata that characterize the Danaini). Espe- dopteran wing patterns have been gained from cially complex androconial systems, such as comparative study of nymphalid wing patterns. those in the Danaini, involve abdominal brushes Wing color pattern signaling functions that are remote from glandular alar areas but include crypsis (e.g., the extraordinary leaf-like make contact with them immediately before Kallima and Coenophlebia; transparent-winged scent dispersal. Secondary­ sexual structures also forest understorey satyrines and ithomiines), are known for females of some taxa, most nota- startle or deflective coloration (e.g., the eyespots bly in some members of the Heliconiinae, which of Caligo and Satyrinae), interspecific recognition ­possess a dorsal abdominal gland and associated (e.g., Nessaea, Catonephele), and both Batesian lateral club-like structures termed stink-clubs or (e.g., certain Nymphalinae and Charaxinae) and clavatia. Müllerian (e.g., Heliconiinae, Danainae) mimetic warning coloration. Color pattern variation includes seasonal polymorphism (e.g., Junonia), Immature Stages local genetic polymorphisms (e.g., Heliconius, Hypolimnas), and often remarkable geographic Nymphalid immature stages are morphologically racial polymorphism (e.g., Danainae, Heliconius). extremely diverse, and although comparative The external morphology is rather uniform, study is in relative infancy compared to adult being responsible, at least in part, for the poorly morphology, immature stage characters may still resolved high-level classification of the family. provide very significant information for the ­Variation in wing venation, thoracic exoskeletal, higher level classification of the family. leg and labial palpal morphology provides the The eggs are typically spherical, ovoid, or foundation for the current subfamilial classification. ­flattened domes, and almost smooth (e.g., Satyri- In certain species the veins and basal wing scler- nae), ribbed (e.g., Danainae), or faceted with ites on either fore or hindwing may be modified to interstitial spines (Limenitidini). Larvae may be form a tympanal organ (e.g., Heliconius, Satyrinae), smooth (e.g., some Danainae), covered with though its function is poorly understood. At the small granulations (e.g., Satyrinae), or decorated subtribal, generic and species level genitalic with fleshy tubercles (e.g., Danainae), dense ­morphology, especially male, has been used exten- spines (e.g., Nymphalinae) that may be modified sively, although there is often no variation between into highly elongate and branched scoli (some closely related species. Biblidinae), or hair tufts (e.g., some Brassolinae). The Nymphalidae exhibit a rich diversity of In later instars of some neotropical Charaxinae secondary sexual structures. Most commonly the third thoracic and first abdominal segments these are modified scales with glandular bases, also may be expanded to form dorsal or dorso- typically confined to the male sex, termed lateral humps. The head capsule may be striped “androconia.” Androconial scales usually form or colored, and may be smooth (e.g., Danainae), patches, fringes, tufts or pockets, and may be or ornamented with chalazae (raised wart-like flattened or elongate, but often are hair-like and processes, frequently bearing setae), that often erectile (e.g., Satyrinae, Danainae). Alar andro- form elaborate dorsal and subdorsal head horns. conia are often associated with wing veins, and The ninth abdominal segment is often bifid, occur commonly in the Satyrinae and Danainae. forming “tails” (e.g., Satyrinae, Charaxinae, Mor- Abdominal androconia may be located on ever- phinae). Larvae may be cryptically colored (most sible glands (e.g., Vila) or contained within a Satyrinae, Limenitidini) or black with bright membranous sheath that can be everted through orange, white or yellow markings that suggest an increase in haemolymph pressure (e.g., the warning coloration. 586 B Brush-Footed Butterflies (Lepidoptera: Nymphalidae) Except for a few satyrines that pupate from 500 to 1,000 m above sea-level, due to ­overlap ­terrestrially, the pupa is suspended by the cremaster of lowland and sub-montane faunas. and never has a girdle. Pupae may be smooth, The variation in dispersal ability within the elongate ovoids (e.g., some Satyrinae and Nymphalidae is perhaps more extreme than in any ­Danainae), or highly ornamented with various other butterfly family. Certain nymphalids are spines, flanges, and elongate projections renowned as great wanderers: the famed Monarch (e.g., some Biblidinae). The pupal color pattern (Danaus plexippus, Danainae) occurs throughout ranges from highly ­cryptic, mottled brown or much of the globe, even on Hawaii, while the green, to bright colors that may be aposematic, ­nymphaline Hypolimnas misippus is almost as and many other species are notable for their widely distributed. However, the vast majority of brilliant ­opalescent or metallic coloration species occur only within a single biogeographic (e.g., Limenitidini, Danainae). region, and a number of species have much more restricted ranges, sometimes down to the level of a single mountain range. Distribution patterns in Diversity, Distribution and neotropical montane satyrines (tribe Pronophilini) Biogeography and the nymphaline genus Hypanartia have been used to examine geographic modes of The family includes approximately 6,000 to 7,000 ­speciation in montane habitats. Ithomiine dan- species and 350–400 genera. The largest subfamily aines and heliconiines have featured promi- is the Satyrinae with some 2,500 species, many of nently in studies of the historical biogeography which remain undescribed. In contrast, the of the Amazon basin. ­Calinaginae contains only a single genus of about eight species and the Libytheinae only two genera with 12 species. Habitats The majority of the subfamilies are cosmo- politan, although the Calinaginae are confined Nymphalid butterflies occur in almost all terrestrial to the Sino-Himalayan region and the Morphinae ecosystems. They are found in deserts, grasslands are entirely tropical. However, at the tribal level (especially Satyrinae), temperate and tropical endemism is much higher, with large tribes ­lowland and montane forests, ranging from ­sea-level ­confined to or overwhelmingly more diverse in to over 5,000 m in high ice-fields of the Himalayas single regions. Notable examples include the and the Andes. They are found in all stages of­habitat ­Brassolini, Morphini and Ithomiini, restricted to succession, from primary forest to arid scrub, with the Neotropics; the Amathusiini, occurring only varying ecological fidelity. in the Oriental region; the Acraeini, with its spec- tacular radiation in the Afrotropical region; and the Danaini, largely confined to the Old World. Ecology Species diversity increases steeply from ­temperate to tropical regions, reaching a peak in Immature Stages the Neotropical region which contains perhaps 40% of the family. Community species richness is All nymphalid larvae are phytophagous, with the also greatest in the Neotropics, in the foothills of vast majority concentrating on about 100 families the eastern Andes, where lowland tropical rainfor- of flowering plants, in addition to a few groups on est may contain over 450 species, about a quarter Cycadaceae (cycads), Selaginellaceae (club-mosses) of the butterfly fauna. Species richness decreases and Neckeraceae (mosses). The Satyrinae and with elevation, though richness peaks may occur Morphinae feed largely on monocotyledons, as do Brush-Footed Butterflies (Lepidoptera: Nymphalidae) B 587 a few Charaxinae, with the remainder almost Adult nymphalids feed on various food sub- exclusively on dicotyledons. strates including flower nectar, pollen, rotting fruit, Eggs may be laid in clusters or singly, varying carrion, and damp sand. Flower nectar and rotting between species, and on or off the foodplant, or, in fruits provide the carbohydrates that power flight, some satyrines, be dropped from the air. Larvae of a while pollen is used by Heliconius butterflies to number of species are gregarious and aposematic, provide nutrients for egg production. Damp sand suggesting unpalatability (e.g., Heliconiinae), while and carrion are thought to provide sodium ions, others adopt a variety of defensive strategies. These important for neuromuscular activity, which are include camouflage through decoration of the early typically in low concentration in larval food plants. instars with frass pellets (stercophory), maintenance These last two sources may also provide amino and extension of the leaf mid-rib with frass to form acids that are used in manufacturing body pro- a perch (common in Biblidinae), and construction teins. To some extent the preferred food source of a mass of frass and leaf material at the base of the may be dependent on habitat, with open-country leaf mid-rib to provide additional camouflage, which species seeking flowers and damp sand, and forest may be elaborated further into an apparent decoy species feeding on rotting fruit and carrion. larva-shaped mass (Limenitidini). Spinose larvae A variety of strategies protect nymphalid may react violently to disturbance, swinging the ­butterflies from predators, particularly birds. Many body and head (e.g., Biblidini), or curl into a defen- species have cryptic underside markings, ­especially sive posture with the spines directed outwards (e.g., in the Satyrinae and Morphinae, while bright Limenitidini), while smooth-bodied satyrine larvae ­dorsal coloration in the same species probably con- may simply drop from the plant into the ground lit- fuses predators. Most Biblidinae and Charaxinae ter. A number of nymphalid larvae hibernate in shel- probably rely on fast flight to evade predators. ters made from cut and sewn leaves, and in some Warningly colored ithomiine danaines and species (e.g., Adelpha), this behavior apparently has ­heliconiines were instrumental in the formulation been co-opted for protection. of mimicry theory, providing some of the most Pupation takes place on or off the foodplant, ­outstanding examples of this phenomenon in the and some satyrines form a weak cocoon on the ­animal kingdom. Unpalatable danaines and ground in which they pupate ­heliconiines are the basis for numerous Müllerian mimicry rings, in which other nymphalids (e.g., Charaxainae, Nymphalinae), as well as other Adults butterflies and moths, participate as probable Batesian (palatable) mimics. Nymphalids exhibit a broad range of behavior. Unpalatable nymphalids obtain protective Unpalatable groups, such as Danainae and chemicals by several means. They may sequester ­Heliconiinae, have a typically slow and even flight, secondary chemicals from larval feeding, such as the while palatable species in the Apaturinae and cardiac glycosides obtained by Danaini from their Charaxinae are some of the fastest and most agile apocynaceous foodplants. Alternatively, ­protective butterflies. They may be found in open areas compounds, such as the cyanogenic glucosides in (e.g., Satyrinae, Nymphalinae), in shady forest H`eliconius, may be synthesized from amino acids understorey (e.g., Satyrinae, Morphinae, Danainae), in the larval or adult food. More ­complex precursors and at various levels within forest subcanopy and also may be stored from the larval stage, or obtained canopy (e.g., Heliconiinae, Biblidinae, Charaxinae). through adult pharmacophagy (literally, “chemical Throughout the day a succession of different groups feeding”). Adult danaines obtain dehydropyrroliz- becomes active, with the fastest-flying­species being idine alkaloids by feeding on Asteraceae flowers active only during the hotter hours of the day. (sometimes Boraginaceae), or dried or withered 588 B Brush-Footed Butterflies (Lepidoptera: Nymphalidae) Boraginaceae plants (sometimes Asteraceae). In species where courtship has been studied in some ithomiine danaines, it is predominantly males detail (Satyrinae, Danainae, Heliconiinae), the impor- which exploit these alkaloid sources, transferring tance of androconially disseminated pheromones the ­compounds to females in the spermatophore in achieving successful courtship has been demon- ­during mating. strated. In the Danainae, sex pheromones like Nymphalids generally seek females for mating ­danaidone (Danaini) are manufactured from by “patrolling” appropriate areas of habitat (e.g., ­pyrrolizidine alkaloids that also confer protection Morpho butterflies may patrol several kilometers from predators. along rivers or roads), or by “perching.” Perching nymphalids wait for passing females in species-­ specific locations, such as a forest light-gap or edge, Economic Importance hilltop, riverside, or prominent patch of vegetation, usually at a characteristic height above ground and With the exception of Brassolis and Caligo at a ­particular time of day. Many satyrines and ­(Brassolinae) which may be pests on coconut palm brassoline morphines are crepuscular, actively and banana plantations, respectively, and certain perching or patrolling only at dusk and dawn. Heliconiinae which attack passion fruit plants, Ithomiine ­danaines perch most actively in the mid- few other nymphalid butterflies cause any serious dle to late afternoon, while fast-flying­forest canopy damage to crops. Nymphalid butterflies, however, species, such as the Charaxinae, are active in the do have a positive economic value. Nymphalid middle of the day. The same perching location may butterflies are an important component of the dead be maintained for years. Perching males are territo- butterfly specimen trade (e.g., Agrias, Charaxes), rial and pugnacious, swiftly engaging in high spi- the trade in specimens for education (e.g., the raling flights with intruding conspecific males, Monarch), and are widely used in butterfly houses with the resident male typically winning the in temperate countries (e.g., Heliconius, Caligo). encounter to return to the perching site. Some Butterfly houses import much livestock from Charaxes butterflies have serrate forewing costal ­butterfly farms in tropical countries, providing an margins, which are reported to be used in male- alternative source of income in rural areas. male interactions. Certain species in the genus Hamadryas (Biblidinae) are notable for loud ­crackling sounds that are emitted by perching Conservation males in flight, by percussion of the forewings. Male ithomiine danaines are remarkable in Because of their aesthetic appeal, butterflies may forming dense aggregations, or leks, of up to be used as flagship taxa for conservation. Attempts 20–30 species, which may last several months. to preserve the spectacular over-wintering ­colonies Pheromones released through the hindwing hair- of the Monarch butterfly in Mexico have raised pencil androconia attract both sexes, including awareness of conservation in that region. Butterfly those of ­non-conspecific but co-mimetic species, diversity and abundance are increasingly being thus ­providing increased protection from predation used at the habitat scale as indicators of distur- and providing a mating place that can be more bance and its effects on biodiversity. Nymphalidae easily located through the concentrated odor. are diverse, one of the easiest groups to identify, Aggregations of similar origin and function also and many respond to baited traps, and are thus a are reported in some danaines (Euploea). principal group in such studies. At the biogeo- Males of certain species of Heliconius patrol graphic scale, the Ithomiini have been proposed as foodplants and mate with females before eclosion an indicator taxon for neotropical lowland forest from the pupa, thus avoiding courtship. In those butterfly diversity, because of their ease of sampling Bubonic Plague B 589 and apparent close correlation with overall butterfly Bubo diversity. Finally, recent shifts in geographic range limits of butterflies, especially nymphalids, have An enlargement of a lymph gland caused by an been used as evidence for global climate change. infection.  Bubonic Plague  Plague: Biology and Epidemiology References

Ackery PR (1988) Hostplants and classification: a review of nymphalid butterflies. Biol J Linn Soc 33:95–203 Bubonic Plague Ackery PR, de Jong R, Vane-Wright RI (1999) The butterflies: Hedayloidea, and Papilionoidea. In: Kristensen NP (ed) Handbook of zoology 4. de Gruyter, Berlin, ­Germany, pp The dominant form of plague (also known as black 263–300 death), caused by the bacterium Yersinia pestis and Brower AVZ (2000) Phylogenetic relationships among the Nymphalidae (Lepidoptera) inferred from partial vectored by several fleas, but especially Xenopsylla sequences of the wingless gene. Proc R Soc (Biol Sci B) spp. It is primarily a disease of rodents, but fleas 267:1201–1211 can spread it to other animals and humans. Bubonic DeVries PJ (1987) The butterflies of Costa Rica and their plague is one form of plague, with the others being ­natural history. Papilionidae, Pieridae, Nymphalidae. Princeton University Press, Princeton, New Jersey. septicemia plague (infection of the blood) and Harvey DJ (1991) Appendix B. Higher classification of the pneumonic plague (infection of the lungs). Bubonic Nymphalidae. In: Nijhout HF (ed) The development plague causes headache, elevated temperatures, and evolution of butterfly wing patterns. Smithsonian chills, tiredness, abdominal pains, and painful ­Institution Press, Washington, DC, pp 255–273 Parsons MJ (1998) The butterflies of Papua New Guinea. Their swellings (buboes) of the lymph nodes. Anyone systematics and biology. Academic Press, London, UK with large, painful, and tender lymph glands and experiencing extreme tiredness and fever should be considered a possible plague victim, especially if Brush Organ they have had potential exposure to animals ­capable of harboring plague. People most likely to Clusters of long setae on the body of certain insects contract bubonic plague are those living in rural (particularly male Lepidoptera and some Neu- environments, and people active in rural environ- roptera). They occur on various parts of the body, ment such as biologists, campers and hunters. but usually on the abdomen. They are associated If untreated, it often is fatal to humans. with exocrine glands, and usually used during Treatment is accomplished by application of ­courtship to disperse sex pheromones. This term is antibiotics, often streptomycin, but early detec- synonymous with “hair pencils.” tion is important. Other important measures to prevent plague are educating the public to avoid Bryopsocidae places where plague may occur, informing the medical community about diagnosis of plague, A family of psocids (order Psocoptera). and treatment using appropriate medicine. An  Bark-Lice, Book-Lice and Psocids early warning sign of potential human infection is die-off of rodents. Although rats have histori- cally been implicated in disease transmission, B.t. plague is also associated with rock and ground squirrels, wood rats, chipmunks, prairie dogs, Abbreviation for the bacterium Bacillus mice and voles. To prevent plague problems, it thuringiensis. may be useful to use insecticides to kill fleas 590 B Buccal Cavity ­during epidemics (e.g., treatment of prairie dog the parental nest of one or more reproductive forms burrows), to apply flea control treatments to pets accompanied by workers. Thus, the parental nest regularly, to avoid handling sick animals, and to remains functional and new ones are founded. use insect repellents.  Plague: Biology and Epidemiology  Fleas (Siphonaptera) Buffalo Gnats  History and Insects Members of the family Simulidae (order Diptera).  Flies Buccal Cavity Buffalograss Chinch Bug, Blissus The entry way to the insect mouth, surrounded by occiduus Barber (Hemiptera: the mouthparts. The oral cavity (Fig. 69). Blissidae)  Alimentary System  Alimentary Canal This insect has become a pest of buffalograss in  Digestion some areas.  Turfgrass Insects and Their Management  Turfgrass Insects of The United States: Biology Bucculatricidae and Management

A family of moths (order Lepidoptera). They are commonly known as ribbed-cocoon maker moths. Buffer Zone  Ribbed-Cocoon Maker Moths  Butterflies This term has different meanings depending on  Moths the context. From the perspective of insect ­control, a buffer zone may be established around a treated field by treating surrounding land and Budding vegetation. This reduces the possibility that an insect can arrive successfully in a susceptible field Among social insects, the same as colony fission: because nearby insects are eliminated not only in multiplication of colonies by the departure from the field, but from surrounding areas. This is most

foregut midgut hindgut gastric esophagus crop ventriculus pylorus ileum rectum caecum pharynx

buccal anus cavity proventriculus mouth Malpighian tubule

Buccal Cavity, Figure 69 Generalized insect alimentary system (adapted from Chapman, The insects: structure and function). Bugs (Hemiptera) B 591 important for dispersive species, and particularly by Louis XV, king of France, bestowing on him the for ­disease vectors. From a regulatory perspec- title of “Comte de Buffon.” He died in 1788, leaving tive, a buffer zone is an area in which a specific his wife Marie and one son. pest of concern does not occur, or occurs at a very low level and is controlled, and also encloses, or is adjacent to, an infested area. In both cases, References ­however, the purpose of the buffer zone is to reduce or eliminate spread of a pest. Anon. 1999 Georges-Louis Le Clerc, Comte de Buffon.  Risk Analysis (Assessment) ­Thomson Gale: World of scientific discovery, 2nd ed.  Farmington Hills, MI, USA Regulatory Entomology Tuxen SL (1973) Entomology systematizes and describes:  Invasive Species 1700–1815. In Smith RF, Mittler, TE Smith CN (ed) History of Entomology. Annual Reviews Inc., Palo Alto, California, pp 95–117 Buffon, Georges Louis Leclerc (Comte De) Bugs (Hemiptera) Georges-Louis LeClerc was born in Montbard, France, on September 7, 1707. He is believed to julieta brambila, greg s. hodges have been educated in the Jesuit college of Dijon Florida Department of Agriculture and Consumer and later received a diploma in law from the Services Division of Plant Industry, Gainesville, ­Université de Dijon. His early scientific studies FL, USA were in mathematics and physics, and he ­performed experiments on the tensile strength of wood. He Hemiptera are the largest order of insects with entered the Academie Royale des ­Sciences of Paris incomplete metamorphosis. This order includes in 1734. Six years later he was appointed director pond skaters, squash bugs, big-eyed bugs, stink of the royal garden, which later was called the bugs, cicadas, leafhoppers, planthoppers, tree- ­Jardin des Plantes and was the French center of hoppers, froghoppers, psyllids, aphids, scales, study not only of ­botany, but also of zoology, mealybugs, whiteflies, and others (Figs. 70 chemistry, and mineralogy. Perhaps he would have and 71). Although less well known than beetles studied insects if his ­eyesight had been adequate. or butterflies, they are a diverse group of insects, Although he did not do so, he had profound ubiquitous, ­interesting, or even spectacular, and ­influence on entomology by his founding a huge in some cases agriculturally and medically work (1749–1804) ­“Histoire naturelle, générale important. Approximately 82,000 ­species have et particulière” in 44 volumes. There were later been described worldwide, comprising about supplements [see for example, Audinet-Serville 8–10 percent of all known insect species, with above]. The work set out to ­contradict Linné, an estimated 105,000 species not yet described. because Georges-Louis did not believe in the They range from minute, wingless scales to fish- ­classification into genera, ­families, orders and eating giant water bugs, which may reach a length classes that Linné had proposed. The work was of 11 cm. These fascinating insects occur in very ­influential especially because so many spe- nearly every type of habitat, including several cialists (including entomologists) became involved species that live on the surface of the ocean in its ­writing, and because of its completeness (for hundreds of miles from land and others that can its time). Furthermore, it was written in French, be found occasionally drifting in the wind. The rather than Latin, breaking the precedent of so majority are plant-feeders, but many ­species are many earlier books. He was made a peer of France predatory on other insects, while others feed on 592 B Bugs (Hemiptera)

Bugs (Hemiptera), Figure 70 (Continued) Bugs (Hemiptera) B 593 the blood of vertebrates and are of great medi- These suborders are Sternorrhyncha, Fulgoromorpha, cal importance. Cicadomorpha, Coleorhyncha, and Heteroptera. In general, hemipterans have simple or incom- These names refer to monophyletic groups and will plete metamorphosis, in which the young, called provide stability to the nomenclature within nymphs, are similar to adults in shape. The wings Hemiptera. Some classification schemes present Het- develop externally as budlike outgrowths which eroptera and Coleorhyncha together as Prosorrhyn- increase in size at each molt and become ­functional cha, another apparently monophyletic group. The old after the last molt. term Homoptera does not refer to a ­monophyletic The mouthparts of Hemiptera are group and has essentially been abandoned. Another ­elongate, forming a slender and usually seg- classification has four ­suborders, Sternorrhyncha, mented beak that is used for piercing the host, Auchenorrhyncha, Coleorhyncha, and Heteroptera; either plant or animal, and sucking liquids again, the term Auchenorrhyncha refers to a non- after injecting enzymes that enable extraoral monophyletic taxon and apparently is being aban- digestion. In many Hemiptera, the basal por- doned. The arrangement of the various groups tion of the front wing is thickened to form a (suborders, superfamilies, and families) in the order wing cover and the apical portion is thin and Hemiptera has been debated for many years. The usually transparent while the hind wings are present ­classification should not be regarded as fixed. entirely membranous. The front wing, or hem- Order: Hemiptera elytron (from the Greek words hemi, meaning Suborder: Sternorrhyncha half, and pteron, meaning wing), gives the Suborder: Fulgoromorpha order its name. The name Hemiptera was Suborder: Cicadomorpha coined by ­Linnaeus in 1758. Suborder: Coleorhyncha Suborder: Heteroptera Classification Suborder Sternorrhyncha The earliest book to deal exclusively with the Hemiptera was written in 1803 by J. C. Fabricius, a Sternorrhynchans are common insects found in a student of C. Linnaeus. He renamed the group Rhyn- wide variety of ecosystems throughout the world. gota, later changed to Rhynchota, a name that is being All members of the Sternorrhyncha feed on phloem used today. The term Rhynchota (from the Greek, or xylem from host plants and many are considered rhynchos, for beak) refers to the morphology of the plant pests. The group name “Sternorrhyncha” mouth parts, an elongate structure known as probos- (Greek, sternon, chest; rhynchos, nose or snout) is cis or rostrum. This name should eventually replace derived from the location of the mouthparts occur- Hemiptera because the rostrum is characteristic to all ring between the bases of the front legs. In previous groups in this order. Up-to-date classifications recog- classification schemes, both the Auchenorrhyncha nize five suborders within Hemiptera instead of the and Sternorrhyncha have been recognized as sub- familiar two ­suborders, Homoptera and Heteroptera. orders of the Homoptera. However, the legitimacy

Bugs (Hemiptera), Figure 70 Representative bugs (Hemiptera): top left, a leaffootted bug, Acanthocephala femorata (Coreidae); top right, a broad-headed bug, Alydus pilosulus (Alydidae); second row left, a largid bug, Largus succinctus (Largidae); second row right, a seed bug, Dieuches armatipes (Lygaeidae); third row left, a plant bug, Creontiades rubrinerus (Miridae); third row right, Jadera bug, Jadera haematoloma (­Rhopalidae); bottom left, avocado lace bug, Pseudacysta persa (Tingidae); southern green stink bug, Nezara viridula (Pentatomidae) (all photos by Lyle Buss). 594 B Bugs (Hemiptera)

Bugs (Hemiptera), Figure 71 (Continued) Bugs (Hemiptera) B 595 of the order Homoptera has been and is the topic of Lecanodiaspididae-false pit scales many debates. There is taxonomic evidence demon- Margarodidae-margarodid scales strating that the “Homoptera” grouping is paraphyl- Micrococcidae etic (derived from a single ancestor but not Ortheziidae-ensign scales containing all descendants). Many taxonomists Phenacoleachiidae agree that this group should be recognized as part Phoenicococcidae-palm scales of the Hemiptera but debates occur when discuss- Pseudococcidae-mealy bugs ing placement of the Homopteran groups as subor- Putoidae-giant mealy bugs ders within the Hemiptera. For the purpose of this Stictococcidae-false soft scales discussion, we will recognize the Sternorrhyncha Superfamily: Psylloidea as a suborder of the Hemiptera. The suborder Calophyllidae Sternorrhyncha contains four major super­ Carsidaridae families: Aleyrodoidea (whiteflies); Aphidoidea Homotomidae (aphids); Coccoidea (scale insects); and Psylloidea Phacopteronidae (jumping plant lice). The classification system is: Psyllidae Order: Hemiptera Triozidae Suborder: Sternorrhyncha One of the most common characters associated Superfamily: Aleyrodoidea with the Hemiptera are the modifications seen in Aleyrodidae-whiteflies the mouthparts that appear to many as being a Superfamily: Aphidoidea “beak.” The mandibles, maxillae, labium and Adelgidae-adelgids labrum are present, but are modified into a ros- Aphidiidae-aphids trum where the mandibles and maxillae are modi- Phylloxeridae fied into needle-like or thread-like stylets lying Superfamily: Coccoidea within a grooved labium. Hemiptera use their Aclerdidae-flat grass scales mouthparts to feed on plant or animal tissues. The Asterolecaniidae-pit scales sternorrhynchans share the mouthpart modifica- Beesoniidae tions, but differ by using their stylets to probe plant Carayonemiidae tissues intercellularly or intracellularly, and form- Cerococcidae-ornate pit scales ing a protective sheath from secreted saliva around Coccidae-soft scales the mouthparts. Conchaspididae Many of the sternorrhyncans are phloem feed- Dactylopiidae-cochineal scales ers with a diet rich in carbohydrates and deficient Diaspididae-armored scales in amino acids and other nitrogenous materials. To Eriocococcidae-felt scales compensate for this deficiency, sternorrhynchans Halimococcidae have endosymbionts (intracellular bacteria or Kermesidae-gall-like scales fungi) housed in special tissues and contribute to Kerriidae-lac scales the nutrition of the insect host. Because many

Bugs (Hemiptera), Figure 71 Additional representative bugs (Hemiptera): top left, acacia whitefly, Tetraleurodes acaciae (Aleyrodidae); top right Asian woolly hackberry aphid, Shivaphis celti (Aphididae); second row left, oleander aphid, Aphis nereii (Aphididae); second row right, twolined spittlebug, Prosophia bicincta (Cercopidae); third row left, grenade scale, Cerococcus deklei (Cerococcidae); third row right, ananas scale, Melanaspis bromeliae (Diaspididae); bottom left, Asian citrus psyllid, Diaphorina citri (Psyllidae); bottom right, thorn bug, Umbonia crassicornis (Membracidae) (all photos by Lyle Buss). 596 B Bugs (Hemiptera) ­sternorrhynchans feed on phloem, too many car- The life cycles of the aphidoids include both bohydrates are taken in and must be expelled. They asexual (parthenogenic) and sexual reproductive expel excess carbohydrates by excreting a sugary strategies. Life cycles where sexual generations substance called honeydew. Honeydew can con- are present are termed holocyclic and those taminate ­foliage and serves as a good growth where sexual generations are absent are termed medium for sooty molds. Sooty molds can detract anholocyclic. There are six stages to development from the overall appearance of the host plant and for the aphidoids; egg, four nymphal stages and the can interfere with photosynthesis. Honeydew can adult stage. Morphological differences occur between also attract ants that may protect the sternorrhyn- and within families. For example, members of chans from their natural enemies and help in the Eriosoma (Aphidae) can produce cottony wax removal of excess honeydew secretions. to cover their bodies, whereas other members of the Aphidae produce no wax. There are three families (Aphididae, Adelgidae and Phylloxeridae) Aphidoidea (Aphidoids) with roughly 4,500 known species comprising the Aphidoidea. The Aphididae (aphids) comprise Aphids or aphidoids are probably the most the largest family within the Aphidoidea, containing ­universally recognized members of the Sternor- roughly 4,300 species. As in the higher classifica- rhyncha due primarily to their presence on orna- tion of the Sternorrhyncha, there is much debate mental plants and crops. Members of the on numbers of subfamilies and/or tribes within superfamily Aphidoidea are best recognized by the Aphididae. There are two genera and roughly the presence of siphunculi (cornicles) arising 50 species within the Adelgidae. Most adelgids are from the abdomen. Other key characteristics in found on coniferous hosts and readily induce gall recognizing aphidoids include: 2-segmented tarsi formation on their hosts. The Phylloxeridae with the second ­segment bearing two claws and ­contain eight genera and approximately 75 species. the presence of a cauda (equivalent to the lingula Most species primarily occur on oaks (Fagaceae) found on ­whiteflies) on the posterior tip of the and hickories (Juglandaceae). abdomen. Aphidoids are generally soft-bodied (ranging between 1 and 8 mm in length) and vari- ously ­pigmented from yellow to green to brown and occasionally red. They tend to be gregarious, Aleyrodoidea (Whiteflies) and live in colonies or aggregations on their host plants. Both alates (winged) and apterous (with- Aleyrodids or whiteflies are one of the most recog- out wings) individuals may be present in colonies. nized plant pests in the world with various ­diseases Immature stages look like smaller versions of the being transmitted to crops and with the over- adults. They typically travel short distances to (or whelming numbers of adults present in infested on) host plants by walking or by being transported crops. A tell-tale sign indicating whitefly presence by ants. Dispersal over great distances can be is the white cloud that emerges when plant foliage accomplished through flight or by wind currents. is disturbed. Adult whiteflies derive their common Most ­aphidoids feed either on phloem or in the name (aleuro, flour) from the powdery, white wax parenchyma tissue with most being monoecious secretions that cover their bodies. The adults are but a few species being heteroecious. Many aphi- small, with wingspans being 4 mm or less. There doids are pests of crops and some species are are roughly 1,200 described species within the capable of transmitting viruses such as barley yel- single family of the Aleyrodoidea. The family lows, plum pox, and various diseases of cucurbits ­Aleyrodidae is recognized as having two subfamilies: and melons. the Aleurodicinae and the Aleyrodinae. The Bugs (Hemiptera) B 597 Aleyrodidae are unusual with the subfamilies being mites and lacewing larvae) and parasitic wasps defined by both adult and nymphal characters, and that are often specific to the whitefly species that the species are defined solely on the ­characteristics they attack. of the puparium. Members of the Aleurodicinae can be distinguished from the Aleyrodinae by hav- ing larger adults with more complex wing venation, Coccoidea (Scale Insects) and also by the presence of large agglomerate wax pores on the puparium. The coccoids or scale insects comprise the most Whiteflies typically reproduce sexually, with diverse group within the Sternorrhyncha. They unfertilized eggs becoming males. There are six derive their common name from the presence of a stages of development for whiteflies: egg, three thin layer of secreted wax, resin, or other secreted nymphal instars, pupal instar and the adult. Once materials held over or affixed to the body of the mating occurs, whitefly females typically lay their insect. Scale insects occur throughout the world stalked eggs in arcs or circles on the underside of on a wide range of host plants, and many are leaves. Once eggs hatch, first instars emerge and ­considered economically important plant pests in generally settle close to deposition sites. Subse- agricultural crops, urban landscapes, greenhouses quent development occurs on the underside of and forests. Many have been the focus of a variety leaves. Economically important species undergo of biology and ecology studies over the years. The multiple generations in a season, whereas many first example of a successful biological control benign species usually have only one to two gen- program was with the vedalia beetle on cottony erations per season. Adult males are interesting in cushion scale (Icerya purchasi). Scale insects that they perform courtship behaviors prior to ­(Dactylopiidae) have even been used as biological mating (abdominal oscillations that cause acous- control agents on prickly pear cacti (Opuntia sp). tic substrate vibrations). Others such as the pela wax scale (Ceroplastes Many species are considered economically pela), cochineal insects (Dactylopius sp.) and lac important. They feed from the plant vascular tissues insects (Kerriidae) have been used to produce and all feeding stages produce honeydew. Adult ­commercial products. whiteflies cue into plant chemicals and colors Scale insects also have many unique biological (green and yellow). Most host plants are angio- and morphological characteristics. They are a good sperms, with relatively few hosts being herbs, example of gender dimorphism with the adult grasses, ferns or palms. Feeding damage from males resembling small flies, with one pair of true whiteflies can be seen in a myriad of symptoms, wings and a second, but reduced pair. The classifica- including leaf chlorosis, wilting, leaf drop and tion has primarily been based on the morpho­logy presence of honeydew. Some species are associ- of the adult female. The adult females are usually ated with viral disease transmission and the most sedentary and affixed to the host plant. The imma- serious pests are associated with orchards, crops ture stages are often smaller than the adult life stages and greenhouses. Probably the most recognized with the dispersal stage (or crawlers) ranging from significant pest of this group is Bemisia tabaci 300 to 700 µm in length and having a flattened (sweetpotato whitefly). This pest is highly polypha- ovoid body shape. Perhaps one of the most unique gous and is thought to vector more than 70 and fascinating morphological oddities within the ­different viruses (e.g., Gemini virus, melon leaf scale insects can be seen in the ground pearls (Mar- curl virus). The most virulent form of this species garodidae). They have a quiescent stage where an is biotype B or B. argentifolii (silverleaf whitefly). immature developmental stage may form a protec- Generally control of these whiteflies is realized tive covering (cyst) around the body to help in with the use of non-specific predators (predaceous adverse environmental conditions. Scale insects 598 B Bugs (Hemiptera) demonstrate a wide range of reproductive systems Some species such as pink hibiscus mealybug including: hermaphroditism ­(cottony cushion scale, (Pseudococcidae: Maconellicoccus hirsutus) and Icerya purchasi), asexual reproduction (up to seven lobate lac scale (Kerriidae: Paratachardina lobata different types of parthenogenesis) and sexual lobata) have multivoltine (numerous generations reproduction. Eggs may be laid outside the body per year) life cycles. Others, such as European fruit underneath a protective covering such as an ovisac lecanium (Coccidae: Parthenolecanium corni) and (some Coccidae, ­Margarodidae, Ortheziidae and Indian wax scale (Coccidae: Ceroplastes ceriferus) Pseudococcidae) or underneath the testa, or scale generally are univoltine. Proper environmental covering, as seen in many armored scales (Diaspidi- conditions, such as prolonged warm periods and dae). In others cases, eggs are withheld in the body high humidity, can allow some univoltine species and live birth occurs (some armored scales and to have more than one generation per season. members of the Phoenicococcidae). After eggs are laid, and once the crawlers or first Taxonomically, scale insects have always instars emerge, they will begin searching for been divided into two informal groups, the ­suitable feeding sites. They will settle on the natal archaecococcids and the neocococcids. The host plant, or will be dispersed to other hosts via archaecococcids are comprised of the Margar- wind currents. Some crawlers have demonstrated odidae (roughly 400 species), Ortheziidae (ensign behaviors (such as arching their bodies) that aid in scales, 135 ­species), Carayonemidae (four species) their ability to become airborne. Once a suitable and the Phenacoleachiidae (two species). The host is found, crawlers settle (becoming sedentary archaeococcid grouping is not monophyletic and in many cases) and begin the feeding process. members of this group share primitive character- Scale insects feed in the phloem or paren- istics (e.g., retention of abdominal spiracles). The chyma of the host plants. The coccoids demon- neocococcoids comprise the rest of the coccoids strate the complete spectrum of feeding preference (17 families, approximately 7,000 species). This ranging from monophagous to oligophagous to informal grouping is considered monophyletic polyphagous. Primary damage to the host plant based on derived features such as apical setae on is through sap removal. This process can cause the the labium, loss of abdominal spiracles. The three plant to have chlorosis in the foliage, premature largest families of neococcoids are the Diaspididae leaf drop, twig die back and possibly death of (armored scales, 2,400 species), the Pseudococci- the host plant. Many coccoids produce copious dae (mealybugs, 2,000 species) and the Coccidae amounts of honeydew. In turn, the honeydew (soft scales, 1,000 species). Other neococcid families becomes a good growth media for sooty molds include: Aclerdidae (flat grass scales, approxi- that can hinder photosynthesis of the host plant mately 50 species), Asterolecaniidae (pit scales, and detract from the aesthetic value of the host. 200 + species), Beesoniidae (nine species), Con- A key factor in controlling scale insect infes- chaspididae (approximately 30 species), Cerococ- tations is detection. Many scale insects are able to cidae (ornate pit scales, 70 species), Dactylopiidae slip by inspections by being present in very small (cochineal insects, nine species), Eriococcidae (felt population numbers. Growers and homeowners scales, 550 species), Halimococcidae (20 species), should attempt to thoroughly inspect their plants ­Kermesidae (gall-like scales, 90 species), Kerriidae to insure that populations of scales do not become (lac insects, 100 species), Lecanodiaspididae established. Control of scale insect infestations is (false pit scales, 80 species), Micrococcidae (eight realized through a variety of methods: (i) cultural species), Phoenicococcidae (one species) and the (ii) natural enemies (iii) oils (iv) pesticides. Cul- Stictococcidae (16 species). tural control methods, such as pruning and There are species of scale insects that repre- destruction of infested material, can be effective sent every major cyclic system seen in insects. when populations are at low levels. In some cases, Bugs (Hemiptera) B 599 natural enemies keep populations of scale insects pyricola (transmits fireblight in pears),Bactericera at low levels. The best scale insect predators are the cockerelli (vectors psyllid yellows in several garden ladybird beetles (Coccinellidae: Chilocorus, Cryp- crops), and ­Diaphorina citri (vectors citrus tolaemus and Rodolia). When crawlers are present, greening disease in citrus). lacewing larvae can be good predators, but should There is much discussion concerning the not be relied upon due to their polyphagous ­taxonomy and numbers of families within the nature. Most parasitoids that attack scale insects Psylloidea. Here we recognize six families: Calo- are from the Aphelinidae (e.g., Aphytis sp.) and phyidae, Carsidaridae, Homotomidae, Phacopter- the Encyrtidae (e.g., Metaphycus sp.). Use of horti- onidae, Psyllidae, and the Triozidae. The majority cultural oils can be a good support treatment when of the families have very select host ranges: natural enemies are present. Horticultural oils are ­Calophyidae feed primarily on plants from the not as toxic as other pesticides to the natural Anacardiaceae; Carsidaridae are restricted to ­enemies. Proper application of oils in conjunction members of the Bombaceae, Malvaceae, and with natural enemies can suppress and keep scale ­Sterculiaceae; Homotomidae are restricted to the populations at levels below the economic thresh- Moraceae; Phacopteronidae feed on plants in old. Lastly, chemical control is relied on in many the Meliaceae; Psyllidae feed on a wide range of situations with severe infestations to help reduce hosts. the scale insect populations. Unlike many of the other sternorrhynchans, psylloids reproduce solely through sexual means. They have seven life stages: egg, five nymphal instars and the adult. Many species occurring in Psylloidea (Jumping Plant Lice) tropical to warm temperate regions tend to have multivoltine life cycles. Those species occurring in The Psylloidea or jumping plant lice are found in northern climates tend to have univoltine or occa- most regions of the world, with the majority of sionally bivoltine life cycles. Psylloids tend to species present in tropical regions. Psylloids are migrate or disperse over short distances by jump- the most attractive of the sternorrhynchans, with ing or flying and much like whiteflies or aphids, many possessing brilliant color patterns. Psylloid can travel great distances on air currents. adults are very small, ranging from less than 1–8 mm Many species are specialists as nymphs, often in length, and often resemble miniature cicadas. feeding on a particular plant structure on a ­specific The immature stages closely resemble the adult life host. Feeding preference exhibited by the adults stage but lack wings. Immatures from the Psyllidae differs from that of the immature stages. They are can occur on the surface of the host plant, within a typically polyphagous but host plants are generally gall or within “lerps.” Lerps are protective cover- defined as those that the immature stages can ings formed from exudates from the immatures develop. Like other sternorrhynchans, psylloids (liquid feces and wax filaments). produce honeydew that attracts ants that benefit The common name (jumping plant lice) the psylloids by potentially driving away their refers to the ability of the adults to jump ­natural enemies. ­backwards when disturbed. All members of this superfamily feed primarily on the phloem of woody-dicotylendonous plants. Many members Suborder Fulgoromorpha of the Psylloidea are plant pests. Damage from psylloids can be in the form of galls, stunting or Fulgoromorphans, or planthoppers, are common poor plant growth. In some instances, psylloids in nearly all habitats and some are either bizarre or can transmit diseases. Examples include Cacopsylla spectacular in form. They occur throughout the 600 B Bugs (Hemiptera) world, although most are from the tropical and the family Fulgoridae, all from subtropical and subtropical regions. All species are plant sap tropical regions. Both adults and nymphs feed ­feeders. Some feed on trees or shrubs, others ­prefer above ground on their host plants, which are usu- lower-growing grasses or sedges. Some feed under- ally are dicots. These insects range from 4 mm to ground on plant roots; still others feed on ferns or 10 cm in length with wingspans of up to 15 cm. In on fungi growing under bark or on moist logs. some species the hind wings have large colorful Some planthopper species are of agricultural eyespots, designed to startle potential predators. importance because of the plant pathogens they The most distinctive feature in many fulgorids is transmit when feeding, or because of the sooty the bizarre shape of their head, which can be long mildew promoted by their sugary exudates and toothed, slender, or bulbous. In Fulgora, the ­(honeydew). One species has caused, if indirectly, lantern bug, the head resembles a crocodile’s head, cases of poisoning in humans. Analysis of molecu- complete with false eyes, nostrils and teeth. Despite lar data and new interpretations of morphological its name, the head of Fulgora does not glow. Most characters of both adults and nymphs strongly likely, though, they mimic lizards, positioning support the monophyly of the Fulgoromorpha. themselves vertically with the head uppermost, About 12,000 planthopper species have been just as lizards do. Another family of planthoppers described and arranged into 20 families, the larg- in which both adults and nymphs feed above the est and most economically important being Del- ground is Dictyopharidae, the sister group of the phacidae. Since only a few families have been Fulgoridae. The 600 described species ranging in shown to be monophyletic, this classification will length from 3 to 33 mm are found throughout the surely be modified in the future. world. Most dictyopharids are green or brown and Order: Hemiptera have a long head projection referred to as a cephalic Superfamily: Fulgoroidea-planthoppers horn. A few species have modified front legs that are Fulgoridae broad and flat. Most species are monophagous and Dictyopharidae feed above ground on their hosts, primarily dicots. Flatidae Flatids are the next most spectacular hoppers, Hypochthonellidae especially those in the tropics. They range from 4 to Issidae 32 mm in length and their front wings, which are Acanaloniidae broad, blunt-ended and opaque, and have many Caliscelidae cross veins in the costal area, may be pink, red, yel- Nogodinidae low, green, white, brown, black, and plain, stripped, Tropiduchidae or spotted. Sexual dimorphism is not uncommon. Delphacidae Mostly pantropical but occurring world wide, Flati- Cixiidae dae is a large family of more than 1,000 species Derbidae related most closely to the Tropiduchid group of Achilixiidae families, Issidae, Nogodinidae, and Tropiduchidae. Achilidae Most species of flatids feed on woody dicots, above Kinnaridae ground, and many are polyphagous. Nymphs and Meenoplidae adults of many species feed together in large groups, Tettigometridae the nymphs protecting themselves by producing Lophopidae long, curly wax threads on the surfaces of their Eurybrachidae bodies. Metcalfa pruinosa (Say), a polyphagous Ricaniidae species from the United States, was introduced into The most spectacular planthoppers are the fulgo- Italy in the late 1970s and is causing damage espe- rids. Seven hundred and fifty species are known in cially to grapes in southern Europe. Wax from the Bugs (Hemiptera) B 601 nymphs covers the fruit, and their honeydew pro- date palms in the Middle East because it can result motes the growth of sooty mold. Hypochthonelli- in the death of the plant. dae, a family composed of only two species in Delphacidae is the largest family in Fulgoro- Africa, is presently considered as a subgroup within morpha, with nearly 2,000 species worldwide. Flatidae. Hypochthonella caeca China & Fennah is Delphacids are small (2–10 mm in length), usually the only known true subterranean fulgoroid, and brown or greenish planthoppers. They are charac- has reduced wings and eyes and lacks ocelli. Both terized by a hind tibia with triangular cross-­section adults and immatures are found in the soil, where coupled with an articulated spur at its distal end. they feed on roots of plants. Delphacids are important pest species because The majority of the 1,000 described species in they feed on monocots that include rice, wheat, the family Issidae feed as adults and nymphs on corn, and sugarcane. Many of them cause more trees and grasses, above-ground. They are widely damage by vectoring viral diseases than by direct distributed, although the majority are found in feeding. tropical regions. More issids are monophagous The most economically important delphacid is than polyphagous. Most adults, which are between the brown planthopper Nilaparvata lugens (Stål). 2 and 8 mm in length, are dark-colored with Since the early 1970s, this species has been the most opaque wings. Some appear beetle-like due to their serious pest of rice in South East Asia, the Pacific, tough, short front wings. Some even resemble New Guinea, India and Sri Lanka. It can travel long weevils because of a long snout-like structure and distances, assisted by strong wings, reaching Korea expanded forelegs. Acanaloniidae (about 80 species), and Japan from China. It transmits a virus (“grassy a group presently considered within ­Isiidae, are stunt disease”) to rice, a crop that feeds at least 60% hoppers that resemble flatids, except that they do of the world. not have the many cross veins in the costal area of The nymphs of cixiids, derbids, achilixiids, the front wings characteristic of Flatidae. They feed achilids, kinnarids, and meenoplids are thought to on grasses and herbaceous plants. have their nymphal stages cryptic or associated Another group of hoppers that resemble ­weevils with soil, or in spaces under bark or on logs, rather is Caliscelidae. They previously were placed within than being in the open on the plants as are the Issidae, and are a small family found worldwide. adults. With almost 2,000 species, Cixiidae is one Caliscelids are small (1–5 mm long) and brachypter- of the largest families in Fulgoromorpha. Cixiids ous. They are known to feed on grasses, sedges, and are found in all regions of the world. Adults (rang- palms, and some are associated with ants. ing from 3 to 13 mm in length) look superficially Nogodinidae is a primarily tropical family of like minute cicadas, being slightly broad and flat approximately 150 species, 4–17 mm long, that and with clear, membranous wings held at a low feed as adults and nymphs above ground on angle over the body when at rest. The nymphs feed woody dicots; all known species are monopha- on the roots of grasses and herbaceous plants, on gous. It is unknown at present if this group is fungi on rotten wood, or on ferns, while adults monophyletic. feed on a variety of tree and shrub species. Some Tropiduchidae has about 350 species described, nymphs have been found in association with ants. ranging in length from 5 to 13 mm; this family is Nymphs in the genus Oliarus are subterranean. primarily pantropical but occurs worldwide. Tropi- In Hawaii, nymphs of Oliarus live in caves and duchids usually have an oddly shaped head and feed on roots while protecting themselves with a wings of variable color patterns. Both adults and cocoon of wax filaments. As adults, they move nymphs feed above-ground, usually on understory through the caves holding to the rock walls with plants in moist, tropical forests. The Dubas Bug, the help of modified pretarsal claws. Some species Ommatissus lybicus (Bergevin), is the worst pest of are blind, unpigmented, and flightless. 602 B Bugs (Hemiptera) Cixiids are economically important because Kinnaridae, have been found in caves. Eighty they can transmit plant diseases. One species, species have been described, mostly from the ­Myndus crudus Van Duzee, acts as disease vector Ethiopian and Oriental tropical regions. Adult for the phytoplasma that causes Lethal Yellowing, a meenoplids are very small, flattened planthoppers lethal disease of palms, including the coconut palm. that range from 3 to 7 mm in length. Most adults It was first reported (1830s) in the West Indies and feed on monocots, the majority of the species later appeared in the Florida Keys (1950) and in feeding across several families (they are among other areas of the United States. It has now spread the most polyphagous in Fulgoromorpha). to others parts of the world. Other cixiids are Tettigometridae is a small family of less than ­suspected of also transmitting this disease. 100 species, sized 3–11 mm, that occurs in the Derbids (4–mm) are planthoppers with long, Ethiopian and Palearctic regions. The nymphs of narrow, fragile wings, sometimes white or brightly most species live underground in groups feeding colored. More than 800 species of Derbidae exist on plant roots, while adults live on foliage, mostly worldwide, primarily in the tropical and subtropi- dicots. In some species ants attend the nymphs. cal regions. Adults of these bugs have been found Lophopidae includes about 140 described feeding on fungi associated with plant or wood species, 5–15 mm long, nearly all from the Old decay, on flowering plants, on palms and on a few World tropics. Their wings are usually opaque tan deciduous trees. Nymphs are thought to be or brown. Pyrilla spp., which feed on monocots ­obligate fungus feeders. Members in the group that include sugarcane, corn and rice, are serious called moth derbids congregate on one leaf and sit sugarcane pests in India. characteristically with their wings held flat against Eurybrachidae (7–29 mm long) is a tropical the underside of the leaf. family of about 200 species with opaque tan or More than 350 species of Achilidae (recog- brown rectangular wings. The group occurs in nized by the overlapping tips of the front wings) the Australian, Ethiopian and Oriental regions. have been described throughout the world. Adults, Adults and immatures are monophagous and which range from 3 to 13 mm in length, feed on feed above ground; one example is Platybrachys the phloem of trees or shrubs while the nymphs leucostigma Walker from Australia, which feeds are thought to feed on fungi in holes in logs, or on Eucalyptus maculatus. The front wings of under loose bark, or in decaying vegetation. some species are shaped and colored at the apex Achilixiidae is a small tropical family with 24 to look like a head, some complete with false described species ranging from 4 to 8 mm in antennae. length. Achilixiid planthoppers are known from Gengid planthoppers are found only in the Neotropics, Philippines, and Borneo. Some South Africa (two species described), believed include Achilixiidae within Achilidae, but their by some authors to belong within the family placement is uncertain at present. Eurybrachidae. Forty species have been described in the Ricaniids (380 species) range from 4 to 12 ­family Kinnaridae (2–4 mm in length) mostly mm long with their wings, when spread, reaching from the Neotropical and tropical Oriental up to 30 mm in some species. These are moth- regions. Nymphs feed on roots and some are cave like planthoppers found in the warmer parts of adapted; most adults feed from the upper portion the eastern hemisphere. They feed above ground of plants, ­usually dicots. Some species lay their ­primarily on dicots, although some feed on egg masses in the soil or on wood, and cover monocots or ferns, with polyphagy common. them with water repellent waxes. The nymphs of Some species damage ornamental and agricultural Meenoplidae, the sister group of the Kinnaridae, crops. A species that occasionally causes poison- are also associated with soil and some, as in ing in humans is Scolypopa australis Walker, a Bugs (Hemiptera) B 603 ricaniid from Australia, now also found in New Melizoderidae Zealand. This species occasionally feeds on the Cicadellidae-leafhoppers poisonous plant Coriaria arborea and produces Myerslopiidae honeydew that, in time of low nectar, may be ­collected by honey bees. This honey is poisonous to humans. Cicadoidea-Cicadas

Cicadas are large insects, reaching lengths of 10 cm, although some are as small as 1 cm. Approxi- Suborder Cicadomorpha mately 4,000 species are known, if not all described. With a stout body, broad head, large compound The suborder Cicadomorpha has three superfami- eyes, and long, usually transparent wings, they are lies with about 30,000 species described, all of which easily recognized. They are also known for their are terrestrial plant-feeders. They are extraordi- loud singing, which usually takes place during the narily diverse and ubiquitous. The most familiar day or at twilight, males calling to attract the insects in this group are the cicadas ­(Cicadoidea), females. Each species has a characteristic song the largest and loudest insects in Cicadomorpha. produced by an enlarged abdomen that serves as Cercopoidea includes the ­two-striped froghopper, the resonating chamber. Prosapia bicincta (Say), a cercopid native to the Although cicadas occur from the tundra to southeastern United States that damages forage the tropics, they are most diverse and abundant in and turf grasses and some ornamentals. Within the tropical regions. Both adults and nymphs Membracoidea are two important groups, the ­usually feed on xylem from trees and shrubs, and Cicadellidae, which is ­considered the tenth largest are commonly polyphagous. Nymphs are entirely family of insects, as well as one of the most abun- subterranean, possessing digging front legs, dant, and the Membracidae, which includes some ­feeding usually on perennial roots, and emerging of the most fantastically designed insects. Cicado- after several years in the soil to molt into adults. morpha is considered a monophyletic group. It was Some cicadas are able to be active at temperatures previously placed in Auchenorrhyncha together that would induce torpor in other insects because with Fulgoromorpha. The classification of Cicado- they are facultatively endothermic. They can warm morpha is: themselves through shivering of flight and/or Order: Hemiptera tymbal muscles or cool themselves by releasing Suborder: Cicadomorpha-cicadas, spittlebugs, water (i.e., evaporative cooling). Within the family leafhoppers and treehoppers Cicadidae, the most famous might be the gregari- Superfamily: Cicadoidea: cicadas ous “periodical cicada” (genus Magicicada, seven Cicadidae-cicadas species) from the eastern United States. Broods Tettigarctidae: hairy cicadas emerge simultaneously in millions at intervals of Superfamily: Cercopoidea-froghoppers either 13 or 17 years. These cicadas can cause Aphrophoridae ­considerable damage to trees. The damage is done Cercopidae-spittlebugs by the egg-laying females, which cut slits in twigs Clastopteridae to insert their eggs. In Australia, sugarcane can be Machaerotidae tremendously damaged (even shredded) when Superfamily: Membracoidea-treehoppers and thousands of cicadas oviposit in a single crop. leafhoppers Two species of importance are the Brown Buzzer Membracidae-treehoppers (Cicadetta crucifera [Ashton]), also known as the Aetalionidae Brown Sugarcane Cicada, and the Grass Fairy 604 B Bugs (Hemiptera) (Parnkalla muelleri [Distant]), also known as the clover, and alfalfa. Some species are capable of Yellow ­Sugarcane Cicada, both of which become transmitting pathogens. Most froghoppers live abundant in sugarcane fields in certain seasons. in grasslands with nymphs feeding on roots. The former lives in open grasslands, and edges of Froghoppers, as a group, are considered the woodland and mangroves, while the latter species most important pest insects of sugar cane in prefers areas of open grassland or woodland/ the Neotropics. scrub habitats. Aphrophoridae is a large family of spittlebugs Only two species are included in the family distributed worldwide. Not all species produce Tettigarctidae, both in the genus Tettigarcta. One froth or foam as immatures. Some species feed on species is found only in southeastern Australia legumes and several are of economic importance. and the second only in Tasmania. Many characters In Australia, the most common and widespread distinguish this family from Cicadidae, including species is Philagra parva (Donovan), which has a a large pronotum, eyes close together, simple curved horn on the head. sound-producing organs (timbals) in both sexes Nymphs of Clastopteridae also hide within rather than only in males; and no true auditory spittle masses. Some clastopterids are of economic tympana. Rather than communicating with audi- importance. For example, the pecan spittlebug ble songs, these cicadas communicate using vibra- (Clastoptera achatina Germar, 2 mm long) heavily tions through substrate. They are called hairy infests and feeds on terminal shoots of pecan trees, cicadas because the underside of their body is reducing the nut crop. densely covered with brown or grey hairs. Also Cercopidae are found worldwide and are unlike Cicadidae, hairy cicadas remain hidden richly represented in the tropics, where they during daylight hours. are the most brightly colored. Nymphs live within spittle masses, explaining their common name “spittlebugs.” They feed on shrubs, trees, and ­herbaceous plants, but some prefer grasses. Cercopoidea-Froghoppers The largest cercopids (including Megastethodon ­urvillei [Le Pelletier and Serville]) are found in Cercopoidea is the least studied lineage of Australia and New Guinea, and may reach up to ­Cicadomorpha, with about 3,000 species known. 20 mm. Spittlebugs are considered the most They are found almost worldwide, with highest important pest insects of Neotropical sugar diversity in the tropics. Their anterior wings are cane. A grassland spittlebug, Prosapia simulans coriaceous and many, especially in the tropics, (Walker), is a threat to sugarcane and forage are of contrasting colors of red with black or grasses and also feeds on many of the major ­yellow. Their hind legs are long and adapted for ­forage grasses, including corn, and also on some leaping, hence their common name “froghoppers.” non-graminoid hosts. It is known from the The hind tibiae are long and have one or two ­lowland tropics from Mexico to Panama but has stout spines and a single or double row of spines now been found in Venezuela and Colombia. It at the apex. Some species are gregarious. Nymphs threatens sugarcane crops in southern United are mostly stationary and hidden, ­protected from States, which already is under attack from the desiccation and parasites by a fluid secreted from native froghopper, Prosapia bicincta (Say). epidermal glands in the abdomen, which is ­Cercopids are also important because they are ­converted into foam (“spittle”) with expelled air. capable of vectoring Xylella fastidiosa, a bacte- Most species feed on sap from herbaceous plants, rium that affects many economic plants in the but some feed on trees. Some are of economic world, including citrus, maple, coffee, grape, importance, causing damage to pecans, cotton, and others. Bugs (Hemiptera) B 605 Machaerotidae is a small family restricted to exposed to extreme heat and when predators tend the Oriental region, tropical Africa, and ­Australia. to be inactive. For defense, nymphs feed among The nymphs do not live within spittle masses, but adults. The nymphs of some species are attended live instead within calcareous tubes attached to by ants. Parental care is common (egg guarding, the host plant, immersed in their liquid ­excretions. principally) in Membracidae. A new classification has recently been proposed Aetalionidae also feed on trees, are gregari- for Cercopoidea, with three families, Cercopidae, ous, are commonly tended by ants, or by Meliponi- ­Clastopteridae (including machaerotid froghop- nae bees, and display parental care. Some are as pers), and Epipygidae, a new family from the long as 28 mm; the beak extends to the hind coxae. Neotropics. In this classification the family Their pronotum and sometimes their head have ­Aphrophoridae is not considered monophyletic cuticular expansions, but some resemble cicadel- and its genera are divided among the other lidae or cercopidae. This family of 44 described families. species is Neotropical, except for two species found in the south of the Himalayas. The genusAetalion , which resembles a large cercopid, occurs in Flor- Membracoidea-Treehoppers and ida, Arizona and California. Leafhoppers Melizoderidae is a very small family of eight species known only from Chile and Argentina. Membracoidea is a monophyletic group com- The pronotum has a unique, somewhat conical prised of approximately 25,000 described species shape. Nothing is known of their biology. This in five or more families. It is the most diverse of family is considered a distinct lineage between the Cicadomorpha superfamilies. Membracidae Cicadellidae and Membracidae. (up to 12 mm long and with 3,200 species) are Cicadellidae, with more than 20,000 described extremely diverse in tropical America, where they species worldwide, is the largest family in Hemip- occur in rainforests, savannas, and deserts. Adults tera and the tenth largest family of insects. Since have cuticular expansions on the pronotum that most species are likely undescribed, an estimate of often extend over the abdomen. The pronotal the family size is not possible at present. The spe- modifications range in shape from simple (spines, cies richness is highest in the tropics. Cicadellids horns) to fantastic, which sometimes differ in are 3–22 mm long, with narrow and often colorful males and females of the same species. Membrac- wings, with posterior tibia prismatic in cross-sec- ids feed primarily on trees and shrubs. Many spe- tion and with spines. For defense they rely mostly cies are gregarious, with young and adults feeding on agility, for they jump and fly. Some leafhoppers together. Much has been speculated on the func- are Batesian mimics of bees or wasps; that is, by tion of the pronotal expansions. Some shapes shape, coloration, and even behavior they mimic might provide protection in the form of mimicry bees or wasps. For example, leafhoppers in the of their host, looking like thorns (as in Umbonia), genus Lissocarta and Propetes imitate paper wasps seeds, or bark; others mimic ants or wasps, as in (Vespidae), and the genus Teletusa imitates bees Cyphonia. Some have aposematic (warning) col- in the family Megachilidae. A trait unique to oration. Others might be protected from verte- Cicadellidae among all insects is the production brate predators by their spiny projections; all those of brochosomes, small protein-lipid particles of with pronotal expansions might survive mutila- intricate structure produced by cells in the tion from predators. However, the latest theory is ­Malpighian tubules. They actively spread this that it has a thermoregulatory function, providing material over their body, wings, and legs and large surfaces for water evaporation. Treehoppers also on their eggs. There is some evidence that tend to be active during the day, when they are this material serves to form a protective layer 606 B Bugs (Hemiptera) that repels water or honeydew and prevents a simple color pattern. Most species lack hind fungal infections. wings and feed on the roots or root-necks of Cicadellid leafhoppers are of major agro- plants, hiding in the soil, although a few feed on nomic importance because they can injure plants shrubs and trees. in several ways, including the transmission of pathogens. Scaphoideus titanus Ball (5–6 mm long) is an example of a cicadellid that can cause Suborder Coleorhyncha-Moss Bugs diseases. It is able to transmit phytoplasmas ­(unicellular organisms without a rigid wall) to The suborder Coleorhyncha contains the single grapevines if they fed previously on infected family Peloridiidae, considered the sister group of plants whether as young or as adult. This North the Heteroptera. Their distribution is limited to American species was accidentally introduced to the Southern Hemisphere. Twenty-five species France in 1960 and has spread throughout have been described from eastern Australia, ­southern and eastern Europe, reaching Spain and ­Tasmania, Lord Howe Island, New Zealand, New Portugal in 2000. The phytoplasma disease called Caledonia, Chile and Patagonia in Argentina; they Golden Flavescence is of considerable economic may also occur in New Guinea. Peloridiids importance, and has been already found in Spain, ­resemble planthoppers but have hemelytron-like France and Italy. forewings. Adult peloridiids are small (between 2 Pierce’s disease is a lethal grapevine disease and 4 mm long), flattened, oval, greenish or caused by Xylella fastidiosa, one of the most brownish. Among their unique characteristics are ­significant disease-causing pathogens in the the broad head and the pronotum with lateral Americas. This bacterium causes water stress areolate expansions. They are primarily phytopha- due to vascular occlusions by aggregates of the gous on mosses, thus known as moss bugs, and ­bacteria. Different strains of this species attack usually live in moist habitats such as damp leaf different hosts, which include citrus, coffee, elm, ­litter on forest floors with mosses, liverworts, and oak, oleander, maple, sycamore, almond, alfalfa, decaying trunks but a few species have been found peach, grape, and ­others. The primary vectors in caves. for Pierce’s disease are cicadellines, or sharp- shooters. Homalodisca ­coagulata (Say) (the glassy-winged sharpshooter) is an important Suborder Heteroptera vector of Xylella fastidiosa in the southeastern United States. Recently, it has become established Heteroptera are the only insects correctly called “true in California, where it is threatening the large bugs.” This is the most abundant and biologically wine industry because of increased spread of diverse group of insects with incomplete metamor- Pierce’s disease. phosis. Species of Heteroptera are characterized pri- Myerslopiidae are a small family found only marily by having the first pair of their wings divided in New Zealand and South America. These into two areas (hence the name “Heteroptera,” differ- ­leafhoppers inhabit forests, and both adults and ent wings), one part thickened and opaque and the nymphs living in leaf litter and soil with high other part membranous and usually transparent. organic content. This family has less than 20 Most true bugs are diurnal plant-feeders with well species. developed eyes and wings, although many variations A group of archaic cicadellids, with 120 spe- and exceptions exist. Some species are of agricultural, cies, is treated by some as a family named veterinary, or medical importance. Heteroptera are a ­Ulopidae. They are 2.5–12 mm long and have relatively small monophyletic group of approxi- stiff front wings that are either plain or that have mately 37,000 described species with at least 25,000 Bugs (Hemiptera) B 607 yet to be described. Although they are arranged Microphysidae among 88 families, the classification will undergo Joppeicidae changes in the future. Presently the suborder Het- Thaumastocoridae-palm bugs eroptera is divided into seven infraorders, as follows: Miridae-plant bugs or leaf bugsTingidae-lace Infraorder: Enicocephalomorpha: unique headed- bugs bugs Medocostidae Aenictopecheidae Nabidae-damsel bugs Enicocephalidae-unique headed-bugs Lasiochilidae Infraorder: Dipsocoromorpha Plokiophilidae-web lovers Ceratocombidae Lyctocoridae Dipsocoridae-jumping ground bugs Anthocoridae-minute pirate bugs or flower Hypsypterygidae bugs Schizopteridae Cimicidae-bed bugs Stemmocryptidae Polyctenidae: bat bugs Infraorder: Gerromorpha: semiaquatic bugs Infraorder: Pentatomorpha Mesoveliidae-water treaders Superfamily: Aradoidea Hebridae-velvet water bugs Aradidae-bark bugs Paraphrynoveliidae Termitaphididae Macroveliidae Superfamily: Coreoidea Hydrometridae-marsh treaders Alydidae-broad-headed bugs Hermatobatidae-coral treaders Coreidae-leaf-footed bugs Veliidae-small water striders Hyocephalidae Gerridae-water striders and pond skaters Rhopalidae-scentless plant bugs Infraorder: Nepomorpha: water bugs Stenocephalidae Belostomatide-giant water bugs Superfamily: Idiostoloidea Nepidae-water scorpions Idiostolidae Gelastocoridae-toad bugs Henicocoridae Ochteridae-velvety shore bugs Superfamily: Lygaeoidea Corixidae-water boatmen Artheneidae Potamocoridae Berytidae-stilt bugs Naucoridae-creeping water bugs Blissidae-chinch bugs Aphelocheiridae Colobathristidae Notonectidae-back swimmers Cryptorhamphidae Pleidae-pygmy back swimmers Cymidae Helotrephidae Geocoridae-big-eyed bugs Infraorder: Leptopodomorpha Heterogastridae Aepophilidae-marine bugs Lygaeidae Saldidae-shore bugs Malcidae Omaniidae-intertidal dwarf bugs Ninidae Leptopodidae-spiny shore bugs Oxycarenidae Infraorder: Cimicomorpha Pachygronthidae Pachynomidae Piesmatidae Reduviidae-assassin bugs (includes ambush Rhypharochromidae bugs, kissing bugs, thread-legged bugs) Orsillidae Velocipedidae-fast-footed bugs Ischnorhynchidae 608 B Bugs (Hemiptera) Superfamily: Pentatomoidea The scutellum, which means little shield, is a Acanthosomatidae-shield bugs triangular part of the thorax seen dorsally between Aphylidae the first pair of wings. The shape and size of the Canopidae scutellum is highly variable among true bugs and Cydnidae-burrower bugs is frequently used for purposes of classification. In Dinidoridae the Scutelleridae (at least 450 species worldwide), Lestoniidae the scutellum is so large that it covers the entire Megarididae abdomen and wings. These insects, known also as Pentatomidae-stink bugs shield bugs, are among the most spectacular of all Cyrtocoridae Heteroptera, some species being iridescent or Phloeidae metallically colored. All shield bugs are plant Plataspidae ­feeders; some are of agricultural importance. Scutelleridae-shield bugs Heteropterans are characterized by elongate Tessaratomidae-giant shield bugs mouthparts in the form of a segmented beak, or ros- Thaumastellidae trum, used for sucking fluids. The beak has two Urostylidae channels, one through which saliva (a fluid with Superfamily: Pyrrhocoroidea enzymes) is pumped to predigest and liquefy their Largidae food and the other through which fluids are sucked. Pyrrhocoridae-cotton stainers Because their beak is located far forward on the Heteropterans differ from other Hemiptera lower surface of the head, in contrast with the other by their characteristic wings, mouthparts, scutel- hemipterans, the heteropteran beak is versatile, lum, and scent glands. They have two pairs of allowing them to exploit a great variety of resources, wings; the first pair is held flat over their body, including plants, other arthropods, carrion, tadpoles above the second pair of wings, which are or small fish, and even blood from vertebrates. ­membranous and transparent. The design of the Nearly all heteropterans have scent glands that forewings is a compromise between the needs for produce pungent chemicals used primarily for efficient flight and protection. The cuticle of the defense. In adults, the external openings of these corium and clavus is thickened for protection but glands are located on each side of the thorax between these wing parts are also shaped and hinged for the second and third pairs of legs. The openings end facilitating and controlling flight. The wing mem- in a variety of grooves, lobes and spouts that allow brane is thin and usually transparent. All parts of the evaporation of the noxious chemicals. These the wing, including corium, clavus, and membrane, external structures are distinctive in many groups are supported by veins. Some adults have lost their and are commonly used for ­classification or identifi- wings entirely, while others are winged but are cation purposes. Some bugs lack functional scent unable to fly due to flight muscle reduction. Many glands; for example, members of the family Rhopali- species of Gerridae (500 species worldwide), an dae (about 210 species described) are commonly aquatic group known as water striders, are wing- referred to as scentless plant bugs. less. In other true bugs, the wings are ­variously modified or strongly abbreviated. An example of a group with modified wings is the rarely encoun- Defense tered family Schizopteridae (120 described species worldwide). Schizopterids resemble tiny beetles Heteropterans are in general highly mobile, ­diurnal due to their near-black coloration, compact and insects with well developed compound eyes. This rotund shape, and uniformly sclerotized, shell-like mobility allows them to find new hosts and allows forewings. them to escape potential predators or parasites. Bugs (Hemiptera) B 609 True bugs escape predators by flying (e.g., stink are generally not effective in the transmission of bugs, plant bugs, leaf-footed bugs), dropping plant diseases. The damage caused to plants is (e.g., lace bugs, shield bugs); burrowing (e.g., bur- ­usually direct, by feeding on the reproductive parts rower bugs or cydnids); running (e.g., shore bugs, of the plants such as flowers, ovaries, developing seed bugs, water striders), moving into narrow fruits, or ripening or mature seeds. Some species, places (e.g., flat bugs, chinch bugs, palm bugs, however, cause indirect damage by feeding on bed bugs), hopping (e.g., toad bugs), jumping stems and roots, forcing the plant to repair dam- (e.g., schizopterids), or swimming (e.g., water aged tissue. Feeding with a beak allows them to boatmen, giant water bugs, velvet water bugs). bypass many of the plants’ defenses (wax, thorns, Aside from their mobility, the main defense spines, setae, tannins) as well as most pesticides, employed by true bugs is the secretion of a which are most effective against insects that bite ­noxious chemical which serves to repel enemies, and chew. Most of the species in the family ­Miridae, especially ants, which are important predators. or plant bugs, (approximately 10,000 described Other natural enemies include lizards, birds, species, or one-third of all Heteroptera), are frogs, spiders, and other insects. Other defense ­phytophagous. Many species in this family are of mechanisms known among Heteroptera are significant economic importance. Most mirids ­biting (e.g., assassin bugs, damsel bugs, creeping feed on growing portions of the plant such as water bugs, and others), sharp spines on the ­flowers, buds, pollen, or new foliage. A few, however, thorax (e.g., some stink bugs, assassin bugs, and feed on both plant and animal material. Most others), cryptic shapes and ­colors (e.g., ambush rhyparochromids are mature-seed feeders, inject- bugs, most seed bugs, ­leaf-footed bugs, toad ing enzymes into the seed where the nitrogen-rich bugs, and others), mimicry (e.g., ant mimetic contents are liquefied and predigested. Most rhyp- seed bugs and others), aggregation (e.g., immature arochromids feed on fallen seeds, although some leaf-footed bugs, scentless plant bugs, cotton feed on mature seeds while still on the plants; stainers), and aposematic, or warning, ­coloration some are of occasional economic importance (e.g., nymphs of scentless plant bugs, milkweed because they can feed in large numbers. Oncopel- bugs, assassin bugs). Some bugs simply stay very tus are colorful lygaeids that feed on maturing still to avoid being noticed, such as the narrow- seeds of the milkweed plant, the same plant known bodied bugs marsh treaders, stilt bugs, water as primary host of the Monarch butterfly caterpil- scorpions, and the spider-web inhabiting lars. An example of stem feeding is presented by ­reduviids. Members of the Coreidae are Blissus, the famous chinch bugs, known by home- ­outstanding in their fantastic shapes and colors. owners as major lawn pests; they often feed in Some designs function as disruptive coloration great numbers and kill large patches, occasionally in which the outline of the insect is obscured by wiping out entire lawns. Extensive biological ­contrasting color patterns. ­studies have been done on this pest. Cydnids are soil-inhabiting bugs that feed on the roots of plants, hence their name, burrower bugs. Aradids, Feeding or bark bugs, feed on the mycelia of various fungi under tree bark. Tingidae, or lace bugs, are entirely About 60% of all true bug species are plant ­feeders, phytophagous, usually found in large numbers on some of which are of great economic importance. mature foliage. Many species attack and damage The remaining 40% are predatory or ectoparasitic. important ornamental plants. All species of lace Because of their method of feeding, in which they bugs of economic significance are in the subfamily insert their beak stylets into tissues between cells Tinginae, comprised of delicate and beautiful to suck juices rather than directly into cells, they forms with lacelike appearance. 610 B Bugs (Hemiptera) Of all hemipterans, only heteropterans feed on T. maculata, T. pseudomaculata, T. rubrovaria, both other arthropods and on vertebrates. Exam- T. sordida, and Rhodnius prolixus, ecuatoriensis, ples of predaceous bugs are the back ­swimmers and pallescens. All feed at night on humans or (Notonectidae, 343 species recognized) that feed on their pets, and hide during the day, often inside insects trapped in the water surface; damsel bugs human habitations. Cimicids, or bed bugs (about (Nabidae, 500 species) that feed on insects among 100 species), are hematophagous as well, acting foliage and on the ground, or on insects caught in as temporary ectoparasites on bats, humans, and spider webs, and ambush bugs (Phymatinae, 281 birds or rodents living in groups. All are wingless species in the family Reduviidae) that commonly and the majority feed on bats. They spend most hide on or below flowers waiting for pollinating of their time in ­crevices and other hiding places insects such a flies or bees, although other insects near their hosts, remaining on the host only while are attacked as well. Other reduviids, within the feeding. They can be found in the bedroom, bed, subfamily Emesinae, can walk on spider webs and and among the bedclothes. Bed bugs exist wher- feed on spiders. Geocorids (219 species described), ever humans live. Much research has been con- known as big-eyed bugs, prey on other insects and ducted on the two cimicid species, both known have proven useful in biological control programs. as the bed bug, Cimex hemipterus and Cimex A unique group of predatory insects are water strid- lectularius. Most bed bugs do not serve as vectors ers in the subfamily Halobatinae, which inhabit an of pathogens of human or animal disease. Their usual marine habitat, the surface of the ocean, both importance is generally as a nuisance pest, near the shore or far out at sea. Plokiophilids, or although large ­populations can result in serious web lovers, live either on spider webs to steal the loss of blood. The word “bug” is derived from the spider’s prey, or with web-spinners (insect order Anglo-Saxon bugge, which almost certainly Embioptera) feeding on the eggs and weak or dead referred to the bed bug. individuals; their tarsi (feet) are adapted to walking on webs. Some aquatic bugs (Belostomatidae or giant water bugs, and Nepidae or water scorpions) Development and Cytogenetics feed on other insects, on tadpoles and even small fish. All species of Polyctenidae, known as bat bugs, Immature heteropterans, called nymphs or larvae, are ectoparasitic, that is, they feed externally on bats. usually pass through five instars or stages before Cimicids and lygaeoids in the tribe Cleradini feed reaching the adult, or winged, form. They usually on vertebrate blood. live in the same habitat as the adults and are com- monly similar to them in coloration, shape, and feeding habits. Nymphs of some species form large Medically Important Species defensive aggregations. True bugs seem to show a great deal of Triatomine bugs (more than 110 species) are ­cytogenetic diversity, including polyploidy of the nocturnal hematophagous reduviids that feed on autosomes, with the sex chromosome number the blood of mammals, including humans. The highly variable as well. Sex determination in insects tend to feed near the mouth area of sleeping ­Heteroptera is not like that of mammals. The humans and are thus commonly called kissing majority of the species have a simple XX:XY bugs. Some species transmit Chagas’ Disease, an ­system, though many species have XO males, and important disease in Latin America caused by some have multiple X and Y chromosomes and Trypanosoma cruzi Chagas. The most important still are males. triatomine species are Triatoma ­infestans, T. san-  Aphids guisuga, T. dimidiata, T. barberi, T. brasiliensis,  Cicadas Bulb Mites, Rhizoglyphus (Acari: Acaridae) B 611  Lace Bugs Bulb Mites, Rhizoglyphus (Acari:  Leafhoppers Acaridae)  Plant Bugs  Planthoppers chyi-chen ho  Scale Insects and Mealybugs Taiwan Agricultural Research Institute, Taiwan-  Spittlebugs Republic of China  Stink Bugs  Treehoppers Bulb mites are mite species of the family Acaridae  Whiteflies that infests the bulb, rhizome, corm and tuber of plants of Amaryllidaceae, Liliaceae, Iviraceae, Sola- References neae and Cruciferae. Customarily, it refers only to mites of the genus Rhizoglyphus. Seventy-three spe- cies are recorded in this genus over the world. How- Ben Dov Y, Hodgson CJ (eds) (1997) Soft scale insects: their biology, natural enemies and control, vol 7A & B. World ever, only two of them, R. echinopus and R. robini, are crop pests. Elsevier Press, Dordrecht, The Netherlands, found worldwide, causing ­serious problems to the 452 & 443 pp culture of numerous crops. R. echinopus has been Bourgoin Th, Campbell BC (2002) Inferring a phylogeny reported from Argentina (as R. callae), Canada, USA for Hemiptera: falling into the “autapomorphic trap.” In: Holzinger WE (ed) Zikaden: leafhoppers, ­planthoppers (Texas), Belgium, Denmark, France, Germany, Hun- and cicadas (Insecta: Hemiptera: Auchenorrhyncha). gary, Italy, ­Netherlands, Poland, Romania, Russia, Denisia 4, Biologiezentrum des Oberösterreichischen Scotland, Spain, the United Kingdom, Ukraine, Landesmuseums, Austria, pp 67–82 Egypt, Israel, China, India, Iran, Japan, Korea and Blackman RL, Eastop VF (2000) Aphids on the world’s crops. An identification and information guide, 2nd edn.Wiley, New Zealand. R. robini has been reported from Can- Chichester, 466 pp ada, USA, Mexico, China, Japan, Korea, Taiwan, New Cassis G, Gross GF (1995) Hemiptera: Heteroptera (Coleor- ­Zealand, Israel, Egypt, Poland and the United King- rhyncha to Cimicomomorpha). In: Houston WWK Maynard GV (eds) Zoological catalogue of Australia, dom. Rhizoglyphys echinopus and Rhizoglyphus rob- vol 27.3A. CSIRO, Australia, 506 pp ini were not properly distinguished in earlier years, Denno RT, Perfect TJ (eds) (1994) Planthoppers. Their not until van Eyndhoven set them apart. Conse- ­ecology and management. Chapman & Hall, New York, quently, records on these two species in early reports New York, 799 pp Dietrich CH, Deitz LL (1993) Superfamily Membracoidea are subject to uncertainty. A third species, Rhizogly- (Homoptera: Auchenorrhyncha). II. Cladistic analysis phus setosus, is reported to infest various hosts in and conclusions. Syst Entomol 18:297–311 Taiwan. This species was reported first by Manson in Gillot C 1995 The Hemipteroid orders. In: Entomology. 1972, from New Guinea. It may also be distributed Plenum Press, New York, New York, pp. 195–232 Holzinger WE (ed) (2002) Zikaden. Leafhoppers, planthoppers in countries nearby. Another ­species, R. hyacinthi, and cicadas (Insecta: Hemiptera: Auchenorrhyncha). that appeared in early reports causing­ heavy loss to Denisia 4, Biologiezentrum des Oberösterreichischen gladiolus and lily is probably not a valid species, as Landesmuseums, Austria, VIII + 556 pp McGavin GC (1993) Bugs of the world. Blandford, London, there is neither a well-defined description on this UK, 192 pp species nor specimens available. Schaefer CW, Panizzi AR (2000) Heteroptera of economic Acarid mites, in the genera Caloglyphus and importance. CRC Press, New York, NY, 828 pp Schwiebea, were also found to infest bulbs in the Schuh RT, Slater JA (1995) True bugs of the world (Hemiptera: Heteropera): classification and natural history. Cornell 1990s. These mites reproduce on bulbs, and may be University Press, Ithaca, NY, 336 pp as hard as the Rhizoglyphus species to control. The Woodward TE, Evans JW, Eastop VF (1970) Hemiptera term “bulb mite” shall, therefore, include mites of (bugs, leafhoppers, etc.). In: The insects of Australia. these two genera. Mites reported under the generic A textbook for students and research workers. Melbourne University Press, Melbourne, Australia, name of Caloglyphus actually belong to three gen- pp 387–457 era: Caloglyphus, Cosmoglyphus and Sancssania. 612 B Bulb Mites, Rhizoglyphus (Acari: Acaridae) Bulb Mites, Rhizoglyphus (Acari: Acaridae), Table 10 List of Rhizoglyphus mites reported as pests, crops and ornamentals affected, and geographic location Species Crop affected Country algericus Gladiolus sp Algeria alliensis Allium sativum Mexico allii Allium sativum China caladii Caladium sp New Guinea costarricensis Oryza sativa Costa Rica echinopus Allium bakeri Japan Allium cepa Argentina (as R. callae), India, Russia Allium sativum India, Korea, New Zealand, Romania, Spain Capsicum sp India Curcuma domestica India Freesia sp UK Gladiolus sp Argentina (as R. callae), New Zealand Hyacinthus sp Argentina (as R. callae), New Zealand, Russia Iris sp New Zealand Lolium longiflorum USA (as R. hyacinthi) Narcissus sp Canada, New Zealand, Russia, Scotland, UK Solanum sp France, India, USA (as R. phylloxerae) Tulipa sp Netherlands, New Zealand, Russia engeli Freesia sp Netherlands Lilium sp Netherlands Gladiolus sp Netherlands fumouzi Narcissus sp Canada (from Netherlands) longispinosus Taro Taiwan Giant alocasia Taiwan narcissi Narcissus sp China nepos Hypomoea sp Italy robini Allium cepa Israel, Japan, Mexico, New Zealand, USA Allium chinense Japan Allium fistulosum Taiwan Allium porrum Taiwan Allium sativum Egypt, Israel, New Zealand Allium tuberosum Japan Mites, Rhizoglyhus (Acari: Acaridae) B 613 Bulb Mites, Rhizoglyphus (Acari: Acaridae), Table 10 List of Rhizoglyphus mites reported as pests, crops and ornamentals affected, and geographic location (Continued) Species Crop affected Country Daucus carrota New Zealand Freesia sp Japan, UK Gladiolus sp China, New Zealand, Taiwan, USA Iris sp New Zealand Lolium longiflorum Japan, New Zealand, USA Narcissus sp Canada, New Zealand, UK Solanum tuberosum New Zealand Secale cereale Poland robustus Allium sativum Mexico singularis Dioscorea sp India, New Zealand (from India) setosus Allium cepa Taiwan Allium porrum Taiwan Allium sativum Taiwan Caladium sp New Guinea Lilium sp Taiwan Gladiolus sp Taiwan solanumi Solanum sp Pakistan tacitri Citrus sp Tahiti tardus Allium cepa USSR tarsalis Sugar Beets USA tsutienensis Lily Taiwan Green onion Taiwan Leek Taiwan Tuberose Taiwan

Species of these genera are often found in stored adequate host plant, and can maintain their popu- products or materials that are rich in organic sub- lation in the soil for a long time. strates. More research is needed to determine The damage caused by bulb mites to plants exactly how often these species infest bulbs. includes direct infestation and indirect transmis- Bulb mites are generally polyphagous, with sion of plant disease. Bulb mites feeding on bulbs numerous host plants recorded. The recorded host or roots can cause yellowing, wilt and early defo- plants of R. robini, for example, include at least 28 liation of lower leaves, dwarfing or even death of crops that belong to 14 families. Bulb mites usually the plant. Plant pathogens transmitted by bulb inhabit the surface of the bulb where the stems or mites include Fusarium oxysporum, Rhizoctonia roots grow. When the population is high, mites solani, Pythium ultimum, and Pseudomonas mar- can also be located between the tissue layers of the ginata, which infest gladiolus and/or lily. Heavy basal part of the stems. Bulb mites can also feed loss can result from the infestation of bulb mites. and reproduce on plant debris when there is no Destruction of 10–70% of bulbs or plants have 614 B Bulldog Ant or Bull Ant, Myrmecia spp. (Hymenoptera: Formicidae) been reported for lily, ­gladiolus, onion and rakkyo. are still required. There seems no way to eradicate When the bulb mite population is too high, farm- bulb mites from a field once they have invaded the ers may have to shift to grow non-bulb crops. field. The best way to protect the crop is: (i) Treat The life cycle of bulb mite normally under- the bulbs before planting to kill mites that may live goes four stages, namely the larva, protonymph, on them. (ii) Reducing the bulb mite population in tritonymph and the adult. When the environment soil before planting by solar heat or fumigating is suboptimal, such as poor quality or quantity of with acaricides. (iii) Apply ­acaricide sometimes food, crowding or poor environmental quality, the later in the growing season. ­However, acaricide protonymph will molt into a deuteronymph. The applied after planting will have alimited ­ effect. deuteronymph stage is also called the hypopus, which does not have a functional mouthpart. The References hypopus will actively seek a host, usually an arthro- pod, to attach to and be transferred to a new envi- Bu GS, Li LS (1998) Taxonomic notes on and key to the ronment with plenty of food. The hypopus or known species of the genus Rhizoglyphus (Acari: Acar- deuteronymph will, then, molt into tritonymph idae) from China. Syst Appl Acarol 3:179–182 and resume the normal life cycle. Garman P (1937) A study of the bulb mite (Rhizoglyphus hya- cinthi Banks). Bull Conn A E S 402:889–907 Rhizoglyphus mites develop quickly. At 28°C, Ho CC (1988) An introduction to the exotic mite-pests in development from egg to adult only takes Taiwan. Chin J Entomol (Special Publ.) 2:155–166 ­approximately nine days. Adult females live about Nesbitt HHJ (1988) Three new mites of the subfamily Rhizo- twenty-four days and produce 180–280 eggs. glyphine. Can Entomol 76:21–27 “Caloglyphus” mites are similar to Rhizoglyphus mites Woodring JP (1969) Observations on the biology of six species in development rate, but have an even higher of acarid mites. Ann Entomol Soc Am 62:102–108 fecundity. The populations of these mites can build up to a huge number within a short time period. A single bulb may harbor a population of ­hundreds Bulldog Ant or Bull Ant, Myrmecia or even more than a thousand mites. spp. (Hymenoptera: Formicidae) Bulb mites are difficult to control. Rhizogly- phus echinopus, Rhizoglyphus robini, and Rhizogly- Bulldog or bull ants are some of the best-known phus setosus are all resistant to a large number of ants in Australia due to their large size, very painful ­acaricides. It appears that Caloglyphus mites are as sting, and aggressive behavior. Their mandibles are potent as Rhizoglyphus mites in the development exceptionally large and well equipped with teeth. of acaricide resistance. Additionally, they inhabit a Their name is derived from their habit of gripping niche below the soil surface, which is difficult for something with their strong mandibles and hang- acaricides to reach. A large amount of acaricide ing on to it. These ants are aggressive and have well must be applied to have it reach bulb mites. developed vision. If disturbed, these large ants will ­Irrigation can affect bulb mites though, some adult often come swarming rapidly from their nest in the females of R. robini could survive immersion for 30 soil straight towards the intruder with mandibles days. In the field, the mites can hide in airbubbles ­ open and ready to use, but they also are quick to among soil ­particles, and, hence, live even longer. sting any intruder after grasping it in its mandibles. Plowing of fields to expose the interior of soil to Their sting is an important cause of anaphylaxis in solar heat to build up its temperature has been Australia, even causing death of humans. There are ­recommended to kill the bulb mites inside. How- about 90 species of bulldog ants in Australia, and ever, some bulb mites may escape by ­moving down they range greatly in size. Many are brightly col- to a depth of thirty cm or more. Fumigation of the ored red or orange on the head and abdomen. soil does not make the crop immune from bulb Bulldog ants are some of the most primitive mites. Applications of ­acaricide later in the season ant species and only have relatively small ­colonies. Bunchy Top of Papaya B 615 The workers forage in a solitary manner, and The ants in this subfamily (Paraponerinae) unlike many other ant species do not form scent are primitive, and their stings are morphologi- trails when foraging. Instead, bulldog ants forage cally ­similar to those of some solitary wasps Wasp independently and upon finding food carry it stings are multi-purpose defensive tools rather back to the nest, which is located in the soil. than the more specialized weapons of more Despite their aggressive nature, adult bull ants advanced ants, and tend to be more painful than feed predominantly on honeydew, nectar and the stings of ants. other sweet substances, but their larvae are car- Bullet ant is a relatively primitive ponerine, and nivorous and are fed on insects collected by for- unlike more advanced ants, does not display a great aging workers. Bulldog ants are most active deal of polymorphism. Queens are only slightly during the day and forage either on the ground larger than workers. Mature colonies are small and or on low vegetation. Some of the smaller species at most contain a few thousand ants. However, are called “jumper ants” due to their tendency to workers exhibit a size-based division of labor, and leap; despite their relatively small size they are the smaller ants tend to remain in the nest as nurse- extremely aggressive. maids while larger workers serve as guards and for-  Ants (Hymenoptera: Formicidae) agers. Colonies consist of several thousand  Venoms and Toxins in Insects individuals, and are usually found at the bases of  Bullet Ant, Paraponera clavata (Fabricius) trees. The workers forage in the trees in the area directly above the nest, where they search for insect prey and plant nectaries. Extra-floral nectar is an Bullet Ant, Paraponera clavata important part of their diet. Water is also collected. (Fabricius) (Hymenoptera: Both nectar and water are shared with nest ants, or Formicidae) placed as tiny droplets on ­feeding larvae. Solid food consists mostly of arthropods, other invertebrates, Paraponera clavata is best known for its large size and occasionally pieces of small vertebrates. Ter- and severe sting. Workers are 18–25 mm long and mites are especially attractive prey. Nestmates are resemble stout, reddish-black, wingless wasps. The recruited using pheromone trails, although experi- pain caused by the sting of this insect is purported enced foragers also use ­landmarks. Most foraging to be greater than that of any other wasp or ant, activity occurs at dusk and during the night. and is ranked as perhaps the most painful insect  Ants (Hymenoptera: Formicidae) sting. The pain may persist for a full 24 h. The pain  Venoms and Toxins in Insects is caused by a paralyzing neurotoxic peptide in the  Bulldog Ant or Bull Ant, Myrmecia spp venom called poneratoxin. The genus Paraponera is found in Central and South America, south from Costa Rica and Bumble Bees Nicaragua to Brazil and Peru. Bullet ants are used by some indigenous people in their initiation rites Members of the family Apidae (order Hyme­ to manhood. In this process, the ants are first noptera, superfamily Apoidae).  immobilized, and then hundreds of them are Wasps, Ants, Bees and Sawflies  woven into sleeves made out of leaves, with the Bees stinger facing inward. As part of this rite, boys slip the sleeve down onto their arm. The goal of this Bunchy Top of Papaya initiation rite is to keep the sleeve on for a full 10 min. After exposure to the ants, the boys’ arms are This is an important bacterial disease of papaya temporarily paralyzed because of the venom, and that is transmitted by insects. they may shake uncontrollably for days.  Transmission of Plant Diseases by Insects 616 B Buprestidae Buprestidae

A family of beetles (order Coleoptera). They ­commonly are known as metallic wood-boring beetles.  Beetles

Burgess, Albert Franklin

Albert Burgess was on October 2, 1873, in Massa- chusetts. He received a first degree in 1895 and an M.S. in 1897 from Massachusetts Agricultural Burgess, Albert Franklin, Figure 72 Albert F. Academy. From 1899 to 1907 he worked as Assis- Burgess. tant in Entomology at the University of Illinois and inspector of nurseries and orchards for the Ohio Department of Agriculture. Then he returned doctorate in medicine and a doctorate in zoology to Massachusetts to work for the U.S. Department in 1929. He did his military service in 1832. He of Agriculture in the Gypsy Moth Project, and taught in schools in Berlin until, in 1837, he continued this work until his retirement in 1943. became professor of zoology in Halle. He ­married However, in 1916, work on the browntail moth in 1836, and had two sons. His first insect collec- was added to his duties. His American Association tion is in Halle. He published a five-volume­textbook, of Economic Entomologists, and for years contrib- “Handbuch der Entomologie” in 1832–1847. uted much time to that society and its Journal of Between 1850 and 1852, with one of his sons, he Economic Entomology. He died on February 23, travelled in eastern Brazil and then returned to 1953, survived by his second wife and two sons Halle. One account of his Brazilian travels was from his first marriage (Fig. 72). published in 1853 as “Reise nach Brasilien, durch die Provinzen von Rio de Janeiro und Minas ­Geraes…,” another in 1854–1856 as “Systematische Uebersicht der Tiere Brasiliens,” although it was Reference incomplete and deals only with mammals and birds. He returned to Halle, but in 1856 he left Mallis A (1971) Albert Franklin Burgess. In: American ento- again, this time for Argentina, and spent four years mologists. Rutgers University Press, New Brunswick, NJ, (1857–1860) travelling within Argentina before pp 435–437 publishing (1862) a 2-volume book “Reise durch die La Plata-Staaten…” He returned to Halle, but resigned from his position in 1861, divorced his Burmeister, Carl Hermann Conrad German wife Marie Elise, and travelled once more to Argentina. His previous work resulted in his Hermann Burmeister was born in Stralsund, being offered directorship of the Museo Publico ­Germany, on January 15, 1807. His early university de Historia Natural in Buenos Aires in 1862. His education was at Universität Greifwald (1825–1827), interests were in all areas of natural history, but whence he moved to Universität Halle. His disser- especially entomology. He wrote on paleontology, tation at Halle and academic training gave him a insect anatomy, the beetle family Scarabaeidae, Burnet Moth Biology (Lepidoptera: Zygaenidae) B 617 The family Zygaenidae is a member of the order Lepidoptera, suborder Ditrysia and the super-­ family Zygaenoidea. Other than Zygaenidae, the ­superfamily Zygaenoidea consist of the following families: ­Megalopygidae (Lagoidae), Heterogyni- dae, Chrysopolomidae, Metarbelidae (Teragrii- dae), Limacodidae (including Cochlidiidae, Heterogenidae, Eucleidae), Cyclotornidae, and Epipyropidae. The Zygaenidae are further subdi- vided into seven ­subfamilies: Zygaeninae (burnet moths), Procridinae (forester moths), Chalcosii- nae, Charideinae, Phaudinae, Anomoeotinae and Himantopterinae from which only Zygaeninae and Procridinae (and to a lesser extent Charidei- nae) are frequently ­mentioned even though Chal- cosiinae are considered to be the largest group Burmeister, Carl Hermann Conrad, Figure 73 living in tropics. It is worth noting that the genus C. Hermann Burmeister. Zygaena is the most studied genus of the family. and many other subjects, and published about 300 External Morphology titles. He remarried in Argentina and had two sons. He died on May 2, 1892, following an ­accident The adults of the family Zygaenidae closely resem- in which he fell from a ladder into a glass ­showcase ble the Ctenuchidae from the superfamily Noctu- at the museum (Fig. 73). oidea, but are readily distinguished by the presence

of Cu2 in the hind wings. Many are very brilliantly colored and there is considerable diversity of References structure. It is interesting to note that all subfami- lies, except Phaudinae and Himantopterinae, have Essig EO (1931) Burmeister, Hermann Carl Conrad. In: A been shown to contain the cyanogenic glucosides history of entomology. The Macmillan Company, New linamarin and lotaustralin. The larvae are short York, NY, pp 562–563 Papavero N (1973) Burmeister. In: Essays on the history of and cylindrical and have short hairs protruding Neotropical dipterology, with special reference to col- from numerous verrucae. The pupae are enclosed lectors (1750–1905). Museu de Zoologia, vol 2. São in tough, elongate, membranous cocoons Paulo, Brazil, pp 292–293 aboveground. Ulrich W (1972) Hermann Burmeister, 1807 to 1892. Ann Rev Entomol 17:1–20 Life History and Habits

Burnet Moth Biology The zygaenid moths (Figs. 74 and 75) usually are (Lepidoptera: Zygaenidae) diurnal in habit, though several species are known as nocturnal or are active during both cyrus abivardi night and day. Zygaena (Mesembrynus) nocturna Swiss Federal Institute of Technology, Z­urich, Ebert, also known as a subspecies of Z. (M.) seitzi Switzerland Reiss, is an example of the latter case. While it 618 B Burnet Moth Biology (Lepidoptera: Zygaenidae)

R Sc 1 R2 R3 R4 M R5 M1 2A M2 M3 Cu1a Cu1b 1A Cu2

M Sc+R1 Rs M1 M2 M3 Cu1a Cu1b 3A 2A Cu2

Burnet Moth Biology (Lepidoptera: Zygaenidae), Figure 75 Resemblance of the family Burnet Moth Biology (Lepidoptera: Zygaenidae), Ctenuchidae (Noctuoidea) (above left) to the Figure 74 The adults of two Zygaena species: family Zygaenidae, but readily distinguished by (above) Z. fraxini Mén.; (below) Z. carniolica Scop. their wing venation (above right: Ctenuchidae (After Abivardi C (2001) Iranian entomology–an (Euchromia polymena); below: Zygaenidae introduction, 2 vols. Springer Verlag, Heidelberg, (Zygaena filipendulae L.). Germany, XXXIII, 1033 pp).

stems and twigs or on the surface of the box was originally described as exclusively nocturnal, ­provided for pupation. The number of instars it is also reported from Yasudj (Iran) to fly during varies among species, with Z. (M.) lydia the day. Staudinger displaying seven instars and Artona In general, the zygaenid larvae live exposed chorista Jordan with seven. on herbaceous plants. The larvae of the genus The most interesting life cycle (Fig. 76) Zygaena show a certain oligophagy: while those ­strategies have been observed in species of the belonging to the subgenera Agrumenia and Palaearctic genus Zygaena. Development time Zygaena feed exclusively on Fabaceae, those of varies markedly within a population. This varia- the subgenus Mesembrynus feed, with few excep- tion is due to repeated ­larval hibernations between tions, on Apiaceae. Laboratory studies on the the third to the tenth instar and are due either to biology of a zygaenid from Iran, Z. (M.) tamara repeated or prolonged diapause periods. This ssp. Kendevanica Tremewan, revealed nine larval phenomenon has been described as “fractionized instars during which two to three stages of dia- development.” ­Larvae normally pupate after six pause were observed. In the final instar, the lar- or seven feeding instars.The high flexibility in vae constructed their cocoons either on the ­different Zygaena life cycle phenologies is based Burnet Moth Biology (Lepidoptera: Zygaenidae) B 619

Burnet Moth Biology (Lepidoptera: Zygaenidae), Figure 76 External morphology of eggs (a), larvae (b & c; left: dorsal position; right: lateral position) and cocoon (d) of Z. carniolica Scop. with its adults (e) resting on thistle flowers. (Courtesy of Professor Clas M. Naumann and Pro Natura- The Swiss Alliance for Nature Conservation, Basel, Switzerland.) on both exogenous and endogenous factors. plants, the enzyme comes into contact with the The variability in diapause and the consequent glucoside leading to the release of hydrocyanic ­variable generation times may (Fig. 77) represent acid. Hydrocyanic acid is a powerful toxin that a strategy of spreading of the risk, thereby buffer- fends off herbivores and thus protects the plants. ing the populations against adverse and fluctuat- Within the insects, cyanogenesis occurs in bee- ing climatic conditions. tles (Coleoptera) and bugs (Hemiptera) and seems to be quite common in Lepidoptera. In the order Lepidoptera, cyanogenesis is reported Cyanogenesis for several families of butterflies (Nymphalidae, Lycaenidae, Pieridae, Papilionidae and Hesperi- The phenomenon of cyanogenesis is known to idae) and moths (Megalopygidae, Heterogyni- occur in more than 2,500 plant species (includ- dae, Limacodidae, Zygaenidae, Thyatiridae, ing important crop plants such as cassava, sor- Geometridae, Notodontidae, Arctiidae, Noctui- ghum, flax, clovers and almond) as well as in dae and Lymantriidae). Within the family some arthropods. Cyanogenesis is the process Zygaenidae, five of the seven subfamilies (except by which either plants or animals release hydro- the Phaudinae and Himantopterinae) have been gen cyanide (HCN) from endogenous cyanide- shown to contain the cyanogenic glucosides containing compounds and is thought to play a linamarin and lotaustralin (Figs. 78 and 79). role in defense against generalist, natural ene- Cyanogenesis is closely related to aposematic mies. In plants, the cyanogenic glucosides and patterns in both larvae and adults, and mimicry the corresponding enzymes are usually stored is common. In Zygaena ­larvae there are three in different compartments. When herbivores defenses against natural enemies: (i) an apose- such as cattle and insects feed on cyanogenic matic coloration that discourages an attack by a 620 B Burnet Moth Biology (Lepidoptera: Zygaenidae)

Burnet Moth Biology (Lepidoptera: Zygaenidae), Figure 77 Fractionized development in Zygaena species: Z. transalpina hippocrepidis Hueb. and Z. filipendulae L. as examples. (Courtesy of Prof. Clas M. Naumann.)

Burnet Moth Biology (Lepidoptera: Zygaenidae), Figure 78 The process of cyanogenesis or enzymatic release of hydrogen cyanide (HCN) from endogenous cyanide-containing compounds.

predator when visual contact is made, (ii) a the viscosity of the fluid, and (iii) when a larva secretion that is released following a relatively is eaten by a predator, the liberated hydrocyanic slight touch that fends off enemies by the nox- acid of the hemolymph deters predation of other ious taste of the cyanogenic glucosides and/or larvae. Burnet Moth Biology (Lepidoptera: Zygaenidae) B 621 Trichogramma evanescens (Hymenoptera: Tricho- grammatidae). However, the percentage of para- sitism was not high enough to control the pest. Economic Importance

Knowledge about the economic importance of the members of the family Zygaenidae is confined to the subfamily Procridinae (forester moths) and, to a much lesser extent, to the subfamily Zygaeninae (burnet moths). The members of both subfamilies have been reported to play a role in pollination of the orchid Anacamptis pyramidalis (Orchidaceae). Among the serious pests are western grape- leaf skeletonizer, European grape leaf skeletonizer, Burnet Moth Biology (Lepidoptera: Zygaenidae), Artona chorista Jordan, and coconut leaf miner. Figure 79 Structure of two cyanogenic glucosides The western grapeleaf skeletonizer, Harri- (above: Linamarin; below: Lotaustralin) produced sina brillians, has been the subject of numerous by the members of the family Zygaenidae. studies in California (USA) and in northwestern Mexico. While the populations of this moth in southern California appear to be maintained at low levels of abundance by the combined activ- Predators and Parasitoids ity of a granulovirus (HbGV) and the parasitoid Ametadoria misella (Diptera: Tachinidae), out- Several natural enemies are known. Ectemnius breaks of this insect have been common in cen- kriechbaumeri (Hymenoptera: Sphecidae) para- tral California. The host plant is damaged as sitizes larvae of the six-spot burnet (Zygaena fil- follows: first, the early fourth instar larvae feed ipendulae L.) in Italy and Spain. In Iran, larvae of on the lower leaf surface, leaving only the veins Zygaena (Agrumenia) esseni Blom are parasitized and upper cuticle. This gives leaves a whitish, by the ichneumonid Casinaria orbitalis Graven- paper like appearance. Then, the late fourth and horst. They also are susceptible to infection by the all fifth instar larvae ­skeletonize the leaves, leav- entomopathogenic nematode Steinernema sp. ing only the larger veins. In high populations, Populations of western grapeleaf skeletonizer, larvae can defoliate vines by July. When the vines Harrisina brillians, in southern California appear are severely defoliated, larvae will then feed on to be maintained at low levels of abundance by the grape clusters, which can result in bunch rot. the combined activity of a granulovirus (HbGV) Defoliation can also result in sunburn of the and the parasitoid Ametadoria misella (Diptera: fruit and quality loss. Furthermore, defoliation Tachinidae). after harvest may also weaken vines by affecting In Italy, the European grapeleaf skeletonizer food reserves. (Theresimima ampellophaga) is attacked by six The European grapeleaf skeletonizer,Theres - species of parasitoids namely, two (chalcidids imima ampellophaga, is a bivoltine species in the ­Brachymeria intermedia and Hockeria unicolor), southern part of its range (south Italy) and a braconid (Apanteles ultor), two tachinids (Zenil- ­univoltine in France, north Italy, Austria, Hungary lia libatrix and Exorista sp.) and the famous and the former USSR. The larvae feed on 622 B Burnet Moths (Lepidoptera: Zygaenidae) Burrower Bugs the lower leaf surface and in late July, they aban- granulovirus of Harrisina brillians (Lepidoptera: don the leaves and move to the stumps left after Zygaenidae) in California. Environ Entomol 28:868–875 pruning in the previous year where they spin Wipking W, Naumann CM (1992) Diapause and related cocoons in which they overwinter. Damage Phenomena in Zyganidae moths. In: Dutreix C, Nau- includes injuries to the young leaves by the small mann CM, Tremewan WG (eds) Recent advances in larvae in summer, injuries to the unopened buds burnet moth research (Lepidoptera: Zygaenidae). Koeltz Scientific Books, Champaign, IL, pp 107–128 immediately after hibernation and destruction of the young leaves by the older larvae in spring, which consume the whole leaf except for the midrib. Burnet Moths (Lepidoptera: Artona chorista Jordan is recorded as a Zygaenidae) Burrower Bugs major pest of large cardamon plantations in India. Eggs are laid on the underside of leaves in Members of the family Cydnidae (order batches of over 300 and hatch after about two Hemiptera). weeks. The young larvae skeletonize the leaves,  Bugs while mature larvae leave only the midribs exposed. There are seven larval instars and the larval and pupal stages last about two months or one month, respectively. Adult males and females Burrowing Water Beetles live for about one week. Coconut leaf miner, Artona catoxantha Members of the family Noteridae (order Coleoptera). Hamps, is an important pest of coconut in  Beetles ­Indonesia. Although Apanteles artonae (Glypta- panteles artonae) has been found to be the most important parasitoid of the pest, hyperparasit- Bursa Copulatrix ism of the ­parasitoid by other insects reduce the activity of A. artonae leading to frequent A sac-like modification of the oviduct, or copula- outbreaks of the coconut leaf miner. tory chamber, that receives the male aedeagus.  Reproduction

References Bursicon

Abivardi C (2001) Iranian entomology–an introduction, 2 vols. Springer Verlag, Heidelberg, Germany, XXXIII, 1033 pp A neuropeptide hormone produced by the neu- Efetov KA, Tarmann GM (1999) Forester moths. Apollo rosecretory cells of the brain that controls scle- Books, Stenstrup, Denmark, 191 pp rotization (tanning) and cuticle expansion. Franzl S (1992) Synthesis, transport and storage of cyanogenic  glucosides in larva of Zygaena Trifolii (Esper, 1783) (Lep- Integument: Structure and Function idoptera: Zyaenidae). In: Dutreix C, Naumann CM, Tremewan WG (eds) Recent advances in burnet moth research ­(Lepidoptera: Zygaenidae). Koeltz Scientific Books, Champaign, IL, pp 21–31 Bush Crickets Naumann CM, Tarmann GM, Tremewan WG (1999) The western Palaearctic Zygaenidae (Lepidoptera). Apollo A subfamily of crickets (Eneopterinae) in the Books, Stenstrup, Denmark, 304 pp Stark DM, Purcell AH, Mills NJ (1999) Natural occurrence order Orthoptera: Gryllidae. of Ametadoria misella (Diptera: Tachinidae) and the  Grasshoppers, Katydids and Crickets Butterflies (Lepidoptera: Rhopalocera) B 623 Butterflies (Lepidoptera: specialists combine Riodinidae with Lycaenidae. Rhopalocera) Contrarily, most of the subfamilies in Nymphali- dae in the past often have been separated as their john b. heppner own families, like Satyridae, Charaxidae, Morphi- Florida State Collection of Arthropods, dae, Amathusidae, Danaidae, Heliconiidae, etc. Gainesville, FLorida, USA Butterflies now are thought to be a lineage from ancestors of what remain now as the most primi- Among the insect order Lepidoptera, butterflies tive of bombycine moths (perhaps resembling comprise about 9% of the order worldwide, Ratardidae and relatives of Southeast Asia), which totaling about 20,400 described species (moths then evolved to geometer moth ancestors (families represent the other 91% of all lepidopterans). Geometridae and Hedylidae) and an alternate lin- There are perhaps another 3,500 butterfly species eage that evolved to diurnal lifestyles and ­modern awaiting discovery and naming, mostly from trop- butterflies. ical regions of the world, and especially among Butterfly adults typically have large eyes, a large the smaller species such as skippers (family Hes- haustellum (or tongue), and knobbed, or clubbed, periidae) and blues (family Lycaenidae). The antennae; but skippers (family Hesperiidae) mostly Nymphalidae are the largest butterfly family, with have the antennae with elongated hooked clubs. about 7,080 known species worldwide; second Although most butterfly adults have strong tho- largest is Lycaenidae with 5,955 known species. racic legs, in the family Nymphalidae the first pair Although the name Rhopalocera is not used in of thoracic legs are not used for ­walking and instead modern ­classification of Lepidoptera, the name are held folded under the ­prothorax. The bodies of can be used to refer to all the butterflies (Hetero- adult butterflies are typically rather slender, but cera is used as the name for all moths). While many groups have very robust bodies, allowing them most moths are nocturnal (with many exceptions), to be very strong fliers (e.g., charaxine and danaine most all ­butterflies are diurnal, although some are Nymphalidae). Some groups have scent organs known to be crepuscular (especially a few tropical (coremata) on the abdomen that can be everted skippers). either for protection or as pheromone releasers Out of the total of 125 families of Lepidoptera, during mating behavior. Danainae butterflies (fam- there are seven families of butterflies, although ily Nymphalidae) have wing vein scent organs many specialists continue to place snout butter- (androconia) in males, and Satyrinae butterflies flies (family Libytheidae, only 12 known species) (family Nymphalidae) have tymbal organs used for among the Nymphalidae and thus have only six hearing within some wing veins. Wings include a families. Likewise, there is controversy about pair of forewings and a pair of typically smaller whether skippers (family Hesperiidae) should be hindwings (some Pieridae have larger hindwings in their own superfamily, Hesperioidea, or together than forewings, particularly in the tropical American with other butterflies in a single superfamily subfamily Dismorphiinae), and generally the fore- ­Papilionoidea. One solution to this controversy is wings are rather triangular in shape and the hind- to use a sub classification below the superfamily wings are more rounded. Great variety of wing level, thus the series Hesperiiformes and series shape, however, is known and many groups have Papilioniformes are used. The main true butterfly hindwing tails (e.g., many Lycaenidae and Papil- families are Papilionidae (swallowtail butterflies), ionidae). A huge variety of color patterns exist Pieridae (yellow-white butterflies), Lycaenidae among butterflies, from monotone browns or grays, (gossamer-winged butterflies), Riodinidae (metal- to extremely colorful, to some that even are nearly mark butterflies), Libytheidae (snout butterflies), colorless or transparent (e.g., some tropical and Nymphalidae (brush-footed butterflies). Some glasswings of the subfamily Ithomiinae, family 624 B Butterflies (Lepidoptera: Rhopalocera)

Butterflies (Lepidoptera: Rhopalocera) , Figure 80 Representative butterflies (Lepidoptera: Rhopalocera): top left, Isoteinon lamprospilus formosanus Fruhstorfer (Hesperiidae) from Taiwan (photo C.C. Lin); top right, Zerynthia polyxena cassandra (Geyer) (Papilionidae, Parnassiinae) from France (photo J.H.H. Butterflies (Lepidoptera: Rhopalocera) B 625 Nymphalidae). The morpho butterflies of the sub- hang upside down (Lycaenidae pupae tend to be family Morphinae (family Nymphalidae), from laid flat on a plant surface). tropical America, are well known for their brilliant Butterflies, while a small percentage of the blue coloration that is the result of structural scales order Lepidoptera, have served as the model organ- that reflect light, rather than the typical lepi- isms for a large number of ecological and biological dopteran wing scales that have pigmented colors. studies of the Lepidoptera, much more than among Butterfly caterpillars for the most part are typ- the moths. Part of this study usage pertains to their ical lepidopteran caterpillars, with the usual num- being diurnally active, and thus easier to study than ber of prolegs (4 pairs plus a posterior pair), but the nocturnal moths. Butterflies also are mostly many different setal vestitures and color forms are more colorful and larger than typical moths, and known. Caterpillars typically have a hard head cap- are thus the most well known lepidopterans among sule, three pairs of clawed thoracic legs, and 4 pairs the general public. Butterflies have complex flight of abdominal prolegs having crochets (hook-like behavior and mating rituals that have been the sub- spines on the base of the prolegs that provide foot- ject of many detailed studies over the years. Flight ing when climbing on plants), plus a posterior pro- among butterflies also involves directed migration leg pair. Most of the Nymphalidae larvae have in some cases, the most well known example being various kinds of bizarre spined and enlarged setae, the yearly mass autumn flights of the American called scoli, typically even on the head. Swallowtail monarch butterfly (Danaus plexippus, family larvae, on the other hand, have a unique defensive Nymphalidae) from as far as southern Canada to odiferous and usually brightly colored forked scent wintering refugia in Mexico, and then back again organ, called an osmeterium, just behind the head the following spring. There are many other cases of capsule that is extruded to help defend against a lesser migrations among other species and on all predator. Larvae among most Lycaenidae are continents. Other studies on butterflies have focused ­slug-like and can retract their head into folds of the on their life ­histories, which involve such intricate prothorax. The more primitive skipper caterpillars aspects as commensal myrmecophilous adaptations, (family Hesperiidae) have few body setae and as among most larvae of the blues (family Lycaeni- mostly feed on grasses and other monocots. Other dae) and metalmarks (family Riodinidae), where butterfly larvae feed on a great variety of hostplants, ants protect the larvae from predators and the lar- although most individual species have a narrow vae provide the ants with desirable secretions. hostplant preference (e.g., monarch ­butterfly larvae ­However, most butterflies still remain unknown feed only on milkweed leaves, Asclepiadaceae). biologically, particularly among tropical species. Most butterfly larvae pupate as exposed pupae and The largest known butterflies are among the do not make cocoons. ­Swallowtail pupae (family birdwings (family Papilionidae) (Fig. 80) of the Papilionidae) typically use a silken girdle to angle Indo-Australian tropics, especially in New Guinea away from a plant stem, while most other butter- and the Solomon Islands, where the largest females flies attach their pupae using the cremaster and attain wingspans of up to 280 mm. One African

Thiele); second row left, Eurytides marcellus (Cramer) (Papilionidae, Graphiini) from Florida, USA (photo H.O. Hilton); second row right, Papilio glaucus Linnaeus (Papilionidae, Papilionini) from Florida, USA (photo H.O. Hilton); third row left, Pieris canidia (Sparrman) (Pieridae, Pierinae) from Taiwan (photo C.C. Lin); third row right, Heliophorus ila matsumurae (Fruhstorfer) (Lycaenidae, Lycaeninae) from Taiwan (photo C.C. Lin); bottom left, Libythea celtis formosana Fruhstorfer) (Libytheidae) from Taiwan (photo C.C. Lin); bottom right, Agraulis vanillae (Linnaeus) (Nymphalidae, Heliconiini) from Florida, USA (photo J. B. Heppner). 626 B Butterflies and Moths (Lepidoptera) swallowtail species (Papilio antimachus) has males The Lepidoptera, one of the main plant-feeding with a wingspan of up to 250 mm (females in this groups of insects in the world, are well known to species are smaller than the males). The smallest most all persons familiar with nature or the ­garden, known butterflies are some of the high altitude or as the day-flying butterflies and the mostly desert blues (family Lycaenidae), where wingspans ­nocturnal moths. Included are all the butterflies as small as 6 mm are known. The average butterfly, and skippers (superfamily Papilionoidea), plus however, has a wingspan of about 30 mm, not much such common moth groups as silkworms (or silk- different from the average moth adult, since there moths) (family Bombycidae), emperor moths (or are a large number of very small skippers and blues, giant silkmoths) (family Saturniidae), hornworms and fewer of the larger swallowtails and Nymphali- (or hawk moths) (family Sphingidae), cutworms dae in the world. (or millers and owlet moths) (family Noctuidae),  Butterflies and Moths inch worms (or geometer moths) (family Geometridae), clothes moths (family Tineidae), References and many others. The spectacular variety of wing coloration and markings of the Lepidoptera has D’ Abrera B (1980–95) Butterflies of the world, 12th vol. Hill evolved over millions of years, from the rather House, Melbourne, Victoria, Australia drab primitive moths that hardly appear much Douglas MM (1986) The lives of butterflies. University of ­different than the related Trichoptera, to the most Michigan Press, Ann Arbor, Michigan, 241 pp, 16 pl Feltwell J (1986) The natural history of butterflies. Facts on brilliantly colored butterflies. The Lepidoptera are file, New York, New York, 133 pp notably differentiated from Trichoptera by the Feltwell J (1993) The illustrated encyclopedia of butterflies. scales which cover the wings and all external body Blandford, London, UK, 288 pp parts. Kitching RL, Scheermeyer E, Jones RE, Pierce NE (eds) (1999) Biology of Australian butterflies. CSIRO, Lepidoptera (or “scaly wings”) are perhaps ­Canberra, Australia, 395 pp (Monograph of the Austra- best known for the colorful day-flying butterflies. lian Lepidopterist’s Society 6) Such famous species as the American monarch Manos-Jones M (2000) The spirit of butterflies: myth, magic, butterfly (Danaus plexippus, family Nymphalidae, and art. H. N. Abrams, New York, NY, 144 pp Nijhout HF (1991) The development and evolution of but- subfamily Danainae), the swallowtails and the terfly wing patterns. Smithsonian Institution Press, tropical birdwings (family Papilionidae), the many ­Washington, DC, 297 pp, 8 pl common yellow butterflies (family Pieridae), and Owen DF (1971) Tropical butterflies: the ecology and behaviour of butterflies in the tropics with special reference to blues and hairstreaks (family Lycaenidae), are African species. Clarendon Press, Oxford, UK, 214 pp, 40 pl known by most persons in the world from their Vane-Wright RI, Ackery PR (eds) (1984) The biology of butter- earliest school days. The name “butterfly” is flies. Royal Entomological Society of London, 429 pp thought to come from Old English usage related to (Reprinted 1989, Princeton University Press, Princeton, NJ) Watson A, Whalley PES (1975) The dictionary of butterflies and yellow butterflies looking like slices of butter on moths in color. McGraw Hill, New York, NY, 296 pp, 144 pl the wing, or “butter-fly” (the Old English or Old German “buterfloege”), or even ancient folklore of fairies stealing butter. Other languages and ­cultures all have their own common names for butterfly: Butterflies and Moths farfalla (Italian), lepke (Hungarian), Schmetterling (Lepidoptera) or Tagfalter (German), papillon (French), vlinder (Dutch), sommerfugl (Danish), psyche (Greek), john b. heppner chô-chô (Japanese), hú díeh ­(Chinese), borborleta Florida State Collection of Arthropods, (Portuguese), mariposa (Spanish), fluture (Roma- ­Gainesville, FL, USA nian), farasha (Arabic), kupu-kupu (Indonesian), Butterflies and Moths (Lepidoptera) B 627 rama-rama (Malaysian), titli (Urdu), boboochka modern understanding of the evolution of the (Russian), kipepeo (Swahili), and so on. Many order, the simplified divisions nonetheless are a names refer to both butterflies and moths, such as way of referring to each group using Latin the German word Schmetterling and the French names and are still commonly encountered in papillon, while moths are sometimes referred to the popular literature. Likewise, for the terms what in English would be “night butterflies,” or Microlepidoptera (or the smaller and primitive special words are available just for moths as, for moths) and Macrolepido­ptera (the usually larger example, Nachtfalter (German), moth (English), and more advanced moths and butterflies): and polilla (Spanish). these terms are not universally applicable since Most cultures in the world have mythology some “micro” -moths include very large species and words for butterflies and moths. Moths, (some Hepialidae and Cossidae) and some ­however, while also having well known common “macro” -moths also include some very small names, have mostly been associated since ancient species (e.g., some Geometridae and Noctuidae). days with those few species that are destructive Some butterflies (e.g., some blues, Lycaenidae) to man: thus, cutworms (Noctuidae), clothes are smaller even than some of the average moths (Tineidae), rice moths and grain moths Microlepidoptera. (Pyralidae), cankerworms (Geometridae), and so There is incredible diversity of form, biol- forth. Folklore for Lepidoptera also includes such ogy, behavior, and feeding habits among the Lep- superstitions as the fear of death associated with idoptera, which occur in almost all known the death-head sphinx of Europe and Asia (Acher- habitats, from the Arctic to the densest jungles. ontia atropos, Sphingidae): the large-bodied adults The only region ­lacking Lepidoptera is Antarc- in this genus have markings on the thorax that tica, although some small brachypterous species resemble a human skull, and they also squeak like could conceivably be present on the northern- a mouse when held by their bodies. Likewise, the most tip of the continent nearest to Tierra del very large black witch moth (Ascalapha odorata, Fuego. There are also ­completely different life- Noctuidae) of tropical America is also feared as styles between the adults and the larvae of Lepi- an omen of death when one flies into a house doptera. For example, while adult butterflies seek through an open window. Many native cultures, nectar for the most part, and most moths at least like in the Amazon Basin, believe butterflies seek moisture (there are a few that do not feed as are the departed souls from recently deceased adults), there are such strange larval adaptations persons. Contrarily, among all the Lepidoptera, as the myrmecophilous larvae of many Lycaeni- perhaps the most beneficial to man has been the dae, where the larvae are tended and protected silkworm moth, Bombyx mori ­(Bombycidae), a by ants. As a contrary example, in larvae of Dal- domesticated variety of a native Chinese silk- ceridae, the larvae are protected from ant attacks worm moth which has been cultured for centuries by an integumental defensive secretion, while in China to produce fine silk, spun from the the adults of these slug caterpillars lead simple strands of its white cocoons. lives in search of mates, as do most moths. The Lepidoptera are estimated to number In the overall world fauna of 255,000 species approximately 255,000 extant species in the of Lepidoptera, most of the evolutionary devel- world, with about 156,100 species already named opment and biodiversity is among the moths and cataloged. The order has often been divided (an estimated 231,500 species), while butterflies into the generalized groupings of Rhopalocera, and skippers total an estimated 23,500 species or ­butterflies, and Heterocera, or moths. worldwide, and represent only about 9% of the Although this separation has no validity in our total extant species of Lepidoptera. 628 B Butterflies and Moths (Lepidoptera) Classification Order: LEPIDOPTERA Suborder: Zeugloptera The order is now divided into four suborders, Micropterigoidea based on modern studies using cladistics and Suborder: Aglossata other techniques for analysis of morphological Agathiphagoidea characters and other evolutionary information: Suborder: Heterobathmiina Zeugloptera, Aglossata, Heterobathmiina, and Heterobathmioidea Glossata. Each of the first three suborders include Suborder: Glossata only a single nominate family of primitive moths Cohort: Dacnonypha and all the remainder of the order is under Glossata. Infraorder: Dacnonypha There are differing modern classifications adhered Eriocranioidea to, although in general most lepidopterists now Infraorder: Lophocoronina agree on the overall treatment of families and Lophocoronoidea higher categories. In the classification adopted Cohort: Myoglossata herein, the Glossata are further divided into the Subcohort: Myoglossata cohorts Dacnonypha and Myoglossata. Dacnonypha Infraorder: Neopseustina are subdivided into two infraorders: Dacnonypha Neopseustoidea and Lophocoronina. Myoglossata are divided into Subcohort: Neolepidoptera two subcohorts, Myoglossata and Neolepidoptera, Infraorder: Exoporia with the first containing only the infraorder Mnesarchaeoidea Neopseustina, and Neolepidoptera having two Hepialoidea infraorders: Exoporia, and Heteroneura. Most Infraorder: Heteroneura Lepidoptera are in Heteroneura, which are divided Division: Monotrysia into two divisions: Monotrysia and Ditrysia. Section: Nepticulina Monotrysia have two sections: Nepticulina and Andesianoidea Incurvariina. Ditrysia, then, contain the majority Nepticuloidea of the order, with section Tineina having most of Tischerioidea the micro-moths, and section Cossina mostly the Palaephatoidea larger moths and the butterflies. The remaining Section: Incurvariina ­classification details in Lepidoptera involve­further Incurvarioidea divisions into subsections, superfamilies, and Division: Ditrysia families. Section: Tineina The following listing gives an overview of the Subsection: Tineina main groupings and superfamilies of Lepidoptera. Tineoidea Butterflies are in Papilionoidea, including skippers Gelechioidea which sometimes are placed in their own super- Copromorphoidea family, Hesperioidea. Butterflies are placed near Yponomeutoidea the middle of the Bombycina, and not at the end Immoidea of the order as many older works have them, Pyraloidea since the Noctuidae are now considered the most Pterophoroidea ­evolutionarily advanced Lepidoptera. Groups Subsection: Sesiina ­preceeding Ditrysia contain the most primitive Sesioidea Lepidoptera, and among these, the first three Zygaenoidea ­suborders contain the most archaic relicts of Section: Cossina ancient lepidopteran lineages still extant. Subsection: Cossina Butterflies and Moths (Lepidoptera) B 629 Cossoidea a subfamily or as a separate family, etc. Even some Castnioidea unusual tribes within subfamilies are considered Tortricoidea separate families by some specialists. Among the Subsection: Bombycina butterflies, nearly all subfamilies have at one time Calliduloidea or another been considered separate families, and Uranioidea some of the currently adopted families were listed Geometroidea as their own superfamilies (viz., Nymphaloidea Papilionoidea and Lycaenoidea, etc.) in some past Drepanoidea classifications. Bombycoidea As the diversity of the Lepidoptera came to Sphingoidea light after Linnaeus, as more species were discov- Noctuoidea ered in tropical regions, more and more categories The arrangement of the classification of and families were needed to classify the enormous ­Lepidoptera follows a progression somewhat in ­biodiversity discovered in the world. Where line with our knowledge of how the order ­Linnaeus had only five “families” of Lepidoptera in evolved, from the most primitive moths that 1758, we now have 125 families, 290 subfamilies, resembled Micropterigidae, to what are now and several hundred tribes. As noted above, considered the most advanced lepidopterans, remaining controversies often involve whether the Noctuidae. Yet, advanced features are also some of the subfamilies should be separate fami- found in other groups, such as the Sesiidae, with lies: for example, in one recent classification, most their unique wing locking mechanism that nearly of the Gelechioidea families have been reduced to approaches the similar wing locking found in subfamilies in one enormous family Elachistidae, wasps (Hymenoptera), and butterflies, where which itself is only a small family among several some have evolved advanced features like the families of Gelechioidea in the classification used chordotonal organs found in wing veins of herein. Another case involves the slug caterpillar Satyrinae (Nymphalidae). families, which evidently have converged on a Overall, the order has 32 superfamilies and common larval habitus while their fundamental 125 families in the classification adopted herein. evolution, as based on the position of the heart There is still some controversy in terms of how vessel, demonstrates that the different families many families and superfamilies there are and belong in two different lineages within the­Ditrysia: how they should be arranged. For example, some the flannel moths (Somabrachyidae and Mega- other recent classifications for Lepidoptera use 46 lopygidae), as well as the burnet-type moths superfamilies, splitting many odd families to their ­(Heterogynidae, Zygaenidae, Himantopteridae, own monobasic superfamilies. However, the foun- and Lacturidae), all Zygaenoidea, being in Section dations of the primitive groups (non-Ditrysian Tineina, while the other families with slug cater- groups) are fairly well established now, although pillars (Dalceridae, Limacodidae, and Chrysopo- new discoveries can still come to light from remote lomidae), of the Cossoidea, belonging in Section tropical regions of the world: for example, one Cossina. However, some specialists continue small family of primitive moths, the Neotheoridae, ­placing all slug caterpillar families together. These was only discovered within the past 25 years and differing arrangements often are dependent on the was based on a single known specimen from experience of various specialists, since many only ­Brazil. Since many specialists elevate odd groups study local ­faunas, for example, and not the to higher levels, many of the remaining controver- entire global fauna of a family, thus limiting their sies in Lepidoptera classification pertain to how knowledge and often resulting in the view that different groups should be treated, i.e., whether as some unusual tropical ­species should be in a new 630 B Butterflies and Moths (Lepidoptera) family or subfamily, etc., rather than integrating it Denmark. Some of the most primitive of butterflies within existing groups. Yet, since most of the bio- still extant, like in the genera Baronia (Papilionidae) diversity of the order is in the tropics, much study from Mexico and Calinaga (Nymphalidae) from is still needed for many ­Lepidoptera groups, and Asia, resemble some of the ancient fossil butter- especially so on their biologies and immature flies. Evidence of larval feeding is also known in stages. One can note below in the biodiversity sec- fossils, as for example, from leafminers. Because tion how many entire families remain completely almost all Lepidoptera are plant feeders, there has unknown biologically. necessarily also been considerable adaptation to various plants, what we now consider as insect- plant coevolution. Evolution The evolution of Lepidoptera lineages to the extant families we have today was undoubtedly Lepidoptera are known as fossils from at least as very reticulate, rather than a simple linear pro- far back as the Lower Jurassic; thus, the split from gression, and this is evident in our classification Trichoptera-like relatives undoubtedly occurred as well. For example, among Ditrysian groups already much earlier. However, fossils of lepi- the families are not related in the sequential dopterans are not as common as they are for other manner they are listed on paper, but rather they insect orders, so the evolutionary record is little represent progressions from ancestral divisions documented. The greatest number of fossil that evolved like branches on a tree. Thus, there ­Lepidoptera are known from amber, particularly remain today in each division both primitive Eocene aged Baltic amber and the younger elements (e.g., those with spined pupae) and Dominican amber from the Caribbean. There are advanced groups. One can see the ­relictual also considerable numbers of Oligocene lepi- groups in the basal families of the main divi- dopteran fossils known from rocky sediments, like sions, as in the first listed families in Tineoidea, from Florissant, ­Colorado, from Tertiary sedi- Sesioidea, Cossoidea and Calliduloidea, while ments in Italy and other parts of Europe, and from advanced families are present in each division as late Jurassic layers from Central Asia, among oth- well, each with some advanced features yet in ers. Most all known fossil Lepidoptera have been ­different lineages than what led to the most found in the Northern Hemisphere, and only a few advanced, the Noctuidae. are known from the Southern Hemisphere, but this may well be the result of more searching in Europe and North America than has been done south of the equator. Characteristics The older fossil lepidopterans are all of the kind of species now found in the most primitive All Lepidoptera have a complete, holometabolous families, such as the mandibulate Micropterigidae life cycle, with separate egg, larva, pupa, and adult and other homoneurous groups of primitive stages. The morphology of the lepidopteran adult ­Lepidoptera. The oldest known lepidopteran fossil and immature stages have been extensively studied, is from Lower Jurassic layers from England, named with some of the larger species, like some of the Archeolepis mane. Primitive Hepialidae have been large hawk moths (e.g., Manduca sp., Sphingidae) found in Palaeocene British limestone and mid- and emperor moths (e.g., the North American Miocene Chinese deposits. Butterflies are most cecropia moth, Hyalophora cecropia, and the well known from deposits found at Florissant, polyphemus moth, Antheraea polyphemus, Sat- Colorado, of Eocene age. An earlier butterfly has urniidae) being used as experimental subjects for been found in Upper Palaeocene deposits in anatomy and physiology studies, due to their Butterflies and Moths (Lepidoptera) B 631 ­availability and large size. The monarch butterfly the genus Itylos from the high Andes of Bolivia (Danaus plexippus, Nymphalidae) has also been and Chile is about 6–10 mm in wingspan, while used as a model for many morphological studies. the genus Micropsyche, from Afghanistan, is about 7 mm in wingspan, and some American Brephid- ium specimens are 6–9 mm in wingspan. Many of Adults the Microlepidoptera are larger than these small ­butterflies. The largest butterflies, such as female Most Lepidoptera are moderate-sized, winged birdwings of Ornithoptera alexandrae (Papilioni- insects, averaging about 30 mm in wingspan. The dae) from New Guinea, are over 280 mm in wing- (Figs. 81 and 82) smallest known species, as small span. Another large butterfly is the African as 2.5 mm in wingspan, are in the pygmy leafminer swallowtail, Papilio antimachus (Papilionidae) family Nepticulidae, while the largest known lepi- where the ­elongated wings of some males attain dopterans are about 300 mm in wingspan, as in 250 mm in wingspan; in this species the females the emperor moth (or giant silkmoth) family (Sat- are smaller in size. urniidae). The largest moths among these Saturni- Lepidoptera typically have four wings and idae include females of the hercules moth scales cover all body parts. Some exceptions occur, (Coscinocera hercules) from Australia, which have whereby various surfaces may be devoid of scales large quadrate wings and a large, heavy body, and (e.g., so-called eyespots or clear spots in some likewise females of the atlas moth, Attacus atlas, and moths and butterflies), but all Lepidoptera have at related species of the genus Attacus of Southeast least some areas of their external body with the Asia; males in these species are somewhat smaller. unique lepidopteran scale structures, or squamae Some of the larger hawk moths (Sphingidae) also (Fig. 83). Trichoptera in rare cases also have some have massive bodies and very thick, strongly veined wing scales, but they typically are hair-like and not wings, as do some of the carpenterworm moths like scales among lepidopterans and do not cover (Cossidae), like the Australian Xyleutes affinis, where other body parts. Most lepidopteran scales are flattened the abdomen in large females attains 70 mm in and ribbed, containing pigments for color. Other length. There also are exceptionally large winged modified scales include androconia, or scent organs, species among the primitive ghost moths, family prevalent in such groups as the monarch subfamily Hepialidae, especially from Australia (e.g., Zelotypia Danainae (family Nymphalidae), where they occur stacyi) and South Africa (e.g., Leto venus), and such as a patch near the central veins of the hindwings. other moth families as the giant butterfly moths Wing scales in such species as Morpho butterflies (Castniidae) and owlet moths (Noctuidae), as well. (subfamily Morphinae, family Nymphalidae) and An owlet moth (Noctuidae) actually has the record the metallic-like spots of some day-flying moths, as wingspan, where some females of the white witch in the metalmark moth family (Choreutidae), have moth (Thysania agrippina) of the Amazon attain the scales modified to refract light, thus producing wingspans of 305 mm, but the largest emperor the brilliant iridescent blues seen in male Morpho moths (Saturniidae) have an overall larger wing area butterflies. Many species also have specialized scales due to their quadrate wing shape. that reflect patterns of ultraviolet light, which wave- Butterflies also average about 30 mm in wing- lengths are in the main spectrum that Lepidoptera span, since even though many are large sized, there actually see. Consequently, the UV pattern of many are a great number of smaller species, particularly lepidopteran wings is very different than what we among the skippers (Hesperiidae), and also the see as their coloration in white light, and the UV blues and hairstreaks (Lycaenidae). Butterflies pattern is what is actually being used as visual cues range in size from less than 7 mm in wingspan to over in mating behavior which may isolate related species. 280 mm. Among the smallest blues (Lycaenidae), Lepidopteran UV patterns have mostly been studied 632 B Butterflies and Moths (Lepidoptera)

Butterflies and Moths (Lepidoptera), Figure 81 Lepidopteran head and associated structures: 1. Head morphology (after Hodges, 1971); 2. Lepidopteran morphology; 3. Head details showing eye cap (after Hodges, 1971); 4. Haustellum (galea), with inneraspect of right maxilla (left) and outer aspect of left maxilla (right); 5. Head scaling, rough (Tineidae) (after Falkovitsh and Zagulajev, 1978); 6. Head scaling, smooth (Gelechiidae) (after Falkovitsh and Zagulajev, 1978); 7. Antennal types: (a) filiform (Eriocraniidae), (b) pecti- nate (Hepialidae), (c) bipectinate (Saturniidae), (d) club-hooked (Hesperiidae), (e) clubbed (Papilionidae), (f) thickened (Sphingidae) (after Zerny and Beier, 1936–38). Butterflies and Moths (Lepidoptera) B 633

Butterflies and Moths (Lepidoptera), Figure 82 Lepidopteran wings: 1. Wing regions (after Hodges, 1971); 2. Wing locking mechanisms: Sesiidae double fold (after Heppner and Duckworth, 1981), (a) jugum (Hepialidae), (b) female frenulum and retinaculum (Sphingidae), (c) male frenulum and retinaculum (Sphingidae) (a–c, after Tillyard, 1926), 3. Wing venation, leafminer (Lyonetiidae) (after Seksjeva, 1981); 4. Wing nomenclature (after Hodges, 1971); 5. Wing venation (Brachodidae) (after Heppner, 1981); 6. Lepidopteran wing scale (after Spuler, 1910). 634 B Butterflies and Moths (Lepidoptera)

Butterflies and Moths (Lepidoptera), Figure 83 Lepidopteran scale morphology (after Ghiradella, 1998): (a) scale ridges may be modified as lamellae for interference coloration (e.g., Morpho wings); (b) flats between ridges may be elaborated to produce Tyndall blue coloration (e.g., some Papilio sp.); (c) lamellae of complex ridges may be shaped to produce reflective coloration (e.g., for metallic-like spots); (d) inter-ridge microribs may have reduced window-like shapes; (e) flats between ridges may be plate-and-pore configuration (e.g., in androconial scales of Pieridae); (f) scale interiors may have body-lamellae to produce thin-film interference colors; and (g) scale interior may be filled with crystallite lattices that produce diffraction colors. (© Ghiradella, 1998; used with permission from author and John Wiley & Sons, Inc.) Butterflies and Moths (Lepidoptera) B 635 in butterflies and not in moths, nor even in day-flying within some species. The more advanced groups moths, but of course all lepidopteran wing macula- display venation that is more reduced in the ­number tion is only seen in UV by the mates, other species, of veins in the hindwings. Some moths, particularly and other insects. While most lepidopteran scale the tiny leafminer groups (e.g., Nepticulidae, Oposte- colors will fade after some time exposed to light, gidae, Tischeriidae, Heliozelidae, Gracillariidae, the structural colors of the modified scales will not Bucculatricidae, among others), often have greatly fade over time. Most lepidopteran colors are pigment­ reduced venation in both fore- and hindwings. In based within the scales, but some is structural. In the homoneurous venation, the fore- and hindwings yellow and white butterflies, family Pieridae, some of have similar venation, while more importantly, the the coloration is from excretory deposits. Color hindwing is “locked” to the forewing in flight by ­patterns in Lepidoptera have been the subject of what is called a jugum, rather than the more evolved extensive studies, especially for butterflies, but also and complicated frenulum and retinaculum for some of the moths. ­wing-locking mechanism of the advanced families Lepidopteran wing shapes can vary consider- of Lepidoptera. The most highly evolved wing-­ ably, although the typical form is of four similar locking mechanism is found in most clearwing wings, with the forewings usually larger than the moths, family Sesiidae, where there is not just a hindwings. Some unusual species have the hind- frenulum-retinaculum arrangement but the entire wings greatly reduced in a few cases, or extremely mesal margins of the fore- and hindwings are narrowed as in the Old World tropical burnet-like recurved to interlock. Butterflies have a humeral moths of the family Himantopteridae (superfamily lobe wing-coupling mechanism. Zygaenoidea) and the Amazonian Copiopteryx Body structure in Lepidoptera adults includes moths (Saturniidae). There are a few rare examples a head, thorax and abdomen, as in other insects, where the hindwings are almost completely but all covered in lepidopteran scales. The head ­atrophied (e.g., some wasp moths, subfamily usually has large compound eyes and prominent ­Ctenuchinae, family Arctiidae), and likewise even labial palpi (one tropical Asian family, the Amphi- for the forewings among a few brachypterous theridae, has the compound eyes of males split in ­species. For typical lepidopterans there also are a half). Labial palpi typically are 3-segmented and variety of wing shapes that are encountered, from the upcurved, but great variation exists in ­different more average shape as found in most Noctuidae, for Lepidoptera families. Maxillary palpi, contrast- example, to the tailed hindwings of swallowtails ingly, are mostly small or even vestigial (sometimes (Papilionidae), or very pointed wings as in some absent), while the most primitive groups have tropical burnet moths (Zygaenidae), or the split 5-segmented maxillary palpi. Lepidoptera have wings found in plume moths (Pterophoridae), and sucking mouthparts as adults, except for the most the even more split many-plumed moths (Aluciti- primitive families (Micropterigidae, Agathip- dae), where each wing vein is separated. Many of hagidae, and Heterobathmiidae), which have the Microlepidoptera have very long hair-like fringe retained mandibular mouthparts (Eriocraniidae scales along the wing edges, particularly on the have a reduced haustellum and vestigial mandi- hindwings, as in Gelechioidea families and many bles). The proboscis, or tongue of typical adult of the leafminers in particular. ­Lepidoptera, more correctly termed a haustellum, Wing venation in Lepidoptera has been used is composed of two parts (galeae) that interlock to for classification since the time of Linnaeus. Most form a sucking tube, usually curled between or families have wing venation that can help to identify beneath the labial palpi. While some moths have them, although we now also use many other the haustellum greatly reduced and very short ­characters of the body that often are more reliable, (even vestigial or absent in some non-feeding since wing venation can vary to some extent even ­Saturniidae, for example), some moths and 636 B Butterflies and Moths (Lepidoptera) ­butterflies have a very long haustellum, possibly families. The usually 5-segmented tarsi have two developed to reach nectar sources in long-stemmed hook-like tarsal claws on the last segment. The flowers. The longest known haustella are in some main thoracic structures of Lepidoptera, however, hawk moth (Sphingidae) species, where lengths of are the enlarged wings of most species. Brachyp- up to 30 cm are known. terous species were already mentioned earlier, but The lepidopteran head has various other most Lepidoptera have well developed wings for structures (or lack thereof) in different families, all active flight. Some females, however, are flightless of which are in part used to define the various and without wings, particularly in the family families, as for example, ocelli and chaetosemata ­Psychidae, and some species of geometer moths sensory organs near the antennal bases, and (Geometridae) and tussock moths (Lymantriidae). ­maxillary palpi: these vary in different families In the bagworm moths, family Psychidae and sometimes are atrophied or even completely ­(Tineoidea), the females are even larviform and absent. The antennae also vary among different remain within the larval shelter and cocoon as families, or even among different genera within a adults, waiting for the winged males to find them. family, with short or very long antennae. Although Like many Lepidoptera, the female bagworm moths moths typically have antennae of many segments emit a pheromone to attract the males. Among the that extend to fine points and butterflies have emperor moths (Saturniidae), even faint phero- antennae with terminal knobs or clubs, there are mone scents have been shown to attract males from exceptions among some moths (e.g., agaristine up to 20 miles downwind from a female. Noctuidae and Castniidae have clubbed antennae) The abdomen of adult Lepidoptera is typi- and even many skippers (Hesperiidae) have curved cally elongated, composed of up to ten segments, clubs that also resemble some moth antennae ­usually with the basal segment and the most dis- (e.g., Sematuridae and Uraniidae). Very long tal ­segments very reduced. The distal segments antennae are typical of the small long horned fairy also usually are reduced to integrate with the moths (family Adelidae), and some others like the genitalic attachments (Fig. 84). The main charac- Asian double eye moths (family Amphitheridae) ters of lepidopteran species identification involve and most of the tropical longhorned moths ­(family the usually complex genitalia of male and female Lecithoceridae). Antennal structure also varies adults. Lepidoptera have some of the most com- considerably, from simple form to complex bipec- plex genital structures of any insect group, both tinate antennae (even quadripectinate) as found in the males and the females. Some of the more in many emperor moths (Saturniidae), or greatly bizarre examples of Lepidoptera genitalia involve thickened as in most clearwing moths (Sesiidae) such things are complicated spines and setae of and hawk moths (Sphingidae). The antennae of males, plus variously shaped claspers, and in male Saturniidae are particularly complex and some females the amazing elongation of the attuned to dedect faint pheromone plumes from ductus bursae into an extremely long, thin and females. convoluted tube, as in some Choreutidae (espe- The thorax of adult lepidopterans has the cially the genus Brenthia). In Gelechiidae, many usual three pairs of thoracic legs, also covered with of the species have asymmetrical male genitalia, scales. Butterflies of the family Nymphalidae where one clasper is larger than the other. Among ­typically use only the posterior two pairs of butterflies, the parnassians ­(subfamily Parnassii- ­thoracic legs for walking, although they possess all nae, Papilionidae) and also some Acraeinae three pairs of legs. The tibiae and femora usually (Nymphalidae), have the strange trait of the male have spurs on the end of the segment and this has adding a post-copulatory plug or covering (called been used to classify various families, particularly a sphragis) to the female abdomen, preventing the tibial spurs, which vary in number in different further mating by the female. Butterflies and Moths (Lepidoptera) B 637 Larvae horned devil, which is the larva of the American regal moth (Citheronia regalis, Saturniidae). Some While adult Lepidoptera present a large array of hawk moth larvae, or hornworms (Sphingidae) characters used in classification, the larvae have a can also be very large, as well as some of the larger completely different set of characters (Fig. 85). In carpenter worm larvae (Cossidae). Leafminers, fact larval classification often conflicts with trends contrarily, are among the tiniest of Lepidoptera one finds in adult classification. Lepidopteran larvae. The vast majority of Lepidoptera, however, ­larvae have mandibles for chewing, and are unique remain unknown biologically and their larvae in having specialized abdominal legs, called prolegs, have never been seen or studied, nor are their which usually have ventral hooked setae called hostplants known. Thus, much research remains crochets. While the similar appearing sawflies to be done on Lepidoptera larvae and their bio­ (Symphyta), in the Hymenoptera, are also caterpillar- logies. It can be noted here that even such large like, they do not have the lepidopteran crochets moths as the white witch moth, Thysania agrippina and also have too many prolegs, usually 6–7 pairs (Noctuidae), mentioned earlier as the species with plus the rear pair, while Lepidoptera typically have the largest known wingspan of any lepidopteran, only four pairs of prolegs plus a rear pair. The only remains completely unknown biologically, and known exceptions with supplemental prolegs in that even though the adults are commonly attracted Lepidoptera occur in one of the families of slug to lights in the Neotropical lowland jungles. caterpillars, Dalceridae, where late instar larvae Proposed phylogenies based on adults often are have six pairs of rudimentary prolegs. Contrarily, not substantiated when larvae are compared, and reduction exceptions are more common, where this often is the cause of taxonomic argument among larvae have fewer prolegs in unusual cases, as in specialists, particularly for those unfamiliar with lar- some Noctuidae and most Geometridae where vae or who do not study larvae but instead rely only there usually are only a single pair of prolegs plus on adult characters. The kind of ­controversies that the rear pair. Most leafminers also have evolved arise between larval taxonomy and adult taxonomy, proleg reduction and even thoracic leg reductions, where the adult taxonomists may not know the lar- like in Gracillariidae and Nepticulidae, where the vae very well or even ignore their characters, can be minute larvae have three or fewer pairs of vestigial seen in the Noctuidae, where a recent larval work for prolegs, or are almost devoid of recognizable European owlet moths has different conclusions for ­prolegs (the feeding style inside of leaves has pro- many of the subfamilies from what those studying duced the evolutionary reduction of the unneeded only adult characters have published. legs in these cases). Likewise, most of the slug-like Since Lepidoptera larvae spend most of their caterpillars (e.g., Zygaenoidea, Limacodidae, and time feeding in microhabitats far different than Megalopygidae) utilize the entire ventral body their adults prefer, larval features are often attuned surface as a moving platform, much like slugs do, to their needs with very specific body characters. such that the prolegs are often reduced to mere Thus, larvae that feed inside plants usually have bumps on the body. reduced setae and smaller legs than do those that Lepidoptera larvae have their own set of feed externally on plants. Some bizarre shapes and ­characters, in particular the array of head and life styles are known among Lepidoptera larvae. body setae and spines that can be mapped (called For example, the only known aggressively carnivo- chaetotaxy) and usually are diagnostic for particu- rous lepidopteran larvae occur in Hawaii: species lar families. Many species can be identified by their of the genus Eupithecia (Geometridae) capture larvae, but only for those where the larvae are flies as food using massive, modified tarsal claws. known and have been studied. Some caterpillars A few other moth larvae are also carnivorous are extremely large and grotesque, like the hickory on aphids and scale insects, like in the genus 638 B Butterflies and Moths (Lepidoptera)

Butterflies and Moths (Lepidoptera), Figure 84 Lepidopteran reproductive structures and eggs; 1. Female genital morphology (after Hodges, 1971); 2. Typical lepidopteran eggs: upper left) Noctuidae (Amathes), upper right) Notodontidae (Hoplitis), second row left) Notodontidae (Phoesia), second row right) Noctuidae (Naenia), third row left) Lycaenidae (Thecla), third row right) Nymphalidae (Limentis), bottom row left) Noctuidae (Spodoptera), bottom row right) Zygaenidae (Zygaena) (after Zagulajev, 1978); 3. Male genital morphology (two types), with detail of typical aedeagus (after Hodges, 1971). Butterflies and Moths (Lepidoptera) B 639

Butterflies and Moths (Lepidoptera), Figure 85 Lepidoptera larvae: 1. Larval morphology, with details of crochets and proleg (after Chapman, 1969; and Mellis and Zocchi, 1958); 2. Larval head morphology (after Common, 1970); 3. Typical lepidopteran larval types: (a) Hepialidae, (b) Tortricidae, (c) Noctuidae, (d) Geometridae, (e) Pyralidae, aquatic (Nymphulinae), (f) Gracillariidae (late instar), (g) Gracillariidae (early instar, Phyllonorycter), (h) Sphingidae) (a-d, after Tillyard, 1926; e, after Bourgogne, 1951; f-g, after Patocka, 1980; h, after Lutz, 1935).

Pyroderces (Cosmopterigidae), but they do not primitive genera in Lycaenidae, where ­larvae feed capture winged insects in rapid attacks like the on ant larvae yet are tolerated by the ants they larvae in Hawaii. Carnivorous butterfly larvae are live with because of the secretions the larvae give known in the Asian genus Liphyra, one of the more the ants. 640 B Butterflies and Moths (Lepidoptera) Eggs Euchloe (Pieridae), Parnassius (Papilionidae), and Erebia (Nymphalidae)), where living larvae (usually Lepidoptera eggs usually are rounded and ­relatively only one) are present in the oviduct of the female small (about 1 mm), but some groups have flattened and presumably remain there until the female dies, eggs, as for example among the Tortricidae (Fig. 84). as no actual deposition of living larvae has been Many butterfly eggs are upright and ribbed. All witnessed in butterflies. ­Lepidoptera eggs have a tough shell, called the cho- rion, plus various degrees of external sculpturing and usually four sperm entry holes, or micropyles Pupae (up to 16 in some Notodontidae). The largest lepi- dopteran eggs are found among some of the The pupal stage varies in form (Fig. 86), from those emperor moth ­species (Saturniidae) and hawk with loose legs, as in the primitive moths such as Eri- moths (Sphingidae), up to about 4 mm in diameter ocraniidae, to the most advanced groups where the (e.g., 4 mm in Argema mittrei and 3.2 mm in Attacus legs of the future adult are fused to the pupal shell. crameri, Saturniidae). Many of the primitive families, as also Tortricidae Eggs usually are laid singly or in groups and Sesiidae for example, have noticeable dorsal directly onto host leaves or stems, but some moth spines on the abdomen of the pupa, used to help females insert the eggs into plant tissues using a the pupa wiggle out of the cocoon when the adult very strong ovipositor, particularly among the emerges. Most Lepidoptera pupae have a cremaster more primitive moths (e.g., Eriocraniidae). The of strong spines or protrusions at the distal end of average lepidopteran female lays about 100–200 the abdomen. Some of the Microlepidoptera pupae eggs. Species with the greatest numbers of eggs per have only thin hooked setae as a ­cremaster-like female are known among the ghost moths (Hepi- structure. While most Lepidoptera larvae spin a alidae), where some females have been recorded cocoon before transforming into the pupal stage, with close to 50,000 minute eggs: these moths spray many groups have an exposed pupa, as in most their eggs randomly about while ­flying over likely butterflies and some advanced moths like Noctui- hosts, leaving it to the young ­caterpillars to find dae. While most pupation and cocoon-making is their hostplants to feed on upon hatching. on the hostplant, many pupate among debris or in Although no lepidopteran has been discov- the ground, as for example most of the hawk moth ered where the adults care for eggs or larvae, as is larvae (Sphingidae) make a pupal cell in soil, from known in some beetles, many lay their eggs in which the adult must burrow upwards to escape by secretive sites or devise other protective solutions, means of temporarily retaining the hard pupal and some species have developed protective com- head covering to push through the soil. The leaf- mensal relationships with other insects. A notable miners pupate within their leaf mine for the most case involves the blue butterflies (Lycaenidae), part. Many butterflies simply hang their pupae where ants typically tend to the larvae and protect upside down from the cremaster plug of silk the them from predators and parasitoids while getting larva spins just before pupation. Some ­butterfly desirable secretions from the larvae. Ovovivipary, larvae (mainly Papilionidae) spin a silken girdle for however, is known in a few groups of lepidopterans, the pupa (also in Hedylidae and some Geometri- notably a few Tineidae, Psychidae, Coleophoridae, dae), thus keeping it upright at the pupation site. and Cosmopterigidae. Psychidae in particular Bagworms (Psychidae) pupate within the larval have numerous species that are parthenogenetic. shelter (or bag), and likewise for such ­families A modified form of this phenomenon is known as the casebearer moths (Coleophoridae) and among some butterflies (e.g., some Colias and some sackbearer moths (Mimallonidae). Most leaf Butterflies and Moths (Lepidoptera) B 641

Butterflies and Moths (Lepidoptera), Figure 86 Lepidoptera pupae: 1. Pupal morphology (after Urguart, 1960), and typical forms: (a) Eriocraniidae, (b) Opostegidae (front and back), (c) Psychidae, (d) Elachistidae, (e) Pyralidae, (f) Pterophoridae (front and side), (g) Papilionidae, (h) Pieridae, 1951), (i) Lycaenidae, (j) Nymphalidae, (k) Hedylidae, (l) Sphingidae, (m) Dioptidae (front and back), (n) Noctuidae (a, e, after Patocka, 1980; b, after Davis, 1989; c, l–n, after Mosher, 1916; d, after Falkovitsh, 1981; f, after Zagulajev, 1986; g–i, after Bourgogne, 1951; j, after Tillyard, 1926; k, after Scoble and Aiello, 1990). 642 B Butterflies and Moths (Lepidoptera) webbers, leaf tiers, and leafrollers pupate within the moths (Saturniidae) which have large bright larval shelter (mostly in the families Oecophoridae, ­eyespots on the hindwings, use startle techniques Gelechiidae, Pyralidae, and Tortricidae). to evade predators, since these moths will flash their hindwings when distrubed from their ­normal resting positions where the hindwings are hidden Ecology beneath the more camouflaged coloration of the forewings. Butterflies use eye spots for startle effects Lepidoptera biology includes many strange behav- as well, as for example among the owl butterflies ioral traits and biologies that have evolved in of the genus Caligo (Brassolinae, Nymphalidae) of ­different groups and species.Whereas most the American tropics, and even such species ­lepidopterans have rather drab colors that lend as the European peacock butterfly, Inachisio themselves to good camouflaging when at rest on (Nymphalidae). leaves or trees, other species have adopted bright Other species, both moths and butterflies, coloration or startle techniques for protection. use bright coloration not for startle effects but as Butterflies, of course, as some day-flying moths, warning colors. One of the reasons the warning use bright coloration or color spots for mating colors are recognized by predators is that the behavior as well. For example, the bright blues of bodies of these Lepidoptera (or other insects) the morpho butterflies (Morphinae, Nymphalidae), contain ­alkaloids their larvae have embibed from already mentioned for their scale structure, are their hostplants, and thus the adults are poison- used by males to keep other males away from their ous to most predators like birds and frogs. For territories, while females may also respond to the example, monarch butterflies (Danaus plexippus, bright coloration during mating rituals. Likewise, Nymphalidae) and relatives contain poisonous the bright coloration of morpho butterflies also alkaloids (heart poisons for predators), and most involves startle defense, since roosting males will birds will not eat the adults once they learn that congregate on a branch and, when disturbed, flash brightly ­colored insects are distasteful. Likewise, their blue colors together (the “flash and dazzle” for such moths as the very colorful flag moths, defense), probably scaring away many predators in subfamily Pericopinae (Arctiidae), which are this way. The morpho flight pattern, a rather believed to all be poisonous as well, due to bodily ­bouncing kind of rapid flight in males, also makes alkaloids. Such moths as Zygaenidae, which are it difficult for predators to find them on the wing, mostly also very colorful, have phytocyanides in since the blue color flashes only every few seconds their bodies. Some adults of various Lepidoptera or so as the butterfly flaps its wings when flying groups also imbibe plant chemicals from nectar through the forest, thus showing only intermit- sources. tantly where the butterfly is at any instant.­However, A varied group of lepidopterans have evolved some birds have learned how to capture them the use of various plant poisons (mostly alkaloids, ­anyway. Some butterflies, especially among the glycosides, phytocyanides, and cardenolides) as hairstreaks (Lycaenidae), use their hindwing tails defensive agents. Monarch butterflies (Danainae, as “false heads” to confuse predators, and many of Nymphalidae), as already noted, sequester alkaloids the other tailed butterflies may have developed from their hostplants, milkweeds (Asclepiadaceae) tails for this purpose as well, and likewise for some by the feeding of their larvae. Burnet moths of the diurnal tailed moths (e.g., Sematuridae and (Zygaenidae) and Heliconius butterflies (Heliconiinae, Uraniidae). Nymphalidae), among others, do the same for plant Among the moths, eye spots are well known cyanides, as already noted for larval defense. In the markings among those species that are not com- case of the burnet moths, the adults are even some- pletely colored for camouflage. The many emperor what resistant to the fumes of cyanide gas, since Butterflies and Moths (Lepidoptera) B 643 they will survive in a cyanide vial much longer than toxic models known in Lepidoptera, and many any other Lepidoptera can. Many of these and other appear and behave so much like true wasps that on traits in Lepidoptera have evolved as defensive the wing one cannot be sure what they are. All measures against birds and other predators, and these kinds of cases involve what is called Müllerian parasitoids. There are also many other forms of mimicry, where the mimic has a clear benefit by defense that lepidopterans use, such as death looking like the model. There is also simple mimicry, ­feigning (e.g., many emperor moths will do this if called Batesian mimicry, where the mimics look disturbed), and excretion of alkaloids from wing like various models and each other, but there is no bases or abdominal glands (e.g., many Arctiidae do apparent benefit evident like that of having a this, especially in Pericopinae and the wasp moths, ­poisonous model. However, there may be some subfamilies Ctenuchinae and Syntominae). Addi- benefit to mimicking a color pattern that has been tional adult defenses include such things as loud found to be advantageous for some reason. For noises, as are found in some brush-footed ­butterflies example, there is a large mimicry complex of swal- in the genus Hamadryas (Nymphalidae), where the lowtail butterflies (Papilionidae) and swallowtail adults make a clicking or crackling sound when moths (Urania, Uraniidae) in the Neotropics, yet they fly, possibly scaring bird predators in this way. where none of the possible models are poisonous Mimicry with other insects and among each but do all have variegated patterns of striped green other is a further use of color and maculation as and black. Likewise, there is a similar mimicry part of defense strategies in Lepidoptera. Mimicry complex in New Guinea involving blue Uraniidae among Lepidoptera involves various species (genus Alcides) and several swallowtail butterflies ­looking similar to one or more that are poisonous (Papilio laglaizei, P. u ly ss es , and P. pericles, and even by their bodily alkaloids, as noted earlier. Thus, a P. woodfordi), where all have bands or patches of poisonous tiger moth (Arctiidae), or butterfly like blue color surrounded by black bands. the monarch, is the model that other lepidopterans Although most Lepidoptera larvae use cam- have taken the appearance to obtain the same ouflage for protection, others use startle effects or defensive protection yet without themselves being bright coloration as a protective strategy, much as poisonous. For example, in the case of the monarch do some adult lepidopterans. For example, the there is the well known North American mimic, bright colors of some hawk moth larvae such as the Viceroy butterfly,Limenitis archippus (Nymph- the giant gray sphinx of the Neotropics, also called alidae), which itself is not distasteful or poisonous the frangipani sphinx (Pseudosphinx tetrio, Sphin- to birds and other predators. Extensive mimicry gidae), where the large larvae are banded in bright complexes occur, particularly in the tropics, yellow and black, with an orange head, are thought ­especially modelled around some of the flag moths to possibly mimic coral snakes, since they also (subfamily Pericopinae, family Arctiidae). Like- move their bodies rapidly when disturbed and will wise, there are also mimicry complexes modelled even “strike” at a predator like a snake. Some make after other insects that are avoided by birds and noises if disturbed, as for example in the death- other predators, such as polistine wasps (Vespidae, head sphinx, Acherontia atropos (Sphingidae), Hymenoptera) and stink bugs (Pentatomidae, mentioned earlier for its adult noises, which also Hemiptera). Thus, we find many so-called wasp makes noises in the larval stage using its mandibles; moths, subfamilies Ctenuchinae and Syntominae and likewise for some Saturniidae larvae and (family Arctiidae), that appear remarkably like real others. Even some larvae among the Microlepi- species of wasps, plus other moths both among doptera make noises when disturbed, as for example Arctiidae and Pyralidae that have modelled them- in the larvae of Diurnea fagella (Oecophoridae), of selves after some bugs or beetles. The wasp moths Europe, where larvae scrap their claws on a leaf include mimics that are among the most precise to surface. Pupal noises are also known among some 644 B Butterflies and Moths (Lepidoptera) lepidopterans. Some Lepidoptera pupae also can are also irritating in some cases. Even deaths have make rasping sounds by moving their abdominal occurred by persons in the tropics from contact segments together. with some caterpillars of the emperor moths Larval defense also takes on the form of ­(Saturniidae), especially the Brazilian Lonomia sp. ­ferocious appearance and head movements, as for (even the adults in this group have irritating wing example in the large hickory horned devil, scales). The larvae of this genus have poison glands ­Citheronia regalis (Saturniidae), of North America, that inject a chemical, when touched, that triggers which not only has large spined horns but will rear human blood coagulation problems and also its head swiftly back to hit anything that grabs its ­haemorrhagic reactions in some cases, thus ­causing body. A number of tropical hawk moth larvae some of the reported deaths in Brazil. Another (Sphingidae) rear up when disturbed and retract potent genus among the emperor moths, both for their head into a large thorax, while thoracic eye larval poisonous spines and irritation from adult spots make them then appear like snake heads. scales, is Hylesia (Saturniidae). These so-called One of the most accurate snake mimics, or “viper stinging caterpillars are well protected in this way worms,” is the larva of the Neotropical hawk from most predators, but still can be subject to the moth, Hemeroplanes ornatus (Sphingidae). As with tiny parasitoid wasps that can insert their eggs adults, some larvae also have poisonous alkaloids between larval spines, or circumvent their defenses as defensive measures that back up their bright by getting to the egg stage instead. ­colors, as in the wasp moths (Ctenuchinae) of the The topic of stinging caterpillars is called lepi- American tropics and their Old World cousins, dopterism in the medical profession, and deals wasp moths in the subfamily Syntominae (family with allergic reactions to certain poisons. The genus Arctiidae), and the American flag moth larvae Lonomia is part of the New World subfamily (subfamily Pericopinae), for example, where larvae Hemileucinae (Saturniidae) and most all of these can also be colorful. have poisonous spines, as for example the io moth Some larvae also make use of defense in num- (Automerisio) of North America and the several bers, thus feeding in large masses so any predator hundred species in this group from South America. finding them will undoubtedly still enable some to The slug caterpillars, families Limacodidae and escape: for example, many of the tent caterpillars Megalopygidae, are likewise well known for their (Lasiocampidae) feed in large masses and make poisonous spines. Some stinging caterpillars even tent protective webs as well. The same massing spin the left over spines from their larval skin into behavior is also known in other lepidopteran their cocoon and protect the cocoon in this way as ­larvae, like the processionary caterpillars of the well, as for example in the Lonomia moths from subfamily Thaumetopoeinae (Notodontidae), Brazil. Lepidopterism is also known in other famous for traveling in a long single file when ­families, even in the Australian Anthelidae, where moving from one host tree to another, both in contact with cocoons of one species can cause Europe and in tropical species of the group. The allergic reactions due to urticating setae. unusual tropical Himantopteridae (Zygaenoidea) Commensal relationships among larvae, where also congregate as masses of larvae. some benefit is obtained from the interaction with Other larval defenses include poisonous setae, another insect, is a further form of protection for which can be very potent for persons particularly some lepidopterans. Many blues and relatives allergic to the “stings.” There are a number of such (Lycaenidae) have commensal relations as larvae stinging caterpillars in North America, as also in with ants, so-called myrmecophily. The larvae other faunal regions, particularly in the moth obtain protection from predators and even parasi- families Limacodidae, Megalopygidae, and Sat- toids in many cases, and the ants obtain wanted urniidae. Setae of tussock moth larvae (Lymantriidae) secretions from the larvae, much like we do with Butterflies and Moths (Lepidoptera) B 645 milk cows. Some metalmark butterflies (Riodinidae) Asia, fly in the late afternoon and at dusk, while also have myrmecophilous larvae. during most of the day they are to be found at rest Flight is what is most typical of Lepidoptera, in dark thickets in the forest. Likewise, many moths besides their often colorful wing maculation. will fly only in the evening hours before midnight, Some groups, like the clearwing moths (Sesiidae) while some fly only before dawn. Some moths are and hawk moths (Sphingidae), have developed also diurnal and like butterflies, have particular very strong wings used for often exceedingly fast flight periods, as before noon (e.g., most Sesiidae), flight. Among the fastest known lepidopterans are or at dusk only (most Hepialidae, and some Sphin- some in the family Sphingidae, especially in some gidae and Saturniidae). Crepuscular moths also of the day-flying species, where flight speeds to include some of the giant butterfly moths (family 35 mph are known. While most lepidopteran flight Castniidae) of the Neotropics, Australia, and is rather slow, with slowly flapping wings and some Southeast Asia, and also a large number of leafro­ gliding, the fastest fliers and hoverers have exceed- ller moths (family Tortricidae). The Hedylidae, ingly rapid wing beats. For example, the hawk which some consider nocturnal butterflies but are moths (Sphingidae) typically fly like humming- herein retained in Geometroidea, fly at night. All birds and can hover in place while feeding on the above is likewise true for larval feeding activity flower nectar. Butterflies can hover at nectar among various groups, with some feeding only at sources to some extent as well, by flapping their night and others at various times, or only during wings, but only hawk moths have the excessively daylight. rapid wing beat that allows hummingbird-like For adults, there is also specialized flight, steady hovering in place. Even within one family besides searching for food or mates, like directed flight behavior can vary considerably among migration, as exhibited in such species as the mon- ­different genera, as for example, in Saturniidae, arch butterfly (Danaus plexippus, Nymphalidae) where most have rather slow lumbering flight in their migrations in North America to spend behavior, yet in the American genus Hemileuca the winter months in Mexico. Western North American day-flying males can rival hawk moths in speed of monarchs overwinter in coastal California. Related flight. Likewise, male yucca skippers (Megathymi- danaines on Hispaniola, of the genus Anetia nae, family Hesperiidae), mostly in the American (Nymphalidae), congregate in the higher elevations Southwest, also typically fly very fast in search of of the Dominican Republic. There are many other females. Of course, flight in Lepidoptera has been migratory species recorded, and in all faunal studied extensively, and particularly how this regions. For example, some owlet moths (Noctuidae) relates to adult mating behavior and migration in Australia and Europe, snout butterflies (Libyt- in butterflies. heidae) in North America and Africa, and black Activity regimes among Lepidoptera vary as danaines (Euploea spp., Nymphalidae) in Taiwan, much as other features of their life histories. While which overwinter in secluded areas protected from most butterflies are diurnally active as adults and sever frosts, like the North American monarchs most moths are nocturnal, there are many excep- do. Hawk moths and owlet moths migrate over tions. Many butterfly species have particular times mountain passes during certain times of the year of active flight, such as only briefly in the morning in Venezuela, as do some butterflies. Some diurnal or at dusk, or only midday. For example, the moths also have migratory flights, like the migra- ­Neotropical owl butterflies (Caligo, subfamily tions of Urania moths (Uraniidae) in the Neotropics. ­Brassolinae, Nymphalidae), and their relatives, Many other cases of migrating Lepidoptera are typically fly at dusk. The related jungle queen known. Some of the cases of large flights are more butterflies, as in the genus Stichophthalma (sub- seasonal and directed mass movement in relation family Amathusiinae, Nymphalidae) from Southeast to population pressure than they are migration in 646 B Butterflies and Moths (Lepidoptera) the sense of the complex annual two-way migration moths, mainly Noctuidae and some Geometridae sequence as evidenced in the American monarch. and Pyralidae, but also a few Notodontidae and Aggregation is well known with some Thyatiridae, which rest on the edges of the eyes of ­overwintering butterflies, but there also are mass large mammals and suck eye juices from the roostings that some species use during the night, ­surface of the eyes. In the case of the blood ­sucking presumably as protection against predators, species, the haustellum has been modified to pierce although this has not been proven conclusively. skin and suck blood, much as in mosquitoes, a For example, Heliconius butterflies (Nymphalidae) modification from fruit-piercing owlet moths typically roost in large assemblages at night. (Noctuidae), like in the Asian genus Othreis and ­Likewise, for morpho butterflies (Morphinae, the New World Gonodonta. Nymphalidae). Roosting behavior has also been Of all studies on Lepidoptera, besides those on documented in other tropical butterflies as well. butterfly and moth life histories, those pertaining to Few moths have roosting activity like those noted population biology and biogeography of butterflies for some butterflies, and most such cases for moths have probably been the most numerous over the involve resting sites for large groups of adults in years, and include most all aspects of lepidopteran one area but not like the dense roosting biology, from larval food preferences, to genetics, to ­documented for butterflies. For example, one finds mimetic relationships, to seasonality, to taxonomy large numbers of grass loopers, genus Mocis of the species involved. Many such studies world- (Noctuidae), resting together in Florida, which wide, many now classic, can be referenced. Among can be startled into mass flight over short distances the hundreds of examples are the well known stud- when disturbed during the day. Likewise, Nyctemera ies on various checkspot butterflies (Euphydryas sp., tiger moths (Arctiidae) have similar mass startle Nymphalidae) in California and other areas of flight responses in the Oriental tropics when North America. Likewise, studies in North America ­disturbed during the day. Various other owlet for Colorado butterflies and the many recent­studies moths (Noctuidae), geometer moths (Geometridae), on swallowtails (Papilionidae), as well as innumer- and snout moths (Pyralidae) also rest in groups able similar studies in Japan, Africa, and other and fly away in swarms when disturbed during regions. In Europe, one has studies like on blues daylight. Most cases of diurnal moths coming to (Lycaenidae), various other British butterflies, and lights at night are due to being disturbed and then many others. Likewise, innumerable studies have going to the nearest light source. There are also been done on the ecology and population biologies cases of cold adaptation techniques where moths of tropical butterflies. Such studies for moths, how- at high altitudes or during the winter will mass in ever, are much fewer, as for example on European large numbers: for example, there are some owlet pine looper moths (Geometridae) and California moths, genus Euxoa (Noctuidae), that do this oak moths (Dioptidae), to give just a few examples ­during cold nights in the North American Rockies, out of thousands of studies, but mainly on ­economic notably recorded as also being a food source species and their control. for bears. Among some of the other more bizarre behav- ior found among the Lepidoptera, one can note Biodiversity the blood sucking activity of one species of owlet moth in the genus Calyptra (Noctuidae) from The following notes summarize the main Southeast Asia, which attacks large mammals such groupings and the 125 extant families of Lepi- as buffalo, cows and deer. This behavior is appar- doptera in the world. The most primitive moths ently a development of the eye-frequenting (or are discussed together, while more advanced lachryphagous) behavior among other Asian families are treated according to their respective Butterflies and Moths (Lepidoptera) B 647 superfamilies. Families are listed in the table. AGATHIPHAGOIDEA The species totals given for each family have AGATHIPHAGIDAE - Kauri Moths been updated to include all valid species Suborder: HETEROBATHMIINA described to the year 2000. HETEROBATHMIOIDEA The world total number of known species HETEROBATHMIIDAE - Valdivian ­Archaic Moths comes to 156,100 species. An estimated additional Suborder: GLOSSATA 100,000 species remain to be discovered and Cohort: DACNONYPHA named, mainly from tropical regions of the world, Infraorder: DACNONYPHA including many of the most imperiled habitats. ERIOCRANIOIDEA During the decade from 1990 to 2000, about 8,500 ERIOCRANIIDAE - Sparkling Archaic Sun Moths Lepidoptera species were described from all ACANTHOPTEROCTETIDAE - Archaic Sun regions, particularly from remote areas of tem- ­M o t h s perate Central Asia and from the tropical forests Acanthopteroctetinae of Southeast Asia and Central Africa. Thus, the Catapteriginae rate of new discoveries and descriptions of new Infraorder LOPHOCORONINA species remains fairly steady, averaging about 850 LOPHOCORONOIDEA species per year among Lepidoptera. However, LOPHOCORONIDAE - Australian ­Archaic Sun unless larger and more active surveys are made of Moths critical and unknown tropical and other remote Cohort: MYOGLOSSATA regions, and unless the training of more taxono- Subcohort: MYOGLOSSATA mists to study new material is increased, it will Infraorder: NEOPSEUSTINA take another 100 years to complete the basic NEOPSEUSTOIDEA inventory of the remainder of the Lepidoptera NEOPSEUSTIDAE - Archaic Bell Moths not yet identified from among the total extant Subcohort: NEOLEPIDOPTERA worldwide fauna of about 255,000 living species. Infraorder: EXOPORIA Unfortunately, estimates of yearly forest and other MNESARCHAEOIDEA habitat destruction do not leave us 100 years for MNESARCHAEIDAE - New Zealand ­Primitive this inventory to be accomplished in many areas ­M o t h s of the world under the most intense human pop- HEPIALOIDEA ulation and development pressures. And likewise, NEOTHEORIDAE - Amazonian Primitive Ghost the basic inventories to describe all extant species Moths do not involve detailed biological studies to deter- ANOMOSETIDAE - Australian Primitive Ghost mine the life histories of these newly discovered Moths species. Even most of the species already described PROTOTHEORIDAE - African Primitive Ghost remain unknown biologically, so another larger Moths cadre of researchers is needed to study the biolo- HEPIALIDAE - Ghost Moths gies involved. PALAEOSETIDAE - Miniature Ghost ­Moths ORDER: LEPIDOPTERA Infraorder: HETERONEURA Suborder: ZEUGLOPTERA Division: MONOTRYSIA MICROPTERIGOIDEA Section: NEPTICULINA MICROPTERIGIDAE - Mandibulate ­Archaic ANDESIANOIDEA Moths ANDESIANIDAE - Valdivian Forest ­Moths Micropteriginae NEPTICULOIDEA Sabatincinae NEPTICULIDAE - Pygmy Moths Suborder: AGLOSSATA Pectinivalvinae 648 B Butterflies and Moths (Lepidoptera) Nepticulinae Eriocottinae OPOSTEGIDAE - Eye-Cap Moths Compsocteninae TISCHERIOIDEA PSYCHIDAE - Bagworm Moths TISCHERIIDAE - Trumpet Leafminer ­Moths Lypusinae PALAEPHATOIDEA Naryciinae PALAEPHATIDAE - Gondwanaland ­Moths Taleporiinae Section: INCURVARIINA Penestoglossinae INCURVARIOIDEA Psychinae INCURVARIIDAE - Leafcutter Moths Oiketicinae Incurvariinae ARRHENOPHANIDAE - Tropical Lattice Moths Crinopteryginae Series Gracillariiformes CECIDOSIDAE - Gall Moths AMPHITHERIDAE - Double-Eye Moths PRODOXIDAE - Yucca Moths SCHRECKENSTEINIIDAE - Bristle-Legged Moths Lamproniinae DOUGLASIIDAE - Douglas Moths Prodoxinae BUCCULATRICIDAE - Ribbed-Cocoon Maker ADELIDAE - Longhorned Fairy Moths Moths Nematopogoninae GRACILLARIIDAE - Leafminer Moths Adelinae Gracillariinae HELIOZELIDAE - Shield Bearer Moths Lithocolletinae Division: DITRYSIA Phyllocnistinae Section: TINEINA GELECHIOIDEA Subsection: TINEINA OECOPHORIDAE - Concealer Moths TINEOIDEA Depressariinae Series Tineiformes Ethmiinae ACROLOPHIDAE - Tube Moths Peleopodinae Amydriinae Autostichinae Acrolophinae Xyloryctinae TINEIDAE - Fungus Moths Stenomatinae Euplocaminae Oecophorinae Myrmecozelinae Hypertrophinae Harmacloninae Chimabachinae Meessiinae Deuterogoniinae Dryadaulinae LECITHOCERIDAE - Tropical Longhorned Moths Scardiinae Ceuthomadarinae Nemapogoninae Oditinae Tineinae Lecithocerinae Setomorphinae Torodorinae Perissomasticinae ELACHISTIDAE - Grass Miner Moths Hapsiferinae Perittiinae Hieroxestinae Elachistinae Erechthiinae PTEROLONCHIDAE- Lance-Wing Moths Siloscinae GELECHIIDAE - Twirler Moths Stathmopolitinae Physoptilinae Teichobiinae Gelechiinae ERIOCOTTIDAE - Old World Spiny-Winged Moths Pexicopiinae Butterflies and Moths (Lepidoptera) B 649 Dichomeridinae IMMOIDEA BLASTOBASIDAE - Scavenger Moths IMMIDAE - Imma Moths Holcocerinae PYRALOIDEA Blastobasinae HYBLAEIDAE - Teak Moths COLEOPHORIDAE - Casebearer Moths THYRIDIDAE - Picture-Winged Leaf ­Moths Coleophorinae Simaethistinae Batrachedrinae Whalleyaninae MOMPHIDAE - Mompha Moths Argyrotypinae AGONOXENIDAE - Palm Moths Thyridinae Agonoxeninae Siculodinae Blastodacninae Striglininae COSMOPTERIGIDAE - Cosmet Moths PYRALIDAE - Snout Moths Antequerinae Group Crambinina Cosmopteriginae Crambinae Chrysopeleiinae Schoenobiinae SCYTHRIDIDAE - Flower Moths Cybalomiinae COPROMORPHOIDEA Linostinae COPROMORPHIDAE - Tropical Fruitworm Moths Scopariinae ALUCITIDAE - Many-Plumed Moths Musotiminae CARPOSINIDAE - Fruitworm Moths Midilinae EPERMENIIDAE - Fringe-Tufted Moths Nymphulinae Epermeniinae Odontiinae Ochromolopinae Noordinae YPONOMEUTOIDEA Wurthiinae OCHSENHEIMERIIDAE - Cereal Stem Moths Evergestinae GLYPHIPTERIGIDAE - Sedge Moths Glaphyriinae Orthoteliinae Pyraustinae Glyphipteriginae Group Pyralinina PLUTELLIDAE - Diamondback Moths Pyralinae Ypsolophinae Chrysauginae Plutellinae Galleriinae Scythropiinae Epipaschiinae Praydinae Phycitinae ATTEVIDAE - Tropical Ermine Moths PTEROPHOROIDEA YPONOMEUTIDAE - Ermine Moths TINEODIDAE - False Plume Moths Saridoscelinae OXYCHIROTIDAE - Tropical Plume ­Moths Yponomeutinae PTEROPHORIDAE - Plume Moths Cedestinae Macropiratinae ARGYRESTHIIDAE - Shiny Head-Standing Moths Agdistinae LYONETIIDAE - Lyonet Moths Ochyroticinae Cemiostominae Deuterocopinae Lyonetiinae Pterophorinae Bedelliinae Subsection: SESIINA ACROLEPIIDAE - False Diamondback Moths SESIOIDEA HELIODINIDAE - Sun Moths BRACHODIDAE - Little Bear Moths 650 B Butterflies and Moths (Lepidoptera) Pseudocossinae METARBELIDAE - Tropical Carpenterworm Mo- Brachodinae ths Phycodinae Series Limacodiformes SESIIDAE - Clearwing Moths CYCLOTORNIDAE - Australian Parasite Moths Tinthiinae EPIPYROPIDAE - Planthopper Parasite Moths Paranthreninae Epipyropinae Sesiinae Heteropsychinae URODIDAE - False Burnet Moths DALCERIDAE - Tropical Slug Caterpillar Moths Galacticinae Acraginae Urodinae Dalcerinae CHOREUTIDAE - Metalmark Moths LIMACODIDAE - Slug Caterpillar Moths Millieriinae CHRYSOPOLOMIDAE - African Slug ­Caterpillar Brenthiinae Moths Choreutinae Ectropinae ZYGAENOIDEA Chrysopolominae HETEROGYNIDAE - Mediterranean ­Burnet Moths CASTNIOIDEA ZYGAENIDAE - Burnet Moths CASTNIIDAE - Giant Butterfly Moths Zygaeninae Synemoninae Phaudinae Neocastniinae Charideinae Castniinae Chalcosiinae TORTRICOIDEA Anomoeotinae TORTRICIDAE - Leafroller Moths Callizygaeninae Tortricinae Procridinae Chlidanotinae HIMANTOPTERIDAE - Long-Tailed ­Burnet Olethreutinae Moths Subsection: BOMBYCINA LACTURIDAE - Tropical Burnet Moths CALLIDULOIDEA SOMABRACHYIDAE - Mediterranean Flannel RATARDIDAE - Oriental Parnassian ­Moths Moths PTEROTHYSANIDAE - Parnassian ­Moths MEGALOPYGIDAE - Flannel Moths Pterothysaninae Aidinae Hibrildinae Megalopyginae CALLIDULIDAE - Old World Butterfly Moths Trosiinae Griveaudiinae Section: COSSINA Callidulinae Subsection: COSSINA URANIOIDEA COSSOIDEA EPICOPEIIDAE - Oriental Swallowtail Moths Series Cossiformes Schistomitrinae COSSIDAE - Carpenterworm Moths Epicopeiinae Chilecomadiinae APOPROGONIDAE - African Skipper Moths Cossulinae SEMATURIDAE - American Swallowtail Moths Cossinae URANIIDAE - Swallowtail Moths Hypoptinae Uraniinae Zeuzerinae Microniinae DUDGEONEIDAE - Dudgeon Carpenterworm EPIPLEMIDAE - Crenulate Moths Moths Auzeinae Butterflies and Moths (Lepidoptera) B 651 Epipleminae Riodininae GEOMETROIDEA LIBYTHEIDAE - Snout Butterflies GEOMETRIDAE - Geometer Moths NYMPHALIDAE - Brush-Footed Butterflies Archiearinae Group Nymphalinina Oenochrominae Tellervinae Orthostixinae Danainae Ennominae Ithomiinae Desmobathrinae Acraeinae Geometrinae Heliconiinae Sterrhinae Nymphalinae HEDYLIDAE - American Butterfly Moths Group Satyrinina PAPILIONOIDEA Calinaginae Series Hesperiiformes Apaturinae HESPERIIDAE - Skipper Butterflies Amathusiinae Megathyminae Morphinae Coeliadinae Brassolinae Pyrrhopyginae Satyrinae Pyrginae DREPANOIDEA Trapezitinae AXIIDAE - Gold Moths Heteropterinae THYATIRIDAE - False Owlet Moths Hesperiinae Thyatirinae Series Papilioniformes Polyplocinae PAPILIONIDAE - Swallowtail Butterflies CYCLIDIIDAE - Giant Hooktip Moths Baroniinae DREPANIDAE - Hooktip Moths Parnassiinae Drepaninae Papilioninae Oretinae PIERIDAE - Yellow-White Butterflies Nidarinae Pseudopontiinae BOMBYCOIDEA Dismorphiinae Series Bombyciformes Pierinae CARTHAEIDAE - Australian Silkworm Moths Coliadinae EUPTEROTIDAE - Giant Lappet Moths LYCAENIDAE - Gossamer-Winged ­Butterflies Janinae Lipteninae Eupterotinae Poritiinae Panacelinae Liphyrinae APATELODIDAE - American Silkworm Moths Miletinae Apatelodinae Curetinae Epiinae Lycaeninae Phiditiinae Theclinae BOMBYCIDAE - Silkworm Moths Polyommatinae Bombycinae RIODINIDAE - Metalmark Butterflies Prismostictinae Styginae MIMALLONIDAE - Sackbearer Moths Hamearinae ANTHELIDAE - Australian Lappet Moths Euselasiinae Munychryiinae Corrachiinae Anthelinae 652 B Butterflies and Moths (Lepidoptera) LASIOCAMPIDAE - Lappet Moths Dudusinae Chondrosteginae Heterocampinae Chionopsychinae Nystaleinae Poecilocampinae Meiceratinae Macromphaliinae DIOPTIDAE - American False Tiger Moths Lasiocampinae Dioptinae Series Saturniiformes Doinae ENDROMIDAE - Glory Moths THYRETIDAE - African Maiden Moths Endrominae LYMANTRIIDAE - Tussock Moths Mirininae Orgyiinae LEMONIIDAE - Autumn Silkworm ­Moths Lymantriinae Lemoniinae ARCTIIDAE - Tiger Moths Sabaliinae Group Pericopinina BRAHMAEIDAE - Brahmin Moths Pericopinae Dactyloceratinae Group Arctiinina Brahmaeinae Lithosiinae OXYTENIDAE - American Tropical Silkworm Arctiinae Moths Group Ctenuchinina CERCOPHANIDAE - Andean Moon ­Moths Ctenuchinae Cercophaninae Syntominae Janiodinae NOCTUIDAE - Owlet Moths SATURNIIDAE - Emperor Moths Group Aganainina Arsenurinae Aganainae Ceratocampinae Group Herminiinina Hemileucinae Herminiinae Agliinae Group Noctuinina Ludiinae Hypenodinae Salassinae Rivulinae Saturniinae Hypeninae SPHINGOIDEA Catocalinae SPHINGIDAE - Hawk Moths Euteliinae Smerinthinae Stictopterinae Sphinginae Sarrothripinae Macroglossinae Chloephorinae NOCTUOIDEA Nolinae NOTODONTIDAE - Prominent Moths Plusiinae Group Oenosandrinina Acontiinae Oenosandrinae Condicinae Group Thaumetopoeinina Amphipyrinae Thaumetopoeinae Stiriinae Group Notodontinina Psaphidinae Pygaerinae Agaristinae Platychasmatinae Cocytiinae Notodontinae Heliothinae Phalerinae Acronictinae Butterflies and Moths (Lepidoptera) B 653 Pantheinae Micropterigidae (mandibulate archaic moths) Bryophilinae total 130 species worldwide. There are two sub- Cuculliinae familes. Adults are minute to small and diurnal. Hadeninae Larvae feed on mosses, liverworts, or detritus. Noctuinae

Agathiphagoidea Primitive Moths Agathiphagoidea are also a monobasic super- family, containing the relict family, Agathiphagi- The families considered the most primitive of all dae. Adults have chewing mouthparts (haustellum lepidopterans, in the groups up to Myoglossata, absent) and are similar to Micropterigidae. include the first six families. The first three Agathiphagidae (kauri moths) total only two ­superfamilies are all relictual base lineages of the known species, from Australia and Fiji. Adults are Lepidoptera and also have only one family in each small and diurnal. Larvae are seed-borers of kauri superfamily and each suborder: Micropterigidae pines (Araucariaceae). (Micropterigoidea, suborder Zeugloptera), Agath- iphagidae (Agathiphagoidea, suborder Aglossata), and Heterobathmiidae (Heterobathmioidea, sub- Heterobathmioidea order Heterobathmiina). They are all small moths (not over 16 mm in wingspan), concentrated most Heterobathmioidea are one of the most obscure in what are now considered refugia regions of the groups, based on only a single family, Heterobath- world where the oldest faunas remain, so-called miidae. Adults have small mandibles (haustellum Gondwanaland distributions, notably in South absent). Africa, Australia, New Zealand, and Chile, Heterobathmiidae (Valdivian archaic moths) although some are more widespread like the include about nine species, with named thus far all Micropterigidae which occur in all regions. All from southern South America. Adults are small have homoneurous venation and a jugum for wing and diurnal. Larvae are leafminers of Nothofagus coupling of the fore- and hindwings during flight, trees (Fagaceae). and the hindwings are mostly about the same size as the forewings. Adults have small mandibles instead of the usual lepidopteran haustellum (or Eriocranioidea proboscis) of the Aglossata, but the primitive ­families of the Glossata also have a reduced The superfamily Eriocranioidea contains two haustellum in addition to vestigial mandibles. ­families, together comprising the Infraorder Most of the primitive moths also have large Dacnonypha. Adults have a reduced haustellum 5-segmented maxillary palpi and the head ver- but retain vestigial mandibles. tex vestiture with long scales or hair-like scales. Eriocraniidae (sparkling archaic sun moths) are a Holarctic family of 25 species, about half in Europe and half in North America. Adults are Micropterigoidea small and diurnal. Larvae are leafminers on a vari- ety of hardwood trees and other plants. Micropterigoidea contain the single family, Acanthopteroctetidae (archaic sun moths) are Micropterigidae (in the past misspelled as very similar to Eriocraniidae, and include only Micropterygidae). four species, all North American except for one in 654 B Butterflies and Moths (Lepidoptera) the Palearctic. Adults are small and thought to be Exoporia ­diurnal. Larvae are blotch leafminers on Ceanothus (Rhamnaceae) for the single species known This first infraorder of the Neolepidoptera, biologically. ­Exoporia, has two superfamilies, Mnesarchaeoidea and Hepialoidea, with six primitive moth families in total. Wing venation is homoneurous and a Lophocoronoidea jugum is used for wing coupling.

Representing the infraorder Lophocoronina, this monobasic superfamily contains the small archaic Mnesarchaeoidea family, Lophocoronidae. Adults have the haustel- lum reduced (mandibles vestigial). This superfamily is contains a single family of Lophocoronidae (Australian archaic sun primitive moths, the Mnesarchaeidae. Adults moths) have six known species in Australia. Adults have the haustellum short (mandibles vestigial). are small and crepuscular in sclerophyll eucalyptus Mnesarchaeidae (New Zealand primitive woods. Biologies and larvae remain unknown.. moths) occur only in New Zealand, with eight known species. Adults are small and diurnally active in forest clearings and near ferns. Biologies Myoglossata and larvae remain unknown.

The cohort Myoglossata are divided into two sub- cohorts: Myoglossata and Neolepidoptera, where Hepialoidea the subcohort Myoglossata contains only a single infraorder, Neopseustina, and the Neolepidoptera This superfamily comprises the first group of have two infraorders (Exoporia and Heteroneura) ­lepidopterans with several families, although most which contain all the remaining Lepidoptera. species are in Hepialidae, the ghost moths. The ­superfamily comprises 616 known species world- Neopseustina wide. All are relict groups that retain a jugum for wing coupling, and are rather small moths, but This infraorder contains only the single superfamily Hepialidae also have some of the largest species of Neopseustoidea. Wing venation is homoneurous the “micro” -moths known (up to 250 mm in wing- and a jugum is used for wing coupling. Adults have span). Adults with reduced haustellum (sometimes the haustellum short (mandibles vestigial). absent) and usually with vestigial mandibles (absent in Hepialidae and Palaeosetidae); antennae are mostly short; hindwings tend to be nearly as long Neopseustoidea as the forewings. Neotheoridae (Amazonian primitive ghost This first group of the Myoglossata includes only moths) include a single species from the Mato the single archaic family Neopseustidae. Grosso area of Brazil (two more species have been Neopseustidae (archaic bell moths) include discovered recently). Adults are medium size. nine known species (six from Southeast Asia and Biologies and larvae remain unknown. three from Chile). Adults are small (bell-shaped Anomosetidae (Australian primitive ghost when at rest) and crepuscular or diurnal. Biologies moths) comprise a single genus with one known and larvae remain unknown, but species in Chile species from Australia. Adults are small. Biologies are thought to possibly feed on native bamboos. and larvae remain unknown Butterflies and Moths (Lepidoptera) B 655 Prototheoridae (African primitive ghost was found to be monotrysian. Only one family is moths) comprise 12 species from southern Africa. known. Adults with head roughened; haustellum Adults are small. Biologies and larvae remain very short (with vestigial mandibles present); unknown, but a pupa has been found in moss. antennae bipectinate in males; labial palpi elon- Hepialidae (ghost moths, or swifts) comprise gated; and maxillary palpi 5-segmented (unfolded). about 594 species from all faunal regions, but most Wing venation is somewhat primitive. are from Australia, South Africa and Chile. Adults are Andesianidae (Valdiviar forest moths) total medium size to very large and typically ­crepuscular only three known species from southern Andean or nocturnal, but a few are diurnally active. Larvae forest zones of Argentina and Chile. Adults are feed as borers on roots, trunks or under bark of trees, robust and of medium size, apparently nocturnal various bushes, or grasses, or even leaf litter. (possibly crepuscular). Biologies are unknown, but Palaeosetidae (miniature ghost moths) com- larvae are likely to be stem borers. prise eight species worldwide (five in Assam, ­Thailand and Taiwan, two in Australia, and one in Nepticuloidea Colombia). Adults are small and crepuscular or active during the day in dark forested areas, typically The superfamily Nepticuloidea includes two near wet moss-covered rock faces. Biologies remain ­families of the tiniest leafminer moths known: unknown but larvae of a species in Taiwan are Nepticulidae and Opostegidae. Adults with haust- thought to feed on mosses. ellum very short; antennae with distinct eye caps; labial palpi reduced; maxillary palpi 5-segmented Monotrysian Moths and folded; and head vestiture very rough-scaled. Wing venation is greatly reduced. The division Monotrysia, of the infraorder Nepticulidae (pygmy moths) comprise 868 ­Heteroneura, comprises sections Nepticulina and species from all faunal regions, although most Incurvariina, and include the first more evolved (over 510 sp.) are from the Palearctic region; actual moths leading to the main Ditrysian Lepidoptera. world fauna likely exceeds 1,200 species. Two sub- All have frenular bristles as the wing coupling families are used. Adults are minute and diurnally mechanism instead of a jugum. The Monotrysia active. Larvae are leafminers, usually blotch mines, comprise nine families in recent classifications, all although some also mine other plant parts. A large with a single genital opening in females (Ditrysia variety of hostplants are used. have two female genital openings). Mandibles are Opostegidae (eye-cap moths) total 122 known not present in any of the species in this group species from all faunal regions and especially (except Andesianidae and Palaephatidae), nor in ­Australia; actual fauna probably exceeds 175 species. any higher lepidopterans. Nepticulina have four Adults are minute to small and diurnally active. The families in four superfamilies (Andesianidae, few larvae known are leafminers, but some are stem ­Nepticuloidea, Tischerioidea, and Palaephatoidea) borers. Hostplants are in several plant families. and Incurvariina have five families in the single superfamily, Incurvarioidea. Tischerioidea

Andesianoidea The superfamily Tischerioidea includes the single family Tischeriidae Adults with head vestiture The superfamily was formed in 2003 for odd rough; haustellum short and scaled; labial palpi ­Valdivian moths formerly considered to be Cossi- short; maxillary palpi minute, 1-segmented, and dae. Their female genital morphology, however, wing venation is very reduced. 656 B Butterflies and Moths (Lepidoptera) Tischeriidae (trumpet leafminer moths) total ­Larvae are leafminers at first, then switch to leaf 81 known species from all regions except Australia, skeletonizing on a variety of hostplants; some are with most species in the Nearctic (48 sp.); actual case bearers or shoot borers. fauna likely exceeds 125 species. Adults are small Cecidosidae (gall moths) total only seven and diurnally active. Larvae are leafminers, usually ­species, with five species from southern South trumpet-shaped mines or blotch mines, on a ­variety America and two from South Africa. Adults are of hostplants. small and probably diurnal. In Argentina larvae are gall makers on Schinus (Anacardiaceae). Prodoxidae (yucca moths) total 65 species, Palaephatoidea mostly western Nearctic. There are two subfamilies. Adults are minute to small and diurnal. Larvae are The monobasic superfamily Palaephatoidea con- seed, flower stalk, or stem borers; rarely gall makers. tains one family from southern refugia regions of Hostplants are various yucca plants (Agavaceae) and the world (except South Africa), the Palaephatidae. other species are on hardwood trees and bushes. Adults with head roughened; haustellum short, Adelidae (longhorned fairy moths) comprise naked (vestigial mandibles usually present); labial 295 species worldwide, but most are Palearctic (143 palpi short; maxillary palpi 5-segmented and sp.), with two subfamilies; actual fauna probably folded, and wing venation is heteroneurous. exceeds 400 species. Adults are minute to small; Palaephatidae (Gondwanaland moths) total antennae extremely long (often 2X wing lengths) 39 described species (28 from Chile and Argentina, in males, but of average length in females (some- and 11 from Australia), but at least 25 more unde- times thickened). Adults are usually diurnal but a scribed species are known from Australia alone; few are crepuscular. Larvae are leafminers, but in actual fauna probably exceeds 90 species. Adults later instars change to casebearers. Hostplants are small to medium size. Biologies little known include a number of different plant families. but adults presumed diurnally active. Larvae tie Heliozelidae (shield bearer moths) total 106 hostplant twigs together (on Verbenaceae and species from all regions, with more than half the Proteaceae). species split between North America (31 sp.) and Australia (36 sp.); actual fauna probably exceeds 200 species. Adults are minute to small and diurnal. Incurvarioidea Larvae make serpentine leaf mines at first, then make blotch mines in later instars. Hostplants This superfamily is the sole group comprising include a variety of hardwood trees and bushes. ­section Incurvariina of the Monotrysia. Included are a number of odd groups that have been consid- ered families in the past, but only five families are Ditrysia now recognized. The superfamily has 589 known species. All have a scaled haustellum, although This division of the infraorder Heteroneura mostly reduced; head vestiture is rough-scaled ­comprises all the remaining Lepidoptera, divided except for Heliozelidae; some have 5-segmented into the sections Tineina and Cossina. All the maxillary palpi (Incurvariidae and Prodoxidae, remaining Lepidoptera have heteroneurous wing plus rarely in Adelidae), while reduced in others. venation (although often with reduced venation in Incurvariidae (leafcutter moths) total about the tiny leafminers) and a frenulum-retinaculum 116 species from all regions, but most are Palearctic wing coupling (rarely reduced). Typically, they (64 sp.), divided into two subfamilies. Adults are have 3-segmented labial palpi, generally upcurved, small and mostly diurnal in shaded habitats. and a haustellum (rarely reduced or absent). Butterflies and Moths (Lepidoptera) B 657 Tineina are used. Adults are small to medium size, with rather robust bodies and ­usually large recurved This section of the Ditrysia involves those groups labial palpi. Adults are mostly nocturnal, but some with a ventral heart vessel in the adult (consid- may be crepuscular. Larvae are root ­feeders, mostly ered more primitive than the dorsal heart vessel of grasses, and construct long underground silken of the Cossina), and are further divided into the tubes to feed on hostplant roots. subsections Tineina and Sesiina. Most of the Tineidae (fungus moths) comprise the first Microlepidoptera families are in this section of very large family of Lepidoptera, with about the Ditrysia, other than the primitive moths and a 2,160 described species. The actual world fauna few groups in Cossina often included among the probably exceeds 4,000 species. The family is micro-moths. The subsection Sesiina have a spined divided into 16 subfamilies. Adults are minute to pupa, while most of the subsection Tineina have an medium size and nocturnal or crepuscular; unspined pupa (Gelechioidea, Copromorphoidea, rarely diurnal. Larval habits vary greatly, but Yponomeutoidea, Immoidea, Pyraloidea, and most are detritus feeders, some making cases, Pterophoroidea), other than the basal groups that tunnels, or silken tubes; also, odd groups are form the Tineoidea, which also have a spined pupa. coprophagous, keratophagous,woolen feeders, (Pterophoridae pupae have scolus-like projections and even myrmecophilous and termitophilous but not “spined” as here defined). larvae are known. Included among Tineidae are some of the most well known household pest species, such as clothes moths and grain moths. Tineoidea Eriocottidae (Old World spiny-winged moths) are a small family of 212 known species, mostly The superfamily Tineoidea includes the most African (120 sp.) and Oriental (66 sp.), now primitive of the Ditrysia and also are basal groups divided into two subfamiles. Adults are small to with ancestors that evolved to the Sesiina groups, medium size and mostly diurnally active, or may Sesioidea and Zygaenoidea, while also having be crepuscular. Biologies are little known but begun the development to the other superfamilies some larvae reported to tunnel in the soil, possibly of the subsection Tineina. Tineoidea are split into feeding on roots or detritus. two series, Tineiformes (Acrolophidae, Tineidae, Psychidae (bagworm moths) total 1,001 Eriocottidae, Psychidae, and Arrhenophanidae) known species, mostly Palearctic and African, with and Gracillariiformes (Amphitheridae, Schreck- only 88 known for the New World; actual fauna ensteiniidae, Douglasiidae, Bucculatricidae, and likely exceeds 1,200 species. The family is now Gracillariidae), which some specialists consider divided into six subfamilies. Adults are ­minute to separate superfamilies. The superfamily total medium size and mostly diurnal or crepuscular. comes to about 5,730 known species. Adults with Larvae are mostly leaf feeders or feed on lichens, head vestiture mostly rough-scaled; haustellum all making distinctive types of larval cases, or bags. naked (unscaled); labial palpi mostly upcurved, Pupation is within the larval case and females 3-segmented (except most Psychidae); maxillary often remain there in a wingless or larviform palpi mostly small; antennae mostly filiform shape, using pheromones to attract the winged (mostly bipectinate in Psychidae); wing venation males. A number of species are economic and reduced in some species (mainly leafminers). many are general plant feeders. ­Larvae with three lateral setae on the prothorax. Arrhenophanidae (tropical lattice moths) Acrolophidae (tube moths) total 270 species in total about 30 species, mostly Neotropical, but the New World, mostly in the large genus Acrolophus; recently with some Southeast Asian additions; actual fauna likely exceeds 350 species. Two sub­families actual fauna probably exceeds 50 species. Adults 658 B Butterflies and Moths (Lepidoptera) are small to medium size. Adult activity mostly from sap feeders with reduced legs, to later instars nocturnal, but some are diurnal. Biologies with a 3-proleg pair larval form, which is unique unknown except for one Neotropical species with among the Microlepidoptera. Later instars some- case bearing larvae that feed on fungi. times feed externally as leaf skeletonizers. Host- Amphitheridae (double-eye moths) are an plants include a great number of plant families. unusual and small family of mostly tropical moths, A few species are of economic importance, such as totaling 57 species, mostly Indo-Australian (one the citrus leafminer (Phyllocnistis citrella). genus occurs in Europe and possibly another in South America). Adults are small, with eyes ­usually divided. Adults active diurnally. Larvae are Gelechioidea ­leafminers, becoming leaf skeletonizers in later instars; host records are mostly in Betulaceae and This superfamily comprises a huge group of micro- Aceraceae. The family has been erroneously called moths, all having a scaled haustellum and unspined Roeslerstammiidae in recent European literature. pupa. There has been considerable turmoil in Schreckensteiniidae (bristle-legged moths) recent classifications proposed for the group, either are a small family of only eight known species with a large family Oecophoridae or with con- (three in North America, one in Central America, glomeration of various groups into an enlarged and one in Europe). Adults are small and diurnal. family Elachistidae. In the classification adopted Larvae are leaf skeletonizers on Anacardiaceae or herein, there are 11 families recognized, the ­largest Rosaceae. being Oecophoridae and Gelechiidae. The entire Douglasiidae (Douglas moths) comprise only superfamily encompasses about 18,230 described 28 known species, mostly Palearctic (20 sp.). Adults species worldwide, but the actual fauna may well are minute to small and crepuscular or diurnal. exceed 45,000 species, since there are huge Larvae are leafminers or borers in ­petioles or ­numbers of undescribed tropical species. Adults stems. Hostplants are known in Boraginaceae, mostly with head vestiture mostly relatively Labiatae, and Rosaceae. smooth-scaled (rarely roughened); haustellum Bucculatricidae (ribbed-cocoon maker always scaled; labial palpi mostly recurved, moths) total 247 species worldwide, with most 3-­segmented; maxillary palpi vary but mostly species being Nearctic (103 sp.) or Palearctic (86 small; antennae mostly filiform. Larvae mostly with sp.); most species are in the genus Bucculatrix. three lateral setae on the prothorax (except two in Adults are minute to small and mostly diurnal. Momphidae). Larvae are leafminers, with some changing to Oecophoridae (concealer moths) is a large external leaf skeletonizing in later instars, but a family of about 7,550 described species from all few are gall makers or stem miners. Pupation is in faunal regions, with most species being from a white spindle-shaped cocoon with a ribbed Australia; the actual fauna may well exceed 12,000 ­surface, unique to the family. Many different host- species worldwide. There are ten subfamilies plants are known but many feed on Compositae. ­recognized. Adults are small to medium size and Some species are economic. mostly nocturnal but some are diurnal or crepus- Gracillariidae (leafminer moths) comprise the cular. Larvae include many leaf litter feeders, but major leafmining family of Lepidoptera, with about also leaf tiers, leaf webbers, bark feeders, and a 1,740 species from all regions. The actual world few leafminers. Hostplants include a large number total probably exceeds 6,000 species. There are of plant families, plus lichens, fungi, and detritus three subfamilies. Adults are minute to small and or leaf litter. Few are economic. active diurnally. Larvae are usually leafminers but Lecithoceridae (tropical longhorned moths) change form in later instars (hypermetamorphism) total about 1,038 described species, mostly tropical Butterflies and Moths (Lepidoptera) B 659 Oriental, but also with one group in the Palearctic; Coleophoridae (casebearer moths) comprise actual fauna probably exceeds 1,500 species. There about 1,525 species worldwide, with most being are four subfamilies. Adults are small and mostly Palearctic and in the genus, Coleophora. The actual diurnal and many have the habit of holding the world fauna likely exceeds 2,000 species. Most are long antennae together to the front when at rest. in subfamily Coleophorinae, while non casebear- Larvae may mostly be leaf litter feeders or leaf tiers, ers are in Batrachedrinae. Adults are small and but few species are known biologically. A few ­varied may be mostly crepuscular but many are diurnal. hostplants are recorded. Larvae make small cases (except for Batrachedri- Elachistidae (grass miner moths) comprise nae), often distinctly shaped for each species, skel- about 723 species worldwide, but most are Palearctic etonizing host leaves, but some are seed borers, (472 sp.). Two subfamilies are used (or only tribes). leafminers, or stalk borers, or skeletonize leaves Adults are small and often crespuscular or noc- beneath frass webs. A few Batrachedrinae are turnal, but some are diurnal. Larvae are leafminers ­predaceous on scale insects (Hemiptera). Various (sometimes gregarious) or stem miners, especially hostplants are utilized. A few species are eco- on grasses (Gramineae) and related plant groups nomic. Ovovivipary has been recorded for a few like Juncaceae and Cyperaceae, but other plant species. ­families are also utilized. Momphidae (mompha moths) total 127 Pterolonchidae (lance-wing moths) total only species worldwide, with about half from the 11 species, mostly Mediterranean, plus two are Palearctic. Adults are small and mostly diur- from South Africa. Adults are small and may be nal or crepuscular. Larvae mostly leafminers, mostly crepuscular. Larvae are root borers as far but some are borers in flowers and stems, as is known. Only recorded hostplants are in or gall makers. Hosts are only known in Compositae. Onagraceae. Gelechiidae (twirler moths) are a very large Agonoxenidae (palm moths) are a small family, with over 4,830 species described, how- ­family of 68 known species from all faunal regions. ever, possibly with a fauna exceeding 10,000 spe- Adults are small and diurnal. Larvae are leaf cies worldwide. Subfamily arrangements have ­skeletonizers, or borers in leaves, stems, and fruits; varied but now include 4. Adults are small and rarely gall-makers. Hostplants mostly in Rosaceae mostly nocturnal but some are diurnal or crepus- or Palmae. A few are economic. cular. Larvae have a range of feeding habits but Cosmopterigidae (cosmet moths) total over most are leaf skeletonizers, using a leaf fold or 1,540 species worldwide, but the extant fauna may leaf tie as protection. A large variety of plants are encompass 3,500 species. There are three subfami- used as hosts. Some species are economically lies. Adults are small and mostly diurnal, but some important. are crepuscular. Larvae mostly leafminers or Blastobasidae (scavenger moths) total over needleminers, but some are borers of various plant 296 species worldwide, with many known from parts; a few are predaceous on Hemiptera. Hosts North America and Europe; actual fauna probably are varied. Ovovivipary recorded in a few species. exceeds 600 species. There are two subfamilies. Some economic species are known. Adults are small and nocturnal as far as is known. Scythrididae (flower moths) total about 523 Larvae are scavengers or detritus feeders, some- species worldwide, but mostly known from Europe. times feeding on plant fruits, flowers, or seeds, Adults are small and diurnal but some may be cre- among a number of plant families, but few are puscular. Larvae are skeletonizers on leaves, buds, known biologically. At least one species lives with flowers, hiding under webbings. Many plant fami- coccids (Hemiptera) but predation on the coccids lies are used as hosts, plus some on lichens and has not been confirmed. mosses. 660 B Butterflies and Moths (Lepidoptera) Copromorphoidea Tineoidea, while other previously contained groups are now in other superfamilies. About 1,853 species This superfamily comprises four families related are known in the superfamily. Adults with head especially by larval characters. The world fauna totals vestiture mostly relatively smooth-scaled (rough- 623 species. Adults with head vestiture mostly ened in Ochsenheimeriidae, Argyresthiidae and smooth-scaled; haustellum naked (unscaled); Lyonetiidae); haustellum developed and naked labial palpi porrect (except for Epermeniidae), (unscaled); labial palpi mostly upcurved; maxillary 3-segmented; maxillary palpi vary; antennae mostly palpi mostly reduced; antennae mostly filiform. filiform. Larvae with two lateral setae on the Larvae mostly with three lateral setae on the prothorax. ­prothorax (two in Glyphipterigidae, and a few Copromorphidae (tropical fruitworm moths) ­Plutellidae and Yponomeutidae). are a small family of 58 species, mostly tropical; Ochsenheimeriidae (cereal stem moths) actual fauna probably exceeds 100 species. Adults include only 17 species from the Palearctic (one are small to medium and nocturnal. Larvae are species is from Kashmir), with one species intro- leaf feeders using a leaf web, or are borers (one duced into North America. Adults are small and feeds beneath bark), but few biologies are known. diurnal. Larvae are leafminers, but become stem Hostplants include Berberidaceae, Ericaceae, borers in later instars, primarily on grasses Moraceae, Podocarpaceae, and Rubiaceae. ­(Gramineae), sedges (Cyperaceae) and rushes Alucitidae (many-plumed moths) total about (Juncaceae). One species is economic. 184 species worldwide. Adults are small; wings with Glyphipterigidae (sedge moths) total 431 all veins as separate wing clefts to near the wing species from all regions, mostly in the genus bases (rarely split only to center of wings). Adults Glyphipterix, with the largest number from the active in deep shade, or may be crepuscular. Larvae Australian-New Zealand region; actual world are borers or gall makers as far as is known. Various fauna probably exceeds 600 species. There are two hostplant records are known. subfamilies. Adults are small and diurnal, usually Carposinidae (fruitworm moths) total about in proximity to the hostplants. Larvae are mostly 279 species from all regions, but most are borers in seeds, stems, or leaf axils, and a few are ­Australian and South Pacific. Adults are small to leafminers, but most tropical species are unknown medium and nocturnal or crepuscular. Larvae biologically. Hostplants are mostly sedges (Cyper- are borers in fruits, seeds, buds, or trunks and aceae), rushes (Juncaceae), and grasses (Gramineae), limbs, but a few are leafminers. Hosts include a plus a few other plant families. variety of plants. A few species are economic. Plutellidae (diamondback moths) include 386 Epermeniidae (fringe-tufted moths) total 102 species worldwide; actual fauna probably exceeds species, with many being Palearctic (36 sp.) and 600 species. There are four subfamilies. Adults are Australian (23 sp.), in two subfamilies. Adults are small to medium size and mostly nocturnal or small and diurnal or crepuscular. Larvae are leaf- ­crepuscular, but some are diurnal. Larvae are leaf miners, leaf skeletonizers, or borers of seeds, fruits, skeletonizers, but most remain unknown biologi- or buds; a few are gall makers. Host records include cally. Hosts include different plant groups. A few several plant families. species are economic. Attevidae (tropical ermine moths) include 48 species, mostly tropical and in the genus Atteva Yponomeutoidea (the single partially non-tropical species known occurs across the southern United States and into This superfamily of varied moths includes nine the Caribbean and Mexico); actual fauna probably families, some of which have been transferred from at least 60 species. Adults are small to medium Butterflies and Moths (Lepidoptera) B 661 size and are diurnal or crepuscular. ­Larvae are leaf ancestors. Adults with head vestiture relatively webbers and leaf skeletonizers on Araliaceae and smooth-scaled; haustellum naked; labial palpi Simaroubaceae. Minor economic species occur upcurved and often prominent, with long second on Ailanthus trees in India and the United States. segment; maxillary palpi minute, 1 to 2-segmented; Yponomeutidae (ermine moths) total 395 antennae mostly filiform; body robust. Larvae with species worldwide; actual fauna likely exceeds 500 three lateral setae on the prothorax. species. Three subfamilies are recognized. Adults Immidae (imma moths) comprise 246 species, are small to medium size and mostly nocturnal. all tropical, and mostly Indo-Australian and South Larvae are leaf skeletonizers and leaf webbers, but Pacific; actual fauna likely exceeds 450 species. some are leafminers or needleminers. Hosts Adults are small to medium size and diurnal, include many different plant families. A few­species but some may be crepuscular. Larvae are leaf are economic. feeders, but only three species have biological data. Argyresthiidae (shiny head-standing moths) Hostplants are in Myrtaceae, Podocarpaceae, and include 160 species, mostly from Holarctic region; Violaceae. actual fauna probably exceeds 450 species. Adults are small and mostly crepuscular, but many may be diur- nal. Larvae are leafminers and needleminers, and Pyraloidea some mine in various plant parts. Numerous plants are recorded as hosts. Several species are economic. This superfamily includes three families but mainly Lyonetiidae (Lyonet moths) total 264 species, the very large family, Pyralidae. The superfamily mostly Holarctic; the actual fauna probably comprises about 17,312 species worldwide. Recent exceeds 600 species. There are three subfamilies. specialists have taken to splitting Pyralidae into its Adults are minute to small and mostly crepuscular two major lineages, as the separate families Cram- and nocturnal. Larvae are blotch leafminers; rarely bidae and Pyralidae, but this reversion to what was mining stems. Many plant groups are recorded as done over 100 years ago is unnecessary and amply hosts. A few species are economic. clarified by using the “group” category below the Acrolepiidae (false diamondback moths) family level within a single family Pyralidae. Some include 96 species, mostly Palearctic. Adults are specialists do even more splitting by placing each small and crepuscular or diurnal. Larvae mostly pyraloid family in its own monobasic superfamily leafminers, but some are borers in seeds, stems and (Hyblaeoidea, Thyridoidea, and Pyraloidea). flower buds. Several hostplant groups are used, but Adults with head vestiture mostly smooth-scaled; mostly on Compositae. Very few are economic. haustellum mostly scaled (not Hyblaeidae and Heliodinidae (sun moths) are a small family Thyrididae); labial palpi mostly porrect, 3-seg- of 56 species, mostly Neotropical (31 sp.); actual mented; maxillary palpi varied; antennae mostly fauna probably exceeds 100 species. Adults are filiform. Larvae have two lateral setae on the small and diurnal. Larvae are mostly leaf skeleton- prothorax. izers, but some are borers in fruit racemes. Several Hyblaeidae (teak moths) are a small tropical plant families are used as hosts. family of 18 species, mostly Indo-Australian and in the genus Hyblaea (one pantropical species is also established in southern Florida). Adults are Immoidea medium size; body usually robust. Adults are diur- nal or perhaps crepuscular. Larvae are leaf rollers. This is a monobasic superfamily for the single Hostplants are in Bignoniaceae and ­Verbenaceae. small family Immidae. It is somewhat related to One economic species: the teak leafroller (Hyblaca Pyraloidea and may represent relatives of ­common puera). 662 B Butterflies and Moths (Lepidoptera) Thyrididae (picture-winged leaf moths) total Oxychirotidae (tropical plume moths) include 794 species worldwide, nearly all tropical, with only six species, all Indo-Australian and South nearly half the species Indo Australian (only a few Pacific. Some specialists include this family as part species are in the Nearctic and Palearctic regions); of the Tineodidae. Adults are small and may be actual fauna likely exceeds 1,200 species. There are crepuscular. Larva of one species feeds on seeds of six subfamilies. Adults are small to large and white mangrove (Avicenniaceae); remainder ­diurnal or crepuscular. Larvae are leafrollers (one unknown biologically. Australian species is gregarious), or borers in Pterophoridae (plume moths) comprise about stems and flower racemes; a few are gall makers. 1,292 species worldwide, with about a third being A number of hostplants are used. Only a few Palearctic; actual world fauna probably exceeds ­species are economic. 1,800 species. Subfamilies number five. Adults are Pyralidae (snout moths) comprise the third small, usually with hindwings split into three largest family of Lepidoptera, with about 16,500 fringed plumes; forewings often entire or split into described species, but a probable fauna of at least two parts near the termen (a few species have both 25,000 species worldwide; 19 subfamilies are used wings entire). Adults mostly nocturnal but some in the classification. Adults are small to large and crepuscular or in shaded areas during the day. Lar- mostly nocturnal, but some are crepuscular and a vae mostly leaf feeders, or miners and borers of few are diurnal. Larvae are mostly leafrollers or leaf various plant parts; a few are gall makers. Host- webbers, but many are borers, root feeders, detritus plants include many families. Several species are feeders (including stored products pests), and a economic. few are leafminers, plus rare myrmecophilous ­species, and even some aquatic groups making cases (Nymphulinae). A large number of economic Sesiina species are in this family, including pests on ­virtually all crops and forest trees. Hostplants are in The subsection Sesiina of the Tineina include two a large number of plant families. superfamilies: Sesioidea and Zygaenoidea.

Pterophoroidea Sesioidea This superfamily includes only three families, but most species are in the Pterophoridae. About The Sesioidea include four families, although many 1,309 species are known for the superfamily. specialists maintain separate superfamilies for most Adults with head vestiture average (rather of them: Brachodidae, Sesiidae, Urodidae, and smooth scaled); haustellum naked (unscaled); Choreutidae. Brachodidae are thought to be the labial palpi porrect; maxillary palpi mostly short; basal group, with close ties to Sesiidae. The world antennae filiform. Larvae have three lateral setae fauna totals 1,963 known species in the superfamily. on the prothorax in Pterophoridae, but only two Adults mostly with head vestiture mostly smooth- lateral setae in ­Tineodidae (not known for scaled (rough in most Brachodidae); haustellum Oxychirotidae). mostly naked (scaled in Choreutidae); labial palpi Tineodidae (false plume moths) include only mostly upcurved; maxillary palpi mostly small; 11 species, all from Australia. Adults are small and antennae vary but many with thickened antennae possibly diurnal or crepuscular. Larvae are leaftiers, (Sesiidae). Larvae mostly with three lateral setae on but most are not known biologically. Only recorded the prothorax, but most Brachodidae and a few hostplants are in Euphorbiaceae and Oleaceae. Choreutidae with only two lateral setae. Butterflies and Moths (Lepidoptera) B 663 Brachodidae (little bear moths) comprise but some are budworms; rarely leafminers (Mil- 140 species, most being Old World tropical, lieriinae). Numerous hostplant families are ­particularly Indo-Australian (none are North recorded, but many in Compositae and Moraceae. American). There are three subfamilies. Adults are small to medium size and diurnal. Larvae are root feeders of grasses (in the European Brachodes, Brachodinae), using silken tubes, or borers in Zygaenoidea palm trunks and leaf stems, or other plants; some are leaftiers (Phycodinae). Hostplants are in This superfamily contains the burnet moth and Gramineae, and also Bromeliaceae, Melistomaceae, flannel moth groups, with six families involved (in Moraceae, and Palmae. A few are economic on Europe also called forester moths, which name is palms. used for one of the Noctuidae subfamilies in North Sesiidae (clearwing moths) include about America). Some very colorful species are included, 1,325 species from all regions; the actual number especially some of the larger Zygaenidae which in probably exceeds 1,800 species. Subfamilies are the Oriental region are as large as some butterflies. three. Adults are small to medium size; antennae The superfamily has 1,609 known species from usually thickened and with a slight distal club all regions. Adults with head vestiture usually (most also with unique small terminal bristles on average but often rough-scaled; haustellum naked antennae). Wings very elongated and with unique (unscaled), but sometimes absent or vestigial; labial wing-locking folding where the margins meet. palpi mostly upcurved; maxillary palpi mostly Adults are diurnal, particularly during morning small or reduced; and antennae mostly bipectinate hours. Many species mimic various wasps (sometimes clubbed). Larvae all have three lateral (Hymenoptera). Larvae mostly borers on various setae on the prothorax and most are slug-like. plant parts, and a few are gall makers; two species Heterogynidae (Mediterranean burnet moths) are predaceous on scale insects (Hemiptera). Host include only seven species, with three ­species specificity is high for most species, but overall many from the Mediterranean region of southern plant families are used as hosts. A number of ­species Europe and northern Africa and four species from are economic, including some major pests of fruit South Africa. Adults are small and diurnal, but trees, forest trees, and grape vines. females are apterous and larviform. Larvae, upon Urodidae (false burnet moths) total only about hatching inside the female cocoon, feed first on 80 species, primarily Neotropical, but with a few the dead female and then become external leaf species in North America and in Eurasia. Adults are feeders. Hostplants are in Leguminosae. small and may be crepuscular or mostly nocturnal, Zygaenidae (burnet moths) comprise about but a few possibly diurnal. Larvae are leaf webbers 1,140 species worldwide, particularly well devel- or skeletonizers, but few are known biologically. oped in tropical Asia (450 sp.) where also the Pupation is in a specialized filigreed cocoon. ­largest species occur; actual world fauna likely Hostplants known in Lauraceae, Leguminosae, exceeds 1,500 species. There are seven subfamilies. Salicaceae, Sapotaceae, and Theaceae. A few are Adults are small to large, with antennae sometimes minor pests. clubbed. Adults are diurnal, often flying like Choreutidae (metalmark moths) comprise 418 ­butterflies, or commonly on flowers. Larvae are species worldwide; actual world fauna probably leaf skeletonizers, sometimes feeding communally exceeds 800 species. There are three subfamilies. and usually at night; often slug-like, with concealed Adults are small, with haustellum scaled. Adults are head. Hostplants include various plant families. diurnal; usually near their hostplants and tend to hop Economic species are mostly pests on grapevines about on leaves. Larvae mostly leaf skeletonizers, in North America and Europe. 664 B Butterflies and Moths (Lepidoptera) Himantopteridae (long-tailed burnet moths) the pupae have dorsal spines (tribe Ceracini of include 56 species from Africa and tropical Asia. Tortricidae are an exception). All the larger moths Adults are small to medium size; hindwings with and butterflies are in subsection Bombycina, where extremely long tails. Adults are diurnal but few are the pupae are unspined. Subsection ­Cossina has known biologically. Larvae are leaf skeletonizers, three superfamilies: Cossoidae, Castnioidea, and often communal; sometimes massing in the 1000s. Tortricoidea. Subsection Bombycina has eight Known hostplants are in Dipterocarpaceae. superfamilies: Calliduloidea, Uranioidea, Geome- Lacturidae (tropical burnet moths) total 138 troidea, Papilionoidea (including Hesperioidea), species, mostly Indo-Australian but with a few in Drepanoidea, Bombycoidea, Sphingoidea, and the southern United States; actual world fauna Noctuoidea. All have the haustellum naked probably exceeds 250 species. Adults are small to (unscaled), when present. medium size and nocturnal, but some may be ­crepuscular. Larvae are leaf skeletonizers and are colorful, but most are not known biologically. Cossoidea Hostplants are in families Celastraceae, Moraceae, and Sapotaceae. This superfamily includes large “micro” -moths, Somabrachyidae (Mediterranean flannel such as in the carpenterworm moths (Cossidae), moths) include only five species, with three­species plus the slug caterpillar moth groups. There are two from southern Europe and north Africa, plus two series used to divide the superfamily: Cossiformes, species from South Africa. Adults are small. Adults for the more primitive carpenterworm families are diurnal, but females are larviform and wingless (Cossidae, Dudgeoneidae, Metarbelidae, Cyclo- (females of the South African species are tornidae, and Epipyropidae), and Limacodiformes, unknown). Larvae are leaf feeders (eggs laid on for the slug caterpillar families (Dalceridae, Limaco- leaves, not in the female cocoon), somewhat didae, and Chrysopolomidae). About 2,054 species ­slug-like, with concealed head. Hosts are grasses are known in the superfamily. Adults with head (Gramineae) and Compositae. ­vestiture mostly rough-scaled; haustellum naked (or Megalopygidae (flannel moths) are a New vestigial); labial palpi upcurved or short; maxillary World family of 263 species, mostly Neotropical; palpi mostly reduced or absent; antennae mostly actual fauna likely exceeds 350 species. Adults are bipectinate; body mostly robust. Larvae have three small to large and nocturnal. Larvae are leaf feeders, lateral setae on the prothorax. usually communal in early instars; slug-like, with Cossidae (carpenterworm moths) total 682 concealed head; with poison spines usually beneath species worldwide; actual fauna probably exceeds long hair-like setae. A large number of hostplants 750 species. There are five subfamilies. Adults are are recorded, and some species are polyphagous. A small to very large and nocturnal. Larvae are few are economic on forest trees and palms, but ­borers in trunks and limbs. Hostplants are recorded most are of medical importance due to urticating in a large number of plant families. A number of setae in adults and the poison spines in larvae. species are economic pests of forest trees. Dudgeoneidae (Dudgeon carpenterworm moths) include only six species in the single genus Cossina Dudgeonea, with two species from Africa, one from India, and three from Australia. Adults are This is the second division of the Ditrysia (with a medium size; abdomen with small tympanal dorsal heart vessel) and includes all the macro- organs. Adults nocturnal as far as is known. ­Larvae moths and butterflies, plus a few more of the mostly unknown, but one Australian species is a Microlepidoptera in subsection Cossina, where stem borer on Rubiaceae. Butterflies and Moths (Lepidoptera) B 665 Metarbelidae (tropical carpenterworm moths) ­dorsally. Large numbers of hostplants ­utilized. Few include 103 species, mainly Afrotropical and species are economic other than medically as ­Oriental, with one species in the Palearctic region; stinging caterpillars, but palm defoliators can be a actual world fauna likely exceeds 150 species. problem in the tropics. Adults are small to medium size and may be Chrysopolomidae (African slug caterpillar ­crepuscular. Larvae nocturnal borers on tree bark moths) are a small African family of about 30 or in tree trunks, but most species remain unknown known species. Two subfamilies are known. Adults biologically. Hostplants include various trees. A few are medium size and nocturnal. Larvae leaf-feeding have minor economic status. and slug-like, with small spines; often colorful. Cyclotornidae (Australian parasite moths) Hostplants include Celastraceae. No economic include only five known species from Australia, species are known. the most primitive of the Limacodiformes group of Cossoidea. Adults are small. Adult activity uncertain but may be crepuscular. Larvae ­flattened, Castnioidea with lateral protrusions; highly evolved as ­parasites of leafhoppers, scale insects, or psyllids (Hemiptera) This superfamily contains only the single family in early instars, and then as predators of ant larvae. Castniidae. Often in the past thought of as the Epipyropidae (planthopper parasite moths) progenitor lineage to butterflies, they are now con- total 40 described species, with at least another 30 sidered only an offshoot of cossoid like ancestors, known species awaiting naming; most diversity is while butterflies are evolved from geometroid-like in Australia. Two subfamilies are known. Adults ancestors that also developed into Hedylidae. are minute to small and crepuscular or nocturnal; Adults with head vestiture smooth-scaled and eyes females are sedentary. Larvae slug-like with large; haustellum naked (rarely vestigial); labial rounded dorsum; parasitic on fulgorids and palpi often with distal segment erect; maxillary ­planthoppers (Hemiptera). palpi 2 to 4-segmented; antennae clubbed. Body Dalceridae (tropical slug caterpillar moths) robust. Larvae with two or three lateral setae on include 84 Neotropical species (one sp. intrudes the prothorax. from Mexico into southern Arizona). Two sub- Castniidae (giant butterfly moths) total 170 families are known. Adults are small to medium known species, mostly Neotropical but with size. Adult activity uncertain; possibly only noc- some species also in the Indo-Australian region; turnal or crepuscular. Larvae slug-like, often with likely world total may exceed 180 species. Three translucent gelatinous wart-like surface; feeding subfamlies are known. Adults are medium to as leaf feeders (early instars as leaf skeletonizers), large size and diurnal or crepuscular. Larvae are but few are known biologically. Various hostplants borers of monocot plants, including grasses are used and some larvae are polyphagous. Few (Gramineae), Cyperaceae, Bromeliaceae, Maran- have any economic status. taceae, ­Musaceae, and Palmae, among others. Limacodidae (slug caterpillar moths) total A few are economic on banana plants, various 1,104 known species worldwide, the largest family palms, and sugarcane. of Cossoidea, mostly tropical and especially bio­ diverse in the Oriental tropics; likely world total is near 1,600 species or more. Adults are small to Tortricoidea medium size. Adults perhaps only nocturnal; many with unique resting postures. Larvae slug-like and Another monobasic superfamily exclusively for mostly polyphagous leaf feeders, usually with an the family Tortricidae. In the past, the tortricid extensive array of poisonous stinging spines subfamilies were often considered separate 666 B Butterflies and Moths (Lepidoptera) ­families, such as Olethreutidae and Chlidanotidae, rounded or ­quadratic, or more acute; hindwings and even groups like Ceracidae and Cocylidae more rounded. Immature stages remain little which now are only tribes (Ceracini are odd for known; larvae with two lateral setae on prothorax Tortricoidea also due to their unspined pupae). in Callidulidae. Adults with head vestiture mostly roughened; Ratardidae (Oriental parnassian moths) are haustellum naked (unscaled); labial palpi mostly butterfly-like moths of the Himalayas and Oriental porrect; maxillary palpi usually 4-segmented; tropics, with ten described species, plus a few more antennae filiform; and body usually relatively still undescribed. Adults are medium sized, but stout. Larvae have three ­lateral setae on the males often much smaller than females. Adults are prothorax. diurnal. Larvae are bark feeders, but biologies and Tortricidae (leafroller moths) are a large larvae are mostly unknown. family of 8,945 described species from all faunal Pterothysanidae (parnassian moths) include regions; the actual fauna likely will exceed 12,000 19 species, from southern Africa (seven sp.) and species. Three subfamilies are known. Adults are Southeast Asia (12 sp.). There are two subfamilies. small (rarely medium sized) and mostly nocturnal Adults are medium size and diurnal, possibly also or ­crepuscular, but some are diurnal. Larvae crepuscular. Biologies and larvae remain unknown. mostly leafrollers, but some are borers in various Callidulidae (Old World butterfly moths) plant parts, including stems, branches, flowers, include 102 species, mostly tropical Oriental, in and seeds; a rare few are leaf litter feeders. Most two subfamilies. Adults are medium size and species are restricted to certain hostplants among diurnal, ­flying like some butterflies in quick innumerable plant families. Many species are bursts to ­alternate leaf perches; resting position economic. with wings held together and upright. Larvae largely unknown, except for two species which are leafrollers of ferns. Bombycina

Remaining larger moths and the butterflies are in Uranioidea this subsection of the Cossina, including eight superfamilies. This superfamily encompasses both very large and small moths among five families, mostly Old World: Epicopeiidae, Apoprogonidae, Sema- Calliduloidea turidae, Uraniidae, and Epiplemidae. Some of these families continue to be mixed up with This superfamily includes three families of ancient Drepanoidea and Geometroidea, or have been lineage with many primitive features: Ratardidae, combined into Epiplemidae. About 814 species Pterothysanidae, and Callidulidae. All are Old are known in the superfamily. Adults with head World and total 131 known species for the vestiture mostly roughened (more average in ­superfamily. Ratardidae are sometimes placed in Epiplemidae); haustellum naked; labial palpi Cossidae by some specialists, but represent a basal mostly upcurved or short; maxillary palpi relict from cossoid ancestors similar to Metarbelidae, ­minute and one segmented; antennae filiform, however on the lineage to Callidulidae. Adults but also bipectinate and clubbed or thickened in with head ­vestiture average (rough in Ratardidae); some species; forewings quadratic to triangular haustellum naked (absent in Ratardidae); labial and somewhat pointed apically; hindwings palpi usually porrect; maxillary palpi vestigial; ­usually rounded (some tailed). Larvae with two antennae filiform or bipectinate; forewings broadly lateral setae on the prothorax, as far as is known. Butterflies and Moths (Lepidoptera) B 667 Epicopeiidae (Oriental swallowtail moths) superfamily total comes to 21,190 known species. are a small family with 25 species known in two Adults with head vestiture normal; haustellum subfamilies, mostly Himalayan and East Asian. naked; labial palpi upcurved; maxillary palpi Adults are medium to large and diurnal. Larvae small; antennae mostly filiform (rarely bipecti- little known, but leaf feeders with waxy secre- nate); forewings ­triangular, usually with somewhat tions over body. Hostplants are in Clethraceae, pointed ­forewings (sometimes rounded), but Cornaceae, Ericaceae, Theaceae, and Ulmaceae. sometimes emarginate or with falcate apex; hind- Apoprogonidae (African skipper moths) wings more rounded in most species (rarely include only a single species from South Africa. tailed); and body mostly slender and abdomen Adults are medium size; antennae clubbed (hooked with tympanal organs. Larvae with two lateral at tip); body robust. Adults presumed diurnal, but setae on the prothorax, and most larvae have a nothing is known of the biology or larvae. reduced proleg number. Sematuridae (American swallowtail moths) Geometridae (geometer moths), also called total 36 Neotropical species, one of which just inch worms, are the second largest family of reaches into the United States, in southern ­Arizona. ­Lepidoptera, with about 21,150 described species Adults are medium to large; antennae thickened, from all faunal regions; the actual fauna probably with elongated club (slightly hooked at tip). Adults exceeds 26,500 species. The major biodiversity is nocturnal but some may be crepuscular. Larvae in the Neotropics, with over 6,500 species are leaf feeders, but few known biologically. described, and the Indo-Australian region with ­Hostplants are unrecorded. about 6,670 species. The family is divided into Uraniidae (swallowtail moths) comprise eight subfamilies. Adults are small to large; a about 120 species from all tropical regions, mostly ­number of genera have brachypterous or apterous Indo-Australian (85 sp.); one species strays into females. Adults mostly nocturnal, but also some the United States-Mexican border region (mainly crepuscular and diurnal groups. Larvae mostly in Texas). Two subfamilies are used. Adults are leaf feeders, typically moving in looping fashion medium to large and nocturnal or diurnal, with due to reductions in proleg numbers. Hostplants some of the larger diurnal species known to include most all plant families. Some major migrate. Larvae are leaf feeders. Hostplants are ­defoliating pests are known in this family. known in Asclepiadaceae, Myrtaceae, and Hedylidae (American butterfly moths) total Euphorbiaceae. only 40 known species, all Neotropical. Adults Epiplemidae (crenulate moths) total about 632 are medium size and nocturnal. Larvae are leaf species worldwide, with most being Neotropical feeders. Hostplants are recorded in Euphorbiaceae, (230 sp.) and Indo-Australian (301 sp.). Two ­Malvaceae, Streculiaceae, and Tiliaceae. ­subfamilies are used. Adults are small to medium size and nocturnal. Larvae are leaf feeders or ­webbers. Hostplants are in several plant families. Papilionoidea

The butterflies, also called Rhopalocera, include Geometroidea seven families, including the skippers, family ­Hesperiidae. Skippers are sometimes placed in One of the largest superfamilies of Lepidoptera, their own monobasic superfamily, Hesperioidea, mainly with the large family Geometridae, but but the differences can also be noted by using also including the odd Hedylidae (some special- series Hesperiiformes and Papilioniformes. True ists place the latter family near the true butter- butterflies include families Papilionidae, Pieri- flies, in its own superfamily, Hedyloidea). The dae, Lycaenidae, Riodinidae, Libytheidae, and 668 B Butterflies and Moths (Lepidoptera) Nymphalidae. In the past, many of the subfami- Pieridae (yellow-white butterflies) total about lies, ­especially in Nymphalidae, have been con- 1,275 species worldwide, most being Indo-Australian sidered separate families, and the entire (ca. 515 sp.). Four subfamilies are ­recognized. superfamily has on occasion been split into sev- Adults are small to large and diurnal. Larvae are eral superfamilies, such as Lycaenoidea and leaf feeding. Various plants are ­utilized. Some Nymphaloidea. Some specialists still include ­economic species are known, particularly on Riodinidae within Lycaenidae, and Libytheidae cabbages amd other crucifers. within Nymphalidae, and controversies about Lycaenidae (gossamer-winged butterflies) this continue. Extant butterflies number about total about 5,955 species worldwide; the actual 20,400 described species, but the actual butterfly fauna probably exceeds 7,000 species. About 1,125 fauna probably is about 23,500 species world- species are Neotropical. The family has eight wide, due to the numerous still unnamed small ­subfamilies. Adults are small to medium size and skippers (Hesperiidae) and blues (Lycaenidae). diurnal, but a few of the relict genera possibly Butterflies have 3-segmented, mostly upcurved ­crepuscular or only in dark forests. Larvae mostly labial palpi (only long and porrect in Libythei- somewhat slug-like, with tubercles and short setae; dae), small or vestigial maxillary palpi (1-seg- head usually retractable into thorax. Larvae feed mented), head scaling relatively smooth in most as leaf feeders (some on other plant parts), but groups, and a naked haustellum; antennae with many are myrmecophilous and some even are clubs (hooked at tip in Hesperiidae); forewings ­carnivorous on ant larvae or hemipterans. mostly triangular, while hindwings are ­usually ­Hostplants are in a wide variety of plant families, more rounded (sometimes with tails). Wing cou- but particularly Fagaceae and Leguminosae. A few pling via a humeral lobe rather than the frenu- economic species are known. lum-retinaculum arrangement of most moths. Riodinidae (metalmark butterflies) total Larvae with two lateral setae on the prothorax. about 1,419 species worldwide but predominate in Hesperiidae (skipper butterflies) include the Neotropics (1,322 sp.); the actual world fauna about 4,100 species from all faunal regions; most probably exceeds 2,500 species. Five subfamilies are Neotropical, with over 2,338 species. The actual are recognized. Adults are small to medium size world fauna probably exceeds 4,500 species. Seven and diurnal; often with rapid flight. Larvae are leaf skipper subfamilies are recognized. Adults are feeders, but many are myrmecophilous; one is small to medium size and diurnal, usually with known to be carnivorous on hemipterans. Larvae very rapid flight, but a few tropical species are mostly slug-like with short setae. Hostplants are ­crepuscular. Larvae are leafrollers or borers. recorded in numerous plant families. ­Hostplants are primarily grasses (Gramineae) and Libytheidae (snout butterflies) are a small other monocots. A few economic species are family of only 12 species, with at least one species known, particularly on rice. in each faunal region. Adults are medium size and Papilionidae (swallowtail butterflies) total diurnal. Larvae are leaf feeders. Hostplants are in about 589 species worldwide, with about 260 Ulmaceae. species being Indo-Australian, including the Nymphalidae (brush-footed butterflies) are largest of all butterflies, the birdwings. Three the largest family of butterflies, with about 7,080 subfamilies are recognized. Adults are medium described species worldwide; the actual fauna size to very large and diurnal. Larvae are leaf probably exceeds 8,000 species. To represent the feeders; with an osmeterium defensive gland division of relict basal groups within the family, behind head. Hostplants include many plant the subfamilies are divided into two groups: groups. Some economic species are known, Nymphalinina, with six subfamilies, and Satyr- mainly citrus feeders inina, also with six subfamilies. Adults are medium Butterflies and Moths (Lepidoptera) B 669 to large and diurnal, although crepuscular activity medium to large size and nocturnal. Larvae are is known in a few cases (some Amathusiinae and leaf feeders. Hostplants recorded so far only in Brassolinae). Larvae are mostly leaf feeders; a few Alangiaceae feeding gregariously. Hostplant records are among Drepanidae (hooktip moths) comprise 812 almost all higher plants. species worldwide, but predominately Oriental (647 sp.); none are known for the Neotropics and only a few are in the Nearctic; the actual fauna Drepanoidea probably exceeds 950 species. Three subfamilies are known. Adults are small to medium size and This superfamily includes four families perhaps nocturnal. Larvae are leaf feeders. Hostplants most related to Geometroidea. The branching and include a variety of plants. A few are economic. reticulate nature of evolution places the butterflies first after Geometroidea and before Drepanoidea when listed on paper, representing a more evolved Bombycoidea side branch. Some recent classifications have greatly disorganized this superfamily, placing ­Axiidae in its This superfamily includes many of the largest moths own monobasic superfamily (Axioidea) and merg- and encompasses 13 families and about 4,810 known ing Cyclidiidae and Thyatiridae into Drepanidae as species. The superfamily is divided into two groups: subfamilies: the latter three families all have some series Bombyciformes (Carthaeidae, Eupterotidae, cohesive features (e.g., abdominal tympanal organs) Apatelodidae, Bombycidae, Mimallonidae, Antheli- but also many unique features that provide evidence dae, and Lasiocampidae) and series Saturniiformes of family status. The superfamily comprises about (Endromidae, Lemoniidae, Brahmaeidae, Oxytenidae, 1,056 known species. Adults with head scaling Cercophanidae, and Saturniidae). Some ­specialists ­normal; haustellum normal (small or absent in use the series names for two superfamilies, or even some Drepanidae); labial palpi mostly upcurved; other superfamilies are added (such as Mimal- maxillary palpi mostly vestigial; antennae varied lonoidea), and there also is some confusion as to but mostly serrate of filiform; body generally robust; how many families are involved (e.g., Oxytenidae forewings mostly triangular or somewhat ­elongated; and Cercophanidae are sometimes included among and hindwings rounded. Larvae with two lateral Saturniidae by some researchers). Adults with head setae on the prothorax. scaling often roughened; haustellum mostly absent; Axiidae (gold moths) are a very small family labial palpi mostly upcurved but sometimes reduced; of only six Palearctic species in the Mediterranean maxillary palpi mostly vestigial or absent; antennae region. Adults are medium size and nocturnal. mostly bipectinate (also quadripectinate in Saturnii- Larvae are leaf feeders. Hostplants are in dae); body generally robust and often with hair-like Euphorbiaceae. setae; forewings mostly triangular and hindwings Thyatiridae (false owlet moths) comprise 224 rounded (some with long tails). Larvae with two lat- species from all regions except Australia, but most eral setae on the prothorax. are tropical Oriental (199 sp.); the actual fauna Carthaeidae (Australian silkworm moths) are probably exceeds 275 species. Two subfamilies are a monobasic relict family in Bombycoidea with a recognized. Adults are medium size and noctur- single species from western Australia. Adults are nal. Larvae are mostly nocturnal leaf feeders. Host- large and nocturnal (usually flying after midnight). plants are recorded in a number of plant groups. Larvae are leaf feeders, with numerous clubbed Cyclidiidae (giant hooktip moths) are a small setae. Hostplants are only in Proteaceae. family of 14 described species, all Oriental plus Eupterotidae (giant lappet moths) total 325 one species in the southern Palearctic. Adults are species worldwide (except the Nearctic), but most 670 B Butterflies and Moths (Lepidoptera) are Oriental (238 sp.); only four species are ­nocturnal. Larvae are leaf feeders. Hostplants recorded in the Neotropics. Three subfamilies are recorded in Betulaceae, Caprifoliaceae, Salicaceae, known. Adults are small to large and nocturnal. Tiliaceae, and Ulmaceae. Larvae are leaf feeders. Hostplants among numer- Lemoniidae (autumn silkworm moths) total ous different plants. Few species are economic 21 species, mostly Mediterranean. There are two (e.g., rice or forest pests). subfamilies. Adults are medium size and noctur- Apatelodidae (American silkworm moths) nal, but some males are diurnal; flight periods are are exclusively New World, and total 252 species, often in the autumn in Europe. Larvae are leaf mostly Neotropical (247 sp.). Three subfamilies feeders. Hostplants are mostly in Compositae and are used. Adults are small to medium size and noc- Euphorbiaceae. turnal. Larvae are leaf feeders. Hostplants are in Brahmaeidae (brahmin moths) are a small various plant families. family of 28 species, mostly Palearctic and African. Bombycidae (silkworm moths) total 166 There are two subfamilies. Adults are medium size described species, all Old World and primarily to very large and nocturnal. Larvae are leaf feed- ­Oriental (146 sp.), with only five species known for ers. Hostplants recorded in Asclepiadaceae and Africa. Two subfamilies are involved. Adults are Oleaceae medium size and nocturnal. Larvae are leaf feeders. Oxytenidae (American tropical silkworm Hostplants predominate in Moraceae. The silk- moths) include 60 species, all Neotropical. Adults worm (Bombyx mori) is used for silk production. are medium size to large and nocturnal. Larvae are Mimallonidae (sackbearer moths) total 254 leaf feeders; some mimic snakes. Hostplants species, all New World and primarily Neotropical recorded in Rubiaceae. (250 sp.). Adults are medium size and nocturnal. Cercophanidae (Andean moon moths) Larvae are leaf feeders, with larval cases. Host- include 30 species of mostly austral South Ameri- plants are recorded in a number of plant families. can moths. There are two subfamilies Adults are A few can be economic. medium size to large and nocturnal. Larvae are Anthelidae (Australian lappet moths) total leaf feeders. Hostplants recorded in Celastraceae, 100 species, all from Australia. There are two sub- Lauraceae, Saxifragaceae, and Tiliaceae. families. Adults are medium size to large; rarely Saturniidae (emperor moths) include 1,435 with micropterous females. Adults nocturnal, but species worldwide, but are predominately Neotro- at least one species with diurnal males. Larvae are pical (860 sp.). There are seven subfamilies. Adults leaf feeders and generally colorful. Host plants are medium size to very large and mostly noctur- recorded in several plant families. Some species nal or crepuscular, but some are diurnal. Larvae have urticating larval setae. are leaf feeders and many are polyphagous, some Lasiocampidae (lappet moths) include 2,130 being communal or gregarious; many are extremely species worldwide, with many in Africa (790 sp.). large. Hostplants are extremely varied. Some spe- Subfamilies are five. Adults are small to large; some cies are economic for agriculture, but major with micropterous females. Adults mostly noctur- urticating larvae are involved in dermatitis and nal but some males are diurnal. Larvae are leaf more severe allergic reactions, and in a few cases feeders, sometimes communally in silken tent-like even from adult scales. webbings. Hostplants are various. Some species are economic as tree defoliators. Endromidae (glory moths) are a monobasic Sphingoidea family of four species, from Europe to Central Asia. There are two subfamilies. Adults are medium This is a monobasic superfamily for the hawk size. Adult males are diurnal but females are moth family, Sphingidae. Some specialists include Butterflies and Moths (Lepidoptera) B 671 the family in Bombycoidea. Adults with head scal- family Arctiidae). Larvae with two lateral setae on ing mostly normal (sometimes roughened); haus- the prothorax. tellum often very long; labial palpi mostly Notodontidae (prominent moths) total 3,562 upcurved; maxillary palpi mostly small; antennae species from all faunal regions, particularly from the mostly clavate or lamellate and thickened; body Neotropics (1,766 sp.); actual world fauna likely robust; forewings mostly elongate-triangular and exceeds 4,000 species. The subfamily ­classification hindwings much smaller. Larvae with two lateral varies, but currently involves ten subfamilies, with setae on the prothorax. segregation into three groups: Oenosandrinina (for Sphingidae (hawk moths) total 1,230 species Oenosandrinae, with three species in Australia), worldwide. Tropical regions of the New World, ­Thaumetopoeinina (for Thaumetopoeinae), and Africa and Asia have the most biodiversity. There Notodontinina (for the remaining eight subfamilies). are three subfamilies. Adults are medium size to Adults are small to very large; some with massive very large and nocturnal or crepuscular, but some bodies. Adults are mostly nocturnal. Larvae are leaf a diurnal. Larvae are leaf feeders, usually with pos- feeders, sometimes gregarious (especially among terior horn-like scolus (thus, the common name, Thaumetopoeinae) and feeding nocturnally. Host- hornworms, for the larvae); many larvae extremely plants include a large variety of plant families, large. Hostplants recorded in numerous plant ­especially for broadleaf forest trees. A number of families. Some are economic. ­economic species are known. Dioptidae (American false tiger moths) total 507 species, primarily Neotropical (505 sp.); actual Noctuoidea fauna likely exceeds 800 species. Two subfamilies are known. Adults are medium size and mostly The largest superfamily, containing nearly a third nocturnal, but some are diurnal or crepuscular. of all lepidopterans, the Noctuoidea comprise Larvae are leaf feeders, particularly toxic plants about 44,025 described species, mainly in the in families like Aristolochiaceae, Euphorbiaceae, ­families Noctuidae and Arctiidae. Six families are Passifloraceae, and Violaceae, but also on various included in the superfamily: Notodontidae, Diop- others like Fagaceae. Very few are economic. tidae, Thyretidae, Lymantriidae, Arctiidae, and Thyretidae (African maiden moths) include Noctuidae. Numerous subfamilies among these 212 species, all African. Adults are medium-size. families have at various times been considered Adults perhaps mostly diurnal; often wasp mim- families, and various specialists are still undecided ics. Larvae are thought to be leaf feeders, but most on the number of families to use. For example, species remain unknown biologically. Hostplant Thyretidae are sometimes included in Arctiidae records include Thymelaeaceae and Ulmaceae. and Dioptidae are included among Notodontidae. Lymantriidae (tussock moths) total 2,490 spe- Contrarily, Oenosandrinae, Thaumetopoeinae, and cies worldwide; actual fauna likely exceeds 3,000 Doinae are often listed as separate families. Adults species. Most of the fauna is Old World tropical (ca. with head scaling mostly normal (rarely rough- 2,090 sp.). Two subfamilies are used. Adults are ened); haustellum naked (sometimes reduced); small to very large and mostly nocturnal, but some labial palpi mostly upcurved but many porrect or are diurnal or crepuscular. Larvae are leaf feeders, recurved; maxillary palpi mostly vestigial or absent sometimes gregariously. Hostplants include many (some larger in Notodontidae); antennae varied; different plant families. Many species are serious body mostly robust; forewings mostly elongate defoliators of forest trees. ­triangular and hindwings more rounded; body Arctiidae (tiger moths) include 11,155 species usually robust and with metathoracic tympanal worldwide, primarily Neotropical (ca. 6,000 sp.); organs (but absent or vestigial in Syntominae, actual world fauna likely exceeds 14,000 species. 672 B Butterfly Counts There are five subfamilies among groups: group Holloway JD, Bradley JD, Carter DJ (1987) Lepidoptera. In: ­Pericopinina (with Pericopinae), group Arctiinina CIE guides to insects of importance to man. 1. CABI and British Museum of Natural History, London, UK, (for Lithosiinae and Arctiinae), and group Ctenu- 262 pp chinina (for Ctenuchinae and Syntominae). Adults Kristensen NP (ed) (1999) Lepidoptera, moths and butter- are small to large; hindwings greatly reduced in flies. Vol. 1: Evolution, systematics, and biogeography. some groups (wasp moths). Adults mostly nocturnal In: Handbuch der Zoologie. Band IV. Arthropoda: Insecta. Teilband 35. W. De Gruyter, Berlin, Germany, but many are crepuscular or diurnal (Pericopinae, 487 pp Ctenuchinae, and Syntominae). Larvae are leaf Portier P (1949) La biologie le lépidoptères. In: Encyclopédie ­feeders. Hostplants are varied among numerous entomologique (A) 23:1–643, 1 pl. P. Lechevalier, Paris, France plant families, including mosses and lichens. Scoble MJ (1992) The Lepidoptera: form, function and Noctuidae (owlet moths) are the largest family ­diversity. Oxford University Press, Oxford, UK, 404 pp of Lepidoptera, with about 26,310 described ­species Stehr FW (ed) (1987) In Lepidoptera. In: Stehr FW (ed) worldwide; actual fauna likely exceeds 30,000 Immature insects [1]. Kendall-Hunt, Dubuque, Iowa, pp 288–596 ­species. Major regions of biodiversity are in the Vane-Wright RI, Ackery PR (eds) (1984) The biology of Neotropics (ca. 8,600 sp.) and the Indo Australian ­butterflies. Royal Entomological Society of London, region (6,500 sp.). Numerous subfamilies and tribes London, UK, 429 pp. (Reprinted 1989. Princeton ­University Press, Princeton, NJ) have been described and the classification is still in Watson A, Whalley PES (1975) The dictionary of butterflies flux, but 26 subfamilies are now recognized, mostly and moths in color. McGraw Hill, New York, New York, in group Noctuinina; also segregated are Aganainae 296 pp, 144 pl (previously in Arctiidae), in group Aganainina, and Young M (1997)The natural history of moths. T. & A. D. ­Poyser, London, UK, 271 pp, 16 pl Herminiinae, in group Herminiinina. Adults are small to very large and mostly nocturnal, but some are crepuscular and several groups are diurnal. Lar- vae mostly leaf feeders, but many are borers. Host- Butterfly Counts plants include numerous plant families, but the majority of owlet moths are not known biologically. linda wiener Some agricultural pests are included in the family St. John’s College, Santa Fe, NM, USA (e.g., cutworms, armyworms, and others).  Butterflies The North American Butterfly Association,  Butterfly Counts together with the Xerxes Society, coordinates the  Butterfly Gardening and Individual Families annual North American butterfly counts. Partici-  Conservation of Insects pants in this event pick a date, usually within two weeks on either side of July 4. On this date, the aim References is to count, in a 24 h period, the number of species of butterflies and the number of individuals of Bourgogne J (1951) Order des lépidoptéres. In: Grassé PP each species within a circle 15 miles in diameter. (ed) Traité de Zoologie. ­Anatomie, Systématique, Biolo- When the same locations are visited year after gie. Insectes 10:174–448, 3 pl. Masson, Paris, France year, a long term record of butterfly diversity and Eaton JL (1988) Lepidopteran anatomy. Wiley, New York, NY, abundance is available from each site. 257 pp Heppner JB (1991) Faunal regions and the diversity of This has been an annual event since 1975 ­Lepidoptera. Trop Lepid 2 (suppl 1):185 when there were 29 official counts. In 2000, 422 Heppner JB (1998) Classification of Lepidoptera. In: Holarctic counts were held; 349 in 44 states in the U.S., 66 Lepidoptera, 5 (suppl 1):1–148 (1998); 14 (suppl 1):149– 320 (2003); 15 (suppl 1): (in prep) Canadian counts in five provinces, and seven Hering EM (1925) Biologie der Schmetterlinge. J Springer, Mexican counts in three states. The purpose of the Berlin, Germany, 480 pp counts is to get long term records, over a wide Butterfly Counts B 673 Butterfly Counts, Table 11 Santa Fe Butterfly Count Results (Glorieta Canyon/Glorieta Peak)a* 1994 1995 1996 1997 SWALLOWTALLS Black Swallowtail 1 – -/5 Anise Swallowtail – – -/1 Western Tiger 14 4 1/3 Two-tailed Swallowtail 5 – 2/1 Pale Swallowtail 5 -/- WHITES AND SULFURS Pine White – – 6 -/- Checkered White 2 44 – 24/- Mustard White 37 11 – 12/- Orange Sulfur 13 30 1 19/13 Southern Dogface 2 – – -/- Mexican Yellow – 14 -/- Dainty Sulfur 1 29 2/- LITTLE BUTTERFLIES Colorado Hairstreak 1 -/- Great Blue Hairstreak 1 – -/- Coral Hairstreak – – 1 -/- Behr’s Hairstreak 7 1 – -/- Banded Hairstreak 72 38 2 10/- Western Pine Elfin – 1 – -/- Thicket Hairstreak 3 – – 1/- Juniper Hairstreak 2 – -/- Gray Hairstreak 1 – 1/- Leda Ministreak 1 – -/- Marine Blue 4 – – -/- Reakirt’s Blue 62 33 – 1/- Western Tailed-Blue – 2 1 -/- Melissa Blue – 2 – -/- Acmon Blue 5 4 – 1/- BRUSH-FOOTED BUTTERFLIES Variegated Fritillary 27 3 – 26/- Atlantis Fritillary 4 20 7 10/4 Arachne Checkerspot 16 – – -/1 Silvery Checkerspot 1 36 1 Northern Crescent – – 2 2/- Field Crescent – – 1 3/- Mylitta Crescent – 1 – 6/- 674 B Butterfly Counts Butterfly Counts, Table 11 (Continued)

Satyr Anglewing 1 Green Anglewing 1 – – Zephyr Anglewing 6 – 2 2/- Mourning Cloak 7 11 3 7/2 American Lady 5 7 – 1/- Painted Lady 20 1 5/7 West Coast Lady 10 – -/- Weidemeyer’s Admiral 3 3 5 21/1 California Sister 3 – – -/- Goatweed Butterfly 1/- SATYRS AND WOOD NYMPHS Canyonland Satyr 1 1/- Common Ringlet 2 – Small Wood-Nymph 74 45 86 27/7 MILKWEED BUTTERFLIES Monarch – 1/- SKIPPERS Silver-spotted Skipper 1 – – -/- Mexican Cloudywing 2 3 -/1 Northern Cloudywing 2 2 -/- Rocky Mountain Duskywing – 2 -/- Persius Duskywing – – – -/8 Afranius Duskywing 1 – – 3/- Common Checkered-Skipper 10 34 4 49/- Sootywing sp – – – 1/- Russet Skipperling 7 7 1 3/- Garita Skipperling – – – 1/1 Pahaska Skipper – – – 1/3 Tawny-edged Skipper 10 10 4 3/- Snow’s Skipper 6 – – Golden Skipper 41 17 16 4/- Dun Skipper 60 9 1 2/- Common Roadside-Skipper – 2 – Total species 36 32 20 35/17 (42) Total butterflies 519 455 146 258/61(319) Butterfly Gardening B 675 ­geographical area, of butterfly diversity and about host plants, habitat, habits and behaviors, ­abundance. A second, but equally important goal, and of course, butterfly identification. Many is to increase public awareness of insect conserva- ­people who show up out of curiosity come back tion. Consequently, counts are advertised and the year after year and find it a great pleasure to general public is invited to participate. Each group ­compare results from year to year. records every species seen as well as the number of For those who want more precise data individuals of each species. Other information ­generated in a more systematic manner, Pollard recorded is how many people counted, total num- transects are a good way to go. This technique ber of miles covered, and total amount of time in uses a transect route which is marked out and the field as well as information about weather and followed, usually once per week. The counter habitat. Annual results are published by the North walks at a standard pace and all butterflies within American Butterfly Association. a fixed ­distance of the path are counted. This The data obtained in these counts is, due to monitoring scheme is used in Great Britain and the uncontrolled conditions, not the most system- the Netherlands, and to a limited degree in the atic. However, it has still proven to be useful for United States. looking at large trends. For example, the count The accompanying table shows some typical data from 1989 to 1997 have been used to assess count data from the Santa Fe, New Mexico, but- patterns of species richness and abundance across terfly count Butterfly Counts From Areas of New North America. The log of party hours (number of Mexico, USA. hours spent making observations in the field was used summed across all groups in a single count References circle) to standardize species richness and abun- dance data. The study concluded that (i) species Kocher SD, Williams EH (2000) The diversity and abundance richness is highest in low latitudes and Rocky of North American butterflies vary with habitat, distur- Mountain longitudes, (ii) total abundance is high- bance, and geography. J Biogeogr 27:785–794 est in northern U.S. latitudes and Great Plains lon- North American Butterfly Association website. Available at gitudes, (iii) species richness increases with greater www.naba.org Pollard E, Yates TJ (1993) Monitoring butterflies for ecology topographical relief, and (iv) species richness and and conservation. Chapman and Hall, London, UK diversity indices are lower in more disturbed ­habitats. The North American Butterfly Associa- tion magazine, “American Butterflies,” publishes a count column which gives information about the Butterfly Gardening counts and analyses of results. Butterfly enthusi- asts interested in starting their own counts should jaret c. daniels visit the NABA web site www.naba.org. At this site University of Florida, Gainesville, FL, USA information is available on running and reporting a count and who to contact in your region about Butterfly gardening has become a very popular count locations which already exist. ­pastime in recent years. Planting a butterfly garden Butterfly counts are a wonderful way to is a simple and rewarding experience for both introduce children, parents, and other interested ­children and adults. If you like bird watching or individuals to butterflies. There does need to be flower gardening, you will love butterfly gardening! at least one experienced butterfly identifier in the Unlike most wildlife, butterflies are not strictly group, but everyone can run around and catch ­limited to remote natural areas. They are commonly them. There are numerous opportunities to teach found in both country and city and can easily be 676 B Butterfly Gardening attracted with a little know-how and the proper The Butterfly Life Cycle planning. A butterfly garden does not require much land; even a few strategic additions to an existing All butterflies go through a life cycle consisting of garden can make a big difference. four distinct developmental stages: the egg, the Whether it fits in a container on the patio larva or caterpillar, the pupa and the adult. Adult or stretches over several acres, a well-planned females typically deposit small eggs singly or in butterfly garden can be as simple or as compli- clusters on or near specific plant species. These cated as you want to make it. The same basic host plants provide growing larvae with the proper concepts and guidelines apply, regardless of nutrition they need to complete growth and the size. The most important thing to under- ­development. Larval host plants may also furnish stand before you begin is that butterflies have shelter, camouflage, and chemicals used for pro- many different behaviors, affinities, and needs. tection, courtship, and reproduction. Caterpillars Also, these requirements often change dra- (larvae) are herbivores (plant feeders) and have matically throughout their ­life-cycle. A well- very selective tastes. Each butterfly species only planned ­butterfly garden should provide feeds on specific plant species. Consequently, but- variety to attract different kinds of ­butterflies terfly larvae rarely become pests of vegetable and and cater to both adult butterflies and their ornamental plants, though they will greedily eat larvae. Proper choice of plants and ­landscape the host plants you provide for them. design is essential. Such decisions will help Butterfly larvae can grow at an astonishing ­determine which butterfly species will be rate, increasing in size and weight many times over attracted, remain in the area, and ultimately before reaching maturity. To accommodate this reproduce. tremendous change in proportion, each larva Why You Should Plant a Butterfly Garden molts numerous times during its life, revealing Butterflies are the most popular of all insects. each time a new and often radically different larval Besides being attractive, they play some important skin. Once fully grown, the larva seeks a safe place roles in the environment, including: to pupate. Most attach themselves to a branch, twig 1. Butterflies help pollinate a wide range of native and or other support by spinning silk. After a short cultivated flowering plants. rest, the larva molts for the last time to reveal the 2. Butterflies provide food for many other organisms. pupa, or chrysalis. Inside, larval structures break Various small mammals, ­nesting birds, lizards, spi- down and reorganize to form the adult butterfly. ders, and other insects all feed on adult butterflies or When environmental conditions are right, the their larvae. pupa splits open and an adult butterfly emerges. 3. Due to their tremendous appeal and popularity, butterflies often serve as “‘umbrella’” species. When butterflies are protected, their habitats and the other The Elements of a Butterfly Garden creatures that live there are also protected. 4. Butterflies are indicator species. They are among There are several simple guidelines that, if fol- the first organisms to show a ­negative reaction to lowed, will result in a successful butterfly garden: environmental changes and pollutants. Just like a Provide a combination of adult nectar sources ­canary in a coalmine, butterflies can help alert us to and larval host plants. A garden with both adult problems in the local environment that may affect nectar sources and larval host plants can accom- our own health and well-being. modate the entire life cycle of a butterfly. Having 5. Butterflies are a convenient way for you and your both adult and larval resources available will children to learn about insects, an abundant, impor- encourage adult butterflies to remain in your yard, tant, but poorly known group of organisms. reproduce, and build populations year after year. Butterfly Gardening B 677 Plant in both full sun and partial shade if you Weeds can be good for your garden. Many can. Most butterflies and their adult nectar sources common weeds serve as larval host plants. Care- are fond of bright sunlight. However, some butter- fully search each plant for larvae before you pull it flies are at home in woodlands or along forest out. If larvae are present, leave the plant alone until edges and rarely venture out into open, sunny they have finished feeding. areas. They often are more attracted to nectar Learn to identify the butterflies in your area. sources and larval host plants located in the shad- Become familiar with your local butterfly species. ier sections of the garden. Try to learn which ones are common, which ones Plan for consistent host plant and nectar are rare, and which ones you most want to attract. availability throughout the growing season. Then when it is time to choose the larval host plants Choose plants that bloom, grow or perform better for your garden, select your plants accordingly. at different times of the year, as well as plants hav- ing one peak season. The added variety insures that your garden will provide continuous food for Adult Nectar Sources butterflies. Plan for diversity. Choose plants that have a Adult butterflies are highly active, but short-lived. variety of different heights and growth habits. A During their brief adult period, they must find a diverse planting scheme helps to increase the mate, reproduce, seek out food and shelter, and number of microclimates and feeding levels avail- avoid being. To accomplish all this, most adult able to butterflies. Also, provide a mix of flower butterflies rely on sugar-rich nectar as fuel. colors, shapes, and sizes. Different butterfly species Nectar-rich, colorful flowering plants, there- have distinct color preferences, feeding behaviors, fore, are the backbone of any successful butterfly and proboscis (tongue) lengths. These factors garden. They draw in adult butterflies from the determine which flowers a butterfly chooses or is surrounding environment like a magnet while able to visit. A wide mix of adult nectar sources adding beauty and interest to the landscape. They provides accessible and attractive food to a greater also attract butterflies rapidly. Therefore, adult number of butterfly species. nectar sources should always be the first additions Plant in groupings. If space allows, try to com- to a new butterfly garden. bine several plants of the same species in a large When selecting flower colors, aim for a vari- grouping. Large drifts of color and clusters of veg- ety. While reds, pinks and purples are generally etation tend to be more apparent and attractive to the most attractive adult nectar source colors, a adult butterflies. Groups of larval host plants pro- great many butterfly species are also drawn to yel- vide larvae with additional resources in the event lows, blues, and whites. Each butterfly species has one is depleted, and help to mask leaf damage or its own color preferences. defoliation. Flower shape also influences visitation. In Include native plants. Native plants are well acquiring nectar, butterflies are limited by the length adapted to the soil type and climate of the region of their proboscis, or tongue. As a result, the nectar where they naturally occur and are not as prone to in long, tubular flowers is typically more accessible disease or pest attack. to butterflies possessing a longer proboscis. A but- Choose the appropriate plant for each loca- terfly’s behavior while feeding affects its flower tion. Determine the basic light, water, and soil choice as well. Many large swallowtail butterflies,­ for requirements of each plant before planting. For example, continuously flutter their wings while example, avoid putting a sun-loving species in ­nectaring. This enables them to feed much like hum- deep shade. This will insure ensure that your plants mingbirds, with access to flowers too delicate to land grow and perform to their maximum potential. on. On the other hand, many smaller butterflies such 678 B Butterfly Gardening as blues and hairstreaks prefer to feed while at rest. butterflies, mourning cloaks, malachites, buckeyes, They are strongly attracted to large clusters of small, as well as some satyrs and wood nymphs are also short-tubed flowers that form a stable platform on drawn to or feed solely on tree sap, rotting fruit, which to alight. dung or carrion. The greater the variety of flower colors, shapes, To accommodate their needs, simply place and sizes available, the greater variety of butterfly one or more shallow dishes on the ground at species will be attracted. Double- and triple-flow- various locations throughout the garden. Fill ered plants are the only major exception to this them with a selection of rotting fruit, banana rule. While such flowers produce spectacular peels, and melon rinds. Mash large pieces or blooms, they have been bred to impress humans, whole fruit to help increase the available surface not butterflies. In the process, external features area and expose the juicy interior. Once a week have been artificially manipulated, often at the or so, rinse out each dish with a garden hose and expense of nectar content or accessibility. refill. If ants are a problem, fill a slightly larger dish with water and set the smaller fruit dish in the center. This creates a small moat and­prevents Larval Host Plants the ants but not the ­butterflies from gaining access to the tasty meal. Larval host plants also are key ingredients to any successful butterfly garden. They are generally not as showy, nor are they absolutely necessary to attract Water adult butterflies. However, a garden composed solely of nectar plants provides nothing more than Males of many butterfly species commonly gather a simple, fast-food refueling spot. It completely at water sources such as stream banks, mud pud- ignores the requirements of the other stages of a dles, moist gravel or damp sand for access to water, butterfly life cycle. Consequently, adult butterflies dissolved salts, and amino acids. Such groupings come into the garden to feed but soon leave. can form rather impressive displays. For the more Larval host plants offer butterflies a reason ambitious butterfly gardener, artificial mud pud- to stay and not just pass through. Adults drawn dles or water stations can be created with varying into the garden by colorful nectar plants will now degrees of effort. find all the necessary resources to reproduce. You The simplest method is to fill a large plastic will soon notice some of the same individuals container, such as a sweater storage box, with sand. returning day after day and many of the same Locate an open, sunlit area of your garden, dig a butterfly­species becoming garden regulars. Most shallow hole, and place the container into the adult butterflies tend not to wander far from their ground so that the rim is even with the top of the larval hosts. Thus, you may notice a greater­number soil. Fill in any gaps around the outside of the con- of butterflies. Instead of just attracting individuals tainer with loose earth and thoroughly wet the from the ­surrounding area, your garden will pro- sand. The plastic container will hold in the water duce new adults from the maturing larvae present. and keep the sand moist for some time. The same process can be accomplished on a larger scale by lining an existing depression or Other Attractants newly dug hole with plastic. Simply make sure that the edges of the plastic are covered with soil Not all butterflies are exclusively attracted to flow- and fill the center with sand or small gravel. A ers. Many species, such as red-spotted purples, leaf slightly concave design will help moisture collect wings, question marks, tawny emperors, ­hackberry from occasional rain and regular garden ­watering. Butterfly Gardening B 679 The spray from a small garden fountain placed Avoid using pesticides. All butterfly life stages nearby can also help keep the ground consis- are extremely sensitive to pesticides. Even the tently moist. slightest drift from nearby spraying can be deadly. To make the area even more attractive, ini- If you want to have a butterfly garden, you must be tially mix in a small amount of table salt with the willing to tolerate insects, including some that eat sand or occasionally add a capful of natural fish the flowers. Try to allow the natural enemies of emulsion (an organic fertilizer available at most insects to take care of the insect problems. Even garden centers). Bacillus thuringiensis, or Bt, a natural bacterial disease of caterpillar pests that is normally consid- ered harmless because it does not affect most Shelter insects, people, or pests, can be deadly to butterfly larvae. If you must use insect control, always In addition to food and water, butterflies often choose the least toxic chemical first. Insecticidal need protection from wind, rain, temperature soaps and horticultural oils, for example, can be extremes, and predators. The easiest way to effective against many small garden pests. They accomplish this in the garden is to include many are harmless to humans and generally biodegrad- kinds of plants, including shrubs and small able. If the problem persists, move on to a stronger trees. Try also to cluster vegetation and add a chemical, but apply it selectively. Apply pesticides few nondeciduous species. Given time, as your only to the infested branch or plant and never treat garden grows and matures, the diversity of the entire garden. Choose short-lived (non-resid- plantings will naturally create several microcli- ual) products. Particularly avoid using systemic mates, or small localized environments, that pesticides on larval host plants. Unlike contact offer butterflies shelter. poisons, systemic pesticides are taken up by the plant. They kill when an insect eats the treated vegetation. Keeping the Butterfly Garden Trim off old blossoms. Periodic “deadheading,” Productive or removal of old, spent blossoms on your nectar plants, will encourage the continued production There are a few basic steps that will help you keep of new flowers. It can also extend the flowering your garden healthy, productive and looking its period of some species. best: Give new plants a good start. New plants can quickly become stressed. As a result, they are more Choice of Butterfly Plants vulnerable to disease and pest attack. They may grow poorly and even die if not properly attended. There- The choice of plants for your butterfly garden is fore, make sure to mulch and regularly water all new determined by several factors, including the amount plants. This will help reduce weed competition, keep of sun or shade, the soil and moisture conditions, them from drying out, and insure that they become and the climate where you live. Therefore, the firmly established. Healthy plants will reward you ­preferred plants vary from place to place, and for with vigorous growth and healthy blossoms. specific recommendations it is advisable to check Fertilize regularly. Routine fertilizer applica- with local butterfly gardening publications and edu- tions will help produce maximum plant growth and cational sources such as the cooperative extension flower production. Consult a local nursery specialist service in your area. As examples, following are lists or Extension agent if you have questions about of plants recommended for a northern climate, ­specific fertilizers or particular plant requirements. Nebraska, and a southern climate, Florida. Note that 680 B Butterfly Gardening although some plants are recommended in both Parsley - Petroselinum crispum {L,N} locations, few are recommended for both locations. Queen Anne’s Lace - Daucus carota {L,N} Sweet Fennel - Foeniculum vulgare {L,N} Thistle - Cirsium spp. {L,N} List of Plants to Attract Butterflies in Nebraska Shrubs Source: Nebraska Cooperative Extension Service, Nebguide G93–1183-A Butterfly Bush - Buddleia davidii {N} {L} = Larval Food Plants Cinquefoil - Potentilla spp. {N} {N} = Nectar Plants Chokecherry - Prunus virginiana {L,N} Cotoneaster - Cotoneaster spp. {N} Lilac - Syringa spp. {N} Annual Flowers Mock Orange - Philadelphus spp. {N} Privet - Ligustrum spp. {N} Ageratum - Ageratum houstonianum {N} Spirea - Spiraea spp. {N} Common Sunflower - Helianthus annuus {L,N} Viburnum - Viburnum spp. {N} Cosmos - Cosmos spp. {N} Wild Plum - Prunus americana {L,N} Fetid Marigold - Dyssodia papposa {L} Globe Candytuft - Iberis umbellata {N} Gomphrena - Gomphrena globosa {N} Perennial Herbaceous Plants Heliotrope - Heliotropium arborescens {N} Lantana - Lantana camara {N} Aster - Aster spp. {L,N} Marigold - Tagetes spp. {N} BeeBalm - Monarda spp. {N} Nasturtium – Tropaeolum spp. {N} Blanketflower - Gaillardia spp. {N} Nicotiana - Nicotiana alata {N} Butterfly Weed - Asclepias tuberosa {L,N} Petunia - Petunia x hybrida {N} Chrysanthemum - Chrysanthemum spp. (open- Salvia - Salvia spp. {N} centered types) {N} Scabiosa - Scabiosa atropurpurea {N} Clover - Melilotus spp., Trifolium spp. {L,N} Snapdragon - Antirrhinum majus {L,N} Coreopsis - Coreopsis spp. {N} Statice - Limonium sinuatum {N} Daylily - Hemerocalli s spp. {N} Sunflower - Helianthus spp. {N} Dogbane - Apocynum spp. {N} Sweet Alyssum - Lobularia maritima {N} Gayfeather - Liatris spp. {N} Verbena - Verbena spp. {N} Goldenrod - Solidago rigida {N} Zinnia - Zinnia spp. {N} Hollyhock - Alcea rosea {L} Ironweed - Vernonia spp. {N} Joe-Pye Weed - Eupatorium spp. {N} Biennials Mallow - Malva spp. {L} Milk-vetch - Astragalus spp. {L,N} Catnip - Nepeta cataria {N} Milkweed - Asclepias spp. {L,N} Chives - Allium schoenoprasum {N} Ornamental Onion - Allium spp. {N} Dame’s Rocket - Hesperis matronalis {N} Partridge Pea - Cassia fasciculata {L,N} Dill - Anethum graveolens {L,N} Phlox - Phlox spp. {N} Lavender - Lavender angustifolia {N} Pinks - Dianthus spp. {N} Mint - Mentha spp. {N} Prairie Clover - Dalea spp. {L,N} Butterfly Gardening B 681 Purple Coneflower - Echinacea spp. {N} Sweet Pepperbush - Clethra alnifolia Pussy-toes - Antennaria spp. {N} Virginia Willow - Itea virginica Rudbeckia - Rudbeckia spp. {N} Sedum - Sedum spp. {N} Vines Shasta Daisy - Chrysanthemum maximum {N} Yarrow - Achillea spp. {N} Bougainvillea - Bougainvillea sp. Coral Vine - Antigon leptopus Plants For Butterfly­ Gardening in Honeysuckle - Lonicera spp. Florida Mexican Flame Vine - Senecio Morning Glory - Ipomoea spp. Star Jasmine - Trachelospermum jasminoides Source: Your Florida guide to butterfly ­gardening. A guide for the Deep South Herbaceous Perennials

Trees Aster - Aster spp Bachelor’s Button - Centaurea sp. American Plum - Prunus americana Black-eyed Susan - Rudbeckia hirta Black Cherry - Prunus serotina Blazing Star - Liatris spp. Chaste Tree - Vitex agnus-castu Blue Sage - Salvia azurea Chickasaw Plum - Prunus angustifolia Bluebeard - Caryopteris chandonensis Coastal Plains Willow - Salix caroliniana Blue-eyed Grass - Sisyrinchium sp. Flowering Dogwood - Cornus florida Butterfly Weed - Asclepias tuberosa Hop Tree - Ptelea trifoliata Cardinal Flower - Lobelia cardinalis Mimosa - Albiza julibrissum Catchfly - Silene spp. Redbud - Cercis canadensis Cigar Plant - Cuphea micropetala Coral Vine - Antigon leptopus Coralbean - Erythrina heracea Shrubs Daylily - Hemerocallis sp. Deer Tongue - Carphephorus sp. Azalea - Rhododendron sp. Fire Spike - Odontonema strictum Blackberry - Rubus sp Firecracker Plant - Russelia equisetiformis Butterfly Bush - Buddleia davidii Frogfruit - Phyla nodiflora Button Bush - Cephalanthus occidentalis Garden Phlox - Phlox paniculata Chinese Privet - Ligustrum sinense Glorybower - Clerodendrum bungei Fire Bush - Hamelia patens Goldenaster - Chrysopsis sp. Glossy Abelia - Abelia x grandiflora Goldenrod - Solidago spp. Golden Dewdrop - Duranta repens Groundsel - Senecio spp. Hibiscus - Hibiscus sp. Heliotrope - Heliotropium arborescens Ixora - Ixora sp. Indian Blanket - Gaillardia pulchella Jatropha - Jatropha integerrima Indigo Bush - Amorpha fruticosa New Jersey Tea -Ceonothus americanus Ironweed - Vernonia spp. Plumbago - Plumbago capensis Joe-pye Weed - Eupatorium fistulosum Pride of Barbados - Caeselpina pulcherima Jupiter’s Beard - Centrantus ruber Red Buckeye - Aesculus pavia Lantana - Lantana sp. 682 B Butterfly Gardening Mexican Heather - Cuphea hysoppifolia Corky-stemmed Passion Vine (P. sub e ros a ), Gulf Fritil- Mexican Milkweed - Asclepias curassavica lary (Agraulis vanillae), Zebra Longwing (Helico- Mist Flower - Eupatorium coelestinum nius charitonius), Julia (Dryas iulia) Moss Verbena - Verbena tenuisecta Cudweed (Gnaphalium sp.), American Painted Lady Mountain Mint - Pycnanthemum sp. (Vanessa virginiensis) Obedient Plant - Physostegia virginiana Dill (Anethum graveolens), Black Swallowtail (Papilio Pentas - Pentas lanceolata polyxenes) Porter Weed - Stachytarphaeta jamaicensis Dutchman’s Pipe (Aristolochia sp.), Polydamus Purple Coneflower - Echinacea purpurea ­Swallowtail (Battus polydamus), Pipevine Swallo- Rattlesnake Master - Eryngium yuccifolium wtail (Battus philenor) Sandhill Milkweed - Asclepias humistrata False Indigo (Amorpha fruticosa), Dogface Butterfly Sedum - Sedum spp (Zerene cesonia) Shepherd’s Needle - Bidens alba False Nettle (Boehmeria sp.), Red Admiral (Vanessa Shrimp-plant - Beloperone guttata atalanta) Society Garlic - Tulbaghia violacea Fennel (Feoniculum vulgare), Black Swallowtail (Papilio Spotted Beebalm - Monarda punctata polyxenes) Stokes’ Aster - Aster laevis Frogfruit (Phyla nodiflora), White Peacock (Anartia ja- Sunflower - Helianthus sp trophae), Phaon Crescent (Pyciodes phaon) Swamp Milkweed - Asclepias incarnata Gerardia (Agalinus sp.), Buckeye (Junonia coenia) Tall Wild Verbena - Verbena brasiliensis Green Ash (Fraxinus pennsylvanica), Tiger Swallowtail Tropical Sage - Salvia coccinea (Papilio glaucus) Tuber Vervain - Verbena rigida Green Shrimp-plant (Blechum brownei), Malachite (Si- Verbena - Verbena sp proeta stelenes), White Peacock (Anartia jatrophe) Wild Petunia - Ruellia brittoniana Hercule’s-club (Zanthoxylum clava-hercules), Giant Yarrow - Achillea millefolium Swallowtail (Papilio cresphontes) Hop Tree (Ptelea trifoliata), Giant Swallowtail (Papilio cresphontes) Some Larval Host Plants and Species Indigo Bush (Indigofera sp.), Ceraunus Blue (Hemiar- Supported: gus ceraunus) Joint Vetch (Aeschynemone sp.), Barred Sulphur (Eure- Beggar’s-tick (Desmodium sp.), Long-tailed Skipper ma daira) (Urbanus proteus) Live Oak (Quercus virginiana), White M Hairstreak Black Cherry (Prunus serotina), Tiger Swallowtail (Parrhasius m-album) (Papilio­ glaucus), Red-spotted Purple (Limenitis Maypop (Passiflora incarnata), Zebra Longwing (Heli- arthemis astyanax) conius charitonius), Gulf Fritillary (Agraulis va- Blue Passionflower (Passiflora caerulea), Gulf Fritil lary nillae), Julia (Dryas iulia), Variegated Fritillary (Agraulis vanillae) (Euptoieta claudia) Camphor Tree (Cinnamonum camphora), Spicebush Mexican Milkweed (Asclepias curassavica), Monarch Swallowtail (Papilio troilus) (Danaus plexippus), Queen (Danaus gilippus) Cassia (Cassia sp.), Cloudless Sulphur (Phoebis sennae), Partridge Pea (Cassia fasciculata), Cloudless Sulphur Orange-barred Sulphur (Phoebis philea), Sleepy (Phoebis sennae), Little Sulphur (Eurema lisa) Orange (Eurema nicippe) Parsley (Petroselinium crispum), Black Swallowtail (Pa- Coastal Plain Willow (Salix caroliniana), Viceroy (Li- pilio polyxenes) menitis archippus floridensis) Pawpaw (Asimina sp.), Zebra Swallowtail (Eurytides Coontie (Zamia pumila), Atala (Eumaeus atala florida) marcellus) Buxton, Patrick Alfred B 683 Pencil Flower (Stylosanthes biflora), Barred Sulphur Swallowtail (Battus philenor), Polydamus Swallo- (Eurema daira) wtail (Battus polydamus) Plantain (Plantago sp.), Buckeye (Junonia coenia) Wax Myrtle (Myrica cerifera), Red-banded Hairstreak Red Bay (Persea borbonia), Palamedes Swallowtail (Pa- (Calycopis cecrops) pilio palamedes), Spicebush Swallowtail (Papilio White Ash (Fraxinus americana), Tiger Swallowtail troilus) (Papilio glaucus) Rue (Ruta graveolens), Black Swallowtail (Papilio poly- White Oak (Quercus alba), Banded Hairstreak (Satyri- xenes), Giant Swallowtail (Papilio cresphontes) um calanus) Ruellia (Ruellia sp.), Buckeye (Junonia coenia), Mala- White Sweet Clover (Melilotus alba), Gray Hairstreak chite (Siproeta stelenes), White Peacock (Anartia (Strymon melinus), Alfalfa Butterfly (Colias eury- jatrophe) theme) Saltwort (Batis sp.), Great Southern White (Ascia mo- Wild Lime (Zanthoxylum fagara), Giant Swallowtail nuste) (Papilio cresphontes) Sassafras (Sassafras albidum), Spicebush Swallowtail Winged Elm (Ulmus alata), Question Mark (Polygonia (Papilio troilus) interrogationis) Shepherd’s Needle (Bidens alba), Dainty Sulphur (Na- Winged Sumac (Rhus copallina), Red-banded Hairstreak thalis iole) (Calycopis cecrops) Slippery Elm (Ulmus rubra), Question Mark (Polygonia The butterfly web site: http://www.thebutterflysite.com/ interrogationis) gardening.shtml Smooth Water Hyssop (Bacopa monnieri), White Pea- cock (Anartia jatrophe) Southern Red Cedar (Juniperus virginiana), Swead nerís Hairstreak (Mitoura gryneus sweadneri) References Spicebush (Lindera benzoin), Spicebush Swallowtail (Papilio troilus) Daniels JC (2000) Your Florida guide to butterfly gardening: a guide for the Deep South. University Press of Florida, Sugarberry (Celtis laevigata), Hackberry ­Butterfly (As- Gainesville, FL terocampa celtis), Tawny Emperor (Asterocampa Minno M, Minno M (1999) Florida butterfly gardening. Uni- clyton), Question Mark (Polygonia interrogatio- versity Press of Florida, Gainesville, FL nis), Snout Butterfly (Libytheana bachmanii) North American Butterfly Association web site. Available at http://www.naba.org/pubs/bgh.html Swamp Bay (Persea palustris), Palamedes Swallowtail Tekulsky M (1985) The butterfly garden. The Harvard Com- (Papilio palamedes), Spicebush Swallowtail (Pa- mon Press, Boston, MA pilio troilus) Sweet Bay (Magnolia virginiana), Tiger Swallowtail ­( Papilio glaucus), Palamedes Swallowtail (Papi- lio palamedes), Spicebush Swallowtail (Papilio Buxton, Patrick Alfred t­ r o i l u s ) Toadflax (Linaria sp.), Buckeye (Junonia coenia) Patrick Buxton was born in 1892. He attended Tree Pawpaw (Asimina triloba), Zebra Swallowtail (Eu- Cambridge University in 1916–1921, and in those rytides marcellus) years completed his medical training and quali- Turkey Oak (Quercus laevis), Banded Hairstreak (Saty- fied with the degrees of M.R.C.S. and L.R.C.P. rium calanus) However, his attendance was disrupted by service Virginia Peppergrass (Lipidium virginicum), Checkered in World War I, during which he was stationed in White (Pontia protodice), Great Southern White Iraq (“Mesopotamia”) and Iran (“northwestern (Ascia monuste), Cabbageworm (Pieris rapae) Persia”). He concluded those studies in 1921, with Virginia Snakeroot (Aristolochia serpentaria), Pipevine a diploma in tropical medicine and hygiene. Then, 684 B Byrrhidae he accepted an appointment to the government of Reference Palestine (which later became Israel) as entomol- ogist, and worked there for two years. Next, he Hall WJ (1956) The president’s remarks. Proceedings of the joined a medical and scientific expedition to Royal Entomological Society of London (C) 20:73–77 Samoa. From the expedition resulted his publica- tions “Researches in Polynesia and Melanesia”; Byrrhidae and “Insects of Samoa.” In 1925, he was appointed director of the Department of Entomology of the A family of beetles (order Coleoptera). They com- London School of Hygiene and Tropical Medi- monly are known as pill beetles. cine, and from 1931 he also held the chair of medical  Beetles entomology in the University of London. He took numerous trips to Africa to work on Glossina and sleeping sickness, and from these visits resulted Byturidae his (1948) “Memoirs on trypanosomiasis in east- ern Africa”; and (1955) “History of tsetse flies.” He A family of beetles (order Coleoptera). They com- was elected a fellow of The Royal Society in 1947. monly are known as fruitworm beetles. He died in 1956. Beetles