Machadorythidae Machaerotidae Machilidae Mackenzie Globular

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Machadorythidae Macleay (Sir) William John

A family of mayflies (order Ephemeroptera). George Hangay  Mayflies Carrabeen, NSW, Australia

William John Macleay was born on June 13, 1820, Machaerotidae in Wick, Scotland. His parents died early and he had to discontinue his medical studies at Edinburgh University, and in 1839 he migrated to Australia. A family of bugs (order Hemiptera, suborder He accompanied his cousin, William Sharp Cicadomorpha). Macleay (a son of Alexander Macleay, the founder  Bugs of the greatest Australian natural history collection at the time, which later became known as the Macleay Collection and consequently the Macleay Machilidae Museum). For about 16 years he lived in the rural Murrumbidge area of New South Wales, chiefly as A family of bristletails (order Archeognatha). a pastoralist and woolgrower. His interest in natu-  Bristletails ral history was evident from an early age and he collected insects, many of which he described later on as new species. He also assisted his cousin in Mackenzie Globular Springtails various curatorial tasks at the Macleay Collection, then housed in Elizabeth Bay House, in Sydney’s Elizabeth Bay. When William Sharp Macleay died A family of springtails (Mackenziellidae) in the in 1865, the collection was entrusted to the care of order Collembola. William John, who left the Murrumbidge property  Springtails and moved into Elizabeth Bay House. By then he took a very active part in politics, eventually serv- ing seven successive parliaments over a period of Mackenziellidae 20 years. However, his main interest was natural history and within that entomology with coleopter- A family of springtails in the order Collembola. ology the focus. He became the main patron and They also are known as Mackenzie globular benefactor of science of his time, amounting to springtails. about 100,000 pounds (a very large sum at that  Springtails time), mainly spent on expanding and curating 2256 M Macquart, Pierre Justin Marie the collections, which contained more than a Reference million specimens. In 1874 he and his friends laid the foundations of the Linnean Society of New Papavero N (1971, 1973) Essays on the history of Neotropical South Wales. Several collectors hired by him worked Dipterology with special reference to collectors (1750–1905). Museu de Zoologia, Universidade de São the field, channeling a constant stream of specimens Paulo, São Paulo to the collections. George Masters was appointed as Curator, although Macleay himself described most species new to science. In 1875, he purchased the barque “Chevert” and organized a major expedition Macrofauna to New Guinea. In 1889 he was knighted, and two years later, on December 7, 1891 he passed away. A term used to describe the larger of the soil invertebrates, usually in the body width size range of 2–20 mm. (contrast with microfauna and References megafauna)

Fletcher JJ (1893) The Macleay memorial volume. Linnean Society of New South Wales, Sydney, pp 7–51 Macropsyllidae Musgrave A (1930) The history of Australian entomological research. Aust Zool 6:189–203 A family of fleas (order Siphonaptera).  Fleas Macquart, Pierre Justin Marie Macropterous P. J. M. Macquart was born at Hazebrouck, France, in 1776. Much of the family was inter- Having long wings. (contrast with brachypterous) ested in natural history, so it is not surprising that Macquart became interested in insects. He served in the military starting at the age of 21, Macroveliidae visiting Germany, Switzerland, and Austria, which provided an opportunity to collect speci- A family of bugs (order Hemiptera). mens and books. Upon his return home in 1798  Bugs he devoted himself to his studies, and came to know the great French entomologist Latreille. He came to specialize in Diptera, publishing Maculate “Diptères du nord de la France” (1828–1833). He then was invited by Latreille to participate in a This describes an object that is marked with irreg- group effort, with Macquart handling the Dip- ular spots. tera, which became known as “Histoire naturelle des Insectes Diptères.” (1834, 1935). Macquart acquired the holdings of Meigen, and tackled the Maggot job of describing all the new species acquired by French naturalists from around the globe. In this An elongate, legless larva that lacks a well-developed monumental effort, he described 1,800 new spe- head. This term usually is reserved for larvae of flies cies. He continued to publish updates of his work (Diptera). until his death in 1855.  Flies Maggot Therapy M 2257 Maggot Therapy troublesome, they expedited the healing of the wounds by shortening the work of nature, and Susan V. Gruner causing the sloughs to fall off.” During the Ameri- University of Florida, Gainesville, FL, USA can Civil War, military surgeon W. W. Keen noted that “maggots were very common in summer – the Maggot therapy, or maggot debridement therapy, resulting maggots were certainly disgusting but is the medicinal use (biotherapy) of live fly larvae so far as I ever observed they did no harm.” J. F. (maggots) for cleaning non-healing wounds and Zacharias of Cumberland, Maryland, USAMD, a osteomyelitis (bone infection). Maggots debride, surgeon for the Confederate Army, wrote, “I first or clean, wounds by eating necrotic (dead) tissue. used maggots to remove the decayed tissue in hos- They secrete therapeutic chemicals such as ammo- pital gangrene and with eminent satisfaction. In a nia and calcium carbonate, which disinfect wounds single day they would clean a wound much better and promote healing. Only larvae that eat dead tis- than any agents we had at our command”. sue (usually calliphorids from the genus Lucilia) During World War I, soldiers with compound can be used for medicinal purposes (Table 1). femur fractures and abdominal wounds, with the Obviously they must display no invasive behavior best of medical care, had only a 75% chance of to living tissue. survival. Those that had maggots in their wounds For centuries, maggots have been used to help were more likely to survive. William Baer, an heal wounds. Historically, it has been military sur- orthopedic surgeon at Johns Hopkins University, geons who noticed the benefits of maggot-infested was the first physician in the USA to promote wounds. One of Napoleon’s surgeons noticed that maggot therapy. His research and results were maggots consumed only putrefying tissue and that published posthumously by his colleagues in the they seemed to promote wound healing. The sur- Journal of Bone and Joint Surgery in 1931. By 1932, geon, Baron Dominic Larrey, stated that “during approximately 300 hospitals in Canada and the US the progress of suppuration, the patients were were using maggot therapy to heal deep tissue only troubled by worms or larvae of the blue flies wounds. Hospitals stopped using maggots in the common in Syria although these insects were 1940s as better antibiotics became available. Though still useful, maggot therapy has been marginalized by the medical community, as has Maggot Therapy, Table 1 The species of flies used use of leaches and some other medical procedures, in maggot therapy (adapted from Sherman et al. but occasionally these approaches remain very 2000) useful. Renewed interest in maggot therapy has Family Species been generated in response to an increase of chronic wound infections that are resistant to anti- Calliphoridae Calliphora vicina biotics. Chronic wound infection is a problem that Chrysomya rufifacies costs billions of dollars worldwide. Wound tissue Lucilia caesar provides a perfect environment for proliferation Lucilia cuprina of bacteria. Wound infection is compounded by Lucilia illustris the widespread occurrence of antibiotic-resistant Lucilia sericata “superbugs.” Maggots secrete antibacterial activ- Phormia regina ity against a range of these superbugs which Protophormia terraenovae include Gram-positive Staphylococcus aureus, Sarcophagidae Wohlfahrtia nuba both methicillin-resistant S. aureus (MRSA), and methicillin-sensitive S. aureus (MSSA), and S. pyo- Muscidae Musca domestica genes. Additionally, larval secretory products can 2258 M Mahogany Pests and Their Management withstand lyophilization (freeze drying) and long- drainage from the wound. Sterile maggots, at a term storage. These secretions may be a potential density of approximately 5–8 per cm2, are placed source of antibiotic-like compounds for treatment on the wound for one 48 h cycle per week. of MRSA. According the BioTherapeutics Education Before use, medicinal maggots are sterilized and Research Foundation, current use of maggots internally and externally. Eggs from adult flies are for wound therapy involves approximately 3,000 sterilized in solutions containing formalin or mer- doctors, clinics and hospitals in over 20 countries, curic chloride, alcohol, hydrochloric acid, dilute including Germany, Britain, Israel, Australia and sodium hypochlorite or prolonged immersion in Japan. In 2004, “medical maggots” were approved hydrogen peroxide. Hatched larvae are placed on a by the FDA as a medical device; however, only a sterile food source and are ready to be used medic- single laboratory in California has been approved inally after two days of growth. Sterile maggots are for production and distribution of medicinal mag- placed on wounds within a cage-like structure or a gots in the USA. sealed pouch for 2–4 days. The maggots are removed and new ones are applied as needed. Most patients, after an initial period of adjustment References (as would be expected), adapt well to the presence of maggots. Baer WS (1931) The treatment of chronic osteomyelitis with Maggot therapy is generally limited to non- the maggot (larva of the blow fly). Am J Bone Joint Surg 13:438–475 acute external wounds that have failed conventional Kerridge A, Sappin-Scott H, Stevens JR (2005) Antibacterial treatment. Treatment is protracted, so if the ailment properties of larval secretions of the blowfly, Lucilia is life threatening, surgery is normally recommended sericata. Med Vet Entomol 19:333–337 rather than maggot therapy. Medicinal maggots pro- Nigam Y, Bexfield A, Thomas S, Ratcliffe NS (2006) Maggot therapy: the science and implication of CAM, Part I – vide three forms of benefit: debridement or elimina- History and bacterial resistance. Evid based Comple- tion of dead tissue, disinfection of the wound by ment Alternat Med 3:303–308 elimination of microbes, and promotion of wound Sherman RA, Hall MJR, Thomas S (2000) Medicinal maggots: healing. Elimination of necrotic tissue is easy to an ancient remedy for some contemporary afflictions. Annu Rev Entomol 45:55–81 imagine, but the antimicrobial maggot exudates are Sherman RA, Pechter EA (1988) Maggot therapy: a review of more important in eliminating infection and in pro- the therapeutic applications of fly larvae in human med- moting wound repair. The species that have been icine, especially for treating osteomyelitis. Med Vet Entomol 2:225–230 used in maggot therapy are shown in Table 1. Inter- estingly, the species most commonly used, Lucilia sericata, is a pest to the sheep industry in some regions of the world. Lucilia cuprina must be used Mahogany Pests and Their with care as it has a tendency to cause myiasis. Management The actual application of maggots to a wound is rather simple. Prior to application, a hole match- F. W. Howard ing the shape and size of the wound is cut out of a University of Florida, Fort Lauderdale, FL, USA hydrocolloid pad, which prevents wound drainage from further contamination of surrounding Mahoganies are the source of an exceptionally healthy skin. Next, Dacron® chiffon is placed over valuable cabinet wood, and are widely considered the hole in the hydrocolloid pad, which creates a the most economically important tropical timber cage-like structure that prevents the maggots from trees in the world. Thus, the insects that attack crawling away. The dressing is further covered mahoganies are of considerable economic impor- with a layer of gauze, which absorbs necrotic tance. True mahoganies include three species of Mahogany Pests and Their Management M 2259 Swietenia (family Meliaceae) that are native to the Hypsipyla spp. (Lepidoptera: American Tropics. These are West Indies mahog- Pyralidae: Phycitinae) any (S. mahagoni Jacquin), Honduras, or big-leaf, mahogany (S. macrophylla King), and Pacific The most important pests of mahoganies are moths mahogany (S. humilis Zuccarini). in the genus Hypsipyla (Lepidoptera: Pyralidae: West Indies mahogany is native to the Greater Phycitinae), whose larvae bore into the shoots and Antilles except Puerto Rico, with its native range seed capsules of mahoganies and their relatives. extending north of the tropics proper to southern The genus includes one species in Tropical America Florida and some islands of the Bahamas. Exploi- and several in the tropics of the Eastern Hemi- tation of West Indies mahogany began early in the sphere. The American species,Hypsipyla grandella European colonial period, especially in Cuba, (Zeller), is known as the mahogany shoot borer. It Hispaniola, and Jamaica, and by the twentieth cen- is considered the most important pest of mahoga- tury the species was greatly depleted from natural nies in the Americas because its damage can reduce areas by excessive logging. It remains a popular growth in height and cause distorted growth of the shade tree in urban areas of southern Florida, the main stem. Damage by this shoot borer is a major Antilles, Bermuda, and other areas with a tropical impediment to establishing and growing mahoga- climate, and potentially could be restored as a nies in plantations. It is also a serious pest of plantation or forest tree. mahoganies grown in nurseries for use as orna- By the twentieth century, mahogany logging mentals. Hypsipyla grandella is distributed in had largely shifted to Honduras mahogany, which southern Florida, the West Indies, northern Mexico is native to mainland Tropical America. This spe- southward through Central America, and South cies occurs in lowland humid regions from about America except Chile. This distribution coincides 23°N latitude on the Atlantic side of Mexico with that of its host plant species, i.e., mahoganies though Central and South America to about 18°S and other tropical meliaceous trees. latitude in Bolivia. Currently, Honduras mahogany Hypsipyla robusta (Moore) plays a similar role is the commercial source of almost all mahogany as an important shoot borer of African mahoganies wood. It is being severely depleted in many areas, and other meliaceous trees in the tropics of the and research and conservation are greatly needed Eastern Hemisphere. The distribution ofH. robusta to conserve this species. Pacific mahogany is dis- was formerly reported as extending from Africa to tributed in a narrow zone along the relatively dry Tropical Asia, Australia, and some Pacific islands, Pacific. but H. robusta as currently understood is a species Khaya is a genus closely related to Swietenia complex and its taxonomy is being resolved. Hyp- with about seven species distributed in Africa. sipyla robusta and perhaps other species of this com- These species are collectively known as African plex have been variously referred to as the toona mahoganies. There are many similarities between fruit and shoot borer, cedar tip moth, cedar shoot Swietenia and Khaya in structure, utilization, and caterpillar, and also in some countries as the mahog- ecology including relationships with insects. any shoot borer. Hypsipyla grandella and H. robusta The family Meliaceae contains several addi- have been the subject of considerable research. Since tional genera and species of large tropical timber the various species of Hypsipyla are very similar trees, notably Cedrela spp., known as cedros or insects in appearance, biology, economic impact, tropical-cedars, an important local wood source and in the approaches to managing them as pests, throughout Tropical America, and Toona spp., this discussion will focus on H. grandella, which is which is widely distributed in Australia and East the better known of the two species (Fig. 1). Asia. Some of these are hosts of the same or simi- The adults ofH. grandella are grayish–brown in lar insects that attack mahoganies. color with a wingspan measuring about 23–45 mm. 2260 M Mahogany Pests and Their Management

Mahogany Pests and Their Management, Figure 1 Mahogany insects: (a) The larva of the mahogany shoot borer, Hypsipyla grandella; (b) A shoot of West Indies mahogany, Swietenia mahagoni, damaged by the mahogany shoot borer, Hypsipyla grandella; (c) A seed capsule of West Indies mahogany, Swietenia mahagoni, with boring damage of the mahogany shoot borer, Hypsipyla grandella; (d) The mahogany webworm, Macalla thyrsisalis; (e) The abaxial surface of a leaflet with the larva of the mahogany leaf miner, Phyllocnistis meliacella within the mine; (f) Leaf mines of the mahogany leaf miner, Phyllocnistis meliacella, in leaflets of West Indies mahogany, Swietenia mahagoni (photos by F.W. Howard). Mahogany Pests and Their Management M 2261 They are nocturnal and oviposit during the early Small trees whose terminal shoots are attacked morning hours on leaf scars, new shoots, leaf veins repeatedly in successive years become extremely and fruits (seed capsules). The eggs hatch in several deformed. Because attacks ultimately result in a days. Recently emerged first instar larvae may begin reduction in the number and length of straight, feeding on the surfaces of the leaves or other plant clear logs, H. grandella is a major pest of mahoga- parts, then bore into new shoots or seed capsules. nies, cedros, and some other meliaceous tropical The total development time including the larval, trees grown as timber. Mahogany shoot borer prepupal, and pupal stages, is usually one to two attack reduces the grade and thus the monetary months and may be extended if the larvae undergo value of young mahoganies grown in nurseries diapause. for use as shade trees, their chief use in southern Larvae that bore in shoots produce a tunnel Florida and urban areas in various tropical countries. of several centimeters in length and expel frass Damage to seeds by H. grandella has usually from the tunnel entrance as a reddish–brown mass been regarded as unimportant or second in impor- which becomes intertwined with the insect’s silk. tance to the damage to the shoots, as seeds are thought The hollowed out portion of the shoot dies and the to be produced abundantly enough to compensate shoot buckles. for losses to the shoot borer. However, in a study in In southern Florida, where the rainy season southern Florida, H. grandella attacked up to 100% usually begins in May or June, and the flush of West of the seed capsules of West Indies mahogany trees Indies mahogany takes place from April to June, and consumed 50–96% of the seeds per capsule. H. grandella attacks shoots from early spring to During the same period, only 14–22% of new shoots mid-summer, with pronounced peaks in May. Pop- on the same trees were attacked. The impact of this ulation surges in spring, i.e., at the beginning of the insect on regeneration should be investigated further, rainy season, also have been observed in some especially in natural areas and managed plantations. studies in the tropics. But generally in the tropics, Management. Considerable research has been H. grandella is active all year with high shoot borer conducted to develop methods of managing Hyp- activity typically coinciding with flushes of mahoga- sipyla shoot borers. This insect is notoriously dif- nies subsequent to periods of high rainfall. ficult to control, primarily because although some Hypsipyla grandella also attacks seed capsules methods reduce the pest population considerably, of mahoganies and cedros, penetrating between even light populations can cause significant dam- the valves of the capsules when they have dehisced. age. In fact, destruction of the leader, which is the There they bore into seeds and hollow them out, most critical damage, is caused by a single larva. after which they bore into the core of capsules. The A review of published information on chemical pupal stage takes place inside the hollowed por- control of Hypsipyla spp. shoot borers reported tions of the twig or seed capsule, or in the leaf litter that after more than eight decades of research in or soil beneath host trees. 23 tropical countries there is still no reliable, cost- Damage. Mahogany trees are susceptible to effective, and environmentally sound chemical con- attack beginning when they reach a height of about trol method available to prevent economic damage 0.5 m. The shoot borers may attack both the termi- by these insects. However, chemical control of these nals of side branches and the leader (central termi- pests might be appropriate in nursery situations. nal). Boring of the leader causes the more serious About 40 species of insects have been identi- damage to the form of the tree, because this breaks fied as natural enemies of H. grandella in the apical dominance, resulting in excessive side- Americas. As a natural enemy complex, they branching, and more importantly, in the replace- undoubtedly are important in regulating popula- ment of the leader with one or more lateral branches tions of this insect, but their effect is generally and thus the formation of a crooked main stem. insufficient to prevent economic damage. 2262 M Mahogany Pests and Their Management Mahoganies growing at low densities in mixed The adult is a small gray–brown moth with forests are generally less frequently attacked by whitish hindwings. They are probably nocturnal. H. grandella than mahoganies in pure plantations. Their peak flight period is in late winter or early This and other ecological principles have been spring prior to the annual flush of mahoganies. The applied in silvicultural techniques to reduce shoot eggs have not been observed in nature, and possi- borer damage, with varying degrees of success. bly are eaten by the recently hatched larvae, as is In testing different provenances of mahoga- known in many Lepidoptera. The larva has a vivid nies and cedros, less damage has been seen in yellow ground-color and lateral bands that consist some selections. Research to identify genetic of three narrow black stripes alternating with two strains of these trees that are resistant or that can white stripes. Each larva spins a web to pull several overcome shoot borer attack has progressed well. leaves together, and remains partially hidden in the An international workshop on Hypsipyla shoot resulting leaf cluster, consuming laminar tissue borers held in 1996 (online at http://aciar.gov.au/ from the margins of leaflets inward, leaving the web.nsf/doc/JFRN-5J472Q), in which 36 papers midveins intact. The larval stage is completed in were presented, concluded that the strategies most about 10 days, and multiple generations may be promising for management of these pests involved produced during the spring season, so that by mid- identification and use of resistant genotypes, and spring webworm populations may consist of larvae silvicultural methods, viz., growing mahogany in early and late instars. As with the mahogany and cedro trees in mixed rather than pure stands shoot borer, their presence on their host trees coin- and under an established canopy. It was also cides with the period of spring flush and leaf emphasized that vigorous growth of young trees expansion of mahogany. The webworm larvae feed should be promoted by cultural methods in the on young leaves before they have matured and nursery and in young plantations. Chemical con- hardened off. Dense populations of these caterpil- trol was seen as a tool for temporarily reducing lars may entirely strip a tree of foliage. shoot borer populations in limited areas. In southern Florida, several years of annual In addition to Hypsipyla species, several other spring outbreaks of mahogany webworms have insect species that are specific feeders on mahoga- alternated with periods of years in which popula- nies and close relatives sometimes cause signifi- tions are diminished, but there has been no long- cant damage. In the Americas, these include a term monitoring to record the patterns of outbreaks. defoliator, a leaf miner, a bark weevil, and a scale Possibly, outbreak cycles of mahogany webworm insect (Fig. 2). are related to cycles of their parasitoid populations. In southern Florida and presumably throughout its native range, the mahogany webworm is under Mahogany Webworm, Macalla natural control. A fly, Lespesia n. sp. (Diptera: thyrsisalis Walker (Lepidoptera: Tachinidae) and two species of wasps, Habrobracon Pyralidae: Epipaschiinae) sp. and Apanteles sp. (Hymenoptera: Braconidae), are parasitoids of mahogany webworm in southern The mahogany webworm is a defoliator of mahog- Florida. anies reported from throughout most of the range When parasitoids and other natural control of mahoganies in the Americas. Nearly all records factors fail to adequately control mahogany web- in Tropical America are based on trap catches of worms, landscape or nursery managers may resort the adult, with no data on the larva and its hosts. It to chemical control. In the interest of discovering has not been reported as a pest except in southern a safe treatment with minimal negative environ- Florida, and the biology of this species has been mental effects, a study was conducted involving studied only in that locality. foliar applications of a neem product. It was Mahogany Pests and Their Management M 2263

Mahogany Pests and Their Management, Figure 2 More mahogany insects: (a) The mahogany bark weevil, Copturus floridanus, resting on bark of the West Indies mahogany, Swietenia mahagoni; (b) A leaflet of West Indies mahogany, Swietenia mahagoni, with feeding damage of the adult mahogany bark weevil, Copturus floridanus; (c) Galleries of the mahogany bark weevil, Copturus floridanus, beneath the bark of West Indies mahogany, Swietenia mahagoni. A cocoon is at upper right in photograph; (d) Exit holes of the mahogany bark weevil, Copturus floridanus, in the bark of West Indies mahogany, Swietenia mahagoni (photos by F. W. Howard).

determined that the product acted as an antifeed- probably some other meliaceous trees. It was ant against this pest, and when applied early in the described from specimens from Honduras mahog- development of an infestation, it prevented any in Costa Rica, and during certain years is com- mahogany webworm attack on the treated trees. mon on West Indies mahogany in southern Florida. More recently this species was listed as an insect on cedro in Tamaulipas, Mexico. Although not Mahogany Leafminer, Phyllocnistis reported elsewhere, it is probably widely distrib- meliacella Becker (Lepidoptera: uted throughout the range of mahoganies in the Gracillariidae) Americas, but seldom noticed. In fact, an uniden- tified leaf mine identical to that of P. meliacella is The mahogany leafminer attacks foliage of visible in a photo of leaves of Cedrela odorata in Honduras and West Indies mahogany, cedro, and Venezuela in a paper on mahogany shoot borer 2264 M Mahogany Pests and Their Management published 12 years prior to the publication of the and texture blend well with the bark of mahog- taxonomic description of P. meliacella. any, upon which they rest for long periods during The adult of the mahogany leafminer is a the day, flying quickly when disturbed. They are minute white moth about 2 mm long from the often seen feeding on the leaf lamina, leaving apex of the head to the folded-back wings. The closely grouped small feeding holes, which even- apodous, wormlike, white larva consumes leaf tually become surrounded by brown necrotic leaf mesophyll, creating a winding gallery in the leaflet tissue. The females bore similarly small holes (mahoganies leaves are compound, with 5–7 leaf- through the bark to the cambium, then turn lets) that eventually terminates in the leaflet around and oviposit in them. margin, which the larva rolls. Pupation takes place The larva is small, apodous, ivory colored, and within the rolled margin. Several hymenopterous has the typical c-shape of weevil larvae. They feed species are parasitoids of the mahogany leafminer in the cambium of mahoganies, producing wind- in Florida. ing galleries, and construct a cell in which they The mahogany leafminer is generally con- pupate. Development is completed in three to six sidered a minor pest at most, and has received months. Adults and larvae are present all year in little study. In observations in a research plant- Florida. ing in Florida during spring 1993, which was a The feeding damage of the adult weevils on year when mahogany leafminer damage was rel- the leaves of a mahogany tree serves as an indica- atively extensive, 62% of the leaves of young tor that the mahogany bark weevil adults are pres- West Indies mahoganies had at least one leaf ent in the area, but does not necessarily imply that mine made by this insect, and 8.8–12.4% of the the same tree is infested with bark beetle larvae. A leaflets were mined. The amount of leaf tissue mahogany bark beetle infestation may result in consumed by one larva is undoubtedly very the formation of drops of a reddish–brown resin- small, but mined leaflets become distorted and ous exudate on the bark, although these may be a stunted and may be shed early. Nevertheless, the result of almost any kind of injury to mahogany effects on tree vigor of mahogany leafminer stems. The presence of round exit holes of about damage, even when populations are high, are 3 mm in diameter in the bark is a stronger indica- presumably negligible. In a test of a neem prod- tor that a tree is infested with the larvae. The holes uct to control mahogany shoot borer, the treat- indicate that weevils have completed development suppressed shoot borer attack and also ment in the tree and it can ordinarily be assumed acted as a preventative against mahogany leaf that additional weevils are still in the larval stage miner damage, but treatments applied specifi- beneath the bark. In Florida, mature mahogany cally to control the leafminer would probably bark weevils are commonly seen in low numbers seldom be economically justifiable. on the bark of mahoganies in plantings where there is no visible borer damage to mahogany trees except for exit holes in or near dead branches. Mahogany Bark Weevil, Copturus Extensive damage to the main stem appears to floridanus (Fall) (Coleoptera: occur mostly on stressed trees, as when trees are Curculionidae) severely damaged by hurricanes or growing under excessively wet conditions. Mahogany saplings The mahogany bark weevil is reported in the transplanted during drought periods are said to Bahamas, Cuba, and southern Florida. The adult be highly susceptible to attack. Thus, like stem weevils are about 4–6 mm long and 3 mm in borers in general, the mahogany bark weevil is width, and dark grey–brown, with patches of fine regarded as a secondary pest which can be man- whitish speckling on the elytra. Their coloring aged by horticultural or silvicultural techniques. Mahogany Pests and Their Management M 2265 West Indies Mahogany Scale, genetics and breeding, there is almost nothing Conchaspis cordiae Mamet known concerning their pollination, except for (Hemiptera: Conchaspididae) results of some observations in southern Florida indicating that the pollen of West Indies mahog- Mahoganies tend to be relatively free of scale any is adapted to entomophily, and various species insects, but West Indies mahoganies were recently of thrips (Thysanoptera) are abundant in mahog- found to be highly infested with West Indies any flowers and apparently transfer the pollen mahogany scale, over a broad area of southern between flowers. No other insects have been impli- Florida, where this scale insect was apparently cated as potential pollinators of mahoganies in accidentally introduced. This species, which is in southern Florida. However, southern Florida is the small and relatively unstudied tropical scale where the West Indies mahogany is isolated at the insect family Conchaspididae, is native to several northern extreme of its natural range, and can be islands of the Caribbean, where it is apparently considered a recent arrival in the context of geo- under natural control factors. In Florida, 5–8% of logical time. Possibly, within the principal range of scale coverings of C. cordiae had parasitoid exit mahoganies in the tropics, pollination of mahoga- holes, and a parasitoid, Marietta sp., was reared nies is accomplished by other insects. That there is from this scale insect. an effective pollination system present in Florida Although this scale insect has been reported is evident in that mahoganies here are typically on mahoganies, Cordia sp. and seagrape (Cocco- highly productive of fruits, i.e., seed capsules. loba uvifera L.) in its native range, it has been Research on insects associated with mahoga- observed only on mahoganies in Florida, and nies has focused almost entirely on Hypsipyla spp., shows a strong preference for West Indies mahog- with far less attention to the other pests noted in any as compared to Honduras mahogany and this discussion. In the natural habitats of mahoga- Khaya nyasica (Stapf.). Heavy infestations occur nies, there are undoubtedly many additional spe- on twigs and branches of up to about 6 cm in cies of insects associated with them that have not diameter, but no more than light infestations have been studied. been seen on larger branches and main stems. Although it has become widely disseminated in southeastern Florida, it has not yet caused serious References damage to mahoganies. Floyd RB, Hauxwell C (2001) Hypsipyla shoot borers in Meliaceae. In: Floyd RB, Hauxwell C (eds) International Workshop on Hypsipyla Shoot Borers in Meliaceae, Other Insects ACIAR Proceedings No. 97, 20–23 August 1996 Howard FW, Nakahara S, Williams DS (1995) Thys- In addition to the above insects, which are spe- anoptera as apparent pollinators of West Indies mahogany, Swietenia mahagoni (Meliaceae). Ann Sci cific to mahoganies and their close relatives, some Forest 52:283–286 insect pests of mahoganies are polyphagous spe- Howard FW, Hodges GS, Gates M (2006) First report of cies whose host ranges include mahoganies. Conchaspis cordiae (Hemiptera: Conchaspididae) in These include various species of ambrosia beetles Florida and the United States. Fla Entomol 80:102–104 Lamb FB (1966) Mahogany of tropical America. Its ecology (Coleoptera: Curculionidae: Scolytinae) that bore and management. University of Michigan Press, Ann the twigs or main stems, and species of Scara- Arbor, Michigan baeidae whose adult beetles feed on the leaves. Lugo AE, Alayaon M, Figeroa JC (2002) Big-leaf mahogany: Although mahoganies are acknowledged as genetics, ecology, and management. Springer, Berlin Heidelberg New York the most important tropical timber trees in the Mayhew JE, Newton AC (1998) The silviculture of mahogany. world and there has been much interest in their CABI Publications, Wallingford, United Kingdom 2266 M Maindroniide Wylie FR (2001) Control of Hypsipyla spp. shoot borers with maize. The major maize producers (2005 data) were chemical pesticides: a review. Pp. 109–115 In: Floyd RB, USA, China, Brazil, Mexico, Argentina, and Indone- Hauxwell C (eds), International Workshop on Hypsipyla Shoot Borers in Meliaceae, ACIAR Proceedings No. 97, sia, which accounted for 40.5, 18.9, 5.0, 3.0, 2.9, and 20–23 August 1996 2.2% of the world’s production, respectively. Thus, though some maize is grown almost everywhere, most of the production is concentrated in a few Maindroniide countries. Note that a considerable amount of maize is grown in southern Europe, but it is easy to under- A family of silverfish (order Zygentoma). estimate its significance in this region because many  Silverfish small countries are involved in its production. Maize is a productive plant, and is rich in many of the nutrients needed by humans and Maize (Corn) Pests and Their livestock. However, alone it does not provide com- Management pletely balanced nutrition. Early Americans supplemented their maize consumption with beans, John L. Capinera fish, meat, and other grains to obtain a complete University of Florida, Gainesville, FL, USA range of amino acids. They also liberated the niacin found in maize through the addition of In some English speaking countries, principally wood ash or lime. Failure to take the steps to pro- USA, Canada and Australia, maize is known as vide balanced nutrition in maize-dependent diets corn. Maize, Zea mays, is one of the world’s most results in severe nutrient deficiency. important cereal grains. More maize is produced Maize is a tall grass, and some varieties surpass than wheat or rice, though because much of the 7 m in height. Male flowers are found at the apex of maize is fed to livestock or used for industrial pur- the stem, in a structure called the “tassel.” Pollen poses, more people are directly dependent on from the tassel falls or blows to the “silk,” which are these other grains. Nevertheless, maize is a tre- elongated stigmas that protrude from the female mendously important crop, particularly in the inflorescence, or “ear.” Once on the silk, the pollen Americas, China, and parts of Africa. produce pollen tubes that grows the length of the Maize was domesticated in Mesoamerica, silk, resulting in pollination. Pollination results in probably in Mexico, sometime between 7,500 and expansion of the individual fruits or “kernels” on 12,000 years ago. Its origin is obscure, but seems to the ear. They are attached to a pithy core called a be derived from a small-seeded wild Z. mays sub- “cob,” and generally occur in rows. Ears usually con- species known as teotsinte. Small teosinte-like cobs tain 200–400 kernels. Different varieties produce have been found in caves that date back to about varying sizes and numbers of ears and kernels, and 2750 b.c., but later, beginning about 1500 b.c., this kernels with differing properties, allowing the grain grain began to be dispersed widely in the Americas. to be used for several purposes. Maize has long been It became a staple of the indigenous peoples not used to feed livestock (as grain corn which uses the only in Mesoamerica, but also in North and South kernels, or silage corn which also uses the stalk and America and the Caribbean. When Europeans foliage), as corn flour for baking, as popcorn, and as (starting with Christopher Columbus) made con- a sweet vegetable called “sweet corn.” Increasingly, tact with the Americas they quickly recognized the however, it is being used as a source of fructose for value of maize, and it became introduced to many sweetening, or fermented and distilled as ethanol areas of the world, where it is grown in all but the for production of liquor or as a gasoline additive. coldest and driest regions. In 2002, for example, Maize removes a considerable amount of over 70 countries harvested at least 100,000 ha of nutrients from the soil, and is often grown as part Maize (Corn) Pests and Their Management M 2267 of a crop rotation with a soil-replenishing legume many pests have adapted to the crop. Some of the crop such as alfalfa or soybean, and with a small most important are shown in Table 2. grain crop such as wheat or barley. Nitrogen fertil- Although there are numerous pest species, for ization is normally required. Maize is not tolerant an overview of the pests and their management, of cold weather, so in temperate areas it is planted most can be grouped together with similar species after all danger of frost is past. It is tolerant of based on their feeding behavior. The principal drought, but must have adequate moisture during groups are stem borers; rootworms; earworms; the pollination period. Sugar-rich maize varieties armyworms; cutworms; aphid, leafhopper, delpha- harvested as sweet corn are harvested soon after cid plant disease vectors; and mites. kernel formation, before starch has begun to form. For silage, the maize may be harvested any time before it dries. For grain production, the ears and Stem Borers kernels are allowed to remain on the plant until they are very dry, which is late fall or even winter. Stem borers are the most important pests of maize As one would expect of a crop grown on wherever it is grown. Most are in the order Lepi- extensive acreage and in most regions of the world, doptera, and usually in the families Noctuidae or

Maize (Corn) Pests and Their Management, Table 2 Some important arthropod pests of maize (corn) and places where they are damaging Feeding behavior Primary taxon Common name Scientific name Location Foliage (leaf), Lepidoptera Fall armyworm Spodoptera Americas chewing frugiperda African armyworm Spodoptera exempta Asia, Africa Common armyworm Pseudaletia Asia, Europe, Africa, unipuncta America Maize webworm Marasamia Africa trapezalis Coleoptera Grey weevils Tanymecus spp. Asia, Europe Foliage, Hemiptera Corn leaf aphid Rhopalosiphum Asia, Europe, Africa, piercing-sucking maidis America Corn delphacid Peregrinus maidis Americas Corn leafhopper Dalbulus maidis Americas African leafhopper Cicadulina spp. Africa Chinch bug Blissus leucopterus N. America Acarina Twospotted Tetranychus urticae Asia, Europe, Africa, spider mite America Banks grass mite Oligonychus C., N. America pratensis Stalk, chewing Lepidoptera European corn borer Ostrinia nubilalis Asia, Europe, Africa, N. America Asian corn borer Ostrinia furnacalis Asia Lesser cornstalk Elasmopalpus Americas borer lignosellus 2268 M Maize (Corn) Pests and Their Management Maize (Corn) Pests and Their Management, Table 2 Some important arthropod pests of maize (corn) and places where they are damaging (Continued) Feeding behavior Primary taxon Common name Scientific name Location Southwestern corn Diatrea N., C. America borer grandsiosella Neotropical corn Diatrea lineolata C., S. America borer Sugarcane borer Diatrea saccharalis Americas Asiatic rice borer Chilo suppresalis Asia Spotted stem borer Chilo partellus Asia, Africa Pink stem borer Sesamia cretica Africa African pink stem Sesamia calamistis Africa borer Mediterranean corn Sesamia Europe borer nonagroides Asiatic pink stem Sesamia inferens Asia borer African maize stalk Busseola fusca Africa borer African sugarcane Eldana saccharina Africa borer Potato stem borer Hydraecia micacea Asia, Europe, N. America Cutworms Various Asia, Europe, Africa, Americas Termites Microtermes spp. Africa, Asia Diptera Frit fly Oscinella frit Europe Shoot flies Atherigona spp. Asia, Africa Coleoptera Epilachna beetle Epilachna similis Africa Ear, chewing Lepidoptera Corn earworm Helicoverpa zea Americas Corn earworm Helicoverpa Asia, Africa armigera Western bean Loxagrotis albicosta N. America cutworm Diptera Cornsilk fly Euxesta spp. Americas Coleoptera Dusky sap beetle Carpophilus lugubris Americas Roots, chewing Coleoptera Western corn Diabrotica virgifera Americas, Europe rootworm Northern corn Diabrotica barberi N. America rootworm Wireworms Various Asia, Africa, Europe, Americas White grubs, chafers Phyllophaga, Cyclo- Asia, Europe, Americas cephala, Melolontha spp. Maize (Corn) Pests and Their Management M 2269 Maize (Corn) Pests and Their Management, Table 2 Some important arthropod pests of maize (corn) and places where they are damaging (Continued) Feeding behavior Primary taxon Common name Scientific name Location Seedcorn beetle Stenolophus spp. N. America Flea beetles Chaetocnema spp. N. America Diptera Seed fly Delia platura N. America. Europe, Asia

Pyralidae. Initially they feed on the foliage, but through several countries in Europe. More insec- then move into the stems and affect movement of ticide is used in North America for suppression of water and nutrients. Fungi, particularly Fusarium corn rootworms than is used for control of any spp., gain access to the plants through the open- other insect pest on any crop, and 80% of the ings created by borers, leading to various rots and insecticides used in North America on corn is the occurrence of mycotoxins. When they bore directed to corn rootworms, so the effect on into the base of the ear they can cause ear drop. In Europe of the establishment of western corn root- North America and Europe, the most important worm is potentially great. In the USA, other corn stalk borer is European corn borer, though some rootworm species can inflict damage, but none European countries also suffer from Mediterra- are as important as western corn rootworm. nean corn borer. Similarly, portions of North and Central America are affected by southwestern corn borer. In South America, the sugarcane borer and Corn Earworms the lesser cornstalk borer predominate. In Africa, the African stalk borer and spotted stem borer are The corn earworm found in the Americas, Heli- most important, but pink stem borer and sugar- coverpa zea, can be a extremely damaging insect cane borer also can be important. In Asia, the most on sweet corn, though it is of lesser significance on important species are Asian corn borer, Asiatic field corn. In the old world, Helicoverpa armigera rice borer, Asiatic pink stem borer, and spotted is the corn earworm of importance. These insects stem borer. feed on both silk and within the ears, with the latter being of importance. Due to their feeding habits, sweet corn has a low tolerance threshold, so a Rootworms great deal of insecticide is used against these insects during sweet corn production. Damage by Corn rootworm larvae feed on the roots and base these insects also facilitates entry of plant patho- of the stem. They disrupt water and nutrient gens. These are not the only earworms, of course, uptake, and cause plants to lodge (fall over), mak- but other ear feeders such as western bean cut- ing harvest difficult. Adults also feed on foliage worm are not nearly as important. and silks, sometimes interfering with pollination, but this generally is not very important. Histori- cally, the Diabrotica rootworm problem was Armyworms mostly a North American issue, though causing some damage in Central and South America. Most armyworms, Spodoptera and Pseudaletia However, western corn rootworm was discovered spp., attack maize at intermediate stages in the in Yugoslavia in 1992, and has since spread growth of the plant, during the whorl stage. They 2270 M Maize (Corn) Pests and Their Management can cause extensive defoliation and occasionally under irrigated conditions in dry environments, affect the ear. In tropical and subtropical areas of mite problems develop when the weather is unusu- the Americas they can be the most severe problem, ally dry or dust is abundant. Along unpaved road- and often cause injury annually. ways, for example, the large amounts of dust produced by vehicles can be lethal to predatory insects while mites harbored beneath a layer of Cutworms silk on the foliage are protected from the desiccat- ing effects of dust. Mites are often resistant to These insects affect mostly the seedling stage, sev- chemical insecticides, and there is risk of their ering the shoot at the soil surface, and often killing populations flaring up when insecticides are the young plant. A large number of noctuids pos- applied against caterpillars or other pests, result- sess this feeding habit, but the most important is ing in the inadvertent destruction of the mite’s black cutworm, Agrotis ipsilon. This species over- natural enemies. winters in subtropical areas throughout the world, but disperses to more temperate areas early each spring, causing considerable damage to young Other Pests corn plantings. Locally, other pests can be quite important due to ecological situations favoring their abundance, or Aphids, Leafhoppers and because the crop is especially susceptible. For Delphacids example, wireworms tend to be more troublesome following rotations of other grasses or when grass Alone, aphids (Hemiptera: Aphididae), leafhop- weeds are abundant in the previous crops. Mois- pers (Hemiptera: Cicadellidae), and delphacids ture conditions can also favor the occurrence of (Hemiptera: Delphacidae) are not usually very wireworms in low-lying areas of fields; corn wire- damaging to maize. However, because they can worm, Melanotus communis (Coleoptera: Elateri- vector plant viruses, they can become quite dae), is commonly associated with more moist areas important. For example, although corn leafhop- of fields. Grasshopper and locust (Orthoptera: per, Dalbulus maidis, can cause plant wilting due Acrididae) outbreaks can occur intermittently, or to direct feeding injury, its principal effect is to occur where weeds or weedy crops are not man- vector disease such as maize rayado fino virus, aged properly, resulting in dispersal of these insects maize bushy plant mycoplasma, and corn stunt into maize fields and causing extensive damage, spiroplasma. Likewise, an African species of Del- especially along the margins of the field. phacidae, Peregrinus maidis, that has become The high value and low threshold for damage redistributed around the world in tropical and associated with sweet corn can create special con- subtropical areas transmits maize mosaic virus ditions favoring the occurrence of pests. Sap beetles and maize stripe virus. such as Carpophilus lugubris (Coleoptera: Nitidu- lidae), and cornsilk fly, Euxesta spp. (Diptera: Otididae), are very damaging to sweet corn in Mites some areas, but they are not considered to be pests of grain corn. Even the earworms, which are dev- Mites are severe pests of maize mostly in arid areas astating pests of sweet corn, because consumers or under dry conditions. However, dry land pro- are repulsed by the presence of insects or insect duction is common with maize, and mites can parts in their food, have little impact on grain corn become the dominant pest in such situations. Also, production. Maize (Corn) Pests and Their Management M 2271 Pest Management in Maize high levels of pest pressure (infestation) on maize, whereas most of the rest of the world has moder- The effect of arthropod pests on corn production ate levels of infestation. is considerable, though quite variable from loca- Cultural or environmental management. A tion to location. Data in Table 3 suggests that the number of approaches are used to manage maize potential level of damage in maize is about 14–17% pests. Cultural practices such as early planting or worldwide. In contrast, the actual level of arthro- harvest, crop rotation, and effective weed suppres- pod-caused losses is about 10–12%. The approxi- sion can be used to advantage in many cases. For mately 5% difference is due to the plant protection example, rotation of maize with a non-grass crop efforts of producers. The different areas of the can usually be used effectively in North America to world vary considerably in the effectiveness at manage corn rootworm because they overwinter protecting maize from damage. Most effective, it as eggs. Upon hatching in the spring, young corn seems, are producers in North America and the rootworm larvae will perish if they cannot reach Near East, which incur only about 6 and 9% loss, the roots of suitable grass crops such as corn. So respectively. In contrast, areas of Africa and Asia simply rotating corn with soybeans was a success- derive little benefit from protection efforts, or ful technique for many years, though in recent make little effort to reduce losses. Virtually all the years a strain of rootworm has begun to evolve African countries (also Mexico and Brazil) have that diapauses for two seasons, necessitating a longer crop rotation period or other management Maize (Corn) Pests and Their Management, Table 3 approaches. Sometimes growers prefer not to rotate Estimated actual and potential losses due to crops, instead growing maize continuously. Under maize pests in the major maize-producing regions these conditions, some benefit can be acquired by of the world (adapted from CABI Crop Protection planting the new crop between the rows of the pre- Compendium, 2002) vious crop, rather than in the same location as the Actual % Potential % previous crop. Moving the crop planting even a few loss with loss without centimeters requires that the rootworm larvae controls controls must disperse to find the roots of the young plants, Africa 14 17 and many die while searching for food. Eastern 17 18 Insecticides. Insecticides (including bioinsec- Western 17 17 ticides such as Bacillus thuringinsis) are a principal Southern 13 16 approach to avoid loss in maize. In the Americas, where rootworms are a problem, most of the insec- Northern 9 17 ticide is applied to the soil to protect roots. The Asia 12 16 rootworms hatch several weeks after the maize is Southeast 15 18 planted, and if the insecticide is to be applied at South 15 16 planting, this requires the use of a persistent insec- East 9 16 ticide. Post planting applications are possible, but Near East 10 14 it is difficult to attain good root protection with Americas 11 15 post-plant applications, and it is more costly. Lesser Southern S. America 13 14 amounts of insecticide are sprayed onto foliage to Andean 10 14 protect against defoliation and ear damage, and North America 6 15 only a small amount is expended via seed treatment to protect the seed and young seedling from Central America 13 14 injury by seed-feeding insects. The insecticide Europe 9 14 used on maize in North America is estimated at 2272 M Maize (Corn) Pests and Their Management over 50% for rootworm suppression, 11% for the confers higher yield gains, often 10% or more. The stalk borers (European corn borer and southwest- detrimental effects of Bt corn are somewhat obvi- ern corn borer), and 12% for corn earworm. In ous, principally higher cost of seed and the risk of other areas of the world, however, proportionally widespread resistance to Bt. On the other hand, more insecticide is used as a foliar protectant and there are certainly economic, health, and environ- seed treatment because soil pests are not as impor- mental benefits associated with decreased use of tant. About 70% of the insecticide used on maize is insecticides in Bt corn. Overall, the benefits of used in the Americas, and of the insecticide used genetically engineered maize will only be known in the Americas, about 2/3 is used in North Amer- with additional time. ica. This pattern is not surprising considering the  African Armyworm preponderance of maize production in North  Armyworm America, and the propensity to maximize yield in  Black Cutworm corporate-type farming operations. In less well  Corn Delphacid financed or subsistence agriculture, insecticide  Corn Earworm purchase is a much more difficult option.  Corn Leafhopper Genetically engineered germplasm. The soil  European Corn Borer bacterium Bacillus thuringiensis has long been  Gramineous Lepidopteran Stem Borers in Africa recognized for its ability to control caterpillars,  Northern Corn Rootworm and in more recent times strains have been identi-  Seedcorn Maggot fied that affect lower flies (e.g., mosquitoes, black-  Spotted Cucumber Beetle flies) and beetles. With the advances in genetic  Western Corn Rootworm engineering, it has proved possible to incorporate components of the B. thuringiensis bacterium into plants (usually called transgenic plants), thereby References conferring a degree of resistance against lepidopterous insects. In maize, the caterpillar-specific James C (2003) Global review of commercialized transgenic elements of B. thuringiensis (cry1Ab gene), which crops: 2002. Feature Bt maize. International service for affect stalk borers, have been rather widely the acquisition of agri-biotech applications, 182 pp Steffey K, Rice M, All J, Andow D, Gray M, Van Duyn J (eds) deployed via genetically modified maize germ- (1999) Handbook of corn insects. Entomological Soci- plasm. The beetle-specific elements (cry3B1), ety of America. Lanham, MA, 174 pp which are active against rootworms, are less well known but are beginning to gain acceptance, at least in the Americas. When farmers plant maize Major Worker that is engineered to resist herbivory by Lepi- doptera and Coleoptera, they effectively eliminate A subcaste of social insects consisting of especially much of the potential damage that they might large workers. In ants, this subcaste is often spe- incur. Such practices do not eliminate all prob- cialized for defense, and called soldiers. (contrast lems, of course, as there are other taxa that can be with media and minor workers) damaging. Also, expression of the Bacillus thur-  Ants ingiensis toxin is not uniform throughout the plant, and not all pests are affected. Nevertheless, yield gains in the USA are attributable to maize Malacopsyllidea containing Bacillus thuringiensis genetic elements (Bt corn) is estimated at 5%. In areas of the world A family of fleas (order Siphonaptera). where insecticide use is less prevalent, Bt corn  Fleas Malaria M 2273 Malaise Trap in the vertebrate host, and an exogenous sexual multiplication (sporogony) in the mosquito host. An interception trap that captures flying insects, The life cycle may start with the ingestion of the Malaise trap is tent-like with vertical nets serv- blood by a female Anopheles mosquito from a ing as baffles and a sloping canopy that funnels malarious person (Fig. 3). The female mosquito insects upward to a jar or other apparatus for cap- requires a blood meal for subsistence and for ture. They may be constructed as unidirectional, egg production. The ingested blood may contain bidirectional or nondirectional traps. sexual cells (gametocytes). In the stomach of the  Traps for Capturing Insects mosquito, the male gamete (microgametocyte) exflagellates, producing microgametes which seek out and fertilize the female gamete (macrogamete) Malaria to form a globular zygote. Within 18–24 h it becomes elongate and motile, and is known as an Eugene J. Gerberg oökinete. The oökinete forces its way into the epi- University of Florida, Gainesville, FL, USA thelial lining of the stomach wall of the mosquito, and is now called an oöcyst. The mosquito stom- Malaria is a debilitating disease caused by an infec- ach may contain several hundred globular oöcysts. tion of one or more protozoan parasites belonging The oöcyst increases in size, and the nuclei divide to the subphylum Sporozoa, family Plasmodiidae, to form many spindle-shaped motile sporozoites. genus Plasmodium. These parasites are found in The oöcyst reaches maturity in 4–15 days, bursts, the blood of mammals, birds and reptiles. Human and liberates thousands of the sporozoites into the malaria is transmitted by the bite of female anoph- body cavity (hemocoel) of the mosquito. Many eline mosquitoes of the genus Anopheles (Diptera: then migrate to the salivary glands. The mosquito Culicidae). is now infective. Malaria infection is initiated Malaria is a major endemic tropical disease when sporozoites are introduced into the new host characterized by severe chills and fever, anemia, following the bite of the infective mosquito. and splenic enlargement. The disease has a wide The sporozoites now enter the parenchymal geographical range, occurring from the temperate cells of the liver where they develop and multiply zones to the sub-tropics and tropics. It has been in what is known as pre-erythrocytic schizogony. estimated that there are 150–400 million malaria As the parasite (schizont) divides, it forms many cases a year, with five million deaths. thousands of merozoites. After about 6–16 days, Malaria once was thought to be caused by the schizont bursts and releases the merozoites vapors arising from swampy areas, and thus in into the tissue and into the blood circulation. The the eighteenth century the Italians called it time between the date of infection and the appear- malaria, or bad air. It wasn’t until 1880 that ance of the parasites in the peripheral blood is Charles Laveran, a French army surgeon, des- known as the pre-patent period. cribed malaria parasites in the red blood cells of After a period of growth, the parasite multi- humans. In 1897, Ronald Ross found a form of a plies in the red blood cell by asexual division, malaria parasite in a mosquito. In 1898, Battista called schizogony, in which a mature schizont Grassi, Amico Bignami and Giuseppe Bastianelli, divides into a number of small merozoites. When in Italy, described the malaria cycle in humans the red blood cell bursts, the merozoites are and mosquitoes. released into the bloodstream. This is the stage Plasmodium undergo two types of multiplica- that is responsible for the morbidity and mortality tion by an endogenous asexual division (erythro- associated with malaria. The merozoites then cytic schizogony, and exo-erythrocytic schizogony) invade fresh red blood cells (erythrocytes) and 2274 M Malaria Endogenous asexual cycle in humans

Multiple merozoites Segmenters

Merozoites invade erythrocytes Presegmenters Merozoites Erythrocytic break out schizogony Exoerythrocytic and invade schizogony erythrocytes Amoeboid trophozoites Ring form Sporozoites inside liver trophozoites reticulo - endothelium

Gametocytes (immature) Sporozoiotes in bloodstream Male Female

Gametocytes Mosquito bite Sporozoites in salivary gland Gametes Rupture of oocyst Sporozoites in oocyst

Sporoblasts in oocyst Zygote

Oocyst Ookinete

Cyst in gut

Exogenous sexual cycle in mosquitoes Malaria, Figure 3 Life cycle of the malaria parasite, Plasmodium falciparum (adapted from Scott and Rice 1966).

grow at the expense of the host cell. A vacuole is are taken up when the mosquito bites, and thus formed, surrounded by a thin ring of cytoplasm. A the circle is completed. small round or oval nucleus lies within the ring. There are four types of human malaria, This stage of the parasite is called the ring form. Plasmodium vivax, P. falciparum, P. malariae and Within a few hours, the cytoplasm becomes some- P. ovale . Based on the length of time of the erythro- what ameboid and is in the trophozoite stage. After cytic cycle of schizogony or schizogonic periodic- a number of nuclear divisions, the mature schizont ity, the species may differ. Thus P. malariae is 72 h may contain 16 merozoites. The blood cell rup- and is known as quartan malaria. The other species tures and the merozoites enter the bloodstream of Plasmodium last 48 h, and are called tertian where they may invade new blood corpuscles. This malaria. P. falciparum is the most dangerous type process of erythrocytic schizogony is repeated of malaria, and is called malignant tertian malaria, over and over again. After several generations of and is also the cause of a condition known as black- merozoites having been produced, sexually differ- water fever. P. v iv a x is known as benign tertian entiated forms or gametocytes are produced. These malaria. These names have become obsolete, and Malcidae M 2275 the various forms of malaria are now known by difficult, and in some countries malaria incidence their specific name, unitalicized, i.e., vivax malaria. has increased. In many areas, indoor spraying of There are approximately 400 species ofAnoph - residual insecticides is still the main control mea- eles mosquitoes throughout the world. Of these, sure. Malaria vaccine research has been extensive, approximately 75 are considered to be important but to date a truly effective vaccine has yet to be vectors of malaria. Resting or feeding adult Anoph- developed. One of the goals of the World Health eles usually have their abdomen at an oblique Organization is to use primary health care as a angle, compared to other genera of mosquitoes means to deliver malaria control services, whether whose abdomen is usually parallel to the resting it be the use of insecticide treated bed nets, distri- surface. The palpi of both sexes ofAnopheles are as bution of drugs, or limited vector control. long as the proboscis. The eggs are boat-shaped with floats. They are laid on the surface of the References water. The larvae that hatch from the eggs do not have a prominent air tube, and have float or pal- Bruce-Chwatt LJ (1980) Essential malariology. William mate hairs on the abdominal segments. The Heinemann Medical Books Ltd., London, United Anopheline larvae lie parallel to the surface of the Kingdom, 354 pp water, in contrast to Culicine larvae which hang Garnham PCC (1966) Malaria parasites and other haemospo- ridia. Blackwell Scientific Publishers, Oxford, United head down from the surface of the water. The Kingdom, 1114 pp aquatic habitats of the larvae may be temporary or Harrison G (1978) Mosquitoes, malaria and man. EP Dutton, permanent, natural or made by humans. Anoph- New York, 314 pp Kreier JP (ed) (1980) Malaria. Vol. 1: Epidemiology, chemo- eline species vary in their oviposition require- therapy, morphology, and metabolism. 416 pp. Vol. 2: ments. Some species may prefer sunlit pools, while Pathology, vector studies and culture. 328 pp. Vol. 3: others may prefer a shady slow-moving stream. Immunology and immunization. Academic, New York Some species prefer brackish water while others 346 pp Russell PF, West LS, Manwell RD, MacDonald G (1963) Prac- may prefer fresh water along the grassy margins of tical malariology. Oxford University Press, London, lakes. Breeding sites inadvertently created by United Kingdom, 750 pp human activity are often troublesome. Roadside Sachs JD (2002) A new global challenge to control malaria. ditches, badly maintained irrigation ditches, gem Science 298:122–123 Shuler AV (1985) Malaria: meeting the global challenge. mining pits and other water collecting structures U.S. Agency for International Development, Washington, can be the source of large numbers of anophelines. 110 pp The flight range of adult anopheline mosquitoes is usually about 2 km, though they have been known to be carried by wind for much greater distances. Malaya Disease Over the past half century, vector control and chemotherapy have reduced, and in some cases A lethal disease of larvae of the Indian rhinoceros eradicated, malaria in many countries. Malaria beetle, Oryctes rhioceros (Linnaeus), caused by the control has been based on a number of measures Orcytes virus.  Orcytes Virus to prevent mosquitoes from feeding on humans:  Other Nudivuruses by environmental control modifications, by residual spraying of habitations to destroy the adult mosquitoes, or larvaciding to destroy the larvae. Malcidae Chemotherapy has been used to eliminate or control the parasite in humans. Insecticide resistance A family of bugs (order Hemiptera, suborder by the vector mosquito and drug resistance by Pentamorpha). the parasite has now made malaria control more  Bugs 2276 M Malignant Jaundice Malignant Jaundice for authoring this tome, which treats most of the pests associated with buildings and the immediate This is a tick-transmitted protozoan disease also environs. It is a remarkably complete and interest- known as canine babesiosis. ingly written treatment of pest control, and any-  Piroplasmosis one who examines it critically is not surprised that it has persisted as the favorite reference manual for the pest control industry for over 50 years. Mallis, Arnold Mallis died on January 16, 1984.

Arnold Mallis was born at New York, New York, USA, on October 15, 1910. He and his family relo- Reference cated to California in 1927 and he entered the University of Southern California with the intent Snetsinger R (1984) Arnold Mallis 1910–1984. Am Entomol of becoming a dentist. The Great Depression inter- 30:90 vened and Mallis had to leave college to work. He then became interested in natural history and enrolled at Pasadena Junior College and the Uni- Mallophaga versity of California, Berkeley. He was awarded a B.S. degree in 1934 and an M.S. degree in 1939, A suborder of wingless ectoparasitic insects com- both in entomology. Mallis worked for several monly called lice, Phthiraptera. It is sometimes years as an entomologist with the building and treated as an order. grounds department of the University of California,  Chewing and Sucking Lice Los Angeles. During World War II, he worked on malaria control, and from 1945 to 1968 he was employed by Gulf Oil Company, where he worked on screening and formulating insecticides. In 1968 Malpighian Tubules he joined Pennsylvania State University as an extension entomologist, where he worked until he Long slender ducts found in the hemocoel that retired in 1975. Mallis is best remembered as the collect nitrogenous wastes, solutes and water, and author of “the bible of the structural pest control terminate at the juncture of the midgut and the industry,” also known as the “Handbook of pest hindgut. A key component of the excretory system control” (1945 and subsequent editions). In retro- (Fig. 4). spect, Mallis’ varied positions prepared him well  Alimentary and Sucking System

Foregut Midgut Hindgut Gastric Esophagus Crop Ventriculus Pylorus Ileum Rectum Caecum Pharynx

Buccal Anus cavity Proventriculus Mouth Malpighian tubule Malpighian Tubules, Figure 4 Generalized insect alimentary system (adapted from Chapman, The insects: structure and function). Management of Insect-Vectored Pathogens of Plants M 2277 Mammal Chewing Lice Chemical Control

Members of the family Trichodectidae (order Chemical control of vectors will limit spread of vec- Phthiraptera). tored plant pathogens if two conditions are met.  Chewing and Sucking Lice First, the vector being controlled must be a colo- nizer of the crop being treated. Some plant viruses are transmitted by transient flying insects. In these cases, chemical control has a poor record. Second, Mammilla (pl., mammillae) most of the spread must come from within the treated area (secondary spread). For the most part, Elevations found on the integument of Orni- insecticides simply prevent the buildup of popula- thodoros ticks. tions of insects within a treated area. Most pesticides will not kill an immigrant insect before it has a chance to transmit a pathogen. Thus, if there is an infected field nearby with a high population of vec- Management of Insect-Vectored tors, pesticide treatment may not be very effective Pathogens of Plants in preventing infection from primary spread. Pesti- cide treatment has a good track record for control Susan E. Halbert of certain luteovirus diseases such as potato leafroll Florida Department of Agriculture and Consumer and barley yellow dwarf, spread by colonizing Services, Division of Plant Industry, Gainesville, aphids. Even if the above conditions are met, depen- FL, USA dence on chemical control of vectored pathogens in perennial crops may be risky, because a single Epidemiology of vectored plant pathogens missed spray application or insecticide failure could involves the plant, the pathogens, the vectors, and result in infection and demise of the crop. the environment, all interacting in various ways. Another variation on chemical control is the Often, an understanding is needed of seasonal use of stylet oil. Certain horticultural oils can reduce cycles of host plants, pathogens, and vectors. transmission of viruses by aphids. This methodol- For example, pathogens and vectors important ogy can reduce transmission of pathogens carried to an annual crop may have non-crop reservoirs by transient insects, something that is not usually between harvest and re-planting. Vectors may possible with standard insecticides. There is also overwinter in the crop, or on alternate host plants. potential for use of insect repellents for vector man- The host range of the pathogen may determine agement. Some work has been done with visual whether inoculum control is feasible or not. Some repellents (mulches, paints, colored netting), but pathogens are transmitted via plant propagation, little has been done with chemical repellents. and others are not. The epidemiology of vectored There is no known chemical control of plant plant pathogens often is complex, and an inte- viruses, but some fastidious bacteria in perennial grated approach to management is needed. Often, tree crops can be controlled with injected antibiot- no single approach will achieve adequate control. ics. Remission of symptoms usually is temporary. This section is organized according to the concept of integrated pest management, including chemical control, biological control, host plant resis- Biological Control tance, cultural control, and regulatory measures. Each of these categories will be considered in The use of biological control for management of terms of the vectors and the pathogens. vectored pathogens has a mixed review. Obviously, 2278 M Management of Insect-Vectored Pathogens of Plants fewer vectors is better; however, sometimes the well for control of citrus tristeza virus, an aphid economic threshold for vectors is so low that it is transmitted closterovirus, in several parts of the not achievable through biological control. Some- world. times, the presence of natural enemies evokes scat- ter responses in vector prey. This can actually cause an increase in pathogen transmission. Host Plant Resistance Total dependence on biological control for a vectored pathogen in a perennial crop is risky. The efficacy of plant resistance to vectors depends Biological control inherently fluctuates between on the means of resistance and the mode of trans- high populations of pests and high populations of mission. Resistance that prevents feeding or repels natural enemies. If pests are not vectors, the crop the insects can prevent transmission of pathogens often can stand temporary high pest populations, spread by feeding. If the resistance merely prevents but if the main concern is pathogen transmission, or slows population growth, it cannot prevent pri- the entire crop can be lost if populations fluctuate mary spread. It can, however, have some effect on in favor of the pest. Similarly, often a grower will secondary spread. have to spray for another pest. The pesticide may Resistance to the pathogen probably is the kill the natural enemies of the vector, resulting in most effective means of controlling vectored plant an increase in transmission of the pathogen and pathogens. If plant resistance to the pathogen is destruction of the crop. available, it should be the first line of defense. Biological control in simpler island ecosys- Complications with host plant resistance can tems may have a better chance to work than in occur if the pathogen evolves strains that can more complex settings. For example, the introduc- break down the resistance. Also, some crops are tion of psyllid parasitoids into RÉunion Island notoriously difficult to breed due to difficult genet- dramatically reduced the transmission of the bac- ics or longevity. teria that cause citrus greening disease. However, Resistance to the pathogen may be the only the same parasitoids are present in Viet Nam, and means of management in some cases. An example citrus greening disease is a major limiting factor in is sugarcane mosaic virus. Sugar cane is propagated citrus production there. vegetatively, so the virus is propagated with the Sometimes disruption of existing biological crop. Once planted, a crop remains in the same control can result in an increase in transmission field for several years of production, and planting is of a plant pathogen. Increased spraying for late staggered throughout the production area. Thus, blight (caused by a fungus) in potatoes was even if clean planting stock could be found, there is linked to a major increase in numbers of green no possibility for an area-wide crop-free (and peach aphids. Evidently, populations had been virus-free) period. The virus is transmitted by tran- controlled by an aphid pathogenic fungus that sient winged aphids, including species that do not was killed by the fungicide applications for late necessarily colonize the sugar cane crop, so pesti- blight. The result was a big increase in incidence cide application is not effective. Fortunately, there of potato leafroll virus (PLRV), transmitted by has been success with mosaic resistant cultivars. the aphids. Biological control of the pathogen is another option. Usually this is done by means of cross pro- Cultural Control tection - infecting a crop with a mild strain of a pathogen that prevents symptom expression of a Many of the effective management practices for more severe strain that may be transmitted by an diseases caused by vectored plant pathogens insect later on. Cross protection has worked very involve some sort of cultural control such as Management of Insect-Vectored Pathogens of Plants M 2279 adjusted planting date, pruning, roguing, and a xylem limited bacteria called Xylella fastidiosa. It removal of volunteer crop plants and other non- moves slowly in the plants. If Pierce’s disease is crop reservoir hosts of vectors or pathogens. transmitted by small leafhoppers that feed on twigs, Adjusting planting dates can minimize crop winter pruning can eliminate most of the infection. exposure to vectored pathogens. In the Pacific However, if the disease is transmitted by the much Northwest, several vectored pathogens, transmitted larger glassy-winged sharpshooter (Homalodisca by eriophyid mites and aphids, can damage early- coagulata), which feeds on larger branches and planted fall cereals. The mite transmitted viruses are trunks, pruning is much less effective. particularly serious because they cause severe yield Control of volunteer crop plants may limit or loss, resulting in total crop failure in some cases. eliminate primary inoculum for newly planted These viruses infect newly seeded winter wheat that crops. Volunteer potatoes are important sources of is planted near a maturing crop from the previous virus inoculum in Idaho potato seed production season, or near infected volunteer grain. These areas. Similarly, volunteer grain can be an impor- viruses are most troublesome in years when the old tant reservoir for aphids and barley yellow dwarf crop is slow to mature, and there is overlap between at planting time for winter wheat. The volunteer late-maturing cereal crops from the previous season wheat provides a “green bridge” for the viruses and and emergence of newly sown winter wheat. The their vectors between harvest of one crop and infective mites are blown from the old crop to the new emergence of the next one. one. After landing on the new crop, they apparently Other cultural control measures include elim- stay put, because there is little secondary spread in ination of weed hosts of vectors or pathogens, use the fall. The mites cannot survive very long off a host of reflective mulches and paints to repel vectors, plant, so any break in the “green bridge” between and various protective row covers. Quite a bit of old and new crops will prevent infection. As little as work also has been done on the use of windbreaks 10 days delay in planting can make the difference and barrier crops to protect susceptible plantings. between crop failure and negligible incidence. Simi- larly, the aphid-transmitted barley yellow dwarf virus complex largely can be prevented by delay in Regulatory Measures planting. Other viruses are managed on an area- wide basis by maintaining a crop-free period at some Regulatory measures for control of vectored plant time during the year. For such a policy to work, all pathogens are a very important aspect of manage- growers in the area must cooperate in field clean-up ment, especially for those pathogens that are and coordination of planting dates. transmitted through propagation. Strict sanitation Pruning and roguing often are used as a means measures for propagative material are common. of management of vectored plant pathogens, espe- Other kinds of regulatory measures include crop- cially in perennial crops. The efficacy depends on free periods, quarantines, and required virus testing. whether latent infections remain, and if so, whether One of the best ways to prevent vector-borne plants with latent infections are suitable source disease in plants is to keep the disease and the vec- plants for vectors. In the early stages of an epidemic, tor out. Many plant diseases and vectors that occur there usually will be more plants with latent infec- elsewhere in the world do not occur in the United tions than with visible symptoms. If plants with States. Some of these are listed as quarantine or latent infections can serve as source plants for vec- actionable pests/diseases. If they are found at U.S. tors to acquire the pathogens, and vectors are pres- ports of entry, the shipment is rejected. If a pest or ent, pruning and roguing will not be very effective. disease has a limited distribution in the U.S., there In some cases, pruning actually can eliminate may be a state quarantine for certain items. For disease. Pierce’s disease of grape vines is caused by example, if a pest is found in Florida but not in 2280 M Management of Insect-Vectored Pathogens of Plants California, California may reject shipments from unacceptably high levels of PLRV. Regulations were Florida that contain the pest. made to prevent sale of infested bedding plants. Production of healthy propagation materials Additionally, the local growers provided home gar- involves regulatory agreements. Potato tubers deners with clean potato seed tubers. Incidence of grown for seed are subject to winter testing for a PLRV in seed potatoes decreased dramatically in variety of vector-borne viruses. Standards are the region after the regulations were implemented. much stricter for early generation seed. Citrus trees are propagated vegetatively by grafting, in order to ensure varietal uniformity. Citrus trees Integrated Management used for budwood in Florida are required to be tested for citrus tristeza virus every year. Those Most often control of vectored pathogens of plants found to contain severe strains are no longer will involve an integrated approach. A good exam- allowed to be used for propagation purposes. Let- ple is potato production. Some popular varieties tuce mosaic virus and bean common mosaic virus of potatoes develop internal discoloration as a are transmitted by seed as well as by aphid vectors. result of infection with PLRV that results in rejec- Some states have regulations in place requiring tion by potato processors. In order to prevent that seed used commercially in the state be tested PLRV infection there are regulatory measures to and meet standards for virus incidence. ensure clean propagation material. Additionally, In warm climates where crops are grown year commercial ware potato growers employ scouts to around, control of diseases caused by vectored survey for green peach aphids. If numbers reach pathogens can be particularly challenging. Some- an economic threshold the crop is treated with times an agreement is made to adhere to a crop-free insecticide to prevent secondary spread of PLRV. period to break the disease cycle. State regulatory Cultural controls include removal of volunteer agencies may be involved to ensure that there are potatoes, and in some cases, removal of peach and consequences for any growers that do not comply. apricot trees that are overwintering sites for vec- Other regulations are tailor-made for a given tors. Department of Agriculture inspectors make situation. Green peach aphids (Myzus persicae the rounds of retail vendors of bedding plants, (Sulzer)) transmit potato leafroll virus (PLRV), preventing sale of infested ones. Finally, there is which causes an important disease in potatoes. The work at the federal and state levels to breed potato aphids overwinter in peach and apricot trees. In the varieties that are more tolerant to PLRV infection, spring, they leave the trees and infest potatoes and but that also retain the taste, baking and process- other plants. In parts of Idaho where seed potatoes ing qualities of the popular susceptible cultivars. are grown, it is illegal to grow peach and apricot Epidemiology of vectored pathogens affect- trees. If the trees are found, the state can require ing crops is a complex and very interesting field of their removal. Guy Bishop, University of Idaho, dis- study. Many more puzzles remain to be solved that covered that another source of green peach aphids will make even more effective management a was greenhouse grown bedding plants. These possibility. infested seedlings were purchased by home garden- ers, who often also grew potatoes. Frequently, the home grown potatoes either were grown from seed References saved from previous years, or from unregistered seed. Thus, the PLRV infection rate in home gar- Hadidi A, Khetarpal RK, Koganezawa H (eds) (1998) Plant dens was high. Bishop found that the closer a seed virus disease control. APS, St. Paul, Minnesota, 684 pp Harris KF, Maramorosa K (eds) (1982) Pathogens, vectors, potato field was to a town with home gardens, and plant diseases: approaches to control. Academic, the more likely it was that the seed farmer had New York, 310 pp Mango Mealybug, Rastrococcus invadens Williams (Hemiptera: Pseudococcidae) M 2281 Mandible have some iridescent scales on the forewings. Larvae are small, slug-like in shape, feeding mostly on One of the pair of jaws in insects, attached to the mosses, liverworts, or detritus, as far as is known. head. The mandibles of insects with biting and chewing mouthparts usually are stout and tooth- like in appearance. Mouthparts of Hexapods. References

Davis DR (1987) Micropterigidae. In: Stehr FW (ed) Imma- Mandibular Glands ture insects 1: 341–343, Kendall/Hunt, Dubuque Issiki ST (1931) On the morphology and systematics of micropterygidae (Lepidoptera Homoneura) of Japan Paired glands that open near the base of the man- and Formosa, with some considerations on the dible, these glands have evolved varied functions. Australian, European, and North American forms. They may produce saliva, pheromones, defensive Proceedings of the zoological society of London 1931:999–1039 secretions, and have antimicrobial activity. Kristensen NP, Nielsen ES (1979) A new subfamily of micropterigid moths from South America. A contribution to the morphology and phylogeny of the Microp- Mandibulate terigidae, with a generic catalogue of the family 1931: Zeugloptera. Steenstrupia 5:69–147 Lorenz RE (1961) Biologie und morphologie von Micropterix Insects that have the mandibles adapted for biting calthella (L). (Lep. Micropterygidae). Deutsche Ento- and chewing. mologische Zeitschrift (n.s.) 8:1–23 Tuskes PM, Smith NJ (1984) The life history and behavior of Epimartyria pardella (Micropterigidae). J Lepidopterists’ Soc 38:40–46 Mandibulate Archaic Moths (Lepidoptera: Micropterigidae) Mange John B. Heppner Florida State Collection of Arthropods, Mange or scabies is an important skin disease Gainesville, FL, USA caused by psoroptid and scarcoptid mites.  Mites Mandibulate archaic moths, family Micropterigidae, comprise 130 sp. known worldwide, in 2 subfamilies: Micropteriginae and Sabatincinae. The actual Mango Mealybug, Rastrococcus fauna likely exceeds 175 species. The family is in the invadens Williams (Hemiptera: monobasic superfamily Micropterigoidea, the only Pseudococcidae) representative group of the most primitive extant Lepidoptera, the suborder Zeugloptera. The family Peter Neuenschwander includes small lepidopterans that have retained International Institute of Tropical Agriculture, chewing mouthparts as adults, yet have lepidopteran Cotonou, Bénin, West Africa scales and other adult and larval features that exclude them from Trichoptera. Adults small (5–12 mm This is one of many insects that came to the attention wingspan), with very roughened head scales, and of science only after it had been inadvertently trans- prominent five-segmented folded maxillary palpi; ported and established on a new continent, where it labial palpi short, one to three-segmented; haustel- became an important pest. To date, most field data lum absent (chewing mouthparts). All species are concerning this species are therefore from West diurnally active as far as is known and most species Africa. In the 1980s, mealybug infestations suddenly 2282 M Mango Mealybug, Rastrococcus invadens Williams (Hemiptera: Pseudococcidae) devastated mango, but also many ornamental and importance of plant genotype on mealybug repro- shade trees, around Lomé, Togo, and Cotonou, Bénin. duction and survival. Population peaks were irreg- From there, this new plague rapidly spread along the ular, but mostly in the wet season. Population coast, west to Ghana and Côte d’ Ivoire and east to dynamics were highly influenced by the parasitoids Nigeria. At the turn of the millennium, it had invaded introduced in a classical biological control project. most of West and Central Africa (from Senegal to R. D. Congo). In Benin, for instance, it was observed most often in and around large cities, being less Damage abundant in commercial orchards and even less so on local mango varieties in farmers’ fields. Wherever R. invadens turned up in Africa, it In 1986, it was described as Rastrococcus infested a wide variety of trees from many families invadens Williams (Hemiptera: Pseudoccocidae) (over 100 hundred plant species were listed as from India, where several cryptic species of Rastro- hosts), being noticeable primarily on shade trees, coccus infest mango, a native of this sub-continent. like Terminalia catappa. The abundant honeydew Among them, only R. invadens had made it to West ejected by the mealybug, and the resulting sooty and Central Africa; but interestingly, the species is mold and leaf drop, led to wide-spread cutting of still absent from East Africa. It is also known from ornamental trees and economic damage, mainly all over India, Bangladesh, Malaysia, Sri Lanka, on mango and citrus. In the early 1990s, mango Indonesia, where it seems to be of minor or no eco- production along the Benin and Togo coast was nomic importance, and it has been intercepted by almost completely jeopardized. quarantine authorities in Hawaii. Control Options Morphology and Biology Wherever this mealybug appeared for the first This is a typical white mealybug. It is covered with time, extension services tried to combat it with waxy dust, oval in shape (3–4 mm length) with no pesticides. As the mealybug is often hidden in the wings, weak legs, and long sucking mouth parts on buds and the large mango trees are difficult to the ventral side. It has characteristic waxy lateral cover, insecticides are generally inefficient. Indig- filaments (anterior up to 6 mm, posterior up to enous natural enemies, like coccinellids, are some- 8 mm long). Females produce up to 200 first instar times abundant, but fail to reduce mealybug larvae, which disperse and develop through three populations to acceptable levels. nymphal instars, which resemble each other and Mango varieties vary a lot in their susceptibil- the adult, except for the size increase. Males are ity, but generally it is the wild type mangos (“man- typical winged adults with long caudal filaments gotiers”) that are least affected, but also least and milky wings. They emerge from a characteris- productive. It is clear that resistant/tolerant variet- tic resting stage (“pupa”) and are short-lived. ies alone are not a satisfactory solution. Similarly, The life cycle (egg to first egg) is completed cutting infested branches or entire trees gave only within one month. The females are long-lived (up temporary relief. to 225 days) and the mealybug reproduces throughout the year. Dispersal is probably mostly through humans, particularly on fruits and cuttings from The Solution: Biological Control nurseries. Population densities were usually higher on young than on old leaves and differed markedly Mango, Mangifera indica L. (Anacardiaceae) has between individual mango trees, indicating the been cultivated in India for about 4,000 years. It Mango Mealybug, Rastrococcus invadens Williams (Hemiptera: Pseudococcidae) M 2283 was brought to East Africa in the tenth century By the end-1990s, G. tebygi was established a.d. and from there by the Portuguese to West everywhere in Africa where R. invadens occurred, Africa. It was therefore surmised that this new having dispersed sometimes long distances from mealybug came from India and that classical the release sites. A. mangicola was more difficult to biological control, i.e., the transfer of natural establish; but is now well represented mainly in enemies that keep this mealybug under control large towns. Both species were never found on any in its original home, could bring the solution. other mealybug. Foreign exploration to find natural enemies Both parasitoids are attacked by indigenous was therefore undertaken by CABI Bioscience hyperparasitoids and compete with several spe- in Southeast Asia. This led to the discovery of cies of indigenous coccinellids, which have now two specific parasitic wasps Gyranusoidea become uncommon on mango. As biological con- tebygi Noyes and Anagyrus mangicola Noyes trol took hold in Africa, the original wide host (Hymenoptera, Encyrtidae). spectrum collapsed and today (2002) R. invadens They were shipped to CABI Bioscience in is confined almost exclusively to mango. Overall, the United Kingdom for quarantine. There, the good biological control was achieved, particularly insects were reared and checked as described for in the more humid areas of West and Central the biological control project against the cassava Africa. In the northern savannas, equilibrium mealybug. With the necessary import permits might not yet have been reached or this equilib- and under the umbrella approval of the Inter- rium might not lead to complete control. African Phytosanitary Council of the Organisa- Economic and sociological studies demon- tion for African Unity, G. tebygi was then sent to strated that homeowners and farmers are well an FAO-supported GTZ project in Lomé, Togo, aware of this biological control and that returns and from there to IITA in Cotonou, Bénin, are similar to those found for the biological con- whereas A. mangicola was sent directly to IITA. trol project against cassava mealybug, with yearly Further studies, mass rearing, and releases fol- gains for southern Benin of $50 million and a ben- lowed, first in Togo in 1987 (six releases of efit-cost ratio of $145 for each $1 invested, again G. tebygi), and from IITA in another ten coun- for Benin alone. tries, from 1988 to 2001 (48 releases/deliveries of G. tebygi and 57 releases/deliveries of A. mangicola). This was always done on request by the References local quarantine authorities and in close collabo- ration with national scientists. Agounké D, Agricola U, Bokonon-Ganta HA (1988) Rastro- Laboratory studies revealed that mated coccus invadens Williams (Hemiptera: Pseudococcidae), females lay their eggs into mealybugs, where a a serious exotic pest of fruit trees and other plants in larva develops freely floating in the coelom of the West Africa. Bull Entomol Res 78:695–702 Bokonon-Ganta A, de Groote H, Neuenschwander P (2002) mealybug. The larva pupates in the sausage-shaped Socio-economic impact of biological control of mango dry remains of the mealybug, called a “mummy,” mealybug in Benin. Agric Ecosyst Environ 93:367–378 from where the adults emerge after a total life cycle Neuenschwander P (1996) Evaluating the efficacy of biologi- of about 2–4 weeks, depending on the host stage cal control of three exotic homopteran pests in tropical Africa. Entomophaga 41:405–424 attacked. The tiny G. tebygi attacks first to third Neuenschwander P, Boavida C, Bokonon-Ganta AH, instars, where as the larger A. mangicola prefers Gado A, Herren HR (1994) Establishment and spread older instars, including adult mealybugs that can- of Gyranusoidea tebygi Noyes and Anagyrus mangicola not be attacked by G. tebygi. As a consequence the Noyes (Hymenoptera: Encyrtidae), two biological control agents released against the mango mealybug, Rastrococcus two wasp species do not strongly compete with invadens Williams (Homoptera: Pseudococcidae) in each other, but are complementary. Africa. Biol Control Sci Technol 4:61–69 2284 M Manicapsocidae Williams DJ (1986) Rastrococcus invadens sp. n. (Homoptera awards from zoological park organizations. He Pseudococcidae) introduced from the oriental region to died October 10, 1960, in Washington, DC. West Africa and causing damage to mango, citrus, and other trees. Bullet Entomol Res 76:695–699 Reference

Manicapsocidae Snyder TE, Graf JE, Smith MR (1961) William M. Mann, 1886–1960. Proceedings of the Entomological Society of Washington 63: 68–73 A family of psocids (order Psocoptera).  Bark-Lice, Book-Lice or Psocids Mannerheim, Carl Gustav Von

Manitoba Trap Carl Gustav von Mannerheim was born on August 10, 1797, near Lemo, Finland. He was born into A trap for capturing horse flies and deer flies (Dip- one of the most distinguished families in Finland tera: Tabanidae). It consists of a dark sphere sus- and trained to enter government administration. pended from a tripod, with a canopy suspen-ded Mannerheim served as a governor of two regions above, and topped by a collection apparatus. The of Finland. Despite his political career, Manner- flies are attracted to the dark color and movement heim was interested in natural science, particularly of the sphere and fly upward where they are entomology. He studied at the University in directed by the canopy into the collection appara- Turku, Finland, under the noted entomologist tus, usually a jar. Traps for Capturing Insects. C. R. Sahlberg. Mannerheim was a coleopterist who described many beetles from Russian collections, including species taken in Siberia, Alaska, Mann, William M and California. A prolific writer, Mannerheim was a member of many scientific societies. Mannerheim William M. Mann was born at Helena, Montana, died on October 9, 1854, in Stockholm, Sweden. on July 1, 1886. He was interested in animals beginning in his childhood, and he earned a B.S. References degree at Stanford University in 1911, and a Sc.D. at Harvard University in 1915. The latter degree Essig EO (1931) A history of entomology. The Macmillan was earned under the guidance of William Morton Company, New York. 1029 pp Wheeler, so it is not surprising that Mann became Herman LH (2001) Mannerheim, Carl Gustav von. Bull Am an authority on ants. He was appointed to the Mus Nat His 265:107–108 United States Department of Agriculture, where he worked as a specialist on ants, from 1917 to Manotidae 1925. In 1925 he became director of the National Zoological Park of the Smithsonian Institution, A family of flies (order Diptera). and served in this capacity until his retirement in Flies 1956. In this capacity he traveled over much of the world, and became renowned as a collector of wild animals. He discovered many new species, and Mantidae was featured many times in National Geographic Magazine. He is remembered as a creative and A family of praying mantids (Mantodea). progressive zoo director, and received many Praying Mantids Mantidflies (Neuroptera: Mantispidae) M 2285 Mantidflies (Neuroptera: Mantispidae)

Kurt Redborg Coe College, Cedar Rapids, IA, USA

The family Mantispidae belongs to the suborder Planipennia of the order Neuroptera. The group receives its name from the remarkable resemblance of the adults to praying mantids. Like mantids, adult mantispids, or mantidflies as they are sometime called, have an elongate prothorax, a freely movable head with prominent eyes, and raptorial forelegs composed of a lengthened coxa and a spined femur, which fits against the tibia to immobilize prey (Fig. 5). Of course, the two groups are not closely related, instead providing an excellent example of convergent evolution. Unlike the mantids, mantispids have membranous wings, no cerci, and are holometabolous. Features that mantispids share in the larval stage with other Planipennia include three instars (with the exception of the Coniopterygidae), grooved mandibles and maxillae that fit together to form a piercing/sucking tube, a blind-ended midgut that accumulates wastes that are then voided as a meconial pellet or fluid when the gut becomes complete at maturity, and Malpighian tubules modified for cocoon silk production in the last larval instar (Figs. 6 and 7). Mantidflies (Neuroptera: Mantispidae), Figure 6 There are four recognized subfamilies: Mantispa uhleri Banks, unfed first instar. Symphrasinae (Anchieta, Trichoscelia, Plega),

Mantidflies (Neuroptera: Mantispidae), Mantidflies (Neuroptera: Mantispidae), Figure 7 Figure 5 Mantispa uhleri Banks, adult male. Mantispa uhleri Banks, mature third instar. 2286 M Mantidflies (Neuroptera: Mantispidae) Drepanicinae (Drepanicus, Ditaxis, Theristria, Gers- with their limited need for locomotion. Mantispids taeckerella), Calomantispinae (Calomantispa, have been described as hypermetamorphic, but Nolima), and Mantispinae (all other genera). this is not really true. The three larval instars are While adult mantispids are general predators, not uniquely different from each other and utilize larval feeding is more specialized. Our knowledge the same basic feeding mechanism. The abdomi- of the developmental biology of the first three sub- nal tip of the third instar is modified into a spin- families is sketchy. The larval stages of some mem- neret. When all of the eggs within the sac have bers of the Symphrasinae have been linked with been consumed, the third instar spins a cocoon immature Hymenoptera, Lepidoptera, Coleoptera, with silk from the Malpighian tubules. Pupation and Diptera. It is possible that larvae of some occurs within the cocoon. The pharate adult chews members of these three subfamilies may simply be its way out both the cocoon and egg sac. Since the generalist predators feeding on a wide variety of egg sac may have been constructed in a constricted sedentary arthropod foods. area, such as under tree bark, the pharate adult In contrast, the biology of the Mantispinae is crawls some distance away before undergoing the far better known. Mantispine mantispids develop final ecdysis. within the egg sacs of spiders. This association has There are two basic strategies for spider egg sometimes been referred to as parasitic, but the location by larval mantispids - direct penetration feeding ecology of mantispines is more appropri- of egg sacs that have already been produced and ately termed spider-egg predation because the first deposited in the environment versus the boarding instar larvae are responsible for finding a source of of female spiders with entry into the sac occurring spider eggs. Adult mantispines lay large clutches of during, or closely associated with, its construction. stalked eggs containing from a few hundred to Mantispa viridis Walker, a green mantispid com- several thousand eggs, depending on the size of mon in the southern United States, is an example the ovipositing female, which can vary greatly. of an obligate egg sac penetrator. Larvae are Extreme size variation in both males and females attracted to spider silk and adept at burrowing occurs because larvae are locked into their supply through it but they display no interest in the spi- and there can be great variation in the quantity of ders themselves. Once inside the egg sac, M. viridis food contained within a spider egg sac. There is no larvae are tolerant of other larvae and will com- compelling evidence indicating where females lay mence feeding immediately. It is not uncommon their eggs. The stalk (produced from the female in this species for more than one adult to emerge colleterial gland) on the egg is quite short and it is from the same spider egg sac. Although Mantispa difficult to see how it could serve as the kind of viridis will enter the egg sacs of a wide variety of protective device that longer stalks afford the eggs spiders, it is particularly adept at entering the sacs of Chrysopids. The eggs hatch in about ten days. of web-building spiders that tend to be relatively Newly hatched larvae are campoediform and less immune from attack from spider-boarding man- than a millimeter in length. They aggregate for tispids. Spiders utilized by M. viridis include the unknown reasons around the empty egg cases for cob-web weaver, Achearanea tepidariorum, the a day or so before they disperse. After entering an orb-builder, Argiope aurantia, as well as several egg sac, they pierce the eggs with their short, species of funnel-web spiders belonging to the straight, modified mandibles and maxillae and genus Agelenopsis. Mantispa viridis overwinters drain the eggs of yolk. There are two subsequent inside the spider egg sac where cool temperatures larval instars with a quiescent period of about a arrest its development; it does not seem to have a day separating the first and second and second specific diapausing stage. Thus, severe winter tem- and third stadia. The second and third instars are perature can kill it, which probably explains its physogastric, with reduced legs that are consistent more southern distribution. Mantidflies (Neuroptera: Mantispidae) M 2287 Climaciella brunnea (Say) is probably the after they board. Larvae can easily negotiate the mantispid most familiar to naturalists. Adults are spider’s molts during which they either remain diurnal, often frequent flowers, and are excellent on the pedicel or enter one of the spider’s book- Batesian mimics of Polistes wasps. Climaciella lungs. More than one M. uhleri larva may ini- larvae are obligate spider boarders. First instar tially board a spider but as the spider progresses larvae exhibit a unique phoretic behavior in through molts, the number of larvae is usually which they rear up on caudal suckers and sway winnowed down to one. Analogous to the behav- back and forth with legs outstretched awaiting a ior within an egg sac, a larva attempts to kill or passing spider that they can board. Larvae enter dislodge any competing larvae on the spider. the egg sac as it is being constructed. Larvae are While aboard the spider, larvae maintain them- unable to directly penetrate the silk of an egg sac. selves by piercing the spider’s cuticle and ingest- In fact, if they arrive at the eggs after the eggs ing blood. Other spider-boarding mantispids have been partially enveloped with silk, they can probably do this also. Thus, in this phase of its be spun into the fabric of the sac and become life cycle, M. uhleri is actually a spider parasite permanently trapped. Climaciella brunnea spe- after all. Larvae will board male as well as female cializes on the egg sacs of wolf spiders of the spiders even though only females will provide family Lycosidae, especially the genus Schizocosa. them with a direct source of spider eggs. This sit- Larvae adopt positions around the edge of the uation is not as “dead end” as it sounds. Larvae spider’s carapace. Multiple boardings of more of M. uhleri will transfer from males to females than one larva per spider do occur. Larvae pass when they are cannibalized after mating. Larvae the winter aboard the spider. Mantispa pulchella of Mantispa pulchella and Climaciella brunnea Banks is also an obligate spider boarder. In this will actually make the transfer during copula- species, there is always only one larva to each tion by their spider hosts. spider; the larva is always found loosely draped The major spider host for M. uhleri in the over the spider’s pedicel. Mantispa pulchella Midwest is the philodromid spider Philodromus specializes on boarding small, foliage-inhabiting vulgaris Hentz. Infestation levels on this spider spiders, particularly spiders of the family often exceed 50% Selection pressure is so Anyphaenidae. great on this spider that it has evolved an anti- Some mantispids facultatively utilize either mantispid mechanism. Without any additional egg location strategy. In the laboratory, first- feeding, female P. v u lg ar i s produce a second, instar Mantispa uhleri Banks will penetrate egg smaller egg sac a few days after the first sac. sacs and can also be found extensively in the The two sacs are constructed next to each other field aboard a variety of spiders. After penetrat- and the female guards both sacs. If a mantispid ing an egg sac, uhleri larvae can halt the develop- successfully enters the first egg sac, all the eggs ment of the spider eggs within the sac with an within it are consumed. But, the second egg sac aggressive allomone, although the manner by escapes predation, at least from mantispids. which the mantispid uses this chemical is not yet known. If more than one larva enters the sac, each larva will attempt to kill the other and References refrain from engorging on eggs until they are the only larva left alive in the egg sac. If the sac con- Brushwein JR, Hoffman KM, Culin JD (1995) Seasonal phe- tains hatching spiderlings, the larva will board nology and overwintering of Mantispa viridis Walker one of the spiderlings and attempt to follow the (Neuroptera: Mantispidae) in South Carolina. J Ento- mol Sci 30:112–119 spiderling through to its adult stage. Larvae wrap Hoffman KM, Brushwein JR (1989) Species of spiders themselves tightly around the spider’s pedicel (Araneae) associated with the immature stages of 2288 M Mantids Mantispa pulchella (Neuroptera: Mantispidae). Many-Plumed Moths J Arachnol 17:7–14 MacLeod EG, Redborg KE (1982) Larval platymantispine (Lepidoptera: Alucitidae) mantispids (Neuroptera: Planipennia): possibly a subfamily of generalist predators. Neuroptera Int 2:37–41 John B. Heppner Redborg KE, Redborg AH (2000) Resource partitioning of Florida State Collection of Arthropods, spider hosts (Arachnida, Araneae) by two mantispid species (Neuroptera, Mantispidae) in an Illinois wood- Gainesville, FL, USA land. J Arachnol 28:70–78 Redborg KE (1998) Biology of the Mantispidae. Annu Rev Many-plumed moths, family Alucitidae, total Entomol 43:175–194 Redborg KE, MacLeod EG (1985) The developmental ecology about 184 species worldwide. The family is part of Mantispa uhleri Banks (Neuroptera Mantispidae). of the superfamily Copromorphoidea in the sec- Illinois Biological Monographs, 53, p130 tion Tineina, subsection Tineina, of the division Ditrysia. Adults small (7–28 mm wingspan), with head smooth-scaled; haustellum naked; Mantids labial palpi porrect, mostly with long second segment; maxillary palpi 3–5-segmented (rarely Members of an order of insects (Mantodea) They vestigial). Wings with rounded shape (hindwing also are known as praying mantids. merges with forewing margin) and all veins as Praying Mantids separate wing clefts to near the wing bases, and fringed (at least one Neotropical species has the clefts split only half way in from the termen). Mantispidae Maculation shades of gray, with various bands or spots, but a few with shades of brown or yellow, or white, and both forewings and hindwings A family of insects in the order Neuroptera. They with matching or merging patterns. Adults active commonly are known as mantidflies. Lacewings in deep shade, or may be crepuscular. Larvae  Antlions and Mantidflies are borers or gall makers as far as is known. The few plant records are in Bignoniaceae, Caprifo liaceae, Compositae, Dipsaceae, Labiatae, and Mantodea Rubiaceae.

An order of insects. They commonly are known as praying mantids or mantids. Praying Mantids References

Buszko J (1977) Alucitidae. In Klucze do Oznaczania Owadów Polski. 27. Motyle-Lepidoptera, 97:1–17. Mantoididae Polskie Towardzystwo Entomologiczne [in Polish] Heppner JB (2003) Alucitidae of North America (Lepidoptera: Copromorphoidea). Holarctic Lepidoptera (Gainesville), A family of praying mantids (Mantodea). [in prep]  Praying Mantids Meyrick E (1910) Lepidoptera Heterocera. Fam. Orneodi- dae. In Genera Insectorum, 108. P. Wytsman, Brussels. 4 pp, 1 pl. Scholz A, Jäckh E (1994) Taxonomie und Verbreitung der Mantophasmatidae westpaläarktischen Alucita-Arten (Lepidoptera: Alu- citidae (Orneodidae)). Alexanor 18(4):1–64 Sutter R (1990) Beiträge zur Insektenfauna der DDR: A family of gladiators (order Mantophasmatodea). Lepidoptera-Alucitidae. Beiträge zur Entomologie  Gladiators (Mantophasmatodea) 40:113–119 Marine Insects and the Sea-Skater Halobates (Hemiptera: Gerridae) M 2289 March Flies Although insects originated in swampy areas some 300 millions years ago, they then moved toward a Members of the family Bibionidae (order Diptera). terrestrial existence, evolving various physiologi-  Flies cal adaptations which allowed them to become independent of water or damp places, and to achieve dispersal though the air. Margarodidae Some of the most important adaptations of many insects living on land include the following: A family of insects in the superfamily Coccoidae (order Hemiptera). They sometimes are called ·· Hardened, impermeable cuticle often impregnated giant coccids or ground pearls. with lipids to cut down on water loss.  Bugs ·· Tracheal breathing system for efficient distribution of oxygen by diffusion. Marginal Cells ·· Wings for long-range aerial dispersal. ·· Complete metamorphosis, which may allow adults and young to exploit completely different habitats. Cells found along the periphery of the wing near the costal margin.  Wings of Insects Surviving the Marine Environment

Marginal Vein In order to return to the sea they have had to solve a number of ecological, physiological as well as A vein found at or near the wing margin. physical problems. Some of these problems, e.g.,  Wings of Insects osmotic regulation, they have succeeded in solv- ing, while others, e.g., underwater respiration, are perhaps insurmountable, hence the rarity of Marginidae insects at sea. Although, several thousand insect species are known to live in various marine envi- A family of flies (order Diptera). ronments, the five oceanic Halobates species are  Flies the only ones known to spend all their lives at sea, but even they are confined to the air-sea interface. Because they do not fly, nor do they normally dive, Marine Bugs Halobates must face certain challenges in order to live in such an unusual habitat. Some of these chal- Members of the family Aepophilidae (order lenges are: Hemiptera).  Bugs ·· Avoidance of drowning – This is probably the foremost problem they have to solve. Storms at sea can be fierce, and it is highly likely that these Marine Insects and the Sea-Skater tiny insects would then be pushed underwater. Halobates (Hemiptera: Gerridae) They solve this by surrounding their bodies with a layer of tiny hairs that trap air and form an air- Lanna Cheng bubble around them (Fig. 8). This not only allows Scripps Institution of Oceanography, University them to bob up to the surface rapidly if they are of California-San Diego, La Jolla, CA, USA pushed underwater, it also acts as a mechanical 2290 M Marine Insects and the Sea-Skater Halobates (Hemiptera: Gerridae) gill in that when the oxygen level in the bubble is low, more oxygen diffuses into the bubble from surrounding sea water. ·· Solar irradiation – On sunny days, Halobates are totally exposed to the tropical sun because there is no shade to be found anywhere in the open ocean. They have, therefore, evolved a sort of sunscreen in the form of a UV-absorbing layer in the cuticle to protect them from radiation damage (Fig. 9). Although the chemical composition of this substance is unknown, it is able to absorb almost all of the UV rays at the potentially damaging wavelength of 280nm, allowing less than 0.01% to pass through the cuticle to reach Marine Insects and the Sea-Skater Halobates reproductive and other soft tissues underneath. (Hemiptera: Gerridae), Figure 8 Section of cuticle ·· Starvation – Prey animals may be found only spo- of Halobates germanus showing micro-hairs layer radically at the sea surface, thus Halobates must in side view (scale = 1 μm, from Cheng, 1973; have the ability to withstand short-term starva- Nature 242: 132–133). tion. They do this by storing triglycerides in their fat bodies, which provide a ready energy source. ·· Mate location – It is not known how adult Halo- ocean, miles away from land. The others occur bates find mates of the opposite sex at sea. Even near the coast and, under ordinary circumstances, if individuals are brought within meters of one do not venture out to the open ocean (Fig. 10). another by winds and waves, it is still necessary for Sea-skaters are found only in warm waters the sexes to come into contact. They may use where the winter temperature is above 20°C. Coastal surface-dispersible pheromones for aggregation species are common around tropical islands fringed or as sex attractants. Although no such chemicals with mangroves or other trees, but are normally have yet been detected in Halobates, they have absent from coral atolls or islands devoid of fring- been demonstrated in a coastal relative, Trochopus ing vegetation. They feed on terrestrial insects that plumbeus (Veliidae) (Fig. 8). have fallen or are trapped at the sea surface, and carry out their life cycle very much like those of their fresh water cousins. Oceanic Halobates, how- Sea-skaters, Halobates spp ever, have evolved many special adaptations necessary for their survival at sea. The sea-skater Halobates is undoubtedly one of The air-sea interface where these insects live is the most remarkable members of the class Insecta. unique in many ways. This is where the ocean It is the only insect that has succeeded in living in meets the atmosphere, where air-borne particles the open sea. It is a member of the Family Gerri- accumulate when they fall, where nutrients are dae, commonly known as pond-skaters or water brought up to the surface from deep water by air striders. The gerrids are some of the most com- bubbles and where various chemical and physical mon aquatic bugs in the order Heteroptera and interactions take place. Although scientists have can be found in a great variety of fresh water as been measuring seawater temperature, salinity, well as brackish and marine habitats. The genus current flow, wind velocity, etc., for decades, almost Halobates is almost exclusively marine. All but one all of the measurements were taken in a water col- of its known species occur in the sea. Of the 45 umn. Physical and chemical measurements of the described species, only five are found in the open surface film have proved to be more difficult until Marine Insects and the Sea-Skater Halobates (Hemiptera: Gerridae) M 2291

Marine Insects and the Sea-Skater Halobates (Hemiptera: Gerridae), Figure 9 UV photomicrography taken at 280 nm of thin sections of Halobates cuticle showing dark UV-absorbent layer (from Cheng et al. 1978; Limnology and Oceanography 23:554–556).

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20� 100� 140� 180� 140� 100� 60� 20� 0� 20� xxxx Marine Insects and the Sea-Skater Halobates (Hemiptera: Gerridae), Figure 10 Distribution of five pelagic Halobates species (from Cheng 1974; Marine Fisheries review 36:1–7). 2292 M Mariner the last 10 years, when special sensing devices were easily distinguished by the presence in the males developed. Attempts to correlate the occurrences of external genital processes that are characteristic of oceanic Halobates with physical or chemical fea- for each species. They are predators, feeding on tures of the sea surface are thus still in their infancy. animals trapped at the sea surface. Adults and We do, however, know quite a lot about their distri- older nymphs are also cannibalistic. They are, in butions, biology and special adaptations. turn, preyed upon by sea birds (by far their most All five pelagic (i.e., open ocean) Halobates important predators), surface-feeding fishes, and species occur in the Pacific Ocean, two are found in occasionally turtles. the Indian Ocean and only one occurs in the Atlan- tic Ocean. Each species has a rather well defined distribution pattern, but we still do not understand References fully what determines such patterns. We do know, however, that these patterns are controlled to a large Cheng L (1973) Marine and freshwater skaters: differences in extent by seawater temperatures and currents. surface fine structures. Nature 242:132–133 Cheng L (1974) Notes on the ecology of the oceanic insect Halobates. Mar Fish Rev 36:1–7 Cheng L (1976) Insects in marine environments. In: Cheng L General Biology (ed) Marine insects. North-Holland Publishing Com- pany, Amsterdam, pp 1–4 Cheng L, Douek M, Goring DAI (1978) UV absorption by The eggs of oceanic Halobates are laid on flotsam: gerrid cuticles. Limnol Oceanogr 23:554–556 seeds, plastic, wood, mollusk shells, sea bird feath- Cheng L (1985) Biology of Halobates. Annu Rev Entomol ers and even tar lumps. There are five larval stages. 30:111–135 The young resemble adults in general morphology Cheng L (2003) Marine insects. In: Resh VH, Carde R (eds) Encyclopedia of insects. Academic, San Diego, although they are smaller. The sexes are not distin- California, pp 679–682 guishable until the final larval stage. The general Herring JL (1961) The genus Halobates (Hemiptera: Gerri- body plan of Halobates is similar to those of dae). Pac Insects 3:223–305 Cheng L, Frank JH (1993) Marine insects and their reproduc- other gerrids (Fig. 11), but Halobates are totally tion. Oceanography and marine biology Annu Rev wingless at all stages of their life cycle. Adults 31:479–506 measure 5–6 mm in body length and the sexes are Mariner

A transposable element that has been engineered for transforming insects other than Drosophila. mariner elements are widely found in most arthropods and in insect-parasitic nematodes, other nematodes, flatworms, hydras, humans, mouse, rat, Chinese hamster, sheep and cow. mariner has been used to transform chicken, zebrafish and a protozoan.

Marker (DNA Marker) Marine Insects and the Sea-Skater Halobates (Hemiptera: Gerridae), Figure 11 Halobates A DNA fragment of known size used to calibrate sericeus female feeding at sea surface. an electrophoretic gel. Marking Insects for Studying Ecology and Behavior M 2293 Marker (Genetic) cotton fields with a blue enamel paint, and it was estimated that about one-third of the boll weevils A trait that can be observed to occur (or not) in an received the marker. However, this method was organism. Marker genes include genes conferring reported as being messy, hard on the spray equip- resistance to antibiotics, expression of green fluo- ment and the cotton plants, and it had unknown rescent protein, eye color, etc. effects on boll weevil behavior. In one study where fluorescent dye was applied to hornflies, Haemotobia irritans L., only Marking Insects for Studying 26–60%; of the dye was detected, and the dye was Ecology and Behavior also lethal to the hornflies. Individually applied external labels often inflict trauma upon the insect Allan T. Showler and are impractical in lieu of other options. Dusts USDA-ARS SARC, Weslaco, TX, USA (including pollen) and dyes have been used to label large numbers of insects. Pollen can be used Insect ecology and behavior studies often occur in to determine the origin of insects in dispersal conditions that preclude visual observations. To studies by passive marking (the insects’ natural assess insect dispersal, subterranean habits, feed- interaction with flora in the area) but these labels ing, and complex ecological relationships among may be lost, are suitable only between molts, and diversified taxa, efficient markers (synonymous are not reliable for monitoring species with cryp- with labels and tags) are useful. An effective and tic habits. Therefore, external markers are usually versatile marker should have the following charac- of little value for studying insect behavior over teristics: easy to apply to large populations, mini- long periods of time, for researching trophallaxis mal manipulation and trauma to the test insect(s), and food webs. Visual labels can affect insect detectable without destroying or killing the insect behaviors by abrasion, added mass, altered appear- sample, persist in the insect or community, and no ance, and health related side effects. Some research- adverse effects on the physical functions or behav- ers have suggested that external visual markers ior of the labeled organisms. A number of marking might make labeled insects more visible to techniques have been used for insect tagging in predators. behavior and ecology studies. Dyes were ingested by imported fire ants, Solenopsis invicta Buren, in an experiment to monitor the intracolony exchange of various Visually Detected Markers foods; however, detection of the label required the destruction of the insects for dye extraction, parti- Visually detected markers include wire ties, paints, tioning and drying before light wavelength absor- dyes, inks, powders, pollen, and spores that are bance was measured. In another study, imported fixed to the insects at least until sampling for fire ants were labeled with ingested dyes which tagged insects is completed. These methods, how- were detected visually after the ants were crushed ever, commonly suffer limitations. One study eval- on white paper. Ants have also been dissected in uated the use of wire ties, paint, and excised legs as order to detect ingested dyes, however, it is diffi- markers for ants (Solenopsis sp.). The wire ties cult to detect dyes and vital stain indicators in stayed on, but attaching them was laborious and small quantities. required anesthetization of the ants. Workers with Ingestion of pollen and spores can also be excised legs were killed by their nestmates, and used to mark insects but the labeled insects must painted labels were scraped off. In another study, a be dissected to determine the presence or absence ground sprayer and an airplane were used to spray of these markers. In spite of the limitations and 2294 M Marking Insects for Studying Ecology and Behavior assumptions required for many applications of Radiotracers visual markers, a large number of studies, especially on dispersal (mark-recapture studies), have A desirable marker (i) provides analogs for bio- been conducted with varying degrees of success. logically essential elements, (ii) does not require the destruction of labeled samples, (iii) persists in readily detectable quantities for longer periods of Rubidium time, (iv) is easily applied to large numbers of insects with minimal manipulation of the popula- Rubidium (Rb) markers can be ingested from tions, and (v) may permit detection in the field, labeled artificial diet, tagged solutions sprayed even when tagged insects are located underground onto host plants, and host plants raised from Rb- or within plant material. Unlike Rb, radioactive treated seeds. For example, pea aphids, Acyrthosi- isotopes (radiotracers) provide analogs of biologi- phon pisum Harris, have been labeled after feeding cally essential elements such as P-32, C-14, H-3, on bean, Phaseolus sp., plants cultured in Rb- I-125, S-35, and Ca-45 that can be applied to study tagged nutrient solutions. Rubidium can be physiological phenomena including reaction detected using atomic absorption spectroscopy in rates, metabolic pathways, and the distribution pea aphids for up to 4 days (77% was eliminated in and incorporation of elements or molecular com- 2 days) after marking, and for up to 34 days after pounds in biological systems. Radioactive analog marking in the adult Mexican bean beetle, Epil- or non-analog nuclides can also be administered achna varivestris Mulsant. Unlike most visually to monitor the behavioral and ecological dynam- detectable markers, ingested Rb can be retained ics of individuals, populations, and biotic commu- from larval to adult stages as has been demon- nities. The sensitivity of radiation detection strated in the corn earworm, Heliothis zea Boddie; exceeds that of most chemical and physical meth- tobacco budworm, Heliothis virescens F.; fall army- ods. To illustrate, carrier-free tritium at 30 Ci per worm, Spodoptera frugiperda J. E. Smith; pink mmole can be diluted by a factor of 1012 without bollworm, Pectinophora gossypiella Saunders; cab- hindering detection. In one study, 200 μ Ci Zn-65 bage looper, Trichoplusia ni Hübner; and the in 20 ml molasses was used to label an entire imported cabbage worm, Pieris rapae L., and other imported fire ant colony. The tracer was easily insects with no observed toxic effects. Cabbage detectable in the ants six months after the tagged looper fecundity, fertility, longevity, mating behav- bait was removed. Radiolabels can be detected ior, and responses to sex pheromones were not while the tagged insect is living or dead, after being influenced by ingested Rb concentrations of as ingested by a predator or while the insect is func- much as 28,000 ppm. Rubidium labels have been tioning in the environment. useful for studying the dispersal patterns of the More than 44 different radionuclides have flights of various insects, including the corn been used in entomological studies. To select a earworm, fall armyworm, and pink bollworm. radiotracer for labeling insects, several factors Food chains to the primary predator level in crop must be considered: (i) the effective half-life of the systems (e.g., cotton and grain sorghum) have isotope in the organism, (ii) possible toxic effects been studied using Rb tags. Despite these advan- to the insect, (iii) the type of radiation emitted, (iv) tages, researchers have reported equivocal results the energy of the radiation, (v) the form or valence because of variation and detectable levels of natu- of the radionuclide, and (vi) the ease of handling rally occurring Rb in their samples. Quantification and detecting the label. of Rb also requires the physical destruction of The amount of a radioisotope retained by an samples for the use of atomic absorption spectros- insect after administration of a single internalized copy or flame emission spectrophotometry. dose can decrease exponentially through time Marking Insects for Studying Ecology and Behavior M 2295 because of biological elimination and radioactive Sr-85 + Co-60 produced lethal effects, Co-60, decay. The time required for the amount of a par- Cs-137, Sb-125, Mn-54 + Zn-65, Mn-54 + Se-75, ticular internalized radiotracer to decrease by Co-60 + Cs-137, and Cs-137 + Se-75 were not one-half in a given insect is termed the “effective toxic to the termites. The wasp Habrobracon half-life.” Effective half-lives of radiotracers decr- juglandis Ashmead developed “radioresistance”; ease in response to excretion, oviposition, length P-32-treated adults survived as long or longer than of exposure to labeled bait, life stage, or caste of controls. In some cases, sublethal doses of radia- the insect, and the nature of the labeled food tion have been shown to reduce insect fecundity. ingested (e.g., oil, protein, carbohydrate). Radio- Habrobracon juglandis adults fed on less than 50 μ activity can, however, be unequivocally detected Ci P-32 per gram of labeled food showed no ill- long after the isotope’s effective half-life has effects, 50–200 μ Ci resulted in decreased (26%) elapsed. To minimize loss of radiotracers in indi- egg production, and 200 μ Ci halted the egg pro- viduals over time, isotopes may be delivered to duction process. Eggs produced from radiolabeled insects in a continuous infusion through a con- adults may also show increased mortality and off- stant supply of radiolabeled food or water, or by spring hatched from labeled eggs may be deformed using large, but nontoxic, single pulse doses of or die soon after eclosion. Boll weevil larvae raised radionuclides. on P-32-labeled diet had reduced longevity, fecun- A radiolabel might be detrimental to the inoc- dity, and pre-oviposition and oviposition periods ulated system (and researcher) because of the nature compared to adults fed on P-32-labeled diet. On of the emitted radiation. The biological hazards of the other hand, radiotracers in other insects, such radiation, although negligible in most studies, have as the screwworm fly, Cochliomyia hominivorax been emphasized by the media, thus the decline in Coquerel, did not affect longevity, fecundity, fertil- radioecology studies after the early 1960s. Radio ity or egg eclosion. Therefore, the use of a fixed tracers have received wide application in insect radionuclide dose may be suitable for one species biochemistry and physiology experiments; various or life stage within the same species, but impracti- isotopes are selectively distributed within insect cal for another species or intraspecies life stage. bodies. Female Aedes aegypti L. mosquitoes were Nuclides that release energy as gamma pho- twice as radioactive as males. Depending on the iso- tons have advantages peculiar to the nature of tope, the dose of radionuclide, the type of radiation, gamma radiation. Gamma-emitting isotopes pro- the insect species and life stage exposed, and the duce characteristic spectral emission’ signatures’ method of administration, radiation levels that such that confusion between different radionu- cause toxic effects may differ. Toxicity can also result clides in the same insect or community is elimi- from a species-dependent overdose of the element nated. Additionally, because gamma rays have itself. Toxic levels of isotopes such as Ca-45, Fe-59, negligible mass and are highly energetic, gamma- Ag-110, Cd-115, and I-131 in certain insect species emitting isotopes have been employed to locate have been documented. cryptic insects through several cm of soil and up White pine weevils, Pissodes strobi (Peck), to 14 cm of wood. painted with 500 μ Ci Co-60 per individual did There are several methods for administering not suffer increased mortality for at least two radiotracers to insects. Radiotracers can be applied months, whereas in boll weevils, Anthonomus as components of biologically essential com- grandis grandis Boheman, mortality increased pounds for biochemical research and radiolabeled when P-32 concentrations exceeded 9.9 μ Ci mosquito sperm has been developed for mating per gram of labeled diet. Mortality studies on ter- studies. The following methods have been imple- mites, Reticulitermes flavipes Kollar, revealed that mented to tag individual insects, populations, or although equivalent amounts of Mn-54, Sr-85, and biotic communities. 2296 M Marking Insects for Studying Ecology and Behavior Dipping and Painting smeared or sprayed with radiotracers have produced desired results in a variety of insects. Labeled Dipping insects in radioactive solutions, including wood, blood, and living insect prey have been I-131, Se-46, Ir-192, and Co-60, has been used to employed to tag termites, mosquitoes, and man- mark individual arthropods such as white pine tids, respectively. A more refined radionuclide weevils, and Co-60 dips for labeling boll weevils. delivery technique involves rearing insects on The addition of a detergent allowed a P-32-labeled plants cultured in radiotagged nutrient solutions water dip to penetrate the cuticle of the ant Lasius or plants injected with radioisotopes. Insect food flavus F. for a detectable retention time of 10 days. webs on the thistle, Cursium undulatum Nutt., bal- Dipping might not work in some instances, such sam fir, Abies balsamea L., and other plants were as when the plum curculio, Conotrachelus nen- determined by injecting the plants with P-32. Sim- uphar Herbst., was dipped in P-32 solution despite ilarly, P-32 injected into living rats, rabbits, goats, supplementation with wetting and sticking agents. sheep, and hamsters resulted in the tagging of However, P-32-glycerin suspensions painted onto insects including A. aegypti, screwworm flies, and the southern pine beetle, Dendroctonus frontalis Oriental rat fleas, Xenopsylla cheopis Rothschild. Zimmermann, enabled the location of the tagged Food interaction studies have been conducted beetles after dispersal by the presence of radiotag in the White Oak Lake bed, an area in South on host tree pitch tubes. Southern pine beetle Carolina contaminated by Cs-137 and Sr-90 adults were also labeled as they emerged from tree wastes that were subsequently translocated by the boles painted with P-32. Painted radiolabels, like terrestrial plant community. Naturally occurring many visual markers, can be chipped or washed U-238 and Th-232 fission products bismuth-214 off, and thus might give false indications of radio- and actinium-228 were similarly used in a stream activity in the environment. ecosystem.

Disc and Wire Attachments Water Culture

The movements of various subterranean beetle Large quantities of aquatic insects such as mosqui- larvae have been monitored with external attach- toes and blackflies have been labeled through ments labeled with Ra-226, Ta-182, and Co-60. adulthood when the larvae were raised in Similarly, Ta-182 wire glued to coccinellid larvae P-32-tagged water. In a large scale application of was used to investigate crawling behavior on foli- this technique, Zn-65 was sprayed onto a lake, and age. Discs and wires glued or tied to the insect P-32 was systematically dripped into a stream to exoskeleton or inserted within the insect’s body examine the trophic structure of each system. have the disadvantages of some visually detected markers. Trans-life Stage Transmission

Ingestion Radiotracers can be passed from one life stage of an insect to other life stages, and in a sense, this Isotopes can be transferred to insects by ingestion can be viewed as being a delivery system if an of radiolabeled food; in this way, large numbers of earlier life stage is more effectively tagged for marked insects can be reared simultaneously. studying a subsequent life stage. This can be Tagged sugar and honey solutions, artificial diets, accomplished when the initially labeled insect royal jelly, milk, raw meat, and living plants stage obtains the tag by injection, ingestion, or Marking Insects for Studying Ecology and Behavior M 2297 water culture. Grasshoppers, Melanoplus mexi- NAA markers are made radioactive by exposing canus Sauss and Camnula pellucida Scudder, were samples to specific thermal neutron fluxes in a shown to retain ingested P-32 from nymphs to nuclear reactor, the thermal neutron capture cross- adults. Similarly, radioisotopes ingested by larvae section of the nuclide should be large (≥ 0.1 barn). of imported cabbageworm (Ca-45 and P-32), The natural abundance of the stable tracer in the Panaxia sp. and Arctia caja L. (S-35), and boll wee- experimental system should be less than 10% of vil (P-32) were retained to adulthood. Screwworm the applied dose to avoid equivocal results such as fly larvae raised on P-32-injected goats and sheep those encountered with Rb labels. The NAA tracer had detectable levels as pupae, adults, and eggs for insect studies should be selected for a short and larvae of the next generation. Examples of half-life and readily detected radiations (prefera- insects that had ingested radiotagged food and bly gamma rays) after the nuclide has been acti- transferred the label to their eggs include Habro- vated. NAA methods provide radio-safety in the bracon juglandis, (Sr-89), the walnut husk fly, environment, a diversity of nuclides from which to Rhagoletes completa Cresson, and the velvetbean choose, and sensitivity of detection. The tech- caterpillar, Anticarsia gemmatalis Hübner (P-32). niques also permit long-term experiments without P-32 was transmitted from tobacco budworm decay of the tracer, nondestructive sample analysis adults to eggs to larvae. Larval mosquitoes and such that the same sample can be repeatedly acti- blackflies raised in P-32-labeled water cultures vated and measured, and quantification of the retained the tag into adulthood, and egg batches of label in each sample based upon the amount of Culex pipiens L. mosquitoes retained P-32 from radiation emitted. Drawbacks to NAA techniques adults raised as larvae in a labeled water culture. include (i) relatively long (≥ 1 d) analyses of the There are a number of different ways of samples, (ii) persistence of the stable tracer in the detecting radioactive decay. The choice of detector environment which may render future experi- depends upon the type of radiation, the physical ments in the same area unreliable, and (iii) “loss” state of the sample, and where detection will of the tracer in the experimental system until NAA occur (e.g., in the laboratory or the field). The is performed. The activated nuclide can be detected Gieger–Müller tube, liquid scintillation and solid and quantified using the same diversity of meth- detectors, autoradiography, and portable rate ods available for conventional radiotracers. meters have received the greatest application in Toxicity to the insect may result from stable- insect ecology and behavior studies. activable tracers, but detectable nontoxic levels Representative insect ecology and ethology may be determined by experimentation. Applica- radiotracer include population measurements, tion of these elements to insects has been achieved dispersal and movement, territoriality, feeding through ingestion and by exposure to the insect’s behavior (including trophallaxis), vector-parasite cuticle. Some plant species, such as white mustard, relationships, and food chains and webs. Brassica hirta Moench, and hairy vetch, Vicia villosa Roth., have been shown to translocate Dy and Eu from soil to leaves; thus certain herbivorous Neutron Activation Analysis insects may be labeled on tagged host plants, and by extension, food webs could be examined using Because of public concern regarding the poten- NAA methods. tially hazardous effects of ionizing radiation, some Rare earth tags have been detected in medi- scientists have used neutron activation analysis cally and agriculturally important insects, includ- (NAA) as an alternative. Rare earth elements, such ing the tsetse fly, Glossina morsitans Westwood as Sm and Dy, are good tracers but are not analo- (from Eu-, Dy-, Au-, and Ir-labeled nutrient solu- gous to biochemically essential elements. Because tions), and the Mediterranean fruit fly, Ceratitis 2298 M Marking Pheromones capitata Wied. (Mn-labeled nutrient solutions). eggs were marked by feeding them with rabbit NAA has been used in some insect ecology and Ig-tagged honey solution, and others were marked ethology studies, including dispersal of Drosophila externally tagged by contact exposure or topical spp. and effects of vegetative cover on the sizes of mist. The Ig marker was retained by the parasitoid imported fire ant territorial areas. throughout the entire adult lifespan (<2.5 d) Other activation analysis methods have been regardless of the application method. conducted with trace elements and compounds such as zirconium oxide, Bi, Pb, cerium oxide, Sn, and Se sprayed on mosquitoes then bombarded References with alpha particles in a cyclotron to produce X-ray emissions. DiGregorio D, Kitchings T, Van Voris P (1978) Radionuclide transfer in terrestrial animals. Health Phys 34:3–31 Hagler JR, Cohen AC, Bradley-Dunlop D, Enriquez FJ (1992) New approach to mark insects for feeding and dispersal Carbohydrate Profiling studies. Environ Entomol 21:20–25 McKibben GH, Robbins JT (1996) Chemical fingerprinting Gas-liquid chromatograph profiles of cuticular of boll weevils using surface lipid analysis. In: Proceed- ings of the Beltwide Cotton Conferences. National Cot- lipids extracted from the surface of insects is a ton Council, Memphis, Tennessee, pp 232–233 form of “passive” marking in that the marker was Showler AT, Knaus RM, Reagan TE (1988) The versatility of naturally acquired by the insect during its lifetime. radiotracer methods for studying insect ethology and This technique has received limited use, including ecology. Fla Entomol 71:554–580 Showler AT, Knaus RM, Reagan TE (1990) Foraging territo- application for determining differences in age, sex, ries of the imported fire ant as determined by instru- and geographical origin of screwworm flies. One mental neutron activation analysis. Insectes Soc preliminary study showed that overwintered boll 36:235–239 Southwood TRE (1978) Ecological methods. (2nd edn) weevils could be distinguished from other indi- Chapman and Hall, London viduals, and that geographic origins of boll weevils may be determined with 90% certainty. Marking Pheromones Immunoglobulin Ronald J. Prokopy Various immunoglobulins (Ig) can be applied to University of Massachusetts, Amherst, MA, USA insects and later detected using enzyme-linked immunosorbent assays (ELISA). Applications of A marking pheromone is a chemical compound this marking method have been few and the pri- (or mixture of compounds) emitted by an insect mary limitation has been relatively rapid loss of that advertises the past or current presence of the unequivocally detectable levels of the Ig (generally insect or its progeny at or in association with a val- measurable loss occurs within a week). The ued resource. The type of resource may be food, an following examples, however, illustrate how Ig egglaying site, or a site of shelter. methods can be used in different ways. Conver- Some kinds of insects foraging for food save gent lady beetles, Hippodamia convergens Guérin– valuable time and energy and improve foraging Meneville, were marked and recaptured after as efficiency by following a trail of marking phero- long as 30 d using rabbit Ig, and chicken Ig was mone deposited by conspecifics that have discov- 75% effective after 11 d. Lygus hesperus Knight ered a quality food resource. Other kinds of were marked for 8 d by submersion in rabbit Ig. insects foraging for food or egglaying sites avoid Anaphes iole Girault, a parasitoid of Lygus spp. investing time, energy, or progeny at depleted Marking Pheromones M 2299 or overcrowded resources by rejecting locales eggs, larvae, or pupae, fruit flies (family Tephriti- scented with marking pheromone. A few kinds of dae) that oviposit in the flesh of host fruit, and insects use pheromone to mark territories around beetles that oviposit on or in seeds illustrate the nests that serve as sites of shelter. role of marking pheromone in preventing over- Marking pheromones may be released from a crowding of larval food resources. Often, the host variety of endocrine or exocrine glands of insects of a parasitoid, tephritid fly, or seed beetle can sup- as well as from other structures associated with port only a single larva to maturity. Pheromone digestive, reproductive and locomotory systems. released during or after egg deposition signals Most marking pheromones are non-volatile and occupancy by a conspecific. In a few cases, host- can be detected only when touched by antennae, foraging females may be able to detect host occu- mouthparts, tarsi, or the ovipositor. Some, how- pancy and associated marking pheromone of a ever, are volatile and can be detected via antennae close or distant relative. at distances of several centimeters. Sometimes, a host is sufficiently large enough Ants and tent caterpillars are good examples to support several larvae to maturity, though never of insects that follow a trail of marking pheromone an unlimited number. In such cases, marking to enhance food-foraging efficiency. After finding pheromone may allow a female to assess not food, fire ant workers and tent caterpillar larvae merely the presence versus the absence of an occu- deposit marking pheromone on their return to the pant, but also to assess the level of occupancy, as nest. The pheromone signals the discovery of food determined by the amount of pheromone present to conspecifics, which then proceed to follow the relative to the size of the host. trail to its source. The greater the amount or qual- Some predatory insects, such as neuropteran ity of the food, the greater the amount of phero- lacewing females and coleopteran ladybird females, mone deposited. Trail marking ceases when the use marking pheromone as a cue for avoiding food supply is exhausted. overcrowding food resources (particularly colo- Honeybees and bumblebees are good examples nies of aphids) that will serve as prey for larval of insects that use information from marking pher- progeny. Although aphids may be numerous at the omone as a cue to cease foraging (at least temporar- time of predator oviposition, they are unlikely to ily) for food at marked sites. Bees may visit a variety remain so in the face of the voracious appetites of of flowers to obtain nectar. When doing so, they lacewing and ladybird larvae. Several members of temporarily deplete the nectar supply of florets, these groups are known to refrain from oviposit- which may not be renewed for an hour or more. If ing in the presence of conspecific larvae. The most a bee were to invest time and energy probing for frequently encountered cue indicating larval pres- nectar in florets whose supply was not yet renewed, ence is the marking pheromone associated with it could jeopardize its ability to acquire a full com- the footprints of conspecific larvae. plement of nectar. Marking pheromone deposited The physiological and informational state of on a floret by a previous forager signals the arriver an insect, along with the state of the environment, that the supply of nectar has been exhausted, or at may have a strong effect on the degree to which an least is not yet fully renewed. Interestingly, honey- individual in search of a resource responds to bees and some species of bumblebees can detect the presence of marking pheromone. If prior expe- each other’s marking pheromone. Moreover, the rience informs an insect that a desired resource is time required for nectar replenishment appears plentiful in the local habitat, then the insect may to correspond closely to the duration of activity of almost always respond strongly to marking phero- marking pheromone. mone and, except in cases of trail-marking pher- Among insects foraging for egglaying sites, omone, leave the marked locale and search hymenopterous parasitoids that oviposit in host elsewhere. On the other hand, if prior experience 2300 M Marlatt, Charles Lester informs the insect that a desired resource is scarce Stout JC, Goulson BD (2001) The use of conspecific and inter- and the insect is highly motivated to acquire the specific scent marks by foraging bumblebees and honeybees. Anim Behav 62:183–189 resource, then the insect may respond weakly to the marking pheromone, or even ignore it, and proceed to attempt to use the depleted or occupied resource at hand. Marlatt, Charles Lester Numerous species of ants deposit marking pheromone in the vicinity of their nests. Such Charles Marlatt was born in 1863. He attended pheromone may serve not only as a home-range Kansas State University, where he received a B.S. marker that circumscribes the territory within in 1884 and an M.S. in 1886. He joined the staff at which colony members forage, but also may serve Kansas State in 1887, but in 1889 C. V. Riley hired as a signal to alien ants from other colonies that him to work in Washington, DC, as an assistant the nest itself is occupied. entomologist and artist. Riley became first assis- Some marking pheromones have been exploi tant entomologist and assistant chief of the Divi- ted for managing pest insects. For example, the sion of Entomology in 1894, a position he held European cherry fruit fly, Rhagoletis cerasi L., until 1925. It is largely through Marlatt’s persis- deposits marking pheromone on the surface of tent efforts that the Plant Quarantine Act of 1912, host fruit after laying eggs. The pheromone has important legislation that helped curb the unreg- been identified, synthesized and sprayed on cherry ulated movement of plants (and insects) into trees in Switzerland to protect cherries against fly the United States, was passed. In 1927 he was oviposition. Formulation with adjuvants helps named chief of the Bureau of Entomology, a job protect the water-soluble pheromone against the he held in addition to the position as Chief of degrading effects of rainfall. It is anticipated that the Plant Quarantine and Control Administra- enhanced knowledge of the identity of marking tion. He administered the Plant Quarantine Act pheromones will be accompanied by the increas- until 1929. Marlatt was an authority on both saw- ing use of such pheromones in pest management. flies and scale insects, and in 1900 assumed  Pheromones responsibility for the government’s collection of scales. He played an important role in identifying the homeland (northeastern China) of the San References Jose scale, and of establishing biological control in the United States through importation of a predator. Under his leadership two successful Fitgerald TD (1995) The tent caterpillars. Cornell University Press, New York eradication campaigns were conducted: the Med- Hölldobler B, Wilson EO (1990) The ants. Belknap, iterranean fruit fly in Florida and the date scale in Cambridge California. Marlatt received a number of honors Landolt P, Averill AL (1999) Fruit flies. In: Hardie J, Minks AK (eds) Pheromones of non-lepidopterous insects associ- during his career, and served as president of the ated with agricultural plants, CAB International, Oxford, Entomological Society of Washington and the United Kingdom, pp 3–25 American Association of Economic Entomolo- Nufio CR, Papaj DR (2001) Host marking behavior in phy- gists. He died on March 3, 1954. tophagous insects and parasitoids. Entomol Exp Appl 99:273–293 Prokopy RJ, Roitberg BD (2001) Joining and avoidance behavior in non-social insects. Annu Rev Entomol Reference 46:631–665 Ruzicka Z (2001) Oviposition responses of aphidophagous coccinellids to tracks of ladybird and lacewing larvae. Mallis A (1971) American entomologists. Rutgers University Eur J Entomol 98:183–188 Press, New Brunswick, NJ, 549 pp Mass Rearing of Natural Enemies M 2301 Marsh Beetles Illustrations. Although acknowledged as an expert on spiders and scorpions, he is remembered pri- Members of the family Scirtidae (order Coleoptera). marily for his excellent illustrations. He died in  Beetles Washington, DC, on January 3, 1895.

Marsh Flies Reference

Members of the family Sciomyziidae (order Diptera). Essig EO (1931) A history of entomology. The Macmillan  Flies Company, New York. 1029 pp

Marsh Treaders Masked Chafers, Cyclocephala spp. (Coleoptera: Scarabaeidae) Members of the family Hydrometridae (order The larvae of these species feed on the roots of Hemiptera). turfgrasses.  Bugs  Turfgrass Insects and Their Management

Marsupial Chewing Lice Mason Wasps

Members of the family Boopidae (order Members of the family Vespidae (order Phthiraptera). Hymenoptera).  Chewing and Sucking Lice  Wasps, Ants, Bees and Sawflies

Marsupial Lice Mass Provisioning

Members of the family Trimenoponidae (order The act of storing all the food required for the Phthiraptera). development of an immature insect at the  Chewing and Sucking Lice time of egg laying. (contrast with progressive provisioning) Marx, George Mass Rearing of Natural Enemies George Marx was born in Hess, Germany, on June 22, 1838. He is known as an illustrator of renown. JosE Roberto Postali Parra Marx completed pharmaceutical studies in Germany Esalq/USP, before moving to the United States in 1860. There, Piracicaba, Brazil he served in the Union army during the American Civil War. After working as a pharmacist in Phila- Mass rearing involves the production of millions delphia, Marx accepted a position as a natural his- of insects, with the objectives of controlling pests tory illustrator with the United States Department and supporting Integrated Pest Management of Agriculture in 1878. He received a M.D. degree in (IPM) programs. Several definitions have been 1885. In 1889 he was made chief of the Division of proposed for mass rearing, including: 2302 M Mass Rearing of Natural Enemies ·· Mass rearing is the economic production of millions agricultural pest) and the natural enemy (parasi- of beneficial insects, as if in an assembly line, in toid or predator) are conducted. Therefore, in order to produce the maximum number of fertile order to produce natural enemies, two species females, with the least number of men/hours and have to be reared, the pest and the natural enemy space, in the shortest time possible, at low cost; (Figs. 12 and 13). The potential for rearing a large ·· Insect production that can accomplish goals at an number of natural enemies increased as artificial acceptable cost/benefit ratio, in numbers exceeding diets began to be developed since the 1960s, with from 10 thousand to 1 million times the average emphasis on artificial diets for Lepidoptera, productivity of a population of native females; Coleoptera, and Diptera. ·· Systematic, automated activity conducted in inte- Considering the fundamental approaches to grated facilities, in order to produce a relatively implementing biological control, i.e., introduc- large supply of insects for distribution. tion (classical biological control), conservation (natural biological control), and multiplication Therefore, mass rearings are truly factories, in (applied biological control), mass rearings assume which cost is highly important, particularly with greater importance in the latter because, in this respect to labor, since it represents 70–80% of total case, inundative releases are made with a similar production cost. To achieve this goal, the person- effect as conventional insecticides, because they nel involved in rearing must be highly qualified in decrease pest populations more rapidly and are the field of insect rearing techniques. Often such well accepted by growers because of their similar- personnel are not readily available. Consequently, ity with conventional agrochemicals. it becomes necessary to automate the process for Although many government-sponsored pro- the production of natural enemies, especially in grams exist worldwide involving mass rearings countries where labor is more costly. of fruit flies, boll weevil and the egg parasitoid Mass rearings are started from smaller-scale Trichogramma spp., most rearings are commercial. or research rearings (conducted by one or two These are companies that sell natural enemies. people), or intermediate-sized rearings, upon Although the first mass production by a pri- which basic research about the target (often an vate company took place in 1926 (Fillmore Citrus

Mass Rearing of Natural Enemies, Figure 12 Rearing schematics of Trichogramma spp. on a factitious host. Mass Rearing of Natural Enemies M 2303

Mass Rearing of Natural Enemies, Figure 13 Relationships between insect rearings and various areas of entomology.

Protective District) in the USA, insect trading was In South America, Colombia is the industry initiated in the 1960s, with ladybugs and mantids leader, with about 20 companies, particularly in the sold to control garden and nursery pests. Begin- Cauca Valley, a region with a well-developed, techni- ning in the 1980s, the number of companies that cal agriculture. Brazil already has a similar number of supplied insects significantly increased. In 1992, companies, with emphasis on the production of 95 suppliers (twice as many as in 1977) made 106 Cotesia flavipes, which is currently released into 1.7 species available in the market; in 1997, there were million ha annually to control Diatraea saccharalis, 142 suppliers and 130 beneficial insect species for the sugarcane borer. Trichogramma spp. is released in sale. In Europe, there was also a great increase in about 200,000 ha of sugarcane, corn, and vegetables, this type of trade from the 1970s. while Trissolcus basalis is released in about 20,000 ha A principal impetus to the use of insectary of soybean to control bugs. India, the Philippines, the production of natural enemies was the successful Canary Islands, Venezuela, and Chile, among others, use of the predatory mite Phytoseiulus persimilis to are players in this industry. New Zealand and control mite pests. Today, several natural enemy Australia have a tradition in rearing natural enemies. species, produced by many companies, are avail- China, Russia, and Cuba, in turn, have government- able for the grower, especially against protected- supported rearings. At present, between 15 and 20 cultivation pests. Encarsia formosa is the most million hectares are treated worldwide with such frequently sold parasitoid on the European conti- agents. Trichogramma is still the most widely used. nent to control whiteflies in protected cultivations. More than 125 natural enemy species are As a result, today many companies worldwide sell available in the market, with hundreds of produc- biological control agents packed in a similar man- ing companies. Currently, a US$50 million annual ner as agrochemicals at market prices. market exists for biological products; even though 2304 M Mass Rearing of Natural Enemies this represents 0.5% of the agrochemicals market, ethical problems that may discredit the reputa- this figure is expected to double or triple in the tion of biological control. first part of this century. An ideal situation in mass rearing would As the number of insects produced in any occur if the insect host could be eliminated and rearing increases, problems related to facilities, the parasitoid or predator reared on artificial costs, microorganisms (contaminants), and insect (in vitro) diets. Although the Chinese demon- quality control also increase. In addition to a strated in vitro advancements to the world in necessity for automation, problems with employ- 1982 by rearing Trichogramma dendrolimi on ees may arise due to allergies, such as those caused artificial diet, the expected developments in this by moth handling, in Trichogramma rearings, for area did not occur, frustrating the scientific example. community, which had high expectations for this As previously commented, two insect species new technology. have to be reared; this requires basic knowledge Further studies are required, since the diets about the pest and the natural enemy (biology, used today are based on those developed in the ecology, biochemistry, behavior, physiology, 1960s. The search for better diets must include nutrition, etc.). Knowledge about temperature greater knowledge of the nutritional requirements requirements (in degree-days) is essential for pro- of insects, but also must take into account the duction planning. technology and equipment used in this food pro- Another problem in mass rearings relates to cessing industry for large-scale production. More the fact that the insect will be used during one refined bioassays, using microscopic, nanotechno- season of the year only. When it is not being used, logical, molecular, and biochemical and fermenta- it must be stored. These techniques, still incipi- tion techniques may provide advancements in this ent, are used with Trichogramma by inducing field. More sophisticated bioassays may improve diapause and subsequently stopping it when microorganism control in large rearings and eluci- demand for the insect arises. Liquid nitrogen has date the role of symbionts (Wolbachia, Buchnera, also been used to store eggs. Quality of the insects etc.) in insect nutrition. Together with these, it is produced is one of the greatest concerns today. essential to foster those that work in the insect- Loss of genetic variability in mass-reared insects rearing sector, training them at both the under- may lead to the loss of wild-insect traits, prevent- graduate and graduate levels. The process of using ing laboratory-reared insects from being as com- natural-enemy agents to control pests is a cultural petitive as those found in nature. There are two as well as an economic process that requires high- types of processes that may result in genetic dete- quality employees, in order to assure acceptance rioration: random and non-random or adaptive by agricultural producers. processes. Among these deterioration mechanisms, genetic drift (or founder effect), inbreeding, and selection are the most relevant. Therefore, References monitoring the production, the process, and the product over successive laboratory genera- Chambers DL (1977) Quality control in mass rearing. Annu tions is essential for the production of laboratory Rev Entomol 22:289–308 Cohen AC (2004) Insect diets: science and technology. CRC, insects that are as competitive as those that occur Boca Raton, FL, 324 pp in nature. The International Organization for Etzel LK, Legner EF (1999) Culture and colonization, Biological Control has already established stan- pp 125–197. In Bellows TS, Fisher TW (eds) Handbook of biological control: principles and applications of bio- dards that take into account biological charac- logical control. Academic, San Diego, CA, 1,046 pp teristics and molecular analyses, which must be Finney GL, Fisher TW (1964) Culture of entomophagous followed up and regulated by law to prevent insects and their host, pp 328–355. In: DeBach P, Matheson, Robert M 2305 Schlinger EI (eds) Biological control of insect pests and Catalogue of the known Coleoptera of New Guinea, weeds. Chapman & Hall, London, 844 pp 1888). Later in life he suffered from nervous com- King EG, Leppla NC (1984) Advances and challenges in insect rearing. USDA-ARS, New Orleans, LA, 306 pp plaints and his eyesight became very poor. He died van Lenteren JC (Ed) (2003) Quality control and production in a cab accident on July 23, 1912. of biological control agents: theory and testing procedures. CABI Publishing, Cambridge, 327 pp Leppla NC, King EG (1996) The role of parasitoid and preda- Reference tor production in technology transfer of field crop biological control. Entomophaga 41:343–360 Leppla NC, Adams F (1987) Insect mass-rearing technology, Lea AM (1929) George Masters. Vic Nat 45:164–167 principles and applications, 20 pp Parra JRP, Botelho PSM, Corrêa-Ferreira BS, Bento JMS (2002) Controle biológico no Brasil: parasitóides e pre- dadores. Manole, São Paulo, Brazil, 609 pp Mastotermitidae Singh P, Moore RF (eds) (1985) Handbook of insect rearing. Elsevier, Amsterdam, 496 pp A family of termites (order Isoptera) presently containing only one species, Giant Northern Aus- tralia termite. Masters, George  Termites

George Hangay Narrabeen, NSW, Australia Maternally Inherited

George Masters was born in July 1837 in Kent, Eng- Characters that are transmitted primarily by cyto- land. Not much is known of his early years, except plasmic genetic factors, including mitochondria, that he was a horticulturist and when he migrated to viruses, etc., derived from the maternal parent. Australia, he lived in Tasmania. Later, the amateur This is also known as cytoplasmic inheritance or entomologist A.W. Howitt in Melbourne employed extranuclear heredity. him. Consequently, many of the specimens which he collected are now in the Howitt Collection in the Museum of Victoria (Melbourne). In 1864 he Matheson, Robert became Assistant Curator and Collector of the Aus- tralian Museum in Sydney. In 1874 William John Robert Matheson was born at West River, Nova Macleay employed him as curator of his zoological Scotia, Canada, on December 20, 1881. He received collections. Masters remained in this position even all his degrees in entomology at Cornell Univer- after the collections (by then Museum) were trans- sity, attaining his Ph.D. in 1911. He worked for ferred to the University of Sydney. He was a very South Dakota State University, Nova Scotia good field worker, not only with insects but also with Agricultural College, and Cornell as a medical most vertebrate animals, especially birds. It was said entomologist. His expertise was on mosquitoes that at time more than half of the natural history and malaria, and he helped in the elimination of specimens in the Australian Museum were of his malaria from the east-central United States. He taking. As Curator of the Macleay Collections he trained many students in medical entomology, participated in the “Chevert” New Guinea expedi- and published “Handbook of mosquitoes of tion. Apart from his collecting and curating activi- North America” (1929), “Medical entomology” ties, his Coleoptera catalogues are his main (1932), and “Entomology for introductory contributions to Australian entomology (Catalogue courses” (1944). He died on December 14, 1958, at of the described Coleoptera of Australia, 1871–1886; Princeton, New Jersey. 2306 M Mating Disruption

Reference Cardo

Mallis A (1971) American entomologists. Rutgers University Press, New Brunswick, NJ, 549 pp Stipes Palpifer

Mating Disruption Lacinia Subgalea

Use of pheromones to interfere with mating Galea and reproduction, resulting in pest population suppression.

Palpus Matsumura, Shonen

Shonen Matsumura was born on March 5, 1872, and is considered to be the “father of Japanese entomol- Maxilla, Figure 14 External lateral aspect of the ogy.” He was interested in insects from an early age, left maxilla in an adult grasshopper, showing and studied entomology at Sapporo Agricultural Col- some major elements. lege (now Hokkaido University). He was appointed to the faculty there in 1896 and in 1898 published Maxillary Palp (or palpus; pl., “Nippon Konchugaku” (Entomology of Japan). In maxillary palpi) 1899 he moved to Europe to advance his knowledge and in 1902 returned to Japan as professor. Much of A one- to seven-jointed sensory appendage (pair his work was on Lepidoptera and Hemiptera, but of appendages) on the insect maxilla (Fig. 15). he published on most orders. He authored about  Mouthparts of Hexapods 240 papers and 35 books during his career. The illustrated 12-volume “Thousand insects of Japan” pub- Maximum Parsimony Methods lished between 1904 and 1921 was especially noteworthy. He also accumulated Japan’s largest Taxonomic methods that focus on the character val- insect collection. He died on November 7, 1960. ues observed and minimizing the number of changes in character state between species over the tree, making the assumption that there have been approx- Reference imately constant rates of change. The changes at each node in the tree are inferred to be those that require Herman LH (2001) Matsumura, Shonen. Bullet Am Mus Nat the least number of changes to give each of the two His 265:108–109 character states of the immediate descendants.  Phylogenetics Maxilla May Beetles A pair of mouthparts located posterior (ventral) to the mandibles, and bearing sensory structures Members of the subfamily Melolonthinae, family or palpi (Fig. 14). Scarabaeidae (order Coleoptera).  Maxillary Palp  Beetles  Mouthparts of Hexapods  Turfgrass Insects and their Management Mayflies (Ephemeroptera) M 2307

Vertex Flagellum

Antenna Frons Pedicel Scape

Median ocellus

Face

Anterior tentorior pit Basimandibular sclerite Frontoclypeal suture Mandible Clypeus Clypeolabral suture Labrum Maxillary palpus Maxilla

Labial palpus

Maxillary Palp (or palpus; pl., maxillary palpi), Figure 15 Front view of the head of an adult grasshopper, showing some major elements.

Mayflies (Ephemeroptera) will molt to the imago or adult stage. The angler or fly fisherman terms the subimago the “dun” and Boris Kondratieff the imago the “spinner.” The imago stage is ready Colorado State University, Fort Collins, CO, USA to reproduce and disperse, the only biological functions of this stage. Some mayflies remain as a The Ephemeroptera or mayflies, are a primitive subimago and still can reproduce. In fact some order of aquatic insects that, as adults, are easily subimagoes have vestigial or nonfunctional legs, distinguished by the presence of two pairs of and can only fly and mate, then die! Adult mayflies membranous wings, the front wings larger and often form enormous nuptial flights, during which triangular in shape, with the hind wings much mating takes place. Swarming behavior can take smaller (and sometimes absent). The antennae place over the water, or sometimes remote from a are bristle-like, and two or three long segmented body of water, and at various times of the day from caudal filaments or “tails” extend at the end of the dawn to dusk, or at night. The eyes of the male abdomen. Additionally, adults are usually found imago are modified, apparently for better acuity at or near bodies of water (Fig. 16). for aerial mating. Mated females return to the Most mayfly adults have two winged stages, stream or pond to oviposit. Eggs of most mayflies one termed the subimago and the other the imago. are modified for different aquatic environments, The subimago, the winged stage after the molt usually with specialized attachment structures. from the nymphal stage (many entomologists pre- Mayfly immatures or nymphs can be distin- fer the term larvae for all immature insects) after a guished from other aquatic insects with hemime- period of time that varies from an hour to days, tabolous or incomplete metamorphosis by the 2308 M Mayflies (Ephemeroptera)

Antenna Ocellus Compound eye Femur Pronotum Trochanter

Tibia

Fused basal tarsal segment

Tarsus

Antenna Clypeus Labrum Mandible Maxilla Pronotum Labial palpus Mesonotum Metanotum Forewing pad Coxa Trochanter Pretarsus Hindwing pad Femur Gills (paired) Tibia

Tarsus Pretarsus

Median caudal filament Cercus

Cercus Median caudal filament

Mayflies (Ephemeroptera), Figure 16 Diagram of mayflies: adult (right) and immature (left). Note that each is divided into dorsal (left portion) and ventral (right portion) perspectives.

presence of two or three caudal filaments or tails at and lentic (standing waters, ponds, lakes, reser- the end of the abdomen, and usually one claw on voirs). However, the greatest diversity of mayflies each leg (absent in Behningiidae). Additionally, is found in lotic habitats, especially those of higher gills are attached to various segments on the side of elevations. Some species of Baetidae can be found the abdomen, either as flattened plates or filaments. in tide pools and alkaline desert pools. Some Gills can also occur on the base of the legs or groups such as members of the family Heptageni- mouthparts. The body length can range from 2 to idae (flatheaded mayflies) have flattened bodies, almost 35 mm, not including the caudal filaments. and are adapted to cling to instream rocks or other Immature mayflies occur in many different firm substrates in fast-flowing streams, whereas habitats, both lotic (flowing waters, streams, rivers) others such as members of the Baetidae (small Mayflies (Ephemeroptera) M 2309 minnow mayflies), Ameletidae (ameletid minnow Family: Ameletopsidae mayflies), and Siphlonuridae (primitive minnow Family: Ametropodidae mayflies) are well adapted for swimming. Mem- Family: Arthropleidae bers of the Ephemeridae (common burrower Family: Baetidae mayflies) are burrowers in soft sediments of lakes, Family: Coloburiscidae ponds and large rivers. Family: Dipteromimidae The higher classification of the Ephemeroptera Family: Heptageniidae is in part provisional. Researchers have presented Family: Isonychiidae much significant work towards a phylogenetic Family: Metretopodidae classification of the order. Currently, about 631 Family: Nesameletidae species are recognized from North America in Family: Oligoneuriidae twenty-three families of the forty-one extant fami- Family: Pseudironidae lies known in the world. A comprehensive index to Family: Rallidentidae North American mayfly species is provided at the Family: Siphlaenigmatidae website http://www.entm.purdue.edu/entomology Family: Siphlonuridae /research/mayfly/mayfly.html. Family: Siphluriscidae Order: Ephemeroptera The majority of mayflies reside in running Suborder: Carapacea waters, but unlike another group of aquatic Family: Baetiscidae insects, the stoneflies (Plecoptera), they attain Family: Prosopistomatidae maximum diversity in warm lotic habitats. Most Suborder: Furcatergalia mayfly nymphs are collector-gatherers or scrap- Family: Austremerellidae ers. A few species are specialized filter-feeders Family: Behningiidae or carnivores. Shredders are very poorly repre- Family: Caenidae sented. Most mayflies of temperate regions have Family: Dicercomyzidae a one-year life cycle (univoltine), the vast major- Family: Ephemerellidae ity of which is spent as an aquatic nymph. In fact, Family: Ephemeridae it is the ephemeral nature of the aerial adult stage Family: Ephemerythidae that is responsible for the Greek name of the Family: Euthyplociidae order. Adults live from one hour to several days, Family: Ichthybotidae depending on weather conditions and the spe- Family: Leptohyphidae cies in question. The gills of mayflies are highly Family: Leptophlebiidae variable. In most species gills are present only on Family: Machadorythidae the abdomen. Gills often occur on the first seven Family: Melanemerellidae abdominal segments, although one or more pairs Family: Neoephemeridae may be absent, depending on the species. A few Family: Oniscigastridae species also possess gills on the legs and head. Family: Palingeniidae Most mayflies possess three caudal filaments; a Family: Polymitarcyidae few have two caudal filaments. Microhabitat Family: Potamanthidae occurrence is reflected more distinctly in the Family: Teloganodidae body form of nymphs than in that of any other Family: Tricorythidae order. Some species have a fusiform body shape Family: Vietnamellidae that enables them to move about on the tops of Suborder: Pisciforma rocks in rapid water, whereas others are flattened Family: Acanthametropodidae dorsoventrally to hug rock surfaces. Other Family: Ameletidae groups construct burrows in the substrate with 2310 M Mayflies (Ephemeroptera) their mandibles, and use their gills to create Family Caenidae (Small Squaregill respiratory and feeding currents. Yet others are Mayflies) adapted for creeping and climbing among accumulations of organic material, or in silty back- The small nymphs are usually found in standing waters, or in plant beds. water, and are often abundant in ponds, lakes and A brief synopsis of the more common fami- wetlands. They are considered sprawlers in silty bot- lies is provided. toms in the zones of rooted vegetation. Nymphs feed usually on decaying plant material. Some species have several generations per year, especially in the Family Ameletidae (Ameletid more southern areas. Caenis is the common genus. Minnow Mayflies)

The nymphs are usually found in small fast- Family Ephemeridae (Common flowing streams among rocks. Some species are Burrower Mayflies) confined to very small brooks, often congregating in pool areas. Nymphs are strong swimmers, but Nymphs of this family construct a U-shaped tunnel often seek quieter waters. Nymphs are scrapers, in bottom sediments with openings at both ends. using the pectinate comb of spines (the diatom They use their feathery gills to maintain a current rake) on part of the mouthparts to feed on per- within the burrows for obtaining dissolved oxygen. iphyton or algae. There is usually only one genera- Additionally, they filter out small particles of organic tion per year. Some species of Ameletus apparently material brought in by the current. Some species are parthenogenetic, reproducing without the ingest sediments mixed with organic material. The presence of males. nymphs are often abundant in lakes, ponds, large rivers, and reservoirs. Mass emergence of the large-sized adults, especially in the Mississippi River Valley Family Baetidae (Small Minnow region, attracts attention, and at times is considered a Mayflies) nuisance. Depending on location, species of common burrowers complete their life cycle in 1–2 years. Nymphs are found in a wide variety of aquatic The two genera, Ephemera and Hexagenia are wide- habitats. They may be the only mayflies present spread throughout North America. in extreme environments such as high-elevation streams, the sources of springs, or mildly polluted waters. They are considered good swimmers, Family Ephemerellidae (Spiny darting in short spurts from one spot to another. Crawler Mayflies) Often they are, in terms of numbers, the most important mayflies of many North American Nymphs occur in almost all types of flowing water. streams. The species ofBaetis collectively occupy Some species occur in steep gradient segments of an extremely wide range of flowing water habi- streams in high elevations to silty microhabitats in tats. Callibaetis is primarily a standing water lower elevations. Some groups also are found in genus, some species of which occur in the back- standing waters of lakes and wetlands. Nymphs waters or quiet margins of running waters. Most crawl about and are well camouflaged. Most spe- members of the family are collector-gatherers or cies are considered collector-gatherers or scrapers, scrapers. Most of the species found in flowing but some Drunella species have been reported to water habitats apparently have two generations be partially predaceous. Nymphs have the peculiar per year, others only one. defensive behavior of raising its three tails in a Mayflies (Ephemeroptera) M 2311 posture called the “scorpion posture.” Most species gills from silt deposition. Members of this genus have one generation per year. are slow-moving sprawlers that feed on sedimen- tary organic material. The genusTricorythodes is a common North American genus. Family Heptageniidae (Flatheaded Mayflies) Family Leptophlebiidae Heptageniids are perhaps the most typical of all (Pronggilled Mayflies) mayfly families found in flowing water. The nymphs are flattened and generally adapted to life in high- The poor-swimming nymphs of this family are gradient mountain streams. Most species are commonly found in shallow streams of all sizes. restricted to running waters; a few also inhabit Some groups are associated with accumulations wave-swept shores of lakes. Species of Heptagenia of leaves and debris in overflow areas or flood generally occupy warmer and siltier running waters plains. Nymphs of some species are filter-feeders than other genera such as Epeorus, and Rhithrogena in rapid sections of large silty rivers of western are restricted usually to cool, fast mountain streams. North America, while others feed on accumu- Most heptageniids are scrapers, removing attached lated decomposing plant material or scrape algae microscopic plants and other particles from rock of various substrates. Nymphs of some species surfaces; a few are collector-gathers and predators. are known for their migratory habits of moving The numerous North American species have one in spring from streams to pools associated with to two generations per year. the floodplain. One to two generations per year are common with most species. Emergence of some species occurs as early as February. Family Isonychiidae (Brushlegged Mayflies) Family Siphlonuridae (Primitive Nymphs of this family can be abundant in a vari- Minnow Mayflies) ety of flowing waters, and especially abundant in shallow riffle reaches of streams of eastern North Nymphs occur both in lotic and lentic habitats, America. Nymphs are strong swimmers, and use usually associated with accumulations of silt or hair fringes on the forelegs for filtering organic the presence of vegetation. Nymphs often congre- particles from the water column. Most species gate in pools or overflow areas of streams. Nymphs have one generation a year, but in more southern are good swimmers but prefer quieter areas of areas they may have two generations per year. streams or edges of pools and ponds. They feed on The genus Isonychia occurs over most of North organic debris, but also engulf small aquatic America, and adults are easily distinguished by organisms. Most species have only one generation their reddish coloration. per year. The genus Siphlonurus is widespread throughout North America (Fig. 16). Family Leptohyphidae (Little Stout Crawler Mayflies) References

Nymphs are often associated with beds of aquatic Edmunds GF Jr, Jensen SL, Berner L (1976) The mayflies of plants or other habitats where silt accumulates. North and Central America. University of Minnesota The opercular gill plates protect the remaining Press, Minneapolis, MN, 330 pp 2312 M McDunnough, James Halliday Jacobus LM, McCafferty WP (2006) Reevaluation of the phy- Reference logeny of the Ephemeroptera Infraorder Pannota (Fur- catergalia), with adjustments to higher classification. Trans Am Entomol Soc 132:81–90 Mallis A (1971) American entomologists. Rutgers University McCafferty WP (1991) Toward a phylogenetic classification Press, New Brunswick, NJ, 549 pp of the Ephemeroptera (Insecta): a commentary on systematics. Ann Entomol Soc Am 84:343–360 McCafferty WP (1996) The Ephemeroptera species of North McGlashan, Charles Fayette America and index to their complete nomenclature. Trans Am Entomol Soc 122:1–54 McCafferty WP (2004) Higher classification of the burrowing Charles McGlashen was born August 12, 1847. mayflies (Ephemeroptera: Scapphodonta). Entomol News After obtaining seminary education in California 115:84–92 and Massachusetts he became a high school prin- McCafferty WP, Wang TQ (2000) Phylogenetic systematics of cipal in Placerville, California, and also was an the major lineages of Pannote Mayflies (Ephemeroptera: Pannota). Trans Am Entomol Soc 126:9–101 accomplished lawyer, editor, and astronomer. He is Sun L, Sabo A, Meyer MC, Randolph RP, Jacobus LM, also remembered, however, as an ardent amateur McCafferty WP, Ferris VR (2006) Tests of current entomologist. He contributed numerous speci- hypotheses of mayfly (Ephemeroptera) phylogeny using molecular (18x rDNA) data. Ann Entomol Soc mens to Henry Edwards’ Lepidoptera studies and Am 99:241–252 collection and developed an all-glass display case Zhou CF, Peters JG (2003) The nymph ofSiphluriscus chinen- for his moths and butterflies. Interestingly, he also sis and additional imaginal description: a living mayfly established a butterfly farm at Truckee, California, with Jurasssic origins (Siphluriscidae new family: Ephemeroptera). Fla Entomol 86:345–352 offered a correspondence course for amateur entomologists, and started a short-lived monthly mag- McDunnough, James Halliday azine, “The butterfly farmer.” He died in 1931.

James McDunnough was born at Toronto, Canada, Reference on May 10, 1877, and studied music before switch- ing to entomology and becoming an authority on Essig EO (1931) A history of entomology. The Macmillan the systematics of Lepidoptera and Ephemeroptera. Company, New York, 1029 pp His zoological education commenced at Kaiser Wilhelm Institute in Berlin, Germany, followed by a McPhail Trap M.S. from Queen’s University in Kingston, Ontario, Canada, and then back to Kaiser Wilhelm for a The McPhail trap is a glass or plastic liquid- doctorate. From 1910 to 1919 he worked as a cura- containing trap that uses protein solutions as bait. tor at William Barnes’ private museum in Decatur, Ammonia given off by the trap is attractive to fruit Illinois. In 1919 he left to head the Division of Sys- flies, which enter the trap from below. As they tematic Entomology at the Canadian National Col- instinctively attempt to move upward, they are lection in Ottawa. He served in this capacity for 28 restrained from escaping by the solid top. years, accumulating one of the finest collections in  Traps for Capturing Insects North America. McDunnough published over 200 papers on Lepidoptera, 38 on Ephemeroptera, and several on other orders. Important works include Meadow and Coneheaded “Check list of the Lepidoptera of Canada and the Grasshoppers United States of America,” and “Saturniidae of North America.” Over the course of his career he A subfamily (Conocephalinae) of katydids in the named about 1,500 species. McDunnough died at order Orthoptera: Tettigoniidae. Halifax, Nova Scotia, on February 23, 1962.  Grasshoppers, Katydids and Crickets Mechanical Protection of Humans from Arthropod Attacks and Bites M 2313 Mealworms Mechanical Protection of Humans from Arthropod Attacks and Bites Larvae of the family Tenebrionidae are sometimes called mealworms, and infest grain and grain Igor Uspensky products. The Hebrew University of Jerusalem, Jerusalem,  Stored Grain and Flour Insects Israel

In addition to chemical repellents for arthropod Mealybugs vectors or annoyers, human protection from their attacks and bites can be provided by numerous Members of the family Pseudococcidae, super- mechanical methods. Mechanical protection is family Coccoidae (order Hemiptera). based on the creation of a barrier that prevents the  Scale Insects and Mealybugs penetration by arthropods to the target humans. Bugs Such a barrier can protect either a group of people or an individual person.

Mean-Variance Model Environmental Design

A model, generally a regression model, which A very simple and effective technique to protect a predicts the variance of a sample from an esti- human locality from malarial mosquitoes is so-called mate of the sample mean. Such models can “zooprophylaxis.” This technique is based on rational characterize dispersion over a large range of planning of localities. The technique was tested at the population densities and are commonly used in end of the 1930s in several areas of the then U.S.S.R. developing sampling plans. Common examples and was later successfully applied in antimalarial are Taylor’s power law and Iwao’s patchiness campaigns in rural areas with developed animal hus- regression. bandry. Thus, if a cattle-ranch is located between a  Sampling Arthropods mosquito breeding site(s) and a village, mosquitoes flying towards the village attack the cattle and only a few specimens reach the human dwellings. The dis- Measuring Worm Moths tance between a large ranch and a village should be from 200–500 m, and between an individual cattle Members of the family Geometridae (order stall and the nearest dwelling, about 25–35 m. To Lepidoptera). protect a human locality from flies which develop on  Geometer Moths cattle ranches, it is recommended to separate these  Butterflies and Moths two sites by creating a brush and tree belt between them of not less than 100 m in width. Several measures should be taken to protect Mechanical Control dwellings from insect penetration. All windows should be fitted with screens of metal netting. The Control techniques that are based on the opera- mesh size to prevent penetration of mosquitoes tion of machinery or manual operations to and most flies is 1.5–2 mm, but in the cases of such destroy insects. Examples of mechanical control small insects as midges or sandflies the mesh techniques include vacuum machines and black- should be as fine as 0.75 mm. Also, it is desirable to light traps. construct a porch before the entrance into the 2314 M Mechanical Protection of Humans from Arthropod Attacks and Bites house, which should be fitted with appropriate role by the suppressive effect on mosquito popula- screen and the entrance should be closed with a tions and their capacity as malaria vectors. Though net fixed at the upper jamb and freely hanging the efficacy of impregnated bed nets differs for dif- down to the floor. Entrances to the animal housing ferent mosquito species and in different areas, they also should be closed with screens. have become an important tool in human protection from mosquitoes and malaria. An important factor to remember with nets for both head veils and Protective Clothing and Bed Nets bed nets is the necessity of good ventilation, a condition not always fulfilled. The easiest method of individual protection is Development of pyrethroid resistance in mos- proper clothing to create a barrier between attacking quito vectors may threaten the sustainability of arthropods and the human body. In general, the impregnated bed nets, though the real impact of more the human body is covered by clothing, the this phenomenon on the efficacy of bed nets is lower the probability of arthropod bites. A head veil controversial. Meanwhile, various combinations of made from a single- or double-layered net (impreg- pyrethroid and non-pyrethroid insecticides for nated by repellents, if possible) put over or under a impregnation of bed nets have been tested. However, head-dress, as well as a hood on a shirt or a jacket, operational difficulties are more critical for effective provide additional protection from insect bites. application of impregnated bed nets, e.g., the neces- A veil made from a fine mesh net covering the whole sity for regular retreatment of bed nets to maintain head and tightly fixed to clothing (similar to that their high efficacy against mosquitoes. Most users used by beekeepers) provides nearly complete pro- do not impregnate their nets in time and properly, tection from insect bites without any necessity of and the limited impact of such bed nets on mosquito repellents (Fig. 17). There are many things specific to population decreases the motivation of people to various groups of arthropods that must be taken use this technique. This stimulated the development into account to provide a better barrier between of “long-lasting insecticidal wash-resistant mosquito them and the human skin. Blackflies that are active net” which should maintain its activity for 3–5 years, during the day prefer darker clothing rather than the average life expectancy of the net. lighter fabric when selecting a landing site. To bite, blackflies must penetrate under the clothing and contact the body, using any minute openings for this Arthropod Behavior and purpose. Thin and delicate materials only partly Protection protect from bites by horse flies or stable flies, whereas mosquitoes can pierce even fabrics with Protection from the bites of ixodid ticks is based rough texture using their long proboscis (Fig. 19). on the specificity of their behavior. After adhering For protection of people from night-biting arthro- to human clothes, ticks usually move upwards, pods during sleep, bed nets have been used for many trying to penetrate under the clothes and to con- centuries both inside and outside human dwellings. tact the body. To make tick penetration onto the They can be of different shape and made from vari- body more difficult, people should seal all possible ous materials. If a bed net is properly organized, it routes for tick penetration under the clothes. Trou- may provide nearly complete protection of the per- ser legs should be tucked into boots or socks, the son using it. Correct maintenance of the bed net shirt into trousers, and the head should be covered during the day prevents it from being used by mos- by a hood. Some researchers have recommended quitoes as a resting site (Fig. 18). The development making two repellent strips, about 2 cm in width of bed nets impregnated with pyrethroid insecti- and 5–7 cm from each other, around each trouser cides has supplemented their exclusively protective leg above the knees. Such strips prevent ticks, most Mechanical Protection of Humans from Arthropod Attacks and Bites M 2315 of which adhere to the clothes at a lower level, protection from both ticks and insects. Two shirts, from moving upwards. Another pair of strips may which are worn one over the other, are the key part be made around the collar to protect the head. of this suit. The inner shirt is made from a thick- People at risk of tick attack must regularly carry ened wide-mesh cotton netting, whereas the outer out self- and/or cross-inspections followed by tick shirt is made from a fine-mesh net material. The removal. The frequency of such inspections outer shirt has elastic cuffs and a hood with an elas- depends on the tick abundance; they should be tic band border. The suit also includes wide trousers carried out at least several times per day, but in with elastic cuffs and a belt, both made from a dura- heavily infested areas, every hour or half hour. ble material. A mosquito able to penetrate through Many areas are populated by both ticks and the material of the outer shirt cannot reach the blood-feeding insects. The necessity of simultane- human body with its proboscis; the thickness of the ous protection from both groups of arthropods has fabric of the inner shirt net material is about 2 mm, always been on the agenda. A protective suit devel- which is close to the maximal length of the probos- oped by Russian scientists provides mechanical cis. Other bloodsucking insects have a shorter proboscis. At the same time, the mesh size of the outer shirt is smaller than the size of the scutum of nymphal ticks. The net shirts made from cotton provide good ventilation so that the suit may be used during hot summer weather even by workers such as lumbermen. Depending on conditions, the suit may be used either for combined protection, or only as an anti-insect or anti-tick device. In the first case, the shirt has no hood but is supplemented by a head net impregnated with repellents. In the second case, only the outer shirt with the hood is used (Fig. 20).

Mechanical Protection of Humans from Arthropod Human Motivation Attacks and Bites, Figure 17 Head veils of different types: (a) Head is partly protected; (b) Head is An important consideration in using different completely protected. protective techniques is human motivation. The

Mechanical Protection of Humans from Arthropod Attacks and Bites, Figure 18 Bed nets of different types: (a) Rectangular bed net inside human dwelling; (b) Conical bed nets outside dwelling. 2316 M Mechanical Protection of Humans from Arthropod Attacks and Bites Mosquito Horse fly endemic but the tick abundance is moderate, people Black fly are reluctant to apply any protective measures creating even minor discomfort. Another aspect concerning human motivation is connected with the purpose for which humans are in areas where they Body skin may be attacked and bitten by arthropods. If they Mechanical Protection of Humans from Arthropod work in such an area and have been well instructed, Attacks and Bites, Figure 19 Thickness of two they usually protect themselves properly. However, net shirts compared with proboscis length of people at leisure, even when specially instructed, do bloodsucking insects from different families. not like any discomfort and use protective measures rather unwillingly, if at all. In some cases, when people are vaccinated against a disease endemic in the area they are habiting, they believe the use of other protective measures is unnecessary. However, the area may also be endemic for other diseases, which is quite realistic since new cases of mixed infection have been discovered. From all these data presented above, one can see that the problem of human protection from arthropod attacks and bites has two aspects: the development of more efficient and comfortable techniques of protection, as well as the necessity of convincing people to apply them.  Repellents of Biting Flies  Mosquitoes  Ticks

References

Asidi AN, N’Guessan R, Hutchinson RA, Traoré-Lamizana M, Carnevale P, Curtis CF (2004) Experimental hut com- parisons of nets treated with carbamate or pyrethroid insecticides, washed or unwashed, against pyrethroid- Mechanical Protection of Humans from Arthropod resistant mosquitoes. Med Vet Entomol 18:134–140 Attacks and Bites, Figure 20 Combined protective Curtis CF (1992) Personal protection methods against vec- suit consisting of two shirts made from net tors of disease. Rev Med Vet Entomol 80:543–553 material of different meshes (man shows the inner Guillet P, N’Guessan R, Darriet F, Traoré-Lamizana M, Chandre F, Carnevale P (2001) Combined pyrethroid shirt). and carbamate “two-in-one” treated mosquito nets: field efficacy against pyrethroid-resistant Anopheles latter depends to a higher degree on the level of dis- gambiae and Culex quinquefasciatus. Med Vet Entomol 15:105–112 comfort than on the real danger created by Harwood RF, James MT (1979) Entomology in Human and arthropods. In areas where the abundance of blood- Animal Health (7th ed). Macmillan Publishing, New sucking insects is enormous, people have willingly York, NY Marquardt WC (1996) Introduction to arthropods and vec- applied protective clothes even if the insects are not tors. In: Beaty BJ, Marquardt WC (Eds) The Biology of vectors but just annoyers. On the other hand, even Disease Vectors. University Press of Colorado, Niwot, in areas where severe tick-borne diseases are CO, pp 1–24 Mediterranean Burnet Moths (Lepidoptera: Heterogynidae) M 2317 Sutcliffe JF (2000) Prevention and control of arthropodborne Median diseases. In: Eldridge BF, Edman JD (Eds) Medical Entomology. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 565–620. Referring to the middle, or near the middle. Uspensky I (1999) Ticks as the main target of human tick-  Wings of Insects borne disease control: Russian practical experience and its lessons. J Vector Ecol 24:40–53 Median Furrow Mechanical Transmission The furrow between the radius and media. In some Transmission of an arthropod transmitted disease Hemiptera, the indentation separating the embo- wherein the causal organism is transmitted more- lium from the remainder of the corium. or-less incidentally. The disease-causing organism  Wings of Insects in not well adapted to the vector, does not multiply in the vector, and usually is not consumed. Flies and cockroaches often are implicated in this process. Mediocubital  Cyclo-Propagative Transmission  Cyclo-Developmental Transmission Referring to the media and cubitus veins of the  Propagative Transmission insect wing.  Wings of Insects Meconium

Wastes accumulated during the pupal stage Mediterranean Burnet Moths and excreted by the adult insect shortly after (Lepidoptera: Heterogynidae) emergence. John B. Heppner Florida State Collection of Arthropods, Mecoptera Gainesville, FL, USA

An order of insects. They commonly are known as Mediterranean burnet moths, family Heterogyni- scorpionflies and hangingflies. dae, include only seven species, with three species  Scorpionflies from the Mediterranean region of southern Europe and northern Africa (genus Heterogynis) and four Media species from South Africa (genus Janseola). The family is in the superfamily Zygaenoidea in the The fourth longitudinal wing vein, extending from section Tineina, subsection Sesiina, of the division the base to at least the middle of the wing. It usually Ditrysia. Adults small (9 to 29 mm wingspan), is branched, but not with more than four branches. with head rough-scaled; haustellum absent or vestigial; labial palpi reduced, 3-segmented; maxillary palpi absent; antennae bipectinate. Wings Media Workers rather rounded. Maculation mostly gray, with similar hindwings. Adults are diurnal, but females are Among ants with polymorphic worker castes, the apterous and larviform. Many of the species intermediate size workers. (contrast with major resemble bagworms and were originally described and minor workers) as Psychidae. Larvae, upon hatching inside the 2318 M Mediterranean Flannel Moths (Lepidoptera: Somabrachyidae) female cocoon, feed on the dead female and then African species are unknown). Larvae are leaf become external leaf feeders. Host plants are in feeders (eggs laid on leaves, not in the female Leguminosae. cocoon), somewhat slug-like, with concealed head. Hosts are grasses (Gramineae) and Compositae. References References Dalla Torre KW Von, Strand E (1923) Heterogynidae. In Lepidopterorum Catalogus, 28: 1–14 W Junk Berlin Epstein ME (1996) Somabrachyidae Hampson, 1920, Daniel F, Dierl W (1966) Zur biologie und anatomie von Het- pp 85–86. In Revision and phylogeny of the limacodid- erogynis penella (Hbn.) (Lep.) Zoologischer Anzeiger group families, with evolutionary studies on slug cater- 176: 449–464 pillars (Lepidoptera: Zygaenoidea). Smithsonian Con- Freina JJ de, Witt TJ (1990) Familie Heterogynidae Herrich- tributions to Zoology 582: 1–102 Schaffer 1846. In Die Bombyces und Sphinges der Freina JJ de, Witt TJ 1990. Familie Megalopygidae Herrich- Westpalaearktis 2: 74–80 pl. 10 Forschung and Wis- Schäffer 1855 (=Somabrachyidae Hampson 1920). In: senchaft Verlag, Munich Die Bombyces und Sphinges der Westpalaearktis, Guenin R (1997) Heterogynidae – Federwidderchen (Mot- 2:48–50, pl 6. Forschung & Wissenschaft Verlag, Munich tenspinner) In Schmetterlinge und ihre Lebensräume: Geertsema H (1998) Studies on African zygaenoid moths Arten - Gefährdung-Schutz. Schweiz und angrenzen- (Lepidoptera: Zygaenoidea) (Somabrachyidae). S Afr J den Gebiete, Lebensräume: 309–312 pl. 10. Pro Natura- Zool 33:210–225 (1998); Afr Zool 35:251–259 (2000) Schweizerische Bund Fuer Naturschutz Basel Powell H (1911) Notes sur les Somabrachys des environs de Sukareva IL (1978) Heterogynidae. In Identification keys to Géryville (Sud-Oranais). In Études de Lépidoptéres Com- the insects of European Russia, 4 Lepidoptera 1: 138–140 parée, 5: 227–301, pl 84–85, A-D. C. Oberthür, Rennes Academic Nauk (in Russian) St. Petersburg Powell H (1916–17) Megalopygidae. In: C. Oberthür, Faune des Lépidoptères de Barbarie (Partie II). In Études de Lépidoptères Comparée, 12: 376–428 (1916); pl. 529–531 (1917). C. Oberthür, Rennes. [all Somabrachyidae] Mediterranean Flannel Moths (Lepidoptera: Somabrachyidae) Mediterranean Flour Moth, John B. Heppner “Ephestia kuhniella Zeller Florida State Collection of Arthropods, (Lepidoptera: Pyralidae)” Gainesville, FL, USA This is a minor pest of stored grain. Mediterranean flannel moths, family Somabrachy-  Stored Grain and Flour Insects idae, include only five species, with three species from Southern Europe and North Africa (genus Somabrachys) and two species from South Africa Mediterranean Fruit Fly, Ceratitis (genus Psycharium). The family is in the super- capitata (Wiedemann) (Diptera: family Sesioidea in the section Tineina, subsection Tephritidae) Sesiina, of the division Ditrysia. Sometimes the group is included in Megalopygidae. Adults small Nikos T. Papadopoulos (18–22 mm wingspan), with head scaling average; Aristotle University of Thessaloniki, Thessaloniki, haustellum absent; labial palpi absent; maxillary Greece palpi absent; antennae bipectinate. Wings very broadly rounded and body robust. Maculation The Mediterranean fruit fly (medfly) belongs to gray or brown on wing margins, with most of the tribe Ceratitidini of the sub-family Dacinae, wings hyaline. Adults are diurnal, but females are and is the most well-known of the 65 species of larviform and wingless (females of the South the genus Ceratitis. It is highly polyphagous, very Mediterranean Fruit Fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) M 2319 widespread (both in tropical and temperate areas), appearance, owing to the yellow, brown, black, and it is considered one of the most important white and whitish stripes on its thorax, abdomen pests for world fruit production. and wings. Compound eyes, which are iridescent royal purple to blue-greenish, occupy most of the head, which is yellowish in color. The antennae Origin and Geographical have a general brown color and several small Distribution black setae. The two base segments of the antennae are red-brown, while the aristae are almost The Mediterranean fruit fly was first described in black. The males are easily distinguished from 1824 by Wiedemann, when he analyzed a speci- females and from other species of the family by a men collected aboard a ship in the Indian Ocean pair of stalky, cornea like, pointed, black-gray that was transporting fruits from Africa. Most of expansions at the apex of the anterior part of their the studies suggest that this insect is native to head. The wings (measuring about 4.5 mm in tropical Africa, originating from areas south of length) are transparent with yellow, brown, and the Sahara desert. This suggestion is supported red stripes. In resting or walking adults the wings by recent genetic studies. It is believed that the fly are semi-open, sloping towards the posterior part invaded first the Mediterranean basin either by of the body resembling a roof. The notum of the dispersing along the valley of the Nile and then thorax is shiny black with discrete whitish stripes, following the Middle East coastline, or by reach- whereas that of the sternum is yellow. The apical ing Spain from the North Western coast of Africa half of the scutellum is completely black. The and Gibraltar. From Spain, where it was first abdomen is orange yellow with two red brown detected in 1850, it probably dispersed to the transverse stripes. The ovipositor is 0.9–1.3 mm New World (Latin America). The fly usually in length. The legs are yellow red with several disperses to neighboring orchards by flying. rather long, yellow setae on the back part of the Invasions of new areas are achieved through tibiae (Fig. 21). the national, international and intercontinental Eggs are oblong, elliptical, glossy white transport of infected fruits. In general, suitable and measure around 0.9–1.1 mm in length and areas for the development of medfly lay between 0.2–0.3 mm in diameter. 45° north and 45° south geographical latitude. In the Northern Hemisphere, the fly is endemic in areas located below 41° latitude. The fly has been reported in many parts of Africa, in the Middle East, in Western Australia, in most of the Central and South America countries and in islands of the Atlantic, Pacific and Indian Oceans. It has invaded North America many times and is believed to be established in California, USA. In Europe, medfly occurs in all the Mediterranean countries and in Portugal.

Morphology Mediterranean Fruit Fly Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), The adult medfly measures 4–6 mm in length, Figure 21 Mediterranean fruit fly, Ceratitis and 1.2–2 mm in width. It has quite a colorful capitata, adult female. 2320 M Mediterranean Fruit Fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) Larvae are white or cream-white, oblong without legs, with the anterior part being narrower than the posterior. There are three instars that can be differentiated from each other by the shape, size and color of their mouthhooks. In general, the first instar measures 0.17–2.2 mm, the second instar 2.3–5 mm and the third 6–10 mm. The puparium is elliptical barrel-like, and measures 4.4–4.5 mm in length and 2–2.5 mm in diameter. The color depends mostly on the larval food and ranges from almost white to dark brown. Mediterranean Fruit Fly Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), Figure 22 Ripe fig infested by medfly larvae. Hosts and Economic Importance

The medfly is the most polyphagous tephritid and Biology infests fruits of plants belonging to more than 67 families. Of the 353 hosts reported (although Medfly is a multivoltine, non-diapausing species some lack confirmed field infestation), 40% belong that usually completes between 3 and 7 generations to the families Myrtaceae (6%), Rosaceae (10%), per year. The number of generations is determined Rutaceae (9%), Sapotaceae (9%), and Solanaceae mostly by geographic area, climatic conditions (6%). Medfly develops in many fruits of tropical, (mostly temperature), host species and host avail- sub-tropical, and temperate fruit trees. In the ability. In the tropics and subtropics, as well as in tropics and sub-tropics, it is a serious pest of cof- the southern Mediterranean areas, this species fee (Coffea arabica), mango (Manifera indica), develops continuously all year round with slower papaya (Carica papaya), avocado (Persea ameri- developmental rates in response to low tempera- cana), guava (Psidium guajava), carambola (Aver- tures. However, in the northern Mediterranean rhoa carambola), sweet orange (Citrus sinensis), coasts only larvae inside infested fruits can survive sour orange (Citrus aurantium), fig (Ficus carica), and maintain the populations throughout winter. grapefruit (Citrus x paradisi), prickly pear (Opun- Adults need to feed on carbohydrates and tia vulgaris), loquat (Eriobotrya japonica), and nitrogen after their emergence in order to reach oriental persimmon (Diospyros kaki). In temper- sexual and reproductive maturity. The mating sys- ate regions, it also infests stone and pome fruits tem of this insect is mainly based on receptive such as apricot (Prunus armeniaca), peach (Pru- female attraction to “calling” males emitting a sex nus persicae), apple (Malus domestica), pear (Pyrus pheromone. Seven to 10 day-old females begin to communis) and other fruits (Fig. 22). lay eggs just after mating, in ripe or semi-ripe Ceratitus capitata is one of the most serious fruits. They open a small hole a few millimeters pests worldwide, with infestation levels reaching deep into the fruit using their ovipositor, and insert 100% in some of its hosts. It is a quarantine pest in a batch of up to nine eggs in the flesh of the fruit. countries such as the United States of America and The oviposition sting is only visible in some hosts. Japan. Intensive control programs have been car- Hatching larvae feed on the flesh of the fruits and, ried out, coordinated by national and international after completing their development, they leave the organizations, with the aim of restricting the fruits to pupate at a small depth (up to 5 cm) in the expansion of the distribution of medfly or of ground beneath host trees. The direct damage of erradicating it from invaded areas. the larvae to fruits is usually accompanied, and Mediterranean Fruit Fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) M 2321 magnified by, secondary infections of fungi and developed and deployed for controlling medfly. bacteria. The mean generation time under con- There is also a set of cultural measures effective for stant conditions in the laboratory (25°C) is esti- the suppression of the fly. The most important of mated at one to two months depending on the them are fruit bagging, sanitation (destruction of host in which the fly developed. Throughout her infested fruits), destruction of all wild host over life span each female lays from 250 to 1,000 eggs. a vast area, or stripping and destroying fruit over a large area. Satisfactory control has been achieved in some cases (mostly under low population densities) Control by biological control and mass trapping. The sterile insect release technique (SIT) has been used with The conventional control of C. capitata is based on success, the aim being in most cases the eradication population monitoring using adult traps and the of the fly from an area. More recently, this method application of bait or cover insecticide sprays. Of has also been used to suppress the pest. There are the many adult traps used, two are the most accept- several cases of successful combination of SIT with able, the McPhail trap with various food baits, and other methods such as bait sprays and/or augmenta- the Jackson trap baited with the male lure trimed- tive releases of parasitoids. The control of this pest is lure. A McPhail trap with the food attractants most successful on an area-wide basis. Succesful ammonium acetate, putrescine and trimeth- implementation of an area-wide control programme ylamine, loaded in dispensers lacking a month, can lead to the establishment of pest free zones constitutes a very effective, female-targeted and within a country and also to the eradication of the medfly-selective trapping system that outperforms pest from a state or country. most of the other trapping systems. Several insecti- In addition to direct control measures, there cides, used in cover or bait sprays, have been proved are other strategies to control this fly. The most effective to control medfly. For example, malathion important of these are the legislative measures. is very effective and is less toxic for invertebrates, Very often, strict quarantine regulations are set and has been used extensively in several, large, up to prevent the entry of the fly into an unin- area-wide control programs (Fig. 23). fested area. Several markets accept only those Besides chemical control, several other pre- fruits and/or vegetables that have undergone a harvest and post-harvest methods have been commodity treatment that secures a mortality of at least 99.9968% (Probit 9) that is generally acceptable as zero infestation. The best-known of the commodity treatments is the exposure of the fruits to lethal low or high temperatures, and to fumigant insecticides.  Citrus Pests and their Management  Tropical Fruit Pests and their Management  Fruit Flies (Diptera: Tephritidae)

References

Carey JR (1991) Establishment of the Mediterranean fruit fly Mediterranean Fruit Fly Ceratitis capitata in California. Science 253:1369–1373 Katsoyannos BI, Heath RR, Papadopoulos NT, Epsky ND, (Wiedemann) (Diptera: Tephritidae), Hendrichs J (1999) Field evaluation of the Mediterra- Figure 23 Jackson trap. nean fruit fly (Diptera: Tephritidae) female selective 2322 M Mediterranean Spotted Fever attractants for the use in monitoring, mass trapping and Megachilidae sterile insect technique. J Econ Entomol 92:583–589 Liquido NJ, Shinoda LA, Cunningham RT (1991) Host plants of the Mediterranean fruit fly (Deptera: Tephritidae): an A family of bees (order Hymenoptera, superfamily annotated world review. Miscellaneous Publication 77. Apoidae). They commonly are called leafcutting Entomological Society of America, Lanham, MD bees. Mitchell AC, Saul SH (1990) Current control methods for the Mediterranean fruit fly, Ceratitis capitata, and  Bees their application in the USA. Rev Agric Entomol  Wasps, Ants, Bees and Sawflies 78:923–940 Papadopoulos NT, Carey JR, Katsoyannos BI, Kouloussis NA (1996) Overwintering of Ceratitis capitata (Diptera: Tephritidae) in northern Greece. Ann Entomol Soc Am Megafauna 89:526–534 Papadopoulos NT, Katsoyannos BI, Carey JR, Kouloussis NA (2001) Seasonal and annual occurrence of the Mediter- The largest of the animals in an area, often greater ranean fruit fly (Diptera: Tephritidae) in northern than 20 mm body width. (contrast with micro- Greece. Ann Entomol Soc Am 94:41–50 White IM, Elson-Harris MM (1992) Fruit flies of economic fauna and macrofauna) significance: their identification and bionomics. CAB International, Wallingford Megalodontidae

Mediterranean Spotted Fever A family of sawflies (order Hymenoptera, suborder Symphyta). Also known as Boutonneuse Fever, this disease is  Wasps, Ants, Bees and Sawflies caused by a tick-transmitted Rickettsia.  Ticks Megalopodid Beetles

Mediterranean Theileriosis Members of the family Megalopodidae (order Coleoptera). This is a tick-transmitted disease caused by the  Beetles protozoan Theileria annulata.  Piroplasmosis Megalopodidae Medocostidae A family of beetles (order Coleoptera). They com- A family of bugs (order Hemiptera). monly are known as megalopodid beetles.   Bugs Beetles

Meenoplidae Megaloptera

A family of bugs (order Hemiptera, suborder Ful- An order of insects, sometimes considered to part goromorpha). All members of the suborder are of the order Neuroptera. They commonly are referred to as planthoppers. known as alderflies and dobsonflies.  Bugs  Alderflies and Dobsonflies Meigen, Johann Wilhelm M 2323 Megalopygidae an early age, but had little opportunity for formal education. By various circumstances, he A family of moths (order Lepidoptera). They com- acquired knowledge of math and French, and monly are known as flannel moths. eventually gained access to books. Thus, he  Flannel Moths became qualified to serve as a tutor in 1784, and  Butterflies and Moths moved away from home. He made the acquain- tance of Mathias Baumhauer, an ardent collector of insects, and became extremely interested in Megalyridae insects. About 1778 he came to realize that Lin- naeus had not described everything, and that the A family of wasps (order Hymenoptera). Linnean genera were too inclusive. He began a  Wasps, Ants, Bees and Sawflies reclassification of Diptera based on wing venation, which eventually was expanded to include other body parts. Meigen taught himself enough Latin to read the works of Fabricius. In 1796 he Megamerinidae took a teaching position in Stolberg. Meigen’s approach to classification, using many body A family of flies (order Diptera). parts, did not find favor at the time, especially  Flies with Fabricius. Due to the political turmoil of the era, Meigen found difficulty with employ- ment, but always maintained his interest in Dip- Megapodagrionidae tera, and eventually became renowned as a pioneer in dipterology. He published several A family of damselflies (order Odonata). volumes on Diptera, but also on Lepidoptera.  Dragonflies and Damselflies Meigen sold his collection and drawings to P.J.M. Macquart in 1839 and retired. He died July 11, 1845 (Fig. 24). Megarididae

A family of bugs (order Hemiptera, suborder Pentamorpha).  Bugs

Megaspilidae

A family of wasps (order Hymenoptera).  Wasps, Ants, Bees and Sawflies

Meigen, Johann Wilhelm

J. W. Meigen was born at Solingen, Germany on Meigen, Johann Wilhelm Figure 24 Johann May 3, 1764. He became interested in insects at Meigen. 2324 M Meinertellidae Reference X and half the Y chromosome) and the ratio of male and female progeny is 1:1. If changes in dis- Steyskal GC (1974) On the life and influence of JW Meigen. tribution of the X and Y chromosome occur Mosq Syst 6:79–87 through meiotic drive, it is detected because more females or males are produced than expected. Whether meiotic drive mechanisms actually affect Meinertellidae the sex chromosomes more frequently, or whether meiotic drive is more frequently discovered A family of bristletails (order Archeognatha). because it is relatively easy to detect due sex ratio  Bristletails changes, is unknown. Meiotic drive has been found most often in Diptera, including Drosophila obscura, D. melan- Meiosis ica, D. tripunctata, D. testacea, D. melanogaster and D. quinaria groups, mosquitoes (Aedes and The sequence of events occurring during two cell Culex), sciarid flies and stalk-eyed flies (Diopsi- divisions to convert diploid cells into haploid dae). Whether meiotic drive is common in other cells. insect orders is controversial. Three examples of sex chromosome meiotic drive are described below, including Segregation Meiotic Drive in Insects Distorter (SD) in Drosophila, male drive (MD) in the mosquitoes Aedes aegypti and Culex quinque- Marjorie A. Hoy fasciatus, and meiotic drive in stalk-eyed flies. University of Florida, Gainesville, FL, USA Segregation Distorter (SD) In Drosophila melanogaster the SD phenotype is present at low, Mendel’s law of segregation proposes that equal but stable, frequencies in most field populations. numbers of alleles (variants of the same gene) D. melanogaster males containing one SD chro- derived from the paternally and maternally- mosome and one normal (SD+) chromosome may derived chromosomes are distributed to eggs produce only progeny with the SD chromosome, and sperm during meiosis (the reductional divi- instead of half with SD and half with SD+, due to sion that results in haploid eggs or sperm having the failure of sperm with the SD+ chromosome to only one copy of each type of chromosome). mature. Segregation distortion occurs because the However, this law is sometimes violated due to a nuclei of the sperm with the normal SD+ chromo- phenomenon called meiotic drive. Meiotic drive some fail to condense at sperm maturation. The has been studied in insects and has been pro- Enhancer locus of SD, E(SD), is required for the posed to be a future tool for suppressing pest full expression of this type of meiotic drive. populations. The SD phenotype actually involves two Meiotic drive alters the equal assortment of overlapping genes, one called HS2ST and the chromosomes during meiosis so that certain second called RanGAP. RanGAP is an essential chromosomes are inherited by the progeny more component of a system that transports proteins frequently than expected (greater than 50% of the and RNA molecules into and out of the cell’s time). Meiotic drive most frequently is observed nucleus. Both HS2ST and RanGAP are present affecting sex chromosomes (chromosomes that twice on the SD, as opposed to once on the SD+, are different in males and females). In most chromosome. This tandem duplication is neces- insects, females are XX and males are XY (or het- sary for segregation distortion. Both genes erogametic, with half the sperm receiving the appear normal in the right hand copy, but the Meiotic Drive in Insects M 2325 RanGAP gene on the left lacks the last 234 amino frequency of the allele or chromosome which is acids. It is possible that the truncated RanGAP favored in transmission, even if it confers a disadvan- protein functions incorrectly and is mislocalized tage on its carriers. It has been proposed that meiotic within the cell. drive might be used to introduce new genes (such as Distorter Gene Meiotic drive also has been cold-sensitive lethal genes, insecticide-susceptibility described in the mosquitoes Aedes aegypti and genes, or behavior-altering genes that would reduce Culex quinquefasciatus. In both species, a Y-linked the impact of pest populations on humans) into nat- gene results in excess males. Excess males are ural populations as a method to achieve control of produced because X chromosomes are broken pest insects. However, much remains to be learned during meiosis in males. As a result, fewer X than about the stability of such drive mechanisms and Y chromosomes are transmitted, leading to the the conditions under which they might function in production of fewer female embryos. TheDistorter pest management programs. Furthermore, as noted gene (D) is linked closely to the sex-determining above, resistance to meiotic drive mechanisms can locus m/M and causes the chromosome breakage. evolve in some species or populations; such resis- Additional genes are involved in the sex ratio tance mechanisms, if developed rapidly, could distortion; sensitivity to Distorter is controlled by reduce the effectiveness of the drive mechanism in m, the female-determining locus. In some strains, the pest management program. sensitivity is influenced by a second sex-linked gene t. Yet another sex-linked gene A enhances the effect of Distorter. Distorter has been found in mosquito Hybrid Sterility and Meiotic Drive populations from Africa, America, Australia and Sri Lanka, but resistance to it is widespread. It is sometimes possible to cross different insect Female-biased Sex Ratios in Stalk-eyed species, and the progeny sometimes show altered Flies Extreme female-biased sex ratios are found sex ratios, with one sex absent, rare, or sterile. The in two sister stalk-eyed flies, Cyrtodiopsis dal- missing or sterile sex is usually the heterogametic manni and C. whitei (Diopsidae), due to a meiotic sex (XY). This phenomenon is known as Haldane’s drive element on the X chromosome. Eye stalks Rule. However, Haldane’s Rule appears to occur are more exaggerated in males than in females in only in taxa with sex chromosome-based meiotic these species and females prefer to mate with drive, such as the Lepidoptera and Diptera. Hal- males with a longer eye span. The longer eye stalks dane’s rule may be occurring if suppression of sex may be an indicator that the male either lacks ratio distorters is lost in the novel nuclear cytotype meiotic drive or can suppress the meiotic drive. of the hybrid. Thus, females prefer to mate with males with longer eye stalks because it should increase the female’s fitness by avoiding a biased sex ratio in her prog- References eny. Apparently, there are both autosomal- and Y-linked genes involved in resistance to the Ashburner M (1989) Drosophila a laboratory handbook. meiotic drive. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY Ganetzky B (2000) Tracking down a cheating gene. Am Sci 88:128–135 Meiotic Drive as a Pest Jiggins FM, Hurst GDD, Majerus MEN (1999) How common Management Tool? are meiotically driving sex chromosomes in insects? Am Nat 154:481–483 Lyttle TW (1993) Cheaters sometimes prosper: distortion of Meiotic drive operates as an evolutionary force mendelian segregation by meiotic drive. Trends Genet which can cause an increase in the population 9:205–210 2326 M Melander, Axel Leonard Wilkinson GS, Presgraves DC, Grymes L (1998) Male eye Melanothripidae span in stalk-eyed flies indicates genetic quality by meiotic drive suppression. Nature 391:276–279 Wood RJ, Newton ME (1991) Sex-ratio distortion caused by A family of thrips (order Thysanoptera). meiotic drive in mosquitoes. Am Nat 137:379–391  Thrips Wrensch DL, Ebbert MA (eds) (1993) Evolution and diversity of sex ratio in insects and mites. Chapman and Hall, New York, NY Melissococcus pluton (Bacteria)

Melander, Axel Leonard The causative agent of European foulbood in honey bees. A.L. Melander was born at Chicago, Illinois, USA,  European Foulbrood on June 3, 1878. He became interested in insects while in high school, and studied with William Morton Wheeler at the University of Chicago and Melittidae the University of Texas. He received his M.S. in 1902. Melander taught at Washington State Univer- A family of bees (order Hymenoptera, superfamily sity from 1904 to 1926, and was head of the depart- Apoidae). ment for 20 years. He completed his Sc.D. at Harvard  Bees University in 1914. He left Washington State in 1926  Wasps, Ants, Bees and Sawflies and moved to the City College of New York where he served as professor of biology and head of the department, and retired in 1943. Melander worked Melittin on many insect problems, and among his accom- plishments was the first documentation of declin- A protein in bee venom thought to be responsible ing effectiveness of an insecticide. He collaborated for the toxic properties. with C.T. Brues on authorship of “Key to families of  Honey Bees North American insects” (1915), and “Classification of insects” (1932). He served as president of the Entomological Society of America in 1938. Melander Melittology also accumulated one of the world’s largest collections of flies, which is now incorporated in the The scientific study of bees. Smithsonian Institution. Melander died at River- side, California, on August 14, 1962. Melittophile

Reference An organism spending at least part of its life in association with bee colonies. Mallis A (1971) American entomologists. Rutgers University Press, New Brunswick, NJ, 549 pp Melizoderidae Melandryidae A family of bugs (order Hemiptera, suborder A family of beetles (order Coleoptera). They com- Cicadomorpha). monly are known as false darkling beetles.  Bugs  Beetles  Leafhoppers Melon Aphid, Aphis gossypii (Hemiptera: Aphididae) M 2327 Mellanby, Kenneth Mellinidae

Kenneth Mellanby was born in 1908 and was A family of wasps (order Hymenoptera). educated at King’s College, Cambridge, England,  Wasps, Ants, Bees and Sawflies and the London School of Tropical Medicine, but his studies were interrupted by World War II. At the time, scabies was widespread in the military, and Mellanby deduced that the purported means Meloidae of spread were erroneous and quickly demonstrated effective control. This work effectively A family of beetles (order Coleoptera). They com- released the equivalent of an additional two divi- monly are known as blister beetles. sions of soldiers from the hospital to aid in the  Blister Beetles war effort. This work also resulted in publication  Beetles of two books, “Scabies” (1943) and “Human guinea pigs” (1945). After the war he moved to Nigeria to start a college, and in a few years had a program operational. Mellanby returned to Melon Aphid, Aphis gossypii England in 1953, worked on various projects, and (Hemiptera: Aphididae) eventually assumed the position of Head of Ento- mology at Rothamsted Experimental Station. Timothy A. Ebert However, it was not until 1961, when he was The Ohio State University, Wooster, OH, USA appointed Director of the Nature Conservancy’s Experimental Station at Monk’s Wood did his The melon aphid is a polyphagous species career again flourish. He quickly assembled the capable of feeding and reproducing on plants largest research station in Britain devoted to in over 90 plant families. There are over 72 studying conservation of wildlife. Work done crops in over 32 plant families worldwide that here included the effects of pesticides on wildlife, require some kind of human intervention for habitat management, monitoring changes in dis- managing this aphid. This aphid is considered tributional status, and establishment of a records a pest in crops produced both in the field and center. Mellanby was the founding editor of the in the greenhouse. Host plant damage includes journal “Environmental pollution,” and he wrote direct feeding and transmission of plant several books related to environmental causes, pathogenic viruses. Reproduction in this aphid including “Pesticides and pollution” (1967), is entirely asexual in warmer climates, but “Farming and pollution” (1991), and “The DDT includes a sexual phase in colder climates. story” (1992). Mellanby was active in several sci- Aphids of any given clonal line do not have the entific societies and received numerous honors, ability to utilize the entire host range reported including several honorary doctorates. He died for this species. Indirect damage by this aphid in 1993. may also occur through the production of honeydew. Honeydew is a sugary liquid excreted by aphids to eliminate excess carbon and water. Honeydew coats plant surfaces below the aphid Reference colony. Fungi able to utilize honeydew as a food source then cover the plant surface, Dempster J (1994) Kenneth Mellanby CBE ScD (1908–1993) thereby reducing the light reaching the Antenna 18:110–112 chloroplasts. 2328 M Melon Aphid, Aphis gossypii (Hemiptera: Aphididae) Systematics and Biology yellow to a “green that is almost black,” and individuals can be found anywhere along a gradient Common Names within this range. Additionally, some individuals may appear to be part yellow and part green. The most popular English common names are The yellow (and smaller) form occurs during the cotton aphid, or the melon aphid. These are warmer summer conditions. The green (and the Entomological Society of America approved larger) form occurs during cooler spring common names. However, there are at least 40 (Fig. 25) and fall temperatures, with uncrowded “common” names which are older, of more conditions. Color is not a host race trait because regional importance, or not English. color morphs are able to produce progeny of the other color morph. Host plant also influences aphid color, presumably due to stress – where the yellow form predominates under Description stressful conditions. The mechanism for color morph development is unknown. Some insecti- Apterous, mature, viviparous, yellow females can cides can cause a reverse stress response: e.g.,

be <0.83 mm long and weigh <5.8 mg, while green LC10 doses of sulprofos (an insecticide). females can be over 1.8 mm long and weigh over 66 mg. The body is generally rounded. Antennae have 5–6 segments. Cornicles (also known as siphunculi, and located between the fifth and sixth Genetics abdominal tergites) are dark, slightly conicle with the proximal end slightly larger in diameter than 2n = 8, with chromosome lengths of about the distal end, and the length up to five times the 2.3–3.65, 3.4–5.42, 3.8–6.24, and 5.0–7.64 μm. diameter. Cornical length ranges from 0.13 to 0.35 mm. The cauda is pale to dark with two or three pairs of lateral setae. The following stages have been observed: fundatrix (first parthenogenic generation from fertilized egg), fundatrigeniae (viviparous females on the primary host), alienicola (viviparous females on a secondary host), gynoparae (viviparous females are born on a secondary host and then migrate to the primary host to produce sexual females), oviparous female (egg laying female), alate and apterous male, hiber- nating viviparae (viviparous female), androparae (viviparous females that exclusively produce males), heteroparae and androgynoparae. In addition to the specific life stages, this aphid displays considerable variability within clones. Adult individuals may have wings that fail to develop fully and range in size from little Melon Aphid, Aphis gossypii (Hemiptera: stubs to nearly functional. Furthermore, this Aphididae), Figure 25 Melon aphid (cotton aphid), aphid has a wide range in color variation, from Aphis gossypii. Melon Aphid, Aphis gossypii (Hemiptera: Aphididae) M 2329 Chromosomes are believed to be holokinetic cordifolia L. (Rubiaceae), Catalpa bignonioides (chromosomes lack a centromere), which could Walter (Bignoniaceae), Zanthoxylum simulans simplify genetic rearrangement and permit more Hance (Rutaceae), or Punica granatum L. (Lyth- rapid adaptation to new conditions: from adapt- raceae). Aphids that remain on the primary host ing to new host plants to developing pesticide for both sexual and parthenogenic reproduction resistance. are described as “autoecious”.

Host Range and Utilization Population Growth

The worldwide distribution ofA. gossypii is partly Population growth is a function of survival, time due to its broad host range and its ability to switch to reproduction and nymphs produced per day. A hosts. One study reported A. gossypii surviving at recent study examined the stage-specific influence least 15 days following transfer from plants in the of temperature on the population growth rate for Scrophulariaceae, Brassicaceae, Asteraceae, Lami- this aphid on cotton. Temperatures examined were aceae, Rosaceae and Malvaceae to plants in the from 10 to 35°C. Individual life table parameters Asteraceae, Solanaceae, Cucurbitaceae, Liliaceae, were optimized at slightly different temperatures; Portulacaceae, Commelinaceae and Araceae. The e.g., total fecundity of 28.3 nymphs per female was broad host range increases survival under unfa- highest at 25°C, while development was fastest at vorable conditions (e.g., when the original host 30°C where it took only 4.6 days from birth to plant species is unavailable), and aids in the time of first reproduction. The development transfer of viruses from reservoir plants to crop threshold was estimated for the first through plants. fourth instar, and the adult, to be 8.2, 8.0, 7.2, 6.2 Reproduction in A. gossypii is mostly asex- and 7.9°C, respectively. Overall, the maximum ual with either alate (winged) or apterous (wing- intrinsic rate of increase (0.386 per day) was less) females. In warmer environments, this achieved at 25°C, which results in a population aphid has an anholocyclic life cycle (reproduc- doubling time of only 1.8 days. While other stud- tion only through parthenogenesis), while in ies have reported specific values that would lead cooler areas, the aphid exhibits either a heteroe- (if combined) to a faster population growth rate, cious or autoecious holocyclic life cycle. The het- in total, this is probably close to the upper limit for eroecious cycle involves a migration from a the population growth rate for this aphid. primary host to a secondary host in the spring and a return to a primary host in the fall for laying eggs. The primary host for the aphid is con- Nutrition sidered to be the ancestral host upon which the aphid evolved, and therefore, it is where the sex- The nutritional requirements of aphids are modi- ual phases of the life cycle are completed. The fied due to endosymbionts that produce some primary host for this aphid is unknown because nutrients the aphid is unable to make without there is the possibility that the aphid has second- them. Typically, nutritional quality for aphids is arily acquired new “primary” hosts. The ances- measured by reproductive rate, or growth rate. tral host is probably one of the following: Citrus Diet pH is best between 7.4 and 7.8. Sugars in the (Rutaceae), Hibiscus syriacus L. (Malvaceae), diet serve as nutrition and to stimulate feeding. Rhamnus dahuricus Pall. (Rhamnaceae), Celas- Optimal sucrose concentrations in artificial diets trus orbiculatus Thunb. (Celastraceae), Rubia are between 20 and 30%, and diets with other 2330 M Melon Aphid, Aphis gossypii (Hemiptera: Aphididae) sugars are less suitable, although 20% sucrose with Production of Winged Aphids (Alates) 10% maltose came close to equaling a sucrose- only diet. Experiments on identifying amino acid There are two proposed triggers for production of requirements have shown that cystine and methi- winged aphids in A. gossypii: nutritional factors onine in the diet improve growth rate, but above (physiological stress), and crowding. Aphid-aphid 30 mg/ml, they are toxic. While not essential, contact has been proposed as a mechanism for improved growth was observed with tyrosine, triggering alate production, but it is possible that phenylalanine and tryptophan in the diet. the aphid has a chemical means of identifying the number of neighbors. It is not known if the trigger for production of alates is continuous, discrete, or Abiotic Environment a combination of the two. As a continuous process, increased numbers of aphids changes plant nutri- One of the most important abiotic factors affect- tion and brings about a corresponding change in ing the life cycle of this aphid is temperature. A alate production. However, it would appear that lower developmental threshold for this aphid production of alates is partly a discrete process was estimated at 7.34°C on squash. Develop- where crowding gets to some threshold level and ment thresholds have also been estimated for suddenly alates are produced. the aphid on cucumber at 5.8°C from birth to Crowding effects have been conclusively dem- age of first reproduction, but the development onstrated for alate production on cotton. One threshold for the nymphal stages was 6.9°C. A study examined crowding using leaf disks with a study of this aphid on speedwell, Veronica per- single, apterous aphid that was removed following sica, estimated a developmental threshold of reproduction. The resulting colonies contained 10.47°C for the preflight period. An upper limit from one to seven nymphs. From 52 colonies with of survival at 35°C was reported on squash in one or two nymphs, no alates were produced. From Saudi Arabia, but the authors pointed out that 41 colonies with three or four nymphs, <10% of the aphid survives in okra fields where the day- the colony became alate. However, of 29 colonies time temperature exceeds 45°C. Temperature is with five to seven nymphs, over 30% of the total also thought to be responsible for some strains number of aphids became alate. The observation of A. gossypii being holocyclic while others are that colonies with one to two individuals never anholocyclic. produce alates has beed reported several times. Light intensity and day length are also Nutritional factors from other sources also important abiotic factors in the reproductive play a role in production of alates. One of the more capacity of this aphid. Increasing day length interesting hypotheses is the possible role of aphid- increases the intrinsic rate of increase, decreases borne plant viruses. The survival of the virus is population doubling time and decreases genera- dependent on having an efficient aphid vector, and tion time. However, there is some indication that the most efficient vector is alate. Therefore, one at 18-h daylengths, population growth rates might expect that a virus would promote condi- decline slightly. The effects of light intensity have tions favoring alate production in the aphid. been studied, but with conflicting results; some- Indeed, zucchini plants infected with the zucchini times light intensity increases reproduction, and yellow mosaic virus increased alate production in sometimes it decreases reproduction. In the field, the melon aphid. increased light intensity may decrease reproduc- The parentage and physiological state of the tion. Reflective mulch can decrease aphid popu- parent influence production of alates. Starved lations, and a suggested mechanism was increased nymphs from apterous parents resulted in 13% light intensity on abaxial leaf surfaces. alates versus 0.4% from unstarved nymphs, but the Melon Aphid, Aphis gossypii (Hemiptera: Aphididae) M 2331 starvation of nymphs from alate parents resulted in wavelengths down to 357 nm. Adults of mixed age no increase in formation of alates. A similar result also preferred this short wavelength, though some was also reported for starved parents, where preference was also shown for wavelengths of starved, apterous parents produced more alate 550 nm. Furthermore, there is a stage-dependent progeny than well-fed, apterous parents (23% and response to light, the adults being more sensitive 2%, respectively), and there was no increase in alate to different wavelengths than the nymphs. formation by starved, alate parents.

Host Plant Behavior Orientation to host plants begins at 6 h after wing Flight development, but has a maximal response after about 24 h. In addition to the type of host present Flight is the beginning of the dispersal or sexual in a field, the arrangement of hosts within the field reproductive phase in the life cycle of the melon is also important. An experiment was done using aphid. It begins with the preflight period (from soybean, dwarf sorghum and tall sorghum planted molt to flight), which lasts from 1 to 70+ hours in monoculture or interplanted. At the sorghum depending on host plant and temperature. Adult canopy level, landing rates were highest on mon- flight activity is most common from about sun- ocultures of dwarf sorghum, then monocultures rise to early afternoon, with little or no activity of tall sorghum, and lowest in mixed plantings. after dark. Alates typically fly within 1 m of the ground. In laboratory colonies, the flight period lasted Feeding from 1 to 4 days. Older colonies produced fewer alates that flew for 1 day and more that flew for 2 In one set of experiments, alates were placed on days. Aphids flew from one to several (about five) squash, Cucurbita pepo, plants and watched under times each day, with the first flight always longer a microscope. Given that probing occurs when than the others. Alates larviposited after flight, and aphids pressed their labium to the surface and flew again when the number of embryos with pig- placed their antennae flush with the body, the mented eyes per ovariole decreased. Alates that aphid took 6–9 min following contact with the flew longer had a shorter reproductive period and plant before probing. However, this is the same produced fewer total progeny. Alates that land on time it took newly emerged alates, and may not be previously colonized plants have a decreased prob- characteristic of alates after migration. ability of larvipositing.

Egg Laying Light Egg laying on Hibiscus syriacus occurred mostly The melon aphid is sensitive to different wave- between the leaf scar and the twig near where the lengths and intensities of light, but the nature of buds would emerge in the spring. Some eggs were the effect is not clearly understood. Aphids were also laid at the branching point of twigs. However, attracted to Auclair’s artificial diet illuminated from the wandering behavior of the oviparous at 570–595 nm, while diets illuminated at 420–485 females, it appears that females searched for pro- nm were repellent. This contradicts other findings tected places to lay eggs rather than for specific where newly molted, alate adults preferred shorter parts of the plant. 2332 M Melon Fly, Bactrocera cucurbitae (Coquillett) (Diptera: Tephritidae) Biotic Interactions Lipolexis scutellaris Mackauer), and some parasitic mites (Allothrombium ovatum, Allothrom- Virus Transmission bium pulvinum Ewing). Several fungi are also able to cause aphid mortality (e.g., Paecilomyces The ability of the melon aphid to transmit plant fumosoroseus, Neozygites fresenii, Cephalospo- pathogenic viruses increases its ability to damage a rium lecanii, Verticillum lecanii, Erynia neoaphidis, wide range of crops. This ability is influenced by the Beauveria bassiana), as well as some bacteria. biochemistry of all three participants: plant host, These lists of names are provided as an indication virus and aphid. Some examples are: Citrus Tristeza of the melon aphid’s importance in the food virus acquisition rates are affected by citrus cultivar. chain and are far from complete. Transmission of the virus is influenced by virus This aphid has also been associated with ants, strain, but not by the aphid strain nor the rearing which both protect the aphid and feed off the host for the aphid. Cucumber mosaic virus (CMV) aphid. The association is opportunistic rather than transmission is governed by virus RNA strands 1, 2 obligate. The ants, which have been found with and 3, but not strand 4. Transmission of CMV is this aphid, include: Camponotus japonicus Mayr, influenced by the previous aphid host, and aphid Camponotus compressus Fabricius, Anoplolepis clones differ in their ability to transmit the virus. spp. and Solenopsis invicta Buren, among others. The relationship between aphid and virus is very  Aphids specific in that changes in amino acids 129, 162 and  Vegetable Pests and their Management 168 of the coat protein significantly alter the ability  Citrus Pests and their Management of the aphid to transmit the virus. The interaction between this aphid and other plant pathogenic References viruses can be equally specific at a biochemical level.

While some viruses like CMV have specific loca- Ebert TA, Cartwright B (1997) Biology and ecology of Aphis tions on the coat protein, which mediate aphid gossypii. Glover (Homoptera: Aphididae). Southwest transmission, other viruses produce helper compo- Entomol 22:116–153 nents, which mediate transmission: e.g., Aphis gos- Miyazaki M (1987) Forms and morphs of aphids. In: Mink AK, Harrewijn P (eds) Aphids: their biology, natural sypii transmission of tobacco etch potyvirus (TEV) enemies, and control. Elsevier, Amsterdam, The and turnip mosaic potyvirus (TuMV). Netherlandspp 27–50 Stoetzel MB, Miller GL (2001) Aerial feeding aphids of corn in the United States with reference to the root- feeding Aphis maidiradicis (Homoptera: Aphididae). Mortality Fla Entomol 84:83–98 Xia JY, van der Werf W, Rabbinge R (1999) Influence of tem- This aphid is an important food resource for perature on bionomics of cotton aphid, Aphis gossypii, on cotton. Entomol Exp Appl 90:25–35 many organisms. These include many insect predators (ladybugs: Coccinella septempunctata L., Hippodamia convergens Guérin-Méneville, Melon Fly, Bactrocera cucurbitae Menochilus sexmaculatus (Fabricius), Scymnus (Coquillett) (Diptera: Tephritidae) louisianae Chapin; lacewings: Chrysopa carnea Stephens, Chrysoperla rufilabris (Burmeister), John L. Capinera Chrysopa sinica Tjeder; hoverflies: Syrphus sp.; University of Florida Gainesville, FL, USA Hemiptera: Orius insidiosus (Say), Geocoris spp., Nabis spp., Zelus spp.), hymenopteran parasitoids Melon fly is found in the tropical regions of Asia, (Trioxys spp., Aphelinus spp., Lysiphlebus testa- a portion of east Africa, and on some Pacific ceipes (Cresson), Aphidius colemani Viereck, islands, including Hawaii, USA. Melon fly has been Melon Fly, Bactrocera cucurbitae (Coquillett) (Diptera: Tephritidae) M 2333 recovered on several occasions in California, and although it has not become established in the western hemisphere, the tropical and subtropical regions would be suitable habitat.

Life History

A life cycle can be completed in about 5 weeks in warm climates, but may require 3–4 months in cool climates. The adults (Fig. 26) can survive for Melon Fly, Bactrocera cucurbitae (Coquillett) months, and will continue to reproduce if fruit is (Diptera: Tephritidae), Figure 26 Adult of melon available. In tropical climates such as Hawaii they fly, Bactrocera cucurbitae (Coquillett). are present throughout the year. Their abundance is determined mostly by availability of suitable host plant material, but they tend to be most common in summer and autumn. Females deposit eggs in small batches, usually 5–20 eggs each. Females may produce 800–900 eggs over their life span. The white eggs are about Melon Fly, Bactrocera cucurbitae (Coquillett) 1.3 mm long and 0.25 mm wide, and are deposited (Diptera: Tephritidae), Figure 27 Mature larva of in the fruit or vegetative parts of plants. The lower melon fly, Bactrocera cucurbitae (Coquillett). and upper developmental thresholds for egg development are about 10 and 40°C, respectively. Eggs measure about 6–9 mm in length. Dark markings hatch, on average, in 1.3 days. resembling a “T” occur on the abdomen, and two The larvae (Fig. 27) are white, and when they lateral and a medial yellow stripe are found on the hatch they are about the length of the egg. Larvae thorax. The presence of wing bands and the dark immediately begin to grow, and attain a length of abdominal markings can be used to differentiate about 2.5, 5.5, and 11.0 mm in length during instars melon fly from oriental fruit fly and Mediterra- 1–3, respectively. The mouth hooks are pale in the nean fruit fly, respectively. The preoviposition first instar, but thereafter are darkened and easily period of adults is about 7.4 days, and they are observed. Larvae complete their development in capable of depositing eggs for about 3 months. 5–8 days, with instars 1–3 requiring about 1, 1–2, Adults spend most of their time associated and 2–3 days, respectively, in soft hosts such as with the adult host plants, seeking vegetable crops papaya. The lower and upper developmental thresh- or other prospective larval hosts intermittently for olds for larvae are about 12 and 34°C, respectively. oviposition. Fly activity in crop fields peaks in the When mature, larvae leave the host, burrow afternoon hours. At dusk, males form aggregations into the soil up to a depth of 10 cm, and pupate. called leks, and by making wing vibrations and The adults emerge from the tan or yellow-brown releasing sex pheromone, attract and copulate with puparium after about 10 days (range of 7–14 days), females. and dig to the soil surface. Melon fly prefers such cucurbits as water- Newly emerged adults crawl to a sheltered melon, cantaloupe, pumpkin, squash, and cucum- location where they rest for 2–3 h before taking ber, but infests other vegetables including tomato, flight. Adults are yellow or yellow-brown in color, pepper, green bean, and cowpea. Wild hosts, par- with yellow wings marked with brown bands. They ticularly bitter melon, Mormordica charantia, can 2334 M Melon Fly, Bactrocera cucurbitae (Coquillett) (Diptera: Tephritidae) be important. Passion fruit, papaya, grape, and cit- Management rus also are suitable larval hosts, but it is the availability of vegetable crops that generally determines Fruit may be sampled for eggs and larvae, and soil melon fly abundance. for pupae, but this is not done routinely because of The adult often is found associated with plants the high labor requirements and expense. A natu- that are not larval food sources, but rather provide ral chemical constituent of some plants, raspberry sustenance for the adults. Honeydew produced by ketone, is highly attractive to male melon flies, and such insects as aphids and scale insects, and secre- a synthetic analog called cue-lure is equally or tions of extrafloral nectaries, attract flies to plants more attractive; the latter is useful with traps for such as corn; castor bean, Ricinus communis; spiny sampling. Fluorescent yellow sticky traps can also amaranth, Amaranthus spinosus; rattlepod, Croto- be used to sample adult densities, and odor and laria incana and C. mucronata; and other culti- visual stimuli are sometimes combined in a single vated and wild plants. trap design. However, the most widely used trap is Extensive research has been conducted the McPhail trap, a liquid-baited trap. around the world to identify effective natural Melon fly adults, unlike many insect pests, do enemies of this serious pest. The wasp Psytallia not remain in contact with larval host plants for fletcheri (Silvestri) (Hymenoptera: Braconidae), a extended periods of time. Instead, they spend a larval parasitoid, is the most effective biological great deal of time in weedy vegetation surround- control agent located. Although P. fl etch e r i is ing crop fields. A program of treating the sur- effective at parasitizing melon fly larvae infesting rounding vegetation, rather than the crops, is often wild cucurbits, it is relatively ineffective in crops. recommended. Treatment of border vegetation Therefore, its use is limited to reduction of back- can be much more effective than treatment of ground populations only. crops. Bait sprays containing insecticide also can be used effectively for adult suppression. Sugar or protein hydrolysate is mixed with various insecti- Damage cides to produce bait sprays. Insecticide and bait treatments have been combined with mass release In the absence of biological or chemical control, of sterile male insects to eradicate melon fly from melon fly is extremely damaging. Melon fly lar- some Pacific islands. Cue-lure can also be mixed vae develop in blossoms, fruits, and some vege- with insecticide to attract and kill flies, but it is tative portions of plants. Among vegetative plant only effective against males. material, newly emerged seedlings and terminal Field sanitation is the most important ele- shoots are preferred. Similarly, among fruits, ment of cultural management. High melon fly immature fruit is usually selected. Larval feeding populations result from continuous availability of also opens the plant tissue to secondary invad- larval food, which may be due either to continu- ers, both microbial and insect. Damage can also ous cropping or failure to dispose of crop residues. occur from egg laying even when larvae cannot Destruction of infested or unmarketable vegeta- survive because oviposition allows entry of bles in a timely manner is essential. Trap crops microorganisms or causes deformities in the have not been effective at protecting vegetables, growing fruit. Some differences in damage probably due to the relatively wide host range and among cucurbits exists. Seedling and stem dam- vagility of the insects. age is more common in watermelon and canta- Protective coverings have long been used to loupe than in squash, cucumbers, and pumpkin. deter oviposition by melon fly. Paper bags and Blossom damage is serious among all cucurbits newspapers are used to wrap individual fruit in except cucumber. the case of large produce such as cantaloupe and Melon Thrips, Thrips palmi Karny (Thysanoptera: Thripidae) M 2335 watermelon. This is effective but tedious, and not when the insects are cultured at 15°C. Melon thrips useful for small-fruited vegetables. Also, it does are able to multiply during any season that crops not protect vines and flower buds. Row covers are cultivated but are favored by warm weather provide more complete protection, but pollination and suppressed by senescent crops. In southern may be interrupted. Florida, they are damaging on both autumn and  Fruit Flies (Diptera: Tephritidae) spring vegetables. In Hawaii, where vegetables are  Vegetable Pests and their Management grown during the summer months, they also become numerous during the summer growing season. References Eggs are deposited in leaf tissue, in a slit cut by the female. One end of the egg protrudes Nishida T (1954) Further studies on the treatment of bor- slightly. The egg is colorless to pale white in color, der vegetation for melon fly control. J Econ Entomol and bean-shaped in form. Duration of the egg 47:226–229 Nishida T (1955) Natural enemies of the melon fly, Dacus stage is about 16 days at 15°C, 7.5 days at 26°C, and cucurbitae Coq. in Hawaii. J Econ Entomol 48:171–178 4.3 days at 32°C. Nishida T, Bess HA (1957) Studies on the ecology and control The larvae (sometimes called nymphs) resem- of the melon flyDacus (Strumeta) cucurbitae Coquillett ble the adults in form except for the lack of wings (Diptera: Tephritidae). Hawaii Agr Exp Stat Tech Bull 34:44 and smaller body size (Figs. 28 and 29). There are Vargas RI, Miyashita D, Nishida T (1984) Life history and two instars during the “larval” period. Larvae feed demographic parameters of three laboratory-reared gregariously, particularly along the leaf midrib and tephritids (Diptera: Tephritidae). Ann Entomol Soc Am veins, and usually on older leaves. Larval develop- 77:651–656 ment time is determined principally by the suitability of temperature, but host plant quality also has an influence. Larvae require about 14, 5, and 4 Melon Thrips, Thrips palmi Karny days to complete their development at 15, 26, and (Thysanoptera: Thripidae) 32°C, respectively. At the completion of the larval instars the insect usually descends to the soil or John L. Capinera leaf litter where it constructs a small earthen University of Florida, Gainesville, FL, USA chamber for a pupation site. There are two instars during the “pupal” Until the mid 1970s, the distribution of melon period. The prepupal and pupal instars are inac- thrips was limited to Southeast Asia. In recent tive, nonfeeding stages, although the insect years it has spread throughout Asia, and to many changes slightly in form at each molt. The prepu- Pacific Ocean islands, North Africa, Australia, pae and pupae resemble the adults and larvae in Central and South America, the Caribbean region form, except that they possess wing pads. The and southernmost mainland USA (Florida). It has wing pads of the pupae are longer than that of the the potential to infest greenhouse crops widely, prepupae. The combined prepupal and pupal but under field conditions likely will be limited to development time is about 12, 4, and 3 days at 15, tropical and subtropical areas. 26, and 32°C, respectively. Adults are pale yellow or whitish in color, lacking blotches of dark pigmentation but with Life History numerous dark setae on the body. The population is heavily weighted toward females. The slen- A complete generation may be completed in about der fringed wings are pale. The hairs or fringe on 20 days at 30°C, but it is lengthened to 80 days the anterior edge of the wing are considerably 2336 M Melon Thrips, Thrips palmi Karny (Thysanoptera: Thripidae) shorter that those on the posterior edge. Adults were more attractive to adults or suitable for sur- measure 0.8–1.0 mm in body length, with females vival and reproduction. averaging slightly larger than males. Unlike the In addition to direct injury, melon thrips are larvae, the adults tend to feed on young growth, capable of inflicting indirect injury by transmit- and so are found on new leaves. Adult longevity ting some strains of tomato spotted wilt virus and is 10–30 days for females and 7–20 days for males. bud necrosis virus. Development time varies with temperature, with mean values of about 20, 17, and 12 days at 15, 26, and 32°C. Females produce up to about 200 eggs, Management but average about 50 per female, which they deposit in leaf tissues in an incision made with To assess population density, nymphs and adults the ovipositor. Both mated and virgin females are collected from foliage. Adults tend to move deposit eggs. toward young foliage, with nymphs tending to be clustered on foliage inhabited by adults several days earlier. Adults can also be sampled with sticky Damage and water pan traps. Blue and white are attractive colors for thrips, and have been used to trap melon Melon thrips is a polyphagous species, but is best thrips. However, yellow has also been suggested to known as a pest of Cucurbitaceae and Solanaceae. be an attractive color. Among vegetables injured are bean, cabbage, can- Foliar insecticides are frequently applied for taloupe, chili, Chinese cabbage, cowpea, cucumber, thrips suppression, but at times it has been difficult bean, eggplant, lettuce, melon, okra, onion, pea, to attain effective suppression. Various foliar and pepper, potato, pumpkin, squash, tomato and drench treatments, alone or combined with oil, watermelon. Other crops infested include avocado, have achieved some success. The eggs, being in the carnation, chrysanthemum, citrus, cotton, hibiscus, foliar tissue, and the pupae, which reside in the soil, mango, peach, plum, soybean, tobacco, and others. are relatively insensitive to insecticide application. Melon thrips cause severe injury to infested Several cultural practices apparently affect plants. Leaves become yellow, white or brown, and melon thrips abundance. Physical barriers such as then crinkle and die. Terminal growth may be fine mesh and row cover material can be used to discolored, stunted, and deformed. Densities from restrict entry by thrips into greenhouses, and to 1 to 10 per cucumber leaf have been considered to reduce the rate of thrips settling on plants in the be the threshold for economic damage in some field. Organic mulch is thought to interfere with Japanese studies. However, studies in Hawaii sug- the colonization of crops by winged thrips. Plastic gested a damage threshold of 94 thrips per leaf mulch also is reported to limit population growth, early in the growth of the plant. Feeding usually but it is uncertain whether this is due to reduced occurs on foliage, but on pepper, a less suitable rates of invasion or denial of suitable pupation host, flowers are preferred to foliage. Because sites. Crop stubble is not an effective deterrent. The melon thrips prefer foliage, they are reported to be effects of intercropping potato with onion are vari- less damaging to cucumber fruit than western able. Although aphid and aphid-borne disease flower thrips,Frankliniella occidentalis (Pergande). incidence was decreased in such potato plantings, Nevertheless, fruits may also be damaged; scars, the density of thrips on potatoes was increased. deformities, and abortion are reported. In Hawaii, Thus, the benefits of such cropping practices are thrips were observed to attain higher densities on largely a function of which pests are likely to be cucumber plants infected with watermelon mosaic most important in an area. Heavy rainfall is virus, but it was not determined whether the plants thought to decrease thrips numbers. However, Melonworm, Diaphania hyalinata Linnaeus (Lepidoptera: Pyralidae) M 2337 there seems to be no evidence that overhead irri- areas where it cannot overwinter, so occurrence gation is an important factor in survival. in the cooler portions of its range is variable, Predation is often considered to be important depending on wind and favorable weather. in population regulation, and misuse of insecticides exacerbates thrips problems by killing predators. The predatory mite Neoseiulus cucumeris Life History (Oudemans) has been investigated for suppression of melon thrips. Mite density is correlated The melonworm can complete its life cycle in with thrips density, but within-plant distribution about 30 days. It is present throughout the year in differs among the two species, suggesting that warm locations, undergoing numerous genera- although the mites may increase in numerical tions annually, but has as few as one generation in abundance they are unlikely to drive the thrips to peripheral, invaded areas. extinction. Melonworm moths (Fig. 28) deposit oval, flattened eggs in small clusters, averaging 2–6 eggs per egg mass. Apparently they are deposited at References night on buds, stems, and the underside of leaves. Initially they are white, but soon become yellow in Capinera JL (2001) Handbook of vegetable pests. Academic color. They measure about 0.7 mm long and 0.6 Press, San Diego, CA, 729 pp mm wide. Hatching occurs after 3–4 days. Castineiras A, Baranowski RM, Glenn H (1996) Tempera- There are five instars. Total larval develop- ture response of two strains of Ceranisus menes (Hymenoptera: Eulophidae) reared on Thrips palmi ment time is about 14 days, with mean (range) (Thysanoptera: Thripidae). Fla Entomol 79:13–19 duration the instars about 2.2 (2–3), 2.2 (2–3), 2.0 Castineiras A, Baranowski RM, Glenn H (1997) Distribution (1–3), 2.0 (1–3), and 5.0 (3–8) days, respectively. of Neoseiulus cucumeris (Acarina: Phytoseiidae) and its Head capsule widths are about 0.22, 0.37, 0.62, prey, Thrips palmi (Thysanoptera: Thripidae), within eggplants in south Florida. Fla Entomol 80:211–217 1.04, and 1.64 mm, respectively. Larvae attain Castineiras A, Peña JE, Duncan R, Osborne L (1996) Potential lengths of about 1.5, 2.6, 4.5, 10, and 16 mm in of Beauveria bassiana and Paecilomyces fumosoroseus instars 1–5, respectively. Neonate larvae are color- (Deuteromycotina: Hyphomycetes) as biological control agents of Thrips palmi (Thysanoptera: Thripidae). less, but by the second instar larvae assume a pale Fla Entomol 79:458–461 yellow-green color. They construct a loose silken Girling DJ (ed) (1992) Thrips palmi. A literature survey with structure under leaves that serve to shelter them an annotated bibliography. International Institute of Biological Control, Silwood Park, Ascot, UK, p 37 Tsai JH, Yue B, Webb SE, Funderburk JE, Hsu HT (1995) Effects of host plant and temperature on growth and reproduction of Thrips palmi (Thysanoptera: Thripidae). Environ Entomol 24:1598–1603

Melonworm, Diaphania hyalinata Linnaeus (Lepidoptera: Pyralidae)

Melonworm is a tropical insect, and occurs throughout most of Central and South America and the Caribbean. It also occurs in some subtrop- Melonworm, Diaphania hyalinata Linnaeus ical locations, such as the southernmost United (Lepidoptera: Pyralidae), Figure 28 Adult States. Melonworm disperses readily, invading melonworm, Diaphania hyalinata Linnaeus. 2338 M Melonworm, Diaphania hyalinata Linnaeus (Lepidoptera: Pyralidae) Natural enemies of melonworm are nearly the same as those of pickleworm, and the parasitoids attacking pickleworm also attack melonworm: Apanteles sp., Hypomicrogaster diaphaniae (Muesebeck), Pristomerus spinator (Fabricius) (all Hymenoptera: Braconidae), Casinaria infesta (Cres- Melonworm, Diaphania hyalinata Linnaeus son), Temelucha sp. (both Hymenoptera: Ichneu- (Lepidoptera: Pyralidae), F igure 29 M ature larva monidae), and undetermined trichogrammatids of melonworm, Diaphania hyalinata Linnaeus. (Hymenoptera: Trichogrammatidae). However, additional species parasitize melonworm, including Gambrus ultimus (Cresson), Agathis texana (Cres- during the daylight hours. In the fifth instar, larvae son) (both Hymenoptera: Ichneumonidae) and an have two subdorsal white stripes extending the undetermined fly (Hymenoptera: Tachinidae). The length of the body. The stripes fade or disappear tachinids known from melonworm are Nemorilla just prior to pupation, but they are the most dis- pyste (Walker) and Stomatodexia cothurnata (Wie- tinctive characteristic of the larvae (Fig. 29). demann). Studies conducted in Puerto Rico Prior to pupation, larvae spin a loose cocoon reported levels of parasitism reaching 24%. Gener- on the host plant, often folding a section of the leaf alist predators such as Calosoma spp. and Harpalus for added shelter. The melonworm cocoon is much (both Coleoptera: Carabidae), the soldier beetle better formed than the cocoon of the co-occurring Chauliognathus pennsylvanicus DeGeer (Coleoptera: pickleworm, Diaphania nitidalis (Stoll), and the Cantharidae), and the red imported fire ant Solano- melonworm’s preference for green foliage as a psis invicta Buren (Hymenoptera: Formicidae) have pupation site also serves to differentiate these also been reported to be mortality factors. insects. The pupa is 12–15 mm in length, about 3–4 mm in width, and fairly pointed at each end. It is light to dark brown in color. The pupal stage Damage persists for 9–10 days. The moth’s wingspan is about 2.5 cm. The Melonworm feeds principally on leaf tissue, espe- wings are pearly white centrally, and slightly iri- cially if foliage of a favored host plant such as sum- descent, but are edged with a broad band of dark mer or winter squash is available. Usually the leaf brown. Moths frequently display brushy hair veins are left i ntact, resulting in lace-like plant pencils at the tip of the abdomen when at rest. remains. However, if the available foliage is Melonworm moths differ from pickleworm in that exhausted, or the plant is a less preferred species they remain in the crop during the daylight hours. such as cantaloupe, then the larva may feed on the While they are generally inactive during the day, surface of the fruit, or even burrow into the fruit. they will fly short distances when disturbed. As is the case with pickleworm, growers some- Melonworm is restricted to feeding on cucur- times refer to these insects as “rindworms” because bits; both wild and cultivated cucurbits may be they cause scars on the surface of melons. In a attacked. Summer squash and the winter squash study of melonworm damage potential to summer species are good hosts. Pumpkin is of variable squash conducted in south Florida, melonworm quality as a host, probably because pumpkins have caused a 23% yield loss due to foliage damage been bred from several Cucurbita species. The (indirect loss) and a 9–10% yield reduction due to Cucumis species, cucumber, gherkin, and canta- fruit damage (direct loss). loupe, are attacked but not preferred. Watermelon Historically, melonworm was considered to is almost never eaten. be a very damaging pest, but because it feeds Melyridae M 2339 preferentially on foliage it is easy to control with a Melsheimer, Frederick Valentine variety of insecticides. In tropical areas it often is considered more damaging than pickleworm. In Frederick Melsheimer was born on September 25, temperate areas, and especially in commercial 1749 at Regenborn, in the Duchy of Brunswick, vegetable production areas, it is treated as only a Germany. He attended the University of Helmstadt minor pest. In insecticide-free cucurbit produc- until 1776 when he was ordained and became a tion and in home gardens, melonworm can cause chaplain with a regiment of Hessian dragoons. serious damage. Soon afterwards he and his regiment were shipped to Quebec, Canada, and captured by American troops during the War of Independence. He Management remained in the United States after the war, and served as a Lutheran clergyman among the Ger- Monitoring the population of moths is difficult. man settlers of Pennsylvania. Melsheimer became The sex pheromone has been identified but is not a professor of languages at Franklin and Marshall available commercially. Moths are not attracted to College, and also served as its president. Melsheimer light traps. Thus, larval populations normally are pursued an interest in insects throughout his life, monitored. a source of amusement to his parishioners, Melonworm is easily suppressed with insecti- who considered it an eccentricity. Nevertheless, cides. Pollinators, particularly honeybees, are very Melsheimer made the first important collections important in cucurbit production, and insecticide and wrote the first important entomological work application can interfere with pollination by killing in the United States, “A catalogue of the insects of honeybees. If insecticides are to be applied when Pennsylvania” (1806). It remained the only publi- blossoms are present, it is advisable to use insecti- cation available on American insects for 25 years, cides with little residual activity, and to apply insec- until Thomas Say’s “American Entomology” was ticides late in the day, when honeybee activity is published. The “catalogue” considered only beetles, minimal. In addition to chemical insecticides, Bacil- and Melsheimer intended to publish additional lus thuringiensis is commonly recommended for tomes to treat other groups, but illness intervened. suppression, and this product does not kill bees. He died on June 30, 1824. Interestingly, two of Row covers can be used effectively to exclude Melsheimer’s children, John F. and Frederick Ernst, melonworm adults. Intercropping of corn and shared their father’s interest in insects and were beans with squash was shown to reduce damage avid collectors, with F.E. Melsheimer gaining by melonworm. Since melonworm prefers squash prominence as a coleopterist. to most other cucurbits, trap cropping has been suggested, and of course destruction of crop residue which may contain melonworm pupae is rec- Reference ommended. Early plantings, except in tropical areas where melonworm overwinters, often escape Mallis A (1971) American entomologists. Rutgers University serious damage. Press, New Brunswick, NJ, 549 pp

References Melyridae

Capinera JL (2001) Handbook of vegetable pests. Academic A family of beetles (order Coleoptera). They com- Press, San Diego, CA, 729 pp Smith RI (1911) Two important cantaloupe pests. NC Agr monly are known as soft-winged flower beetles. Exp Sta Bull 214:101–146  Beetles 2340 M Membracidae Membracidae Mentum

A family of insects in the order Hemiptera. They The distal section of the insect labrum, bearing the sometimes are called treehoppers. moveable parts; it is sometimes fused with the  Bugs submentum (Fig. 30).  Treehoppers  Mouthparts of Hexapods

Membrane Meridic Diet

The thin portion of the wing between wing veins. A diet that contains a chemically defined (holidic In the case of Hemiptera, the thinner, distal por- base), but which also contains one or a few poorly tion of the hemelytron. defined substances (e.g., leaf extracts). (contrast with holidic and oligidic diet).

Ménétriés, Edouard Meristem Edouard Ménétriés was born at Paris, France, on The cells capable of division located at the growing October 2, 1802. He was employed as conserver of point of a plant. rarities at the Zoological Museum in the Imperial Academy of Sciences, St. Petersburg, Russia. He was an authority on Lepidoptera and Coleoptera. He made extensive collections in Russia, Siberia, Meroistic Ovaries Alaska, and California. He died at St. Petersburg on April 10, 1861. Ovaries that have nurse cells associated with the oocytes. (contrast with panoistic ovaries).

Reference

Essig EO (1931) A history of entomology. Macmillan, New York, 1029 pp

Submentum

Mengenillidae Palpiger

Mentum A family of insects in the order Strepsiptera. Glossa  Stylopids Paraglossa

Palpus Menoponidae

A family of chewing lice (order Phthiraptera). Mentum, Figure 30 External aspect of the labium They sometimes are called poultry lice. in an adult grasshopper, showing some major  Chewing and Sucking Lice elements. Mesothorax M 2341

Antenna Meropeidae Labrum Clypeus Maxillary palpus Mandible 3 2 Tarsus Compound eye 1 A family of scorpionflies (order Mecoptera). They Tibia Pronotum commonly are known as earwigflies. Femur  Scorpionflies Trochanter Mesonotum Merothripidae Metanotum

A family of thrips (order Thysanoptera). They commonly are known as large-legged thrips.  Thrips

Genitalia Mesadene (pl., mesadenia) Cercus Mesonotum, Figure 31 Diagram of a webspinner Accessory glands of mesodermal origin found in showing the location of the wings relative to the the male reproductive system of some insects. thoracic segments. Note that the front wings are  Accesory Gland attached to the mesothorax (the upper surface of the mesothorax, or mesonotum, is labeled). The Mesenteron hind wings are attached to the metathorax (seen as metanotum).

Another name for the midgut. Mesopleuron

Mesepimeron The lateral surface of the mesothorax.

The epimeron of the mesothorax. Mesopsocidae

Mesepisternum A family of psocids (order Psocoptera).  Bark-Lice, Book-Lice or Psocids The sternum of the mesothorax or lateral extension of the mesothorax that meet dorsally Mesoscutellum in a ridge. The scutellum of the mesothorax; often simply Meson called the scutellum.  Thorax of Hexapods The mid-line of the body; an imaginary line separating the body into right and left halves. Mesothorax

Mesonotum The second or middle thoracic segment. The thoracic segment bearing the middle pair of legs. The The upper surface of the second or middle tho- thoracic segment bearing the first pair of wings racic ring (mesothorax) (Fig. 31). (Fig. 31).  Thorax of Hexapods  Thorax of Hexapods 2342 M Mesoveliidae Mesoveliidae de novo straight chain fatty acid biosynthesis which occurs at two different steps. The first one A family of bugs (order Hemiptera). They some- involves condensation with coenzyme A (CoA) to times are called water treaders. provide acetyl-CoA units, which are then con-  Bugs verted to malonyl-CoA by the multienzyme system called acetyl-CoA carboxylase. At the second step, both acetyl-CoA and malonyl-CoA are Messenger RNA (mRNA) required for long chain fatty acid synthesis through the multienzyme system of the cytosolic fatty acid RNA molecules which code for proteins and which synthetase (FAS) from the integument. Reaction are translated on the ribosomes. will usually proceed until a 16- or 17-carbon fatty acid is released as the end product, remaining as free fatty acid or incorporated into acylglycerols Metabolism of Insect Cuticular (Fig. 33). Aphids are unusual in this regard, with Lipids C14:0 as the major fatty acid due to the presence of an active thioesterase. Exogenous fatty acids of M. Patricia Juárez 16 and 18 carbons are incorporated into acylglyc- University of La Plata, La Plata, Argentina erols and phospholipids. Most of the cuticular lipids are biosynthetically related. Insect cuticular lipids, also called cuticular waxes, One or more malonyl-CoA units might be consist of a complex mixture of very long chain replaced by methylmalonyl-CoA during fatty acid compounds with low reactivity and rather high formation, leading to the formation of methyl- melting point. They provide a variety of functions branched fatty acyl precursors. An integumental ranging from water-proofing properties to chemi- microsomal FAS is involved in these reactions, as cal cues (sexual attractants, deterrents, defensive shown in the German cockroach Blatella german- secretions, kairomones), as well as barrier against ica, the housefly Musca domestica, and the assassin microbial or chemical penetration. Among the bug Triatoma infestans. Endogenously produced most usual and major lipid components of the epi- fatty acids serve as primers for microsomal elonga- cuticle are hydrocarbons, fatty alcohols, wax esters, tion and or desaturation reactions, prior activation and free fatty acids. They have been reported for as the fatty acyl-CoA derivative by the action of more than a hundred species. Minor components fatty acyl-CoA synthetases, as shown in the cock- include ketones, aldehydes, acetate esters, sterol roaches B. germanica and Periplaneta americana. esters, and less frequently, acylglycerols. Different There is now overwhelming evidence that insects chain length, branching pattern, substitution, and synthesize hydrocarbons and other cuticular wax or unsaturation, determine characteristic blends components from fatty acids, in a pathway similar for different orders, although their relative amounts to that postulated by Kolattukudy and co-work- depend on a variety of internal and external factors: ers in plants in 1976. The reaction occurs through developmental stage, sex, feeding status, reproduc- chain elongation by the action of fatty acyl-CoA tion cycle, etc (Fig. 32). elongases producing very long chain fatty acyl Unique metabolic pathways for the epicuticu- (VLCFA) moieties that are finally converted to lar lipids have been disclosed in the last 20 years, hydrocarbons one carbon shorter, rendering mostly mostly by Blomquist and co-workers. Depending odd-numbered straight chain hydrocarbons. on the diet, a short chain amino acid, glucose, or The major endogenous mono-unsaturated fatty acids will be converted to acetate – the build- or di-unsaturated fatty acids, rather than newly ing block of two-carbon units – in order to initiate synthesized unsaturated chains, were suggested Metabolism of Insect Cuticular Lipids M 2343 Nonacosane

9,15,19-trimethylnonacosane C 18

Octacosanol C-OH

Palmitoyl tetracosanoate O

O Oleic acid

OH O Metabolism of Insect Cuticular Lipids, Figure 32 Representative straight and methyl-branched insect cuticular lipids.

Acetyl-CoA + malonyl-CoA

Fatty acid NADPH synthetase Fatty acid elongase(s) Palmitoyl-CoA Very Long Chain Fatty Acyl CoA

NADPH Acyl-CoA reductase NADPH

Fatty aldehyde Aldehyde reductase CO2 Cytocrome P-450 (hyd) NADPH + O2 Primary Fatty alcohol Hydrocarbon

Secondary Fatty alcohol

Ketone Metabolism of Insect Cuticular Lipids, Figure 33 Biosynthesis of insect cuticular lipids. to be the precursor for multi-methylene inter- acyl-CoA reductase. Finally, a microsomal cyto- rupted alkadiene, and no reports on desaturase chrome P-450 type enzyme releases CO2 to yield activity in the integument are available. After- odd-chained alkanes. This step was shown in wards, chain elongation reactions will proceed as M. domestica, the house cricket Acheta domesticus, described above. The VLCFA precursors are con- the dampwood termite Zootermopsis nevadensis, verted into aldehyde intermediates by a fatty and B. germanica, among others. 2344 M Metabolism of Insect Cuticular Lipids Methyl-branched hydrocarbons are abun- determined? One of the most powerful and dant in a large number of insect species. They worldwide accepted methodologies is to employ arise through a modification of the straight-chain radioactive (labeled) tracer molecules of the same pathway described above. Methyl branches or similar structure than the putative precursor, located on carbon 3 or greater originate from containing labeled isotopes, usually 13C-, 2H-, 3H-, propionate in the form of methylmalonyl-CoA, 14C-or 32P with the label located at specific posi- which replaces one or more malonyl-CoA units tions helps to follow the biosynthetic pathways during early fatty acid synthesis leading to the both by in vivo and in vitro techniques. The most formation of internally-branched methyl-alkanes, simple in vivo experiments are performed by multiple-methyl-branched alkanes and 3-methy- injecting an appropriate fatty acid precursor (i.e., lalkanes. An integumental microsomal FAS is the labeled acetate) to a certain number of insects of major enzyme responsible for methyl-branched the target species, following the transport of fatty acid formation, whereas the cytosolic integ- labeled lipids into the cuticle at selected time inter- umental FAS shows less activity. Alkanes can then vals. Then, lipids might be washed off from the undergo sequential oxidations by cytochrome epicuticular surface (or those from the whole P-450 oxidation to form secondary alcohols integument by a previous dissection) by solvent and ketones, as shown by the conversion of extraction. After concentration and preliminary 3,11-dimethylnonacosane into 3,11-dimethyl- fractionation, information on the total amount nonacosan-2-one, the contact sexual pheromone and classes of lipids formed is usually obtained in B. germanica. employing various kinds of radioactive detectors Fatty alcohol biosynthesis has been scarcely and methods, i.e., by liquid scintillation counting addressed, but the action of an aldehyde reductase (LSC) to determine the total amount of metabo- was proposed in Manduca sexta for the conver- lites produced in the experimental conditions of sion of the appropriate very long chain aldehyde an assay, and by radio-thin layer chromatography into the corresponding even-chain primary fatty (radio-TLC) to determine the kind of lipid classes alcohol. Primary alcohols can then be combined produced. After fractionation, and sometimes with free fatty acids to form wax esters. Cell frac- derivatization in order to facilitate detector tionation studies have shown that many of the response, radio-high performance liquid chroma- enzyme activities of wax biosynthesis are located tography (radio-HPLC) and radio-gas chroma- in the microsomal fraction. Other than FASs, the tography (radio-GC) are widely used to provide a wax biosynthetic pathway is composed of various preliminary identification of the intermediates enzyme activities; fatty acid elongase, acyl-CoA and end products of the biosynthetic process reductase, aldehyde reductase and wax synthase. under study. Final identification and structure The relative activities of the enzymes determine assignment require the use of more sophisticated the chain lengths of the waxes found in the cuticle. techniques such as capillary gas chromatography- However, very little is known about the enzymes mass spectrometry (CGC/MS), HPLC/MS, and of these biosynthetic pathways, the regulation of nuclear magnetic resonance (NMR). Enzyme wax production, and the secretion of wax compo- studies might be carried out employing appropri- nents onto the surface of the insect. ate label tracers and/or by spectrophotometric measurements for preliminary characterization. Studies on enzyme location, purification, cofactors Methodology required, kinetic parameters and, regulation are carried out by more complex studies including How can these reactions be followed up, the HPLC purification, molecular mass determina- enzymes involved, and metabolite production tion, amino acid sequence, electronic microscopy, Metalmark Butterflies (Lepidoptera: Riodinidae) M 2345 immunofluorescent assays, protein purification Metalmark Butterflies and characterization in addition to the previously (Lepidoptera: Riodinidae) mentioned techniques. Furthermore, if isolation of genes encoding the target enzyme and insertion Jason P. W. Hall in an appropriate vector are feasible, the overex- National Museum of Natural History, pression of such enzyme in an appropriate system Smithsonian Institution, Washington, DC, USA can increase the quantity of intermediate precursors, i.e., very long chain fatty acids, and thus This is one of the five families of “true” butterflies increase the substrates available to study wax for- (in the superfamily Papilionoidea). Recent mor- mation (Figs. 32 and 33). phological and molecular evidence, for the first time based on sufficient taxon sampling, indicates the Riodinidae to be the sister group to the References Lycaenidae (blues, coppers and hairstreaks). Based on the only confirmed riodinid fossils, ofNapaeina and Nymphidiini species in Dominican amber, the Blomquist GJ, Nelson DR, de Renobales M (1987) Chemistry, biochemistry and physiology of insect cuticular lipids. family is at least 25 million years old. The higher Arch Insect Biochem Physiol 6:227–265 classification of the Riodinidae is now relatively Blomquist GJ, Tillman-Wall JA, Guo L, Quilici DR, Gu P, Schal well resolved, and the group is currently divided C (1993) Hydrocarbon and hydrocarbon derived sex into three subfamilies, twelve tribes and six pheromone in insects: Biochemistry and endocrine regulation. In: Stanley-Samuelson DW, Nelson DR (eds) Insect subtribes, with only one incertae sedis section of lipids. Chemistry, biochemistry and physiology. Univer- unplaced riodinine genera still remaining. How- sity of Nebraska Press, Lincoln, Nebraska, pp 317–351 ever, intertribal relationships in the largest sub- Juárez MP, Chase J, Blomquist GJ (1992) A microsomal fatty acid synthetase from the integument of Blatella ger- family, the Riodininae, are poorly understood. manica synthesizes methyl-branched fatty acids, pre- Order: Lepidoptera cursor to hydrocarbons and contact sex pheromone. Superfamily: Papilionoidea Arch Biochem Biophys 293:333–341 Family: Riodinidae Grote Buckner JS (1993) Cuticular polar lipids of insects. In: Stanley- Samuelson DW, Nelson DR (eds) Insect lipids. Chemistry, Subfamily: Nemeobiinae Bates biochemistry and physiology. University of Nebraska Nemeobiini Bates Press, Lincoln, Nebraska, pp 227–270 Zemerini Stichel Kolattukudy PE, Croteau R, Buckner JS (1976) Biochemistry Abisarini Stichel of plant waxes. In: Kolattukudy PE (ed) Chemistry and biochemistry of natural waxes. Amsterdam Elsevier Subfamily: Euselasiinae Kirby North Holland, pp 289–347 Corrachiini Stichel Euselasiini Kirby Subfamily: Riodininae Grote Metallic Wood-Boring Beetles Mesosemiini Bates Mesosemiina Bates Members of the family Buprestidae (order Napaeina Hall Coleoptera). Eurybiini Reuter  Beetles Riodinini Grote Stalachtini Bates Helicopini Metallyticidae Symmachiini incertae sedis of Harvey A family of praying mantids (Mantodea). Nymphidiini Bates  Praying Mantids Aricorina Hall & Harvey 2346 M Metalmark Butterflies (Lepidoptera: Riodinidae) Lemoniadina Kirby more obvious alar organs, the family can reason- Theopeina Clench ably be described as exhibiting among the great- Nymphidiina Bates est morphological diversity of androconial organs in the butterflies. Morphology Diversity and Biogeography The Riodinidae present perhaps the most kaleido- scopic array of colors, patterns, shapes and sizes The Riodinidae contain about 1,350 species, only a of any butterfly family. Many have metallic silver few of which remain undescribed. The family has or gold markings, hence their common name of a worldwide distribution, but it is unique among metalmarks. They are generally rather small and the butterflies in being almost exclusively confined range in size from about 12–60 mm. The only dis- to a single biogeographic region, the Neotropics, tinguishing characteristic of the Riodinidae that is where approximately 95% of the familial diversity visible to the naked eye is their greatly shortened occurs. Riodinid diversity peaks in the lowlands of male forelegs, which are no longer used for walk- the Amazon basin, where as many as 400 species ing. Although the Nymphalidae share this charac- can be found in a single heterogeneous locality, ter, Riodinidae additionally have a coxa on the constituting more than 20% of the local butterfly male foreleg that extends as a spine-like projection fauna (including Hesperiidae). Species richness in below the trochanter (a character only weakly Central America is roughly half that of Amazonia, developed in the two species of Corrachiini, and and only two dozen species extend northwards also quite well developed in various poritiine and into North America. Species richness also tapers curetine lycaenids), trichoid sensilla on the female off gradually with increasing elevation, and very foretarsal segments that are clustered into single few species occur above 2,000 m. instead of medially divided patches, and no poste- On average, riodinids have smaller geographic rior apophyses extending anteriorly from the ovi- ranges than their close relatives the lycaenids, and positor lobes of the female genitalia. this makes them ideal subjects for biogeographic Although their external morphology is com- study. Detritivora Hall & Harvey, a genus of small, paratively uniform (Fig. 34), the male and female drab, forest-dwelling riodinines, provides perhaps genitalia exhibit a remarkable diversity of form the most extreme example in the Lepidoptera of given the relatively small size of the family. The a continuously distributed lowland group with most comprehensive set of drawings of venation, highly fragmented species ranges. The D. cleonus palpi, legs and genitalia is still that of Stichel group is divided into an incredible nineteen parap- (1910–1911). Although androconia, specialized atrically distributed species across Amazonia, each male secondary-sexual scales, have historically occupying a variably small area of endemism. A been thought to be rare in the Riodinidae, espe- cladogram of these riodinids, superimposed over a cially, for example, compared to the Lycaenidae, a map of their distributions, led to the most detailed recent comprehensive study found that at least hypothesis yet of Amazonian area relationships. 25% of riodinid species possess a wide morphological array of them. Because the Riodinidae are now known to have abdominal coremata (similar Adult Ecology to those of danaine nymphalids), concealed internal and visible external abdominal androconia, Riodinids are found in a wide variety of primary genital brush organs and hind leg hairpencils and secondary habitats, from dry Acacia scrub to (unique within the Papilionoidea), as well as the pluvial forest, but most are exclusive denizens of Metalmark Butterflies (Lepidoptera: Riodinidae) M 2347

Metalmark Butterflies (Lepidoptera: Riodinidae), Figure 34 Adult riodinids. A. Neotaxila thuisto Hewitson “male” (Nemeobiinae, Nemeobiini). B. Euselasia labdacus Stoll (Euselasiinae, Euselasiini). C. Hermathena candidata Hewitson (Riodininae, Mesosemiini, Napaeina). D. Perophthalma lasus Westwood “male” (Riodininae, Mesosemiini, Mesosemiina). E. Alesa amesis Cramer “male” (Riodininae, Eurybiini). F. Chorinea batesii Saunders (Riodininae, Riodinini). G. Baeotis sulphurea R. Felder (Riodininae, Riodinini). H. Calydna calamisa Hewitson “male” (Riodininae, incertae sedis of Harvey). I. Helicopis gnidus Fabricius (Riodininae, Helicopini). J. Synargis fenestrella Lathy (Riodininae, Nymphidiini.) K. Symmachia suevia Hewitson (Riodininae, Symmachiini). L. Stalachtis phaedusa Hübner (Riodininae, Stalachtini). primary rainforest. Most species are very localized Mimicry is perhaps more rampant in the in time and space. Years of observations in an area Riodinidae, especially in females, than in any usually result in finding only one or two places other butterfly family in terms of the diversity of where a particular species occurs and even then taxa that its species mimic. There are tiger striped the species will most likely only be present for a riodinids that resemble papilionids, pierids and couple of hours a day, and perhaps only during cer- various nymphalid subfamilies, clear-winged tain months of the year. It is not surprising then species that seem to mimic ithomiine nympha- that so many riodinids are very rare in collections. lids and dioptine and arctiine moths, and gaudy Intergeneric and interspecific differences in male blue, red, orange, or yellow patterned species riodinid perching behavior, involving variably that seem to be mimicking dioptine, arctiine, sized groups of males resting at characteristic sites geometrid and tortricid moths. Such riodinids and investigating passing butterflies in search of also mimic the same flight behavior of the pre- conspecific females, can be explained these differ- sumed model(s), often even holding the anten- ences in the context of premating isolating mecha- nae at the same angle. Most of these mimetic nisms. Such perching behavior, better known in relationships are probably Batesian, with moths birds, is known as lekking, a word derived from the generally being the unpalatable models, but we Swedish verb “leka,” meaning “to play.” Male rio- know essentially nothing about the palatability dinids most frequently lek along forest edges, of mimetic riodinids. streamsides, and especially on ridgetops and hill- Like other butterflies, riodinids can be found tops, where they may use the same patch of vegeta- feeding on flowers, or imbibing nutrients and ions tion year after year, arriving from the surrounding from damp sand or mud (known as puddling). forest and departing at roughly the same time every However, carrion is the most frequently recorded day, and always resting on leaves or tree trunks at food source, both in terms of number of individu- about the same height above the ground. als and taxa. This behavior is common elsewhere 2348 M Metalmark Butterflies (Lepidoptera: Riodinidae) in butterflies only in certain subfamilies of the Although this phenomenon is very widespread Nymphalidae and Lycaenidae. There is also a cor- in the Lycaenidae, only about one quarter of the relation between food substrate choice and wing Riodinidae are myrmecophilous, encompassing area to thoracic volume ratio in male riodinids, the tribes Eurybiini and Nymphidiini. Myrmeco- with puddlers and carrion feeders having lower philous larvae possess a suite of “ant-organs” that such ratios (i.e., relatively larger thoraces for their facilitate their interactions with ants. Tube-like overall size). These feeding behaviors are believed paired tentacle nectary organs (TNOs) on abdom- to supplement nutrient stores from larval feeding inal segment eight, which secrete nutritionally rich to increase reproductive success and provide the droplets to be harvested by ants, are present in necessary nutrients to maintain high metabolic both tribes, but a further two “ant-organs” are rates during rapid flight. restricted to the Nymphidiini. Setose paired anterior tentacle organs (ATOs) on thoracic segment three appear to influence ant behavior through the Immature Stages and use of semiochemicals, and a pair of stridulatory Myrmecophily rod-like appendages on the first thoracic segment, termed vibratory papillae, grate against granula- The early stages of the Riodinidae remain proba- tions on the head as it moves in and out to pro- bly the most poorly known of all the butterfly duce an acoustical call that is thought to function families and only a small fraction of the genera in attracting ants. The function of bladder or bal- have been reared, making the immatures a fertile loon setae, a corona of inflated setae on the first field for further study. Riodinid eggs are generally thoracic segment which also occur in the non- laid singly, but in certain groups, such as the Euse- myrmecophilous Helicopini and incertae sedis lasiinae, they are often laid in clusters, resulting in section, is still unclear, but, at least in the Nymphi- gregarious groups of often aposematic larvae. diini, they may release an ant alarm pheromone Riodinid eggs are remarkably diverse in form analogue, when squeezed by an ant, to confer pro- compared to those of the Lycaenidae, in anthro- tection on the caterpillar. pomorphic terms resembling crowns, pies, cakes, Riodinids are known to feed on over forty cones, footballs, automobile tires and more. Those families of flowering plants, using leaves, extraflo- larvae that have symbiotic relationships with ants ral nectaries and, more rarely, flower parts, but are tend to be smooth, whereas those that are non- of little economic importance. Certain members myrmecophilous are generally hairy. Riodinid of the Euselasiinae feed on harvested myrtaceous pupae are generally smoothly cylindrical, girdled, plants such as guava, and some Napaeina species and best distinguished from those of other but- can be pests on ornamental Neotropical bromeli- terflies by their broadly flattened cremaster. Some ads and orchids. Aphytophagy, or feeding on non- pupae have spines, others are moth-like cocoons plant material such as ants or their regurgitations, made from the shed larval setae, and those of or on hemipterans and their secretions, is rare in Eurybia Illiger are extraordinary in having an the Lepidoptera and in butterflies also present elongate spine-like posterior projection almost as only in the Lycaenidae (e.g., Liphyrinae, Polyom- long as the remainder of the pupa to enclose the matinae and Miletinae) and “Riodinidae (Eury- very long proboscis. biini and Nymphidiini). Although aphytophagy Myrmecophily, or the ability of butterfly cat- has only been unequivocally documented for two erpillars to form symbioses with ants by providing riodinid species, there is evidence to suggest that food secretions in exchange primarily for protec- this phenomenon is significantly more common tion from arthropod predators, is almost entirely in the family. confined to the Lycaenidae and Riodinidae.  Butterflies and Moths Metalmark Moths (Lepidoptera: Choreutidae) M 2349 References

Callaghan CJ (1983) A study of isolating mechanisms among Neotropical butterflies of the subfamily Riodininae. J Res Lepid 21:159–176 DeVries PJ (1997) The butterflies of Costa Rica and their natural history, vol 2: Riodinidae. Princeton University Press, Princeton, NJ, 288 pp Hall JPW, Harvey DJ (2002) A survey of androconial organs in the Riodinidae (Lepidoptera). Zool J Linn Soc 136:171–197 Hall JPW, Harvey DJ (2002) The phylogeography of Amazo- nia revisited: new evidence from riodinid butterflies. Evolution 56:1489–1497 Hall JPW, Willmott KR (2000) Patterns of feeding behav- Metalmark Moths (Lepidoptera: Cho reutidae), iour in adult male riodinid butterflies and their rela- Figure 35 Example of metalmark moths tionship to morphology and ecology. Biol J Linn Soc (Choreutidae), Saptha beryllitis (Meyrick) from 69:1–23 Taiwan. Stichel HFEJ (1910–1911) Lepidoptera Rhopalocera. Fam. Riodinidae. In: Genera insectorum, vol 112. J. Wytsman, Brussels, Belgium, 452 pp are diurnal; usually near their host plants and tend to hop about on leaves. Larvae mostly leaf skeletonizers, but some are budworms; rarely Metalmark Moths (Lepidoptera: leafminers (Millieriinae). Cocoons are white and Choreutidae) spindle-shaped. Numerous hostplant families are recorded, but many in Compositae and Moraceae. John B. Heppner The subfamily Millieriinae and nominate genus Florida State Collection of Arthropods, Millieria are named after the French lepidopterist Gainesville, FL, USA Pierre Millière (1811–1887).

Metalmark moths, family Choreutidae, comprise 418 species worldwide, in three subfamilies (in References the past incorrectly included in Glyphipterigi- dae); actual world fauna probably exceeds 800 Arita Y, Diakonoff AN (1979) A survey of the Japanese species species. There are three subfamilies: Millieriinae, of Anthophila Haworth and Eutromula Froelich and their early stages (Lepidoptera, Choreutidae), with an Brenthiinae, and Choreutinae. The family is in appendix. Zool Verhandlingen 166:1–42 the superfamily Sesioidea in the section Tineina, Diakonoff AN (1986) Glyphipterigidae auctorum sensu lato. subsection Sesiina, of the division Ditrysia. (Glyphipterygidae sensu Meyrick, 1913). In Amsel HG et al. (eds) Microlepidoptera Palaearctica, vol 7. Adults small (7–24 mm wingspan), with head G. Braun, Karlsruhe. 2 pts. 436pp, 175 pl mostly smooth-scaled; haustellum scaled; labial Heppner JB (1981) Family Choreutidae, pp 45–58. In: palpi often with a scale tuft on second segment; Heppner JB, Duckworth WD (eds) Classification of maxillary palpi 1 to 2-segmented. Forewings the superfamily Sesioidea (Lepidoptera: Ditrysia). Smithson Contrib Zool 314:1–144 somewhat elongate or more triangular (Fig. 35). Heppner JB (1982) Millieriinae, a new subfamily of Choreuti- Maculation variable but usually with brilliant dae, with new taxa from Chile and the United States metallic-iridescent spots or marks; sometimes (Lepidoptera: Sesioidea). Smithson Contrib Zool more colorful markings, or subdued in a few spe- 370:1–27 Heppner JB (2004) Metalmark moths of North America cies. Hindwings colorful or dark, and often with a (Lepidoptera: Choreutidae). Scientific Publishers, light band near termen; sometimes pale. Adults Gainesville, FL 2350 M Metamorphosis Metamorphosis functional wings, genitalia and internal changes that accompany sexual maturation. These insects Judith H. Willis, John S. Willis have larval wings, which though small and University of Georgia, Athens, GA, USA non-functional, are visible as pads on the thorax. Such insects are called exopterygotes because of Insects are the only invertebrates that fly. The these external wings. development of a winged form is the culmination In insects with complete metamorphosis of metamorphosis that converts a larva capable (holometabolous development), there is a dra- only of moving by squirming, crawling or swim- matic change in appearance, physiology and ming into a flying machine. behavior between larvae and adults, and a physi- Issues of interest in insect metamorphosis ologically and morphologically distinct stage, the include its evolutionary origin, the source of adult pupa, has been inserted between the final larval structures, hormonal control, and the identity of instar and the adult. Available evidence indicates genes that regulate metamorphosis and code for that there was a common ancestor for all of the proteins that form the structures of the different holometabolous insects. These include the orders, metamorphic stages. Diptera (flies), Hymenoptera (bees and wasps), Coleoptera (beetles) and Lepidoptera (butterflies and moths). Such holometabolous insects account Evolution for about 90% of all insect species. Their success is due presumably to their ability to exploit radi- Among the orders of insects, patterns of cellular cally different environmental resources at differ- participation in metamorphosis vary from the ent stages in their lives. simplest case, adults only slightly different from larvae, their structures having arisen from the same cells, to the most advanced in which differ- Morphology and Physiology entiated larval cells in effect commit suicide and are replaced by new cells arising from undifferen- The morphological changes in an individual that tiated precursors. By examining insects in differ- accompany metamorphosis can be created in one ent orders we can get an idea of how metamorphosis of two ways: First, a single lineage of cells can form may have evolved from simple to complex. larval, then pupal and finally adult structures. Sec- A few “primitive” insects do not undergo ond, change may involve the death of most of the metamorphosis (are ametabolous) and hence cells of the larva and their replacement by the are flightless. Thysanura (silverfish), for example, proliferation and differentiation of clusters of “stem hatch from the egg looking much like the adult, cells”. An example of the first type, persistence of and only undergo subtle anatomical changes cells throughout the life of an insect, is the abdomi- between molts. They never develop wings and con- nal epidermis of lepidopteran larvae. Here a single tinue to molt as sexually mature adults (Fig. 37). row of epithelial cells secretes first the cuticle of Incomplete metamorphosis (or hemimetab- each larval stage, then switches and forms a pupal olous development) is found in Blattodea (cock- cuticle, and finally, accompanied by special differ- roaches), Orthoptera (grasshoppers), Hemiptera entiative cell divisions forms the scales and sockets (bugs) and others. Here the larval and adult and background cuticle of the adult. forms are also similar. After several molts from The second type of change involves groups one larval stage (called instar) to the next, major of cells that contribute little or nothing to larvae, changes appear at the final molt from larva but are used to build the pupa and adult. An to adult. These include the development of example of the second type is seen in wing Metamorphosis M 2351 development. The cells that will contribute to the lost. Flight muscles develop and the nervous sys- wings of holometabolous insects are present as tem is rewired to accommodate this. Some neu- imaginal discs in larvae. Imaginal discs are rons die; others develop from neuroblasts; while infoldings of the single layer of cells that consti- others change their outgrowths, (axons and den- tute the surface epithelium. Once formed, they drites) to connect with new targets. do not contribute to the external structure of the larva but evaginate to the surface at pupation, forming first pupal and then adult cuticle. Insects Hormonal Control with such hidden, undifferentiated larval wings are also called endopterygotes, a synonym for There is far less variation in the hormonal con- holometabolous insects. trol of metamorphosis than in the morphological Imaginal discs are found in all holometab- changes themselves and the cellular events that ola, but arise in various ways. They first appear underlie them. Essentially two classes of hor- during late embryonic development of some mones (ecdysteroids and juvenoids) are involved, insects like the higher Diptera, and only shortly and the same mechanisms of metamorphic con- before pupation in others like some Coleoptera. trols apply to both hemi- and holo-metabolous In the former case, they are attached to the sur- insects (Fig. 36). Briefly, ecdysteroids make face epithelium by a thin stalk; in the latter they insects molt. Juvenoids determine what they are no more than a thickening of the epidermis. molt into. When juvenoids are absent at a criti- In some insects, imaginal discs are only used as cal period early in a molt cycle, the cells respond the source of a few adult structures, in others to ecdysteroids by forming the structures of the there are discs for all of the adult structures. In next metamorphic stage instead of making some cases, a few cells at the base of a larval another larval instar. In this case, unimpeded structure, legs, antennae etc. may proliferate at by juvenoids, ecdysteroids also cause meta- pupation and be the exclusive source of the cor- morphosis. Final instar hemipteran or lepi- responding pupal and adult structures. In the dopteran larvae that receive an extra dose of Drosophila abdomen, there are small clusters of juvenoids by injection or by implanting active diploid cells, histoblasts that lie amidst the poly- corpora allata (the glands that make juvenoids) ploid larval cells. Both types of cells secrete lar- will molt into a giant extra instar larva rather val and pupal cuticles. Then larval cells die, the than undergoing a metamorphic molt (to adult histoblasts proliferate and spread to form the in the hemipteran or to pupa in the lepi- adult abdomen. dopteran). If a lepidopteran pupa receives excess In addition to the creation of these morpho- juvenoids, it will molt into another pupa, some- logical structures definitive for the pupa and thing not seen in nature. This action of juvenoids adult, complex changes also occur in the internal results in their being recognized as “status quo” organs in the transition from larva to adult. As hormones, for they direct the repetition of the the food source changes in many cases from pattern of syntheses necessary to reform the leaves to nectar, changes occur in the mouthparts characteristics of the previous stage. from munching via strong mandibles to sipping In the hornworm Manduca sexta, when a crit- via an extensible proboscis. Accompanying these ical larval size is reached, it has a metamorphic changes in food source are changes in appear- molt. Thus size is in some sense the signal that the ance and physiology of the digestive system. Dif- time has come for metamorphosis. The signal to ferent enzymes are needed to handle different undergo metamorphosis causes the corpora allata food sources. In lepidopterans, the abdominal to cease making juvenoids and other tissues to prolegs and their muscles, useful in walking, are synthesize enzymes that metabolize and inactive 2352 M Metamorphosis

Ecdysis Ecdysis Ecdysis Ecdysis

JH Ecdysteroids

01 2340 1 23456780 5 10 15 19 DAYS 4th 5th Pharate Pupa Developing adult Adult pupa Metamorphosis, Figure 36 Diagram of the titers of ecdysteroids and juvenoids (JH) in Manduca during the final two larval instars, the pharate pupa, pupa, and developing (pharate) adult. The time at which ecdysis to the next stage occurs is also shown. (Adapted from Riddiford in “Metamorphosis/ post-embryonic reprogramming of gene expression in amphibian and insect cells.” Reprinted with permission of Cambridge University Press.)

juvenoids. The mechanism of how size is measured they initiate the larval/pupal molt, but it is not and the nature of the metamorphic signal in other expressed at larval/larval molts. A gene with a simi- insects remain unknown. lar sequence is expressed in Manduca larvae in the There are exceptions to these findings. Dros- same manner, at the larva/pupal molt, but not at ophila larval tissues, except for the histoblasts, are larval/larval molts. In Manduca, juvenoids prevent insensitive to the antimetamorphic actions of the activation of broad, in keeping with their status juvenoids. Some larvae continue to grow rather quo action. than have an extra larval instar in the presence of excess juvenoids, and not all pupae or all pupal tissues can be induced to molt again to a pupa. Effector Genes

Also of interest are the genes that code for pro- Genes and Metamorphosis teins that contribute directly to the form and function of the morphologically distinct meta- Regulatory Genes morphic stages of the holometabolous insects. These can be structural proteins, such as cuticular Ecdysteroids initiate a cascade of gene activity that proteins, or enzymes that participate in physio- involves both early and late genes. Most of these logical activities such as digestion and intermedi- genes code for transcription factors that activate a ary metabolism, or even enzymes necessary for series of genes for the proteins that build the struc- the formation of pigments found in different tures of the various stages. Thus flies, mosquitoes, stages. Analyses of cuticular proteins and their beetles and moths have homologous genes that are genes revealed that quite different structures activated in the same order in response to ecdys- could be built from the same cuticular compo- teroids, although the culmination of their action is nents. Thus, the hard structures found in lepi- to build very different kinds of insects. One goal dopteran larvae, the head capsule and tubercles, has been to identify early ecdysteroid-response that dot the thorax and abdomen, are composed genes whose activities differ between larval and of the same cuticular proteins that contribute to metamorphic molts. One such gene, named broad, the hard cuticles of the pupa that cover most has been found. It was first discovered inDrosophila of the body surface, the pupal dorsal-fore wing where it is expressed in response to ecdysteroids as and the abdominal sclerites. The soft cuticles Metamorphosis M 2353

Metamorphosis, Figure 37 Three types of development in insects. Left, ametabolous development illustrated by Machlis (Thysanura). Note that there is little change in external form, and the adults continue to molt. Center, hemimetabolous development illustrated by Rhodnius (Hemiptera). There are five nymphal (larval) instars, and wing pads are clearly visible in the later ones. Only the adult has functional wings and is capable of reproduction. Right, holometabolous development illustrated by the moth Manduca (Lepidoptera). Wings in the larva are not visible, as their precursors exist internally as imaginal discs. Both pupae and adults have wings, but they are only functional in the adult. (adapted from H. E. Evans, Insect Biology) found across the larval abdomen and in the modified genes to code for those features that are intersegmental membranes of pupae and adults unique to each metamorphic stage. also share many of the same cuticular proteins. In It is the complex orchestration of spatial and these cases, the same genes are reused to code for temporal activities of similar hormones and genes the structural proteins of vastly different morpho- that results in the vast diversity of form and func- logical structures. The evolution of metamorpho- tion that is displayed by metamorphosing insects. sis thus required the development of new  Juvenile Hormone morphogenetic signals (architectural plans)  Ecdysteroids affecting the spatial and temporal expression of  Diapause different genes, so that common structural pro-  Howard Schneiderman teins could be assembled in new ways. Accompa-  Carroll Williams nying this was also the appearance of new or  Vincent Wigglesworth 2354 M Metanotum References groups, and population genetics analysis, Metarhiz- ium may be represented by a large number of spe- Nijhout HF (1994) Insect hormones. Princeton University cies found worldwide. Thus, the taxonomy and Press, Princeton, NJ, 267 pp systematics of this genus are not fully resolved. Pop- Truman JW, Riddiford LM (2002) Endocrine insights into the evolution of metamorphosis in insects. Ann Rev Ento- ulation genetics analysis showed that in nature mol 47:467–500 Metarhizium reproduces clonally but also has the Willis JH (1996) Metamorphosis of the cuticle, its proteins, potential for recombination. Recombination may and their genes. In: Gilbert LI, Atkinson BG, Tata J (eds) Metamorphosis/post-embryonic reprogram- occur through a process called parasexuality, a form ming of gene expression in amphibian and insect cells. of mitotic recombination, where vegetatively com- Academic Press, Orlando, FL, pp 253–282 patible hyphae fuse and exchange nuclei to form a Zhou X, Riddiford LM (2002) Broad specifies pupal develop- heterokaryon. The nuclei fuse to produce a diploid ment and mediates the “status quo” action of juvenile hormone on the pupal-adult transformation in Droso- homokaryon, the chromosomes recombine, and phila and Manduca. Development 129:2259–2269 thereafter the diploid nuclei haploidize. True sexual recombination also may exist; a Cordyceps sp. ana- morph has been recorded for at least one of the spe- Metanotum cies and ITS analysis suggests that Cordyceps is a related Ascomycete. The upper surface of the third or posterior seg- Microscopically, the conidia are ellipsoidal in ment of the thorax (metathorax). In Diptera, it is shape (8 × 5 µm2) and are arranged in columns the oval arched section behind the scutellum. (Fig. 38). It grows on a variety of commercially  Thorax of Hexapods available agar and conidiates well on potato dex- trose agar. Initially, the colonies are white to buff- yellow and turn yellow-green to olivaceous-buff or Metarbelidae

A family of moths (order Lepidoptera) also known as tropical carpenterworm moths.  Tropical Carpenterworm Moths  Butterflies and Moths

Metarhizium

Michael Bidochka Trent University, Peterborough, ON, Canada

Metarhizium is a haploid, deuteromycetous, insect- pathogenic fungus and a common inhabitant of soil worldwide. At least two species are formally recognized, Metarhizium anisopliae and Metarhizium fl avoviride. Of the two, M. anisopliae is by far more common and occurs over a wide range of insect species. However, based on ITS (internally tran- Metarhizium, Figure 38 Scanning electron scribed spacer region of DNA encodings ribosomal micrograph of the palisade of conidia produced by RNA) sequence analysis, vegetative compatibility Metarhizium anisopliae. Metarhizium M 2355 dark green when conidia are formed from conidio- membrane (approximately every 15 min) restricts phores of the mycelia. Metarhizium may be selec- fungal attachment to the insect gut. tively isolated from soil on media that contains Infection is initiated when the Metarhizium dodine, chloramphenicol and crystal violet. It also conidium adheres to the insect cuticle. The conidial may be isolated from waxworm larvae (Galleria surfaces are covered by a rodlet, a structural feature mellonella) that have been placed in soil samples in composed of “hydrophobin” protein. Since the insect a technique known as the “Galleria bait method”. cuticle is hydrophobic, adherence of the conidia to Metarhizium, the causal agent of the green the insect cuticle is achieved through non-specific muscardine disease, is a broad range insect patho- hydrophobic mechanisms. Once attached to the gen that frequently infects soil insects. Ecologically, cuticle, the conidia germinate by utilizing lipids and it can best be described as a facultative insect patho- soluble nutrients found on the insect cuticle (Fig. 39). gen; it is not an obligate pathogen and grows well The germ tube grows for approximately 10–50 μm on artificial media. Over 200 different insect species then differentiates and produces a hold-fast struc- are susceptible to infection by Metarhizium. One ture on the insect cuticle termed an appressorium, subspecies isolated from Brazil, M. anisopliae var. usually within 18 h of infection. From the appresso- majus, shows specificity toward rhinoceros beetle rium, Metarhizium hyphae penetrate through the larvae while another from Australia and Mexico, insect cuticle primarily by the action of hydrolytic M. anisopliae var. acridum, shows specificity toward enzymes. The most important of these enzymes is grasshoppers and locusts. However, this level of an extracellular protease termed Pr1. This protease insect host specificity has not been entirely eluci- belongs to the subtilisin class of proteases that are dated with strains from temperate environments. In homologous to proteinase K from Tritirachium fact, there is evidence that genotypes of this fungus album and have a characteristic catalytic amino acid from temperate areas are associated with different habitats. Generally, Metarhizium is isolated more frequently from agricultural or disturbed areas but also can be found in forested habitats. The association of various genotypes of Metarhizium with host insect or habitat is still largely unclear. Of all the insect-pathogenic fungi, Metarhiz- ium may be regarded as a model organism for understanding the molecular mechanisms of insect pathogenesis. The infection process includes the following themes: (i) adhesion and germination, (ii) invasion of the host, (iii) dissemination within the host, (iv) role of toxins, (v) avoidance of host immune response, (vi) outgrowth from the host. Like most other insect pathogenic fungi, Metarhiz- ium infects the host insect by penetrating the insect cuticle; the fungus need not be ingested. In fact, the potential for infection after ingestion is low since Metarhizium, Figure 39 Conidia of Metarhizium anti-fungal substances may be produced by indig- anisopliae germinating on the surface of insect enous microbes in the insect gut. Furthermore, in cuticle. Note the appressoria adhered to the locusts, food transit time in the insect gut is gener- cuticle. Under the appressorium, a hyphae ally shorter than the time required for germination, penetrates through the cuticle. (Photo courtesy of and frequent delamination of the peritrophic Dr. R.J. St. Leger, University of Maryland.) 2356 M Metarhizium triad of serine, aspartate and histidine. Pr1 is regu- Metarhizium flavoviride has been used to control lated by the presence of carbon and nitrogen. In locusts in Africa where it is formulated with an nutrient rich media, Pr1 is not expressed, but under oil-based emulsion. There are numerous other starvation conditions such as those found on the examples of insect biocontrol using Metarhizium. insect cuticle, Pr1 is expressed in large amounts. Mass culture of M. anisopliae for biological Other extracellular enzymes such as trypsin-like control has been accomplished using two basic proteases, metalloproteases, carboxypeptidases, methods: (i) submerged culture, and (ii) surface dipeptidylpeptidases, chitinases and lipases are also culture. Submerged culture is much more prob- implicated in cuticle degradation. lematic since M. anisopliae produce yeast-like After approximately 48 h,Metarhizium trans- blastospores and/or hyphal fragments when grown gresses the insect cuticle and enters the insect in liquid medium. These have little persistence and hemocoel. Since the hemocoel is nutrient rich, Pr1 low infectivity in the field. Submerged culture is is not produced. Here, Metarhizium differentiates most often used in a diphasic system of produc- into yeast-like blastospores that proliferate in the tion. The blastospores and hyphal fragments that liquid insect hemolymph. Many Metarhizium are grown in liquid culture are transferred to a isolates produce a toxin called destruxin, a surface culture. Surface culture results in the pro- cyclodepsipeptide ionophore that may expedite duction of aerial conidia. Many inexpensive sub- insect death. Metarhizium is confronted with strates and culture methods have been used and insect immune responses, such as insect blood these generally depend on the availability of sub- cells called hemocytes, but can generally outcom- strates in the country of use. In Brazil, M. anisopliae pete these encounters. Metarhizium utilizes the has been grown on sterilized rice in polyethylene soluble nutrients within the insect and then exits bags. In the People’s Republic of China, conidia the insect and grows over the cadaver producing are produced on rice, wheat, or ground corn stalks conidia. The Metarhizium conidia now are able to in shallow trays. Unfortunately, M. anisopliae is infect other insects. not being extensively used in North America. There have been many successes usingMetar - Problems with public perception, relatively short hizium to control pest insects. Metarhizium is use- shelf-life, and longer time for insect kill compared ful especially for control of insects with sucking to chemical insecticides have hampered the wide- mouthparts since ingestion is not necessary for spread implementation of M. anisopliae as a infection to take place. Its first documented use biocontrol fungus. Nonetheless, many regions, was to control wheat cockchafer in Ukraine in particularly in developing countries, have found 1884, where up to 80% mortality was estimated. that M. anisopliae is a viable, locally cultivated Metarhizium also has been successfully used to and manageable alternative to chemical pesticides control spittlebugs (Hemiptera: Cercopidae) on for insect control. sugar cane in Brazil. One of the most interesting applications of Metarhizium was to control the larvae of a scarab beetle, Aphodius tasmanae, References which is a pasture pest in Tasmania. Previously, control of this pest was generally achieved by Bidochka MJ, Kamp AM, Lavender TM, DeKoning J, De Croos JNA, (2001) Habitat association in two genetic removing livestock from a pasture and spraying groups of the insect-pathogenic fungus Metarhizium the pasture with chemical insecticides. An eco- anisopliae: uncovering cryptic species? Appl Environ nomically viable alternative was to apply a bait Microbiol 67:1335–1342 formulation of Metarhizium onto the pasture. At Bidochka MJ, Kasperski JE, Wild GAM (1998) Distribution and occurrence of deuteromycetous entomopathogenic night, the scarab grub would carry the bait to their fungi in temperate and near northern habitats. Can burrows, where they became infected and died. J Bot 76:1198–1204 Metcalf, Zeno Payne M 2357 Driver F, Milner RJ, Trueman JWH (2000) A taxonomic revi- administrative and research prowess. Among his sion of Metarhizium based on a phylogenetic analysis of important publications are “Destructive and use- rDNA sequence data. Mycol Res 104:134–150 St Leger RJ, Frank DC, Roberts DW, Staples RC (1992) ful insects” (with W. P. Flint and later with his son, Molecular cloning and regulatory analysis of the cuti- R. L. Metcalf) (1928) and “Fundamentals of insect cle-degrading protease structural gene from the ento- life” (1932). “Destructive and useful insects” in its mopathogenic fungus Metarhizium anisopliae. Eur J various forms remains the most complete and use- Biochem 204:991–1001 Samuels RI, Charnley AK, Reynolds SE (1988) The role of ful treatment of common insect pests of North destruxins in the pathogenicity of 3 strains of Metarhiz- America, and formerly was the most widely used ium anisopliae for the tobacco hornworm Manduca text and reference manual for economic entomol- sexta. Mycopathologia 104:51–58 ogy courses. Metcalf was president of the Entomo- logical Society of America in 1934. Metcalf died on August 21, 1948. Metatarsus

The basal segment of the tarsus. Reference  Legs of Hexapods Mallis A (1971) American entomologists. Rutgers University Press, New Brunswick, NJ, 549 pp Metatentorium (pl., metatentoria)

The arm of the tentorium invaginated on the ven- Metcalf, Zeno Payne tral area of the head adjacent to the foramen mag- num; the posterior arms of the tentorium. Zeno Metcalf was born at Lakeville, Ohio, in 1885.  Head of Hexapods He received a B.A. degree from Ohio State Univer- sity in 1908 and a D.Sc. from Harvard University in 1924. He was an instructor at Michigan State Metathorax University from 1907 to 1908, followed by an appointment with the North Carolina Department The third segment of the thorax, bearing the third of Agriculture from 1908 to 1912, before he joined pair of legs and (if present) the second pair of the faculty at North Carolina State University. He wings. served the balance of his career at North Carolina  Thorax of Hexapods State, leaving for other universities only for brief periods. Metcalf served as head of the Zoology and Entomology Department from 1912 to 1950, Metcalf, Clell Lee as director of instruction for the School of Agri- culture from 1923 to 1944, and as associate dean C. L. Metcalf was born at Lakeville, Ohio, USA, on of the Graduate School from 1943 to 1950. Metcalf March 25, 1888. He attended Ohio State Univer- had an active professional life in addition to his sity, where he received his B.S. and M.S. degrees in administrative duties. He was a fellow of the Ento- 1911 and 1912, respectively. He received a doctor- mological Society of America and the American ate from Harvard University in 1919. He held sev- Association for the Advancement of Science. He eral positions in entomology but had the greatest also served as president of the Entomological impact at the University of Illinois, where he Society of America, the Ecological Society of served as professor and department head from America, and the American Microscopical Society, 1921 to 1947. He was known for his teaching, served on the editorial board of four journals, 2358 M Methodology and authored nearly 100 papers and nine books. yet sufficiently robust to be useful over range of His most significant publishing accomplishment dynamic field situations. was completion of 15 volumes of “A catalogue of Several methods have been used to estimate the Homoptera of the World.” At the time of his the relationship between insect population den- death, several additional volumes were nearly sity and plant yield response. These include completed. He died at Raleigh, North Carolina, observing naturally occurring populations, mod- on January 5, 1956. ification of these populations, creating artificial populations, and simulating insect damage. Each of these methods has advantages and disadvan- Reference tages. Selected examples are presented along with a brief discussion of the advantages and disad- Smith CF (1956) Zeno Payne Metcalf 1886–1956. Ann Ento- vantages of each. mol Soc Am 49:302

Observation of Natural Methodology Populations

The study of methods. Many writers erroneously The simplest, and one of the most effective, meth- use the term methodology when they simply mean ods of measuring crop loss is to compare yields methods. from individual plants with different population levels or from infested and uninfested plants. In the example that follows, infested and uninfested stems Methods for Measuring Crop were compared to assess the damage in wheat by Losses by Insects two insect species (Table 4). Larvae of the grass sheathminer, Cerodontha dorsalis (Loew) (Diptera: Wendell l. Morrill, B. Merle Shepard Agromyzidae), feed and pupate within tissues of Montana State University, Bozeman, MT, USA the leaf sheaths that surrounds stems. Larvae of Clemson University, Clemson, SC, USA another pest, the wheat jointworm, Tetramesa tritici (Fitch) (Hymenoptera: Eurytomidae), feed and Measurement of crop losses that occur within a range of pest insect population densities is fundamental for developing pest management pro- Methods for Measuring Crop Losses by Insects, grams. The dynamic and complex relationships Table 4 Impact of two species of phytophagous between herbivore and host are affected by insects on wheat production inherent insect fecundity, the phenology of the Insect infestation Mean head weight, pest and crop, and the impact of beneficial organ- grams isms such as parasitoids, predators and entomo- Jointworm 0.29a pathogens. Assessments of crop losses are further Jointworm 0.28a complicated by soil moisture and nutrient avail- (B) sheathminer ability that affect plants’ ability to compensate None (control) 0.95b for insect injury. The major reason for quantify- One sheathminer 1.28bc ing crop yield and/or quality losses is to estimate Two sheathminers 1.51c the pest population density at which crop loss value equals the cost of applied control. This (Source: Morrill WL (1995) Insect pests of small grains. APS estimate must be precise enough to be meaningful Press, St. Paul, MN) Methods for Measuring Crop Losses by Insects M 2359 cause galls to form at the stem joints. The interac- Methods for Measuring Crop Losses by Insects, tion of these pests and yields was investigated by Table 5 Percent loss of wheat grain caused by evaluation of mature plants were collected from a wheat stem sawflies within plant size categories field. Plant head weights were determined from Stem dia. mm Percent loss plants with and without infestations. Each mean is 2.2–2.3 14.4 for 200 plants, and means followed by the same let- 2.3–2.4 26.1 ter are not significantly different (P = 0.05). 2.4–2.5 24.0 Jointworms reduced wheat yields by about 2.5–2.6 17.5 70%. However, yields of plants that were infested by sheathminers were higher than yields of unin- 2.6–2.7 22.4 fested plants. This suggests that sheathminers overall mean loss = 20.8 may have selected the most vigorous plants for oviposition, or oviposition may have occurred (Data from Morrill WL et al. (1994) J Econ Entomol 87:1373–1376) when the primary stems were more vulnerable to attack than the lower-yielding tillers that appeared later. The advantage of working with naturally Preferential selection of host plants by phy- occurring pest infestations is that this is very close tophagous insects also plays a role in crop loss. to real field conditions. A disadvantage is that field For example, ovipositing wheat stem sawflies, trials are dependent upon natural populations that Cephus cinctus Norton (Hymenoptera: Cephi- occur over a range of densities. dae), prefer the largest and most productive wheat stems. The resulting larvae bore and feed within host stems, and material cannot move Modification of Existing upward in damaged stems to the developing Populations grain. However, there is very little difference in yields of infested and uninfested plants unless Densities of naturally occurring pest populations plants within size categories are compared in crops can be modified and related to the result- (Table 5). In this example, 400 stems were placed ing loss levels by applying different rates or types in five categorized according to diameters of the of insecticides. For this example, we will look at a upper stem internodes. Mean weights of grain forage legume, sainfoin, Onobrychis viciifolia from infested and uninfested stems and the esti- Scop., that is attacked by Lygus hesperus Knight mated losses within each category were deter- (Hemiptera: Miridae) and several other species of mined, illustrating that actual loss was over 20%. plant bugs. The bugs feed on blossoms and devel- The advantage of selecting the largest and oping seeds, thereby significantly reducing seed most suitable host for progeny production was that production (Table 6). female progeny were larger, lived longer, and laid Three rates of insecticides (carbofuran) were more eggs. Also, individuals that developed in the applied when sanfoin reached the blossoming stage. largest stems were more likely to be females due to Then, insect populations were estimated twice selective fertilization at the time of oviposition. weekly by using a sweep net. Plant bug population Beneficial insects also affect the extent of densities were lower in the treated plots, and there damage caused by sawfly larvae. Partially grown was a significant increase in seed production. larvae are attacked by two species of parasitoids Another example of the use of insecticides to (Hymenoptera: Braconidae). If sawfly larvae are eliminate or modify pest populations involves the paralyzed at the time of attack, plant damage does cereal leaf beetle, Oulema melanopus (L.) not continue. (Coleoptera: Chrysomelidae). Larvae and adults 2360 M Methods for Measuring Crop Losses by Insects Methods for Measuring Crop Losses by Insects, densities of larvae of variegated cutworms, Peri- Table 6 Pest insect populations and seed droma saucia (Hübner) (Lepidoptera: Noctuidae) production in sainfoin treated with three rates of were placed on alfalfa enclosed with aluminum insecticide barriers, and the subsequent foliage yield and Carbofuran Mean number of Seed yield quality was determined. This was then related to (kg AI/ha) mirids/10 sweeps (kg/ha) the cost of treatment and value of foliage lost. 6 days 17 days 24 days Cages (Fig. 40) can also be used to confine untreated 48.5a 56.5a 69.3a 238.0a pest insects at predetermined densities. Malayan 0.28 11.0b 19.0a 77.0a 290.6b black bug, Scotinophara coarctata (F.) (Het- eroptera: Pentatomidae) feeds on rice in Asia. 0.56 4.8b 15.0a 78.0a 277.0b Adults migrate into fields, and damage from tox- 0.84 0.5b 7.5b 47.8a 339.6c ins and juice removal includes leaf desiccation,

(Source: Morrill WL et al. (1984) J Econ Entomol “dead heart,” and plant mortality. Caged rice 77:966–968) plants were infested with 0, l, 2, 4, or 6 bugs per rice panicle, and were permitted to feed for 1, 2, 4, or 6 days. Plant response recorded included num- feed on foliage. The impacts on larval feeding on ber of filled spikelets, number of unfilled spike- yields in fields were estimated by applying insecti- lets, and weight of grain per panicle. Grain weight cide in test plots. Wheat leaves were collected, and was significantly reduced when two bugs fed for leaf area consumed was measured by using a flat six or more days per panicle. Cages can be used bed scanner. Data showed that a mean of 0.50 eggs to exclude, and thereby protect, plants from per stem resulted in 0.34 fourth instar larvae. expected pest invasions and attack. These larvae caused 4.0% yield loss, which equaled An advantage of using artificial populations is the cost of material and application with ground that numbers of insects and feeding durations can equipment. be managed. On the other hand, cages have the dis- The advantage to the use of insecticides is that advantage of affecting wind, sunlight, and other populations can be easily modified (downward) at environmental factors that impact plant growth all stages of crop development. Disadvantages are and yield. Therefore, the experimental design that many insecticides produce a “fertilizer” effect, should include caged and uncaged plants (Fig. 40). especially the organophosphates and can increase yields over an untreated crop due solely to the added input of nutrients from the insecticide. Simulated Damage In addition, most chemical pesticides seriously impact natural enemies, thereby making an other- Plants can be damaged by leaf/flower or fruit wise natural field situation unrealistic. The com- removal to simulate insect feeding (Fig. 40). In one position of resurgent pest populations may differ example, manual defoliation and feeding by the from untreated populations. This is important migratory grasshopper, Melanoplus sanguinipes because female and nymphs may feed more than (F.) (Orthoptera: Arididae), were compared for male individuals. seedling wheat plants. Treatments were 0, 1/3, and 2/3% foliage removal by grasshopper feeding and by manual clipping with a razor blade. Subsequent Creating Artificial Populations plant height, tiller production, and plant weights were compared. Results indicate that grasshopper Barriers can be used to confine pest insects within feeding had more of a negative impact on plant selected field regions or plants. For example, six growth than artificial defoliation, suggesting that Methods for Measuring Crop Losses by Insects M 2361

Methods for Measuring Crop Losses by Insects, Figure 40 Techniques in crop loss assessment. Top row, left: applying insecticide to small plots of wheat to remove pest insects top row right: assessing insect abundance in a sainfoin plot with a sweep net; middle row, left: cages used to protect rice from dispersal of ricebugs; middle row, right: cages to enclose ricebugs with rice plants; bottom row, left: removal of blossoms and pods from cowpea, simulating insect damage; bottom row, right: visual estimation of insect abundance and damage in field plot. 2362 M Methods for Measuring Crop Losses by Insects grasshopper feeding may impact wound response Natural Enemies and Crop Loss of wheat seedlings. Assessment Another example involved a trial with larvae of the bean leaf roller, Urbanus proteus (L.) (Lepi- Natural enemies such as insect predators, parasi- doptera: Hesperiidae), which feeds on foliage of toids, and entomopathogens often are major fac- beans in southeastern United States. Prior to tors regulating pest insect populations in the field. blooming, plants could lose 66% of their foliage Thus, because natural enemies influence in pest before blooming, or 33% during blooming with no densities, resulting estimates of crop losses will measurable impact on yield. Consumption by last change depending upon the communities of natu- (fifth stage) larvae was 83% of the total consumed ral enemies present. This is particularly true when during larval development. About two larvae sur- action thresholds are based on pest insect eggs or vive from one stage to the next. About 4.4 fifth early instars; insect life stages that are especially stage or 70 first stage larvae were needed to reduce susceptible to the action of natural enemies. yields. Similarly, response of soybean to artificial Unfortunately, there are few studies of crop losses leaf damage was determined by clipping leaves to that include the impact of natural enemies on represent losses from 17 to 76% defoliation. Foli- pests and how this may affect crop loss assessment. age losses of 67%, when plants were blooming, did Therefore, most field sampling strategies used to not result in yield losses and 17% leaf loss did not make treat/no-treat decisions are based only on affect yields at any stage of the plants phenology. insect pest density/crop loss relationships. Greatest losses occurred when 67% of the leaf tis- A sampling scheme to assess crop loss that sue was removed at pod set or when 17% of the included the major predators of planthoppers was leaf area was removed on a continued basis. developed for rice. This scheme was compared to There are major disadvantages to using surro- one based a traditional action threshold that did gate injury to mimic insect injury. Most insects feed not include predators as a factor. The result was by gradual removal of plant tissue. Studies that that there was a higher pest threshold when at least employ the simulated injury often use scissors to five major predators were found in five samples. excise large sections of tissue. Others defoliating/ The two plans were tested over a range of field sit- plant part removal work have used manually remov- uations and insect complexes in Philippine rice ing buds, whole leaves, punching holes in leaves by fields. The sampling plan that included predators hole punches, or using forceps to remove various as well as pests led to a significant reduction in the plant parts. Thus, plant compensation for damage number of insecticide applications without com- by artificial means may be quite different from that promising yields. caused by insects. In addition, the distribution of Another example of how natural enemies can manually-induced damage in the field may not be affect crop loss estimates and treatment decisions the same as the pest insects. Surrogate injury also comes from North Sulawesi, Indonesia. The major excludes insect feeding toxins and vectored patho- pest of cabbage is the diamondback moth, Plutella gens. Another disadvantage is the indirect impact xylostella (Lepidoptera: Plutellidae). Most farmers on beneficial insects. Infested plants may utilize the treat this pest with applications of mixtures of dif- phytophagous insects’ saliva to produce volatile ferent insecticides at frequent intervals. Field chemicals that attract parasitoids. observations revealed populations of diamond- The advantage of using artificial damage is back moth with and ensuing outbreak of a disease, that it provides an overall gross response to dam- Zoophthora radicans (Brefeld) Batka, that infects age. The level of damage can be easily manipulated the pest. Collections of diamondback larvae were to allow for a range of damage at any stage of plant made and held to determine the incidence of the development. disease. All of the larvae collected were infected Methods for Measuring Crop Losses by Insects M 2363 and died of the disease. The field population of the that insecticide applications to the seedling stage diamondback moth was high enough to cause of rice were not needed. most farmers to treat with insecticides. However, However, the plant cannot compensate for if farmers understood that the population was insect feeding directly on the fruit or grain. On the dying from the insect disease, all insecticide treat- contrary, this feeding damage is often exaggerated ments could have been avoided because little dam- as the fruit or grain matures. The type of damage age resulted. also varies. This includes defoliation, root and stem boring, grain or fruit damage, vectoring of plant diseases, and feeding toxins. General Interaction of pests and plants may be important. Insects may select the most vigorous and The use of insect-day (ID) can be applied for therefore the most productive individual plants, development of new models. For example, the thereby maximizing their impact while insuring number of days that the pest insects will feed dur- production of the largest progeny. ing the plant’s period of susceptibility X number In summary, there are a number of methods of insects. This can be further modified to “feeding that can be used to related the population level of intensity” because the impact of one insect feeding the pest insect to plant damage. But all methods have for 10 days (10 ID) can be less than the impact of advantages and disadvantages. The most frequently ten insects feeding for 1 day, also 10 ID. used methods involves natural populations over a Pest biology must also be considered. Aphid range of infestation levels. The use of insecticides to populations can potentially increase rapidly, but manipulate populations also is common and the use other pests, especially in northern latitudes, have of these two methods will probably suffice in most one generation per year. So, pests including army instances, for determining an acceptable insect pest cutworms and grasshoppers cannot increase in density/crop loss relationship. All methods, however, number within one growing season. Dispersion of must be tested under field conditions in farmers’ highly mobile pests may require a knowledge of fields and with current market acceptability. In addi- the agricultural landscape. tion, the use of action levels or thresholds implies An understanding of plant phenology is that farmers have a viable means of intervention, important. Plants may compensate or recover e.g., they are able to apply an insecticide to reduce from defoliation that occurs early in the season. the insect population. In developing countries, how- For example, the rice whorl maggot, Hydrellia ever, this is not often the case and more long term philippina Ferino (Diptera: Ephydridae), damages strategies must be developed (host plant resistance, the early seedling stages of rice. Feeding by the companion cropping, planting dates, etc.) for sus- maggot inside whorls and on the margins of tained suppression of the pest population. unopened leaves causes visible damage and rice  Sampling Arthropods farmers often apply insecticides that induce out-  Integrated Pest Management breaks of other plant feeders such as the brown planthopper, Nilaparvata lugens (Stål) (Homoptera: Delphacidae). By scoring damage ranging from 0 References to 100% and tagging individual plants, yields were compared at the end of the season. In general, Buntin GD (2001) Techniques for evaluating yield loss from there was no significant difference in yields among insects. In: Peterson RKD, Higley LG (eds) Biotic stress and yield loss. CRC Press, Boca Raton, FL, pp 23–41 plants with different levels of damage. Plants were Morrill WL (1984) Wireworms: control, sampling methodol- able to compensate for damage by this early sea- ogy, and effect on wheat yield in Montana. J Georgia son foliage feeder. This work strongly suggested Entomol Soc 19:67–71 2364 M Metretopodidae Onstad DW (1987) Calculation of economic-injury levels References and economic thresholds for pest management. J Econ Entomol 80:297–303 Pedigo LP, Hutchins SH, Higley LG (1986) Economic injury Anon (1938) Edward Meyrick BA, FRS Entomologist levels in theory and practice. Ann Rev Entomol 71:121–122 31:348–368 Anon (1938) Edward Meyrick BA, FRS Entomol Monthly Shepard BM, Justo HD Jr, Rubia EG, Estano DB (1990) Mag 74:136–137 Response of the rice plant to damage by the rice whold maggot Hydrellia philippina Ferino (Diptera: Ephydri- dae). J Plant Protect Trop 7:173–177 Mexican Bean Beetle, Epilachna varivestris Mulsant (Coleoptera: Metretopodidae Coccinellidae)

A family of mayflies (order Ephemeroptera). John L. Capinera  Mayflies University of Florida Gainesville, FL, USA

Mexican bean beetle is native to Mexico and Cen- Meyrick, Edward tral America. By the 1800s it was damaging to beans throughout the southwestern United States, Edward Meyrick was born at Ramsbury, Wiltshire, wherever beans were cultivated. A major increase United Kingdom, on November 24, 1854. in damage followed the accidental transport of Educated at Marlborough College and Trinity Mexican bean beetle to the eastern United States, College, Cambridge, he went on to be a school- to northern Alabama about 1918, apparently in master for 37 years. The early portion of his career shipments of alfalfa hay from Colorado and New (1877–1886) was spent in Australia and environs, Mexico. The beetle, once gaining access to eastern but he served in a similar position in England states, spread rapidly to the northeast, and is now from 1887 to 1914. Meyrick is well known for his found throughout much of the United States and contribution to the Lepidoptera fauna of Australia, eastern Canada. New Zealand, the South Pacific Islands, India and Southeast Asia, South Africa, South America, and England. A specialist on the smaller forms of Host Plants the order, he was a prodigious worker, and described over 20,000 species, many new genera, Mexican bean beetle develops only on legumes. and several new families. He made major contri- Other plants are occasionally reported injured. butions to “Genera insectorum,” “Lepidoptero- Vegetable crops eaten are cowpea, lima bean, rum catalogus,” and “A handbook of British and snap bean, particularly the latter two bean Lepidoptera.” He also published his own maga- types. Related crops such as faba bean, lentil, and zine, comprised of over four volumes totaling mung bean seem to be immune. Field crops that 2,500 pages, and important books: “Moths and may be attacked include alfalfa, sweet clover, their classification” (1898) and “Moths and their various dry beans, and soybean. Formerly the classification, a revised handbook” (1928). Mey- field crops other than dry beans were relatively rick worked diligently with several zoological, unsuitable and rarely injured. However, starting entomological, and natural history societies in the 1970s the eastern, and then midwestern until he died on March 31, 1938. His immense states, began experiencing considerable damage collection of Lepidoptera was bequeathed to the to soybean by Mexican bean beetle. The natural British Museum. host appears to be tick trefoil, Desmodium spp.; Mexican Bean Beetle, Epilachna varivestris Mulsant (Coleoptera: Coccinellidae) M 2365 however, in the United States, Mexican bean generations are more common, a few beetles deposit beetle is almost always found associated with eggs that form a small fourth generation. Adults are cultivated legumes. the overwintering stage. A life cycle may be completed in 30–40 days during the summer months, but may require 60 days during cooler weather. Natural Mortality Factors

Numerous predators, parasitoids, and microbial Egg disease agents of Mexican bean beetle have been identified, but few native natural enemies are con- Eggs are deposited on end in clusters of 40–60 sidered to be important. Species native to the United eggs, usually on the underside of leaves. They are States have not adapted to Mexican bean beetle as a elliptical in shape, and measure about 1.3 mm in host, whereas species imported from Central and length and 0.6 mm in width. The eggs generally South America have failed to establish permanently. are yellow in color, but turn orange-yellow prior to A parasitoid from India and Japan, Pediobius foveo- hatch. Eggs hatch in 5–14 days, averaging 5.7 days. latus (Crawford) (Hymenoptera: Eulophidae) has All females from the first generation deposit eggs, been cultured and released in eastern states. Annual but in South Carolina only 94% of the second and release is necessary because the parasitoid is unable 60% of the third generation beetles reportedly to overwinter in the United States. Small gardens, produced eggs as more and more beetles entered such as those in urban and suburban communities, reproductive diapause. are most suitable for Pediobius release. Microbial pathogens, especially Nosema epil- achnae and N. varivestris (both Microsporida: Nose- Larva matidae), occur in bean beetles. These pathogens are deleterious to Mexican bean beetle; Nosema epilach- The larvae are yellow in color, and armed with a nae, in particular, reduces longevity and fecundity in dense covering of branched spines arrayed in six bean beetles. However, these pathogens also infect longitudinal rows (Fig. 41). There are four instars. the parasitoid Pediobius foveolatus. Infection of the The mean duration of the instars in a South parasitoid occurs when the immature stage develops Carolina study has been reported to be 3.9, 3.6, 3.6, in its host, or when the adult ingests the pathogen. Although natural enemies may affect bean beetle abundance, weather is also thought to play an important role in population dynamics. Hot, dry weather is thought to be detrimental to survival of all stages, but especially the egg stage. Temperatures above 35–37°C can be lethal.

Life Cycle and Description

Mexican bean beetle usually exhibits 1–3 generations annually. In the western United States there Mexican Bean Beetle, Epilachna varivestris normally is one complete generation with some Mulsant (Coleoptera: Coccinellidae), individuals reproducing and developing a small Figure 41 Mexican bean beetle larva, Epilachna second generation. In the southeast, where three varivestris. 2366 M Mexican Bean Beetle, Epilachna varivestris Mulsant (Coleoptera: Coccinellidae) and 3.6 days, respectively. After attaining its full ground color is usually orange or copper, but size, about 8 mm in length, the larva attaches its ranges from yellow when freshly emerged, to anal end to a substrate, usually the leaf on which it reddish brown when old. The beetles normally fed, and pupates. measure about 6–8 mm in length and 4–6 mm in width, but size varies considerably depending on availability of food. Females commonly produce Pupa about 500 eggs, sometimes depositing over 1,200 eggs. Adults overwinter under leaves and other During the process of pupation the larval cover- plant debris, and under logs and stones. ing, which contains the spines, is pushed back toward the point of attachment to the substrate. Thus, the pupa appears to bear spines, but this is Damage simply remnants of its earlier life, and not firmly attached. Rather, the yellow-orange pupa is quite Larvae and adults feed principally on leaf tissue, but free from projections. Duration of the pupal stage under high density conditions, and when faced with averages 8.1 days in South Carolina. starvation, they also feed on blossoms, pods, and stems. Bean beetles feed on the lower surface of the foliage, removing small strips of tissue and usually Adult leaving the upper epidermis and veins intact. The upper epidermis soon dies and becomes transparent, Adults are brightly colored beetles that resemble leaving characteristic injury consisting of a number many beneficial ladybird beetle species. The beetle of small transparent spots that is reminiscent of a is hemispherical in shape, and bears 16 black spots. stained-glass window. Entire leaves are quickly The spots are arranged in 3 rows, with 6 spots in reduced to skeletal lace-like remains that have little each of the first 2 rows and 4 in the third row; thus, photosynthetic value and usually dry and die quickly. there are 8 on each elytron (Fig. 42). The back- The larvae are particularly damaging, and a mature larva may consume an entire leaf in a day. Mexican bean beetle also is capable of plant disease transmission. Larval and adult bean beetles fed on plants infected with cowpea mosaic virus become capable of transmitting the virus to healthy plants for a 2–4 day period

Management

Modern insecticides have relegated Mexican bean beetle to minor status in commercial bean production. They remain a serious problem, however, in home gardens and elsewhere when insecticides are not used. Cultural practices are of limited value. The beetles fly long distances for overwin- Mexican Bean Beetle, Epilachna varivestris tering, so crop rotation and destruction of over- Mulsant (Coleoptera: Coccinellidae), wintering sites is generally not practical. It is a Figure 42 Mexican bean beetle adult. useful practice, however, to destroy bean plants as Microbial Control of Insects M 2367 soon as they have been harvested, as this may domestic settings. Natural epizootics of insect disrupt development of many immature insects disease can result in spectacular declines in insect and inhibit development of additional generations. populations of economic and medical importance. The principal means of biological suppression of However, dependence upon naturally occurring Mexican bean beetle is release of Pediobius wasps. epizootics for insect control can be risky when However, commercial bean producers rarely con- economic thresholds might be surpassed, or when sider such an approach, tending to rely instead on plant and animal diseases could be transmitted by chemical insecticides. Some degree of resistance the insects before they succumb to disease. Micro- occurs within commercially available cultivars of bial control of insects is the concerted use of beans, but this is not completely adequate. insect-specific pathogens and nematodes for the  Vegetable Pests and their Management biological control of insects. Microbial pesticides have a number of advantages over conventional References chemical pesticides. Although the advantages of microbial pesticides are numerous, some of their characteristics are regarded as disadvantages. Auclair JL (1959) Life history, effects of temperature and relative humidity, and distribution of the Mexican bean beetle, Epilachna varivestris Mulsant (Coleoptera: Coc- cinellidae), in Quebec, with a review of the pertinent Advantages and Disadvantages of literature in North America. Ann Entomol Soc Quebec 5:18–43 Entomopathogens for Insect Capinera JL (2001) Handbook of vegetable pests. Academic Control Press, San Diego, CA, 729 pp Friend WG, Turner N (1931) The Mexican bean beetle in Advantages Connecticut. Conn Agr Exp Stat Bull 332:108 List GM (1921) The Mexican bean beetle. Colorado Agr Exp Stat Bull 271:58 ·· specificity to the target organism or to a limited number of host species, ·· little or no direct impact upon parasitoids and Mexican Fruit Fly, Anastrepha invertebrate predators, ludens (Loew) (Diptera: ·· harmless to vertebrates and plants, Tephritidae) ·· no toxic residues, ·· little or no environmental pollution, This fruit pest occurs in Mexico and adjacent areas ·· little or no development of resistance by the target of the USA. organism (however, resistance has developed in  Citrus Pests and their Management some target insects to Bt and Bacillus sphaericus)  Fruit Flies (Tephritidae) ·· no secondary pest outbreak, ·· compatibility with other biological control agents, ·· possibility of long-term control, Microbial Control of Insects ·· ease of application, and ·· adaptable to genetic modification through Lawrence A. Lacey biotechnology. USDA-ARS, Wapato, WA, USA

A wide variety of pathogenic organisms (virus, Disadvantages bacteria, protozoa, fungi and nematodes) attack insects and result in reductions in insect numbers ·· specificity only to target organism, within natural ecosystems, agroecosystems, and ·· strict timing of application for maximal effect, 2368 M Microbial Control of Insects ·· long period of lethal infection (i.e., little or no Conservation biological control fosters patho- “knock-down” effect), gen abundance by reducing harmful influences ·· inactivation by environmental factors (e.g., ultra- and enhancing positive ones. This may entail violet light, desiccation, temperature extremes, replacing a broad-spectrum fungicide with one etc.) and therefore, short field persistence, with a narrower spectrum of activity, changing the ·· expensive to produce, especially for obligate timing of insecticide use to avoid killing host pathogens, and difficult to formulate, insects while pathogens are developing and ·· short shelf life, increasing within the population, and other prac- ·· development of resistance by target organisms, tices that enhance the activity of pathogens that especially to Bt and B. sphaericus, codling moth are present within the targeted insect population. granulovirus An excellent example of this strategy is the encour- ·· expensive to produce except for niche markets, agement of epizootics of the fungal pathogen, and Neozygites gossypii in populations of the cotton ·· risks or perceived risks associated with geneti- aphid, Aphis gossypii. cally-modified organisms. Augmentative biological control consists of two types of strategies: inoculative and inundative Like insect biological control agents (preda- applications. Inoculative control can be used to tors and parasitoids), microbial control agents can counteract seasonally repeating problems typical be employed in classical, conservation and aug- of annual cropping systems, such as the use fungi- mentation biological control. Microbial control cides, tillage, etc. Insect pathogens can also be agents have been used in most settings where introduced earlier in the season than they would insect pests are found including glasshouse and normally occur, giving them time to reproduce and row crops, orchards, ornamentals, range, turf and suppress pests earlier in the cropping cycle. The lawn, stored products, forests, households, aquatic most commonly employed augmentative strategy environments, animal waste, and for control of for microbial control agents is inundative applica- insects of veterinary and medical importance. tion of microbial pesticides. Inundative approaches In classical biological control using insect differ from classical and inoculative strategies in pathogens, the disease causing agents are isolated that the activity of the applied pathogens, not nec- from diseased insects and introduced into an essarily that of secondary inoculum, provides con- insect population in which they are not currently trol of the pest insects. Using this strategy, one to present. The objective is to establish the pathogen several applications of microbial control agents are or nematode within the population resulting in made for control of the pest insect. Microbial recycling within the insect population and provid- agents that are currently used in commercial prod- ing long term control. Some of the most successful ucts are listed in the following table. examples of establishment and long term control include the use of the fungus, Entomophaga maimaiga against the gypsy moth, Lymantria dispar, Entomopathogens Commonly the Oryctes non-occluded virus against the palm Used for Microbial Control rhinoceros beetle, Oryctes rhinoceros, the nematode Deladenus siricidicola against the woodwasp, Bacteria Sirex noctilio and the fungus Zoophthora radicans for control of alfalfa aphid, Therioaphis trifolii. The most widely used insect pathogen for inunda- Classical biological control using insect pathogens tive augmentative control is the bacterium, Bacillus has been most successful in perennial agroecosys- thuringiensis (Bt). It was the development and tems and forests. commercial production of Bt that ushered in the Microbial Control of Insects M 2369 practical use of microbial control on a large scale. fermentation on a large scale, may be formulated (as The larvicidal activity ofBt is due to a proteinaceous wettable powders, granules, flowable concentrates, toxin inclusion that is formed at the time of sporula- etc.) for ease of application and enhancement of tion which must be eaten by the targeted insect in activity, are applied using conventional equipment order to be active. Collectively, the toxins are referred and are stable in storage for months or even years to as delta endotoxins. For detailed information on depending on storage conditions. their chemistry and mode of action see section on Several varieties of Bt have been discovered Bacillus thuringiensis in this volume. Besides relative over the past century that have activity against Lepi- specificity and efficacy, the other advantages of doptera, certain families of Diptera and Coleoptera Bt products are that they can be produced by as well as other insects. Bt is used to control a wide

Microbial Control of Insects, Table 7 Representative invertebrate pathogens that are currently used in microbial control products Microbial control agents Targeted insects Bacteria Bacillus thuringiensisa Bt kurstaki, Bt aizawai Several species of Lepidoptera Bt tenebrionis Colorado potato beetle Bt israelensis Mosquitoes, black flies, fungus gnats Bacillus sphaericus Mosquitoes (especially Culex spp.) Paenibacillus popilliae Japanese beetle Serratia entomophila New Zealand grass grub Fungi Lecanicillium (Verticillium) spp. Aphids, whiteflies, and thrips Metarhizium anisopliae Grasshoppers, termites, cockroaches Beauveria bassiana Colorado potato beetle, white flies, other insects Virus Nucleopolyhedrovirusesb several species of Lepidoptera Granuloviruses several species of Lepidoptera Nematodesc Steinernema carpocapsae Numerous insect pests S. feltiae Diptera, Lepidoptera, other insect pests S. riobrave weevil larvae, Lepidoptera, Orthoptera S. scapterisci mole crickets S. glaseri scarab larvae Heterorhabditis bacteriophora Numerous insect pests H. megidis scarab larvae, other insect pests Phasmarhabditis hermaphrodita Slugs arepresentative varieties bnumerous species have been developed, see Miller (1997), Hunter-Fujita et al. (1998) crepresentative species 2370 M Microbial Control of Insects variety of lepidopteran pests in several row crops, field collected infected larvae, a distinct disadvantage stored foods, orchards and forests. Aerial application in terms of large scale production. Properly prepared for gypsy moth control is one of the larger scale spore powders can persist for several years. Unlike Bt applications of this bacterium against lepidopteran and B. sphaericus, infected larvae are not rapidly larvae. The beetle active varieties are predomi- killed, but slowly develop milky hemolymph and nantly used against the Colorado potato beetle, usually die as full grown larvae which serve as source Leptinotarsa decemlineata, and certain other Chry- of inoculum for neighboring larvae (Fig. 43). somelidae. The variety Bt israelensis is insecticidal for mosquito, black fly, and fungus gnat larvae and certain other nematocerous Diptera. (For further Viruses reading on this bacterium for mosquito and black fly control, see Microbial control of medically Although there are a huge numbers of viruses important insects.) Genes that encode production that are pathogenic for hundreds of species of of Bt toxins have been incorporated into varieties of corn, cotton, potatoes and other crop plants. These genetically modified crops provide continuous control of susceptible insects. Various strategies have been proposed or employed to counteract or forestall development of resistance by the targeted pests to the toxins. Public acceptance of Bt- transgenic plants is currently a major obstacle to their widespread use as human food. Other bacteria that are used as microbial control agents against pest insects are Bacillus sphaericus (against mosquito larvae), Paenibacillus popilliae (against Japanese beetle larvae), and Serratia entomophila (against Costelytra zealandica [grass grub] in New Zealand). Of these, B. sphaericus is second to Bt in commercial production and sales. It offers several of the same advantages of Bt in terms of ease of production and formulation, application using conventional equipment and good shelf life. It rapidly kills susceptible species within 24 h of ingestion and is more active than Bti against certain mosquito species especially in organically enriched habitats. Its two main disa dvantages are a narrower host range than Bti and the development of very high levels of resistance in certain populations of Culex quinquefasciatus, one of the main targeted species. The success of P. popilliae or milky disease as a Microbial Control of Insects, Figure 43 Cabbage microbial control agent of Japanese beetle larvae looper infected with nucleopolyhedrosis virus, has been variable with substantial long term con- displaying characteristic symptoms including trol reported in certain situations and little or no hanging from the prolegs and liquefaction of body control reported in others. Spores of P. popilliae must contents (photo courtesy of Pat Vail and Darlene be produced in living host larvae or harvested from Hofmann). Microbial Control of Insects M 2371 pest insects, only the baculoviruses have been the targeted insect in order to be active. This is an commercially developed and used on a wide scale. important consideration when formulating viruses Baculoviruses have been reported with activity to facilitate application and protection from UV against Lepidoptera, Hymenoptera (sawflies), Dip- inactivation; adjuvants that inhibit feeding will tera and a few other arthropods. Most varieties reduce efficacy. The use of optical brighteners with have been isolated from Lepidoptera and are repre- baculovirus has markedly improved efficacy sented by the singly occluded granuloviruses (GV) against some species of Lepidoptera through their and multiply occluded nucleopolyhedroviruses activity on the peritrophic membrane allowing (NPV). The GVs and several of the NPVs are greater contact between virus and the midgut specific for one species or closely related group of epithelium. Adjuvants that protect the virus from species. For example, the codling moth GV is highly UV inactivation have also improved efficacy, but virulent for codling moth and to a lesser extent with an increase in cost. related species such as pea moth and the oriental Some of the baculoviruses have been success- fruit moth, but does not infect most other species in fully employed on a large scale for control of agricul- the same family (Tortricidae). The two baculovi- tural pest insects. For example, the NPV of the velvet ruses with the broadest host range are the multiply bean caterpillar, Anticarsia gemmatalis, is currently enveloped NPVs isolated from two noctuids, the used to treat approximately one million ha of alfalfa looper, Autographa californica (AcMNPV), soybeans in Brazil annually. In many agricultural and the celery looper, Syngrapha (=Anagrapha) settings, the cost of entomopathogenic virus will falcifera (AnfaMNPV). AnfaMNPV has been reported restrict their use to high value niche markets and to infect over 31 species of Lepidoptera in ten fam- sensitive areas where chemicals cannot be used. ilies. The host range ofAc MNPV includes 33 species of Lepidoptera in 12 families. The virulence of both viruses for species in the Noctuidae is especially Fungi high. For example, the LC50 values for Anfa MNPV against Trichoplusia ni, Heliothis virescens, Helicov- Fungi comprise another large group of micro- erpa zea and Spodoptera exigua are 0.093, 0.095, organisms that have been developed as micro- 0.147 and 0.327 occlusion bodies/mm2. bial control agents. A rich diversity of fungi are The principal advantages of the baculoviruses found causing disease in a wide variety of are their efficacy, specificity, and production of insects. Because they invade insects via the secondary inoculum (i.e., recycling in host popu- integument, they are the only effective micro- lations). These benefits make them attractive alter- bial control agents used for control of sucking natives to broad spectrum insecticides and ideal insects such as aphids and whiteflies. Viruses, components of IPM systems due to their lack of bacteria and protozoa on the other hand must untoward effects on beneficial insects including be ingested in order to infect insect hosts. Spe- other biological control organisms. The need to cies of fungi in the order Entomophthorales produce virus in living cells, either in cell culture (subdivision Zygomycotina, class Zygomycetes) or whole insects, increases the cost of virus pro- are among some of the most virulent and have duction. Some of the other drawbacks of using been responsible for dramatic crashes in insect entomopathogenic viruses are their relatively slow populations. Their success as natural and clas- action as compared to chemical insecticides, sen- sical biological control agents has been men- sitivity to UV light and the need to time applica- tioned above (e.g., N. gossypii and E. maimaiga). tions to coincide with susceptible instars. However, several of the most efficacious Like the bacterial microbial control agents, Entomophthorales are problematic to manipu- entomopathogenic viruses must be ingested by late due to difficulty in producing them on 2372 M Microbial Control of Insects artificial media and limited shelf life of infec- artificial media. Infective stages of these families tive propagules. are non-feeding and can be stored for several Entomopathogenic species in the Hypocre- months, especially under refrigeration. The micro- ales (formerly placed in the subdivision Deu- bial aspect of steinernematids and heterorhabdit- teromycotina class Hyphomycetes) are the fungi ids stems from the symbiotic relationship they most commonly used as inundatively applied have with bacteria in the genera Xenorhabdus and microbial control agents. These fungi do not Photorhabdus, respectively. The infective stage of have sexual stages, can be produced on artificial the nematode is the means by which the bacterium media, and are fairly stable in storage (for several gains entry to the insect host. The bacteria facili- months when stored in cool conditions). Beau- tate rapid death of the host, digestion of host tis- veria bassiana, Lecanicillium (Verticillium) spp., sues and the production of antibiotics that provide Isaria (Paecilomyces) fumosoroseus and Metar- protection of the host cadaver from invasion by hizium anisopliae are commercially produced other microbes. The nematodes may actively pur- and have been employed against a wide range of sue host insects (cruisers) or wait for hosts to come insect species. Most species of fungi require to them (ambushers). These nematodes have high humidity in order to germinate and infect potential for the persistent control of several insect insect hosts. Environmental manipulation and species, especially in soil and cryptic habitats. formulation have been used to improve efficacy Their main limitations are prior to invading an and protect spores from deactivation by UV insect host. Rapid desiccation severely restricts the radiation. Although shelf life is somewhat lim- window of opportunity for foraging for a host in ited relative to bacteria and viruses, refrigera- the absence of sufficient moisture. Some species tion and formulation have improved the are limited by temperatures at or below 10°C longevity of fungal preparations. (S. carpocapsae), but there are species that are active at temperatures as low as 5–7°C (S. kraussei, S. feltiae). Some species have a fairly narrow host Nematodes range (e.g., S. scapterisci) while others attack a wide range of species (e.g., S. carpocapsae). Several families of nematodes parasitize insects. The majority of the research that has been published pertains to the Mermithidae, Steinernema- General Considerations tidae, and Heterorhabditidae. The mermithids are obligate parasites of a broad spectrum of insects. Microbial control agents can be applied using One species, Romanomermis culicivorax had been a variety of conventional pesticide application commercially produced and used as a biological equipment as well as some non-conventional control agent of mosquito larvae. The necessity of methods. Autodissemination using attractant traps using living hosts for production and a limited is one of the more innovative approaches. Targeted shelf life (a few months under refrigeration) has insects are attracted to traps using pheromones, limited the prospects for commercial production floral lures and the like and become contaminated of mermithids. On the other hand, they have good with fungi, virus, etc. and disseminate the inocu- potential as classical biological control agents and lum to other individuals of their species through may persist and recycle in certain habitats in which direct contact (mating, aggregations) or by dying they have been introduced. in larval habitats. The application of microbial Several species of the Steinernematidae and control agents using chemagation (application Heterorhabditidae, collectively referred to as ento- through irrigation systems) in combination with mopathogenic nematodes, have been grown on remote sensing also appears to have promise. Microbial Control of Medically Important Insects M 2373 Microbial control may provide adequate Hunter-Fujita FR, Entwistle PF, Evans HF, Crook NE (eds) suppression of insect pests used as a stand alone (1998) Insect viruses and pest management. Wiley, Chichester, UK, 632 pp measure in certain situations or may be inte- Lacey LA, Kaya HK (eds) (2007) Field manual of tech- grated into a more complex strategy that includes niques in invertebrate pathology: application and other biological control agents, environmental evaluation of pathogens for control of insects and modification or manipulation, use of other alter- other invertebrate pests, 2nd edn. Springer, Dor- drecht, The Netherlands, 868 pp native interventions (such as mating disruption) Lacey LA, Frutos R, Kaya HK, Vail P (2001) Insect pathogens or the judicious use of conventional pesticides. as biological control agents: do they have a future? Biol For example, the use of a chemical pesticide Control 21:230–248 Miller LK (ed) (1997) The Baculoviruses. Plenum Press, against a specific life stage that is unaffected by New York, NY, 468 pp the microbial agent, or use of chemical pesticides Tanada Y, Kaya HK (1993) Insect pathology. Academic Press, and a microbial agent in synergistic combination New York, NY, 666 pp such as the chloronicotinyl insecticide, imidaclo- prid and the Hypocreales fungus, Metarhizium anisopliae. Microbial Control of Medically The comparison of microbial control agents Important Insects with chemical pesticides is usually made from the perspective of only their efficacy and cost. In Lawrence A. Lacey1, James J. Becnel2 addition to efficacy, the advantages of using 1USDA-ARS, Wapato, WA, USA microbial control agents are numerous includ- 2USDA-ARS, Gainesville, FL, USA ing safety for humans and other nontarget organisms, reduction of pesticide residues in food, Microbial control of insects of medical and veteri- preservation of other natural enemies and nary importance is the use of insect-specific patho- increased biodiversity in managed ecosystems. gens and nematode parasites for the control of The selectivity and safety of microbial control insects that are vectors and pests of humans or agents should facilitate their incorporation into domestic animals. Medically important insects IPM programs where their effects on other natu- include those that suck blood such as mosquitoes ral enemies will be minimal as compared to most (Culicidae), black flies (Simuliidae), and other dip- presently used chemical pesticides. Increased terans, lice (Phthiraptera), fleas (Siphonaptera) and use of entomopathogens for control of arthro- those that do not suck blood but are nevertheless a pod pests will depend on a variety of factors nuisance (house flies, cockroaches, etc.). Infectious including improvements in the pathogens related agents of some of the most devastating diseases of to their efficacy and cost and the perceived ben- humans are transmitted by insects. These include efits of using them relative to conventional organisms that cause malaria, yellow fever, den- chemical pesticides. gue, several encephalitides (such as West Nile virus), plague, onchocerciasis, typhus, sleeping References sickness, and Chagas disease. Domestic and wild animals also suffer from insect transmitted diseases, some of which result in death and/or severe Burges HD (ed) (1981) Microbial control of pests and plant diseases 1970–1980. Academic Press, London, UK, economic losses. Pestiferous insects are also causes 949 pp for decreased quality of life, weight loss in animals Gaugler R (2002) Entomopathogenic nematology. CABI and allergic reactions in humans and domestic ani- Publishing, Wallingford, UK, 402 pp mals. The majority of research on microbial con- Grewal PS, Ehlers RU, Shapiro-Ilan DI (eds) (2005) Nema- todes as biological control agents. CABI Publishing, trol of medically important insects has been Wallingford, Oxon, UK, 480 pp conducted on the Diptera, most notably larvae of 2374 M Microbial Control of Medically Important Insects mosquitoes and black flies. This discussion will pathogens of mosquitoes do not require intermedi- focus on microbial control of these two groups. ate hosts. For example, Edhazardia aedis is a viru- There is a large number of microbial agents lent pathogen of the yellow fever mosquito, Aedes (virus, bacteria, fungi, protozoa, rickettsia) and aegypti that has good potential as a classical biologi- nematodes (Mermithidae and others) reported to cal control agent. This microsporidian is well infect medically important insects. The most com- adapted to the host mosquito and its container monly observed in nature are microsporidia [now breeding habitats and can persist in Ae. aegypti included in the fungi], other fungi, viruses, and populations through transovarial transmission and nematodes. Several microsporidia and certain other spread to additional breeding sites. fungi that infect mosquitoes and black flies include Although viruses and mermithid nematodes species with complex life cycles, such as Ambly- also require living hosts in order to propagate, cer- ospora spp. and Coelomomyces spp. that involve tain species have good potential as augmentative intermediate hosts. These requirements and the and classical biological control agents (see also, need to multiply in living hosts decreases their Microbial Control of Insects for definitions). The potential as applied microbial control agents. How- potential of mermithid nematodes has been dem- ever, their impact as naturally occurring pathogens onstrated in rice fields and other non-polluted on populations of medically important insects can freshwater habitats. An advantage of this group is be substantial. Amblyospora spp. and Coelomomyces the potential to become established and recycle in spp. are particularly common in Aedes and Culex mosquito habitats, but they are less effective in mosquitoes found worldwide and are a crucial part organically enriched and saline habitats. In the case of a complex of biotic and abiotic factors that impact of Romanomermis culicivorax, for example, a spe- the dynamics of mosquito populations due to a cies that has been studied extensively, the egg stage reduction in the survival, vigor and reproductive can be stored in moist sand for use in subsequent success of infected m osquitoes (Fig. 44). Their microbial control efforts. When flooded with water, importance must be viewed not for short-term stored eggs hatch to produce infective preparasites. population reduction but rather for the benefits of These can then be applied to larval habitats with long-term abatement as part of an overall manage- conventional spray equipment. The shelf live of eggs ment strategy. Some of the other microsporidian is somewhat curtailed and the cost and logistics of production in living hosts are factors limiting widespread use. A protocol for the application and evaluation of R. culicivorax against mosquito larvae in rice fields have been developed. The mermithid nematode Strelkovimermis spiculatus, isolated from mosquitoes in Argentina, has a life cycle similar to R. culicivorax (Fig. 45). Unlike R. culicivorax, S. spiculatus has a demonstrated tolerance for high levels of organic pollution and dissolved ions relative to other mermithids and is currently being evaluated for introduction as a biological control agent of mosquitoes, particularly Culex spp. Several insect specific viruses have been reported from mosquitoes and black flies includ- Microbial Control of Medically Important Insects, ing Deltabaculoviruses, Cypoviruses, Iridoviruses Figure 44 Culex salinarius larva infected with and Densoviruses. Those with the best potential Amblyospora salinaria. for mosquito control are the Deltabaculoviruses Microbial Control of Medically Important Insects M 2375 (formerly nucleopolyhedroviruses) within the transmit and epizootics in field populations were family Baculoviridae (Becnel, 2007). Deltabaculo- rarely observed. Recently, a newly discovered DBV, viruses (DBVs) have been isolated from thirteen designated CuniDBV, has been discovered that mosquito species within the genera Aedes, Anoph- was responsible for repeated and extended epi- eles, Culex, Ochlerotatus, Psorophora, Uranotaenia zootics in field populations of Culex nigripalpus and Wyeomia. Historically, mosquito baculovi- and Culex quinquefasciatus in Florida, USA. ruses have been extremely uncommon, difficult to CuniDPV infects and destroys the larval midgut (Fig. 46) causing patent infections within 48 h post-inoculation (p.i.) and death 72–96 h p.i. Each Romanomermis culivorax of the small globular occlusion bodies measures approximately 400 nm and contains four, some-

Pre- times up to eight, singly enveloped virions per parasitics occlusion body. While initial attempts to transmit 7-10 Days this baculovirus to mosquitoes in the laboratory parasitic phase were unsuccessful, further investigations revealed conclusively that transmission is mediated by divalent cations: magnesium is essential for transmission whereas calcium inhibits virus transmis- Emergence and host death sion. This has been an important finding in understanding transmission of baculoviruses in Post- parasitics Adults Eggs mosquitoes and can explain, in great part, condi- hatch tions that support epizootics in natural popula- 1 Week 2 Weeks tions of mosquitoes and allow evaluation of

Egg laying CuniNPV as a new microbial control agent. A multitude of entomopathogenic fungi Larval development infect mosquito and black fly larvae and adults. The speciesLagenidium giganteum, formerly clas- Microbial Control of Medically Important Insects, sified with the fungi, has now been placed in the Figure 45 Life cycle of Romanomermis culicivorax, Kingdom Chromista. Compared with mosquito- an obligate parasite of mosquito larvae (courtesy cidal fungi, it has the greatest potential for micro- of Ed Platzer). bial control. The main advantages of this species

Microbial Control of Medically Important Insects, Figure 46 Culex quinquefasciatus larva infected with nuclepolyhedrosis virus (CuniNPV). White areas of the gastric caeca and posterior midgut (indicated by arrows) are the sites of infection. Inset shows details of viral rods with individual occlusion bodies. 2376 M Microbial Control of Medically Important Insects is that it can be produced on artificial media, has order to be active. The active moieties of each spe- good larvicidal activity against a wide range of cies are proteinaceous toxins that are produced by mosquito species, and the resting spores have an the bacterium at the time of sporulation. The tox- extremely prolonged shelf life. The infective stage ins in Bti, found in large parasporal inclusions, are is a short lived zoospore that is formed in vesicles active against a wide range of species in the Culi- on infected larvae, by mature mycelia in artificial cidae and Simuliidae and certain other families of media, or through the germination of resting Nematocera. After ingestion, the toxins are solubi- spores. The zoospores attach to and encyst on the lized in the alkaline environment of the midgut cuticle of mosquito larvae and the subsequent and cleaved by enzymes to the active moieties that general infection of the larvae results in produc- bind with the epithelial cell membranes. The resul- tion of zoospores (secondary inoculum) within tant pore formation in the membranes alters the 1–7 days of infection depending on environmen- osmotic balance of the cells, ultimately resulting in tal conditions and water quality. When grown in rupture of the cells and eventual death of larvae. artificial media, zoosporogenesis (the production In many mosquito abatement programs in of zoospores) results from nutrient deprivation of North America, Europe and elsewhere, Bti is used mature mycelia (presporangia) from 1–4 week- as the larvicide of choice. In addition to its ele- old cultures. This can be accomplished by diluting vated larvicidal activity, the effects on nontarget mycelial preparations with distilled or deionized organisms, including mosquito predators are water. The application of mature mycelia to larval minimal to non-existent. Various formulations habitats will result in the production of infective (liquid, pellets, granules, etc.) and methods of zoospores within hours or days of application application have enabled a tailored approach to depending on conditions. Although resting spores larval control of mosquito larvae in a variety of can be stored for extended periods and retain via- habitats, including slow release formulations that bility, they require 30 or more days of immersion enable prolonged control in certain smaller habi- in water before germination begins. The combi- tats. For the most part however, Bti has very little nation of L. giganteum mycelia and resting spores residual activity, especially in organically enriched could provide a rapid and high level of infection habitats necessitating fairly frequent application in targeted larvae and a prolonged release of zoo- when mosquito breeding is continuous. spores as new cohorts of larvae begin to hatch. For control of black fly larvae, Bti is a potent Similarly the combination of larvicidal bacteria larvicide with negligible impact on non-target and resting spores could provide rapid and con- organisms. As an intervention used in the tinuous control. Lagenidium giganteum has Onchocerciasis Control Program (OCP), it was become established in several habitats into which responsible for control of Simulium vectors of it has been introduced providing a certain level of Onchocerca volvulus, the causal agent of River classical biological control in years subsequent to Blindness, in an area where the black fly had devel- the original introduction. Commercial produc- oped resistance to organophosphate insecticides. tion of L. giganteum has been facilitated by a It is currently a seasonally implemented control number of research breakthroughs in the 1980s component in the OCP and is used to forestall or and 1990s that enabled production of mature avoid the development of insecticide resistance. mycelia and oospores in artificial media. Because of the nature of black fly habitats (i.e., By far the most commonly employed patho- running water) and the tendency of Bti to become gens for control of mosquito larvae are Bacillus rapidly diluted after application, it must be applied thuringiensis var. israelensis (Bti) and Bacillus at regular intervals in order to control larvae along sphaericus. Bti is also insecticidal for black fly (Sim- the course of a river or stream. The distance down- uliidae) larvae. Both bacteria must be ingested in stream from the treatment point where control is Microbivores M 2377 achieved is referred to as effective carry. As in insect pathology. Academic Press, London, UK, pp mosquito habitats, if black fly breeding is continu- 251–268 Lacey LA (2007) Bacillus thuringiensis serovariety israelensis ous, regular applications must be made in order to and Bacillus sphaericus for mosquito control. In: Floore achieve effective control. The time between appli- TG (ed) Biorational control of mosquitoes, Bulletin 7. cations depends on the developmental cycle of the American Mosquito Control Association, Fresno, CA, targeted species. pp 251–268 Lacey LA, Orr BK (1994) The role of biological control of Bacillus sphaericus functions similarly to Bti, mosquitoes in integrated vector control. Am J Trop Med but has a narrower host range within the Culicidae Hyg 50 (suppl):97–115 and is not active against black fly larvae. Species in Lacey LA, Merritt RW (2003)The safety of bacterial microbial agents used for black fly and mosquito control in the mosquito genera Psorophora and Culex are aquatic environments. In: Hokkanen HMT, Hajek AE highly susceptible to B. sphaericus toxins. Anoph- (eds) Environmental impacts of microbial insecticides: eles and Mansonia spp. larvae are also susceptible, Need and methods for risk assessment. Kluwer but to a lesser extent. Aedes aegypti and certain Academic Publishers, Dordrecht, The Netherlands, pp 151–168 other Aedes spp. exhibit little or no susceptibility Lacey LA, Undeen AH (1986) Microbial control of black flies to this bacterium. One of the main advantages of and mosquitoes. Ann Rev Entomol31:265–296 B. sphaericus is greater persistence of larvicidal Lucarotti CJ, Andreadis TG (1995) Reproductive strategies and adaptations for survival among obligatory activity in organically enriched habitats. It has also microsporidian and fungal parasites of mosquitoes: a been reported to recycle within mosquito cadav- comparative analysis of Amblyospora and Coelomomy- ers and populations under certain conditions. ces. J Am Mosq Control Assoc 11:111–121 There have been reports in India, Brazil, Thailand Skovmand O, Kerwin J, Lacey LA (2007) Microbial control of mosquitoes and black flies. In: Lacey LA, Kaya HK and other locations of extremely high levels of (eds) Field manual of techniques in invertebrate resistance to B. sphaericus in larvae of Culex pathology: application and evaluation of pathogens quinquefasciatus, a common species in organically for control of insects and other invertebrate pests, enriched aquatic habitats. 2nd edn. Springer, Dordrecht, The Netherlands, pp 735–750  Microbial Control of Insects  Fungal Pathogens of Insects  Nematode Parasites of Insects  Amoebae Microbial Pesticide  Baculoviruses  Microsporidia Microbial organisms that are applied like chemical  Individual Taxa pesticides for the suppression of pest abundance. Examples including various bacterial, fungal, viral, and microsporidian pathogens. References  Microbial Control of Insects

Becnel JJ, White SE (2007) Mosquito pathogenic viruses-the last 20 years. In: Floores G (ed) Biorational control of Microbiota mosquitoes, Bulletin 7. American Mosquito Control Association, Fresno, CA, pp 35–49 The microflora and microfauna of an organism. Becnel JJ (2007) Current status of deltabaculoviruses, cypo viruses and chloriridoviruses pathogenic for mosquitoes. Virol Sinica 20:117–127 Chapman HC (ed) (1985) Biological control of mosquitoes, Microbivores Bulletin 6. American Mosquito Control Association, Fresno, CA, 218 pp Kerwin JL, Petersen EE (1997) Fungi: Oomycetes and Chytrid- Small animal fauna that feed on fungi and other iomycetes. In: Lacey LA (ed) Manual of techniques in soil flora. 2378 M Microcaddisflies Microcaddisflies to associate with ants only long enough to lay eggs and will be killed and eaten by the ants if Members of the family Hydrobiosidae (order they dally too long at that task. In contrast, the Trichoptera). slug-like larva are so highly integrated into the  Caddisflies nest of their hosts that worker ants will protect them and carry them away from danger as readily as they do their own brood. Micrococcidae There are 31 species of Microdon in North America. The adults are about one-half inch A family of insects in the superfamily Coccoidae long (1.5 cm) and highly variable in appearance (order Hemiptera). between species. The larvae do not have the  Bugs typical maggot form, and are so atypical in appearance that they were confused with snails and scale insects (Fig. 47), and have been Microcoryphia described as such in early literature. Typical of cyclorrhaphous flies (Diptera), Microdon exhibits three larval instars, followed by a prepupa An apterygote order of insects, also called Archeog- and pupa that forms inside the puparium, the natha. They commonly are known as bristletails. hardened integument of the third instar. The  Bristletails larvae, when active, creep through galleries or tunnels of ant nests and are most often found deep within the nest in close proximity to ant Microdon spp. (Diptera: brood. For most temperate species of Microdon, Syrphidae) there appears to be only one generation a year, with the third instar overwintering. Pupation Gregory S. Paulson (pupariation) occurs in the early spring about Shippensburg University, Shippensburg, PA, USA the time ants become active. The integument of the larvae and puparia of most species is Ants (Hymenoptera: Formicidae), despite their elaborate social organization, are plagued by a multitude of arthropods that live in their nests, from mites to members of their own family. The majority of these myrmecophilous (“ant loving”) arthropods feed upon ant brood, workers, food brought into the colony, or upon other organisms such as fungi which occur in the nest. Some of the most unusual of these myrmecophilous insects are flies of the genus Microdon (Diptera: Syrphidae). Unlike most myrmecophiles, behavioral and morphological adaptations to myrmecophily in Microdon are found only in the immature stages. Adult Microdon are typical syr- Microdon Spp. (Diptera: Syrphidae), phid flies that lack the usual adaptations or Figure 47 Larvae of Microdon. Note the highly behavior that would integrate the fly with the sculptured surface. The large protuberance is habits of the ant. Instead, adult Microdon appear the posterior spiracle. Microfauna M 2379 heavily sculpted with a series of fine lateral and are less specific and can be found in nests of sev- connecting ridges, over a strongly convex dor- eral genera of ants. Microdon are found most com- sal surface. In contrast to the larvae, puparia are monly in nests of Camponotus spp. (carpenter found most frequently near the drier surface of ants) and Formica spp. the nest away from the brood chambers. Pre- sumably this provides the newly emerged adults an opportunity to escape the nest undetected References and unscathed. Adults emerge from puparia in the spring and will generally live only 1–2 Akre RD, Garnett WB, Zack RS (1988) Biology and behavior months. of Microdon piperi in the Pacific Northwest (Diptera: For many years, the food preference of the Syrphidae). J Kans Entomol Soc 61:441–452 Garnett WB, Akre RD, Sehlke G (1985) Cocoon mimicry and larvae was unknown but they were assumed to predation by myrmecophilus Diptera. Fla Entomol feed upon either fungi, infrabuccal pellets of 68:615–621 ants, or even upon tree sap oozing from gallery Howard RW, Akre RD, Garnett WB (1990) Chemical mimicry in an obligate predator of carpenter ants (Hymenoptera: wood. It has been determined that many, if not Formicidae). Ann Entomol Soc Am 83:607–616 all, species of Microdon are actually predators of Howard RW, Stanley-Samuelson DW, Akre RD (1990) Bio- their hosts, feeding upon ant larvae and pupae. synthesis and chemical mimicry of cuticular hydrocar- First instars actually will penetrate the cocoon bons from an obligate predator, Microdon albicomatus Novak (Diptera: Syrphidae) and its ant prey, Myrmica of their host ants to feed upon the enclosed incompleta Provancher (Hymenoptera: Formicidae). brood. Because of this peculiar relationship, J Kans Entomol Soc 63:437–443 Microdon are considered to be “aggressive mimics” of their hosts. Microdon mimic their hosts physically and Microencapsulation chemically. When Microdon larvae are disturbed, they will curl longitudinally approximating the A method of formulating insecticides and other shape of an ant cocoon. More importantly, Micro- chemicals for controlled release. Microscopic don are able to produce chemicals, a variety of spheres containing the chemical are formed from large hydrocarbon molecules, that are distrib- a polymer with various degrees of cross-linking, uted over their integument. These cuticular thickness of the capsule wall, and sphere size, hydrocarbons are the same recognition chemi- thereby regulating release rates of the chemicals. cals used by the ants to identify other members This usually produces a longer-lasting method of of their nest. The type and amount of these mol- application, reduced volatility, and lower mamma- ecules produces a colony-specific chemical pro- lian toxicity. Sometimes bees are at greater risk, file that the Microdon are able to almost however, due to their tendency to confuse the identically match, chemically integrating them spheres with pollen grains. into the host nest. This is truly an example of  Insecticides chemical mimicry. In other words, the Microdon  Insecticide Formulation larvae are not using cuticular hydrocarbons produced by the ants to camouflage themselves but rather are somehow able to sense the chemical profile of their hosts and produce cuticular Microfauna hydrocarbons to mimic that profile. Host range of Microdon varies with species. Soil invertebrates in the small size class, usually Some species are highly host specific and are found less than 2 mm in width (contrast with macro- only in nests of one or two species, while others fauna and megafauna). 2380 M Micromalthidae Micromalthidae under high magnification, and impart a rough feel to the body when they are numerous. A family of beetles (order Coleoptera). They commonly are known as telephone-pole beetles.  Beetles Microsporidae

A family of beetles (order Coleoptera). They com- Micropezidae monly are known as minute bog beetles.  Beetles A family of flies (order Diptera). They commonly are known as stilt-legged flies.  Flies Microsporidia (Phylum Microsporida)

Microphysidae Leellen F. Solter Illinois Natural History Survey, Champaign, A family of bugs (order Hemiptera). IL, USA  Bugs Microsporidia are obligately pathogenic, single- celled, eukaryotic organisms of which nearly 1,000 Micropterigidae species have been described, over 700 from insect hosts. Lacking mitochondria, centrioles, peroxi- A family of moths (order Lepidoptera). They com- somes and classical Golgi bodies, and possessing a monly are known as mandibulate archaic moths. nonmotile amoeba-like vegetative form, microspo-  Mandibulate Archaic Moths ridia were considered until recently to be primi-  Butterflies and Moths tive members of the Protozoa. Molecular analyses, however, have determined that the group possesses several gene sequences that suggest a close Micropterous relationship to the fungi. The first microsporidium studied was the The condition in which the wings of the insect are causal agent of “pebrine disease” of silkworms small, and usually non-functional (compare with (Bombyx mori L.), a disease that nearly caused the brachypterous and macropterous). demise of the silk industry in France in the 1860s. Louis Pasteur recognized the infectious nature of the disease and developed a screening technique Micropyle to rid the industry silkworm colonies of the pathogen. The microsporidium was later described as One or more pores or small holes in the egg Nosema bombycis Naegli, the type species of the chorion through which sperm enter. well-known genus Nosema. Microsporidia infect all groups of vertebrate and invertebrate animals, as well as some protozo- Microspines ans, but are particularly common in fish and arthropods. Mammals also host some microspo- Minute spines located on various locations of the ridian taxa and immune-compromised humans body of some insects; they usually are visible only are among the known hosts. Insects, though, Microsporidia (Phylum Microsporida) M 2381 comprise the largest group of animals from which from terrestrial hosts typically possess smooth microsporidia have been described, probably non-ornamented spores; spores of microsporidia because of the ease of collecting large numbers of from aquatic hosts such as mosquitoes and black hosts for diagnosis and the impetus to discover flies may include “wings,” mucoid coats, flagella- biological control agents for insect pests. Some like appendages, or a patterned surface structure. well-studied insect species have been shown to Spores of all species are discernable as brightly harbor several species of microsporidia. No refractive forms under 250–400 x phase contrast microsporidia occur as plant pathogens. light microscopy in crushed host tissues, although Microsporidia from insects are most often aquatic spores, with their typically thinner spore and most easily observed in their environmen- walls may appear more grayish with internal tally resistant infective form, the spore (Fig. 48). structures somewhat apparent. Spores are relatively uniform within a species but Infection by microsporidia occurs either via different species range in size from 1 to 12 µ in ingestion of infective environmental spores by a length and vary in shape from long oval to round, susceptible host, transmission inside or on the reniform, spindle-like, or tear-shaped. Species surface of eggs oviposited by infected female hosts

Microsporidia (Phylum Microsporidia), Figure 48 Images of microsporidia. Top left, transmission electron micrograph of an environmentally resistant microsporidian spore, approximately 4 µ in length (courtesy J. Maddox and Society of Invertebrate Pathology); top right, scanning electron micrograph of germinating spore (courtesy J. Becnel and Society of Invertebrate Pathology); bottom right, transmission electron micrograph of vegetative form, approximately 6 µ in diameter (photo by J. Maddox); bottom left, light photomicrograph of an insect host midgut epithelial cell cytoplasm filled with spores (photo by L. Solter). 2382 M Microsporidia (Phylum Microsporida) or, much less frequently, mechanical injection by quite virulent, nearly always killing larval hosts parasitoids. Very often, a microsporidium is trans- prior to or during pupation, but most appear to be mitted both orally and via the eggs. The most chronic pathogens that are more likely to suppress unique characteristic of microsporidia is the infec- the host populations by lowering fitness of indi- tion mechanism. Along with a single or double viduals due to decreased adult life span, fecundity nucleus (diplokaryon), cytoplasm and plasma and movement, and higher larval mortality in membranes, a polar filament is coiled within the infected offspring. Most microsporidian species spore. When the spore is activated to germinate by seem to have some deleterious effects on the host, conditions in the gut lumen of the host, the polar but some may be nearly benign. filament everts through a disk at its attachment The epizootiology of microsporidia in host point on the spore and the contents of the spore populations also varies greatly but many, if not are emptied into the host gut cell to form a vegeta- most, species appear to be strongly host density tive sporoplasm. dependent and can occur in high prevalences, up The membrane bound sporoplasm undergoes to 100% of the host population, in high-density division in the cytoplasm of the host’s gut cells. host populations. Some species may be maintained Some species of microsporidia form a rudimen- in host populations for long periods of time at tary autoinfective spore form, which germinates very low prevalences in stable host populations. inside the cell and appears to be a mechanism for There are (Table 8) numerous examples of insect ensuring that the non-motile pathogen locates the species, both agricultural pests and naturally suitable tissues for proliferation and maturation of occurring, that are strongly regulated by the pres- infective spores. The tissues infected vary for dif- ence of microsporidian pathogens. Two such ferent species of microsporidia; some species per- examples are the European corn borer, Ostrinia vade all host body tissues and some are limited to nubilalis, which is regulated by Nosema pyrausta one or more specific tissues, such as the midgut or in parts of midwestern North America, and Cana- the fat body. dian populations of the spruce budworm, Choris- Transmission mechanisms may be deter- toneura fumiferana, which are often strongly mined by the tissues that are targeted. For exam- suppressed by Nosema fumiferanae. ple, species that infect the gonads, especially of In general, efforts to use microsporidia as the female hosts, are usually transmitted to the microbial insecticides have been unsuccessful. host’s offspring. Infective spores from midgut Long-term studies of Nosema locustae, the only infections may be shed in feces of infected hosts, microsporidium ever registered (U.S. EPA) for use and silk gland infections may be transmitted by as an insecticide, have shown that it probably func- exposure of individual hosts to the silk of infected tions more effectively as a long-term biological conspecific individuals. Fat body utilizing species control agent rather than as a “biological insecti- are probably released into the environment when cide.” In general, microsporidia being evaluated dead larvae decompose. Some microsporidia for use as biological control agents against insect require an intermediate host for transmission and pests should probably be considered as similar in produce several spore types. For example, the dynamics and host effects to parasitoids. Amblyospora spp. in mosquitoes require copepod One of the most common problems associated hosts in the life cycle to produce spores infective with microsporidia are infections in colony insects in turn to the mosquito hosts. and arthropods used for research, or in beneficials The effects on hosts of a microsporidian infec- that are mass produced for biological control proj- tion vary widely depending on the microsporidian ects. As in natural insect populations, symptoms are species, initial dosage, mechanism of transmission, often subtle and may involve straggling or slow lar- host condition, and other factors. Some species are val development, lowered fecundity, and early larval Midges M 2383 Microsporidia (Phylum Microsporidia), Table 8 Common insect microsporidioses Microsporidium Host Host common name Amblyospora spp. Aedes spp. and Culex spp. mosquitoes Edhazardia aedis Aedes aegypti yellow fever mosquito Endoreticulatus schubergi various Lepidoptera Nosema algerae Anopheles spp. mosquitoes Nosema apis (“pebrine disease”) Apis mellifera European honey bee Nosema fumiferanae Choristoneura fumiferana spruce budworm Nosema locustae various spp. grasshoppers and crickets Nosema kingi Drosophila spp. fruit flies Nosema lymantriae Lymantria dispar gypsy moth Nosema pyrausta Ostrinia nubilalis European corn borer Nosema tortricis Tortrix viridana green tortrix Nosema whitei Tribolium spp. flour beetles Octosporea spp. muscoid and syrphid flies Thelohania solenopsis Solenopsis invicta fire ants Vairimorpha necatrix various Noctuidae armyworms and other noctuids

death. Infection can alter experimental results due Microthoraciidae to changes in host physiology and compromise biological control efforts. A family of sucking lice (order Phthiraptera).  Chewing and Sucking Lice References Microtrichia Becnel JJ, Andreadis TG (1999) Microsporidia in insects. In: Wittner M, Weiss LM (eds) The microsporidia and Minute hair-like processes on the wings of certain microsporidiosis. American Society for Microbiology, insects, though sometimes this term is used to Washington, DC, pp 447–501 describe processes elsewhere. Boucias DG, Pendland JC (1998) Principles of insect pathology. Kluwer Academic Publishers, Boston, MA, 537 pp Undeen AH, Vavra J (1997) Research methods for entomopathogenic protozoa. In: Lacey L (ed) Manual of tech- Middorsal niques in insect pathology. Academic Press, San Diego, CA, pp 117–151 A term referring to the middle of the upper region Bulla LA Jr, Cheng TC (1977) Comparative pathobiology, vol 2: Systematics of microsporidia. Plenum Press, New or “back” (as opposed to the subdorsal or slightly York, NY, 510 pp to the side, or lateral). Tanada Y, Kaya HK (1993) Insect pathology. Academic Press, Inc., San Diego, CA, 666 pp Midges

Microsporidiosis Members of the family Chironomidae (order Diptera). Infection with microsporidia.  Flies 2384 M Midges as Human Food Midges as Human Food

Meir Broza University of Haifa, Haifa, Israel

Cakes made from non-biting midges (Diptera: Chaoboridae) are a traditional food in African communities living along the shores of lakes in the African Rift Valley. Chaoborid swarms above the lakes may stretch over 10–32 miles and contain many millions of insects. They were first described from Lake Nyasa by the famous explorer David Livingstone, and also occur on the Ugandan side of Lake Victoria. The swarming gnats are called “E sami” by local people. It has been reported that the people compressed the flies into cakes that were used in some unknown manner as food. Also noted was the malodor of masses of dead flies that accumulated after the swarms, and the fact that the arrival of huge clouds of these gnats produced outbreaks of nasal catarrh among the white inhabitants. Gnat cakes are called “kungu cakes” (Fig. 49) in the literature. In the Lake Victoria area, kungu is a term used as a prefix for insect specimens, or product made from insects. A major component of such cakes is a species of fly belonging to the family Chaoboridae, Chaoborus edulis Edwards. As the specific name implies, F. W. Edwards knew that this species was edible when he described it. Minor constituents of the cake include chironomid species in the genus Tany- tarsus and Cladotanytarsus. Phylogenetically and anatomically, the Chaoboridae are a Nema- toceran family somewhat closer to Culicidae than to Chironomidae. They still bear mouthparts, but not functional ones, and they do not feed as adults, similar to chironomid adults. The male flies have plumose antennae, as do chironomid males. Midges as Human Food, Figure 49 Midges as The chaoborid larvae are known as phantom human food: above, insect “cakes” prepared from midges. They rest close to the bottom of the lakeflies; center, basket for sweeping flies, Lake water body during the daytime, but are active Victoria, Kenya; bottom, swarm of midges above predators during the night. A common North Lake Victoria (bottom photo by Hanna Nadel). Midgut M 2385 American species in the same family, Mochlonyx when sunny. Cakes are stored in a dry place cinctipes, swarms in clearings of woods at sunset. inside the house before cooking in vegetable or The African species, C. edulis, undergoes a peri- chicken soup, or boiling in water only, and serv- odic emergence according to the lunar cycle. ing with a dip prepared from milk and salt. Synchronous emergence of adult males and They are also served fresh as a black cake (not females creates huge swarms and mating takes too tasty to an inexperienced western palate, in place above the lake surface. The flying females contrast to termites which are delicious). drop their eggs, packed together in gelatinous Analysis of kungu cake indicates that its masses, into the water and the swarm then moves water content is 20% and the dry weight towards the lakeshore. includes 58.9% protein and 20.3% fats. The These clouds of insects on the Kenyan other 20.8% is mainly chitin. This protein is shore of Lake Victoria can be observed during highly digestible (about 73%) for human diet, the long rains. They can be seen at a consider- and nutritious. It may serve as high quality food able distance from the shore above the middle additive. of the lake during the early afternoon, and they  Entomophagy: Human Consumption of reach land around sunset or soon thereafter. Insects The edge of the lake at this time becomes an impenetrable column of insects that filled the ears, nostrils and eyes. It is reported that four References local fishermen once lost their way inside such a cloud in the middle of the lake and died in a Bergeron D, Bushway RJ, Roberts FL (1988) The nutrient subsequent accident. Adjacent plants may be composition of an insect flour sample from Lake completely covered with flies, wings touching Victoria, Uganda. J Food Compost Anal 1:371–377 wings. In many cases, the swarms develop dur- Carr A (1964) Ulendo, travels of a naturalist in and out of ing the early afternoon together with a build- Africa. University Press of Florida, Gainesville, FL Cranston PS (1995) Medical Significance. In: Armitage P, up of dark clouds and, according to local claims, Cranston PS, Pinder LCV (eds) The Chironomidae. their appearance often precedes a strong Chapman and Hall, London, UK, pp 365–384 thunderstorm. Yashuv A, Ben Shachar R (1967) Breeding and growth of Flies may be collected by local women; it is Mugilidae II: feeding experiments under laboratory conditions with Mugil cephalus. Bamidgeh 19:50–66 possible to fill large plastic bags, many gallons (In Hebrew with English summary) in volume, with flies. “Kungu” (insect) cakes are prepared from the flies. They are similar in size to a commercial hamburger, but are completely black. Although preparation and eating these Midgut midge cakes is not a common habit today, it still can be seen along the shore of the Rift Valley The middle portion of the gut, distinguished as Lakes. Traditionally, flies are collected by rotat- being unprotected by cuticle but lined with a peri- ing a basket with a long handle in a manner trophic membrane. In most insects the midgut is very similar to that (Fig. 49) of a modern insect the principal site of digestion and absorption, and sweep net. The simple preservation procedure the source of digestive (Fig. 50) enzymes. Anatom- used is as follows: the accumulated flies are ically, the midgut commences after the proventric- removed from the basket and flattened in the ulus and terminates at the ileum and juncture of hands as when making chapatti bread; the cakes the Malpighian tubules. are then laid on banana leaves on the straw roof  Alimentary System of the local houses to dry. This takes 3–4 days  Alimentary Canal and Digestion 2386 M Midgut and Insect Pathogens

Foregut Midgut Hindgut Esophagus Gastric Ileum Crop caecum Ventriculus Pylorus Rectum Pharynx

Buccal Anus cavity Proventriculus Mouth Malpighian tubule Midgut, Figure 50 Generalized insect alimentary system (adapted from Chapman, The insects: structure and function).

Midgut and Insect Pathogens is the primary infection site of the major insect viral pathogens including baculoviruses, cypo- Ping Wang viruses and entomopoxviruses. Infection of Cornell University, Geneva, NY, USA some viral pathogens in the midgut is limited and the infection in the midgut epithelium is a The alimentary canal in insects is the primary mode of entry of the viruses into the hemocoel location interfacing with their host organisms to establish systemic infection (e.g., baculovirus and other biotic and abiotic factors from the infection and entomopoxvirus infection in lepi- environment. The insect alimentary canal can be dopterans). For some viruses, the infection in divided into three distinct regions, the foregut, insects is restricted to the midgut cells (e.g., midgut and hindgut, based on their embryonic cypovirus infections in insects). The midgut is origins, structure and physiological functions. not the common portal of entry for fungal The foregut and hindgut are derived from embry- pathogens, but fungal infection through the onic ectoderm and are covered by cuticle. The gut may occur in some cases. Protozoan patho- midgut is derived from embryonic mesoderm gens mostly infect insects through the diges- and does not have the protective cuticle cover- tive tract. In addition to microbial pathogens, ing. The midgut is the region of the alimentary insect pathogenic nematodes may also enter canal that actively interacts with the gut content and penetrate through the midgut as a mode of from the environment and performs the primary entry into the hemocoel. functions of food digestion and subsequent The midgut encounters a variety of micro nutrient uptake. In direct contact with the gut organisms ingested with dietary materials. In the contents without protection by cuticle covering, midgut, insects are equipped with various mech- the midgut constantly faces physical, chemical anisms of defense against the pathogens. The and biological challenges from the environment. midgut peritrophic membrane (PM), alkaline pH It is a primary target and portal of entry for vari- in the midgut lumen, digestive enzymes, antimi- ous pathogenic organisms. crobial proteins and other factors contribute to Bacterial pathogens primarily target the the defense against pathogens. Meanwhile, patho- midgut to gain entry into the hemocoel. Patho- gens have adapted mechanisms to infect insect genic bacteria (e.g., Bacillus thuringiensis and hosts. The outcomes of midgut-pathogen inter- B. sphaericus) commonly produce enzymes or actions, which are often multifaceted, critically toxins to target and eventually disrupt the determine the pathogenesis of the pathogen. midgut epithelium, which enables the bacteria The bacterial pathogen B. thuringiensis (Bt) pro- to penetrate through the midgut barrier into the duces proteinaceous toxins to target the midgut hemocoel for productive infection. The midgut epithelial cells to break the midgut barrier. The Migratory Grasshopper, Melanoplus sanguinipes (Fabricius) (Orthoptera: Acrididae) M 2387 major Bt toxins are known as Cry proteins (crys- The midgut is in constant contact with vari- tal proteins) or Cry toxins, which are produced ous ingested microorganisms, and interactions of as protoxins in a form of stable crystals in the the midgut with the microorganisms are complex. bacterium. Once ingested by an insect into the The interactions between the midgut and micro- midgut, the toxin crystals dissolve in the alka- organisms critically determine the insect-microbe line pH in the midgut and the dissolved toxin is association to be pathogenic, non-pathogenic or proteolytically activated by midgut digestive pro- symbiotic. teinases. The activated Cry toxin then penetrates  Alimentary Canal and Digestion through the peritrophic membrane and specifically binds to its receptor on the midgut epithelial cells. With involvement of other midgut References components, the binding of a Cry toxin to the midgut receptor leads to midgut cell lysis, which Lehane MJ, Billingsley PF (1996) Biology of the insect midgut. enables entry of the bacteria into the hemocoel Chapman and Hall, New York, NY, 486 pp Tanada Y, Kaya H (1993) Insect pathology. Academic Press, for infection. The insect pathogenic baculovi- San Diego, CA, 666 pp ruses, cypoviruses and entomopoxviruses are Wang P, Granados RR (2001) Molecular structure of the peri- embedded in proteinaceous crystalline inclu- trophic membrane (PM): identification of potential PM sions, the viral occlusion bodies, which facilitate target sites for insect control. Arch Insect Biochem Physiol 47:110–118 survival of the viruses in the environment. In the insect midgut, under the condition of alkaline pH and presence of rich proteinases the occlusion bodies are dissolved and infectious virus Migration particles (virions) are released into the midgut lumen to initiate infection of the midgut cells. A special form of dispersal in which insects The midgut peritrophic membrane plays an move in a specific direction, and movement is important role in defense against pathogens in at least partly under the control of the insects, general. However, some pathogens have evolved rather than passive (e.g., being blown by wind). mechanisms to overcome the peritrophic mem- Migrants that are arriving are called immi- brane barrier. A unique group of proteases, namely grants, and those that are departing are called baculovirus enhancins, are produced by some bac- emigrants. uloviruses and co-embedded in the viral occlusion bodies. In the midgut, an enhancin is released with the virus particles and specifically degrades the Migratory Grasshopper, major peritrophic membrane protein, the insect Melanoplus sanguinipes intestinal mucin. The degradation of the intestinal (Fabricius) (Orthoptera: mucin in the peritrophic membrane results in dis- Acrididae) integration of the peritrophic membrane structure, leading to permeability of the peritrophic mem- John L. Capinera brane to the virus particles. Similarly, in the infec- University of Florida, Gainesville, FL, USA tion of malaria parasites in mosquito midgut, the malaria parasite disrupts the peritrophic mem- This native grasshopper is extremely adaptable, brane by secretion of a chitinase to digest the chitin and found throughout most of North America. It in the peritrophic membrane, enabling the parasite is found in every state in the continental United to pass through the peritrophic membrane barrier States, and in every province in Canada. It is absent and reach the midgut cells. from only the northernmost, coldest regions of 2388 M Migratory Grasshopper, Melanoplus sanguinipes (Fabricius) (Orthoptera: Acrididae) Canada, and from southern Florida and Texas. Its conditions about 80% of embryonic develop- distribution does not extend south into Mexico. ment occurs in the autumn before the onset of diapause, with the remainder of development in the spring after a period of cold weather termi- Life History nates egg diapause. Nymphs can develop over a range of about In most areas of its range, migratory grasshopper 22–27°C, but early instars suffer high mortality at produces a single generation, and overwinters in both extremes in temperature. Nymphal develop- the egg stage. However, in southern portions of its ment requires about 42, 27, and 23 days when cul- range two generations may occur annually. Eggs tured at a constant temperature of 27, 32, and 37°C. hatch relatively early, usually beginning in early Diet also affects development rate. When reared at June but about a week after twostriped grasshop- 30°C, favorable plants such as tansymustard allow per, Melanoplus bivittatus (Say) begins to hatch. complete nymphal development in about 29 days, Hatching is protracted and may require up to six whereas nymphs developing on less suitable plants weeks in an area, resulting in asynchronous devel- such as western wheatgrass require about 42 days. opment of the population. Early hatching individ- Most field observations suggest that nymphal uals mature early in the summer and have adequate development requires 35–45 days. Normally there time for reproduction whereas late-hatching indi- are five instars, though if cultured at low tempera- viduals are handicapped by the onset of cold tures, six instars is most common. weather. The nymphs are tan or gray, occasionally Eggs are yellowish in color, elongate-elliptical greenish, throughout nymphal development. They and slightly curved in shape. One side is convex bear a curved black stripe that extends from and the opposite side concave, causing the eggs behind each eye across the pronotum. The lower to resemble a banana in shape. Eggs measure edge of the stripe is bordered in white. The outer about 4.5 mm in length and 1.2 mm in width. face of the hind femur is marked with an inter- The eggs are arranged in two columns within a rupted black stripe. Body length in instars 1–5 is frothy egg pod. Egg pods contain 18–20 eggs 4–6, 6–8, 8–11, 11–16, and 16–23 mm, respectively. per pod, and are buried to a depth of about 35 The number of antennal segments is 12–13, 15–17, mm. The pods are curved, about 25 mm in 18–20, 21–22, and 22–24 in the corresponding length, and 3–4 mm in diameter. The upper por- instars. tion contains only froth, allowing ready escape The adult is a medium-sized species, of the nymphs when they hatch. Females can measuring 20–26 mm in length in males and produce 7–10 pods if fed high-quality diets; up 20–29 mm in females. They are grayish brown in to 20 per female is recorded, usually at 2–3 day color, and often tinged with reddish brown. A intervals. Thus, fecundity of about 200 eggs per broad black stripe extends back from the (Fig. 51) female is possible. Natural habitats vary greatly eye and about two-thirds of the length of the pro- in suitability, however, and reproductive poten- notum. The forewings are grayish brown or tial is sometimes affected. In one study con- brown, usually with a row of brown spots cen- ducted in Montana, for example, females were trally. The hind wings are colorless. The hind able to produce only 3–4 egg pods annually. Egg femora are not distinctly marked. The hind tibiae pods are inserted into the soil among the roots are greenish blue or red in color. The cerci of of plants. Migratory grasshopper is more likely males are broad and flat, turning dorsally at the to deposit pods within crop fields, particularly tip. The subgenital plate is elongate, and bears a among wheat stubble, than other common crop- notch and groove apically. Females have a preovi- feeding Melanoplus spp. Under normal weather position period of 2–4 weeks. Adults normally Migratory Grasshopper, Melanoplus sanguinipes (Fabricius) (Orthoptera: Acrididae) M 2389 abundance of annual broadleaf plants. Among the preferred plants are dandelion, Taraxacum offici- nale; stinkweed, Thlaspi arvense; Johnsongrass, Sorghum halepense; Kentucky bluegrass, Poa pratensis; shepherdspurse, Capsella bursa-pastoris; pepperweed, Lepidium spp.; tansymustard, Descu- rainia sophia; western wheatgrass, Agropyron smithii; winter mustard, Sisymbrium irio; young Migratory Grasshopper, Melanoplus Russian thistle, Salsola kali; and young rabbit- sanguinipes (Fabricius) (Orthoptera: Acrididae), brush, Chrysothamnus spp. Among the preferred Figure 51 Adult male of migratory grasshopper, weeds eaten in North Dakota alfalfa fields are awn- Melanoplus sanguinipes (Fabricius). less bromegrass, Bromus inermis; kochia, Kochia scoparia; field sowthistle, Sonchus arvensis; field live 60–90 days, though with good food and bindweed, Convolvulus arvensis; and Russian this- weather, and living under low density conditions, tle, Salsola kali. On prairie, however, the preferred longevity may be extended considerably. They host plants are Kentucky bluegrass, Poa pratensis; can mate repeatedly. leadplant, Amorpha canescens; white sage, Artemi- Nymphs and adults are affected by daily sia ludoviciana; and western ragweed, Ambrosia change in temperature. Activity levels at the soil psilostachya. surface, including feeding, are at their maximum Migratory grasshopper does not normally when the air temperature is 18–25°C. This often infest vegetable crops to a great extent, preferring results in a peak in feeding in late morning, fol- weedy areas along fences, irrigation ditches, road- lowed by cessation of feeding at mid-day due to sides, and in pastures. However, as favored food excessively hot temperatures, and then perhaps a plants become over-mature, desiccated, or depleted, secondary peak in feeding in the afternoon as grasshoppers will move into vegetable crops. This temperatures cool. Mass flights by adults take is especially likely during periods when grasshop- place only if air temperatures are high, often pers are extremely abundant. Field crops are more about 29°C, but high densities and light wind often injured, particularly alfalfa, barley, corn, oat, also are requisites. When it is hot, grasshoppers and wheat. However, as in the case with vegetables, tend to climb upward to escape the soil, which is when grasshoppers are numerous they will damage usually considerably warmer than the air tem- buckwheat, clover, flax, millet, rye, youngsorghum, perature. However, they also tend to roost on tall soybean, sugarbeet, timothy, and tobacco. Even vegetation at night, as this allows them to be fruits such as apple, cherry, currant, grape, peach, warmed by sunlight early in the morning, thus plum and strawberry, as well as numerous flowers extending their period of activity. and shrubs, are attacked during periods of This species accepts a wide range of food abundance. plants, and occurs in a wide range of habitats. Rel- Not surprisingly, there is a strong positive ative to the other common crop-feeding Melano- relationship between plant preference and grass- plus spp., migratory grasshopper is more tolerant hopper survival. Among the plants most suitable of arid, shortgrass environments. It tends to prefer for nymphal survival were wheat, sunflower, alfalfa, annual broadleaf plants, but will eat grasses. Dry corn and barley, accounting for the reputation of plant material is an important element of the diet this species as a severe pest in central and western in addition to succulent leaf tissue. Many authors North America. (Alfalfa is an unusual host, how- have noted that the population abundance of ever, because although it is quite suitable for large migratory grasshopper is correlated with the nymphs, it is but a poor source of food for the 2390 M Migratory Grasshopper, Melanoplus sanguinipes (Fabricius) (Orthoptera: Acrididae) youngest of the species.) Several broadleaf weeds and deposit an egg on the surface of the grass- including dandelion; downy chess, Bromus tecto- hopper. Upon hatching, the larva devours the rum; tumblemustard, Sisymbrium altissimum; paralyzed grasshopper. Predatory beetles (Coleoptera) slimleaf scurfpea, Psoralea tenuiflora; and prickly attack the egg, nymphal and adult stages of grass lettuce, Lactuca scariola are quite satisfactory for hoppers, and include ground beetles (Carabidae), survival, though not as suitable as the crop plants. tiger beetles (Cicindelidae), soldier beetles (Can- Among the least suitable plants are common prai- tharidae), and blister beetles (Meloidae). Blister rie grasses such as prairie sandgrass, Triplasis pur- beetles are most important, though because the purea; blue grama, Bouteloua gracilis; six-weeks grasshopper egg pod is the stage destroyed, their fescue, Festuca octoflora; needle-and-thread, Stipa effect is often not appreciated. Several studies comata; desert saltgrass, Distichlis stricta; green conducted during the period 1938–1940 pro- needlegrass, Stipa viridula; and Indian ricegrass, duced an average of 8.8% of egg pods destroyed Oryzopsis hymenoides. Diet also affects fecundity, by blister beetles. Flies also are important preda- with favored food such as dandelion resulting in tors, particularly robber flies (Asilidae) and bee production of a mean value of 3.5 egg pods per flies (Bombyliidae). Robber fly larvae and Gryllus female during a 3-week period, whereas grasshop- spp. field crickets (Orthoptera: Gryllidae) occa- pers fed a mixture of prairie grasses produce only sionally attack egg pods, and robber fly adults rou- 0.3 pods per female. tinely attack nymphs and adults of grasshoppers, Many insects parasitize or eat Melanoplus though other insects also are taken. Robber flies grasshoppers. The most important parasitoids undoubtedly are important predators under range- are nymph- and adult-attacking flies (Diptera) in land conditions, but predation rates of grasshop- the families Anthomyiidae, Nemestrinidae, Sar- pers in cropping systems has not been determined. cophagidae, and Tachinidae, though egg parasi- Also, the propensity of robber flies to capture other toids (Hymenoptera: Scelionidae) also cause predators, such as sarcophagids, significantly mortality in grasshopper populations. In Oregon, reduces their value. Bee fly larvae are predatory on over 70% of migratory grasshoppers were para- grasshopper eggs and on other insects. In western sitized by the nemestrinid Neorhynchocephalus studies, an average of 6.2% of egg pods were sackenii (Williston), resulting in reduced longevity destroyed by bee fly larvae. and reproduction. Other Melanoplus spp. also are Birds are known to be important predators of affected by this fly, though grasshopper popula- grasshoppers. They are among the most important tions on rangeland, not cropland, are usually sources of food for many avian species due to their affected. In a study of migratory grasshopper large size and abundance. The great abundance of parasitism conducted in Ontario, the incidence grasshoppers in the spring coincides with the of parasitism reached about 7% by the end of period when most birds are nesting. Birds forage September, with Blaesoxipha hunteri (Hough) and freely on grasshoppers in open areas such as B. atlantis (Aldrich) (both Diptera: Sarcophagi- grasslands, with some species consuming 65–150 dae) the most effective parasitoids. In Montana, grasshoppers per day. Although avian predators parasitism of migratory grasshopper parasitism significantly reduce the abundance of grasshop- was estimated to 15–41%, with anthomyids and pers in grasslands, it is less certain that they for- sarcophagids accounting for 50 and 35% of the age freely in crops. parasitism, respectively. Microbial pathogens can be quite impor- Among the most important predators are tant mortality agents, especially when weather sphecid wasps (Hymenoptera: Sphecidae). Adult conditions are suboptimal for grasshoppers, or sphecids capture and paralyze nymphal and adult when grasshoppers are very abundant. The grasshoppers, bury them within cells in the soil, principal microbial pathogens of grasshoppers Migratory Grasshopper, Melanoplus sanguinipes (Fabricius) (Orthoptera: Acrididae) M 2391 are fungi, viruses, protozoans, and nematodes desiccation-resistant eggs. The eggs hatch when and nematomorphs. consumed by grasshoppers, and the resulting lar- The fungusEntomophthora grylli causes “sum- vae kill the grasshoppers, return to the soil, and mit disease,” a behavior wherein grasshoppers continue the life cycle. These nematodes appar- ascend vegetation, cling to the uppermost point, ently do not thrive in arid areas, as the adults only and perish. In some areas, particularly near bodies emerge during wet periods, and are more com- of water, large numbers of dead grasshoppers can mon in irrigated croplands than dry rangeland. be found attached to plants. Melanoplus spp. are Sometimes they parasitize up to 70% of grasshop- susceptible to one pathotype of the fungus, and pers in an area. Nematomorphs, commonly called significant grasshopper population decreases have horsehair worms, resemble nematodes but tend to been linked to the incidence of summit disease. be much longer. They are rare, possibly because Infection normally occurs when nymphs contact part of their life cycle must occur in water, but they spores that are sheltered in the soil. Spores pro- attract considerable attention because of their duced in grasshoppers dying from this disease large size. remain in cadavers or soil for protracted periods Migratory grasshopper is greatly influenced of time. Attempts to manipulate this pathogen by weather. Through most of its range longevity have met with mixed results. This is the only com- and reproduction are limited by shortage of warm mon naturally occurring fungus of grasshoppers. weather. Thus, abnormally warm and dry periods Several viruses called entomopoxviruses of about 3 years stimulate increase in grasshopper affect grasshoppers. One such virus, Melanoplus abundance. Warm weather during spring and sanguinipes entomopoxvirus, affects the crop- autumn is particularly important. Cool and cloudy feeding Melanoplus spp. and American grass weather in the spring inhibits feeding by young hopper, Schistocerca americana (Drury). The nymphs, and results in high mortality. Also, adults virus disease spreads naturally by cadaver feed- have the potential to be long-lived and highly ing. Infected grasshoppers are pale colored and fecund, but their reproductive effort is normally lethargic, have prolonged developmental periods, terminated prematurely by the onset of cold and often perish. These diseases are quite rare in weather. When summers are hot or prolonged, the field. development proceeds faster or longer, resulting Several types of protozoa are associated in greater egg production. In southern areas grass- with grasshoppers, including amoebae, eugre- hoppers are less limited by shortage of warm garines, and neogregarines, but the most impor- weather, but more affected by shortages of food. tant are microsporidia. Species of Nosema are Therefore, occurrence of precipitation early in the most common, and Nosema locustae has been season to provide luxurious foliage, especially developed as a microbial insecticide. Nosema broadleaf weed vegetation, is an important prereq- spp. affect feeding, development, reproduction uisite for population increase. and survival, and are transmitted by ingestion. However, they infrequently appear at high levels in natural populations. Damage Nematodes are important mortality factors of grasshoppers in South America, New Zealand and Migratory grasshopper is a defoliator, often com- Australia, but in North America only Mermis pletely removing leafy vegetation and leaving only nigrescens, Agamermis decaudata, and Hexamer- stem tissue. Sometimes other tissue is eaten; heads mis spp. affect grasshoppers. Mermis nigrescens is of wheat may be clipped, for example. Migratory most important, and is unique in that nematodes grasshopper thrives on rangeland that has a high crawl from the soil onto vegetation to deposit density of broadleaf weeds, so it sometimes moves 2392 M Migratory Grasshopper, Melanoplus sanguinipes (Fabricius) (Orthoptera: Acrididae) from grazing land to nearby irrigated crops. In this injured. Therefore, application of insecticide behavior it differs from some other species, par- to the borders of crop fields is often adequate to ticularly differential grasshopper, Melanoplus dif- protect an entire field. It is even better to apply ferentialis (Thomas), and twostriped grasshopper, insecticides to the developing grasshopper pop- M. bivittatus (Say), which favor the taller undis- ulations in weedy areas before they move to turbed vegetation usually associated with fences crops. This not only minimizes damage to crop and irrigation ditches, and usually do not develop plants, but often results in younger grasshoppers high numbers on grazing land. Migratory grass- being targeted for elimination. Younger grasshopper is often quite dispersive, and of course this hoppers are more susceptible to insecticides, behavior is the basis for the common name. When with large nymphs and adults sometimes diffi- the grasshoppers are developing at high densities, cult to kill. the weather is abnormally warm, and a light wind Application of insecticide-treated bait is an is present, swarms of grasshoppers may disperse effective alternative to foliar treatments for Mel- tens or even hundreds of kilometers and descend anoplus spp. because these grasshoppers spend without warning to cause immense damage. With considerable time on the soil where they come the availability of modern insecticides and aircraft into contact with baits. Bait formulations are for application, such potential disasters can be bulky and more difficult to apply than liquid dealt with quickly and efficiently. When such products, so they are less often used, but have the insecticide and effective application technologies advantage of limiting exposure of crops to insec- are not available, or where environmentally sensi- ticide residue and of minimizing mortality of tive land or crops are concerned, grasshopper beneficial insects such as predators and parasi- swarms can be disastrous. This species is the most toids due to insecticide exposure. Also, the total important grasshopper pest in western North amount of insecticide active ingredient neces- America. sary to obtain control is usually considerably less when applied by bait because the grasshoppers actively seek out and ingest the toxin. Finally, Management for relatively expensive products that must be ingested to be effective, such as microbial insec- Grasshopper populations are usually assessed by ticides, baits are the most effective delivery visual observation. A sweepnet is a useful tool to system. aid in collection, and its use a prerequisite to iden- The attractant used most commonly for tification of the species complex. It is important to grasshopper bait is flaky wheat bran, though determine if grasshoppers collected from noncrop other products such as rolled oats are sometimes areas are crop-feeding species because there are suggested. No additives, other than insecticide many nonpest grasshoppers that restrict their (usually 5% active ingredient), are necessary feeding to grasses or weeds. It is advisable to mon- because the wheat bran alone is quite attractive itor nearby uncultivated land, particularly weedy to Melanoplus grasshoppers. Other additives such areas, in addition to crop plants, due to the ten- as sawdust, water, vegetable or mineral oil, molas- dency of the pest species to invade crops later in ses, amyl acetate, salt, or sugar have been sug- the season. gested, but provide little or no additional benefit Liquid formulations of insecticides are over dry bran. The bait should be broadcast commonly applied to foliage to protect against widely to maximize the likelihood of grass damage. Because grasshoppers rarely develop hopper contact, and should be applied while in crops, but instead invade from weedy areas, it grasshoppers are in the late instars because adults is often the edges of crop fields that are most ingest less bait. Migratory Grasshopper, Melanoplus sanguinipes (Fabricius) (Orthoptera: Acrididae) M 2393 Elimination of weeds within, and adjacent to, the long period of time that is required to induce crops is the most important cultural practice, and mortality and reduction in feeding and fecundity. can have material benefit in preventing damage to Also, the level of mortality induced by consump- crop borders. However, during periods of weather tion of Nosema is quite low, often imperceptible. It is when grasshoppers become numerous they may best used over very large areas, not just on individ- move long distances and invade crops. ual farms, and should be applied at least one year in Tillage is an effective practice for destruction of advance of the development of potentially damag- eggs, particularly in migratory grasshopper which is ing populations. especially likely to deposit eggs among crop plants. Fungi have also been investigated for grass- Deep tillage and burial are required, shallow tillage hopper suppression. A grasshopper strain of having little effect. All the crop-feeding Melanoplus Beauveria bassiana has been effective in some species deposit some eggs in crop fields, especially trials, and Metarhizium anisopliae var. acridum during periods of abundance, but it is fence row, irri- has worked well for grasshopper and locust sup- gation ditch, field edge, and roadside areas that tend pression in Africa and Australia, so it may prove to be the favorite oviposition sites, so tillage is not useful for Melanoplus spp. Behavioral thermo- entirely satisfactory unless other steps are taken to regulation by grasshoppers, wherein they bask in eliminate grasshopper egg pods from these areas the sun and raise their body temperatures, is that cannot be tilled. Though providing suppressive potentially a limiting factor for use of fungi. effects, deep tillage is not consistent with the soil and Basking grasshoppers easily attain temperatures water management practices in many areas, so may in excess of 35°C; such high temperatures decrease not be a good option. or even prevent disease development in infected Row covers, netting, and similar physical bar- grasshoppers. Inconsistent quality control in pro- riers can provide protection against grasshoppers. duction of fungi also limits use of these organisms This approach obviously is limited to small plant- for grasshopper control. ings, and can interfere with pollination. Also,  Grasshopper Pests in North America grasshoppers are capable of chewing through all  Grasshoppers and Locusts as Agricultural Pests except metal screening, so this approach does not  Grasshoppers, Katydids and Crickets guarantee complete protection. The opportunities for biological control are limited. Historically, poultry were found to con- References sume large numbers of grasshoppers and could provide considerable relief if the grasshopper- Capinera JL, Scott RD, Walker TJ (2004) Field guide to the infested garden was small or moderate in size and grasshoppers, katydids, and crickets of the United States. the birds were plentiful. This remains a viable Cornell University Press, Ithaca, NY, 249 pp option for some people, and turkeys are usually Parker JR, Newton RC, Shotwell RL (1955) Observations on mass flights and other activities of the migratory grass- considered most suitable among poultry. The birds hopper. USDA Tech Bull 1109, 46 pp may also inflict some direct damage to plants, Parker JR (1930) Some effects of temperature and moisture however, so introduction of poultry is probably upon Melanoplus mexicanus Saussure and Camnula most viable when grasshoppers are plentiful and pellucida Scudder (Orthoptera). Mont AES Bull 223, 132 pp threatening. Pfadt RE (1949) Food plants as factors in the ecology of the The microsporidian pathogenNosema locustae lesser migratory grasshopper, Melanoplus mexicanus is well studied as a microbial control agent of Mel- (Sauss.). Wyoming Agri Exp Stat Bull 290, 51 pp Pfadt RE (2002) Field guide to common western grasshoppers. anoplus spp. and is available commercially. It is fairly Wyoming Agri Exp Stat Bull 912, 288 pp stable, and easily disseminated to grasshoppers on Shotwell RL (1930) A study of the lesser migratory grass bait. However, its usefulness is severely limited by hopper. USDA Tech Bull 190, 34 pp 2394 M Milichiid Flies Milichiid Flies Miller, David

Members of the family Milichiidae (order George Hangay Diptera). Narrabeen, NSW, Australia  Flies David Miller was born in 1890 in Glasgow and was educated in Edinburgh, Dunedin and Milichiidae Wellington, New Zealand. He had a keen interest in entomology from an early age. From 1916 he was Government Entomologist and in 1926 he A family of flies (order Diptera). They commonly joined the Cawthron Institute as Chief Entomol- are known as milichiid flies. ogist in Nelson. While holding this position, in  Flies 1929 he also became the Director of the Forest Biological Research Station. He held this post until 1932, when he was appointed Assistant Milk Gland Director of the Cawthron Institute. He remained in this position until 1956; however, from 1937 Some female flies that give birth to well- until 1956 he was also the Director of the Ento- developed larvae rather than eggs secrete nour- mological Research Station, when he became the ishment for their offspring prior to deposition Director of the Cawthron Institute. Dr. David from a gland called a milk gland. Viviparous Miller was a very active, productive entomolo- insects display such glands, producing little or gist, who left a great body of work behind. He no yolk, and no chorion. Such insects typically published many scientific papers, monographs produce few offspring, but the survival rate of and books. One of his most read works is “Com- progeny is high. mon Ins ects in New Zealand” (1971). He was a leading figure in New Zealand entomology, holding two or more important positions simultane- Milkweed Butterflies ously in scientific institutions during most of his working life. He passed away in Nelson in 1973 at the age of 83. Members of the family Nymphalidae, subfamily Danainae (order Lepidoptera).  Brush-Footed Butterflies  Butterflies and Moths Reference

Miller D (1971) Common insects of New Zealand. A.H. and A.W. Reed Ltd., Wellington Milky Disease of Scarabs

Multiplication of bacteria in scarab beetle larvae, causing turbidity of the hemolymph and a white Miller Moths color in the posterior region of the body. The bacteria usually associated with this disease are Members of the family Noctuidae (order Paenibacillus (formerly Bacillus) popilliae and Lepidoptera). Paenibacillus lentimorbis.  Owlet Moths  Paenibacillus  Butterflies and Moths Millipedes (Class Diplopoda) M 2395 Millipedes (Class Diplopoda) Order: Spirobolida Order: Spirostreptida Though the name “millipede” suggests that these Order: Polydesmida – flat-backed millipedes animals have 1,000 legs, and although the presence Millipedes are quite diverse morphologically, of numerous legs is a characteristic of this group, though they all consist of a long chain of rather none have more than 375 pairs, and most have uniform body segments, and lack wings (Fig. 52). considerably fewer. In differentiating this group Some are rather short, and may be covered with from the similar-appearing centipedes and sym- feather or scale-like adornment. Others look phylans, the presence of two pairs of legs per body greatly like woodlice (pillbugs and sowbugs), and segment is the key character used to identify even roll into a ball in the manner of pillbugs. millipedes. Most, however, are elongate and thin in general body form. There are three basic body regions: the head, which bears a pair of moderately long Classification antennae; the body, consisting of numerous leg- bearing segments, and which normally are rather The Class Diplopoda is one of six classes in the cylindrical but sometimes bears prominent lat- Subphylum Atelocerata of the Phylum Arthro- eral projections; and the telson, or posterior body poda. The other classes in the subphylum are segments bearing the anus. The integument is Chilopoda, the centipedes; Pauropoda, the pauro- very hard. pods; Symphyla, the symphylans; Entognatha, the collembolans, proturans, and diplurans; and Insecta, the insects. There are several orders of diplopods, and several arrangements of the taxa have been proposed. These are fairly common arthropods, and as they occasionally are numerous or damaging, they sometimes are confused with insects. More commonly they are confused with centipedes. Phylum: Arthropoda Subphylum: Atelocerata Class: Diplopoda Subclass: Pselophognatha Order: Polyxenida – bristly millipedes Subclass: Chilognatha Order: Glomeridesmida Order: Sphaerotheriida – giant pill millipedes Order: Glomerida – pill millipedes Order: Siphoniulida Order: Platydesmida Order: Siphonophorida Order: Polyzoniida Order: Stemmiulida Order: Callipodida Order: Cordeumatida Millipedes (Class Diplopoda), Figure 52 Garden Order: Julida millipede, Oxidus gracilis. 2396 M Millipedes (Class Diplopoda) Life History stage. The number of pairs of legs present in the juveniles is about 3, 6, 11, 16, 22, 26, 28, and 30 for Millipedes are poorly known animals, with almost instars 1 to 8, respectively. Body length is about all our information based on studies in northern 0.5, 1.5, 3.6, 4.1, 4.8, 7.4, 12.4, and 20 mm during Europe. The life cycle of millipedes is often long. the corresponding instars. Development time is Many live for a year, but some persist for 2–4 years 1, 11–18, 13–18, 16–30, 20–38, 28–46, 42–60, during before attaining maturity. In a Julus sp. studied in a instars 1 to 7, with the final (eighth) instar gener- temperate environment, oviposition took place in ally overwintering, though in some cases instar April, with instar 6 to 7 was attained by winter and seven overwinters. instars 8 to 9 by the second winter. They overwin- Adult millipedes vary considerably in size, tered as instars 9–11, then mated and oviposited the often measuring from 10–30 mm in length, but in following spring, their third year of life, before they some species exceeding 100 mm. Their color perished. Following is a description that is based on ranges from whitish to brown and black. The sexes the life cycle of a common millipede, Oxidus gracilis are separate. The external genitalia of adult milli- Koch, a species with a 1-year development time. pedes are located between the second and third Oxidus gracilis is somewhat flattened dors- pairs of legs. Some adult millipedes have the abil- oventrally, and bears 30 or 31 pairs of legs in males ity to molt from a sexually active adult to an inter- and females, respectively. They generally measure mediate stage that is not functional sexually. 18.5–22.2 mm in length and 2.0–2.5 mm in width. Parthenogenesis occurs in some species and some Initially they are light brown in color but gradu- populations, but this is not usual. Millipedes lack ally attain a dark brown coloration, and sometimes a waxy cuticle and are susceptible to desiccation. are bordered with yellow. Adults seem to live for They have glands, with openings usually located about two months in the spring or summer, and laterally, which secrete chemicals that are toxic like all millipedes, are intolerant of dry conditions. and may immobilize predatory arthropods such Oxidus gracilis is nocturnal. as spiders and ants. The creamy white, yellow or brownish eggs of Oxidus gracilis are deposited in the soil, usually in clusters. A glutinous material causes them to adhere Ecology to one another. The eggs are nearly spherical in shape, measuring 0.35–0.4 mm in width and about Millipedes normally eat dead plant material, usu- 0.40 mm in length. The female may create a chamber ally in the form of leaf litter. However, they occa- or cell for her eggs. She deposits 50–300 eggs in a sionally graze on roots and shoots of seedlings, cluster, and eggs can be found throughout the sum- algae, and dead arthropods and molluscs. They are mer months. Duration of the egg stage is 9–10 days. selective in their consumption of leaf litter, prefer- The first instar juvenile millipedes bear only a ring some leaves over others. They also tend to wait few segments and three pairs of legs, but body seg- until leaves have aged, and are partially degraded ments, legs, and ocelli are added with each molt. by bacteria and fungi. Thus, they function princi- By counting the number of rows of ocelli and add- pally as decomposers, hastening the break-up of ing one, the instar can be estimated for many mil- leaf material into smaller pieces, and incorporating lipedes. Thus, fourth instar millipedes have three the organic matter into the soil. Whether they rows of ocelli, fifth instars have four rows, etc. derive most of their nutritional requirements from Maturity is often attained after about 10 instars, the organic substrate or the microorganisms devel- but some species continue to molt as adults. oping on the substrate is uncertain. Millipedes also In Oxidus gracilis, most individuals develop tend to consume their own feces, and many species through eight instars before they attain the adult fare poorly if deprived of this food source. Mimicry M 2397 Millipedes sometimes are viewed as a severe Carabidae), and rove beetles (Coleoptera: Staphylini- nuisance as a result of exceptional abundance in an dae) also consume millipedes, though ants are inappropriate location such as in yards, homes, or usually deterred. Various disease-causing agents commercial or food processing facilities. Milli- such as fungi, iridoviruses, rickettsia, and protozoa pedes can exist in tremendous quantities in the are documented from millipedes, though they seem soil and become a problem only when they come to be only sporadically effective. Parasitic flies have to the surface and disperse as a group. This often been reared from millipedes in Europe. occurs following abnormally large rainfall events, though hot and dry conditions also are sometimes suspected to be a stimulus for dispersal. References Several species of millipedes are reported to be injurious to plants, or present in high enough Enghoff H (1984) Phylogeny of millipedes–a cladistic analy- numbers to be considered a nuisance. Probably sis. Zeitschrift für Zoologische Systematik und Evolu- tionsforschung 22:8–16 the most important is garden millipede, Oxidus Hopkin SP, Read HJ (1992) The biology of millipedes. Oxford gracilis Koch (Diplopoda: Paradoxosomatidae). It University Press, Oxford, UK apparently was accidentally introduced to most Kime RD, Golovatch SI (2000) Trends in the ecological strate- temperate areas of the world from the tropics, gies and evolution of millipedes (Diplopoda). Biol J Linn Soc 69:333–349 probably via transport of specimen plants. In cool areas it is principally a greenhouse pest. Millipedes produce various foul-smelling flu- Mimallonidae ids (sometimes including hydrogen cyanide) from openings along the sides of their body. Despite A family of moths (order Lepidoptera). They com- the formidable chemical defenses of millipedes monly are known as sackbearer moths. (Fig. 53), several natural enemies are known. Small  Sackbearer Moths vertebrate predators such as shrews, frogs, and  Butterflies and Moths lizards eat millipedes. Invertebrate predators such as scorpions (Arachnida), ground beetles (Coleoptera: Mimicry

Heather J. McAuslane University of Florida, Gainesville, FL, USA

Mimicry, broadly defined, is the superficial resemblance of one organism to another organism, usually providing a selective advantage to the mimicker. The term mimicry is used occasionally to describe organisms that mimic inanimate objects in their environment (such as young swallowtail larvae resembling bird droppings and grasshoppers or katydids resembling leaves). How- ever, this phenomenon is also variously labeled as Millipedes (Class Diplopoda), Figure 53 A crypsis, camouflage, mimesis or special resem- millipede in a coiled position, a common defensive blance, and will not be discussed under the term behavior. mimicry. 2398 M Mimicry Many insect species have evolved to mimic Batesian Mimicry other species of insects, and even other groups of organisms, for a variety of reasons. Likewise, some This form of mimicry was described in 1862 by non-insect organisms have evolved to mimic spe- Henry W. Bates, an English naturalist studying cific insects. The most common type of mimicry is butterflies in Amazonia, and was later named visual, where mimics and their models look very after him. He noticed remarkable resemblances similar to each other. The perceived commonness between palatable pierid butterflies (related to of this type of mimicry may be elevated somewhat cabbage white butterflies) and unpalatable Ithomi- by the visual emphasis of humans, the studiers and inae butterflies (related to monarch butterflies). cataloguers of nature. However, visual resemblance The larval host plant of the Ithomiinae butterflies also can be enhanced by acoustic, olfactory, tactile renders them toxic to predators, whereas the diet and behavioral mimicry. The mimicry can be so of the pierid larvae gives them no such protection close that even seasoned entomologists are fooled against predators. He suggested that natural selec- at first glance. tion had caused the appearance of the palatable In the majority of cases, mimicry has evolved pierids to move toward that of the unpalatable in the mimicking species to reduce the likelihood of Ithomiinae butterflies. suffering predation (as is the case in Batesian and Batesian mimicry, then, is the result of evolu- Müllerian mimicry). Species that mimic a toxic or tionary convergence in shape, patterning, color, unpalatable species experience less predation than behavior, or smell of an edible mimic toward close those that do not. In many cases, but not all, the resemblance of a less palatable and distantly toxic or unpalatable species and their mimics have related model. The predator, after trying to eat a aposematic, or warning, coloration. Aposematic col- few of the toxic models, learns that an insect with oration is striking, usually black next to red, yellow this particular shape, color or smell is toxic and or orange, and serves to enhance the learning of therefore unpalatable. The mimic takes advantage distastefulness by predators. Batesian and Müllerian of this predator learning and, in fact, is a parasite mimicry are effective against predators that are on the model species. The model suffers greater capable of learning and that have good color vision predation when it is sympatric with a mimic (shar- (if the insect is aposematic). Birds, and to a lesser ing the same range) than when it is alone because extent, amphibians and lizards, seem to have been the encounter of predators with palatable mimics the driving force for the evolution of mimicry in delays the learning process. The predator is also insects. The model usually has a true toxin in its harmed in this system because it learns to avoid a body that could kill a predator if the model were profitable prey item, the mimetic species. consumed in its entirety. However, the model also Batesian mimics must evolve very close resem- often contains emetic and bitter chemicals (or the blance to their models so that predators cannot dis- toxin itself may have emetic and bitter properties). tinguish them. If the mimics become too abundant Thus, the predator lives another day and associates in the habitat relative to their models, predators the regurgitation of the prey item and its bitter taste may never learn to associate their appearance with with a particular morphology or pattern. distastefulness; thus, both model and mimic suffer In a few cases, insects and other organisms increased predation. The models cannot evolve to have evolved mimicry so that they become more look too different from their original morphology effective predators (aggressive mimicry) or are or they will experience more predation. So, in these better adapted as social inquilines, living in the situations, it is the mimic that evolves to resemble nests of their host ants (Wasmannian mimicry). other toxic model species in the area. The evolution In these types of mimicry, the mimics and their of polymorphisms (many morphs or appearances) models are rarely aposematic. is common in Batesian mimics. As one morph Mimicry M 2399 becomes too common in a population relative to its in the Neotropics. They wrote independently that model, it is selected against, and other morphs many species of unpalatable butterflies resembled within the population increase in abundance. An each other. In 1879, Müller published a mathematical extreme example of polymorphism in a Batesian model that showed that pairs of unpalatable spe- mimic occurs in the African swallowtail species, cies mutually benefit from resembling each other. Papilio dardanus. There are thought to be 31 morphs Müllerian mimicry, later named for him, is the of this species, mimicking several species of danaid result of evolutionary convergence in shape, pat- butterflies in the genera Danaus and Amauris terning, and color of two, or more, distantly related throughout their ranges in central and southeastern unpalatable species (Fig. 54). In this type of mim- Africa. The models feed on toxic milkweeds while icry, all species benefit from the mimicry because the mimics are innocuous to predators. Curiously, predators need only learn a single appearance and the males of all P. dardanus morphs resemble a there is less total death among the co-mimetic spe- typical yellow and black swallowtail and only the cies than if the predators needed to learn two dif- females are mimetic. ferent patterns. Predators also benefit because they Batesian mimicry has been studied best among can quickly learn to sight reject unpalatable prey, species of butterflies but it is also common in arthro- and avoid wasting time on them. pods that mimic bees, wasps or ants – insects that are Müllerian mimicry is common in the tropics all equipped with predator-deterring stings. For of South America. One large mimicry “ring” example, in Honduras, the ant Camponotus planatus involves two species of Heliconius butterflies is mimicked by four species of arthropod: a clubi- and several other more distantly related butter- onid spider, a salticid spider, a mirid bug (Barbariella flies and even a day-flying moth. All are toxic due sp.), and a praying mantid (Mantoida maya). Inter- chemicals sequestered from their larval host plants estingly, the mimetic mantid nymph resembles and all resemble each other visually. the ant model only in the earliest instars when it The classic example of Müllerian mimicry measures 3–9 mm. When the mantid nymph grows known from the temperate world is that of the longer than 9 mm, and can no longer pass for an ant, monarch butterfly, Danaus plexippus, and the its morphology and color change to mimic a species viceroy, Limnetis archippus. In this example, adults of vespid wasp common in the area. of the viceroy butterfly are presumed to be palat- Most examples of Batesian mimicry involve able mimics of adults of the toxic monarch only visual resemblance between models and butterfly whose larvae feed on milkweeds and mimics. However, some insects mimic the sound sequester heart poisons (cardiac glycosides). of their model, in addition to their appearance. For example, a syrphid fly that visually mimics a yellow jacket wasp, also mimics it acoustically, having a wing beat frequency of 147 Hz, which is very similar to the 150 Hz frequency of the wasp. The stridulations of a Necrophorus burying beetle that mimics a bumblebee visually have the same frequency as the wing beat of the bumblebee. Mimicry, Figure 54 The viceroy butterflies ( Limenitis archippus, left) was long thought to be a palatable Batesian mimic of the toxic monarch Müllerian Mimicry butterfly (Danaus plexippus, right). Research has indicated that, at least in Florida, the viceroy Henry W. Bates and Fritz Müller, a German natu- and the monarch are both unpalatable and are ralist, first noted examples of this type of mimicry Müllerian co-mimics. 2400 M Mimicry Cardiac glycosides protect monarch butterflies desirable. The second species is attracted to the from bird predation. However, this example had to mimic and usually ends up being eaten by the be revised after the 1991 publication of a paper by mimic; thus, the mimicry is aggressive in nature. David Ritland who was a student of Lincoln A classic example of behavioral aggressive mim- Brower, one of the pioneers of the study of chemi- icry occurs in fireflies. It has long been known cal defense in the monarch butterfly. that male and female fireflies communicate visu- Pre-1991, the viceroy butterfly in Florida, ally by flashing their light organs in a species- whose larvae feed on willow, poplar and other specific pattern. Adult female fireflies, usually trees, was considered to be a Batesian mimic of the stationary, flash in response to the flash pattern monarch butterfly and the Florida Queen butter- of flying males. The male locates the female by fly, Danaus gilippus berenice, whose larvae can feed her flashing and copulation ensues. However, on toxic cardiac glycoside-containing host plants. several firefly species in the genus Photuris are However, Ritland and Brower found that the vice- aggressive mimics of Photinus species. The roy was just as unpalatable to bird predators as was female Photuris flashes the female Photinus- the monarch butterfly. Furthermore, the viceroy specific pattern in response to the signaling of was considerably less palatable than the Florida the male Photinus. The male Photinus is lured Queen if the larvae of the Queen fed on a host to the female Photuris, expecting a female of plant that was low in cardiac glycosides. Thus, in his own species, and is then eaten. JE Lloyd this study, the monarch and the viceroy butterflies has termed these deceptive Photuris females were actually Müllerian co-mimics and the Florida “femmes fatales.” Queen butterfly was a Batesian mimic of the vice- An example of aggressive chemical mimicry roy and the monarch. Thus, the type of mimicry involves several species of bolas spiders in the cannot be ascertained unless the palatability of the genus Mastophora. The females in this genus do species involved is known. not spin a web but rather swing a silk thread A further issue that complicates our under- with a droplet of sticky material at its end (the standing of mimicry complexes is that of auto- bolas) at passing insects. The majority of the mimicry. Researchers have found that the insects that are caught on the bolas are male unpalatability of the monarch butterfly varies moths of a select few species. Chemists deter- across a spectrum depending on the larval diet. If mined that the female spiders synthesize the sex a larva feeds on a host plant species with low con- attractant pheromone of the females of the moth centrations of cardiac glycosides, it will develop species that is their predominant prey. Male into an adult that is nontoxic and palatable to bird moths are lured to what they perceive as a virgin predators. If a larva feeds on a plant species with female but instead are caught and eaten by high concentration of cardiac glycosides, the but- the spider. terfly will be toxic and unpalatable. Thus, monarch butterflies with low concentrations of cardiac glycosides are Batesian mimics of monarchs with Wasmannian Mimicry high concentrations of cardiac glycosides (i.e., automimicry). A final, and very specialized, form of mimicry is Wasmannian mimicry, which occurs in some organisms that live in the nests of ants. E. Was- Aggressive Mimicry mann first described this phenomenon in museum specimens of staphylinid beetles. Many species in Aggressive mimicry occurs when one species several genera of staphylinid beetles (e.g., Was- mimics something that a second species considers mannia, Myrmeciton, and Ecitosius) live in ant Minima M 2401 nests and closely resemble ants, having a petiole- Miniature Ghost Moths like restriction in the abdomen, and an overall (Lepidoptera: Palaeosetidae) slender and dark body. In addition to looking like ants, they produce appeasement substances from John B. Heppner glands that calm the ants and allow for their entry Florida State Collection of Arthropods, into the nests. Wasmann originally thought that Gainesville, FL, USA the morphology of the staphylinid’s body tactilely mimicked the ant’s own body and fooled the ant Miniature ghost moths, family Palaeosetidae, are into tolerating its presence. However, because ants a small family related to Hepialidae, comprising rely primarily on chemicals for intraspecific com- eight species worldwide (five in Assam, Thailand munication, this hypothesis seems less reasonable. and Taiwan, two in Australia, and one in Colom- It may be that staphylinids that forage outside the bia). The family is in the superfamily Hepia- nest with their ant hosts may gain protection loidea, in the infraorder Exoporia. Adults are from potential predators by mimicking the sting- small (12–18mm wingspan), with head rough- equipped ants. ened; haustellum absent (with no mandibles);  Crypsis labial palpi short and 2 to 3-segmented; axillary  Aposematism palpi absent; antennae are relatively short. Mac-  Myrmecomorphy ulation can be rather sparkling, with metallic-  Myrmecophiles iridescent markings on the forewings on a brown or blue base color. Adults are crepuscular or active during the day in dark forested areas, References typically near wet moss-covered rock faces. Adults often rest head down under leaves in moist, shaded forest areas near water courses. Huheey JE (1984) Warning coloration and mimicry. In: Bell WJ, Cardé RT (eds) Chemical ecology of insects. Sinauer Biologies remain unknown but larvae of a spe- Associates, Inc., Sunderland, MA, pp 257–297 cies from Taiwan have been described and are Mallet J, Joron M (1999) Evolution of diversity in warning thought to feed on mosses. color and mimicry: polymorphisms, shifting balance and speciation. Annu Rev Ecol Syst 30:201–233 Ritland DB (1991) Revising a classic butterfly mimicry scenario: demonstration of Müllerian mimicry between References Florida viceroys (Limenitis archippus floridensis) and queens (Danaus gilippus berenice). Evolution Davis DR, Karsholt O, Kristensen NP, Nielsen ES (1995) Revi- 45:918–934 sion of the genus Ogygioses (Palaeosetidae). Invertebr Sheppard PM (1962) Some aspects of the geography, genetics, Taxonomy 9:1231–1263 and taxonomy of a butterfly. In: Nichols D (ed) Taxon- Heppner JB, Balcázar MA, Wang HY (1995) Larval morphol- omy and geography. Systematics Association Publica- ogy of Ogygioses caliginosa from Taiwan (Lepidopera: tion No. 4, Systematics Association, London, UK, pp Palaeosetidae). Trop Lepidop 6:149–154 135–152 Kristensen NP, Kristensen NP (ed) (1999) Lepidoptera, Wickler W (1968) Mimicry in plants and animals. McGraw- moths and butterflies, vol 1: Evolution, systematics, and Hill, New York, NY, 253 p biogeography. In Handbuch der Zoologie. Band IV. Arthropoda: Insecta. Teilband. W De Gruyter, Berlin, 35:51–63

Mineral Oil Minima Horticultural oil that is derived from petroleum.  Horticultural Oil Among ants, a minor worker. 2402 M Minor Workers Minor Workers Minute Moss Beetles

Among ants, the smallest subcaste of workers Members of the family Hydraenidae (order (contrast with major and media workers). Coleoptera).  Ants  Beetles

Minute Bark Beetles Minute Pirate Bugs (Hemiptera: Anthocoridae) Members of the family Cerylonidae (order Coleoptera). David R. Horton  Beetles USDA, Agricultural Research Service, Yakima, WA, USA

Minute Black Scavenger Flies Insects in the family Anthocoridae are referred to as minute pirate bugs or flower bugs. Pirate Members of the family Scatopsidae (order bugs occur worldwide and occupy a variety of Diptera). natural and disturbed habitats. All but a few spe-  Flies cies are predaceous, feeding on small soft-bodied arthropods from a variety of taxonomic groups. Minute Bog Beetles Pirate bugs contribute to biological control of pest arthropods in a wide variety of habitats, Members of the family Microsporidae (order including orchards, row crops, forests, ornamen- Coleoptera). tal plants, greenhouses, and granaries.  Beetles Classification and Distribution of Minute Brown Scavenger Beetles the Anthocoridae

Members of the family Lathridiidae (order The family Anthocoridae includes between Coleoptera). 500–600 species in 80–100 genera worldwide. The  Beetles systematic position of the Anthocoridae and close relatives remains somewhat unsettled, and there Minute Fungus Beetles is a distinct need for additional taxonomic and phylogenetic work. Diversity of Anthocoridae Members of the family Corylophidae (order tends to be highest in the tropics and the Holarc- Coleoptera). tic Region. Thorough faunistic studies for some  Beetles geographic regions are lacking, and estimates of diversity will require revision as these studies are done. Checklists for the North American fauna, Minute Marsh-Loving Beetles including information on distribution, are available in publications by Kelton, Henry, and Maw Members of the family Limnichidae (order et al. Citations for these works are provided at the Coleoptera). end of this chapter. Keys to many North American  Beetles species are available in Blatchley and Kelton. Minute Pirate Bugs (Hemiptera: Anthocoridae) M 2403 The discussion of classification and distribution Anthocorini to be presented here is based on treatments by Cassis and Gross, Schuh and Štys, Schuh and Slater, The Anthocorini is a highly speciose group Carayon, and Ford (full citations follow at the end of found primarily in temperate areas. Members this article). The Anthocoridae are found in the of this group include a number of species infraorder Cimicomorpha within the suborder Het- important in biological control, particularly in eroptera (“true bugs”). Classification of the Anthoc- orchards and coniferous forests. The most well oridae has seen extensive study and revision since known of these insects are in the genus Anthoc- the family was erected in the 1800s, particularly with oris, which includes over 50 described species reference to placement of related families such as the found commonly in temperate regions. Species bed bugs (Cimicidae), bat bugs (Polyctenidae), and in the Anthocorini feed on phytophagous web lovers (Plokiophilidae), but also with respect to arthropods primarily in the canopies of decidu- higher level groupings of taxa within the Anthocori- ous or coniferous trees, or on the foliage of dae. Three modern treatments of the pirate bugs deciduous shrubs. allocate genera among seven or eight tribes (Table 9). Carayon, and Cassis and Gross include three subfamilies (Lasiochilinae, Lyctocorinae, Anthocorinae) Blaptostethini within the family Anthocoridae. Schuh and Slater elevate the Lasiochilinae and Lyctocorinae to family This is a poorly known group of about seven rank, following the phylogenetic analysis of Schuh described species known primarily from the Ori- and Štys. Four tribes included within the Lyctocori- ental and Pacific regions. nae by Carayon (i.e., the Almeidini, Cardiastethini, Scolopini, and Xylocorini) are placed in the Anthoc- orinae by Cassis and Gross, or in the Anthocoridae Dufouriellini by Schuh and Slater. Carayon’s Cardiastethini is considered a junior synonym of Dufouriellini Van The Dufouriellini is a large group of species whose Duzee in both the Schuh and Slater treatment and in systematic affinities remain somewhat uncertain. the Cassis and Gross treatment, following the assess- The Dufouriellini are well represented in the Neo- ment of Štys. Péricart used Carayon’s classification tropical, Australian, and Palaearctic regions. in his summary and checklist of the Palaearctic Cardiastethus is the most common genus, com- Anthocoridae. I follow the Schuh and Slater scheme prising about 40 described species having a wide throughout this article. Because of the close taxo- distribution. nomic affinity among the Lyctocoridae, Lasiochili- dae, and Anthocoridae – and because taxonomic rank for these groups is still open to discussion – the Oriini present article will not be limited to the Anthocori- dae, but will include as necessary reference also to The Oriini contains the geographically widespread the Lyctocoridae and Lasiochilidae. and well-known genus Orius, having approximately 70 described species. This group has strong representation in the Oriental, Ethiopian, Palae- Family Anthocoridae – Tribe Almeidini arctic, and Neotropical regions, but is relatively poorly represented in the Nearctic. The Oriini This is a poorly known group with few described includes a number of species important in biologi- species, known from the Old World tropics, Japan, cal control of pests on row crops, in greenhouses, Nepal, and Australia. and on ornamental plants. 2404 M Minute Pirate Bugs (Hemiptera: Anthocoridae) Minute Pirate Bugs (Hemiptera: Anthocoridae), Table 9 Comparison of three classification schemes for the pirate bugs and relatives, including representative genera Carayon Cassis and Gross Schuh and Slater Anthocorinae Anthocorinae Anthocoridae Anthocorini Almeidini Almeidini Acompocoris Reuter Almeida Almeida Anthocoris Fallén Anthocorini Anthocorini Coccivora McAtee & Malloch Acompocoris Acompocoris Elatophilus Reuter Anthocoris Anthocoris Macrotrachelia Reuter Coccivora Coccivora Temnostethus Fieber Elatophilus Elatophilus Tetraphleps Fieber Macrotrachelia Macrotrachelia Blaptostethini Temnostethus Temnostethus Blaptostethus Fieber Tetraphleps Tetraphleps Oriini Blaptostethini Blaptostethini Bilia Distant Blaptostethus Blaptostethus Macrotracheliella Champion Dufouriellini Dufouriellini Montandoniola Poppius Amphiareus Amphiareus Orius Wolff Brachysteles Brachysteles Paratriphleps Champion Buchananiella Buchananiella Wollastoniella Reuter Cardiastethus Cardiastethus Lasiochilinae Dufouriellus Dufouriellus Lasiochilus Reuter Oriini Oriini Lyctocorinae Bilia Bilia Almeidini Macrotracheliella Macrotracheliella Almeida Distant Montandoniola Montandoniola Cardiastethini Orius Orius Amphiareus Distant Paratriphleps Paratriphleps Brachysteles Mulsant & Rey Wollastoniella Wollastoniella Buchananiella Reuter Scolopini Scolopini Cardiastethus Fieber Calliodis Calliodis Dufouriellus Kirkaldy Nidicola Nidicola Lyctocorini Scoloposcelis Scoloposcelis Lyctocoris Hahn Xylocorini Xylocorini Scolopini Xylocoris Xylocoris Calliodis Reuter Lasiochilinae Lasiochilidae Nidicola Harris & Drake Lasiochilus Lasiochilus Scoloposcelis Fieber Lyctocorinae Lyctocoridae Xylocorini Lyctocoris Lyctocoris Xylocoris Dufour

Modification of a table in Cassis and Gross Minute Pirate Bugs (Hemiptera: Anthocoridae) M 2405 Scolopini including in stored products, in decaying vegetation, beneath bark, and in the nests of birds or The Scolopini include at least 13 genera distrib- mammals. uted primarily in the Neotropical Region, but with at least some representation in most areas of the world. Species of Scoloposcelis are important pred- Morphology ators of bark-feeding Coleoptera. Members of the Anthocoridae are relatively small (1.5–5 mm), having an oval or elongate-oval shape Xylocorini (Figs. 55 and 56). Most are brownish in general coloration. Wing markings or shadings give some The Xylocorini occur virtually worldwide, but species a checkered appearance. The body is have heavy representation in the Palaearctic and generally somewhat flattened, and may be either Nearctic regions. This tribe includes a single genus, glabrous or pubescent. The head extends horizon- Xylocoris, having about 40 described species. Spe- tally, with large compound eyes on each side. cies of Xylocoris are sources of biological control Paired ocelli are present near the eyes in the adult in stored products, granaries, and beneath the bark (ocelli are not present in nymphs). Antennae are of trees. Xylocoris flavipes (Reuter) is a geographi- four-segmented and inserted anterior of the eyes. cally widespread species which has been intro- Mouthparts are of the piercing-sucking type, in duced into a number of regions apparently by the form of a slender beak or labium. The labium human commerce. has three visible segments, and may be short or quite long (in some species extending to the end of the abdomen). The labium serves to house the four Family Lasiochilidae piercing stylets (paired mandibles and paired maxillae), which collectively form the two chan- The Lasiochilidae are a poorly studied group with nels through which digestive enzymes and the species occurring in most geographic regions, but ingested food products are moved. The pronotum having the strongest representation in the Neotro- is trapezoidal, bearing paired callosities that are pical Region and on Pacific islands; the family is virtually absent from the Palaearctic. Lasiochilus is composed of approximately 50 described species having a relatively wide distribution. Members of this family are small (3–4 mm), and occur on the ground in litter, under the bark of trees, or on plant surfaces.

Family Lyctocoridae

The Lyctocoridae are widely distributed, but with a strong presence in temperate regions. One species, Minute Pirate Bugs (Hemiptera: Anthocoridae), Lyctocoris campestris (Fabricius), is essentially cos- Figure 55 A common North American pirate bug, mopolitan, likely because of unintentional intro- Orius tristicolor (White) (Oriini) (photograph by ductions outside of its native range. Members of Jack Kelly Clark, courtesy of University of this family can be found in a number of habitats, California Statewide IPM Program). 2406 M Minute Pirate Bugs (Hemiptera: Anthocoridae)

Minute Pirate Bugs (Hemiptera: Anthocoridae), Figure 56 Some Anthocorini and Oriini. (a) Macrotrachelia sp. (possibly M. nigronitens (Stål)) (Anthocorini), length approximately 3.3 mm excluding antennae; (b) brachypterous Anthocoris dimorphicus Anderson & Kelton (Anthocorini), 2.9 mm; (c) Elatophilus sp. (Anthocorini), 3.1 mm; (d) Macrotracheliella nigra Parshley (Oriini), 2.4 mm; (e) Melanocoris nigricornis Van Duzee (Anthocorini), 3.1 mm; (F) Anthocoris nemoralis (Fabricius) (Anthocorini), 3.5 mm.

prominent in some species and inconspicuous in forewing has a triangular cuneus, unlike what is other species. Anthocorids have two pairs of wings: found in many other Heteroptera. Genitalia in the the membranous hind wings, and the thickened male are asymmetrical (discussed below). The ovi- forewings (hemelytra) that are characteristic for positor is well-developed in most species, but is the true bugs. Most members of the family have greatly reduced in some taxa (e.g., Cardiastethus). fully sized wings, although there are species in Specimens of Anthocoridae may resemble some genera (e.g., Xylocoris, Temnostethus, Anthoc- insects from other families of Heteroptera, including oris, and Elatophilus) that exhibit brachyptery. The especially members of the Miridae. Morphological Minute Pirate Bugs (Hemiptera: Anthocoridae) M 2407 characteristics in the Anthocoridae that can be Harris & Drake has been collected from guano used to separate them from other Heteroptera beneath roosting bats. include: two ocelli; labium with three visible seg- Anthocoridae may often supplement their ments; generally an absence of pronounced veins diets with pollen or plant juices. Species of Orius in the hemelytral membrane; presence of a cuneus; occur commonly in the flowers of herbaceous veg- and presence of asymmetrical genitalia in males. etation, and are known to supplement their diets Insects within the Lasiochilidae, Lyctocoridae, with pollen. Orius pallidicornis (Reuter) appears to and Anthocoridae may often be very similar in have an exclusively plant diet, feeding on pollen appearance. Placement of specimens in the cor- from a limited number of species. Paratriphleps rect family may require access to faunistic treat- laeviuscula Champion is a Central and South ments that include keys for identifying genera American species now known to occur in Florida, and species, from which family affiliation can where it inhabits the flowers of sapodilla then be derived. Examination of genitalia may be (Manilkara zapota) and feeds on pollen. Species of necessary in some cases to confirm or to ascertain Anthocoris and Orius are known to accumulate family affiliation. systemic insecticides from root-treated plants, due to their habit of ingesting plant juices. Diet breadth in the Anthocoridae shows a Biology and Life History range from highly generalized species to highly specialized species. The generalist species Anthoc- Members of the Anthocoridae, Lasiochilidae, and oris nemoralis (Fabricius) has been recorded from Lyctocoridae are predaceous on small soft-bodied over 20 plant genera in Europe and from 13 plant arthropods in a variety of natural or managed genera in North America, with the latter records habitats. Many species prey upon herbivorous occurring only since 1958 following the accidental arthropods that attack forbs, shrubs, or trees. and intentional introductions of this predator into Important prey taxa include aphids, psyllids, mites, the Nearctic. Anthocoris antevolens White, a wide- thrips, scale insects, psocids, and eggs or small lar- spread North American species, has been recorded vae of Lepidoptera, Coleoptera, and Diptera. Spe- from well over 20 plant genera. Species such as cies of Orius are commonly associated with flowers Orius tristicolor (White) and Orius insidiosus (Say) of herbaceous plants, where they feed extensively occur on the flowers of a diverse number of plant on thrips and other small arthropods. A number species, apparently because a primary prey species, of genera in the Anthocorini (Melanocoris Cham- the western flower thrips (Frankliniella occidenta- pion, Tetraphleps, Elatophilus) occur exclusively lis (Pergande)), is itself highly generalized. Lycto- on coniferous trees, where they feed on aphids and coris campestris occurs in a variety of habitats, scale insects. Species of Anthocoris are common including compost piles, moldy grain, beneath leaf on deciduous trees and shrubs, and prey exten- or straw litter, birds nests, mammal burrows, or sively on psyllids, aphids, and other soft-bodied beneath the bark of trees. arthropods. Scoloposcelis, Xylocoris, and Lyctocoris In contrast, many other Anthocoridae show are often found beneath the bark of trees feeding highly restricted diets. Several species of Anthoc- on eggs and larvae of bark beetles. Xylocoris and oris reproduce largely or entirely on a few plant Lyctocoris also occur in stored products and gra- species (e.g., A. gallarumulmi (De Geer) on elm naries, in nests of birds or mammals, in poultry [Ulmus], A. bakeri Poppius on manzanita [Arcto- houses, in decaying plant litter, in manure piles, staphylos], A. sarothamni Douglas & Scott on under tree bark, or in ant nests. Lyctocoris campes- broom [Cytisus], A. dimorphicus Anderson & tris may occasionally feed on the blood of mam- Kelton on willow [Salix], and A. visci Douglas on mals, including on humans. Nidicola marginatus mistletoe [Viscum]). Presumably, the limited host 2408 M Minute Pirate Bugs (Hemiptera: Anthocoridae) plant range reflects some type of diet specializa- incomplete metamorphosis, and resemble the tion (A. bakeri, for example, appears to prey adults morphologically except in lacking wings, extensively on aphids that gall Arctostaphylos). ocelli, and reproductive structures. Nymphs have Other Anthocoridae are restricted to a few related five instars. Development rates of eggs and nymphs plant species, and include species of Melanocoris increase with increasing temperature. Anthocori- (restricted to Pinus and Picea), Elatophilus dae in temperate regions overwinter as adults in (restricted to Pinus), and Acompocoris (Pinus and reproductive diapause. For those species which Picea). Species of Elatophilus often appear to have been examined, diapause is controlled by occur in association with scale insects (Matsu- photoperiod, with long days prompting reproduc- coccus Cockerell) occurring on Pinus; some tion and short days leading to diapause. The critical Elatophilus species are attracted to the sex phero- photoperiod that prompts diapause for a given mones of Matsucoccus scale insects. Brachysteles species may often depend upon latitude. Sex ratios parvicornis (Costa) may feed largely on mites for overwintering adults are often female-biased, within the Oribatida. Diet breadth in some spe- and in some Anthocoridae the males appear not to cies may change seasonally. For instance, females overwinter. Most species of Anthocoridae have two of some Anthocoris species accumulate on wil- or more generations per year depending upon lati- lows (Salix) in early spring as the bugs emerge tude and elevation. Some species (e.g., Anthocoris from overwintering sites, and may complete a gallarumulmi) appear to be univoltine throughout generation on those hosts before the summer their respective geographic ranges. hosts (which can include a number of different plant taxa) are later colonized. Anthocoridae that occur on plants insert Reproduction, Mating, and the their eggs into plant tissues. Species that attack Paragenital System aphids or scale insects on coniferous trees insert their eggs into the needles, whereas those species The pirate bugs have several reproductive traits that inhabit the foliage of deciduous plants often and associated structures that differ from most insert the eggs into leaf tissues. Anthocoridae that other Heteroptera. Unlike most Heteroptera, the occur under bark insert their eggs into the inner Anthocoridae, Lyctocoridae, and Lasiochilidae surface of the bark, into rotting wood, or into (plus some related taxa such as the Cimicidae) have cracks in the bark. Species of Xylocoris that inhabit fertilization of the eggs occurring within the vitel- manure piles insert their eggs into cracks in the larium of the ovaries, rather than in the genital manure, whereas those species that inhabit straw ducts. The anthocorid egg lacks micropyles, and piles insert their eggs into the decaying straw. In fertilization takes place before the chorion is depos- species having a reduced or vestigial ovipositor ited. Oocyte maturation is inhibited in unmated (e.g., Cardiastethus), eggs are deposited on the females. Unfertilized eggs generally degenerate and substrate near prey. Lifetime egg production per are resorbed before they reach maturation, and female is highly variable even within species, and unmated females deposit few or no eggs. is probably affected extensively by diet quality. The Anthocoridae and related taxa have Lifetime estimates of fecundity obtained from evolved a number of unique reproductive struc- laboratory trials are available for Anthocoris tures that are used extensively by taxonomists in (70–220 eggs), Cardiastethus (35–45 eggs), Lycto- developing classification schemes and in defining coris (95 eggs), Montandoniola (50–150 eggs), phylogenetic affinities among higher level taxa Orius (90–130 eggs), and Xylocoris (20–80 eggs). (Table 10). In the Anthocoridae and Lyctocoridae, The pirate bugs have hemimetabolous devel- insemination of the female by the male is not done opment, in which the immatures (nymphs) undergo via the usual route through the female genitalia. Minute Pirate Bugs (Hemiptera: Anthocoridae) M 2409 Minute Pirate Bugs (Hemiptera: Anthocoridae), Table 10 Comparison of reproductive traits and structures (including the female paragenital system) among Lasiochilidae, Lyctocoridae, and Anthocoridae Lasiochilidae Lyctocoridae Anthocoridae 1. Insemination 1. intragenital 1. extragenital 1. extragenital 2. Intromittent organ 2. phallus 2. phallus with acus 2. paramere and/or phallus 3. Paragenital system 3. none 3. spermalege 3. spermalege, often in form of copulatory tube(s) 4. Site of copulation 4. female‘s genital 4. between segments 4. variable opening VII-VIII to right of genital (intragenitalic) opening 5. Sperm storage 5. bursa copulatrix 5. seminal conceptacles 5. seminal conceptacles or spermatic pocket

Rather, insemination occurs outside of the repro- used to penetrate the abdominal wall of the female ductive tract, within the abdominal cavity, and is for insemination (“traumatic insemination”). For thus referred to as extragenital insemination. The the Anthocoridae, the left paramere or the phallus sperm migrate through the haemocoel or through acts as the intromittent organ. In the Oriini, for specialized structures in the female (see below) to example, a portion of the left paramere (the flagel- the ovaries, and fertilize the developing egg within lum) is inserted within a specialized female organ the vitellarium before deposition of the chorion. It (the copulatory tube, as discussed below), and is not clear what evolutionary pressures have led the short membranous phallus slides along the to extragenital insemination in the Anthocoridae paramere to deposit sperm. The paramere itself or other taxa showing this trait, but it has been may be of quite complex shape in the Oriini, and in suggested that it is a means by which the male cir- fact is used extensively in differentiating species of cumvents female resistance or bypasses female Orius within some difficult species complexes. The control of sperm allocation and egg fertilization. Anthocorini exhibit a different strategy. In these Characteristics of the reproductive system species, the paramere is reduced to a relatively sim- show some similarities and some differences among ple, sickle-like organ, which is inserted only par- the Lasiochilidae, Lyctocoridae, and Anthocoridae, tially within the copulation site of the female. The and these traits have been used extensively in male then inflates his long, membranous phallus assessing phylogenetic affinities among these through the female’s copulatory tube to deposit groups. The Lasiochilidae differ from the Anthoc- sperm. In the Xylocorini, the left paramere is oridae and Lyctocoridae in that insemination is of sharply pointed, and is used to pierce the abdomi- the more typical insect type, occurring within the nal wall of the female at the copulation site. Copu- female’s reproductive system (i.e., intragenital lation may actually lead to scars that are visible on insemination), as opposed to the extragenital the surface of the female. insemination characteristic of the Anthocoridae Extragenital insemination in the Anthocori- and Lyctocoridae. In all three families, the male dae and related taxa has led to the evolution in genitalia are asymmetric. The right paramere is females of structures collectively referred to as the highly reduced or is absent. The intromittent organ paragenital system (spermalege). These organs are in the Lasiochilidae and Lyctocoridae is the phal- thought to have evolved as a means for the female lus. In the Lyctocoridae, the apex of the phallus is to reduce costs associated with traumatic insemi- sclerotized and in the form of an acus (needle), nation, caused by wounding of the cuticle at the 2410 M Minute Pirate Bugs (Hemiptera: Anthocoridae) copulation site or by the introduction of infections between abdominal segments VII and VIII. In the and infectious agents within the haemocoel of the Xylocorini, the site of copulation in some species female as the male inseminates her. The sperma- is on the dorsal side of the female, towards the lege consists of simple to complex structures that anterior end of the abdomen, while in other spe- act to guide the male’s intromittent organ to a species copulation takes place on the lateral (right) cific insemination site (the ectospermalege), and side of the abdomen. to receive the sperm (the mesospermalege). In The spermatheca is reduced to a small vermi- some taxa (e.g., the Anthocorini and Oriini), the form gland having no sperm storage function ectospermalege consists of a specialized copula- (Lasiochilidae), or is absent altogether (Lyctocori- tory tube, produced as an invagination of the epi- dae and Anthocoridae). In the Lyctocoridae, sperm dermis that opens between sternites VII-VIII on travel from the spermalege at the site of insemina- the ventral surface of the female, just lateral of the tion through the haemocoel into sperm storage female’s genital opening. The copulatory tube organs (seminal conceptacles) located at the base receives the paramere and phallus (as in the Oriini) of the ovaries. In the Anthocoridae, sperm are or phallus (as in the Anthocorini). The distal end of stored either in the sperm pocket (species having the copulatory tube enters a pouch (spermatic copulatory tubes: Oriini, Anthocorini, Scolopini, pocket or sperm pouch), which acts to temporarily Blaptostethini) or in seminal conceptacles (Xylo- store the sperm. In the Lyctocoridae, newly depos- corini). The seminal conceptacles in the Xylocorini ited sperm collect first in the mesospermalege (a and Lyctocoridae are not homologous, as they collection of specialized cells at the copulation derive from different tissues in the two taxa. From site), and then migrate through the haemocoel to the sperm storage organs (sperm pocket or semi- the sperm storage structures at the base of the ova- nal conceptacles), the sperm move to the ovaries ries. In the Xylocorini, the mesospermalege may through specialized conducting tissues, and fertil- be partially open or completely enclosed. If the ize the eggs within the vitellarium. mesospermalege is partially open, sperm move from the mesospermalege into the haemocoel, and migrate through the haemocoel to the sperm stor- Economic Importance age sites at the base of the ovaries. If the mesospermalege is completely enclosed, the structure The pirate bugs are sources of biological control extends to and connects with the sperm storage in annual and perennial crops, in forests, in structures. greenhouse crops, on ornamental plants, and in The actual site of copulation in the Anthoc- stored products. Several species of Anthocoris are oridae and related taxa is highly variable. In the known important sources of biological control in Lasiochilidae, which lacks a paragenital system, temperate fruit orchards, where they feed exten- insemination takes place within the female’s sively on pest psyllids and aphids. Species of genital tract. In the Lyctocoridae, the male pierces Orius occur in greenhouses and in a variety of the female on her ventral side between segments row crops, where they feed on thrips, mites, VII and VIII, to the right of the female’s genitalic aphids, and eggs of pest Lepidoptera. These pred- opening. Within the Anthocoridae, site of copula- ators may be particularly important natural ene- tion varies among tribes. In the Oriini and Anthoc- mies of flower thrips. Xylocoris and Lyctocoris orini, the copulatory tube opens between attack beetle and moth pests in stored products abdominal segments VII and VIII on the female’s and granaries. Aphid and scale pests that inhabit ventral side, usually to the left of her genital open- the canopies of coniferous trees are attacked by ing. Female Blaptostethini actually have paired Elatophilus, Tetraphleps, Melanocoris, and Acom- copulatory tubes, located on her ventral side pocoris, whereas bark beetle pests are fed upon Minute Pirate Bugs (Hemiptera: Anthocoridae) M 2411 beneath bark by species of Xylocoris, Scoloposce- into North America from Europe but which has lis, and Lyctocoris. Other species are important moved into habitats other than the target pear natural enemies of pests on ornamental plants, orchard, may compete with native Anthocoris including Montandoniola, Macrotrachelia, and species. Species that associate with stored food Macrotracheliella on ornamental fig (Ficus), where products (Lyctocoris, Xylocoris) have spread dra- they feed on the Cuban laurel thrips (Gynaiko- matically outside of their native ranges, appar- thrips ficorum (Marchal)). Species reared in insec- ently because of human commerce. These and taries for shipment and release include Orius other species of Anthocoridae are regularly inter- insidiosus, Orius laevigatus (Fieber), Orius majus- cepted at ports-of-entry on transported flowers, culus (Reuter), and Anthocoris nemoralis. fruits and vegetables, or on other plant materials. The Anthocoridae have been used in a num- As of 1999, it was thought that more than 50% of ber of classical biological control efforts. Classi- the anthocorid fauna in Hawaii was non- cal biological control is the importation and indigenous, with many of the exotic species release of exotic natural enemies for controlling arriving because of accidental introductions. non-indigenous pests. Anthocoris nemoralis, a Montandoniola moraguesi, which has been used species native to Europe, was released into west- extensively in classical biological control efforts ern North America in the early 1960s to control against thrips on Ficus, is now established in the an introduced psyllid pest of pears (Cacopsylla southeastern United States, apparently because pyricola (Förster)). The predator is now estab- of accidental introduction or natural dispersal. lished in British Columbia, Washington, Oregon, In North America, non-indigenous species that and California. Its effectiveness in controlling the have become established because of apparent psyllid pest of pears, however, is unclear. The accidental introductions or natural dispersal can North American Orius insidiosus has been intro- be found in the genera Anthocoris, Brachysteles, duced into Europe and Hawaii for controlling Buchananiella, Dufouriellus, Lyctocoris (Lycto- Thysanoptera and Lepido-ptera, and is estab- coridae), Montandoniola, Orius, Temnostethus, lished in Hawaii. Montandoniola moraguesi and Xylocoris. Effects of these exotic species on (Puton) is native to southeast Asia, but has been North American ecosystems are unknown. released in southern California, Texas, Bermuda, and Hawaii to control Cuban laurel thrips. The References predator has become established in Bermuda and Hawaii, apparently as a consequence of these Blatchley WS (1926) Heteroptera or true bugs of eastern introductions. Two species of Tetraphleps were North America. The Nature Publishing Company, Indi- introduced into North America from India and anapolis, IN, 1,116 pp Pakistan for control of the balsam woolly aphid Carayon J (1972) Caractères systématiques et classification (Adelges piceae (Ratzeburg)), a non-indigenous des Anthocoridae (Hemipt). Annales de la Société Entomologique de France (N.S.) 8:309–349 pest of various coniferous trees. Apparently nei- Carayon J (1977) Insemination extra-génitale traumatique. ther species became established. In: Grassé P-P (ed) Traité de Zoologie. Anatomie, systé- A number of species have become estab- matique, biologie. Tome VIII. Insectes. Gamètogenèses, lished outside of their native ranges because of fécondation, métamorphoses. Masson, Paris, France, pp 351–390 accidental introductions or dispersal. Effects of Cassis G, Gross GF (1995) Hemiptera. Heteroptera (Coleor- these introductions upon native predators (via rhyncha to Cimicomorpha). In: Houston WWK, May- competition) and native prey (via predation) are nard GV (eds) Zoological Catalogue of Australia, vol 27.3A. CSIRO, Melbourne, Australia, 506 pp unknown, but are potentially important. There Ford LJ (1979) The phylogeny and biogeography of the Cimi- has been speculation, for example, that Anthoco- coidea (Insecta: Hemiptera). M.S. thesis, University of ris nemoralis, which was introduced intentionally Connecticut, Storrs, CT, 139 pp 2412 M Minute Tree-Fungus Beetles Henry TJ (1988) Family Anthocoridae Fieber, 1837. In: Henry TJ, Mite Pests of Crops in Asia Froeschner RC (eds) Catalog of the Heteroptera, or true bugs, of Canada and the Continental United States. E.J. Brill, Leiden, The Netherlands, pp. 12–18 (Corrections and addi- Chyi-Chen Ho tions to the catalog are available. In: Henry TJ, Froeschner Taiwan Agricultural Research Institute, Wufeng, RC (1992) Proc Entomol Soc Wash 94:263–272) Taichung, Taiwan Herring JL (1976) Keys to genera of Anthocoridae of America north of Mexico, with description of a new genus (Hemiptera: Heteroptera). The Fla Entomol 59:143–150 Acarine pests of agricultural crops include mites in Kelton LA (1978) The insects and arachnids of Canada, pt 4. the families Tetranychidae, Tenuipalpidae, Tarsone- The Anthocoridae of Canada and Alaska. Heteroptera: Anthocoridae. Agriculture Canada Research Publica- midae, Eriophyidae, and Acaridae. Members of all tion 1639. Ottawa, ON, Canada, 101 pp these families are reported to damage various crops Lattin JD (1999) Bionomics of the Anthocoridae. Annu Rev in Asia. Among the damaging species are Amphitet- Entomol 44:207–231 ranychus viennensis, Eotetranychus cendanai, Eo. Lattin JD (2000) Minute pirate bugs (Anthocoridae). In: Schaefer CW, Panizzi AR (eds) Heteroptera of economic kankitus, Eotetranychus pruni, Eotetranychus importance. CRC Press, Boca Raton, FL, pp 607–637 sexmaculatus, Eutetranychus africanus, Eu. orienta- Maw HEL, Foottit RG, Hamilton KGA, Scudder GGE (2000) lis, Oligonychus coffeae, O. litchii, O. mangiferus, Checklist of the Hemiptera of Canada and Alaska. NRC Panonychus citri, P. u lmi , Petrobia latens, Tetranychus Research Press, Ottawa, ON, Canada, 220 pp Péricart J (1972) Hémiptères. Anthocoridae, Cimicidae, cinnabarinus, T. fijiensis, T. hydrangeae, T. kanzawai, Microphysidae de l’Ouest-Paléarctique. Faune de T. macfarlanei, T. piercei, T. truncatus, T. urticae l’Europe et du Bassin Méditerranéen. Masson et Cie, (Tetranychidae); Brevipalpus californicus, B. obova- Paris, France, 402 pp Péricart J (1996) Family Anthocoridae Fieber, 1836 – Flower tus, B. phoenicis, Dolichotetranychus floridanus, bugs, minute pirate bugs. In: Aukema B, Rieger C (eds) Larvacarus transitans, Tenuipalpus pacificus, Raoi- Catalogue of the Heteroptera of the Palaearctic Region. ella indica (Tenuipalpidae); Phytonemus pallidus, The Netherlands Entomological Society, Amsterdam, Polyphagotarsonemus latus, Steneotarsonemus The Netherlands, pp 108–140 Schuh RT, Štys P (1991) Phylogenetic analysis of cimicomor- bancrofti, S. spinki (Tarsonemidae); Acaphylla theae, phan family relationships (Heteroptera). J N Y Entomol Acaspina litchii, Aceria cajani, A. doctersi, A. eriobot- Soc 99:298–350 rya, A. litchi, A. mangiferae, A. sheldoni, A. tulipae, Schuh RT, Slater JA (1995) True bugs of the world (Hemiptera: Aculops lycopersici, Aculus schlechtendali, Eriophyes Heteroptera): Classification and natural history. Cornell University Press, Ithaca, NY, 336 pp litchii, Phyllocoptruta oleivora (Eriophyidae); Rhizo- Štys P (1975) Suprageneric nomenclature of Anthocoridae glyphus echinopus, R. robini, R. setosus (Acaridae). (Heteroptera). Acta Universitatis Carolinae – Biologica Among them, Amphitetranychus viennensis, 1973:159–162 T. urticae, T. cinnabarinus, P. c itr i , P. u lmi , O. coffeae, B. obovatus, B. phoenicis, B. californicus, Polyphago- tarsonemus latus, Phytonemus pallidus, Phyllocoptruta Minute Tree-Fungus Beetles oleivora, and A. tulipae are worldwide-distributed species and are commonly found from East Asia. Members of the family Ciidae (order Coleoptera). These species are important pests of a wide range of  Beetles crops. Many of them are notorious in having developed resistance to various acaricides. In addition, T. urticae, B. phoenicis, B. californicus, and A. tuli- Miridae pae are known to be able to transmit virus diseases of plants. Distribution of Amphitetranychus vienn- A family of bugs (order Hemiptera). They some- ensis is limited to the temperate zone or, in sub- times are called plant bugs or capsids. tropical areas, to high elevations with cold climates.  Plant Bugs Tetranychus kanzawai is another notorious  Bugs polyphagous mite pest distributed commonly in Mites (Acari) M 2413 East Asia, but is rarely recorded from other area of Rhizoglyphus echinopus, R. robini, and R. setosus the world. Tetranychus truncatus is recorded from are recorded only from a few Asian countries. The the Far East and Southeast Asia, and is not consid- former two species are distributed worldwide, and ered to be a serious crop pest except in China are infamous in being difficult to control. They may and Thailand. Eutetranychus orientalis has been be distributed in more Asia countries than their recorded from most Asian countries, mainly current distribution record, as may R. setosus. infesting citrus. However, it is not considered an  Mites important pest in Japan and Taiwan. The other mites either are recorded as pests from limited countries, or have a narrow host range. References Petrobia latens infests wheat, barley, sorghum, grasses, and a few other crops and is known from CABI (2001) Crop protection compendium, 2001 edn. CAB China, India, Japan, Korea, and Taiwan. Aceria International, Wallingford, UK Ehara S (1999) Revision of the spider mite family Tetranychi- mangiferae and O. mangiferus mainly infest mango dae of Japan (Acari, Prostigmata). Jpn Soc Syst Zool and are recorded only from a few Asian countries, 4:63–141 though mango is commonly cultivated in southern Ho CC, Lo KC, Chen WH (1997) Spider mite (Acari: Tetrany- Asia. Eotetranychus kankitus, Eo. pruni, and Eo. sex- chidae) on various crops in Taiwan. J Agric Res Chin 46:333–346 maculatus damage citrus, apple, and citrus and Kongchuensin M, Charanasri V (1999) Mites injurious to rubber trees in China, respectively. Aceria cajani agricultural crops of economic importance in Thailand transmits the sterility mosaic virus disease of pigeon (abstract). The 4th International symposium on popula- pea in India and neighboring countries. Aceria tion dynamics of plant-inhabiting mites. May 10–14, 1999, Kyoto, Japan doctersi decreases the oil content of cinnamon Wang HF (1981) Acariformes: Tetranychoidea. Econ insect (Cinnamomum zeylanicum) leaves in Indonesia and fauna Chin 23:1–150 Sri Lanka by 18–43%. Aceria sheldoni and Aculops lycopersici are mainly recorded from west Asia. The former species infests citrus. The latter infests tomato Mites (Acari) and several other crops of Solanaceae, and may cause serious reductions in yield of tomato. Aculus Lewis B. Coons, Marjorie Rothschild schlechtendali is a pest of apple and pear, and is The University of Memphis, Memphis, TN, USA recorded from Japan, India, Pakistan, and Leb- anon. Eutetranychus africanus is an important pest Mites belong to the subclass Acari, the largest and of durian, a well-known, peculiar fruit produced in most diverse group in the class Chelicera. Because several countries of Southeast Asia. Eotetranychus of their small size and secretive lives, much remains cendanai, T. hydrangeae, T. macfarlanei, and T. fijien- to be known about their biology and classification. sis also are important crop pests in Thailand. Mites are distributed worldwide. Some species are Aceria eriobotrya infests the tip of loquat of great economic importance as pests of agricul- twigs. Eriophyes litchii and Acaspina litchii cause tural crops and vectors of important diseases of leaf erenia to litchee. Larvacarus transitans is a man, domestic animals and plants. serious pest of ber in India. Dolichotetranychus floridanus is a pest of pineapple. Raoiella indica infests betelnut and coconut. Steneotarsonemus Evolution and Diversity of Mites bancrofti scars the surface of sugarcane. Infesta- tion of Oligonychus uruma, Schizotetranychus Mites are an ancient group of chelicerates. The earli- nanjingensis, and Aponychus corpuzae can cause est known mite fossils are from the Devonian period the death of entire bamboo forests. of geologic time. The fossil record suggests that 2414 M Mites (Acari) during the late Mesozoic to early Cenozoic an The protonymph is the first nymphal instar after the adaptive radiation of mites occurred with the devel- larvae. Protonymphs are usually found in the same opment of many nonpredatory species. Flowering type of environment as are other nymphal instars. plants and insects as well as birds and mammals The protonymph can be either an active or inactive became more widespread during this same period, feeding stage depending on the species. The providing many novel habitats for mites to exploit. deutonymph is the next nymphal instar. This stage Mites are distributed throughout the world is like the adult in size and design, but often differs and inhabit almost every ecosystem. They play an in having a less complex sclerotization and setal important ecological role as inhabitants of the for- pattern. The final nymphal instar is a tritonymph. In est floor and soil where they are secondary decom- its absence the deutonymph molts into an adult. posers of organic matter. Mites are vectors of The adult forms can be similar (homomorphic) or diseases that affect humans, livestock and crops, dissimilar (heteromophic) in one or both sexes, and and are stored product pests and crop pests. various male forms (andropolymorphism) are Mites can be broadly divided into free living found in a few groups. Molting is rare during the and parasitic species. Free living species are by far adult stage but occurs in some species. the most common and are found in all the orders with the exception of the Ixodida (ticks). Ecto and endoparasitic mites attack both vertebrates and Classification: The Orders of Mites invertebrates. Most of endoparasitic species found on vertebrates reside within the respiratory tract. There are over 30,000 named species of mites Mites are the most common arthropod ectopara- (Table 11) and possibly up to a million unknown sites of vertebrates, and humans. Species of the species. A list of the major taxa of the Acari human follicle mite Demodex are present on most follows. people throughout the world. Most scientists divide the Acari into two major groups, the Anactinotrichida and the Acti- notrichida. We consider the Anactinotrichida Generalized Life History and Actinotrichida superorders, and the major groups within each as orders. Traditionally, the All mites pass through the same four life stages, position of the respiratory opening, the stigmata egg, larva, nymph and adult, but much variation has been used to name the major groups within occurs within the active stages. The most common the two superorders. However, as discussed under active stages include a prelarva, larva, protonymph, the different orders, this system is ambiguous and deutonymph, tritonymph, and adult. A molt occurs has mostly been abandoned for a terminology between each stage. During the molt, the old cuti- that ends in “–ida.” Many of the orders that use cle is cast off and replaced by a new one. the position of the stigmata are now lesser taxa. The prelarva is the most primitive postembryonic form and commonly remains within the egg. It is usually a nonfeeding quiescent stage. Anactinotrichida Larvae of most species are six legged. Larvae lack external genital openings and are not well sclero- “Anactinotrichida” refers to the lack of a birefringent tized. They have few useful taxonomic characteris- material in cuticular setae. The Anactinotrichida is tics. Most larvae are active feeding forms. divided into four orders, the Oplioacarida, Holothy- Nymphs are eight legged and their body is rida, Ixodida, and Gamasida. Some scientists group more sclerotized and has more taxonomic charac- the Holothyrida, Ixodida and Gamasida as the teristics than larvae, making them easier to identify. Parasitiformes and separate out the Oplioacarida Mites (Acari) M 2415

Mites (Acari), Table 11 Major taxa of the Acari. Mites (Acari), Table 11 Major taxa of the Acari. Numbers in parentheses refer to number of Numbers in parentheses refer to number of families in the taxon families in the taxon (Continued) Subclass: Acari Parantennuloidea (2) Lordalycidae Superorder: Heterozerconina Nanorchestidae Hydryphantoidea Anactinotrichida Bimichaeliidae Eylaioidea Order: Opilioacarida Heterozerconidae Nematalycidae Hydrovolzioidea Opilioacaridae Discozerconidae Proteonematalycidae Hydrachnoidea Order: Holothyridae Sejina Micropsammidae Lebertioidea Holothyridae Sejidae Oehserchestidae Hygrobatoidea Allothyridae Grandjeanicidae Arrenuroidea Neothyridae Ichthyosomatogasteridae Terpnacaridae Teneriffidae Order: lxodida (3) Uropodellidae Caeculidae Stigmocheylidae Order: Gamasida Microgyniina Adamystidae Paratydeidae Cercomegistina Microgyniidae Eupodina Order: Oribatida Cercomegistidae Uropodina Bdelloidea (2) Macrophylina Asternoseiidae Thinozerconoidea Halacaroidea (1) Palaeosomata (6) Davacaridae Polyaspidoidea Labidostommatidae Seiodidae Uropodoidea Eupodoidea (5) Archeonothroidea Antennophorina Diarthrophalloidea Tydeoidea (2–3) Palaeacaroidea Aenictequoidea (4) Epicriina Eriophyoidea (3) Ctenacaroidea Antennophoroidea (1) Epicriidae Eleutherengona Enarthronota (13) Celaenopsoidea (8) Zerconina Tetranychoidea Fedrizzioidea (4) Zerconidae (5–6) Megisthanoidea (2) Arctacarina Cheyletoidea (8) Hypochthonoidea Arctacaridae Alicorhagiidae Raphignathoidea (9) Parasitina Proterorhagiidae Pterygosomatoidea Brachychthonoidea Parasitidae Prostigmata (9) Pergamasidae Anystina Pomerantizioidea (1) Dermanyssina Anystidae Pseudocheylidae Atopochthonioidea Rhodacaroidea (3) Parasitengona (58) Tarsonemina (11) Veigaioidea (1) Trombidia Tarsocheyloidea Heterochthonoidea Eviphidoidea (5) Heterocheyloidea Protoplophoroidea Ascoidea (7) Calyptostomatoidea Pyemotoidea Parhyposomata (3) Dermanyssoidea (18) Erythraeoidea Pygmephoroidea Parhypochthonioidea Superorder Trombidioidea Tarsonemoidea Mixonomata (10–11) Actinotrichida Phthiracaroidea Plateremaeoidea Order Actinedida Hydrachnidia Damaeoidea Endeostigmata Euphthiracaroidea Cepheoidea Sphaerolichidae Stygothrombioidea Lohmannioidea 2416 M Mites (Acari) Mites (Acari), Table 11 Major taxa of the Acari. because they appear to be the most primitive mite Numbers in parentheses refer to number of group. Others group only the Gamasida and the families in the taxon (Continued) Ixodida as the Parasitiformes (Fig. 57). Polypterozetoidea Eulohmannioidea Charassobatoidea Oplioacarida Perlohmannioidea Microzetoidea Amerobelboidea These are relatively large mites, greater than 1 mm in length, with a leathery cuticle. They resem- Epilohmannioidea Eremaeoidea ble the opilones or daddy long-legs. This is the Zetorchestoidea smallest order of mites. One family is recognized, Collohmannioidea Gustavioidea Nehypochthonioidea Carabodoidea Desmonomata (8) Tectocepheoidea Crotonioidea Oppioidea Hydrozetoidea Nanhermannioidea Hermannioidea Ameronothroidea Brachypylina(>100) Pycnonota Cymbaeremaeoidea Poronota Hermannielloidea Licneremaeoidea Neoliodoidea Oripodoidea Ceratozetoidea Phenopelopoidea Oribatelloidea Achipterioidea Galumnoidea Order Acaridida Acaridia Schizoglyphoidea (1) Histiostomatoidea (2) Canestrinioidea (2) Hemisarcoptoidea (6) Glycyphagoidea (7) Acaroidea (4) Hypoderatoidea (1) Psoroptidia Mites (Acari), Figure 57 Dorsal view of Pterolichoidea (13) Opilioacarus segmentatus (Anactinotrichida, Analgoidea (14) Opilioacarida) Oc, ocelli; st, stigmata (from Alberti Sarcoptoidea (14) G,Coons LB (1999) The Acari-mites, used with permission of John Wiley and Sons, Inc). Mites (Acari) M 2417 with eight genera and about 20 species. Oplioacar- ids often have bright pigments distributed in bands across their bodies. The life stages consist of a six- legged quiescent prelarva that molts into a larva. Opiloacarid larvae are unusual in that they have vestiges of the fourth pair of legs. The larva molts into a protonymph, which molts into a deutonymph then a tritonymph which molts into an adult. Adults are unusual in that they may continue to molt. These mites are considered omnivorous, feeding on both small insects and pollen, but they may also be scavengers. Oplioacarids are distributed in Texas in the USA, through South America, the island of Puerto Rico, central Asia through to Africa and southern Europe. They are found especially in semiarid regions where they often are found in the forest litter or dark places such as under rocks, particularly during the day. Oplioac- arida are sometimes known as the Notostigmata since they have four pairs of stigmata on the dorsolateral body.

Holothyrida

The Holothyrida have three families, six genera Mites (Acari), Figure 58 Ventro-lateral view of and about 15 species. Holothyrids are found in Holothyrus coccinella (Holothyrida) (from Hughes. Australia, New Zealand, islands in the Indian and 1959. Mites or the Acari, used with permission of Pacific Oceans, and the Neotropics. These are large The Athlone Press). predatory mites that vary in length from about 2–7 mm. The life stages are larva, protonymph, deutonymph, tritonymph and adult. Holothyrids are moderately to heavily sclerotized mites with Ixodida long legs and an oval body that shows no visible subdivisions. Holothyrids (Fig. 58) are closely Ixodids or ticks are obligatory blood feeding related to the Ixodida. They have a sensory area on ectoparasites of vertebrates. Ticks are found their first pair of legs that resembles Haller’s organ worldwide. They are divided into three families, of ixodids. Holothyrids are found under stones or the Argasidae or soft ticks, the Nuttalliellidae in humus in tropical forests around the world. with one species, and the Ixodidae or hard ticks. They may be scavengers that mostly eat solid food Some 850 species have been described. They such as dead woodlice and amphipods. These transmit serious diseases to humans, livestock mites have been implicated in poisonings of poul- and companion animals. Ixodida were previ- try and humans. Holothyrida were previously ously known as the Metastigmata, however the known as the Tetrastigmata despite the fact that stigmata are found behind the fourth pair of they have only two pair of stigmata. legs only in the hard ticks while soft ticks have 2418 M Mites (Acari) the stigmata between the third and fourth pair size from 0.2 to 2.0 mm in length. They are often of legs. Ticks are covered in a separate entry. highly sclerotized with several cuticular shields such as the sternal, genital and anal shields (Fig. 59) that are useful as taxonomic characters as are the Gamasida positions and number of setae. Setae are hairlike projections of the cuticle and are common on many This is the most diverse order and contains the mites in both superorders. These taxonomic char- largest number of species in the Anactinotrichida. acters are also used throughout the Acari. The There are some 77 families divided into 11 sub- Gamasida are still known by some acarologists as groups with about 5,000 species. Gamasids are the Mesostigmata since they have a pair of stigmata found worldwide in diverse habitats. A typical dorsolateral or ventrolateral to the legs. gamasid life cycle consists of an egg, and four active Most Gamasida are free living predaceous or stages: larva, protonymph, deutonymph and adult. fungivorous soil-inhabiting mites or are epizoons, The most common variation on this life cycle is the attached to the body of arthropods, or commen- occurrence of a nonfeeding larval stage and a pho- sals with other arthropods. Commensals benefit retic stage in the deutonymph. Gamasids range in from a common food supply but do not harm the

Hypostome

Basis capituli

Peritreme Sternal shield

Genital seta Genital shield

Stigma

Anal shield

100µm

Mites (Acari), Figure 59 Ventral view of female tropical poultry mite Ornithonyssus bursa (Gamasida, Dermanyssoidea, Macronyssidae) (from Kettle DS (1995) Medical and veterinary entomology, used with permission of CAB International). Mites (Acari) M 2419 other species. Some gamasids are parasites of ver- predatory mites found in mosses and litter in tem- tebrates and invertebrates. perate forests. The superfamily Eviphidoidea are The Cercomegistina are made up of four fam- mostly free-living mites found in litter and humus ilies that are mostly free living mites in litter and of soils or are associates of other arthropods. This humus, but the species of one family are associ- superfamily contains several species of mites that ated with other arthropods. The Antennophorina are used as biological control agents. The super- are divided into six superfamilies with mites that family Ascoidea are a diverse assemblage of mites. are associated with arthropods, lizards or snakes. Phytoseiulus persimilis (Ascoidea: Phytoseiidae) is The Heterozerconina comprise two families that used as a biocontrol agent against red spider mites are commensals or parasites on millipedes, centi- (Tetranychidae) (Fig. 62) in greenhouses. The pedes or snakes. Very little is known about these superfamily Dermanyssoidea includes many eco- curious mites. The Sejina contain three families nomically important parasites as well as predatory that are associated with other arthropods or found species found in nests or in the soil, and contain in forest litter or the nests of vertebrates but other- all gamasid species of medical or veterinary wise their biology is not known. They are distrib- importance. The Dermanyssidae, Macronyssidae, uted worldwide. The little known Microgyniina Spinturnicidae, and Histrichonyssidae are para- have a single family found in woody debris in the sites that feed on the blood of birds and mammals. Holarctic Region. The families Halarachnidae and Rhinonyssidae The Uropodina, with four superfamilies, are are parasites of the respiratory tracts of birds and found throughout the temperate and tropical mammals. The family Varroidae contains the zones where they occur mostly in forest litter. bee parasite Varroa destructor which is further Some are seashore dwellers. Species in this group described in the section on “Bee mites.” are fungivores, scavengers or predators. Species of Uropodina have phoretic deutonymphs. The Diar- thropalloidea, a superfamily of Uropodina, are Actinotrichida parasitic on passalid beetles and are distributed in the neotropical and Australian zones. The Epicriina, “Actinotrichida” refers to the presence of a bire- Zerconina and Arctacarina, each with one family, fringent material in cuticular setae. Some workers have similar distributions and habitats. They are use the name Acariformes for Actinotrichida. The found in the northern hemisphere in leaf litter and Actinotrichida contain the largest number of humus. Their biology is poorly known. The Parasi- species and has the most morphological and eco- tina contain two families whose species are com- logical diversity of the two superorders. There are mon in soils and organic debris throughout the three orders in the Actinotrichida, namely, Actin- world. They are associated with insects or are edida, Oribatida and Acaridida. The last two orders predators of smaller arthropods and nematodes. are closely related and are referred to by some The Dermanyssina, with five superfamilies, workers as Sarcoptiformes. have the largest number of species and the most diversity in the Gamasida. This is the only sub- group of Gamasida that contains species of medi- Actinedida cal and veterinary importance. Parasitic mites of the Dermanyssoidea often have highly modified This is the largest order of mites with some 136 external morphology and life cycles. The superfamilies, over 1,100 genera and more than 14,000 family Rhodacaroidea make up the dominant species so far described. Unfortunately, the higher gamasid predators in tropical soils. The super- classification of this important group is not family Veigaioidea contains a single family of settled. Actinedids are distributed worldwide in 2420 M Mites (Acari) terrestrial, freshwater and marine habitats. They range in size from about 0.1–16 mm. Most Actin- Cheliceral blade edida are soft bodied mites, but heavily sclerotized species occur in some families and there is a wide range of intermediates between the soft-bodied Scutum and sclerotized forms. The Actinedida is divided into the Endostigmata and the Prostigmata. The Endostigmata contain 12 families and Sensillum is considered to be the most primitive Actine- Eye dida. These are small soft bodied free living mites that occur in humus, litter and soil in South Africa. They are believed to be predaceous or microphytophagous. The Prostigmata are divided into three subgroups, the Anystina, Eupodina and Eleutheren- 100µm gona. The Anystina are mostly free-living predators Mites (Acari), Figure 60 Dorsal view of the larva or that occur in soil litter, on vegetation and on the chigger of Leptotrombidium deliense (Actinedida, seashore. The Parasitengona are a large group of Trombidioidea, Trombidiidae), a vector of chigger mite species in which most species have a parasitic borne typhus. (from Kettle DS (1995) Medical and larva. The Trombidia contain three superfamilies veterinary entomology, used with permission of among which are the Trombidioidea with the fam- CAB International). ily Trombiculidae whose larval forms or chiggers are important parasites of terrestrial vertebrates and man (Fig. 60). The other life stages are predators on small invertebrates. The Hydrachnidia contain eight superfamilies. These are freshwater mites, although one family, the Pontarachnidae have secondarily spread into marine habitats. The Eupodina is the second group and consists mostly of free-living mites. The superfamily Bdelloidea contain the snout mites that prey on other mite species. Some species of snout mites use silk to capture their prey and many spin a cocoon for use during molting. The superfamily Halacaroidea contain marine mites with some freshwater forms. The family Penthaleidae has one species of economic importance, the winter grain mite Penthaleus major. The Eriophyoidea (Fig. 61) Mites (Acari), Figure 61 The two principal body are plant pests that cause severe damage and can types of Eriophyoidea (Actinedida, Eupodina). induce gall formation. Phytoptus leucothonius (top) with a vermiform The Eleutherengona are found in various habi- body and Anthocoptes helianthella (bottom) with tats. Spider mites of the superfamily Tetranychoidea a fusiform body (redrawn from Lindquist et al. are worldwide in distribution. Many species are (1996) Eriophyoid mites: their biology, natural serious pests of plants. Some produce galls and enemies, and control, used with permission of other types of plant damage (Fig. 62). Some species Elsevier Science). Mites (Acari) M 2421 Palp I

II P Aedeagus Epimeres

Genital opening

III Anus

IV Mites (Acari), Figure 62 The spider mite Tetranhychus urticae (Actinedida, Tetranychoidea). Mites (Acari), Figure 63 Dorsal view of male Legs are numbered I, II, III, IV (redrawn from Evans (left) and female (right) Demodex (Actinedida, GO, Sheals JG, Macfarlane D (1961) The terrestrial Cheyletoidea, Demodicidae) (from Kettle DS Acari of the British Isles, vol 1. British Museum of (1995) Medical and veterinary entomology, used Natural History). with permission of CAB International). are the only known mites to transmit plant viruses. and humus. The Tarsonemina are small mites from An inactive period occurs between each of the final 200 to 600 μm in size. They have unusual life histo- three life stages. During this inactive period, the ries and reproductive strategies. Physogastry, a type larva or nymph uses silk to anchor itself to the plant. of reproduction where eggs develop in the female, Spider mites have the capability of rapidly coloniz- is found in many parasitic tarsoneminids. In some ing plants. This ability comes from the large number species, the entire postembryonic development of generations produced during a given season and occurs within the female or the eggs transform not from fecundity. Two heteromorphic females directly into adults. The physogastric genus (Fig. 64) may be produced, the specialized overwintering Pyemotes of the family Pyemotidae has a life cycle form, and the typical female form. The superfamily where all post embryonic development occurs Cheyletoidea are ectoparasites of birds and mam- within the body of the female. Some members of the mals, and contain the follicle mites. These are further family Pyemotidae are predators of insects of both discussed in the section on “skin parasites.” Mites of positive and negative economic importance. the family Cloacaridae are found in the cloaca of turtles. The superfamily Raphignathoidea contain mostly predaceous mites and species that are pests Oribatida of plants. The superfamily Pterygosomatoidea contains species that are mostly parasites on other The Oribatida are known as beetle mites arthropods or on lizards. The superfamily Pomeran- (Figs. 65–68) from their outward appearance, or tizoidea are mostly free living predators in soil litter moss mites from their habitats, or box mites from 2422 M Mites (Acari)

Mites (Acari), Figure 64 Lateral view of a gravid Pyemotes tritici. The opisthosoma is the swollen posterior area behind the legs containing eggs Mites (Acari), Figure 66 The oribatid Eupelops and offspring (from Kettle DS (1995) Medical and torulosus has a well developed cerotegument or veterinary entomology, used with permission of secretion layer (CR) that covers the body surface (S), CAB International). and movable cuticular plates or pteromorphs that cover lateral body parts (arrowheads) (redrawn from Alberti G, Coons LB (1999) The Acari-mites, used with permission of John Wiley and Sons, Inc.)

Mites (Acari), Figure 65 Phthiracarus sp. (Oribatida, Phthiracaroidea), a box mite. When attacked, the mouthparts (gnathosoma) and retracted legs are covered by an operculum-like aspis (arrows), and the lateral body parts are covered by cuticular plates or pteromorphs (arrowheads) (redrawn from Alberti G, Coons LB (1999) The Acari-mites, used with permission of John Wiley and Sons, Inc.). Mites (Acari), Figure 67 The oribatid Heterochthonius gibbus (Heterochthonioidea, Heterochthoniidae), a beetle-like mite. Note the their ability to (Fig. 65) cover their retracted legs eyes (arrowheads). The long dorsal setae are able with their body. There are some 150 families, over to erect (from Alberti G, Coons LB (1999) The 1,000 genera, and more than 7,000 described spe- Acari-mites, used with permission of John Wiley cies of Oribatida. The order is divided into the and Sons, Inc). Mites (Acari) M 2423 particulate feeders with mouthparts modified to cut or tear particles up so they can be swallowed. They are saprophagous on decaying higher plant material or microphytophagous on soil microorganisms. The fecal pellet contributes to the soil structure. The oribatids act on the soil system principally by regulating the rate of organic matter decomposition and are considered to be important decomposers. This order is most diverse in the tropics where these mites are the dominant Acari in soils. Some oribatids are intermediate hosts to the sheep tapeworm Moniezia expansa. Many species are parthenogenetic, otherwise sperm transfer occurs by stalked sper- matophores deposited by a penis. The female picks it up with the genital vestibule. An ovipositor is common. Oribatid mites have a lower fecundity than most other mites.

Mites (Acari), Figure 68 A tritonymph (T) of the Acaridida oribatid Cepheus dentatus (Cepheoidea, Cepheidae) with three scalps on its dorsum, one from each of its The Acaridida contain some 70 families divided previous instars, larva (1), protonymph (2), into 800 genera and about 5,000 species. The deuteronymph (3) (relabeled from Hughes TE Mites Acaridida are thought to have evolved within the of the Acari, used with permission of The Athlone Press). Oribatida. Acaridids are worldwide in distribution. Sperm transfer occurs by the use of a penis or aedeagus. Sexual dimorphism is common. Macropylina, also known as lower oribatids or Most species have a hypopus in the deutonymphal Archoribatida, and the Brachyplyina, also known stage. The hypopus is highly modified for survival as the higher oribatids or Euoribatida. The Macro- in marginal conditions and for dispersal by pylina are divided into five subgroups, and the phoresy, or by wind. Acarids include free living Brachyplyina are divided into two subgroups. The species and those that are associated with other Oribatida were previously known as the Cryp- animals such as mammals, birds and insects. Par- tostigmata but many of these mites completely asitic species include skin, hair follicle, or feather lack a stigmata or a tracheal system. parasites of birds and mammals. Others are respi- Oribatids are worldwide in distribution. ratory parasites of birds and mammals. Most are Most range in size 0.3–0.7 mm in size with the nonpredatory. Free living species are found in a smallest 0.15 mm and the largest 1.5 mm in size. variety of habitats including decaying organic Sexual dimorphism is scant or nonexistent. Most matter and nests of other animals. The free living oribatids are soil dwellers, but they are also found forms have evolved some interesting and unusual in moss, humus, lichens, and occasionally on veg- feeding habits that vary from filter feeding of etation. A few species are phoretic, usually on microorganisms to eating solid food to direct beetles. Phoresy is discussed in the section on absorption of food material. Many Acaridida have “Dispersion of mites.” Oribatids are slow moving, a short generation time which rapidly produces 2424 M Mites (Acari) large populations. This allows the exploitation of are found in the nests of birds and rodents. Often patchy or ephemeral food resources. Acaridida the deutonymphs are subcutaneous or less com- are weakly sclerotized mites, although sclerotiza- monly internal parasites. tion of the dorsal area occurs to some extent in The Psoroptidia contain three superfamilies. several species. Acaridida were known as the Mites of the superfamilies Pterolichoidea and Astigmata. Analgoidea are associated with birds. All the Pter- The Acaridia are divided into two subgroups, olichoidea and part of the Analgoidea constitute the Acarida and the Psoroptidia. The Acarida con- the feather mites. Feather mites (Fig. 69) are a large tain seven superfamilies. The Schizoglyphoidea group that are commensals or parasites of birds. are only known from the phoretic deutonymphs They are found on wing, tail feathers or flight collected from a tenebrionid beetle in New feathers. A few are free living in birds nests. In Guinea. The Histiostomatidea contain the Ano- some feather mites with male polymorphism, etidae, the slime mites. Slime mites are filter feed- homeomorphic males have female-like mouth- ers with a unique gnathosomal structure that parts and heteromorphic males have strongly strains microorganisms and other food sub- aberrant enlarged chelicerae and elongated palpi. stances. Species of slime mites are found world- Other species of Analgoidea are parasites of the wide in liquid or semiliquid habitats where respiratory tract of birds. The superfamily Sarcop- organic matter is undergoing putrefaction. Some toidea (=Psoroptoidea) contains many economi- slime mites are found in marine environments cally important mites. Some species cause mange such as intertidal algal habitats, others occur in and (Fig. 70) scabies, which are further described the unusual aquatic habitat of pitcher plants. The in the section on “skin parasites.” Guanolichidae are unusual acarids in that they are completely sclerotized in the adult forms. These mites are found in bat guano where they are most likely filter feeders. Canestrinioidea are mostly commensals or parasites found on adult Coleoptera. Most are found under the elytra of beetles where they are thought to feed on exudates, but some occur near the mouthparts of the host from which they obtain food. They are widely distributed except in the Nearctic. The Hemisar- coptoidea occur in a variety of habitats. Most species are associated with wood related habitats. Other habitats of hemisarcoptids include the nests of solitary bees, intertidal zones, and some species live in aquatic or semiaquatic habitats in sap exudates of water-filled tree holes. Mites of the superfamily Glycyphagoidea are mostly associated with mammals, birds, and insects, but some Mites (Acari), Figure 69 Male (a) and female species are pests of stored food products. Most (b) of the feather mite Euschizalges laglaizeae species of the Acaroidea are found in the nests of (Acaridida, Analgoidea) showing sexual vertebrates and insects, but some species are dimorphism. Note the adanal suckers of the male found in carrion and dung. The super family (arrow) (from Kettle DS (1995) Medical and Hypoderatoidea are believed to be closest to taxa veterinary entomology, 2nd edn, used with of the Psoroptidia. Species of Hypoderatoidea permission of CAB International). Mites (Acari) M 2425

Anterior vertical and the Acaridida. Phoretic forms vary from seta those that resemble the non-phoretic instar to highly specialized forms such as hypopi. Phoretic hypopi use claspers or suckers to attach to other Pulvillus animals. Not all attach to animals, some are inert and rely on wind dispersion. The association between phoretics and their hosts ranges from the specific use of a single host species, to the use of a variety of host species. Most phoretic mites Scales are species that can rapidly colonize and exploit temporary habitats. These mites are r-strategists with high rates of reproduction and rapid onto- genetic development. Some associations are not Spines strictly phoretic, i.e., the mites derive nourish- Anus 100 µm ment from their hosts. In these mites, the larva is the dispersal form and the other life stages are free-living and usually predatory. The host is used by ticks and many other par- Mites (Acari), Figure 70 Dorsal view of a asitic mites for dispersal. This is most effective female scab mite Sarcoptes scabei (Acaridida, when the parasitic mite is not host specific, or Sarcoptoidea). Legs III and IV are not visible when the host has a large home range, as is the from the dorsum (from Kettle DS (1995) Medical case of some birds. and veterinary entomology, 2nd edn, used with permission of CAB International). External Anatomy

Dispersion of Mites The body of mites, like all arthropods, can be divided into regions that are based on segments Although mites lack the wings of insects, they have and their appendages. However, mites have little other means of dispersal. Crawling short distances external evidence of segmentation, which makes is one method. Wind borne dispersal is a common naming body regions (Fig. 71) difficult. Acarolo- and effective method. In the Tetranychoidea gists have relied on developmental evidence of (Actenida: Prostigmata) two methods of becom- segmentation during embriogenesis. The most ing airborne occur. Some species use silk threads obvious body divisions is the anterior gnathosoma, produced from glands in a form of ballooning. and the rest of the body, the posterior idiosoma. Other species use a dispersal posture to launch Another division is the prosoma which constitutes themselves into the air. that part of the body that bears the appendages Phoresy, the process where a mite actively and includes the gnathosoma and the podosoma. seeks out and becomes attached to the outer sur- Divisions of the idiosoma are discussed below. face of another animal is an important method of The gnathosoma bears the mouthparts. It is dispersion. Phoretic mites do not feed and onto- not comparable to the head of insects, except that genetic development ceases. Phoresy is the most both contain the mouthparts. The gnathosoma common method of dispersal from one tempo- (Fig. 72) lacks eyes, antenna, mandibles and does rary sources of food to another. Phoresy occurs not contain ganglia of the nervous system. The in the Gamasida, the Actinedida, the Oribatida head of insects contains all of these. 2426 M Mites (Acari) Chelicerae Palp

Gnathosoma

Propodosoma Podosoma Idiosoma

Hysterosoma

Opisthosoma

Mites (Acari), Figure 71 Divisions of the body of a mite (from Kettle DS (1995) Medical and veterinary entomology, 2nd edn, used with permission of CAB International).

TA Gnathosoma TI GE TG sl The gnathosoma is separated from the idiosoma AP FE PS by a circumcapitular furrow or suture. In many ss TR taxa the gnathosoma fits into an anterior cavity TR formed by the idiosoma, the camerostome. Because it is composed of several compli- CO cated structures in a small space, the gnathosoma is best understood by a diagram of its main components, simplified and drawn in such a way as to Mites (Acari), Figure 72 Lateral view of the emphasize their relationship to one another. The gnathosoma of a gamasid mite. AP, apotele gnathosoma is made up of two components, the (tined claw); CO, corniculus; FE, femur; GE, genu; cheliceral frame (Fig. 73) and the infracapitulum TA, tarsus; TI, tibia; TG, tegulum; TR, trochanter (=subcapitulum or hypostome). In ticks, the (of chelicera and palp); PS, principal segment of hypostome becomes the toothed device that is chelicera; sl, supracheliceral limbus (gnathotectal used to anchor the parasite to its host. The cheli- process); ss, salivary stylus (from Alberti G, Coons LB ceral frame, which is part of the integument, (1999) The Acari-Mites, used with permission of serves to anchor the cheliceral sheath. The infra- John Wiley and Sons, Inc). capitulum is located ventral to the chelicerae and bears the palps or pedipalps, labrum and lateral The gnathosoma is specialized for sensory lips. Each palp inserts into the cheliceral frame perception and food gathering. The adaptations of via the cheliceral sheath which is the coxal region the gnathosoma to the many types of food used by of the chelicerae. The mouth or oral cavity is a mites is comparable to the great diversity of mouth- space designed to move food into the pharynx parts in insects and has helped make the extensive and esophagus. The muscular pharynx acts to colonization of diverse habitats by mites possible. “suck up” the food. Three structures commonly Mites (Acari) M 2427 Capitular trochanter. In this configuration, the chelicerae cervical Apodeme Cheliceral frame take the form of a pincer. The chelicerae of the Cheliceral sheath varroa mite Varroa destructor have a vestigial fixed digit and a movable digit with two strong Cervix Coxal region teeth that are used to tear the cuticle of the bee of pedipalp to allow the mite to feed on its hemolymph. Chelicerae tend to be elongated in obligate blood feeders of the Dermanyssina and form a Js channel through which blood can pass into the Labrum preoral channel. Chelicerae may be modified for functions other than food gathering. In some Js� Ji gamasida, male chelicerae are modified as gono- pods that transfer packages of sperm, the spermatophore, to females. Malapophysis The palps which were originally sensory Lateral lips appendages used to probe surroundings for the presence of food, remain so in many species. How- Mites (Acari), Figure 73 A diagram that shows ever, in several groups the palps have undergone the relationships of the main components of a many modifications: they may be leg-like, as in typical gnathosoma. For clarity, only the base of many gamasids, grasping as in the Cheyletidae the pedipalps and chelicerae are shown. Ji, inferior and Hydrachnidia, involved in spinning silk in commissure; Js, Js, superior commissures (from some species of spider mites, reduced to one or Alberti G, Coons LB (1999) The Acari-Mites, used two segments in some species of Tarsonemina with permission of John Wiley and Sons, Inc). and Tetranychoidea. Palps may have as many as five segments which are named from proximal to distal: trochanter, femur, genu, tibia, and delineate the mouth: dorsally the labrum, and trochanter. laterally a pair of lateral lips. A fourth structure, The gnathosoma has undergone changes for the labium, occurs ventral to the lateral lips, but it adaptation to the different habitats and type of is most often reduced or highly modified. The food used by different mites. One of the most paired malaphophysis lie lateral to the labrum unusual involves the filter feeding slime mites of and lateral lips. In some gamasids the mala- the Histiostomatoidae (Acaridida, Histiostoma- phophysis have been modified into a corniculus. toidea) who inhabit wet, rotting organic mate- They may be further modified in other mites. rial. These mites have modified palps and The infracapitulum encloses the mouth and the chelicerae adapted for filter-feeding. The palps pharynx. have a freely movable flattened distal segment, Chelicerae are movable and function to rip, used to sweep the fluid food suspension towards squeeze, cut, or pierce the wide variety of food the anterior part of the infracapitulum. From utilized by present day mites. Chelicerae often here particles are raked back into the preoral consist of a basal article or trochanter, a princi- cavity by means of the specialized non-chelate ple segment or body which ends with a fixed chelicerae. Other unusual adaptations include digit that is heavily sclerotized or hardened, the gnathosoma (=capitulum) of ticks and the and a movable digit located ventrad of the fixed gnathosoma of Psoroptes equi. The former is dis- digit and hinged to the principle segment. The cussed in the entry on “Ticks,” the latter in the heavy muscles of the chelicerae attach to the section on “skin parasites.” 2428 M Mites (Acari) Idiosoma greatly increase their body size during feeding (see the entry on “Ticks”). Some species of oribatids The body proper or idiosoma varies considerably can retract their gnathosoma and legs like a box in shape and is closely adapted to the type of habi- into an operculum-like device of the cuticle like a tat occupied by the mite. Common body shapes box. Others have cuticular plates termed ptero- include a dorso-ventrally flattened body found in morphs that extend over the lateral body parts and unfed hard ticks, a vermiform or fusiform shape, a protect them. Some Euroribata carry the dorsal sac-like body found in gravid Pyemotes, and a box cuticle from a previous molt around as a scalp shape. Other shapes such as a laterally flattened which may help conceal the mite from predators. body can occur. Sexual dimorphism occurs in Other oribatids stick debris on to their body some mites. surface which may have the same function. The idiosoma is further divided into the podosoma which contains the four pair of legs, and the opisthosoma which is the rest of the body poste- Legs rior to the legs. Other divisions of the idiosoma include the propodosoma which contains the first Legs are numbered I through IV from anterior pair of legs, and the hysterosoma which contains to posterior. Each leg is divided into segments or the last pair of legs and the rest of the body. podomeres which are from proximal to distal: Specialized structures are found on the surface coxa, trochanter, femur, genu, tibia, and tarsus. of the idiosoma. The tritosternum is a medioven- The distal end of the tarsus forms (Figs. 74 tral structure that extends from the groove separat- and 75) the terminal part of the leg, the ambu- ing the gnathosoma from the idiosoma in all orders lacarum, which bears the claws and a pulvillus of Actinotrichida except the Ixodida. In some gamasids it functions to direct prey fluids to the mouth region. A pair of podocephalic channels or canals, which may be open or closed, occur in all TI BT GE TT Actinotrichida. They usually run from the bases of TF AM the first pair of legs to the gnathosoma and carry CX TR BF the products of the coxal glands and other glands. In Opilioararida, these channels run from an area TI between the first pair of legs to the gnathosoma. GE TA No other order of Anactinotrichida has these. Ven- AM tral and dorsal sclerotized (hardened) cuticular TF shields and plates occur on the idiosoma of mites. BF The shape and location of these are important tax- EP TR onomic features. A genital opening and an anus are found on the ventral idiosoma. Some mites have a Mites (Acari), Figure 74 Legs of a gamasid (top) penis (aedeagus). The position of these three struc- and an actinedid (bottom) mite showing the tures varies with the species of mite. podomers. AM, ambulacrum; BF, basifemur The cuticle of many blood sucking ectopara- (femur I); BT, basitarsus; CX, coxa; EP, epimeron sitic mites, such as Echinolaelaps echidninus and (coxisternum); GE, genu: TA, tarsus; TF, telofemur Dermanyssus gallinae (Gamasida, Dermanyssoidea, (femur II); TI, tibia; TR, trochanter; TT, telotarsus Dermanyssidae) expands during feeding to accom- (redrawn from Alberti G, Coons LB (1999) The modate large quantities of blood. The most Acari-Mites, used with permission of John Wiley dramatic of these occur in female ixodid ticks that and Sons, Inc.). Mites (Acari) M 2429

pc ex

Mites (Acari), Figure 75 A velvet mite, dz prc Trombidium meyeri (Actinedida, Trombidoidea, a en Trombidiidae) that uses its first pair of legs as feelers (from Alberti G, Coons LB (1999) The Ep Acari-Mites, used with permission of John Wiley b and Sons, Inc). GLC TR Mites (Acari), Figure 76 Diagram of sclerotized between the claws which functions as a type of (a) and unsclerotized cuticle (b) of the tick Boophilus cushion. Secondary divisions, especially with the microplus (Ixodida, Ixodidae). dz, deposition zone; trochanter and femur can occur. A free movable ec, epicuticle; en, endocuticle; EP, epidermis; ex, coxa exists in the Anactinotrichida but not in exocuticle; GLC, dermal gland cell; pc, pore canal; the Actinotrichida. Many acarologists doubt the pre, procuticle; TR, trichogen cell (simplified) (from presence of a true coxa in the Actinotrichida and Coons LB, Alberti G (1999) The Acari-Ticks, used therefore use the term epimeron for this leg with permission of John Wiley and Sons, Inc). component. Epimeres are often fused with other components of the ventral idiosoma and are sometimes referred to as a coxisternum. Joints have specialized leg spurs that grasp the female between the body and the legs, between the during sperm transfer. In some Acaridida legs podomeres, and between the tarsus and the apo- are modified for holding females during copula- tele allow movement of the legs. Muscles and tion. Mites capable of jumping occur in all tendons run between joints. Muscles, hydrostatic orders of Actinotrichida. Jumping is associated pressure from hemolymph, and bending stresses with modification of the fourth pair of legs. are used to produce movement of leg segments. Many water mites (Hydrachnidia) are fast and Legs of mites are modified for different elegant swimmers. Their legs have movable, flat- types of locomotion, and for special uses such as tened seta that passively erect during the power habitat adaptation, nutritional and sensory stroke to increase the thrust and collapse during functions, and sexual behavior. In general, slow the recovery movement of the leg to reduce water moving mites have stout heavily sclerotized legs, resistance. while faster moving mites tend to have long, slender legs. Many Acari have the first legs modified as elaborate sense organs or feelers that are Integument used to touch the soil with their distal parts or are waved in the air in a similar fashion as insect The integument is made up of a non-cellular antenna. Often these legs are not used for loco- cuticle and an underlying layer of cells, the motion. In some soil mites the second pair of epidermis. The epidermis secretes the cuticle legs is much stronger and bears modified setae (Fig. 76). Interposed between the epidermal adapted for digging. Often endoparasitic mites cells are trichogen cells that extend into seta and have reduced legs. In some Gamasida, males dermal gland cells whose product is released 2430 M Mites (Acari) into canals that lead to the surface. The cuticle is Sclerotization is a process that imparts greater shed during molts which allow the mite to grow strength by hardening the cuticle. Heavily sclero- in size and develop adult characteristics. The tized armor plates protect against the attacks of cuticle is thrown into projections termed setae. predators (Fig. 77). Unsclerotized (Fig. 76) cuticle Shapes of setae commonly include but are not is more flexible. The cuticle has two layers, a thicker limited to simple hair like projections, bipecti- internal procuticle and a thinner external epicuti- nate, spine-like, fan-like. Setae may be scarce, or cle. Chitin is found in the procuticle. In some cases, they may completely cover the body of the mite. the procuticle is divided into an inner epicuticle Some setae have the ability to erect. Setae have and an outer exocuticle. The epicuticle contains different functions. Some are sensory and are several sublayers depending on the mite species. further discussed in the section on “Nervous These are named from the most external: the and sensory organs.” The number, position and cement, wax, cuticulin, and dense homogeneous shape of setae are important taxonomic charac- layers. External to the cuticle, two additional layers teristics. Cuticular scales occur in some mites. may be present that are collectively termed the The cuticle has many functions. It acts as a secretion layer or cerotegument. The secretion barrier to pathogens such as bacteria and patho- layer may take the form of distinct granules or genic protozoa and the eggs of insect parasites. It other structures which contribute to the appear- provides protection from mechanical injuries of ance of the surface (Fig. 77). Pore canals pass predators. through the procuticle to join structures known as The cuticle helps to prevent desiccation epicuticular canals, wax filaments or wax canals through loss of water. Hydrophobic substances in that extend through the epicuticle to the surface. the cuticle prevent excess wetting. The cuticle is Pore canals have an unknown function, they involved in gaseous exchange with the atmo- may allow the exchange of material such as gas, sphere when the tracheal system is lacking or not water and lipids between external and internal well-developed as in all larval mites and in compartments. acaridid mites. Cuticular spines and ridges help retain a film of air around the body during flooding. In aquatic species these cuticular modifications are further developed for use in plastron respiration. Regularly spaced surface microstruc- tures or granulations occur on some mites in polar regions. A layer of air trapped by the granulations may facilitate survival by providing a mechanism of cuticular respiration in water- logged polar soils. This layer of air may also prevent freezing by insulating the mite from direct contact with the ice. The cuticle is a site for muscle attachment. Glands and receptor organs open onto the surface of the cuticle. A cuticular lining occurs in the fore and hind Mites (Acari), Figure 77 Tritonymph of Conoppia gut of the digestive system, the tracheae, ducts of palmicincta (Oribatida, Cepheoidea, Cepheidae) many glands, and part of the reproductive system. with fan-shaped setae that completely cover the The general structure of the acarine cuticle is body (redrawn from Alberti G, Coons LB (1999) The similar to the cuticle of other arthropods. The Acari-Mites, used with permission of John Wiley and cuticle is either sclerotized or unsclerotized. Sons, Inc). Mites (Acari) M 2431 The cuticle varies considerably in thickness Physiology of Mites depending on the species of mite and the region of the body. It is a dynamic structure; many of its Glands parts can be modified, or rebuilt or replaced during molting, sclerotization, wound repair or after Mites have endocrine and exocrine glands. abrasion of the secretory layers.The impermeable Endocrine glands or endocrine organs produce nature of the cuticle is important in preventing hormones and empty internally while exocrine desiccation. Mineralization of the procuticle in glands produce a variety of substances and empty some Oribatida may further harden the cuticle. onto the surfaces of the mite. Molting includes apolysis, the separation of the Unlike insects where endocrine organs have old cuticle from the epidermis and ecdysis, the cast- been identified and well studied at the cell and ing off of the remnants of the old cuticle. In between molecular level, acarine endocrine organs are clas- apolysis and ecdysis, the old separated cuticle, except sified only by their structure, and thus they are for (Fig. 78) the epicuticle and secretion layers, is spoken of as putative endocrine glands. These digested and a new cuticle is deposited. Following are located mostly around the central nervous ecdysis, the new cuticle may be sclerotized or miner- system and consist of a retrocerebral organ com- alized. The pharate form is the next instar still within plex, the lateral organs and paraganglionic plates. the old exuviae. Molting is similar in most mite spe- Exocrine glands are described based on their cies. In general, the old cuticle splits along different morphological location. Dermal glands are com- lines depending on the species of mite, and the new mon throughout the Acari. They are small glands instar leaves the exuvia. Little is known about the located within or just below the epidermis. A duct hormones involved in the molting of mites. leads to the cuticular surface. These glands have a In some mites there is little or no period of variety of functions that include secretion of an inactivity accompanying apolysis. In others, the allomone, a sex attractant pheromone in ticks and instar becomes inactive just before and during some other mites, and the secretion of a glue in apolysis. In general there are no molts after the some males of the family Arrenuridae (Hydrach- adult phase except in Prostigmata. nidia: Arrenuroidea) that is used to attach the female during mating. Arrenuroids are freshwater mites. Other glands are the prosomal glands, lateral glands and anal glands. Two important types of prosomal glands are salivary glands and silk glands. Salivary glands produce digestive enzymes used by the mite to liquefy or predigest their prey and other food prior to swallowing it. In ticks, salivary glands are specialized for osmoregulation. Silk produced by silk glands is used for a variety of functions.

Mites (Acari), Figure 78 Molting in Uroobovella Muscles marginata (Gamasida, Uropodoidea, Urodinychidae). The old cuticle has split around All muscles in mites are striated. There are two the anterodorsal border, and the new instar leaves types of striated muscles, somatic and visceral. the exuvia (from Alberti G, Coons LB (1999) The Somatic muscles are connected to the integument Acari-Mites, used with permission of John Wiley via specialized attachment complexes. Somatic and Sons, Inc). muscles are divided into three groups: those 2432 M Mites (Acari) muscles that move the legs, those that move the large foreign objects, such as parasite eggs, by gnathosoma and those that move the body proper. hemocytes. Encapsulation is a defense designed to Visceral muscles are found around hollow organs isolate foreign objects. Mites have immune reac- such as the digestive system, Malpighian tubules, tions similar to those of insects. and parts of the reproductive organs. They are Nephrocytes or pericardocytes are round sin- used to move their contents. In many mites a spe- gle cells that are associated with various organs, cialized structure, the endosternite, lies within the especially reproductive organs. They function to podosoma. It is analogous to a “floating tendon” sequester certain toxic compounds from the and serves as a central suspensory attachment for hemolymph. certain somatic muscles.

Respiratory System Fat Body Mites have three different respiratory mechanisms: The fat body is a diffuse organ that consists of gas diffusion through the integument, gas trans- strings of cells, the trophocytes, that are often portation through a tracheal system, and gas closely associated with trachea, internal organs exchange through specialized porose areas on the and nephrocytes. While a fat body occurs in both integument. All prelarvae and most larvae respire superorders, not all mites have a fat body and some through their integument. In adults, respiration develop a fat body only during certain parts of through the integument is limited to soft bodied their life cycle. In mated fed female ticks, the fat forms such as the Acaridida. Respiratory mecha- body under the influence of the hormone ecdy- nisms in mites must also be adapted to avoid des- sone, undergoes a complete ultrastructural reor- iccation as well as exchange gasses in these small ganization and produces the female protein animals with large surface areas. vitellogenin, which is secreted into the hemolymph A tracheal system is made up of internal tubes and taken up by developing eggs to become the that become smaller as they lead to the various yolk protein vitellin. Yolk is used as food for the organs. Spiral coils inside trachea termed taenadia developing embryo. impart rigidity that keeps them open. Trachea lead to the outside through openings, the stigmata, that are sometimes associated with a peritreme, a canal Circulatory System or gutter-like extension from the spiracles. In some species the peritreme is partially closed. A peri- Mites have several types of hemocytes that treme usually extends anteriorly or less commonly circulate in the hemolymph. Some mites have a posteriorly from the stigma. It is thought that pulsating organ or heart, other mites do not. The peritremes evolved to help keep the spiracles free heart has a specialized striated muscle with an from blockage. Peritremes are found only in the ultrastructure similar to the striated muscle of Holothyrida, Gamasida and Prostigmata. The per- insect hearts. Hemolymph enters the heart through itreme and stigma are sometimes surrounded by a openings, the ostia, and then is pumped out the prominent sclerotized shield like area of the cuti- anterior end. With or without a heart, circulation cle, the peritrematal shield. The position of the is aided by body movements and muscular stigmata, the presence and shape of the peritreme contraction. and associated shield are used as taxonomic The hemolymph of ticks undergoes coagula- characteristics. tion when exposed to air. Mites can recognize self In mites that live in water, plastron respiration from nonself and can initiate encapsulation of occurs as trapped air in specialized areas of the Mites (Acari) M 2433 body. Often a plastron is associated with modifica- Several generalized anatomical types of diges- tions in a peritreme. Trapped air is also believed to tive systems occur in mites. A parasitiform type act as a flotation bubble. Porose areas of the integ- occurs in the Oplioacarida, Holothyrida, Ixodida, ument that are involved in gas exchange occur in and Gamasida. It is characterized by an esophagus, some species of Oribatida. They are believed to a small ventriculus with relatively large paired have originated independently from the respira- caeca, a short postventricular midgut leading to a tory systems of related mites. short hindgut that in turn leads to an anus. One pair of Malpighian tubules is present except in the Holythrida which have two pair. A trombidiform Digestive System type of digestive system occurs in most of the Actinedida. It consists of an esophagus that leads Mites utilize a wide variety of food that ranges to a midgut that is divided into a small ventriculus from solids such as pollen, fungi and tissues of with large paired caeca. The midgut ends blindly, prey to liquids such as vertebrate blood and plant no postventricular midgut or anus exists. The fluids. The range of food habits in free living mites midgut is closely associated with a dorsomedian include predaceous (feeding on animals), phytopha- excretory organ that opens to the outside via a gous (plant feeding), mycetophagous (feeding on uropore. A sarcoptiform type of digestive system fungi), saprophagous (feeding on dead organic occurs in the Oribatida and Acaridida. It consists matter), microphagous (feeding on small food of an esophagus that leads to a midgut that is pieces), and coprophagous (dung feeding) forms. divided into a ventriculus with small caeca and a The digestive system has three major divi- postventricular midgut consisting of a colon and sions: a foregut lined with cuticle that extends postcolon that in turn lead to a hindgut and anus. from the mouth, a midgut that lacks a cuticle, and Malpighian tubules, described in the section on a hindgut that also has a cuticular lining. The the “Excretory system,” are present in some taxa foregut consists of the muscular pharynx and but reduced or absent in others. esophagus that passes through the synganglion to enter the midgut. The foregut acts mostly as a con- duit of food into the midgut where digestion and Excretory System and Osmoregulation absorption of food takes place. Mites partially digest their food before it is taken up into the Excretory organs are involved in the elimination digestive system using secretions from prosomal of the end products of nitrogenous metabolism, glands, especially salivary glands. The meal is which in the Acari is guanine and rarely uric acid. taken up in cells that line the midgut, sorted into Excretory organs include Malpighian tubules and the lysosomal system of the cell and digested the dorsomedian excretory organ. Osmoregula- within the lysosomes in a process termed het- tory organs regulate water and or ions, and include erophagy. The digested material is then released coxal glands or nephridia, the salivary glands of into the hemolymph. A peritrophic membrane ixodid ticks, genital papillae, ClaparÈde organs, occurs in some mites. The digestive system, espe- axillary organs and pregenital capsules. cially the midgut, is modified depending on the Malpighian tubules originate in the posterior type of food eaten. Substantial modifications occur region of the digestive system and end blindly in the blood feeding ticks which take in a large within the anterior hemocoel. They are present in meal of blood and in the plant feeding mites which the Holothyrida, Ixodida, Gamasida and some must deal with plant fluids. Microorganisms, Acaridida, but are absent in the Actinedida and which are probably symbiotic, occur in the diges- Oribatida. The ultrastructure of cells in the Mal- tive systems of mites. pighian tubules are similar to those of Insecta. 2434 M Mites (Acari) Wastes from the Malpighian tubules pass into the band of sclerotized porous cuticle. Cells associ- digestive system and are eliminated with the feces. ated with these organs have an ultrastructure typi- The dorsomedian excretory organ is found in cal of transport cells. Axillary organs are probably actinedids and consists of the postventricular homologous to ClaparÈde organs. Pregenital cap- midgut and the hindgut which together are modi- sules occur only in the Opilioacarida where they fied as an excretory organ. The organ functions in are found anterior to the genital openings in both nitrogenous metabolism and osmoregulation. It is sexes. Their function is unknown. Each capsule most developed in mites that are predators on has an external cover and an evertable sac. plants such as the tetranychids. Some mites such as the human follicle mite store metabolic wastes in cells rather than eliminate them. Nervous and Sensory System Coxal glands are derived from the nephridia of annelid arthropod ancestors and are found in The ventral chain of ganglia, which is common in both superorders. Coxal glands consist of a thin arthropods, is condensed in mites into a mass of walled sacculus that faces the hemolymph and a nervous tissue termed the synganglion. This is the convoluted tubule that leads to an opening to the central nervous system from which sensory and outside. The sacclus filters the hemolymph, and motor nerves originate and extend to parts of the the convoluted tubule is thought to reabsorb sub- body and organs. A peripheral nervous system is stances including ions from its lumen. Salivary present in some species. glands are the principal osmoregulatory organs of The sensory system includes setiform sensilla ixodid ticks during feeding. In addition, they play sensory hairs and sensory setae which are often an important role in preventing dehydration by grouped as setiform sensilla, nonsetal sensilla, secreting a compound that takes up water from and photoreceptors. Different setiform sensilla the air onto the mouthparts. The compound is function as chemoreceptors, temperature and swallowed or reabsorbed through a specialized humidity receptors, and mechanoreceptors. Some cuticular region of the tick. setiform sensilla have multiple functions, for Genital papillae are commonly found in Acti- example, as both a chemoreceptor and a mechano- notrichida where they are considered to be a char- receptor. The ultrastructure of mite sensory recep- acteristic feature of this taxon. Genital papillae tors is similar to those of insects. A great number have different shapes but generally consist of an of setae are found on most mites, only some of eversible sac-like structure located anterior to the which are known to have a sensory function. The genital opening. This sac-like structure has an position and pattern of setae is an important taxo- ultrastructure typical of transporting cells. The nomic characteristic. papillae are protected by two progenital lips. The Sensory setae, like those of insects are classi- number of papillae varies or they may be com- fied by their external shape as follows. A peg or pletely lacking. In some species of water mites, cone shaped seta is a sensillum basiconicum, a multiple papillae may be found on the external bristle or spine shaped seta is a sensillum chaeti- surface. Prelarvae and larvae, which lack a pro- cum, and a seta that has its external portion freely gential chamber, have Claparède organs located moving in the form of a hair articulated with a between the bases of legs I and II which function base is a sensillum trichodeum. as osmoregulatory organs. Axillary organs are Nonsetal sensilla function as mechanorecep- found on some acaridid mites that inhabit tors that can sense a variety of stimuli such as semiaquatic or aquatic environments. These gravity, substrate vibrations, sounds and strains organs are found between the bases of the first within the exoskeleton caused by movements of and second pairs of legs and have an elevated the mite. Nonsetal sensilla are classified as slit Mites (Acari) M 2435 sense organs, cupules, and lyriform fissures. The the Phytoseiidae (Gamasida, Ascoidea). Either sex latter are unlike those of spiders. can develop from unfertilized eggs in deutero- Photoreceptors in mites are divided into three toky. Deuterotoky is not considered to be an inde- types: eyes, secondary light receptors and photo- pendent type of reproduction, but is part of a sensitive areas. The eyes of mites are simple ocelli cyclical type of parthenogenesis. Thelytoky pro- that lack facets found in the compound eyes of duces females by parthenogenesis. Males are insects. Typically they have a lens, which is the either rare or most commonly absent. It is most only cuticular part, and an underlying photore- common in the Oribatida. ceptor apparatus. Eyes are located in various places Mites have both indirect and direct sperm on the prosoma depending on the species of mite. transfer. In indirect sperm transfer, the male uses Not all mites have eyes. a package of sperm, a spermatophore, that it places on the substrate, and the female transfers the spermatophore to its reproductive opening. Reproductive System In direct sperm transfer, sperm is directly transferred to the genital opening of the female in a A major reason for the success of mites is their spermatophore, or transferred with a penis dur- diversity of reproductive strategies. Few common ing copulation. Direct sperm transfer using a themes occur, but all mites are dioecious, i.e., with spermatophore can occur via the primary genital separate sexes, and all have internal fertilization. opening of the female in a process termed Three modes of reproduction exist in the Acari: tocospermy or via the insemination pore, a sec- diplodiploidy, haplodiploidy and thelytoky. ondarily developed genital opening in a process Mites with diplodiploidy are biparental, par- termed porospermy. Insemination pores lead to a thenogenesis is absent. Sexual reproduction is complex specialized organ, the sperm access used to produce offspring. Somatic cells of both system in the Dermanyssina (Gamasida). Copu- sexes are diploid. Diplodiploidy is thought to be lation occurs in some mites of the Actinedida the ancestral form of reproduction in mites, and it and Acaridida. is the most common mode of reproduction of the Acari. It is found in the Ixodida, the Gamasida, the Actinedida, the Acaridida and the Oribatida. Economic Importance Diplodiploidy is the dominant form of reproduction in the Ixodida and Oribatida. Skin Parasites Parthenogenesis occurs in haplodiploidy and thelytoky. Haplodiploidy produces diploid females Skin parasites of vertebrates are found in all Orders and haploid males. Two kinds of haplodiploidy, of mites except Opiloacarida and Holothyrida. We arrhenotoky or parahaploidy, occur. Arrhenotoky shall consider only those known to cause pathol- produces diploid females from fertilized eggs ogy in humans and domestic animals. The canary while haploid males are produced parthenoge- lung mite, Sternostoma tracheacolum (Gamasida: netically. This results in biparental females and Dermanyssoidea: Rhinonyssidae), occurs in the uniparental males. Often arrhenotoky produces a respiratory tract of canaries and can cause illness female-biased sex ratio. Arrhenotoky is not com- and even death. This mite is thought to be larvipa- mon in mites, but is found in some Acaridida. rous. Treatment includes pesticides administered Fertilization occurs in parahaploidy, but the pater- in diets or as aerosols. Pneumonyssoides caninum nal set of chromosomes is lost in the diploid male (Gamasida: Dermanyssoidea: Halarachnidae) is embryo and thus only the maternal set of chro- usually a benign inhabitant of the sinuses and nasal mosomes are passed on. Parahaploidy occurs in passages of dogs, but they can cause pathological 2436 M Mites (Acari) conditions such as sinusitis. Pneumonyssus group of rickettsiae. Rickettsialpox is found in simicoloa (Gamasida: Dermanyssoidea: Halarach- many urban areas of the United States, Russia, and nidae) is found in the lungs of monkeys and Korea. The disease is mild with no recorded fatali- baboons. It is tolerated in the natural state, but in ties, and has a benign clinical course. Rickettsial- captivity can cause a disease with a mortality up pox is characterized by a vesicular rash, a local to 70%. The tropical rat mite, Ornithonyssus eschar or tache noire, and a local cutaneous lesion. (=Liponyssus) bacoti (Gamasida: Dermanyssoidea: The eschar, an ulcer covered with a black crust, is a Macronyssidae) is found in tropical and temperate local reaction that occurs at the bite site. The anti- regions worldwide. It is normally a parasite of rats biotics tetracycline and chloramphenicol are used but can bite humans producing a sharp pain and as treatments. Prevention includes controlling severe itching. Sensitive people can develop a rodent and mite populations. dermitis from the bite. Chiggers are larvae of trombiculids (Actine- Several species of skin parasites attack poul- dida: Prostigmata: Trombidioidea: Trombiculi- try. The tropical fowl mite, Ornithonyssus bursa dae) that parasitize every major group of terrestrial (Gamasida, Dermanyssoidea, Macronyssidae), vertebrates. In humans, chiggers transmit the occurs in tropical and subtropical areas world- serious disease chigger-borne typhus. The adults wide. It is a common parasite of the English spar- are fungivorous mites that feed within fungal cells row, Passer domesticus and an ectoparasite of using stylettiform chelicerae. The small chelicerae poultry. Heavily infested poultry can become of chiggers are used for penetration of the hosts listless. Workers associated with poultry are epidermis and serve as anchors during the attach- frequently bitten resulting in a slight irritation. ment of the parasite. A saliva produced by the The northern fowl mite, Ornithonyssus sylviarum mite dissolves the integumental layers producing (Gamasida, Dermanyssoidea, Macronyssidae), a feeding channel, the stylostome, through which occurs in the north temperate regions, and in the parasitic larvae takes up predigested material. New Zealand and Australia. Heavy infestations Several species of larval trombiculids trans- in poultry can reduce egg production. This mite mit chigger-borne typhus also known as scrub bites poultry workers and can cause extensive typhus or tsutsugamushi disease. The causative itching. The chicken mite (red chicken mite or agent of this disease is Orientia tsutugamushi, a roost mite), Dermanyssus gallinae (Gamasida, member of the typhus group of rickettsiae. Chigger- Dermanyssoidea, Dermanyssidae), is worldwide borne typhus is a zoonosis, humans are only acci- in distribution. It parasitizes domestic poultry, dental hosts of the pathogen. The disease has four pigeons, starlings and sparrows. The mite attacks essential components: Orientia tsutugamushi, chig- at night; during the day it hides in crevices, gers, rats, and secondary or scrub forms of vegetation. under floors and in debris where its eggs are laid. Chigger-borne typhus occurs in Australia, India, Damage to poultry includes less egg production, Korea, and Japan. Orientia tsutugamushi exists as and weight loss which makes poultry less three major antigenic types which has prevented marketable. the development of an effective chigger-borne The house mouse mite Liponyssoides (=Allo- typhus vaccine. Infection with one strain pro- dermanyssus), sanguineus (Gamasida, Dermanys- duces long term immunity only to that strain. soidea, Dermanyssidae) transmits the pathogen of Other strains can cause another cases of chigger- rickettsialpox to humans. Both nymphs and adults borne typhus in the same individual. All strains feed on the blood of a variety of rodents. The mite produce a similar disease which manifests itself as is a nest dweller and is usually found on its host chills, fever, and headache after an incubation only when feeding. Rickettsialpox is caused by period of one to three weeks. An eschar followed Rickettsia akari, a member of the spotted fever by a skin rash occurs in less than half of the cases. Mites (Acari) M 2437 Fatal outcomes of chigger-borne typhus ranges mites. Psoroptic mange, caused by species of the from 0 to 50%. The same antibiotics used for rick- genus Psoroptes, is severe and can sometimes be ettsialpox are used to treat chigger-borne typhus. fatal in cattle and sheep. The family Psoroptidae is All species of the genus Demodex (Actine- worldwide in distribution and is found on many dida, Cheyletoidea, Demodicidae) are parasites mammalian species. Psoroptic mange is caused by a on mammals and cause demodectic mange or single cosmopolitan ectoparasitic species, Psoroptes demodecosis which can be serious or of little equi (Acaridida: Sarcoptoidea: Psoroptidae). This pathology depending on the host species which mite has many varieties that are named for their include but are not limited to humans, dogs, cats, hosts, thus P. equi var. ovis on sheep, P. equi var. bovis cattle, hogs, deer, hamsters and various rodents. on cattle, etc. P. equi is a very small mite about 0.5 Transmission is by bodily contact. Two species mm in length that spends its entire life on its host. parasitize humans. These mites are minute, Mites are spread rapidly by the close contact of ani- 0.1–0.4 mm long, with an elongated abdomen mals. Psoroptes equi is most often found at or near and eight stubby legs. The follicle mite, Demodex the base of hairs. Mites pierce the host’s skin to feed folliculorum, lives head down in hair follicles. It is on lymph and tissue fluids which results in an the most widespread parasite of man with a prev- inflammatory response that causes a debilitating alence that approaches 100%. All life stages includ- dermatitis and mangy or puritic scab formation. ing eggs may be present in a single follicle. These The mouthparts of Psoroptes equi are adapted to mites are most common in facial areas, especially feed on liquefied and semi-liquefied material from oily regions around the eyelids and nose. Demo- abrasions caused by the shearing actions of their dex brevis is found in sebaceous glands. Neither mouthparts. The mouthparts form a suctorial cup mite causes much pathology. Demodex canis that serves to direct food into the preoral cavity. causes a more serious pathology in dogs. The Infected animals often have lesions that ooze, and demodecosis is either localized or generalized. they suffer a great deal of irritation. This irritation The latter is a severe form and must be treated or often causes the infected animal to scratch against a fatal septicemia can develop. About 10% of cases objects to relieve itching which results in further are of the generalized form. damage to fur and skin. A complete life cycle of Pso- Many species of the family Pyemotidae roptes equi from egg to egg can occur in as little time (Actinedida: Tarsonemina: Pyemotoidea) are as 11 days in some hosts, or up to three weeks in stored product pests and secondarily cause prob- others. In sheep and cattle, psoroptic mange is most lems with workers. Pyemotes tritici which kills its common in autumn and winter. In the summer the prey with a toxin can cause skin lesions and other disease enters a latent phase due mostly to shearing problems in humans. The hay itch mite, Pyemotes or shedding of hair, host nutrition and grooming. ventricosus, attacks people who come in contact Psoroptic mange annually causes millions of dollars with infected grain or hay. in losses in North America. Mange and scabies are terms often used Chorioptic mange, caused by species of the interchangeably to describe diseases caused by genus Chorioptes, is a less serious disease than species of mites from the families Psoroptidae psoroptic mange. Chorioptic mange is caused by and Scarcoptidae of the superfamily Sarcoptoidea two species of mites, Chorioptes bovis that infests (Acaridida). Usually scabies or the scab describes horses, sheep goats, cattle and llamas, and Chori- a collective disease, while mange is used to dis- optes texanus that infests goats and cattle. These tinguish which mites cause the disease. mites feed on debris on the skin surface and do not Three genera of Psoroptidae, Psoroptes, burrow. Their mouthparts are modified to scrape Choriptes, and Otodectes, are important skin the surface of the hosts skin. The mites infest new parasites of mammals. These are non-burrowing hosts by contact with uninfected animals. 2438 M Mites (Acari) Parasitic otitis is caused by Otodectes cynotis and turkeys where populations can reach in the (Acaridida: Sarcoptoidea: Psoroptidae). These millions. The condition presents itself as nodules mites infest the ears of a wide variety of carnivores. that become calcified on the death of the mite thus Convulsions can occur in heavily infested dogs reducing the value of the meat. This mite occurs in and cats. North and South America, Australia, and Europe. Sarcoptic mange occurs in a variety of mam- The Listrophoridae or fur mites are parasites malian hosts including man. It is caused by the that have evolved specialized structures to attach scab mite Sarcoptes scabiei (Acaridida: Sarcop- to the skin and hair of their hosts. The gnathosoma toidea: Sarcoptidae), which has varieties on differ- of the fur mite, Listrophorus leuckarti (Acaridida: ent hosts. Scab mites are very small; females are Sarcoptoidea: Listrophoridae), is hidden under a about 0.3–0.5 mm long and 0.2–0.4 mm wide. projection that together with the mouthparts Males are about 3/4 the size of females. Most scab and modified legs grasp the hosts hair shaft and mites complete their life cycles in 10–14 days. The provide support to the attached mite. The mite varieties that infest humans, dogs and hogs are the grazes on the hair surface using unmodified cheli- most studied. Males and females burrow about cerae. The clasping apparatus is closed or opened 1 mm into the skin of the host. Gravid females lay indirectly by movements of the gnathosoma. eggs in the burrows. The hexapod larva commonly enters hair follicles where they feed and molt into an octopod protonymph. This stage is followed by Stored Product Pests a tritonymph and the adult. The scaly leg mite, Knemidokoptes (=Cnemido- Some species of mites are serious pests of stored coptes, = Knemidocoptes) mutans (Acaridida: Anal- products. Many of the stored product pests can also goidea: Knemidokoptidae), causes scaly leg disease cause a type of dermatitis known as occupational in domestic poultry. This mite burrows into the skin acarine dermatitis. Lardoglyphus zacheri (Acaridida: where it lives and deposits its eggs in channels. The Acaroidea: Acaridae) is a pest of stored meat and disease presents as a swollen condition in the shank Lardoglyphus konoi (Acaridida: Acaroidea: Acari- of the bird with deformity and encrustation of dae) is a pest of dried fish. The acarid bulb mites, shank scales. Mites are easily transmitted from Rhizoglyphus echinopus and R. callae (Acaridida: bird to bird by contact. The depluming mite, Knemi - Acaroidea: Acaridae), are pests on ornamental and dokoptes gallinae (Acaridida: Analgoidea: Knemi- vegetable bulbs, tubers and the roots of some culti- dokoptidae), feeds at the base of feathers causing vated crops. Carpoglyphus lactis (Acaridida: Acaroi- intense itching in the bird which then may pluck dea: Carpoglyphidae) occurs in fruit, dried milk its feathers for relief. Mange of parakeets is caused products, flour and other stored food, and honey by Knemidokoptes pilae (Acaridida: Analgoidea: from hives where this mite lives. Chortoglyphus arc- Knemidokoptidae). Knemidokoptes jamaicensis uatus (Acaridida: Acaroidea: Chortoglyphidae) is infests canaries. Epidermoptes bilobatus (Acaridida: found in stables in hay dust or fodder. The mold Analgoidea: Epidermoptidae) can cause a scaly skin mite, Tyrophagus putrescentiae (Acaridida: Acaroi- disease in poultry that can result in weight loss, dea: Acaridae), is found in processed cereals and and is fatal in some birds with heavy infestations. causes grocer’s itch or copra itch which can affect Two species of mites are internal parasites anyone handling infected products. The scaly grain of poultry. Cytodites nudus (Acaridida: Analgoi- mite, Suidasia nesbitti (Acaridida: Acaroidea: Acari- dea: Chytoditidae) is found in the linings of the dae), causes wheat pollard itch. The dried fruit mite, respiratory tracts of poultry, mostly chickens. Carpoglyphus lactis (Acaridida: Acaroidea: Carpg- Laminosoptes cysticola (Acaridida: Analgoidea: lyphidae), causes dried fruit dermatitis. The grain Chytoditidae) is found in the tissue of chickens mite, Acarus siro (=Tyrophagus farinae) (Acaridida: Mites (Acari) M 2439 Acaroidea: Acaridae), causes baker’s itch. The Tetranychoidea and the Eriophyoidea. A compre- house mite, Glycyphagus domesticus (Acaridida: hensive list of pest species of tetranychids and Glycyphagoidea: Glycyphagidae), and Lepidogly- eriophyoids can be found in the books given in phus destructor (Acaridida: Glycyphagoidea: the literature cited section of this article. Here, we Glycyphagidae), are common on the walls, furni- will consider only the most economically impor- ture and clothing in dwellings where dampness tant species. helps the growth of fungi. The former species There are five families in the Tetranychoidea causes a contact dermatitis described as a form with over 450 phytophagous species. The most of grocer’s itch which occurs mostly in food important pests are found in the Tetranychidae or handlers. Glycyphagus destructor (Acaridida: Gly- spider mites and the Tenuipalpidae or false spider cyphagoidea: Glycyphagidae) causes hay itch. mites. Many of these are important pests of agricultural crops worldwide. Spider mites can infest every major food crop and many ornamental House Dust Mites plants. Their chelicera are modified into whip-like structures which they insert either through or Some ten species of mites of the family Pyroglyph- between palisade cells of the plant into the paren- idae are common in human dwellings throughout chyma which lies below. Here they feed and may the world where they exist in the dust found on inject a toxic saliva. Destructive symptoms include floors, furniture and bedding. The most common reduction of plant growth, loss of plant vigor, stip- house dust mites are the American house dust pling of the tissue at the feeding site and drop off mite, Dermatophagoides farinae (Acaridida: Anal- of the leaf and fruits. goidea: Pyroglyphidae) the European house dust The clover mite,Bryobia praetiosa (Actinedida: mite, D. pteronyssinus and Euroglyphus maynei Tetranychoidea: Tetranychidae), infests grasses (Acaridida: Analgoidea: Pyroglyphidae). The Euro- throughout the world. These mites can overwinter pean house dust mite and Euroglyphus maynei in any stage. In the spring they can occur in large prefer climates with a higher humidity while the numbers in buildings where they molt and ovi- American house dust mite occurs in more temperate posit. The clover mite may be a complex of races zones. These mites can produce human allergies that differ somewhat in their life histories and the especially in susceptible individuals. House dust plants they infest. The brown mite, B. rubrioculus, is mites feed on shed human and animal skin. The a pest of pome and stone fruits. However, the brown allergens they produce are in their feces and in mite may be a race of the clover mite. The brown their skins shed during molts. Allergic reactions wheat mite, Petrobia latens (Actinedida: Tetrany- range from asthma and atopic dermatitis to itchy choidea: Tetranychidae), the legume mite Petrobia noses and eyes. House dust mites survive best at apicalis, and Tetranycopis horridus (Actinedida: relative humidities greater than 70% and tempera- Tetranychoidea: Tetranychidae), a pest of filberts, tures from 75 to 80°F. They do not survive well at are serious crop pests. The two-spotted spider mite, low relative humidities and higher temperatures. Tetranychus (Tetranychus) urticae, (Actinedida: Tet- Under the best conditions, their life cycle takes ranychoidea: Tetranychidae), and T. (Armenychus) approximately one month from egg to adult. mcdanieli, infest deciduous fruit trees. The European red mite, Panonychus ulmi (Actinedida: Tetrany- choidea: Tetranychidae), attacks deciduous fruit Pests of Agricultural Crops trees in Europe, North America and Japan. In North America, South Africa and Japan, the citrus red The most serious mite pests of agricultural crops mite, Panonychus citri, is a serious pest on citrus are found in two Actinedida superfamilies, the fruit trees. 2440 M Mites (Acari) The false spider mites (Actinedida: Tetrany- sheldoni, causes deformation in fruit and leaves. choidea: Tenuipalpidae) are most common in Some species of eriophyids can spin silk which subtropical and tropical climates but some species may act as a defense against predators. Eriophyid occur in the temperate region. Three genera con- mites also cause plant stunting, shortening of tain economically important species: Brevipalpus, internodes and adventitious twig development or Tenuipalpus, and Cenopalpus. These mites usually witches broom. Some species of Eriophyidae feed on the underside of a leaf. Some species attack transmit plant viruses. Eriophyes tulipae transmits grass and occur in leaf sheaths. Some species occur wheat streak and wheat spot mosaic virus. Ceci- in galls. Three species of Brevipalpus, B. lewisi, dophyopsis ribis transmits currant reversion, B. obovatus, and B. phoenicis attack citrus trees in a viral disease of black currants. Eriophyes commercial orchards. Brevipalpus species also ficus transmits fig mosaic virus. Eriophyes insidio- attack ornamentals, grapes, berry crops, orchids sus transmits peach mosaic virus. Aculus fockeui and olives. Species of Tenuipalpus attack grasses, transmits latent plum virus. tea, orchids and other crops. Cenopalpus lanceola- tisetae and C. pulcher attack deciduous fruit trees in North Africa, Asia and Europe. Bee Mites Members of the superfamily Eriophyoidea (Actinedida: Eupodina), are distributed world- Over 100 species of mites are associated with wide. In their northern areas of distribution, honey bees. Three species are important pests: the some species produce deutogynes that function varroa mite, Varroa destructor (formerly jacobsoni) as overwintering females. Eriophyoids are found (Gamasida: Dermanyssoidea: Varroidae); and the mostly on perennial plants. They injure but sel- tropilaelaps mite, Tropilaelaps clareae (Gamasida: dom kill plants. Eriophyoids feed in a similar man- Dermanyssoidea: Laelapidae); the honey bee tracheal ner as tetranychids, but eriophyoids are more host mite, Acarapis woodi (Actinedida: Tarsonemoidea: specific and produce very different host reactions. Tarsonemidae). These host reactions have resulted in several com- The varroa mite is considered the major pest mon names for this group as gall mites, blister of bees. It is found throughout the world with the mites, bud mites and rust mites. Catarhinus tricho- exception of Australia, New Zealand and Hawaii. laenae (Rhyncaphytopidae) causes leaf rust on It causes varroasis (varroatosis or varrosis). The corn in Brazil. The peach silver mite,Aculus coma- mite rips open the integument of the bee and feeds tus (Eriophyidae), causes leaf spotting or curling. on hemolymph. It prefers young bees to older Galls are reactions of the plant to feeding by mites. workers. Female mites are phoretic on adult bees. Several eriophyoid mite species cause galls of dif- Varroa destructor is now considered to be a com- ferent shapes, but all are due to abnormal growth plex of at least five species. Control has been hard of papillary material of the plant. Galls may be to achieve because chemicals must kill only the open or closed but all provide an area where mites, and biological methods are often very labor mites can feed without pressure from predators intensive. Both the honey bee tracheal mite and and where feeding mites are protected from the varroa mite have also been implicated in the desiccation. Eriophyes brachytarsus (Eriophyidae) spread of bee viruses. attacks California black walnut where it causes The tropilaelaps mite is found in Asia from either leaf puckering or purse galls. Blisters are Iran south to New Guinea. It has a similar but formed within the parenchymal leaf tissues by shorter life cycle to that of the varroa mite. Female feeding mites. The Eriophyes pyri species complex mites are phoretic on bees. It is believed that the produces blisters on pears, apples, and other poma- mites feed only on the soft tissues of brood bees. ceous plants. The citrus bud mite, Eriophyes Tropilaelaps mites can out-compete varroa mites Mitochondrion, (pl., Mitochondria) M 2441 Evans GO (1992) Principles of acarology. C.A.B. Interna- because they have a shorter life cycle, and emerging tional, Wallingford, UK, 561 pp mites spread by attaching to adult bees. However, Houck MA (ed) (1994) Mites: ecological and evolutionary both species can coexist because they occupy analyses of life-history patterns. Chapman and Hall, different niches in the same hive. New York, NY, 357 pp Helle W, Sabelis MW (eds) (1985) Spider mites. Their biology, The honey bee tracheal mite lives within the natural enemies and control. World crop pests, vol 1A. tracheae of their hosts and have a foreshorten life Elsevier, Amsterdam, The Netherlands, 405 pp cycle with only three stages. In the tracheae, they Helle W, Sabelis MW (eds) (1985) Spider mites. Their biology, feed on bee hemolymph. Except for a brief period natural enemies and control. World crop pests, vol 1B. Elsevier, Amsterdam, The Netherlands, 458 pp when searching for a new host, these mites spend Krantz GW (1978) A manual of acarology. Oregon State Uni- their entire life within the tracheae. Females prefer versity Book Stores, Corvallis, Oregon, 509 pp to lay their eggs in the tracheae of younger bees, Lindquist EE, Sabelis MW, Bruin J (1996) Eriophyoid mites: their biology, natural enemies, and control. World preferably drones. Infestations cause a cascade of crop pests, vol 6. Elsevier, Amsterdam, The Nether- problems from loss of brood area, and smaller lands, 790 pp bee populations, to lower honey yields. The honey Walter DE, Proctor HC (1999) Mites: Ecology, evolution and bee tracheal mite is found worldwide except in behaviour. CABI Publishing, New York, NY, 322 pp Denmark, Sweden and Norway, New Zealand and Australia and Hawaii. Several other species of mites are parasites Miticide of wild bees. Locustacarus buchneri (Actinedida: Tarsonemoidea: Podapolipidae) is a tracheal par- A pesticide used to control mites. It also is called asite of bumble bees of the genus Bombus. The an acaricide. female mite overwinters in the trachea of queen  Acaricides and Miticides bees. In the spring she feeds on hemolymph and  Insecticides lays a moderate clutch of eggs that hatch into non feeding fertile males and motile six legged fertile larviform females. Mating occurs just after hatch- Mitochondrion, (pl., ing and the gravid females go directly to worker Mitochondria) bees where they attach inside the tracheal system and molt to an adult female. The adult female is An organelle that occurs in the cytoplasm of all sac like and much larger than males. She has only eukaryotes, capable of self-replicating. Each mito- one pair of legs. In this unusual life cycle, eggs chondrion is surrounded by a double membrane. hatch directly into adult or adult like forms. The inner membrane is highly invaginated, with  Ticks projections called cristae that are tubular or lamel-  Four-legged Mites lar. Mitochrondria are the sites of oxidative phos-  Acaricides or Miticides phorylation which result in the formation of ATP.  Tracheal Mite Mitochondria contain distinctive ribosomes,  Varroa Mite transfer RNAs, and aminoacyl-tRNA synthetases. Mitochondria depend upon genes within the nucleus of the cells they inhabit for many essential References mRNAs. Proteins translated from mRNAs in the cytoplasm are imported into the mitochondrion. Mitochondria are thought to be endosymbionts Alberti G, Coons LB (1999) The Acarimites. In: Harrison FW, Foelix R (eds) Microscopic anatomy of invertebrates, derived from aerobic bacteria that associated with vol 8C: Chelicerate arthropoda. Wiley-Liss, New York, primitive eukaryotes and have their own circular NY, pp 267–514 DNA molecules. The genetic code of mitochondria 2442 M Mitosis differs slightly from the universal genetic code. Mode of Action Mitochondria are transferred primarily through the egg, and thus maternally inherited. The means by which a toxin affects an organism physiologically or metabolically. This term is usually used in concert with discussion of insecticides. Mitosis Most insecticides are neurotoxins, disrupting normal nervous transmission by affecting either The sequence of events that occur during the divi- axonic or synaptic transmission. Others are sion of a single cell into two daughter cells. metabolic inhibitors, affecting central cellular metabolic functions such as membrane permeability. Still others are more selective, affecting insect Mixed Infection growth or molting.  Insecticides Concurrent infection by two or more pathogenic microorganisms. Molannidae

A family of caddisflies (order Trichoptera). M’Lachlan, Robert  Caddisflies

Robert M’Lachlan was born near Ongar in Essex, England, on April 10, 1837. He was educated at Molar Ilford and was independently wealthy, allowing him to pursue his interests in botany and entomol- The grinding surface of the insect mandibles, often ogy. He became a leading British authority on ridged or roughened. Neuroptera and became the first editor of the British journal “Entomologist’s Monthly Maga- zine.” He was a member of many scientific societ- Mole Crickets (Orthoptera: ies, and published monographs on caddisflies and Gryllotalpidae) and Their psocids, in addition to Neuroptera. He died in Biological Control London on May 23, 1904. J. Howard Frank, Norman c. Leppla University of Florida, Gainesville, FL, USA Reference Mole crickets are strange creatures, highly adapted Essig EO (1931) A history of entomology. The Macmillan for a subterranean existence, including the devel- Company, New York, 1029 pp opment of their forelegs for digging. They are currently classified into two tribes, Gryllotalpini and Scapteriscini, although some taxonomists consider Mnesarchaeidae these to be subfamilies, Gryllotalpinae and Scap- teriscinae. Adult of most species are long-winged A family of moths (order Lepidoptera). They also and capable of flight, but in some species the adults are known as New Zealand primitive moths. are brachypterous and flightless. Within some spe-  New Zealand Primitive Moths cies there are populations having long-winged  Butterflies and Moths adults and populations with brachypterous Mole Crickets (Orthoptera: Gryllotalpidae) and Their Biological Control M 2443 adults. The trochanter of each foreleg bears a long Pacific islands, and southern Africa, these are blade. The medial (inner) side of the tibia of each species of Gryllotalpa. In South America, the West foreleg bears a tympanum (hearing organ). The Indies, the southern USA, and eastern Australia, tibia of each foreleg also bears a line of (in Gryl- they are species of Scapteriscus. Almost all con- lotalpini) four, or (in Scapteriscini) three or two trol attempts have been by physical methods or large, fixed (immobile) dactyls (claws). There also by use of chemical pesticides. There have been are mobile tarsal dactyls. Each forewing of males few attempts at biological control albeit that some bears a harp-shaped cell and a stridulatory file of level of population regulation by native natural minute pegs; these structures are used to produce enemies undoubtedly occurs everywhere. a loud, species-specific song, of about 70 decibels Five mole cricket species have been the tar- when adequately projected. Adequate projection gets of classical biological control programs. In entails construction of a calling chamber at the Hawaii an invasive species of Gryllotalpa was mouth of a tunnel in the soil, formed in the shape detected in the late 19th century. Its precise origin of a loudspeaker and needing adequate moisture and means of arrival seem unreported. However, it to make it fully functional. Song is projected by is not G. africana Palisot de Beauvois as was ini- males to attract flying females, from sunset onward tially assumed, and it may be G. orientalis Bur- on humid nights in the flight season. The flight meister, a species native to southeastern Asia. It season is that time of year when most flight occurs, was reported to damage sugarcane. There are no and in some species there may be a major flight native mole crickets in Hawaii. In Puerto Rico, season in spring and a minor one in autumn. Scapteriscus didactylus (Latreille) is of South Flying adults are mainly females. Females of at American origin. Hundreds of years ago it began a least some Gryllotalpini care for their eggs and the gradual range extension northward through the resultant small nymphs, showing a presocial chain of islands of the Lesser Antilles, eventually behavior. The number of nymphal instars is vari- reaching Puerto Rico and Hispaniola. This range able even within species, ranging perhaps from extension most likely was by flight, from island to seven to ten. At all events, the nymphs develop island. At all events, there is evidence that it had slowly. The number of generations per year may reached Puerto Rico at least as early as the eigh- vary even within a species, so the populations of a teenth century. By the late nineteenth century, it given species may have as few as one generation was reported to cause severe damage to sugarcane every two years at high latitudes, but one annual and many other crops in Puerto Rico. Early reports generation at lower latitudes, or may have one of its presence in Cuba, Jamaica, and the south- generation per year at higher latitudes, but two at eastern USA were incorrect, the result of mistaken lower latitudes. For the most part, the diet of adults identity. Much later, it was detected in New South and nymphs is plant material, but in some species Wales, Australia, undoubtedly having arrived at the diet has adapted to a major proportion of ani- least by 1982 as a contaminant of some air cargo mal material such as earthworms and some small or sea cargo. There are no native (pre-Columbian) insects. Adults and nymphs spend most of their mole crickets in Puerto Rico. In Florida, three lives in the ground, but venture to the surface on South American Scapteriscus spp. arrived at dates warm, humid nights. They form galleries (tempo- between 1899 and 1925, very likely in solid (sand) rary horizontal tunnels only just below the soil ballast of ships trading with ports in southern surface) as well as deeper, more permanent tunnels. South America. They are S. abbreviatus Scudder, More than 90 species of mole crickets have S. borellii Giglio-Tos, and S. vicinus Scudder. They been described, but only a few have been reported were first noticed as pests of vegetable crops. Later, as pests. In eastern and southern Asia, some as they spread and, as turf- and pasture-grasses of islands of Indonesia and the Philippines, some foreign origin (bermudagrass and bahiagrass) 2444 M Mole Crickets (Orthoptera: Gryllotalpidae) and Their Biological Control were imported and grown widely, the three mole L. (Rubiaceae), by its adults in Brazil and Puerto crickets caused more and more damage to these Rico. Damage by pest mole crickets seems to grasses. There are no native species of the tribe have declined dramatically in Puerto Rico since Scapteriscini in Florida. that time, but nobody has measured the effect of Thus, appropriately, classical biological L. bicolor as a contributor to that decline. It may control attempts were made only in new territo- not have been the only contributor, especially ries that the mole cricket species had invaded. because Bufo marinus L. (Amphibia: Bufonidae), All were attempts to find and import specialist a generalist predator of large insects had already natural enemies, especially from the homelands been imported by the same Puerto Rican of the pest species. entomologists, and became established. To the extent that S. didactylus and two other Scapteriscus spp. (S. abbreviatus and S. imitatus Nickle and Larra (Hymenoptera: Sphecidae) Castner) are still at least occasional pests in Puerto Imported into Hawaii Rico (they seem to be constant pests on golf courses), continued effort in their biological con- In 1924, small numbers of two South American trol might have been expected. But control attempts Larra spp. (Hymenoptera: Sphecidae) were after ~1950 reverted to the use of chemical pesti- imported. Observation showed that the mole cides, and renewed effort in biological control did crickets were not suitable hosts for them, which not occur until the twenty first century. was not surprising because their natural hosts are Scapteriscus mole crickets, not Gryllotalpa. A few were released and failed to become Larra (Hymenoptera: Sphecidae) established. In 1925, Larra polita (Smith) ssp. Imported into Florida luzonensis Rohwer specimens captured in the Philippines were imported into Hawaii, released University of Florida entomologists in the 1940s and became established. It is now believed that noted what seemed to have been achieved by the mole cricket attacked by L. polita in the Phil- importation of L. bicolor into Puerto Rico and ippines is G. orientalis, which is thought to be made feeble attempts to do the same. They were the natural host of that wasp. The precise effect unsuccessful, in part because a war was then in of the establishment of L. polita was not mea- progress and travel was difficult, in part because sured. The only evidence of success is lack of of the discovery of the chemical chlordane, which subsequent reports of damage caused by mole seemed at least to their administrators to provide crickets in Hawaii. a long-term and inexpensive means of controlling mole crickets, so that there was no need for biological control. Those entomologists were Larra (Hymenoptera: Sphecidae) aware of the importance of Spermacoce verticil- Imported into Puerto Rico lata, and it may have been they who introduced this plant into Florida. The presence of the plant Puerto Rican entomologists in the 1930s explored in Florida was not detected by botanists until the northern South America for potential biocontrol 1960s, so the timeline matches. After chlordane agents of their pest mole cricket, S. didactylus. In was banned by the US EPA in the 1970s, Univer- Belém, on the Amazon in Brazil, they encountered sity of Florida entomologists were mandated by Larra bicolor (F.) and, after several attempts, finally the Florida legislature to begin a program that got it established in their island. They noted heavy would solve the problem caused by Scapteriscus use of a nectar-source plant, Spermacoce verticillata mole crickets. One of their early actions was Mole Crickets (Orthoptera: Gryllotalpidae) and Their Biological Control M 2445 importation of L. bicolor wasps from Puerto Rico, chasing the denizens to the surface. There, they released at sites prepared with plantings of Sper- grapple with the mole cricket in attempt to sting macoce verticillata. They were successful at their and paralyze. A sting to the head paralyzes a first attempt in 1981 with a release at Ft. Lauder- mole cricket for a few minutes only, during dale, but unsuccessful with subsequent releases at which time the female wasp lays an egg on the sites farther north. Regrettably, the L. bicolor underside of the thorax. From the egg hatches a population near Ft. Lauderdale failed to spread. larva (grub) that feeds as an ectoparasitoid (on Worse, its measured effect on the local pest mole the outside of the mole cricket). When the grub cricket population was trivial. Perhaps the reason has killed the mole cricket, it spins a cocoon was because the founding stock was originally and pupates in the ground. The duration of the from the equator, and was too tropical to spread pupal stage is highly variable, lasting many widely in Florida. months during the winter in northern Florida, In 1988–1989, University of Florida ento- and allowing survival of the population during mologists imported stock of this same wasp spe- freezing temperatures. There are more annual cies from a higher altitude, in Bolivia, and released generations in tropical areas and fewer genera- it in northern Florida (Gainesville). The Bolivian tions in more temperate areas, with the pupal stock became established and began to spread stage in diapause acting as the means of surviv- and, as of August 2006, has been reported from ing winter in places where freezing tempera- 28 Florida counties (reports from a few addi- tures occur. The northern limit of occupation tional counties need confirmation by specimens by L. bicolor in the southeastern USA has not or photographs). A satellite release at Tifton, yet been determined, but likely is little more Georgia, in 2001, established it there; it has sub- than 31°N. sequently been reported from Georgia locations 150 miles northeast and >100 miles southwest of Tifton. It has also been encountered in coastal Ormia depleta (Diptera: Tachinidae) Mississippi; assuming that it spread there from Imported into Florida Florida or Georgia, it should be present in coastal Alabama and may possibly spread to coastal Ormia depleta (Wiedemann) larvae parasitize at Louisiana and Texas. There is no published eval- least some species of Scaptericus mole crickets. uation of its effect on pest mole crickets any- This fly’s distribution includes not only Amazo- where in the USA. A preliminary estimate for nian Brazil (as was discovered by Puerto Rican two sites in Alachua County is of almost 70% entomologists) but also southern Brazil at least mortality of Scapteriscus vicinus in the autumn as far as 30°S, and at least part of Paraguay. Stock months of 2000–2001, but verification needs of the fly obtained at 27°S at Piracicaba in the mathematical modeling because there are several Brazilian state of São Paulo was imported into wasp generations per one annual mole cricket Florida in several shipments in the late 1980s. generation. At all events, L. bicolor is a major Painstakingly reared individually by the thou- mortality agent of pest mole crickets in northern sands on mole cricket hosts, progeny were first Florida, and its population should spread every- released in 1988 near Gainesville (Alachua where in Florida where there are pest mole County) and Bradenton (Manatee County). More crickets. releases followed over the next four years in all Adult female wasps are active during the parts of Florida. By 1994, it was recognized that warmest hours of each day. They search the the stock had occupied all peninsular counties ground surface for evidence of mole cricket (38 of them) to 29°45’ N, but that occupation of the activity, entering mole cricket burrows and northernmost of these counties was temporary, 2446 M Mole Crickets (Orthoptera: Gryllotalpidae) and Their Biological Control with a permanent population occurring only evaluate current effects and to design methods south of 28°45’ N, and with increase of that area to enhance effects. An effort to import the fly but little to the north each autumn. The estab- into Puerto Rico in the 1930s was unsuccessful, lished stock of the fly did not overwinter rou- and the effort has not been repeated. tinely north of about 28°45’ N. Southernmost Brazil (Rio Grande do Sul) was then explored for this same fly, and stock was imported from Steinernema scapterisci the southernmost locality where it was detected (Rhabditida: Steinernematidae) (at 30°S), near Osorio, northeast of Porto Alegre, Imported into Florida in 1999. Progeny were reared, and were supplied to collaborators in Georgia, Louisiana, and Detected by its emergence from dying pitfall- North Carolina for release, but these collabora- trapped Scapteriscus mole crickets in Uruguay tors reported no evidence of establishment in in 1995, this nematode was brought to Florida their areas. Study of the diapause capabilities of and later described as a new species. Dauer lar- this southern stock was entrusted to two Uni- vae of S. scapterisci Nguyen and Smart harbor versity of Florida PhD students who were to specialist bacteria of the species Xenorhabdus characterize development of the fly at assorted innexi Lengyel et al. When the larvae, lurking in conditions of photoperiod, temperature and the soil, detect a passing Scapteriscus mole humidity, and determine whether diapause can cricket, they attempt to enter it through its or cannot occur, the idea being to determine mouth or spiracles. If they are successful, they whether the fly can survive cold winters in dia- break into its body cavity and release the bacte- pause. Neither student succeeded before the fly ria. The bacteria reproduce inside the insect’s culture died out, likely due to inbreeding. For body cavity, killing it through septicemia. The the present, we have to conclude that there is no nematodes feed within the dying mole cricket, evidence that the fly can diapause in winter, so mature, undergo two generations, and release perhaps there is no hope that it can establish bacterium-carrying dauer larvae back into the permanent populations in northern Florida and soil. This process (from attack to release of off- states to the north. spring into the soil) can be accomplished within Adult flies are nocturnal and gravid females ~10 days at warm temperatures, but may per- are phonotactic (use the song of mole crickets haps be extended for weeks at cool winter tem- to detect hosts). They larviposit, and larvae pen- peratures when pest mole crickets retreat deeply etrate the host mole cricket, killing it within ~8 into the soil and activity by mole crickets and days. Larvae then pupate in the ground for nematodes alike is greatly slowed. A further 11–12 days before the new adult generation complication is that Scapteriscus nymphs are emerges. Evaluations of mole crickets trapped scarcely susceptible to attack by S. scapterisci, in pitfall traps in May 1993 and May 1994 in perhaps because their body apertures (mouth Orange County revealed parasitism of 24–25%. and spiracles) are too small to be penetrated by Because parasitized mole crickets die after ~8 the dauer larvae. Releases of this nematode, days, and because O. depleta has several genera- reared within laboratory cultures of mole crick- tions each year in contrast to just one for the ets, were first made in Florida on a very small mole crickets, the mortality inflicted by the fly scale in 1985. They established permanent pop- is likely to be considerable. At all events, the ulations and began to spread. level of control exerted by this fly is now free in Development of mass-production methods central and southern Florida. If funds were by industry allowed sales of Steinernema scap- made available, it should be possible to further terisci (several trade names have been used) as a Mole Crickets (Orthoptera: Gryllotalpidae) and Their Biological Control M 2447 biopesticide. It also allowed experimental appli- Conclusion for Florida cations on a bigger scale than before. These experiences showed that applications are best Classical biological control of Scapteriscus mole timed when adult mole crickets (not nymphs) crickets in north-central Florida has been highly are abundant and active, so in February–April successful due to establishment of three biologi- and September–November in central and south- cal control agents from South America, and suc- ern Florida (February is perhaps too early in cess is spreading throughout Florida as populations northern Florida). Applications are effective of Larra bicolor and Steinernema scapterisci spread against Scapteriscus borellii and S. vicinus. They (Ormia depleta may already have spread to its do not kill as high a percentage of pest mole fullest possible extent). The ultimate level of suc- crickets measured in the short term (days) as do cess should be enough to obviate all need for the most effective chemicals. However, applica- chemical treatment of lawns, playing fields, and tions generally initiate permanent populations pastures to control pest mole crickets. This leaves that suppress pest mole cricket populations for four situations where classical biological control years in pastures, playing fields, and golf courses. may need enhancement. The first, in pastures Cost of application in pastures has been greatly where Steinernema scapterisci is not yet present; reduced by treating one swath (strip) in eight owners/operators need to be aware of the avail- across a pasture, because easily within the space ability of this nematode, and that it may be applied of a year the nematode population spreads in swaths (strips) across a mole-cricket-infested throughout the pasture. Such spread is due to pasture, at the level of one treated swath per seven transport of nematodes within newly-infected untreated swaths, to achieve distribution through- mole crickets. The same transport eventually out the pasture within a few months, a big reduc- allows the nematode to occupy distant sites with tion in cost over complete pasture treatment; they mole cricket populations. also should be aware of the possibility of planting Spermacoce verticillata to enhance Larra bicolor presence. The second is organic farms, where Steinernema scapterisci owners/operators need to be aware of their ability (Rhabditida: Steinernematidae) to buy and apply Steinernema scapterisci if it has Imported into Puerto Rico not already been applied, and to plant Spermacoce verticillata or another nectar-source plant to In 2001, under USDA-APHIS permit, Stein- encourage populations of Larra bicolor (alterna- ernema scapterisci was applied at two localities tives to S. verticillata are under investigation). in Puerto Rico, and in subsequent years in The third is regular commercial vegetable farms three more localities, all in the west of that island. where owners/operators need to be aware that use In the laboratory, it was demonstrated to be effec- of Steinernema scapterisci is compatible with use tive in attacking and killing adult Scapteriscus of many if not all chemical insecticides, so they didactylus, but survival of its dauer larvae in should not be reluctant to buy and apply the nem- some Puerto Rican soils seemed to be poor. Such atode because this provides partial control of pest soils included highly organic sandy soils in which mole crickets indefinitely, at a huge potential cost antagonists may have been present. They also saving. The fourth is golf courses, most of which included a sandy loam. Such high mortality had have experienced a decline in damage caused not been observed in the sandy soils where by mole crickets. Although this decline is due to survival has been so good in Florida. Neverthe- the spread of classical biological control agents, less, the nematode should now be established in the golf course personnel in general have no expe- Puerto Rico and should gradually spread. rience in detection of the presence of any of the 2448 M Mole Crickets (Orthoptera: Gryllotalpidae) and Their Biological Control three biological control agents, so their assump- Conclusion for Puerto Rico tion has been that they now have wonderful new chemical insecticides that solve their previous Larra bicolor seems to have provided partial sup- problems with mole crickets. A little thought pression of pest mole cricket populations for many should reveal to them that it is strange that the decades. Steinernema scapterisci should now be wonderful new “chemicals” have suppressed mole established in northwestern Puerto Rico. If so, it crickets only, while damage by other insect pests should continue to spread. Landowners/managers has “increased” dramatically. What of course has should familiarize themselves with biological happened is that classical biological control control solutions and urge distributors to import has decreased pest mole cricket populations Steinernema scapterisci for sale; there should dramatically, and that golf course personnel are be no bureaucratic impediment to such importa- left to deal with the previously minor (at least in tion because that nematode already is established. Florida) problem caused by larvae of Scara- It may be possible to introduce Ormia depleta. baeidae. Further, mole cricket populations have declined also in pastures, where chemicals are not applied. There is an enormous educational task Conclusion for Eastern Australia, to be performed – and a new biological control Islands of the Lesser Antilles, and challenge – how to suppress populations of pest the Dominican Republic scarab larvae, many of which are native. Now is the time to consider whether importation of biological control agents (Ormia depleta, Larra Conclusion for Other Southeastern bicolor, Steinernema scapterisci) would be an advan- States of the USA tage over current repeated chemical applications against Scapteriscus didactylus control. It is not a Larra bicolor should continue to spread, deliber- good idea to delay because the easiest source of ately helped or not, to the coastal areas of Alabama, these biological agents is Florida, where biological Missisippi, Lousiana, and Texas. It is unlikely to control expertise is winding down with retirements. spread much to the north of about 31°N. Ormia depleta is highly unlikely to spread to northern Florida, and not beyond Florida’s borders. Stein- Conclusion for South America ernema scapterisci may (at least at present) be purchased and applied against pest mole crickets Where Scapteriscus mole crickets are a problem, anywhere in the continental USA. Its purchase for example on golf courses using fresh soils that and application is a good investment if applied Steinernema scapterisci has not yet reached, appli- in early spring, even if it cannot overwinter. But cation of the nematode is the most immediately perhaps it can overwinter, in at least parts of viable biological control option. This would now Alabama, Louisiana, Mississippi, North Carolina, demand the purchase of these nematodes from South Carolina, and Texas and suppress pest mole the only current producer, in North America. crickets for several seasons. It is up to entomologists/nematologists in those states to investigate. At all events, it does overwinter in southern Conclusion for Hawaii Georgia. If sales of Steinernema scapterisci are not sufficient, its producing company is likely to There is no current problem with pest mole discontinue production. Thus, now is the time crickets. It would be satisfying to identify defini- for trial applications in states north of Florida. tively the one pest species present, which may or Molecular Diagnosis M 2449 Nguyen KB, Smart GC (1990) Steinernema scapterisci n. sp. (Rhabditida: Steinernematidae). J Nematol 22:187–199 Parkman JP, Frank JH, Walker TJ, Schuster DJ (1996) Classical biological control of Scapteriscus spp. (Orthoptera: Gryllotalpidae) in Florida. Environ Entomol 25:1415–1420 Vicente NE, Frank JH, Leppla NC (2007) Use of a beneficial nematode against pest mole crickets in Puerto Rico. Proceedings of the Caribbean Food Crops Society 42(2): 180–186 Williams FX (1928) Studies in tropical wasps – their hosts and associates. Hawaiian Sugar Planters’ Association Experiment Station. Entomol Ser Bull:191–79 [Note: the adventive mole cricket detected in Hawaii in1896 is Mole Crickets (Orthoptera: Gryllotalpidae) and in reality probably Gryllotalpa occidentalis, and the wasp that was successfully imported as a biological control Their Biological Control, Figure 79 Medial (inner) agent was Larra polita (Smith) ssp. luzonensis Rohwer] side of left foreleg of Scapteriscus borellii Giglio-Tos Wolcott GN (1938) The introduction into Puerto Rico of showing trochantal blade (b), tympanum Larra americana Saussure, a specific parasite of the (t), two fixed dactyls of tibia (d), and movable “changa” or Puerto Rican mole cricket, Scapteriscus vicinus. J Agric Univ Puerto Rico 22:193–218 [Note: in real- tarsal dactyls. Photo: Lyle Buss. ity, the wasp is Larra bicolor and the mole cricket is Scapteriscus didactylus] may not be Gryllotalpa orientalis, and is not Gryllotalpa africana as was assumed for decades. Molecular Biology

Conclusion for Africa and Southern A term broadly used to describe biology devoted Asia Including the Philippines and to the molecular nature of the gene and its Indonesia biochemical reactions such as transcription and translation. Taxonomic revision of Asian mole crickets is essential. Decades of “basic” studies of potential biological control agents may be necessary before suitable species for use in any given geographical area are Molecular Diagnosis adequately researched. The various biological control agents researched in Florida and Puerto Rico for Maria Navajas1, George Roderick2 use against Scapteriscus mole crickets are not suitable 1INRA, UMR CBGP (INRA/IRD/Cirad/ for use against Gryllotalpa mole crickets (Fig. 79). Montpellier SupAgro), Montferrier-sur-Lez,  Turfgrass Insects of the United States: Biology France and Management 2University of California, Berkeley, CA, USA  Grasshoppers, Katydids and Crickets  Mole Crickets and their Biological Control Molecular diagnosis refers to the taxonomic deter-  Turfgrass Insects and their Management mination of organisms based on molecular criteria. Correct taxonomic determination is critical References for entomological applications in many fields, including agriculture, environmental science, bio-

Frank JH, Walker TJ (2006) Permanent control of pest mole security, and human health. Because a major chal- crickets (Orthoptera: Gryllotalpidae: Scapteriscus) in lenge in taxonomy is the discrimination among Florida. Am Entomol 52:138–144 closely related forms, diagnosis mainly concerns 2450 M Molecular Diagnosis the identification of organisms at the species level. Another commonly held view of species is One example is the case of cryptic species com- the evolutionary species concept, in which a spe- plexes, which are groups of closely related species cies represents a single lineage of ancestral- that are difficult or impossible to distinguish by descendant populations that maintains its identity morphological traits alone. These complexes are from other lineages and that has its own evolu- known from a wide variety of arthropods and have tionary tendencies. This view is similar to the bio- been well studied in medically and economically logical species concept, in which species are important insects. For example, despite a near viewed as a set of interbreeding organisms. While identity in morphological appearance, several sib- the biological concept of species is a meaningful ling species of mosquitoes are separable with a one for many applications in which a species variety of molecular-based methods. Conversely, determination is necessary, biological experi- molecular systems can be used to establish syn- ments to assess biological species are not possible onymy between presumed cryptic species. Often, for some species. identifying closely related species using traditional Tools of molecular biology provide a power- taxonomic methods is difficult for non-specialists ful means to determine whether organisms belong and requires expert knowledge of the group; to a single evolutionary lineage or interbreeding molecular identification keys based on targeted unit. Analysis of gene genealogies using coales- DNA sequences can provide a valuable identifica- cent theory can be used to identify single lineages. tion system for such groups, as for example for Individual organisms differ in the DNA sequences species of thrips in the genus Scirtothirps. Molecu- that make up their genomes and differentiation lar diagnosis is a great motivation for recent initia- between species is based on mutations in the tives in DNA barcoding in which a standard genes that accumulate through time. Because any section of DNA, typically part of mitochondrial given allele in an organism derives from an allele cytochrome-oxidase I, is used to identify species. in an ancestor, DNA data have the potential to define the genealogies of genes and infer phylogenetic relationships of taxa. Molecular genetic data The Species Concept can also help to understand the nature of biological species, as well as the extent and causes of There has been considerable debate in the litera- intra-specific variability, including ecotypes, host ture concerning the most appropriate definition races, or phenotypically adapted forms. of species. Classically, species are described on the basis of morphological characters, and the common basis for species identification is the Molecular Methods for Diagnosis presence of one or more fixed or non-overlapping differences. If these differences are both shared The analysis of DNA is an increasingly impor- and derived, the groups are considered phyloge- tant tool in studies of insects, particularly for netic species. However, morphological data alone systematics and population biology. DNA has may be inadequate for defining species bound- several significant features that make it espe- aries. For example, two species may be sympatric cially useful: (i) the genotype rather than the in range (overlapping) or parapatric (abutting), phenotype is assayed; (ii) one or more loci but be so similar in morphology that their spe- appropriate to a problem can be selected on cific status goes undetected. Conversely, mor- the basis of evolutionary rate or mode of inheri- phological variation may be so great in one tance, (iii) the methods are applicable to all species, that identification of single biological developmental life stages and both sexes, and unit is difficult. (iv) DNA can be prepared from small amounts Molecular Diagnosis M 2451 of tissue and is relatively stable, even in tissues randomly throughout the genome. Although that are not stored cryogenically (deep frozen). fingerprinting and fragment approaches offer less One reason for the success of molecular diagno- resolution than nucleotide sequencing in some sis is the use of the polymerase chain reaction respects, they are powerful and cost-effective alter- (PCR) in which specific stretches of DNA are natives where large numbers of individuals or amplified, allowing the development of fast large segments of a genome are being screened. In and sensitive molecular techniques. As a result, general, these techniques have the great advantage only a small portion of the insect is needed for that they can be applied to systems where there is molecular diagnosis. no prior molecular information about particular Two major classes of DNA-based approaches loci. Multi-locus markers are often detected by are used in taxonomy. The first involves compari- annealing primers of arbitrary short sequences son of nucleotide sequences for a particular locus during PCR amplification and looking for species- or loci, usually amplified by PCR. The DNA diagnostic bands among the array of randomly sequence variation can be examined directly fol- amplified fragments, as in the method of randomly lowing automated DNA sequencing. This is the amplified polymorphic DNA (RAPDs). More approach used in DNA barcoding. Sequence vari- complex and more reliable methods use a combi- ation can also be assessed indirectly by comparing nation of restriction enzymes and PCR, as is the electrophoretically homologous DNA fragments case of amplified fragment length polymorphisms to look for variation in number, size or conforma- (AFLPs). The most widely used markers for popu- tion. In a method termed restriction fragment lation genetics of insects are now microsatellites, length polymorphism (RFLP), a PCR product is which are non-coding sections of repeated small first generated and then digested to completion motifs of a few base pairs. Microsatellites are with a restriction enzyme to yield a species-spe- repeatable and can be sufficiently variable for use cific pattern of bands that can be visualized on a in many types of population studies including gel. Another powerful technique, allele specific studies of the origins of individuals, population amplification (ASA), is based on the fact thatTher - structure, and hybridization. Typically, microsatel- mus aquaticus (Taq) DNA polymerase will only lite loci must be developed anew for each new extend primers that are matched to their template species, or set of closely related species. DNA and will not extend primers that do not There is a trade-off between the detailed match the template DNA. PCR primers can there- information that can be obtained by sequencing fore be designed so that they only match one allele the DNA at one or a few loci and the more abun- and, providing that the allele is specific to a spe- dant, though less detailed, information that can cies, a PCR product will only be generated be obtained through studies of restriction sites, with the primer matching the genomic DNA of fingerprinting, or microsatellite analysis. For the corresponding species. Other approaches for most population genetic analyses the power of a assessing similarity of sequences are based on statistical test increases with the number if loci the fact that the presence of point mutations of the examined. Towards this end, single nucleotide nucleotide sequence that differ among species polymorphisms (SNPs) provide the smallest will affect the tertiary conformation of the DNA possible (and potentially the greatest number) of molecule. genetic loci, but to date studies involving SNPs The second class of approaches used in DNA have only been possible for organisms where taxonomy is so-called DNA fingerprinting or frag- there is some prior genomic information that can ment analysis. Each of these methods simultane- help to guide the discovery of loci, such as ously screens many different DNA regions or through whole genome sequencing. Initially fragments, which are thought to be distributed whole genomes were available only for a select 2452 M Molecular Diagnosis group of model organisms, including species of Drosophila, mosquitoes, and the honey bee. How- ever, in the last few years many new projects have made available the genome sequence of more insects and other arthropods (e.g., ticks and spider mites) and the list of these species is continuously increasing. Currently, advances in sequencing technology and bioinformatics are revolutionizing the production of genomic sequence data; accordingly, in the not too distant future whole genomes will be available for a wide spectrum of species. Selecting the sequence or markers to be analyzed is the first decision to be made in designing any molecular systematic or population genetic study, whether it concerns DNA sequences or fragment variation. In broad terms, choices are made according to evolutionary rate and mode of inheritance. The ribosomal DNA (rDNA) and the mitochondrial DNA (mtDNA) have been the most commonly used genomic regions for systematic studies of animals. The processes governing the evolution and inheritance of mtDNA and rDNA are now well understood and have an impact in their relative performances for systematic inference. For example, the two very closely related but reproductively isolated spider mite species, Tetrany- chus urticae and T. turkestani are polyphyletic for mtDNA but monophyletic for rDNA. The Molecular Diagnosis, Figure 80 Identification influence of life history, mainly haplodiploidy of a tephritid fruit fly species using DNA of these species and their female-biased sex- barcoding. In this example, fly eggs from an ratio, might explain this apparent contradiction. unknown species were found in fruits that Another fundamental to establish synonymy were intercepted at the border in New Zealand. between presumed species choice is whether Because the eggs of tephritid fruit flies are information concerning the phylogeny of the not possible to identify to species alleles is necessary; some techniques (e.g., morphologically, similarity in mitochondrial RAPDs, AFLPs, microsatellites, SNPs) provide DNA COI was used to match the intercepted information only on the latter. Recent develop- eggs (noted as “new capture”) with DNA from ments in population genetic theory use infor- known voucher specimens. In this example, mation on allele relationships as well as their the unknown species was identified as distribution to combine inferences about popu- Bactrocera xanthodes. (Data used with lation structure and history. However, for spe- permission of Karen Armstrong, Lincoln cies diagnosis, information on allele frequency University, New Zealand; for additional distributions may suffice. examples, see Clarke et al., 2005.) Molecular Diagnosis M 2453

Molecular Diagnosis, Figure 81 The morphological characters classically used to separate Tetranychus species are presented for T. pueraricola: a = female dorsum; b = lobes on dorsa hysterosomal striae of female (schematic); c = distal palpus segment of female; d = distal palpus segment of male; e = female peritreme; and f–i = aedeagi. Comparison of T. peuraricola aedeagi (f–i) with T. urticae aedeagi (j–l) illustrates the difficulty in separating the two species by morphological criteria alone. (Data used with permission of Tetsuo Gotoh, Ibaraki University, Japan.)

sequence from a standardized and agreed-upon DNA Barcoding position in the genome for molecular diagnosis and identification at the species level. For most DNA barcoding is the use of a short DNA animals, including insects, the cytochrome C 2454 M Molecular Diagnosis insects. Within species, COI sequence variability is typically very low, making it useful as a species diagnostic marker. Species are identified based on the similarity of COI sequences to known voucher specimens. However, the widespread use of DNA barcoding has been controversial, particular in its application to systematics. Accordingly, it is now well recognized that additional loci and other sorts of biological data will be necessary for applications in evolutionary and population biology that involve systematics or studies of complex population histories including hybridization (Figs. 80–82).

References

Avise JC (2004) Molecular markers, natural history and evolution, 2nd ed. Chapman and Hall, New York Behura SK (2006) Molecular marker systems in insects: current trends and future avenues. Mol Ecol 15:3087–3113 Molecular Diagnosis, Figure 82 Molecular Bickford D, Lohman DJ, Sodhi NS, Ng PKL, Meier R, diagnosis of two closely related species of Winkler K, Ingram KK, Das I (2007) Cryptic species as a window on diversity and conservation. Trends Ecol agricultural mite pests, Tetranychus urticae and Evol 22:148–155 Tetranychus pueraricola, which are impossible Caterino MS, Cho S, Sperling FAH (2000) The current state of to separate by morphological criteria. Shown insect molecular systematics: a thriving tower of Babel. Annu Rev Entomol 45:1–54 is a PCR-RFLP test in which the second internal Clarke AR, Armstrong KF, Carmichael AE, Milne JR, Raghu S, transcribed spacer (ITS2) of the ribosomal DNA Roderick GK, Yeates DK (2005) Invasive phytophagous has been PCR amplified and digested by the pests arising through a recent tropical evolutionary restriction enzyme RsaI for the two species. In the radiation: the Bactrocera dorsalis. complex of fruit flies. Annu Rev Entomol 50:293–319 figure, RsaI digestion of the PCR-amplified ITS2 Excoffier L, Heckel G (2006) Computer programs for popula- derived from the DNA of a single mite clearly tion genetics data analysis: a survival guide. Nat Rev shows that T. urticae sequence produces 3 Genet 7:745–758 fragments (implying 2 recognition sites of the Gomez-Zurita J, Galian J (2005) Current knowledge on genes and genomes of phytophagous beetles (Coleoptera: enzyme; lane 2), while the restriction profile of Chrysomeloidea, Curculionoidea): a review. Eur J Ento- T. pueraricola yields only 2 fragments (implying a mol 102:577–597 single recognition site; lane 3). In lane 1 the “100 Gotoh T, Gutierrez J, Navajas M (1998) Molecular comparison of the sibling species Tetranychus pueraricola. Ehara base pair (bp) ladder” size marker is shown. & Gotoh and T. urticae Koch (Acari: Tetranychidae). Entomol Sci 1:55–57 Krzywinski J, Besansky NJ (2003) Molecular systematics of oxidase subunit 1 mitochondrial region (COI) Anopheles.: from subgenera to subpopulations. Annu has become the standard barcode region. Because Rev Entomol 48:111–139 of conserved genetic regions flanking this gene Luikart G, England PR, Tallmon D, Jordan S, Taberlet P (2003) The power and promise of population genom- and because it is so abundant within individuals, ics: from genotyping to genome typing. Nat Rev Genet the COI gene sequence is easily obtained from 4:981–994 Mompha Moths (Lepidoptera: Momphidae) M 2455 Manelm S, Gaggiotti OE, Waples RS (2005) Assignment meth- Molt ods: matching biological questions with appropriate techniques. Trends Ecol Evol 20:136–142 Navajas M, Boursot P (2003) Nuclear ribosomal DNA mono- To shed or cast off the outer body covering, a nec- phyly versus. mitochondrial DNA polyphyly in two essary prerequisite to grow and attain the adult closely related mite species: the influence of life history stage. The period of molting is a vulnerable stage and molecular drive. Proc R Soc Lond B (Suppl) 270:S124–S127 for insects, as they are susceptible to desiccation Navajas M, Gutierrez J, Williams M, Gotoh T (2001) Synon- and easy prey for predators. ymy between two spider mite species, Tetranychus kanzawai. and T. hydrangea, shown by ribosomal ITS2 sequences and cross-breeding. Bull Entomol Res Molting Fluid 91:117–123 Noor MAF, Feder JL (2006) Speciation genetics: evolving approaches. Nat Rev Genet 7:851–861 An enzyme-rich fluid secreted into the apolysial Robinson GE, Evans JD, Maleszka R, Robertson HM, space by the epidermal cells. The molting fluid Weaver DB, Worley K, Gibbs RA, Weinstock GM (2006) Sweetness and light: illuminating the honey bee genome. consists of proteinases and chitinases that digest Insect Mol Biol 15:535–539 the endocuticle during molting. The molting fluid Rosenberg NA, Nordborg M (2002) Genealogical trees, is reabsorbed through the epidermal cells shortly coalescent theory and the analysis of genetic polymor- before ecdysis in many insects, though in some phisms. Nat Genet 3:380–390 Rugman-Jones PF, Hoddle MS, Mound LA, Stouthamer R insects the new instar apparently swallows the old (2006) Molecular identification key for pest species of fluid. Scirtothrips. (Thysanoptera: Thripidae). J Econ Entomol 99: 1813–1819 Savolainen V, Cowan RS, Vogler AP, Roderick GK, Lane R (2005) Towards writing the encyclopaedia of life: an Molting Hormone introduction to DNA barcoding. Philos Trans R Soc Biol Sci 360:1805–1811 A homone regulating molting in insects. Also Schlötterer C (2004) The evolution of molecular markers–just a matter of fashion? Nat Rev Genet 5:63–69 called ecdysone.

Molecular Genetics Mompha Moths (Lepidoptera: Momphidae) Genetic studies that focus on the molecular nature of genes and gene expression. John B. Heppner Florida State Collection of Arthropods, Molecular Phylogeny Gainesville, FL, USA

An analysis of the relationships of groups of organ- Mompha moths, family Momphidae, total 127 isms as reflected by the evolutionary history species worldwide, with about half from the detected in molecules (proteins, DNA). Palearctic. The family is part of the superfamily Gelechioidea in the section Tineina, subsection Tineina, of the division Ditrysia. Adults small Molicutes (8–18 mm wingspan), with head smooth-scaled; haustellum scaled; labial palpi recurved; maxil- A class of wall-less microorganisms, surrounded lary palpi small, 3-segmented. Wings elongated by a membrane, and related to bacteria. They are and hindwings mostly lanceolate with long small, gram-negative, and highly variable in fringes (Fig. 83). Maculation often white with appearance. golden iridescent markings, or darker with 2456 M Momphidae Monarch Butterfly, Danaus plexippus L. (Lepidoptera: Danaidae)

Thomas c. Emmel, Andrei Sourakov University of Florida, Gainesville, FL, USA

The monarch is one of the world’s best-known butterflies. Its distribution is among the widest for Mompha Moths (Lepidoptera: Momphidae), any butterfly species. Not only it is found through- Figure 83 Example of mompha moths out the Americas, including the islands of the West (Momphidae), Mompha eloisella (Clemens) from Indies, but it reaches as far as Australia and New Florida, USA. Guinea, and occasional individuals migrate to Western Europe.

various marks. Adults mostly diurnal or crepus- The monarch butterfly is native to tropical cular. Larvae mostly leafminers, but some are America where populations breed throughout the borers in flowers and stems, or gall makers. year. These sedentary populations are different Hosts are only known in Onagraceae. from the migratory North American ones and bear separate names. For example subspecies, megalippe Hübner is found in Mexico and Central References America and southeastern United States. The southern South American subspecies is called menippe Hübner. Several subspecies have also Bradley JD (1951) A comparative study of four European species, including one new species from Britain, belong- been described from the islands in the Caribbean. ing to the genus Mompha Huebner, (Lepidoptera: None of these geographic races are “pure,” with Lavernidae). Entomol Gaz 2:173–182, pl. 5 occasional individuals of the migratory subspecies Hodges RW (1992) Two new species of Mompha from Cali- fornia (Lepidoptera: Momphidae). J NY Entomol Soc phenotype, D. plexippus plexippus, found in all of 100:203–208 them. It has even been suggested, yet not proven, Riedl T (1969) Matériaux pour la connaissance des Momphi- that sedentary subspecies might indeed prove to dae paléarctiques (Lepidoptera). Part IX. Revue des be separate sibling species. Due to the versatility of Momphidae européenes et compris quelques espéces d’Afrique du Nord et du Proche-Orient. Polsk Pismo its weedy host plants – the milkweeds – and its Entomol 39:635–919 ability to cover large distances, this highly adapt- Riedl T, Popescu-Gorj A (1974) Catalogue of the Momphi- able butterfly occupies a variety of ecological dae (Lepidoptera-Gelechioidea) from the collections zones, but is found mostly in open sunny areas. In of the Natural History Museum “Grigore Antipa” of Bucharest. Trav Mus Natl Hist Nat Grigore Antipa Costa Rica, for example, monarchs fly from sea 14:273–298 level up to 2,500 meters in elevation and are particularly common above 1,500 meters. Though the monarch male has been observed Momphidae to exhibit a basic kind of courtship behavior, wig- gling in its flight while approaching a female, the A family of moths (order Lepidoptera). They com- essence of the mating “ritual” in this species can be monly are known as mompha moths. described as “rape.” Copulation involves the male  Mompha Moths grasping the female with its legs in flight and bring-  Butterflies and Moths ing the female down from the air to the ground in Monarch Butterfly, Danaus plexippus L. (Lepidoptera: Danaidae) M 2457 order to clasp her abdomen with the external genita- California. There, they hang in trees such as coastal lia. The white eggs are laid singly on the flowers or groves of pine, cypress, redwood, and the intro- the underside of the leaves of one of the many milk- duced Australian eucalyptus trees in clusters or weed species, and larval feeding commences imme- colonies of several hundred to several tens of diately upon hatching; there is no diapause stage, thousands of individuals from late fall to early except that adults on the overwintering sites go into spring. Some overwintering colonies have recently reproductive diapause. Toxicity of the milkweeds been discovered in Saline Valley, north of Death of varies and so does toxicity of resulting butterflies, Valley in the eastern desert areas of California, as has been demonstrated through bird-feeding while other population movements through experiments. The striped larvae with two pairs of southern Nevada and Arizona suggest that there tentacles (the elongate tubercles, the function of are still as yet undiscovered overwintering sites in which remains unknown) develop into green, gold- northern Mexico for these western monarchs. studded pupa within two weeks. The larvae from the East of the Rocky Mountains, Canadian and Caribbean island of Hispaniola show much wider U.S. monarchs move south to the Gulf Coast where black stripes than these of the North American the vast majority turn southwest and enter Mexico population. Differences in length of tentacles and across the Texas border, flying south by the hun- abundance of gold coloration in pupae have also dreds of billions. They ascend the Sierra Madre de been recorded between the migratory population Oriente into the Central Plateau and eventually and one in Jamaica. Overall, though it was one of end up in the high coniferous forests of the Trans- the earliest butterflies to acquire its scientific name verse Neovolcanic Belt of central Mexico, princi- (Linnaeus, 1758), the taxonomy of Danaus plexippus pally within the states of Mexico and Michoacan. remains a widely debated issue. The existence of an over-water pathway used by eastern Monarchs has been documented recently. They fly across the Gulf of Mexico between the Monarch Migration southwest coast of Louisiana to the northeast coast of Tamaulipas, Mexico, an over-water flight of 400 At some time in the relatively recent past, probably miles. In addition, some monarchs are known to during the Pleistocene advances and retreats of fly to various points on the northern Florida coast great glacial masses across the northern areas of (from which they may still cross the Gulf of temperate North America, a subset of the North Mexico) or to south Florida, from which they may American monarch population began its marvel- fly to overwinter in Cuba. Most of the eastern ous annual movements. Its movements represent a monarchs, flying in a south-southwesterly direc- true migration, involving a periodic movement tion, take advantage of southward moving cold from a given area and a return to that area, and fronts. The stored fat allows for only 11 h of wing- likely evolved to exploit dozens of seasonally avail- flapping flight, or 44 h of cruising flight, but thanks able milkweed species north of the tropics. Migra- to the frequent tail winds, monarchs use soaring tion apparently is triggered by changes in flight that allows for a theoretical transit distance temperature in an ultimate sense and perhaps to exceed 1,000 km on their available energy changes in photoperiod in a proximate sense. sources without refueling. In actual fact, monarchs Typically, the monarch populations across the feed heavily during migration, and arrive at the North American continent begin moving in a gen- overwintering sites with more stored fat than when erally southerly direction starting each fall around they started. Migratory monarchs have been September 1. West of the Rocky Mountains, these observed flying at altitudes as high as 11,000 feet populations move primarily to about 129 sites above the land and individuals normally fly along the Pacific coast of California and Baja 11–12 h, covering 200–400 miles a day. Much of 2458 M Monarch Butterfly, Danaus plexippus L. (Lepidoptera: Danaidae) our understanding of the movement rates and due to heavy feeding on desert flowers as they fly migratory pathways followed by the monarchs south through the Central Plateau. Adequate lipid have been revealed by tagging programs, initiated energy reserves are essential for passing the win- in 1952 by F.A. Urquhart at the Royal Ontario ter successfully. Spring monarchs are severely Museum in Toronto, Canada, and subsequently depleted of fat reserves (fat accounts for only 37% taken up by hundreds of other workers. The maxi- of dry weight in March) and they need to feed mum distance traveled by a single tagged monarch heavily during their spring northward movement is 2,595 miles (from New Brunswick, Canada, to to successfully reach the United States again and the Cerro Pelon colony in Michoacan). reproduce. Once the monarchs arrive at their overwin- The monarch movements represent the tering sites, they remain largely quiescent for a world’s greatest modern animal migration, period of 4.5 months, until late the following involving the movements of at least one billion March. They may leave the colony area briefly to individual monarchs annually and perhaps as drink water or nectar but return the same day many as three billion in some years. The orienta- (often in the same hour or two) to their trees. The tion ability of the monarchs to move nearly 3,000 overwintering butterflies remain reproductively miles and arrive precisely at a point to which they inactive with the diapause being terminated in have never been before (at the end of the fall late March by the combined influence of temper- migration) is only beginning to be understood. A ature and photoperiod onto the monarchs’ neuro- remarkably accurate sun compass mechanism endocrine system. In the last ten days of March, keeps the monarchs on their general bearing. the Monarchs become increasingly active, mate at Considerable evidence also exists for orientation the colony site and then take off again for the by magnetic fields. The Mexican Transvolcanic north. These same individuals who flew south in Range where the largest overwintering colonies the fall return in a generally northward direction exist contains magnetic anomalies a hundred to recolonize the North American continent for times stronger than other surrounding terrain, the summer. The adults from the Mexican colo- due to heavy metallic ore deposits. The presence nies are known to reach the southern boundary of of magnetic materials in the monarchs’ head and the United States by early April, lay their eggs, and thorax has been demonstrated, significantly then die. The eggs are laid on newly leafed out exceeding magnetite contained in its non-migra- milkweed plants and growth is rapid. The first tory relatives. Scent may be involved in locating generation of adults for the new year emerges in the exact trees that their ancestors used the year late April, flies north through the middle tier of before. The odor must come from billions of states and lays eggs throughout the area. The sec- scales and perhaps scent molecules which still ond generation of adults emerges by late May or remain on the evergreen firs into the fall months, early June and again flies northward. A third and following the spring departure of their predeces- fourth annual generation may emerge by the end sors. Almost equally remarkable is the ability of of August. At this point, third, fourth and even the monarch colony to adjust its exact position fifth generation adults of the original northward on the mountain slope in elevation above sea moving migrants prepare to move south, over a level, height in tree, and even position on tree path that they have never followed themselves. trunks and fir boughs daily to compensate for Physiologically, monarchs have to build up changes in weather, nightly temperature minima, fat protein reserves for the migration. However, fluctuating insulation values in cloud cover, etc. they arrive on the overwintering sites with even Migration of the monarchs is truly one of more lipid reserves than they started with; this the natural wonders of the world, a phenome- increase (up to 73% of their dry body weight) is non equal to none and one that richly deserves Monarch Butterfly, Danaus plexippus L. (Lepidoptera: Danaidae) M 2459 preserving for posterity. It impressed the early bacterium Bacillus thuringiensis (known as Bt civilizations: images of monarchs were carved in corn), once fallen on the milkweeds adjacent to the ancient stonework at the San Juan Teotihua- corn fields and ingested by the monarch cater- can archeological site north of Mexico City more pillars, causes the death of the latter. Studies are than 1,300 years ago. It continues to impress us underway to estimate the effect this phenome- now, with monarchs remaining the most popular non might have on monarch populations. How- insect in modern North American cultures. ever, it is known that field margins and hedgerows have been the monarchs’ breeding grounds in the highly developed environment Conservation Concerns of the North American Great Plains, and losing this breeding environment might indeed prove The greatest threat to the monarch is not the to be detrimental for the migratory population. direct destruction of the butterfly species but the destruction of its overwintering habitat sites. Along the California coast, where the species once Monarchs Among Other Butterflies ranged from Mendocino County southward 650 miles to Baja California, a great many sites have The Jamaican monarch,Danaus cleophile (Godart), been destroyed or severely altered by develop- is a smaller species found in the highlands of ment. In Mexico, a number of the high mountain Jamaica and Hispaniola. Remarkably, to date noth- sites (10,000 to over 11,000 foot elevation) are ing is known about the life history of this colorful, being threatened by logging, firewood gathering, though much less glamorous, butterfly. Danaus forest thinning by fires, and clearing for agriculture. Forest thinning opens the colony sites to severe winter storm effects, colder temperatures, and restriction of available area to shift the colony site if environmental conditions change. The Mexican government on both federal and state levels has responded with declarations of pre- serves, parks, and protection for the butterfly. Most of the protection, however, depends on the ejidos or associations of local communities that only recently have begun to recognize the economic benefits of ecotourism. monarch colonies today attract hundreds of thousands of visitors annually from throughout Mexico and abroad. Though tourism creates economic incentives for conserving the forest around the colonies, development of permanent trails with concrete steps up the mountains and hundreds of shops and small restaurants also take their toll on the environment. Another, recently emerged concern is tied Monarch Butterfly, Danaus Plexippus L. to genetically engineered crops in the U.S. It (Lepidoptera: Danaidae), Figure 84 Aggregations appears that the pollen from Lepidoptera pest- of overwintering monarchs in northern Mexico resistant corn plants that contain genes of the (photo T. Emmel). 2460 M Monarch Butterfly, Danaus plexippus L. (Lepidoptera: Danaidae)

Monarch Butterfly, Danaus Plexippus L. (Lepidoptera: Danaidae), Figure 85 Eggs (left), larvae (middle), and pupae (right) of monarchs in Florida (photo A. Sourakov).

Monarch Butterfly, Danaus Plexippus L. (Lepidoptera: Danaidae), Figure 87 Viceroy, Limenitis archippus, a Müllerian mimic of monarch, Florida (photo A. Sourakov).

Within the subfamily Danainae, all monarchs belong to the tribe Danaini, subtribe Danaina, genus Danaus Kluk. None of the other 11 species in the genus is migratory. However, Anetia panth- Monarch Butterfly, Danaus Plexippus L. rata (Martyn), a primitive danaeine from Hispan- (Lepidoptera: Danaidae), Figure 86 Mature larva iola, recently has been found to aggregate by the of monarch from Dominican Republic has much hundreds on pine trees in the highest mountains darker coloration than this of migratory monarch of Hispaniola. (photo A. Sourakov). Almost all danaines, monarchs included, form aggregations of dozens of adult individuals that cleophile is an extremely local and relatively rare feed on alkaloid-rich plants such as Boraginiaceae island isolate that flies in the montane areas of the and Fabaceae (Fig. 84). The alkaloids play a role in islands, ovipositing almost exclusively on Asclepias pheromone production. It also has been suggested nivea. As far as is known, it is non-migratory. that they might contribute to the butterflies being Monoculture M 2461 toxic to the predators, though most of this toxicity Moniliform has been attributed to larvae incorporating the substances called cardenolides from the milkweed Composed of round or elongate segments and host plants (Figs. 85 and 86). resembling the beads of a necklace. This term usu- The unpalatability of monarchs and other ally is used to describe the form of certain danaeines accounts for their bright aposematic antennae. coloration designed to repel potential predators. Several other butterfly species exhibit coloration similar to that of monarchs, though they are not Monitoring related to them. Monarchs, being a very common distasteful species, are thought to serve as Careful observation of pest abundance and a model in various mimicry complexes. For damage. Pest scouting. example, mimicry between monarchs, queens (Danaus gilippus (Cramer)), and viceroys (Lime- Monkey Grasshoppers nitis archippus (Cramer)) (Fig. 87), is a textbook example of such a mimicry complex. All three A family of grasshoppers (Eumastacidae) in the of these species are toxic and supposedly com- order Orthoptera. bine their efforts to leave an imprint of their  Grasshoppers, Katydids and Crickets wing pattern in the memory of a bird that has the misfortune of tasting them. In the case of the viceroy, which occasionally is eaten by birds, Monoclonal Antibody but not to the extent “normal” palatable butterflies are eaten, the toxic compounds must result A single antibody produced in quantity by cul- from toxic substances contained in its host tured hybridoma cell lines. plant, the willow (Salix spp.). Such complexes where the model and the mimic are both distasteful are called Müllerian (vs. a Batesian com- Monocondylic Articulation or plex, in which only the model is toxic, while the Joint mimic is perfectly palatable).  Butterflies A joint with a single point of articulation between  Butterflies and Moths adjacent segments. Having one condyle.  Conservation of Insects  Condyle  Mimicry  Legs

References Monocot A plant with seedlings having a single cotyledon. Ackery P, Vane-Wright RI (1984) Milkweed butterflies: their cladistics and biology. Cornell University Press, Ithaca, Most monocots are grasses. (contrast with dicot) NY, 425 pp Browser LP (1995) Understanding and misunderstanding the migration of the monarch butterfly (Nymphalidae) Monoculture in North America 1857–1995. J Lepidopterists Soc 49:304–385 Browser LP (1996) Monarch butterfly orientation: missing A uniform or homogeneous planting of a crop pieces of a magnificent puzzle. J Exp Biol 199:93–103 over a large area. 2462 M Monoecious Monoecious Monophyletic

In botany, having sexual parts of both genders in This refers to a group consisting of the ancestral one individual plant, i.e., hermaphroditic. In ento- form and all the descendants of that ancestor. mology, infrequently and confusingly used as a  Phylogenetics synonym of monophagous – best not used in this sense. Monophyletic Group

Monogyny Taxa that are believed to contain all the known descendents of a single stem-species.  The existence of only a single functional queen in Phylogeny a nest. (contrast with polygyny) Monotomidae

Monomachidae A family of beetles (order Coleoptera). They commonly are known as root-eating beetles. A family of wasps (order Hymenoptera).  Beetles  Wasps, Ants, Bees and Sawflies

Monotypic Monommidae This generally means that a taxon contains only A family of beetles (order Coleoptera). They com- one subdivision. A family, for example, could have monly are known as opossum beetles. only one genus, or a genus could have only one  Beetles species.

Monomorphic Mordellidae A family of beetles (order Coleoptera). They com- Occurring in only one form. monly are known as tumbling flower beetles.  Beetles Monomorphism Morgan, Thomas Hunt Among social insects, the existence of only a single worker subcaste in a colony. T.H. Morgan was born at Lexington, Kentucky, USA, on September 25, 1866. He received a B.S. degree in 1886 from the University of Kentucky, Monophagous and a Ph.D. in 1890 from The Johns Hopkins University. He served on the faculty at Bryn Mawr An insect that feeds only on a single species of College from 1891 to 1904, at Columbia Univer- plant or animal. sity from 1904 to 1928, and at the California Mormon Cricket, Anabrus simplex Haldeman (Orthoptera: Tettigoniidae) M 2463 Institute of Technology from 1928 to 1945. Mor- name is likely derived from its appearance, which gan initially worked in descriptive embryology, (at high densities) is blackish and nearly wingless, but soon switched to experimental embryology. giving it the appearance of a field cricket. The other He then moved to genetics, and worked with portion of its common name has its origin in the Drosophila, aphids and phylloxerans. This was an early history of Utah. Destruction of crickets in important era, in that he demonstrated that the 1848 by California gulls, Larus californicus, saved chromosome theory of sex determination was the early Mormon settler’s grain crops; a fact com- operable in these complex life cycles. His work memorated by a large statue in Salt Lake City. with Drosophila is perhaps best known, and he discovered exchange between homologous chromosomes, and linkage between sex-linked genes. Distribution Morgan’s pioneering work laid the groundwork for the chromosome theory of heredity. He also Mormon cricket is native to western North was first and foremost an experimentalist, and America. Mormon cricket occurs widely, with a had little patience for anything less than scien- range that includes southern British Columbia to tific evidence. His work largely supported Dar- Manitoba in the north, and south to northern win’s theories of evolution. He served as president California and northern New Mexico. As a per- of the National Academy of Sciences and the sistent pest, however, its range is limited to the American Association for the Advancement of Rocky Mountain and Great Basin regions. Science, and was a Nobel laureate. He died at Pas- adena, California, on December 4, 1945. Host Plants

References Mormon cricket and coulee cricket are often considered to be omnivorous, but despite their wide Muller HJ (1946) Thomas Hunt Morgan 1866–1945. Science host range they display some specific preferences 103:550–551 until confronted by starvation. Virtually all field Sturtevant AH (1946) Thomas Hunt Morgan. Am Nat 80:22–23 crops and vegetable crops can be consumed, but due to the nature of the cropping systems in the areas inhabited by these crickets, alfalfa and wheat Moribund are most often injured. Over 400 species of native grasses, forbs, trees A lethargic or immobile state, usually immediately and shrubs are reported to be eaten by Mormon preceding death. cricket. Most of these records occurred during the arid “dust-bowl” era of the 1930s when cricket densities were extremely high. Thus, they are not Mormon Cricket, Anabrus simplex typical of cricket feeding behavior. Crickets often Haldeman (Orthoptera: feed preferentially on the flowers and seed-heads Tettigoniidae) of plants, ignoring the leaf material. Seed-head consumption is especially pronounced in grasses, John L. Capinera though grasses are a minor component of cricket University of Florida, Gainesville, FL, USA diet. Forbs such as bitterroot, Lewisia rediviva; wild onion, Allium spp.; arrowleaf balsamroot, Despite its common name, the Mormon cricket is Balsamorhiza sagittata; wild mustard, Brassica not a cricket, but a katydid. Part of its common spp.; tumblemustard, Sisymbrium altissimum; and 2464 M Mormon Cricket, Anabrus simplex Haldeman (Orthoptera: Tettigoniidae) lupine, Lupinus spp.; are preferred by nymphs. In with any degree of frequency, and although levels the adult stage, crickets eat mostly big sagebrush, of up to 50% parasitism have been reported, it is Artemisia tridentata. In an analysis of Mormon usually quite low. The parasitoids responsible for cricket diet in Colorado, the diet consisted of: attacking eggs are Sparaison pilosum Ashmead 50% forbs, 21% arthropods, 16% fungi, 6% grasses, (Hymenoptera: Scelionidae) and Oencyrtus anab- 5% clubmoss, and 2% grasslike plants. rivorus (Hymenoptera: Encyrtidae). As suggested from the Colorado dietary anal- Pathogens vary greatly in their effect on crick- ysis, crickets actively prey on other insects, includ- ets. The microsporidian Heterovesicula cowani ing cicadas, ants, aphids, and beetles if they have (Vairimorpha) can naturally infect substantial the opportunity to catch them. They are quick to proportions of Mormon cricket populations, and consume injured or dead crickets as well, and one causes rapid mortality when young crickets ingest of the distinctive characteristics about these crick- spores. Heterovesicula appears to be the most ets is their tendency to stop and feed on comrades important pathogen of crickets. The nematode that have been crushed on roadways by vehicles. Agamaspirura anabri (Nematoda) and the horse- Because the healthy crickets remain on the high- hair worm Gordius robustus (Nematomorpha) ways to feed on fallen crickets, they often become have also been observed in crickets. Gordius was crushed also, resulting in long, dark, greasy road reported to be quite common in crickets near slicks consisting of pulverized crickets. standing water because part of the horsehair worm’s life cycle takes place in water; unfortunately, water is not plentiful in the habitat of these Natural Enemies crickets.

Predators are perhaps the best known mortality factor associated with crickets. Gulls are not the Life Cycle and Description only vertebrates attracted to these insects when they become numerous, and among the avian Normally there is one generation per year. Eggs predators most commonly observed feeding on overwinter, with egg hatch occurring in March– crickets are crows, Corvus brachyrhynchos May, often while snow remains on the ground. brachyrhynchos; hawks, Falco spp. and possibly The nymphs are present until June when adults others; meadowlarks, Sturnella neglecta; and begin to emerge and begin egg production. Adults blackbirds, various spp. (Wakeland 1959). Mam- usually perish by late August, often earlier. The mals such as coyotes, Canis latrans; ground combined nymphal and adult development time squirrels, Citellus spp.; and kangaroo rat, requires about 100 days Dipodomys spp.; also feast on crickets when they are abundant. Also, the wasps Palmodes laeviven- tris (Cresson) and Tachysphex semirufus (Cres- Egg son) (both Hymenoptera: Sphecidae) capture crickets and feed them to their young. Despite The egg is elliptical in shape and measures the frequency at which predation is observed, about 7–8 mm in length and 2.0–2.5 mm in there is little evidence that predators are nor- width. Initially brown in color, it soon turns mally effective at maintaining crickets at low whitish and then gray. Eggs are deposited in the densities, or capable of suppressing crickets dur- soil singly or in small clusters at a depth of ing periods of population outbreak. 6–25 mm during the summer, where they Parasitism is surprisingly uncommon in remain until spring. Sometimes eggs are depos- cricket populations. Only the egg stage is parasitized ited around the base of plants, but more often Mormon Cricket, Anabrus simplex Haldeman (Orthoptera: Tettigoniidae) M 2465 bare soil is favored, including the mounds of Adult ants. Females deposit, on average, about 85 eggs, but up to 160 per female has been observed. The adult is very similar to the mature nymph in Eggs are ready to emerge early in the spring, form and color but larger, measuring 35–45 mm in and begin to hatch when soil temperatures length. Also, the sword-shaped ovipositor of the attain about 5°C, a much lower temperature adult female is longer (Fig. 88), and the short wings than grasshoppers. of the adult male protrude from beneath the pronotum and are used as a stridulatory organ. As is the case with nymphs, the adults will cluster under Nymph shelter during the evening and during inclement weather. They will also climb into bushes to escape Upon hatching from the soil, the nymphs are the hot soil during excessively warm weather. dark in color, resemble the adults in form, and Adults continue to move in bands in the same measure about 6 mm in length. There are seven manner as nymphs, stopping only to eat and instars, and by the time they attain the last instar oviposit. they are about 30 mm in length. The initial Reproduction commences 10–14 days after instars are black with white along the lateral attaining the adult stage. Males call from perches edge of the posterior end of the pronotum, and on vegetation during the morning hours. Females the ovipositor of the female is not apparent. As compete for the attention of males, mount the they attain the fourth instar, however, they males, and are inseminated. Males are selective in acquire green, red, purple, or brown color and their choice of partners, often choosing the largest in the female the ovipositor becomes increas- female with which to mate. During insemination, ingly obvious. Mean duration of development the male provides the female, attached to the sac period of crickets cultured at 21–26°C is 9.5, containing sperm, a large proteinaceous mass that 7.4, 5.1, 6.5, 5.6, 5.6, and 10.4 days, respectively, protrudes from her genital opening. While the for instars 1–7. Thus, the mean total develop- sperm is draining into the female’s reproductive ment time of nymphs is estimated at 50 days, system the proteinaceous mass provides a meal for though weather significantly affects develop- the female. ment rate. Mormon cricket exists in solitary and gregari- The crickets tend to aggregate, seeking ous forms. The aforementioned description applies shelter together beneath bushes and debris dur- mostly to the gregarious form, which is the only ing inclement weather and at night. Once they form causing damage and the only form that has reach the third or fourth instar crickets the been thoroughly studied. The solitary form occurs aggregations begin to move long distances, with at low density between periods of population huge numbers of crickets coalescing into groups that move in bands. The density of crickets in bands may be 10–30 per square meter. The width of a band is often 300 m or more, but only 10 m deep, with crickets moving in the same direction along the entire width. The crickets all seem to move independently and consis- tently in the same direction, often at a rate of 1 km per day. There is no indication that they Mormon Cricket, Anabrus Simplex Haldeman follow one another, and the basis of orientation (Orthoptera: Tettigoniidae), Figure 88 Adult is unknown. female Mormon cricket, Anabrus simplex. 2466 M Morphogenesis outbreak and in areas where crickets do not populations or migrating bands. An alternative is become numerous. In contrast to the gregarious to apply insecticide-treated bait. The preferred bait form, solitary crickets are green in color, and do is flaky wheat bran, and it may be applied dry. not aggregate or form bands. Sexual behavior is also reversed, with females choosing among males. This change in mating behavior seems to be related Cultural Practices to better nutrition of crickets when they are not at high densities. In earlier times a common practice to prevent invasion of crop fields by cricket bands was to surround the crop with ditches possessing steep Damage sides; crickets falling into such ditches had great difficulty regaining the soil surface. Similarly, Mormon crickets occur in arid sagebrush range- vertical barriers of metal topped by a deflector land, and generally cause little injury unless they served to prevent crickets from entering areas move into irrigated cropland. In earlier times when surrounded by such “cricket fences.” settlers had to be nearly self-sufficient, vegetable  Cannibalism gardens and grain crops were critically important  Gregarious Behavior to ranchers, and crop losses caused by Mormon crickets were a significant threat to the existence of western communities. Presently, however, crop References production is much less significant in these arid lands, and control technologies have improved Capinera JL (2001) Handbook of vegetable pests. Academic, markedly, so cricket importance has declined. San Diego, 729 pp Cowan FT (1929) Life history, habits, and control of the Mor- Crickets remain a threat, however, and when bands mon cricket. USDA Tech Bull 161, 28 pp of crickets attain lush crop vegetation, they can be MacVean CM (1987) Ecology and management of the Mor- devastating. mon cricket, Anabus simplex Haldeman. In: Capinera JL (ed). Integrated pest management on rangeland: a shortgrass prairie perspective. Boulder, CO, Westview, pp. 116–136 Management Wakeland C (1959) Mormon crickets in North America. USDA Tech Bull 1202, 77 pp Sampling

Cricket bands are easily detected when they cross Morphogenesis roads, and their presence in an area rarely is a surprise. However, they move rapidly and their Growth and change in form during develop- course of travel is unpredictable, so when crick- ment, either embryonic or post-embryonic ets are discovered control efforts are usually development. directed at the bands before they enter crop- growing areas. Morphology

Insecticides Study of the form and function of organisms. Many writers erroneously use the term morphology when Persistent insecticides are sometimes applied by they simply mean shape, or form, or structure. aircraft to foliage in areas supporting nymphal  Abdomen of Hexapods Mosquito Larval Feeding Ecology M 2467  Antennae of Hexapods assistant at Wellesley College. He served as cura-  Head of Hexapods tor or similar scientific capacity at several institu-  Internal Anatomy of Insects tions, including the Peabody Museum and  Legs of Hexapods Carnegie Institution. He also served as a teacher  Mouthparts of Hexapods of entomology and zoology. Despite his lack of  Thorax of Hexapods formal education, Morse became a leading author-  Wings of Insects ity on New England Orthoptera, principally Acrididae. He was an associate of S.H. Scudder, also an acridologist. Morse traveled widely and Morphotype also published on other insect groups, particularly Odonata. Noteworthy publications The collection of physical characteristics that pro- authored by Morse include “Researches on vides for the distinct physical appearance of the North American Acrididae” and “Manual of the organism. Orthoptera of New England.” He died April 29, 1936. Morrison, Herbert Knowles References Herbert Morrison was born in Boston, Massa- chusetts, USA, on January 24, 1854. He was an Essig EO (1931) A history of entomology. The Macmillan individual of great physical strength and endur- Company, New York, 1029 pp Mallis A (1971) American entomologists. Rutgers University ance, and became a professional insect collector. Press, New Brunswick, NJ, 549 pp He specialized in Lepidoptera, traveling widely in the American west and south. He named a number of species of western Lepidoptera, but much of what he collected was named by others. He Mortality Rate contracted dysentery on one of his collecting trips, to Key West, Florida, and died on June 15, Death rate; the number of deaths per unit popula- 1885, at Morgantown, North Carolina. tion during a given period of time.

Reference Mosquito Larval Feeding Ecology

Essig EO (1931) A history of entomology. The Macmillan John R. Wallace Company, New York. 1029 pp Millersville University, Millersville, PA, USA

Mosquitoes serve as hosts and vectors to a suite of Morse, Albert Pitts pathogens and parasites such as viruses, bacteria, fungi, nematodes and protists. Because of the Albert Morse was born at Sherborn, Massa number of disease-causing agents that mosquitoes chusetts, USA, on February 10, 1863. His formal transmit, as well as the magnitude of health prob- education was limited because he was needed to lems these diseases cause to humans and livestock assist with the family’s farming operation. He worldwide, mosquitoes are medically the most abandoned farming at the age of 23, however, important group of insects. Specifically, in an and eventually accepted a position as a zoology attempt to lower the incidence of mosquito-borne 2468 M Mosquito Larval Feeding Ecology diseases such as malaria, dengue, yellow fever more accurately described as a layer of dissolved and most recently West Nile virus, hundreds of substances, particles and microorganisms that millions of dollars have been spent on mosquito accumulate due to simple diffusion, rising bubbles, surveillance and control. Early observations of convection, upwelling from sediments and sub- insect vector behavior prior to the advent of DDT surface water as well as from atmospheric dry fall- in the 1920s and 1930s helped formulate control out. Thus, the surface microlayer becomes an strategies around this period. In fact, because of accumulation layer where the concentration of the availability and effectiveness of synthetic insec- various chemical compounds and microorgan- ticides, and their effective application under a wide isms such as bacteria and algae exceeds that of range of conditions, the need for vector behavior subsurface water by orders of magnitude. Most and ecological studies was reduced. However, the Anopheles mosquito larvae feed at the surface, pre- development of insecticide resistance is the pri- sumably because food resources are more abun- mary reason why vector control has moved from dant at these interfaces. broad spectrum, persistent chemicals to more spe- The subsurface microhabitat within the cific biological control agents, e.g., bacterial insec- water column utilized for feeding by mosquito ticides such as Bti (Bacillus thuringiensis var. larvae is characterized as the zone below the israelensis) and Bs (Bacillus sphaericus). Because surface microlayer, and extends to the benthos. these bacilli species are obligatory stomach toxins Several species of Culex, Culiseta and Ochlerota- in mosquito larvae, their success as particulate tus larvae feed in this microhabitat on the sus- larvicides has been enhanced significantly with pended particles in the subsurface water column. increased knowledge of larval feeding ecology Mosquito larvae (e.g., Coquillettidia and Man- in terms of where mosquito larvae feed, as well sonia spp.) that inhabit plant root zones tap as how and what larvae feed upon, in their into the oxygen source trapped inside the plant environment. using specialized respiratory siphons. Rock pools along tidal zones or riverine systems accumulate water, and consequently provide a type Mosquito Larval Habitats of mineral surface with organic material on which some Ochlerotatus spp. can forage. The ovipositing adult female selects larval mos- The distribution and quantity of available food quito habitats. Female mosquitoes will generally resources largely determine mosquito larval distri- oviposit above, or upon, the water surface of ponds, bution, growth and feeding success. Stress imposed swamps, lake edges, salt marshes and artificial on larvae due to food limitations within microhab- containers. In addition, oviposition will occur in itats has shown to have adverse effects on larval areas where water is absent (e.g., along the dried survival, developmental rates, adult size and fitness edges of temporary pools or other ephemeral pud- as well as competence as disease vectors. dles, along the inner side of dry tree hole habitats, crab burrows or in phytotelmata). The microhabitats in which larvae feed within these aquatic habi- Mouthpart Morphology and tats include (i) at the air-water interface, (ii) within Feeding Modes the water column, (iii) along plant root zones, and (iv) on mineral and organic surfaces. Mosquito larvae use different morphological struc- The air-water interface of natural aquatic sys- tures and feeding modes (e.g., filtering, suspension tems has been defined as a thin zone (less than feeding, grazing, interfacial feeding or predation) 1 mm) of the water column and has been classified in food acquisition. The larval mouthparts possess as the surface microlayer. This interface can be specialized setae that are configured into brushes Mosquito Larval Feeding Ecology M 2469

APBr LPB LPB

Collecting- filtering Mn

Mosquito Larval Feeding Ecology, Figure 89 Scanning electron micrograph of the larval head of Culiseta. Abbreviations: LPB, lateral palatal brush; APBr, anteromedian palatal brush; Mx, maxilla; Mn, mandible; FG, feeding groove Collecting- gathering (Photograph by Doug Craig). or combs, and commonly referred to as the lateral palatal (or mouth) brushes (LPBs) (Fig. 89). The LPBs move through the water similar to the turn- Mosquito Larval Feeding Ecology, ing of pages in a book, and generate currents that Figure 90 Mosquito larvae displaying collecting assist in the removal of suspended food particles feeding modes (After Clements, 1992). from the water surface, and subsurface or benthos. Other mouthpart actions assist with ingestion, the feeding mode most commonly observed by chewing, or the formation of the food bolus prior mosquito larvae. The collectors are divided into to swallowing. Morphologically, a reduction in the those taxa that filter vs. gather. Filter-feeders or numbers and lengths of LPBs, maxillary brushes suspension feeders generally remove fine particu- and mandibular setae tends to occur in a progres- late organic material (FPOM size range = 0.45 μm sion from filter-feeders to predators. to 1 mm) from the water surface or column. The Excluding mosquito larvae predators, the feeding microhabitat of collector-filterers extends classification of non-predatory mosquito larvae from the air-water interface to feeding in the water is divided into four behavioral feeding modes: column or at plant root zones. Collector-gatherers (i) shredding, (ii) collector-filtering, (iii) collec- resuspend food, and remove particles deposited tor-gathering, and (iv) scraping (Fig. 90). These on, or loosely attached to, surfaces by the action of feeding modes are based on morpho-behavioral the LPBs. Conversely, those larvae that specialize adaptations that have evolved to allow mosquito in the removal of food resources tightly adhered larvae to feed on a wide array of food resources. to submerged plants or mineral surfaces are Nonetheless, because mosquito larvae feed on termed scrapers. such diverse food resources, they are likely not restricted to a single feeding mode. The shredder feeding mode entails chewing Larval Dietary Components or biting-off small fragments of coarse particulate organic material (CPOM size range >1 mm) such An important determinant of mosquito larval dis- as leaves, algae or dead invertebrates. Collecting is tribution and feeding success is the distribution of 2470 M Mosquito Overwintering Ecology larval food resources. Most mosquito larvae are many of which serve as vectors of disease-causing omnivorous, i.e., the major part of their diet con- organisms to humans and animals. Mosquitoes sists of microorganisms such as bacteria, algae and are ubiquitous in their distribution, being found protoctistans and particulate organic detritus. in practically every habitat except permanently Using DNA binding fluorochromatic stains, gut frozen areas. Approximately 75% of all mosqui- content analyses as well as microhabitat surveys of toes are found in the tropics and subtropical larval food items have shown that larvae ingest areas, and many mosquito-borne illnesses are detritus particles, algae, euglenoid protozoans, considered to be more tropical in their distribu- diatoms, cladocerans and hydrocarina or water tion (e.g., malaria or dengue fever). However, mites. However, in terms of overall dietary per- several diseases are found principally in colder, centage, bacteria (cocci, rods, spriochetes, and more temperate climate regimes, including East- cyanobacteria) have been considered the most ern Equine Encephalitis and La Crosse Enceph- important of the microorganisms consumed by alitis. Because worldwide travel has increased mosquito larvae. Several studies have noted that the potential for new disease introductions (e.g., ecological succession and diel periodicity of dengue and West Nile viruses in North America) microorganisms in larval feeding microhabitats to more temperate areas of the world, overwin- directly affects what the larvae ingest through tering eco-physiological aspects of mosquito direct availability. The mixed diet of larval mos- biology have recently become a focal point of quitoes provides the necessary proteins, vitamins epidemiological study. and fatty acids for growth, development and The survival mechanisms that mosquitoes survival. employ to overwinter are important from both  Mosquitoes biological and epidemiological perspectives. Early studies were initiated in order to address the mechanisms mosquitoes use to survive References adverse winter climates. However, the mechanisms for overwintering by several species are Clements AN (1992) The biology of mosquitoes. Vol 1. Devel- poorly understood. Also, the mechanism of dis- opment, nutrition and reproduction. Chapman Hall Publishers, London, United Kingdom, 509 pp ease overwintering is often not well known. An Laird M (1988) The natural history of larval mosquito habi- assemblage of physiological/morphological, eco- tats. Academic, New York, 555 pp logical and behavioral mechanisms are needed in Merritt RW, Dadd RH, Walker ED (1992) Feeding relation- order to survive cold temperatures. ships, natural food, and nutritional relationships of larval mosquitoes. Annu Rev Entomol 37:349–376 Wallace JR (1997) Larval feeding ecology of Anopheles quadrimaculatus (Say) and An. punctipennis (Say) Life Histories (Diptera: Culicidae) in southcentral Michigan ponds. Ph.D. Dissertation, Department of Entomology, Michigan State University, East Lansing, Michigan Mosquitoes exhibit complete or holometabolous metamorphosis. In order to emerge or survive from one season to the next, mosquito life histo- Mosquito Overwintering Ecology ries have evolved diapausal or hibernation components among all the developmental stages. John R. Wallace Many species of spring mosquitoes (e.g., several Millersville University, Millersville, PA, USA taxa within the genera Aedes, Ochlerotatus and Psorophora in temperate North America) over- To date, there are nearly 3,500 species of mosqui- winter in the egg stage. Many of these mosquitoes (Diptera: Culicidae) identified to science, toes inhabit either treeholes, vernal pools or Mosquito Overwintering Ecology M 2471 other types of transient freshwater habitats. The climates of North America. These studies have adult females of these taxa will oviposit in the not examined the mechanisms used by northern late spring or early summer along the outer mar- populations to survive colder climates. Of most gins of these vernal pools treehole or other con- recent interest are those tropical species (e.g., tainer habitats. As water levels diminish, more Aedes albopictus and Ochlerotatus japonicus) ovipositional habitats are exposed along these that have been introduced to North America that drier margins. These eggs require a dry period have survived winters in northern latitudes and will survive until the following spring despite much different from their tropical origins. dry and possibly re-flooded conditions. In other species, e.g., Ochlerotatus atropalpus (rock-hole mosquito) it has been observed that females will Eco-Physiology and Behavior glue an egg batch to the side of a rock-hole above the waterline for the overwintering generation. As stated previously, low temperatures present a It is unknown what this glue-like substance is, or suite of ecological and physiological challenges how it is produced. Among mulitivoltine species for insect survival. From an ecological perspec- (i.e., those species with more than one genera- tive, hibernaculum (or place to hibernate) selection per year), morphological differences in egg tion may be critical for physiological mechanisms structure have been observed between diapaus- to be effective. In order to escape the formation ing-winter and summer eggs. For example, of ice crystals that freeze cells and/or tissue, Anopheles walkeri eggs exhibit seasonal differ- insects, and mosquitoes in particular, may opt for ences in that diapausing-winter eggs have larger protected environments in which to overwinter. floats and a reduced exochorion compared to These hibernacula should offer protection from summer eggs. significantly colder temperatures, as well as wind Because many aquatic systems freeze over for and low humidity. Adult mosquitoes tend to be several months during the winter, the larval stage found in two types of overwintering hibernacula: of mosquitoes seems like an unlikely develop- (i) anthropogenic or human-constructed shelters mental choice in which larvae would overwinter. (e.g., houses, garages, barns, culvert pipes, steam However, there are several taxa from five genera, tunnels, rabbit hutches, and dog houses), or (ii) Culiseta, Coquilletidia, Wyeomyia, Orthopodomyia, natural hibernacula, such as in tree hollows or and possibly a few Toxorhynchites that are found under bark, and animal burrows. It is possible in unique freshwater habitats that overwinter in that other forms of natural hibernacula exist but the larval stage. The larval habitat of these taxa, in have not been identified. Two anopheline mos- most cases, freezes – implying simply that possi- quitoes, Anopheles quadrimaculatus and An. bly the larvae freeze solid, as is the case of the punctipennis, have been observed in both anthro- pitcher-plant mosquito, Wyeomyia smithii. With pogenic and natural hibernacula. Culex pipiens, the exception of the W. smithii, it is most likely or the house mosquito, has been collected from that larvae are not freeze tolerant, and therefore anthropogenic hibernacula. The microclimates use some microhabitats protected from lethal of these hibernacula have not been characterized temperatures. in terms of temperature or relative humidity In temperate climates, overwintering popu- throughout the hibernation period. Adult mos- lations of adult mosquitoes include a few taxa quitoes do not experience a true diapause in from four genera, Culex, Culiseta, Anopheles and these hibernacula; if temperatures increase Uranotaenia. Most studies on overwintering enough to allow flight, mosquitoes will move adult mosquitoes have examined those popula- within, or sometimes leave, a hibernaculum dur- tions distributed in southerly regions or warmer ing warmer periods. 2472 M Mosquito Overwintering Ecology Generally, in colder climates, female mosqui- References toes enter the winter season for hibernation or a quiescent period, whereas males typically will Bates M (1949) The natural history of mosquitoes. Harper & copulate and die before winter begins. Female Row, Publishers, New York, NY, 378 pp mosquitoes may take a blood meal prior to hiber- Clements AN (1992) The biology of mosquitoes. Chapman and Hall, New York, NY, 509 pp nation, and use this meal for fat production instead Crans WJ, McNelly JR (1997) A classification system for the of for egg production; this is termed gonotrophic life cycles of mosquitoes in New Jersey. Proceedings concordance. Movement is limited within hiber- 46th Annual Meeting of the New Jersey Mosquito nacula; however, females have been observed to Extermination Association, pp 148–153 Lee RE, Lee MR, Strong-Gunderson JM (1993) Insect cold- leave a hibernaculum in search of a blood meal hardiness and ice nucleating active microorganisms during a warm period of early spring. For many including their potential use for biological control. mosquito taxa in temperate climates, ovarian J Insect Physiol 39:1–12 Pratt HD (1959) A new classification of the life histories of development is essentially arrested during the North American mosquitoes. Proceedings 84th Annual winter, and resumes again in late spring when Meeting of the New Jersey Mosquito Control Associa- females obtain their first blood meal. tion, pp 42–48 Cold hardiness in insects pertains to the Wallace JR, Grimstad PR (2002) A preliminary characterization of the physiological ecology of overwintering capacity of an organism to survive such low tem- Anopheles mosquitoes in the Midwestern USA. J Am peratures. Two strategies potentially employed Mosq Control Assoc 18:126–127 by insects to survive winter include freeze avoidance and freeze tolerance. Because cases of freeze tolerant insects are rare, if non-existent, it can be Mosquito Oviposition assumed that insects, in general, employ the former of the two strategies. In order to avoid freez- Christopher Tipping1, Richard G. Weber2 ing, insects may be able to depress or lower the 1Delaware Valley College, Doylestown, PA, USA temperature at which the insect body freezes or 2University of Delaware, Newark, DE, USA when ice crystals begin to form. This is termed supercooling. The capacity for an insect to super- The larval stages of the Culicidae are exclusively cool may be influenced by several factors such aquatic. Therefore, gravid females must seek ovi- as season, life stage, feeding status, thermal position sites that are aquatic or will become acclimation and cryoprotectants (e.g., glycerol aquatic in the future. Some of these sites include or trehalose). In the case of mosquitoes, little temporary woodland pools, tree and crab holes, information is available for assigning potential man made containers such as abandoned automo- disease vectors to either a freeze avoidance or bile tires, phytotelmata, moist soil in low lying freeze tolerant strategy. To date, one study has areas that readily become flooded as well as a great shown that Anopheles quadrimaculatus and An. variety of other aquatic environments. punctipennis may exhibit a freeze avoidance Mosquitoes maximize their reproductive strategy. It has been shown that An. quadrimacu- potential by using habitats that are of differing latus will supercool to a temperature of −17°C resource richness and this use depends heavily on compared to An. punctipennis at −20°C. Lower how quickly batches of eggs are matured by the lethal temperatures for these species were −15°C female. The larvae of mosquitoes are filter feeders, and −17°C, respectively. Consequently, if An. browsers, and predators that utilize the microor- punctipennis can survive colder temperatures, it ganisms and other organic matter present in the may have more natural choices in which to water they inhabit. Mosquitoes deposit their eggs overwinter. either singly or in floating masses that are referred  Mosquitoes to as “rafts.” The mosquitoes that mature and Mosquito Oviposition M 2473 deposit most or all of their eggs at one time usually do so in the form of rafts or other orderly aggregations above or below the surface of the water. Many of these species tend to use resource- rich environments that have relatively high microbial populations and are rich in organic materials. Pools of foul water or artificial containers containing infusions of plant materials are highly attractive to these mosquitoes. The larvae of these species can often occur in enormous numbers under ideal conditions. Mosquitoes that develop a series of eggs over time usually occur in lower densities and use aquatic habitats that are often not resource rich. These species tend to distribute their eggs over a considerable area and take an appreciable time to deposit an entire clutch. The gross morphology of mosquito eggs is extremely variable and relate directly to the where and how they are deposited (Figs. 91 and 92). The eggs of Aedes, which are often deposited onto soil and are exposed to periods of drying, possess a Mosquito Oviposition, Figure 91 Representative thick chorion that is resistant to desiccation. The Anopheles eggs, showing typical variation of eggs of Anopheles are deposited onto the surface of the float among species: (a) An. gambiae, (b) An. water and remain there until eclosion due to tiny walkeri, (c) An. maculipennis, (d) An. novaguinensis, hollow floatation structures referred to as “frill (e) An. pharoensis (adapted from Mattingly, 1969. floats.” The eggs ofCulex are deposited on end into Mosquito Systematics Newletter). an organized floating raft. These eggs have a distinct exo/endo chorionic space that allows water to rise upwards and create an apical droplet on each egg. The apical droplet is hydrophobic and helps in maintaining the correct orientation of tilted eggs and egg-rafts. Mosquitoes use a variety of olfactory, visual, and tactile cues to locate suitable oviposition Mosquito Oviposition, Figure 92 Representative sites. Undoubtedly, many species use a combina- Aedes egg: lateral view of Aedes (Aedimorphus) tion of these cues that may affect the female’s domesticus egg (adapted from Reinert, JF, 1972. choice of where to deposit eggs (Fig. 93). Because Mosquito Systematics). many species of mosquitoes use aquatic habitats that are ephemeral in nature, the rapid detection segments. Over sixty years of studies have gener- and subsequent assessment of potential ovisites ated an enormous data base of some of the vola- are essential for successful reproduction. Mos- tile compounds that are attractive to dozens of quitoes can readily sense exceedingly small species. Many of these studies involved the use of amounts of volatile compounds that are emitted individuals obtained from laboratory colonies from aquatic habitats by using receptors located and perhaps might not be considered applicable on their antenna, mouthparts and or tarsal to understanding the oviposition behavior of 2474 M Mosquito Oviposition change associated with the senesce of the leaves of pitcher plants could also indicate the quality of the water held within. Studies involving treehole inhabiting mosquitoes have determined that darker rather than lighter-hued colors are attractive to gravid females indicating that they can recognize a dark tree hole from other similar aquatic habitats by color. Many species of mosquitoes in the genus Aedes deposit their eggs singly onto soil that is regularly exposed to periods of flooding and Mosquito Oviposition, Figure 93 Female Culex drying. Often, this wetting and drying is a pre- pipiens adding an egg to the egg raft she is about requisite for successful eclosion of the eggs. to complete. During the next hour, the white eggs Interestingly, one species of Aedes found in areas will darken to a color that blends well with the of Africa will often oviposit upon the legs of water upon which the raft floats (image courtesy crabs that inhabit tidal flats. These crabs crawl of Richard G. Weber). in and out of the water as part of their normal foraging behavior and can act as phoretic trans- porters for the mosquito eggs deposited on their wild populations of mosquitoes, but they do pro- shells. The eggs of Anopheles are deposited sin- vide important information about the ability of gly on the surface of the water and float until gravid female mosquitoes to detect and respond eclosion. Many species of mosquitoes that use to a multitude of minute quantities of airborne tree holes and phytotelmata as oviposition sites molecules. The dynamic microbial ecology asso- tend to deposit their eggs singly due to the lim- ciated with many temporary aquatic environ- ited nutrient resources offered by such sites. The ments often creates an equally dynamic mosquitoes of the genus Culex contain the most combination of volatiles that provide important species that construct floating egg rafts. Other cues for gravid female mosquitoes. Additionally, raft-building genera include Mansonia, Coquil- many species of mosquitoes can detect the vola- lettidia, Uranotaenia, Trichoprosopon, Eret- tiles associated with presence of life history stages mapodites and Culesita. Some species attach of their own or other species. their egg rafts to submerged vegetation. Several Chemoreception of volatile compounds is species of the genus Armigeres deposit their likely the most important cue for mosquitoes eggs into small rafts that are held by the metatho- that oviposit at night, and visual cues are impor- raxic legs of the female until they hatch. Addi- tant for mosquitoes that are diurnal or cre tionally, females of Trichoprosopon and puscular. Day-flying mosquitoes that use Eretmapodites display post-ovipositional mater- phytotelmata or plant parts that contain water nal care in the form of brooding of egg rafts. have been shown to discriminate between col- For many species of mosquitoes, distinct ors. This visual discrimination could be essen- preoviposition behaviors have been observed tial for mosquitoes that use pitcher plants as and recorded. Often these behaviors are associ- oviposition sites. Many mosquito species will ated with the assessment of potential ovisites only deposit their eggs into a particular plant and include distinct, observable flight patterns. species. The color of the leaves for each species The larvae of Toxorhynchites are predatory on is unique and therefore offers a reliable cue the arthropod inhabitants of tree holes, includ- for gravid mosquitoes. Additionally, the color ing the larvae of many species of mosquitoes. Mosquito Oviposition M 2475 Females of this large species perform an oviposi- will often release eggs as a strategy to maximize tion flight that consists of a series of elliptical reproduction. Mosquitoes that are dying near or loops over the potential ovisite before they drop on ovisites can release eggs that could eclose a single egg from the air. The function of the successfully. looping flight has been postulated to be a form  Mosquitoes of assessment of the volatiles from the site as  Phytotelmata well as a mechanism to deposit eggs. Many tree holes often have narrow openings that would not allow for easy access to the surface of the water References contained within. Additionally, mosquitoes of the genus Wyeomyia use the aquatic habitat Allan SA, Kline DL (1998) Larval rearing water and preexist- offered by pitcher plants and drop their eggs into ing eggs influence oviposition Aedes aegypti and Ae. the pitfall trap during an oviposition flight. albopictus (Diptera: Culicidae). J Med Entomol 35:943–947 The observed preoviposition behaviors of a Bates M (1949) The natural history of mosquitoes. MacMillan, few species of Culex include locating and assess- New York ment of potential oviposition sites as well as, dis- Beament J, Corbet SA (1981) Surface properties of Culex pipi- tinct behaviors associated with the successful ens pipiens eggs and the behaviour of the female during egg-raft assembly. Physioll Entomol 6:135–148 deposition of egg rafts. At dusk, femaleCx. restu- Bentley MD, Day JF (1989) Chemical ecology and behavioral ans fly upwind approximately a meter above the aspects of mosquito oviposition. Annu Rev Entomol ground as they search for the plume of volatiles 34:401–421 produced by potential ovisites. After finding a Christophers SR (1945) Structure of the Culex egg and egg raft in relation to function (Diptera). Trans R Entomol potential ovisite, females perform a bobbing Soc Lond 95:25–34 flight over the surface of the water for several Davis EE, Bowen FM (1994) Sensory physiological basis for minutes. This flight has been termed obstetric attraction in mosquitoes. J Am Mosq Control Assoc 10:316–325 dancing and most likely is involved in assess- DeCoursey JF, Webster AP (1952) Effect of insecticides and ment of the volatiles emitted by the site. Females other substances on oviposition by Aedes sollicitans. then land on vertical surfaces near the potential J Econ Entomol:451030–1034 ovisite. During this loitering period, females Frank JH (1986) Bromeliads as ovipositional sites for Wyeo- myia mosquitoes: form and color influence behavior. most likely swallow air into the ventral divertic- Fla Entomol 69: 728–742 ula. Several minutes later, females land on the Goiny H, Van Someren ECC, Heisch RB (1957) The eggs of surface of the water and then begin to drink. Aedes (Skusea) pembaensis Theobald discovered on After drinking, females initiate egg rafts between crabs. East Afr Med J 34:1–2 Hinton HE (1981) Biology of insect eggs. Pergamon, Oxford parallel metatarsi onto the surface of the water. Hudson BN (1956) The behaviour of the female mosquito in Females continue to drink during later stages of selecting water for oviposition. J Exp Biol 33:478–492 egg raft construction. The air swallowing and Kennedy JS (1942) On water-finding and oviposition by cap- tive mosquitoes. Bull Entomol Res 32:279–301 drinking behaviors are important for the opera- Linley JR (1987) Aerial oviposition flight of Toxorhynchites tion of the hydrostatic skeleton and essential for amboinensis (Diptera: Culicidae). J Med Entomol successful oviposition. Future field studies with 24:637–650 mosquito species that deposit their eggs at one Lounibos LP (1983) Behavioral convergences among fruit- husk mosquitoes. Fla Entomol 66:32–41 time in a mass or raft will most likely also dis- Mattingly PF (1969) Mosquito eggs III. Tribe Anophelini. play the behaviors of swallowing of air and Mosq Syst Newslett 1:41–50 drinking. Okazawa T, Miyagi I, Yong HS (1992) Oviposition and eggs of Finally, death stress oviposition has been Armigeres (Leicesteria) flavus (Diptera: Culicidae). Jpn J Entomol 60:54–58 documented to occur in mosquitoes as well as Steffan WA, Evenhuis NL (1981) Biology of Toxorhynchites. many other insects. Gravid females that are dying Annu Rev Entomol 26:159–181 2476 M Mosquitoes (Diptera: Culicidae) Weber RG, Tipping C (1993) Preoviposition drinking by Morphology and Physiology Culex restuans (Diptera: Culicidae). J Insect Behav 6:343–349 Eggs

Mosquitoes (Diptera: Culicidae) Mosquito eggs have a small pore, the micropyle, at the anterior end for sperm penetration. Females C. Roxanne Rutledge lay approximately 50–500 sculpted eggs on the Florida Medical Entomology Lab, University of water surface or in areas that will become flooded. Florida, Vero Beach, Florida, USA Eggs are soft and white when laid and later darken and become hard. Floodwater mosquitoes lay their The family Culicidae within the order Diptera, the eggs on moist soil and are tolerant of dry condi- two-winged flies, comprises of approximately tions. Various modifications exist that will allow 3,500 species of mosquitoes. This family of eggs to float. Anopheles eggs are laid singly on the nematocerous (long-horned primitive flies whose surface of the water. The boat-shaped eggs of most larval head is well developed with laterally moving Anophelines possess two air-filled floats on either mandibles) flies is divided into three subfamilies, side; in those that lack floats, the eggs sink if Toxorhynchitinae, Anophelinae, and Culicinae. touched. Other mosquitoes lay egg rafts that may There are 37 genera of mosquitoes. contain up to 200 eggs per raft.

Distribution Larvae

Mosquitoes live in humid tropics and subtropics, The larval stage of the mosquito is aquatic. The warm moist climates, temperate and cool zones, larvae are legless and spend a majority of time everywhere except areas that are permanently at the surface of the water. However, they can frozen. stay submerged for some time. This stage is commonly referred to as “wriggler” or “wiggler,” due to the lashing movements of the abdomen Metamorphosis that move them forward, backward, or sideways in the water. The only functional respiratory Mosquitoes undergo holometabolous, or com- apertures are a pair of dorsal spiracles near the plete, metamorphosis, meaning their life cycle end of the abdomen; lateral spiracles remain includes four distinct forms: eggs, larvae, pupae, closed except during ecdysis. The head can be and adults. Their eggs require water to hatch. oval, ovate, or almost rectangular in shape, The larvae develop through four instars before depending on the genus. The larvae possess they transform into active, non-feeding pupae. slender shafted antennae with spines and tufts The adult’s wings, sucking mouthparts, and legs of hairs. The eyes are simple lateral eyes with no can be seen through the transparent pupal skin. lenses and are present from the beginning of the The adult emerges from the pupal skin onto the larval stage into the adult stage. The large pig- surface of the water, and then flies to seek car- mented spots on the side of the larval head are bohydrates and mates. The adults and larvae are the compound eyes of the adult developing anatomically different, reside in different habi- beneath the cuticle of the larva. Larval mosquito tats (terrestrial vs. aquatic, respectively), and mouthparts are composed of lateral brushes obtain nutrients from entirely different sources which move currents of water toward the head of food. and pectinate hairs that serve as combs for Mosquitoes (Diptera: Culicidae) M 2477 retaining particles filtered from the water. The the mosquito life cycle is very active and is rela- thorax is oval with no appendages and becomes tively short. The average time spent in the pupal enlarged during the fourth instar. The abdomen stage is 2–3 days, but varies with species and tem- is ten-segmented with the respiratory append- perature. The pupa can submerge in their aquatic age on the eighth segment. In the Anophelini, habitat or move around at the surface. They may the last 5 or 6 abdominal segments bear palmate remain inactive and passively rise to the surface brushes that aid to suspend the larva from the or actively swim up by abdominal movements water surface. These are the only breathing assisted by the large tail paddles. Mosquito pupae apertures of the larvae. Mosquitoes in the gen- do not possess functional mouthparts, and, there- era Mansonia and Coquillettidia possess a mod- fore, do not feed during this period; this stage is ified respiratory siphon with spines, hooks, and dependent on the larvae for nutrition. teeth for insertion into the roots of aquatic The head and thorax combine to form a plants. The larvae and pupae in these genera cephalothorax with nothing of the structure of remain submerged and obtain oxygen from the the larval head remaining. Large black com- plant. Late in the fourth instar, the cuticle is sep- pound eyes are located beneath the cuticle. The arated from the abdomen and the mosquito thorax is approximately the size and shape that it develops into a pupa (Fig. 94). will be during adult life and bears the legs, wings, and respiratory trumpets. The abdomen projects from the cephalothorax and differs from the lar- Pupae vae in the lack of respiratory appendages and the presence of tail fins (paddles). The paddles are The pupal stage of the mosquito is also aquatic. located at the end of the abdomen and can Unlike other holometabolous insects, this stage of increase the motor efficiency of the abdomen. The respiratory organ of the pupae are called “trumpets” and are connected to the anterior ends of the dorsal longitudinal tracheal trunks and project from the thorax with the open ends projecting above the water surface. As with the larvae, the pupae of Mansonia and Coquillettidia obtain oxygen from the roots of aquatic plants. They remain attached to the aquatic plants until the end of the pupal stage when they detach and float to the water surface for the winged adult to emerge. The appearance of a film of air under the cuticle of the thorax is an indication that the adult is about to emerge from the pupal skin. Prior to emergence, air is drawn forward and begins to form an air bubble at the base of the proboscis that is extended back to the fourth Mosquitoes (Diptera: Culicidae), abdominal segment. The pressure from the abdo- Figure 94 Mosquito life cycle: above, eggs are men ruptures the cuticle where the adult will deposited singly or in groups; right, the larval emerge. When the entire adult body is free from stage, which often is found at the surface of the pupal thorax, the mosquito steps onto the water; bottom, the pupal stage; left, the adult or water surface, walks away from the pupal skin blood-feeding stage. and is soon able to fly. 2478 M Mosquitoes (Diptera: Culicidae) Adults mouth. Salivary glands of the mosquito are made up of three lobes and lie at the sides of the anterior The adult mosquito is a terrestrial insect pos- end of the ventriculus and are important in the role sessing one pair of wings. Males and females are of transmission of viruses and other parasites. The distinguishable by the plumose antennae of the salivary glands are the avenue of escape for patho- male and the circles of short hairs on the female gens from the mosquito to the new host blood. antennae. The bases of the antennae arise close The saliva serves as an anticoagulant, and possibly together on the head. The pedicel of the anten- a food solvent and source of antimicrobial nae houses Johnston’s organ, a sensory structure substances. for sound reception which, in males, is used to The mesothorax of the adult mosquito recognize conspecific females. The sides of the bears one pair of scaled wings. Two halteres, head are occupied by compound eyes that organs that maintain the equilibrium of the almost meet dorsally and ventrally. Male mos- mosquito, are present instead of a second pair quitoes feed on carbohydrates for energy; the of wings. Veins and scales on the wings form females also require carbohydrates for flight patterns that are characteristic in species iden- energy and they consume blood which is neces- tification. The flight muscles, located in the sary for egg development. Species of the Toxo- thorax, make up from 16 to 19% of the total rhynchites genus do not blood-feed. Autogeny, body weight. The rate of wing vibration varies the ability to lay eggs without a prior bloodmeal, among species, and among males and females exists in some species. within species. The adult female mosquito that feeds on One pair of legs is associated with each of blood uses a proboscis, a slender structure com- the three thoracic segments of the mosquito. posed of seven parts: the labrum, two mandibles, The legs are made up of the coxa, trochanter, a hypopharynx, two maxillae, and a labium. The femur, tibia, and tarsus. The tarsus is divided labium houses, or encloses, the other six struc- into five tarsomeres. The fifth tarsomere has tures of the mouth. The hypopharynx contains two curved claws, and most species possess a the salivary canal and the maxillary stylets are secondary element of the claw, a tooth. The legs the piercing organs. Once a small blood vessel in bear scales that are used as key characters in the host is encountered, the mandibles are drawn identification. back and blood enters the food canal by suction The abdomen is made up of ten segments, from the cibarial pump. Saliva is discharged from the last two being greatly reduced. The last two the hypopharynx while blood is taken into the segments in males are modified to form a genital food canal. The pharyngeal pump, a large bulb- clasper used in mating. The male genitalia are like structure located behind the brain, works used in identification of male mosquitoes. with the cibarial pump to keep the blood meal flowing into the stomach. When the bloodmeal is completed, the mosquito pulls out the stylets and Internal Systems of the Mosquito once again they are sheathed in the labium. In male mosquitoes, the mandibles and maxillae are Respiratory System reduced and the hypopharynx is not separated from the labium as it is in the female. In nectar Oxygen is carried to the tissues of the adult and feeding females and males of Toxorhynchites spe- larval mosquitoes in essentially the same man- cies, the proboscis is strongly decurved. ner, through the spiracles to the trachea to the A pair of salivary glands located ventrally in smallest tracheoles which reside in close prox- the thorax enter the head and open just below the imity to the tissues. The respiratory system in Mosquitoes (Diptera: Culicidae) M 2479 mosquito larvae includes a pair of lateral and where the blood meal passes through to a stomach dorsal tracheal trunks with spiracles that run the that retains the blood meal. The function of the length of the insect. The last pair of lateral spira- midgut is to aid in nutrient absorption, diuresis, cles on the eighth abdominal segment and the and secretion of digestive enzymes. It is the dorsal spiracles on the ninth abdominal segment primary organ of digestion of the blood meal. The allows the mosquito larvae to breathe at the hindgut includes a pyloric chamber, anterior intes- water surface. In adult mosquitoes, there are tine, and the innervated rectum and anal canal. eight pairs of spiracles on the abdomen and two There are five Malpighian tubules inserted between pairs on the thorax. the midgut and hindgut which hang freely in the body cavity. Water, salts, and excretory products pass from the hemolymph into the Malpighian Circulatory System tubules. These structures aid in excretion and regulation of water and salts. The circulatory system of the mosquito is an open The foregut of the larval mosquito includes system where the blood, or hemolymph, bathes the innervated pharynx which is involved in fil- tissues with nutrients, transports waste, and dis- tering and swallowing, and the esophagus. The tributes hormones. It does not transport oxygen larval midgut consists of cardia, gastric caeca, and to tissues. The hemolymph is circulated by a dor- the anterior and posterior stomach. As with the sal blood vessel. The structure of the dorsal vessel adult, the larval hindgut includes the Malpigian does not vary considerably between the larval, tubules, pylorus, anterior intestine, and the rec- pupal, and adult stages. The dorsal blood vessel is tum and anal canal. a muscular tube that extends from the eighth abdominal segment to the head and is divided into the aorta (head and thorax) and the heart Nervous System (abdomen). Blood is freely discharged into the head and flows backward through the body. Pul- The nervous system consists of a brain, subesoph- satile organs that help to circulate the hemolymph ageal ganglion, and ventral ganglia in the abdo- are located in the bases of the antennae, the adult men ending in the eighth abdominal segment. The labium, and possibly in the adult scutellum. The most complex part of the nervous system is located heartbeat runs the length of the dorsal vessel in the head where the primary sense organs are in peristaltic waves. The waves run forward in also located. The subesophageal ganglion receives larvae, and in the pupae and adults may run either input from the mouthparts. Each of the ventral forward or backward. ganglia provide coordination for the body segment with which they are associated.

Digestive System Reproductive System The digestive track (alimentary canal) of the adult mosquito includes the stomodeum (foregut), the Reproductive organs develop during the larval mesenteron (midgut), and proctodeum (hindgut). life. Males mature sexually several hours or days The foregut includes a pharyngeal pump, esopha- after adult emergence. To be sexually mature, the gus, and three diverticula. The largest of the diver- male antennal fibrillae (long, articulated inner- ticula is a highly elastic ventral crop. Sugars from vated setae) must be erect and the genitalia must nectar feeding are hydrolyzed in the crop. The be inverted 180° from their position at emergence. mosquito midgut is essentially a narrow tube Male genitalia are located on the abdominal 2480 M Mosquitoes (Diptera: Culicidae) segments 8–10, usually bilobed with claspers that in blood, making it difficult to fly. Their excretory hold on to the female. So distinct are they that system is able to eliminate over 40% of water and they are used to identify male mosquitoes to spe- sodium from the blood meal within an hour after cies. Mosquito ovaries contain ovarioles and each consuming the blood. Blood-host preferences ovariole consists of an egg follicle. Females store vary among species; some females are opportu- spermatozoa from the male in organs known as nistic and will feed on a variety of hosts, while spermathecae. The number of spermathecae var- some are more discriminating and have a single ies among mosquito genera: Anopheles (1), Toxo- host preference, or a very narrow range of pre- rhynchites (3), most Culicinae (3), and some Aedes ferred hosts. Some species exhibit a change in (1). The spermatozoa fertilize the oocytes as they host-feeding as the seasons change. For some are ovulated. species this is explained by host availability, for others, such as Culex nigripalpus, the switch is stimulated by rain and humidity. Mosquito Behavior

Feeding Oviposition

Feeding during the larval mosquito stage is Egg production is cyclic. At oviposition the accomplished through ingestion of particles fil- eggs are white and soft. After several hours, the eggs tered from the water column or surface, removal darken and harden, and there is some evidence that and ingestion of surface biofilms, shredding of this is due to sclerotization. Female Toxorhynchites leaves, and predation of other larvae and insects lay their oval, barrel shaped eggs individually in their own size or smaller. Food is carried to the flight. Egg rafts are laid byCulex , Culiseta, and Ura- mouth by currents that are produced with the oral notaenia species. Aedes/ Ochlerotatus and Psoro- brushes on the larval mouthparts. The larvae pro- phora eggs are laid singly on surfaces that are moist, vide nutrition for the non-feeding, yet active, not wet, at the time of oviposition. Almost all Aedes stage of the pupa. eggs can withstand desiccation. Mansonia species In the adult stage, male and female adult mos- may lay their eggs in rafts on the underside of float- quitoes feed on sugars from plants and from other ing or emergent leaves. Coquillettidia egg rafts are insects that feed on plant sugars. This is the only laid on the surface of water containing aquatic veg- source of nutrition for the males as they do not etation, which the larvae and pupae will attach to feed on blood. The females use the sugar meals for for the duration of their aquatic life. Mimomyia energy and the blood meals for egg development. eggs resemble Anopheles eggs but do not have the Sugar meals are obtained from flower necta- floats attached to the sides.Ficalbia eggs are laid on ries, extrafloral nectaries, rotting fruit, and vege- leaves that hang over the water surface. Wyeomyia tative parts of plants. An important source of eggs commonly are associated with bromeliads and sugar for mosquitoes is honeydew produced by pitcher plants. Trichoprosopon digitatum females Hemipteran insects. Some females of species of hold their egg rafts in their legs until they hatch, and Malaya consume fluids that are regurgitated by will add eggs they find to their own raft. ants belonging to the genus Crematogaster. Blood is essential for egg development in the female mosquito. The midgut of the adult female Mating mosquito is grossly distended immediately following consumption of a blood meal. Many mos- Males and females can come together for mating quitoes will imbibe more than their own weight purposes in several ways: males form swarms Mosquitoes (Diptera: Culicidae) M 2481 and as females approach, the males grab hold of can last 45 min or longer. Males of some species them; males and females gather around their lar- of Wyeomyia, Sabethes, and Limatus will locate val habitat or around potential blood meal hosts; females by flying up and down the vegetated or males approach resting females. Once a male areas where the females are resting. obtains a female in flight, he turns around so that the pair is venter-to-venter. Mating is initiated in flight and copulation is completed in seconds in Disease Transmission most species. Males of some Aedes and Manso- nia species will make their way to hosts of inter- Mosquitoes are vectors of many pathogens that can est to the blood-seeking female and attempt to cause morbidity and mortality in humans and other mate with the virgin females. Opifex fuscus and animals (see Table 12). The pathogens most often Deinocerites cancer males will approach pupae associated with mosquito vectors are arboviruses that are close to emergence and compete for (arthropod-borne viruses), nematodes, and proto- individual pupae. When the adult mosquito zoa. The most studied and well-known mosquito- begins to emerge from the pupal case, the male borne protozoan pathogens belong to the genus forces his way in to make genital contact just Plasmodium and cause malaria in humans and birds. prior to emerging. If the pupa is female, copula- Nematodes carried by mosquitoes and passed to tion will begin. If not, the male will leave. In spe- humans and dogs during blood-feeding cause human cies that mate when settled rather than during filariasis and dog heartworm disease. There are over flight, such as Deinocerites cancer, copulation 200 known viruses vectored by mosquitoes.

Mosquitoes (Diptera: Culicidae), Table 12 Pathogens that can cause morbidity and mortality in humans and other animals Pathogen Disease Known outbreaks Hosts with morbidity Arboviruses Togaviruses Venezuelan equine Central America, South America, Horses encephalitis North America Eastern equine Central America, South America, Horses, humans encephalitis North America Western equine South America, North America Horses, humans encephalitis Highlands-J North America Humans Chikungunya Africa, Asia, India, Philippines Humans O’ Nyong Nyong Africa Humans Ross River Australia, New Guinea, Humans Solomon Islands, South Pacific Islands Sindbis Africa, Asia, Australia, Humans Czechoslovakia, Russia Barmah Forest Australia Humans Flaviviruses Yellow fever Africa, Central America, South Humans, monkeys America St. Louis encephalitis North America, South America Humans Japanese encephalitis Australia, Asia Humans, swine 2482 M Mosquitoes (Diptera: Culicidae) Mosquitoes (Diptera: Culicidae), Table 12 Pathogens that can cause morbidity and mortality in humans and other animals (Continued) Pathogen Disease Known outbreaks Hosts with morbidity West Nile Africa, Middle East, North Humans, horses, birds America Wesselsbron disease Africa Humans, sheep Rocio Brazil Humans Murray Valley Australia, New Guinea Humans encephalitis Dengue Asia, Africa, Polynesia, Humans Micronesia, Caribbean, Central America, South America Bunyaviruses Bunyamwera Africa Humans Cache Valley North America Humans, cattle California encephalitis North America Humans Jamestown Canyon North America Humans LaCrosse North America Humans Snowshoe hare North America Humans Tahyna Asia, Europe Humans Trivittatus North America Humans Rift Valley fever Africa Humans, sheep, cattle Rhabdoviruses Bovine ephemeral fever Africa, Asia, Australia, Middle Cattle East Nematodes Wuchereria Filariasis: Bancroftian Africa, India, China, Bangladesh, Humans bancrofti filariasis Myanmar, Thailand, Malaysia, Laos, Vietnam, Indonesia, Philippines, Papua New Guinea Brugia malayi Filariasis: Brugian China, India, Republic of Korea, Humans filariasis Asia Brugia timori Filariasis: Timorian Indonesia Humans filariasis Dirofilaria immitis Dirofilariasis: Dog North America Canines heartworm Protozoa Plasmodium vivax, Malaria Africa, Central America, South Humans ovale, malariae, America, Middle East and falciparum

Methods of Control methods often is employed in mosquito Integrated Pest Management (IPM) programs. Because mos- Management of mosquito populations can be quitoes have two very different types of habitats attempted in a number of ways; the use of several during their life cycle, there are two opportunities Mosquitoes as Vectors of Viral Pathogens M 2483 to apply control techniques: during the aquatic Mosquitoes as Vectors of Viral stage and during the terrestrial stage. In the aquatic Pathogens stage, mosquitoes are more concentrated and less mobile than they are during their terrestrial life, Ann M. Powers, Aaron C. Brault, Barry making control in the larval stage more efficient. R. Miller The major methods of mosquito control include: Centers for Disease Control and Prevention, Fort Collins, Colorado, USA ·· Larviciding – Bacterial products specific for mosquitoes can be applied to the aquatic habitats. The role of arthropods in the transmission of Insect growth regulators also are available for con- human and animal disease agents is a significant trol during this stage, as well as some organophos- focus of research for medical entomologists. phates. Monomolecular films and some oils are Insects in the families Culicidae, Psychodidae, used for control of larvae as well as pupae. Ceratopogonidae, Simuliidae, Glossinidae, Pulici- ·· Adulticiding – Organophosphates, pyrethroids, and dae, Reduviidae, along with several species of natural pyrethrins are available to target flying mos- ticks are responsible for the vast majority of vec- quitoes. These products are applied either by ground tor-borne disease. These insects are capable of fogging units mounted to trucks or by handheld transmitting pathogens as diverse as protozoa, backpack sprayers. Another mode of application is helminths, bacteria, and viruses. This section will by aerial spraying from airplanes or helicopters. focus specifically on viruses that are transmitted ·· Source reduction – This method includes removal of by mosquitoes, or arboviruses (from arthropod- water-holding containers that are not necessary (used borne viruses). These viruses are defined by their tires, cans, bottles, empty buckets, etc.) as well as ability to replicate in, and be transmitted between, drainage projects that are more costly and labor inten- both their vertebrate host and their invertebrate sive and require approval by water and land manag- vector. It is this unique ability to propagate in dual ers. Impoundment projects have been used to control host systems that differentiates them from other salt-marsh mosquitoes around coastal areas. These viruses that may be able to be spread only mechan- structures are designed to prevent female salt-marsh ically by insect vectors. However, this characteris- mosquitoes from laying eggs. This method of control tic is also likely to be one factor that delineates the also requires the cooperation and approval of land natural cycles of these viruses. Here, we describe and water managers as well as mosquito control one half of the natural cycle, how an arbovirus districts. would enter, replicate in, and ultimately be transmitted by a mosquito vector (Fig. 95). References Factors Associated with the Clements AN (1992) The biology of mosquitoes. Vol 1. Devel- Biological Transmission of opment, nutrition and reproduction. Chapman and Hall. University Press, Cambridge, Massachusetts Arthropod-Borne Viruses Clements AN (1999) The biology of mosquitoes. Vol 2. Sen- sory reception and behaviour. Chapman and Hall. Uni- Viruses (Table 13) can be transmitted by an versity Press, Cambridge, Massachusetts Eldridge BF, Edman JD (eds.) (2000) Medical entomology. A arthropod vector through two distinct mecha- textbook on public health and veterinary problems caused nisms, mechanical or biological transmission. by arthropods. Kluwer Academic Publishers, Dordrecht With mechanical transmission there is no repli- Snodgrass RE (1959) The anatomical life of the mosquito. cation of the virus in the insect. This mode of Smithsonian Miscellaneous Collections, Vol 139, No. 8. Publication 4388. The Smithsonian Institution, transmission has been demonstrated for a num- Washington, DC ber of viruses with mosquitoes, biting midges 2484 M Mosquitoes as Vectors of Viral Pathogens

Enzootic cycle Epidemic/Epizootic cycle

Culex (Mel.) spp. Aedes, Psorophora, etc. Human (tangential)

Small rodents Jungle/sylvatic Small rodents Equines Peridomestic Equines habitat habitat

Culex (Melanoconion) spp. Aedes, Psorophora, etc. Mosquitoes as Vectors of Viral Pathogens, Figure 95 Transmission cycles of Venezuelan equine encephalitis virus. Solid arrows indicate known transmission. Hatched arrows indicate possible transmission route.

Mosquitoes as Vectors of Viral Pathogens, Table 13 Important mosquito-borne viruses causing human illness Virus Major disease Invertebrate vector chikungunya Febrile/arthralgic illness Aedes aegypti dengue 1–4 hemorrhagic fever Aedes aegypti, Aedes albopictus Eastern equine encephalitis Encephalitis Coquilletidia perturbans, Aedes vex- ans, Culex nigripalpus, Ochlerotatus sollicitans, Culiseta melanura Japanese encephalitis Encephalitis Culex univittatus complex, Culex tritaeniorhynchus LaCrosse Encephalitis Ochlerotatus triseriatus Murray Valley encephalitis Encephalitis Culex annulir ostris O’nyong nyong Arthralgic/febrile illness with Anopheles gambiae, Anopheles rash funestus Rift Valley fever Febrile illness Hemorrhagic Culex pipiens complex, Aedes spp. fever, Retinitis Ross River Febrile illness Culex annulirostris St. Louis encephalitis Encephalitis Culex pipiens complex, Culex restuans, Culex nigripalpus Venezuelan equine encephalitis Encephalitis Aedes spp., Ochlerotatus spp., Psora- phora spp., Culex spp. West Nile Febrile/encephalitis Culex spp. yellow fever Hemorrhagic fever Aedes aegypti, Aedes africanus, Aedes simpsoni complex, Aedes furcifer, Haemagogus spp. Mosquitoes as Vectors of Viral Pathogens M 2485 and black flies. One prominent example of a Once the virus enters the mosquito midgut epi- virus transmitted in this manner is myxoma thelium, it may fail to disseminate from produc- virus that is transmitted mechanically by mos- tively infected midgut epithelial cells resulting in quitoes in Australia. However, with most viruses, an abortive infection. After infection of the midgut, mechanical transmission typically only contrib- the virus enters the hemocoel of the mosquito, utes to occasional cases of viral transmission where it infects numerous tissues, especially the and usually is not involved in the maintenance fat body, and disseminates to secondary infection cycle of arthropod-borne viruses. In contrast, sites. The acinar cells of the salivary glands are sec- biological transmission, in which virus replica- ondary targets that must be infected if transmis- tion occurs within the arthropod, is the basis for sion is to subsequently occur. If any of these steps maintaining arboviral transmission cycles and is inhibited, transmission is unlikely to occur in is characterized by a complex interaction sufficient levels to maintain the virus in nature. between virus and an arthropod vector in which numerous factors combine to determine the efficacy of the virus-vector relationship. Infection Process A number of viral and vector factors, both intrinsic and extrinsic, can affect each stage of bio- The first stage of biological transmission, infection logical transmission (Fig. 95). The first event in the of the midgut epithelium, has been studied exten- infection of any arthropod (mosquito) cell is viral sively in a number of virus-vector systems. The binding via specific receptors and entry of virus midgut epithelium is the primary site of the virus into the cytoplasm. Once in the cell, the virus must replication that must occur if the infection is to be first uncoat, or have the outer proteins removed, to productive. As the virus enters the cells of the expose the genetic material. The RNA (virtually all midgut and begins the replication process (Fig. 96), arboviruses have an RNA based genome) is then the titer of detectable virus drops significantly. transcribed and translated to produce replication This eclipse phase marks the time when replica- machinery components and structural proteins tion is occurring within midgut cells but no virus that will assemble to form new virions. The non- particles have been expelled into the hemocoel of structural proteins produced from the viral genome the mosquito. This period typically lasts from 1–4 combine with cellularly encoded factors to repli- days depending on the vector species, virus, and cate the viral genome. This process results in the extrinsic factors that can affect midgut infection production of nascent, full-length genomes that such as larval nutrition and ambient temperature. can then be packaged into the assembling viral After the eclipse phase is completed, virus titers in particles. The new virions complete the maturation the mosquito multiply by a factor of 1,000 or more and assembly process by release from the cell, typi- within just a few days during a period referred to cally by budding from the plasma membrane. as the amplification phase. Virus spreads rapidly For biological transmission to take place, a through the hemocoel of the mosquitoes and number of events must occur including infection infects secondary susceptible target organ systems of the midgut epithelium, dissemination of virus including the salivary glands, flight muscle, neural from the midgut to the hemocoel, infection of sali- tissue, fat body, and ovaries (Fig. 97). The mainte- vary glands, and deposition of virus in the apical nance phase begins when the titer of the virus lev- cavities and ducts of the salivary glands for trans- els off or decreases presumably due to the mission. This chain of events covers the time frame mosquito’s modulation of the viral infection. Com- know as the extrinsic incubation period, or the ponents of the insect immune system including period between the ingestion of an infectious hemocytes and antiviral proteins presumably act blood meal and the transmission of an arbovirus. to limit the replication of the virus; however, they 2486 M Mosquitoes as Vectors of Viral Pathogens

Attachment Entry

Uncoating

Nucleus Transcription and replication Translation

Assembly and maturation Budding

Mosquitoes as Vectors of Viral Pathogens, Figure 96 Generalized viral replication strategy.

Fat body

Dorsal diverticulum Midgut Ovaries

Salivary Ventral glands diverticulum Hemocoel

Basal plasma membrane Microvilli

Basal lamina

Mosquitoes as Vectors of Viral Pathogens, Figure 97 Diagram of mosquito anatomy indicating organs important in virus infection, dissemination, and transmission.

do not entirely clear the virus as mosquitoes A number of hypotheses have been proposed to remain persistently infected. explain the refractoriness of a virus for midgut infection. These include: (i) cellular charge/charge distribution differences within the mesenteronal epithelia; Abortive Midgut Infections (ii) digestive inactivation of virions while within the midgut lumen and, (iii) differential expression of If the virus fails to enter or replicate in the midgut, specific receptors on the mesenteronal epithelia of the infection is non-productive and the virus will susceptible mosquitoes. The presence of charged not be transmitted in future blood feeding events. ions in an infectious blood meal can significantly Mosquitoes as Vectors of Viral Pathogens M 2487 alter the midgut infection rate of some mosquitoes (PFU)/ml blood ingested, yet fails to infect Cx. pipi- for a given virus. However, this phenomenon is not ens at bloodmeal titers in excess of 8 log10 PFU/ml. universal and not very well understood. Laboratory Furthermore, minimal infection titers differing by as experiments have demonstrated midgut surface much as 1,000-fold have been identified for geo- charge differences among various mosquito species graphic strains of Aedes albopictus. Viral genetic fac- and it is postulated that charged molecules in the tors can also play a major role in the infectivity of a blood meal might affect how the virus interacts with given mosquito species. For example, a genetic vari- specific midgut receptors. The second hypothesis, ant of LaCrosse (LAC) virus demonstrated a reduced digestive inactivation of virions in the midgut lumen, ability to productively infect the mesentery of Aedes may be a result of secretion of the digestive enzymes triseriatus mosquitoes (5% infection rate as com- trypsin and chymotrypsin. Exposure of viral parti- pared with an 89% rate for wildtype LAC virus). cles to digestive enzymes may result in cleavage of Serial passage of this viral variant in Ae. triseriatus viral surface proteins resulting in either up or down regenerated the midgut infectivity to the level of the regulation of efficient binding to mosquito cells. The wildtype virus. Similarly, the development of a final hypothesis, differential expression of specific monoclonal antibody resistant mutant of a Venezu- midgut receptors is an exceptionally complex issue. elan equine encephalitis (VEE) virus vaccine strain The mesenteronal epithelium consists of columnar resulted in a virus that exhibited reduced infectivity and squamous epithelial cells with interspersed in Aedes aegypti mosquitoes. The genetic determi- regenerative cells. The apical side is microvillate and nate was mapped to a single amino acid substitution highly invaginated to provide a large surface area in the E2 glycoprotein, the major antigenic determi- from which materials from the lumen can be nant for alphaviruses. This single amino acid altera- absorbed. Numerous surface and transmembrane tion within the vaccine strain reduced viral infection proteins are present in this region to aid in nutrient of, and dissemination from, the midgut. uptake but it is unclear which of these receptors are Recent advances in molecular virology are used by viruses to bind and enter the midgut cells. allowing researchers to systematically elucidate the Until further studies clearly elucidate the relative viral components of vector specificity. An engi- importance of various receptor proteins in viral neered viral clone based on the genome of Sindbis binding, it will remain unclear how critical this com- (SIN) virus is incapable of infecting Ae. aegypti ponent is in the infection process. mosquitoes orally. However, a distinct Malaysian strain of SIN virus, MRE-16, efficiently infects this mosquito species following oral ingestion. A genet- Viral and Vector Genetics ically constructed virus containing the structural Associated with Differences in genetic components of MRE-16 substituted for the Midgut Infection corresponding genes in the parent clone, produced a virus that efficiently infected Ae. aegypti orally. Genetic differences between mosquito vectors can result in drastic differences in vector susceptibility to infection with the same virus. For example, the Dissemination from the Midgut WR Culex tarsalis genetic variant is resistant to infection by western equine encephalitis (WEE) Failure of a virus to infect peripheral tissues after virus, while another genetic variant (WS Cx. tarsalis) initiation of a productive infection of the midgut is extremely susceptible to oral infection with the epithelium can also result in an aborted infection same WEE viral strain. WEE virus has been shown and lack of transmission. The virus must trans- to infect Cx. tarsalis mosquitoes efficiently with verse the mesenteronal epithelium from the apical bloodmeals containing 3 log10 plaque forming units to basolateral side, exit the cell, and bypass the 2488 M Mosquitoes as Vectors of Viral Pathogens basal lamina (BL). The thickness of the basal lamina, which can be modulated by factors such as larval nutrition, may be one component in the failure of a virus to reach the mosquito hemocoel. The mechanisms allowing viruses to bypass this potential barrier are not completely understood, particularly since the basal lamina has a size exclusion between 5–8 nm, a pore size significantly smaller than many arboviruses. Interestingly, intrathoracic inoculation of mosquitoes with viruses showing no dissemination from the midgut after per os infections have developed midgut infections, indicating that the virus was capable of bypassing the BL from the basal side. Some evidence has suggested that viral dissemination from the midgut Mosquitoes as Vectors of Viral Pathogens, could occur through alternative mechanisms such Figure 98 Ochlerotatus triseriatus midgut infected as pathology to the mesenteron or dissemination with LaCrosse virus. Infection occurs in the midgut from the foregut-midgut junction (Fig. 98). epithelial cells while longitudinal and circular muscle cells remain uninfected. Viral and Mosquito Genetic Basis for Lack of Dissemination designated small (S), medium (M), and large (L), have demonstrated that viruses containing the M A number of examples of arboviral transmission RNA fragment of SSH with the L and S RNA seg- refractory mosquitoes can be linked to an inability ments of LAC virus infected the midgut epithe- of virus to propagate outside the midgut. For lium of Ae. triseriatus efficiently; however, these example, failure of yellow fever virus or dengue viruses failed to disseminate from the midgut. viruses to move from infected midgut cells to the Reassortants containing the M segment of LAC hemocoel was demonstrated in isofemale lines of virus (with the L and S segments from SSH virus) Ae. aegypti that were resistant to infection. In efficiently infected and disseminated from the another example, Cx. (Melanoconion) taeniopus, midguts of Ae. triseriatus mosquitoes. Again, while an enzootic VEE mosquito vector, transmits VEE these viral genetic elements can be elucidated, it is subtype IE viruses efficiently. However, although a less clear how they interact with a given mosquito closely related alternate subtype of VEE (subtype vector resulting in productive or non-productive IAB) infects Cx. taeniopus midgut epithelium, interactions. the virus fails to invade tissues beyond the mes- Recent advances in molecular virology have enteron. The vector genetic determinants that aided in the process of identifying the viral regulate these highly specific interactions are determinants of vector specificity. The existence clearly present, but poorly understood. of full-length infectious clones of numerous Viral components are also undoubtedly alphaviruses and flaviviruses and the ability to involved in this inability to escape into the hemo- perform site-directed mutagenesis on them are coel of midgut-infected mosquitoes. Reassortant enabling researchers to examine the role of indi- experiments performed with LAC and snowshoe vidual genetic elements in binding and replica- hare (SSH) bunyaviruses, viruses that have a tion. Using this approach, chimeric viruses have genome consisting of three segments of RNA been generated that contain portions of multiple Mosquitoes as Vectors of Viral Pathogens M 2489 viral strains. In one example, complete structural protein genes from a virulent VEE strain were introduced into an infectious clone of an avirulent strain that poorly infects an epizootic mosquito species, Ochlerotatus (Aedes) taeniorhynchus. This led to the identification of the envelop gly- coproteins (E1 and E2) as potential determinants of vector specificity. Further genetic studies identified only three E2 amino acid differences between two VEE viruses exhibiting dramatically different abilities to infect Oc. taeniorhynchus. Some combination of these three amino acids was hypothesized to be responsible Mosquitoes as Vectors of Viral Pathogens, for extreme differences in the ability to infect the Figure 99 Adult female, Ochlerotatus triseriatus mosquito vector. Site directed mutagenesis of salivary glands infected with Sindbis virus (one the non-infecting clone to contain all possible gland only infected). combinations of the three amino acids identified a single point mutation that was responsible for If the acinar cells of the salivary glands do vector infectivity. Undoubtedly additional clari- become infected, the virus could still fail to be fication of viral determinants of infectivity will released into the lumen and ducts. Few examples be forthcoming with further advances in molec- of this phenomenon exist. One example may be ular arbovirology. Ae. albopictus infected with chikungunya (CHIK) virus; this species transmitted CHIK virus less efficiently after longer incubation times even though Infection of the Salivary Glands the salivary glands were still productively infected. The genetic basis for this is completely unclear. Viruses that escape the mesenteron and disseminate through the mosquito via the hemolymph must finally infect the salivary glands and repli- Vertical Transmission of cate in this organ system before transmission Arboviruses can occur. However, many vectors are unable to complete this final step that is often dose and In addition to mechanical and horizontal bio- time dependent. Thirty-eight percent of Cx. tar- logical transmission, arboviruses can be trans- salis infected with low concentrations of WEE mitted vertically to naÏve mosquito vectors. A virus have been unable to replicate virus in the number of viruses have been identified to have salivary glands while those receiving higher been transmitted in this fashion; however, only doses transmit efficiently. Aedes albopictus a few viruses, most notably LAC virus, have exhibit a similar phenomenon with eastern been determined to utilize this form of trans- equine encephalitis (EEE) virus; after fifteen mission efficiently. Transovarial transmission days of extrinsic incubation, only 57% of mos- (TOT) of LAC virus requires that the virus quitoes could transmit by bite, despite the fact enter the ovaries, infect germ cell lines, persist that 100% of mosquitoes were positive for infec- in the embryonic and larval stages, and survive tion. Antigenic tests demonstrated that the mos- the enzymatic processing as the larva transi- quitoes failing to transmit did not have infected tions into the pupal stage. Flaviviruses also have salivary glands (Fig. 99). been shown to be transmitted vertically but 2490 M Mosquitoes as Vectors of Viral Pathogens Mosquitoes as Vectors of Viral Pathogens, Table 14 Components of vectorial capacity Viral Genetic variants that differ in infectivity Vector Inherent vector competence – susceptibility to oral infection and efficiency of transmission Population structure – density, longevity, etc. Host preference Geographic distribution Vertebrate reservoir Able to develop high titered viremia necessary to infect vectors Population structure – density, longevity, etc. Immune status Overlap in space and time with vectors

through a distinct mechanism. In contrast to vectorial capacity, there can be substantial sus- LAC virus, many flaviviruses, including yellow ceptibility variation within a given species of fever virus, St. Louis encephalitis virus, West mosquito for a particular virus. Additionally, Nile virus, and dengue viruses are transmitted since environmental factors are involved, this via the micropyle rather than germ cell infec- range of susceptibility or refractoriness can tion. Again, there is no clear genetic under- vary with the time of year or geographic loca- standing of either process. tion. Only a greater understanding of the interactions among the various components to produce a competent system will eventually Elements of Vectorial Capacity lead to methods for disease prediction and control. Vectorial capacity is the combined effect of all  Mosquitoes of the physiological, ecological, and environ-  individual diseases mental factors relating vector, host and pathogen that ultimately determine the ability of a given mosquito species to serve as a competent vector for a particular virus (Table 14). This References definition encompasses factors other than the biological interaction of virus and vector such Guerrant RL, Walker DH, Weller PF (eds) (1999) Tropical infectious diseases: principles, pathogens, and practice. as the host preference and longevity of the Vols 1 and 2. Churchill Livingstone, Philadelphia, PA, potential vectors. Intrathoracic infections of 1644 pp multiple mosquito vectors resistant to oral Hardy JL, Houk EJ, Kramer LD, Reeves WC (1983) Intrinsic infection reveal that the ability to infect the factors affecting vector competence of mosquitoes for arboviruses. Annu Rev Entomol 28:229–262 midgut epithelium appears to be the most criti- Kettle DS (1990) Medical and veterinary entomology. CAB cal component of vector competence. However, International, Wallingford, 658 pp even an unlikely vector could transmit virus Knipe DM, Howley PM (eds) (2001) Fields virology (4th given the correct environmental and ecological ed). Vols 1 and 2. Lippincott Williams and Wilkins, Philadelphia, PA, 3200 pp conditions. It is significant to note that, because Monath TP (ed) (1988) The arboviruses: epidemiology and both vector and viral genetics contribute to ecology. Vol 1. CRC, Boca Raton, FL, 329 pp Moths (Lepidoptera: Heterocera) M 2491 Moss Bugs considered the most advanced, the Noctuidae (owlet moths). Butterflies, while often listed as Bugs in the family Peloridiidae (order Hemiptera, the most advanced lepidopterans, are placed suborder Pentamorpha). among the macro-moths after the geometer  Bugs moths in our modern classification as based on the overall evolutionary development of the Lepidoptera. Butterflies are now thought to be a Moth Flies lineage from ancestors of what remain now as the most primitive of bombycine moths (per- Members of the family Psychodidae (order haps resembling Ratardidae and relatives of Diptera). Southeast Asia), which then evolved to geometer  Flies moth ancestors (families Geometridae and Hedylidae) and an alternate lineage that evolved to diurnal lifestyles and modern butterflies. Moths (Lepidoptera: Heterocera) The main moth families are the Noctuidae (owlet moths), which is the largest family, with a John B. Heppner known total of about 26,310 species worldwide, Florida State Collection of Arthropods, the Geometridae (geometer moths), with about Gainesville, FL, USA 21,150 species, the Pyralidae (snout moths), with about 16,500 species, the Arctiidae (tiger moths), Among the insect order Lepidoptera, moths com- with 11,155 species, and the Tortricidae (leafroller prise most of the order worldwide, totaling about moths), with 8,945 known species. The other more 135,700 described species, representing 91% of all well known moth families, but with fewer species, lepidopterans (the other 9% are butterflies). There are the Saturniidae (emperor moths), Sphingidae are an estimated additional 100,000 species of (hawk moths), Lymantriidae (tussock moths), moths waiting to be discovered and named, mostly Bombycidae (silkworm moths), Lasiocampidae from tropical regions of the world. Although the (lappet moths), Notodontidae (prominent moths), name Heterocera is not used in modern classifica- Gelechiidae (twirler moths), and Tineidae (fungus tion of Lepidoptera, the name can be used to refer moths) (Fig. 100). to all the moths (Rhopalocera is used as the name Moths are known from all faunal regions and for all butterflies). The moth divisions, Macrolepi- occupy virtually all terrestrial niches on the planet. doptera and Microlepidoptera, likewise have no Many are of economic importance as pests of scientific basis but commonly are used as a conve- crops, horticultural plants, or stored products nience in grouping the mostly larger macro-moths and woolens. Most of the extreme biodiversity versus the mostly more primitive and smaller known for Lepidoptera is among the moths, from micro-moths (extraordinary exceptions in size are horn-feeding larvae of Tineidae moths in South known for each group). Africa, to carnivorous hunting inchworms of the Of the 125 known families of Lepidoptera, Geometridae in Hawaii, to planthopper parasites moths comprise 118 families, all but the seven among the widespread Epipyropidae larvae, among families which involve the butterflies. Some clas- other examples. Most moths, however, are plant sifications are slightly different, since some spe- feeders, feeding on every possible niche of plants, cialists split more groups as separate families. although the majority are simple leaf feeders. Among the moths are found both the most Adult moths typically have medium-size eyes, primitive living lepidopterans, the Micropterigi- a large haustellum (or tongue) which sometimes is dae (mandibulate archaic moths), and what are scaled, and filiform antennae. There are variations 2492 M Moths (Lepidoptera: Heterocera)

Moths (Lepidoptera: Heterocera), Figure 100 Representative moths (Lepidoptera: Heterocera): top left, Thyris maculata Harris (Thyrididae) from Maryland, USA (photo J.H.H. Thiele); top right, Glyphodes bivitralis Guenée (Pyralidae) from Taiwan (photo C.C. Lin); second row left, Saptha beryllitis (Meyrick) (Choreutidae) from Taiwan (photo J.B. Heppner); second row right, Eterusia aedea (Clerck) (Zygaenidae) from Taiwan (photo C.C. Lin); third row left, Vindusara moorei (Thierry-Mieg) (Geometridae) from Taiwan (photo C.C. Lin); third row right, Timandromorpha discolor (Warren) (Geometridae) from Taiwan (photo C.C. Lin); bottom left, Protambulyx strigilis (Linnaeus) (Sphingidae) from Ecuador (photo J.B. Heppner); bottom right, Alypia octomaculata (Fabricius) (Noctuidae) from Florida, USA (photo M.C. Thomas). Moths (Lepidoptera: Heterocera) M 2493 in many families, where some have large eyes (one of abdominal prolegs having crochets (hook-like family even has split eyes) or very small eyes, and spines on the base of the prolegs that provide foot- where antennae are clubbed like in butterflies or ing when climbing on plants), plus a posterior pro- skippers, or greatly enlarged to being even quad- leg pair. Specialized feeders have many variations ripectinate (many Saturniidae). The most primi- from this standardized form, including the minute tive moth families still retain vestigial chewing flattened leafminers (as in Nepticulidae and Gracil- mouthparts (more well developed in Micropterigi- lariidae, among others) and the nearly apodous dae), and have either no haustellum or only a very slug caterpillars (superfamilies Zygaenoidea and small haustellum; some macro-moths also have a Cossoidea). Some of the more bizarre caterpillars reduced or no haustellum, since they do not feed are found among the Saturniidae and Notodonti- as adults in those species. Moth bodies tend to be dae, and among the slug caterpillar groups, while covered with more hair-like scales than among most hawk moth larvae have a horned posterior butterflies but all kinds of variations are known. and a few mimic snake heads. Moth larvae mostly Moth adults have various abdominal scent organs pupate by first making a silken cocoon, or pupate (coremata) among some families (e.g., some Arc- within their leaf mine (e.g., in such families as Nep- tiidae), and most of the groups in the superfamily ticulidae and Gracillariidae), or larval shelter (e.g., Noctuoidea have chordotonal organs in the thorax in such families as Psychidae and Mimallonidae), for hearing (Geometridae, in Geometroidea, have or in leaf rolls (e.g., as in families Pyralidae and abdominal tympanal organs). Wings include a pair Tortricidae). Hawk moth larvae make an under- of forewings and a pair of typically smaller hind- ground pupal cell when ready to pupate. Among wings (most primitive moths have hindwings other families, there are many other larval life styles about equal in size to the forewings), and generally and pupation methods, as also adult behavior. the forewings are elongated or triangular in shape However, perhaps as many as 90% of all moths and the hindwings are more rounded. Great vari- remain unknown biologically, particularly among ety of wing shape, however, is known and many the tropical species, and this is likewise true for groups have hindwing tails (e.g., some Uraniidae, their life histories and behavior. Zygaenidae, and Saturniidae, among others) or The largest known moths are among the many other irregular wing margins or shapes (e.g., emperor moths (family Saturniidae), where the tropical Himantopteridae have exceedingly some of the female atlas moths (genus Attacus) of long and thin tails that almost are all that remains Southeast Asia attain wingspans of up to 300 mm of the hindwings). Many of the Microlepidoptera (even to 320 mm if the wings are angled somewhat have linear wings, especially the hindwings, and for maximum distance). Likewise, there are very very long hair-like scale fringes on the hindwing large hawk moths (family Sphingidae), to 200 mm margins. A number of moth families also have wingspan, and even among some primitive moths adults that have the wings greatly reduced (brac- there are large species, as among the ghost moths hypterous) or even vestigial (apterous), as for (family Hepialidae). The largest known moth actu- example among some female Geometridae and ally is in the family Noctuidae, where females of Lymantriidae. Maculation typically is more som- the white witch moth (genus Thysania) from the ber browns or grays among the moths, but some Amazon attain wingspans of as much as 305 mm exceedingly colorful species are known among using the standardized wingspan measuring posi- most families, many with sparkling spots or bands tion. The smallest moths are among the pygmy of metallic-iridescent scales. moths (family Nepticulidae), where some wing- The caterpillars of moths are commonly spans among these leafminers are as little as encountered, typically with a hard head capsule, 2.5 mm. The average for all moths, however, is three pairs of clawed thoracic legs, and four pairs about 25 mm in wingspan. 2494 M Motile References collected extensively from Russia, including Sibe- ria and Russia’s (at the time) possessions of Alaska Barlow HS (1982) An introduction to the moths of South and California. As a colonel in the military, he had East Asia. Malayan Naturalist Society, Kuala Lumpur, unusual access to travel, and took full advantage of Malaysia, 305 pp, 50 pl his journeys, collecting and studying Coleoptera in Common IFB (1990) Moths of Australia. Melbourne Univer- sity Press, Carlton, Australia, 535 pp, 32 pl Europe, North Africa, and much of North America Covell CV Jr, (1984) A field guide to the moths of eastern in addition to the locations previously mentioned. North America. Houghton Mifflin, Boston, MA, 496 pp, Indeed, it is sometimes stated that his collecting 64 pl trips were a cover for military intelligence. He also Dominick RB, Hodges RW, Dominick T, Edwards CR, Hodges ER (eds) (1971) – The moths of America north of Mex- processed enormous amounts of material collected ico, including Greenland. Wedge Entomological Foun- by others. Motschulsky was a strong-illed, inde- dation, Washington, DC, 27 fasc pendent, and controversial individual. He was pos- Hering EM (1951) Biology of the leaf miners. W. Junk, The sessive, superficial with his descriptions, rough on Hague, The Netherlands, 420 pp, 2 pl Holloway JD, Kibby G, Peggie D (2001) The families of Male- specimens, and unconventional with his mounting sian moths and butterflies. E. J. Brill, Leiden, The Neth- techniques. This led him to clash with other coleop- erlands, 455 pp, 8 pl terists of the time, particularly Kraatz. He died June Inoue H, Sugi S, Kuroko H, Moriuti S, Kawabe A (1982) Moths of Japan. Kodansha, Tokyo, Japan, 2 vol, 392 pl 5, 1871, at Simferopol, Crimea, Russia. Krenek V (2000) Small moths of Europe. Cesky Tesín, Czech Rep, 174 pp Pinhey EGC (1975) Moths of Southern Africa. Tafelberg, References Capetown, South Africa, 273 pp, 63 pl Robinson GS, Tuck KR, Shaffer M (1994) A field guide to the smaller moths of south-east Asia. Malaysian Naturalist Essig EO (1931) A history of entomology. The Macmillan Society, Kuala Lumpur, Malaysia, 309 pp, 32 pl Company, New York, 1029 pp Watson A, Whalley PES (1975) The dictionary of butterflies Herman LH (2001) Motschulsky, Victor Ivanovich. Bull Am and moths in color. McGraw Hill, New York, NY, 296 pp, Mus Nat Hist 265:110–112 144 pl Young M (1997) The natural history of moths. T. & A.D. Poyser, London, United Kingdom, 271 pp, 16 pl Mountain Midges Motile Members of the family Deuterophlebiidae (order Diptera). Active. Able to move freely.  Flies

Motor Neurons Mountain Pine Beetle, Neurons associated with the central nervous sys- Dendroctonus ponderosae tem that transmit information to muscles and (Coleoptera: Curculionidae, glands. Scolytinae)

Barbara Bentz Motschulsky, Victor Ivanovich USDA Forest Service, Logan, UT, USA

Victor Motschulsky was born in 1810 in Russia, The mountain pine beetle, Dendroctonus pondero- and became one of the most famous Russian ento- sae Hopkins, is considered one of the most eco- mologists and greatest coleopterists of his time. He nomically important insect species in coniferous Mountain Pine Beetle, Dendroctonus ponderosae (Coleoptera: Curculionidae, Scolytinae) M 2495 forests of western North America. Adult beetles other mountain pine beetles on the tree. Aggrega- are capable of successfully reproducing in at least tion pheromones enable mountain pine beetles to 12 North American species of Pinus (Pineacea) overcome the defenses of large, vigorous host trees from southern British Columbia to northern Baja by rapid and highly concentrated attacks. In this Mexico. Mountain pine beetle adults attack live manner, mountain pine beetles are functionally trees, and typically must kill the host for success- able to expand their own food supply. Larger trees ful reproduction. Population outbreaks are most require more adults to overcome the tree resin common in a few selected host species, such as defensives, but also produce a larger number of lodgepole pine (P. contorta), ponderosa pine brood the following generation for continued tree (P. ponderosa), western white pine (P. monticola), attack. Because a single tree is a finite resource, whitebark pine (P. albicaulis), and sugar pine pheromones are also produced which interrupt (P. lambertiana), which often grow in relatively the aggregation of adults on a tree. The interrup- homogeneous groups over large acreages. Moun- tive aggregation pheromones direct incoming tain pine beetles typically attack older lodgepole adults to unoccupied portions of the tree under and whitebark pine (e.g., greater than 80 years), attack, and also to nearby host trees, thereby reduc- while younger ponderosa, western white, and ing competition for resources within a single tree. sugar pine can also be attacked. Trees that are In this manner, during an outbreak, thousands of stressed by factors such as overcrowding, water, trees can be attacked and killed in a single year. and pathogens are especially vulnerable. Once inside a new host tree, adults mate and The lifecycle of the mountain pine beetle is eggs are laid individually on each side of galleries highly dependent upon temperature. Commonly, excavated vertically in the phloem. Phloem is the populations are univoltine, although at higher ele- inner tissue layer just below the outer bark which vations where average temperatures are colder, 2 translocates carbohydrates up and down the tree. and sometimes 3 years are required to complete a Mountain pine beetle larvae feed horizontally in generation. Adult beetles emerge from host trees the phloem, cutting off nutrient translocation, and disperse to new hosts in the warm summer thereby killing the host tree. Larval development months when temperatures are above 15.5°C. rate, which is highly dependent on temperature, Although timing of emergence will vary from dictates the life stages present during the winter. year to year depending on beetle development Available evidence indicates that the mountain and temperature, peak adult emergence typically pine beetle does not diapause, and all larval life occurs within a 2–3 week time span. Rapid and stages may be found overwintering under the bark synchronous emergence of the population is of host trees. The larvae, which are intolerant of essential for mountain pine beetle success in over- freezing temperatures, survive low temperatures coming the resinous defenses of healthy host trees. by supercooling. Populations in Idaho have been Adult dispersal involves movement within an found to survive temperatures as low as −35°C. infested patch of trees, movement between infested Mortality due to cold temperatures is usually patches of trees, and movement out of the imme- greatest during the spring and fall months when diate area for initiation of new patches. Long range larvae may not be appropriately acclimated to dra- dispersal to new areas is often aided by wind cur- matic swings in temperature. Woodpeckers, clerid rents, whereas local dispersal is directed by aggre- beetles (Enoclerus spp., Thanasimus spp.), and par- gation pheromones, compounds released when asitic wasps are also the cause of a small amount of adult beetles attack and feed on new host trees. mountain pine beetle mortality, mostly at endemic Monoterpenes, which are major constituents of population levels. pine resin, are converted by adult beetles to com- Pupation occurs in the early summer followed pounds which, when released, act to aggregate by a teneral adult stage during which the new 2496 M Mountain Pine Beetle, Dendroctonus ponderosae (Coleoptera: Curculionidae, Scolytinae) adults feed on a diverse flora of microbial symbi- growth. A mosaic of vegetation types across a onts including fungi (Ophiostoma spp.) and yeasts landscape, partitioned by age and host and non- found within the pupal chamber. During this feed- host species, may also help to reduce large scale, ing period, the microorganisms are acquired in widespread mortality. the mycangia, a specialized structure of the integ- Options for management of mountain pine ument. When the adult beetle emerges from the beetle populations depend on the specific land use host tree for dispersal to a new tree, the fungi and objectives. Forested areas targeted for timber pro- yeasts are carried inside the mycangia and inocu- duction can be silviculturally treated to facilitate lated into the phloem of the new host. Although reduced susceptibility to mountain pine beetle the role of Ophiostoma spp. in mountain pine outbreaks. Many areas designated as wilderness, beetle population dynamics are not fully under- however, are managed as natural areas and timber stood, at least one species appears to be beneficial harvest is not a major objective. Within these areas to population success, while detrimental effects the historical role of the mountain pine beetle in are attributed to another species. Following matu- forest ecosystems may be emphasized. Mountain ration feeding in the teneral adult stage, new adults pine beetle populations, which are native to western emerge from the dead trees to disperse, attack new North America, have evolved with their pine hosts live host trees, and begin the cycle again. and are significant components of healthy, func- Given appropriate weather and stand condi- tioning ecosystems. In particular, the mountain tions, populations of mountain pine beetles are pine beetle and fire are considered important dis- capable of attacking and killing hundreds of thou- turbance agents favoring the regeneration of lodge- sands of trees in a few years. This magnitude of pole pine. While tree death is a difficult concept for mortality can disrupt forest management plans, humans, it is a normal step in the rejuvenation and recreation, watershed, wildlife, and timber pro- succession of forest ecosystems, and the mountain duction. In areas of high value, such as forest pine beetle is an important part of this process. campgrounds and ski areas, direct control tactics  Bark Beetles in the Genus Dendroctonus such as insecticides are often used to temporarily reduce mountain pine beetle caused mortality. Synthetic forms of the aggregation pheromone References may also be used to concentrate adults in traps or trees which are then removed from the area. Ongo- Amman GD, Cole WE (1983) Mountain pine beetle dynamics ing research is aimed at understanding the role of in lodgepole pine forests Part II: Population Dynamics. USDA Forest Service, Intermountain Forest and Range interruptive aggregation pheromones in mountain Experiment Station, General Technical Report INT-145 pine beetle population dynamics, in the hope that Borden JH, Chong LJ, Lindgren BS (1990) Redundancy in the synthetic forms of these compounds may also pro- semiochemical message required to induce attack on vide a tool for direct population control. While lodgepole pines by the mountain pine beetle Dendrocto- nus ponderosae Hopkins (Coleoptera: Scolytidae). Can direct control tactics are useful in small, high value Entom 122:769–777 areas, they are not effective or feasible over large Logan JA, Bentz BJ (1999) Model analysis of mountain pine areas, and do not alter the habitat and stand condi- beetle (Coleoptera: Scolytidae) seasonality. Environ tions that are favorable to mountain pine beetle Entomol 28:924–934 McGregor MD, Amman GD, Schmitz RF, Oakes RD (1987) populations. The optimum approach in areas Partial cutting lodgepole pine stands to reduce losses to which have been targeted for management is pre- the mountain pine beetle. Can J For Resour vention. Silvicultural practices such as thinning, 17:1234–1239 Raffa KF (1988) The mountain pine beetle in western North which decrease the density of host trees, help to America. In: Berryman AA (ed) Dynamics of forest maintain vigorous trees and create a less favorable insect populations, patterns, causes and implications. habitat for mountain pine beetle population Plenum Press, New York, NY, pp 506–531 Mouthparts of Hexapods M 2497 Shore TL, Safranyik L (1992) Susceptibility and risk rating characteristic of the hexapods. Therefore, the systems for the mountain pine beetle in lodgepole pine division of the mandibles into mono- and dicon- stands. Forestry Canada, Pacific Forestry Centre, Victoria, Canada dylic is not fitting (Koch 2001); because of this, and owing to the great variability existing in the hexapods, this author prefers to treat separately the mandibles of each one of the large groups: Mouth Beard Collembola, Protura, Diplura, Archaeognatha, Thysanura and Pterygota. In robber flies (Asilidae), the prominent tuft of Despite the opinion of Koch, many authors hairs at the front of the head. This is also called consider, at least from a practical point of view, the the mystax. type and number of articulations within the head capsule to separate two fundamental types of mandibles: monocondylic (one articulation) and Mouth Cone dicondylic (two articulations). The monocondylic type is characteristic of the majority of Apterygota, A term used to describe the mouthparts arrange- although in Collembola, Protura and Diplura an ment of thrips (Thysanoptera). authentic mandibular condyle does not exist as in  Mouthparts of Hexapods the case of Archaeognatha. This monocondylic type appears secondarily in entognathous Ptery- gota, with mouthparts transformed into stylets. Mouth Hooks The dicondylic type is typical of the Pterygota, where two mandibular articulations are differenti- In larvae of the higher Diptera, the mandible-like ated, one in the anterior position and another pos- feeding structures located at the oral cavity. terior. An intermediate condition exists between the mono- and dicondylic types. In it the mandibles, in addition to the principal articulation (cor- Mouthparts of Hexapods responding to the only condyle of Archaeognatha), present a secondary articulation known as the Severiano F. Gayubo epicondyle. It is situated in the anterior third of Universidad de Salamanca, Salamanca, Spain the mandibular body and therefore differs from the second articulation of Pterygota, which has The hexapods are trignathan, that is to say they a clearly posterior position. This intermediate present three pairs of buccal appendages, each one model is displayed in Thysanura and nymphs of of them situated in the corresponding cephalic Ephemeroptera. segment: a pair of mandibles (mandibular seg- The morphology of the mandible varies ment), a first pair of maxillae (maxillary segment), according to the diet and is usually characteristic and a second pair of maxillae that fused, form the in each of the hexapod orders. Nevertheless, it labium (labial segment). basically consists of an incisor zone in the distal Recently, certain authors affirm that the clas- or subdistal position and another molar zone sit- sic point of view, according to which the true uated on the internal mandibular face. The greater capacity of “biting” by the Dicondylia [Thysanura or lesser development of these two zones is found (Zygentoma) plus Pterygota] is functionally cor- in the function of the alimentary behavior. Thus, related to the acquisition of dicondylic mandi- in predatory species the incisory zone is usually bles, cannot be maintained, taking into account well developed, since it serves to cut and tear the that the capacity of “biting” transversely is a trait prey. On the contrary, in phytophagous species 2498 M Mouthparts of Hexapods that consume solid food, the molar zone, which differentiated: cranial-maxillary muscles and ten- carries out a triturating function, is more devel- torial-maxillary muscles. oped. The internal face of the mandibles can bear During embryonic development a fusion of secondary cuticular or tegumentary differentia- two maxilla-like structures is produced (second tions: tubercles, keels, spines, and bristles of dis- pair of maxillae), from which the labium origi- tinct development and morphology. Additionally, nates. The number and development of pieces that a lobe lacking musculature, called lacinia mobilis comprise the labium can vary depending on the or prostheca, is differentiated from this internal hexapod group. In the generalized models two face in Diplura and nymphs of Ephemeroptera. regions are differentiated: the postmentum (basal, In the majority of Pterygota the musculature united to the oral cavity) and the prementum (dis- related to the mandibles is very profuse, being dif- tal). There can also be three: submentum, mentum ferentiated into four types of muscles: hypop and prementum. Although the majority of authors haryngeal muscles, tentorial-mandibular muscles, consider the mentum to be an apical part of the zygomatic adductors, and cranial-mandibular mus- postmentum, in certain cases it is a basal subdivi- cles. In Pterygota they are generally reduced to two sion of the prementum. These regions correspond types of muscles, abductors and adductors, although to a postlabium (postmentum plus mentum) and a in primitive groups the cranial-mandibular muscles prelabium or prementum. are conserved. The prementum, which in the most primitive The maxillae are considered more complete groups is a paired structure, basically carries one appendages than the mandibles. The most gener- pair of palps (lateral position) and four apical alized model is found in the Thysanura. Modifica- pieces, two in the lateral position or external (para- tions of this model are produced that tend to glossae) and two in the median position or inter- reduce certain structures adapted to different nal (glossae). The glossae can be welded to each trophic models. The basal part is called the cardo. other or to the paraglossae, forming the alaglossa It is of reduced size, and it articulates from the and totaglossa, respectively. Sometimes the four proximal part of the head capsule in the hypos- lobes (glossae and paraglossae) are fused, forming tomal zone of the buccal area. In the apical part, the ligula or tongue. The palpus typically consists the cardo is joined to the stipes, which is the larg- of three segments and, like the maxilla, is inserted est component and forms the maxillary “body”. on a projection named the palpifer. On the stipes, two structures are differentiated Various types of muscles related to the labium apically, the lacinia (internal) and the galea (exter- exist. Those standing out most include the nal). The lacinia is usually well sclerotized and extrinsic muscles of the labium, the extrinsic and carries out alimentary type functions, while the intrinsic muscles of the palps, the retractors of the galea (having little sclerotization) develops func- glossae and paraglossae, and the median post- tions of a sensory nature. prelabial muscles. The maxillary palps are inserted in the stipes According to their position, various types on a piece named the palpifer or palpiger, and in of mouthparts can be distinguished. Orthogna- Hexapoda they exhibit a maximum number of thous or hypognathous mouthparts are situated seven segments (Archeognatha), a number that more or less perpendicularly to the cephalocau- tends to be reduced. In advanced groups of hexa- dal axis. Prognathous mouthparts are those pods there is a tendency for the cardo and even all in which the buccal area is situated in the of the maxilla to be incorporated into the ventral anteroventral part of the head and the mouth- face of the cranium, as occurs in larvae of parts are directed toward the front. The opist- Coleoptera and Diptera. In the basic model of the hognathous type is characterized by displaying maxilla two types of related muscles are clearly the buccal area situated in the posteroventral Mouthparts of Hexapods M 2499

Antenna Antenna Movable hook of palpus Eye Labrum

Palpus Eye

Proboscis Mentum Leg Maxillary palpus

Mouthparts of Hexapods, Figure 101 Orientation of insect mouthparts: hypognathous (left), prognathous (center), and opisthognathous (right). part of the head and the mouthparts directed Spheciformes)]. In the more advanced forms of toward the back, being situated during rest Hymenoptera, the maxillae and the labium are between the anterior legs. These terms are also elongated, giving rise to a sucking and licking used to define the head capsules. proboscis that serves to collect nectar. In this way a maxillolabial organ is differentiated, in which the maxillary stipes have the form of a sheath Chewing Mouthparts and surround the base of the labium. The glossae are united, forming a long structure that is the The mouthparts above described correspond to a functional part in the collection of nectar and basic model of chewing mouthparts. However, which certain authors call the ligula, the tongue, numerous modifications exist due to the lifestyle or the glossa proper. This structure is hollow, and and alimentary diet of the insects, resulting in an internally it is bathed in circulatory liquid, whose elevated number of types of mouthparts, although greater or lesser pressure allows its complete all fit into five types with certain variations in each extension or its retraction, which is aided by the (Figs. 101–104). action of special retractor muscles. When the bee is feeding, the ligula is alternatively extended and retracted, such that the alimentary fluid ascends Chewing-Sucking Mouthparts by capillarity through the central channel of the ligula (Fig. 105). Within the basic chewing mechanism, among the more important modifications are those related to the functions of licking or sucking, as occurs Piercing-Sucking Mouthparts in Hymenoptera. In these cases, the modifications affect the maxillae and the labium, with the This type of mouthpart is found in hematopha- mandibles developing functions of work and not gous Hemiptera and Diptera, although morpho- of trophic type [for example, in predatory wasps, logically they exhibit differences. In Hemiptera, whose females use the mandibles to construct the mandibles and the maxillae are transformed the nest and transport the prey (Hymenoptera: into more or less chitinized stylets that arise 2500 M Mouthparts of Hexapods

Vertex Flagellum Antenna Frons Pedicel Scape

Median ocellus

Face Anterior tentorior pit Basimandibular sclerite Frontoclypeal suture Mandible Clypeolabral suture Clypeus Labrum Maxillary palpus Maxilla Labial palpus

Mouthparts of Hexapods, Figure 102 Mouthpart components and their placement in a chewing insect (Orthoptera: Romaleidae).

Cardo

Submentum Stipes Palpifer Palpiger

Mentum Lacinia Subgalea Glossa

Paraglossa Galea

Palpus

Mouthparts of Hexapods, Figure 103 Labium of Palpus grasshopper (Orthoptera: Romaleidae).

separately from a gnathal bag and come near Mouthparts of Hexapods, Figure 104 Left maxilla toward the apex, such that the four stylets unite in of grasshopper (Orthoptera: Romaleidae). a fasciculus. The stylets are united along their length, the mandibles being external and the maxillae internal. Internally, these maxillary stylets an elongated structure (with one to four divisions) form two superimposed canals: one dorsal (gen- that forms a sheath protecting the stylets; the erally of greater diameter), which is the alimen- labial palps have disappeared. All of the mouth- tary canal, and the other ventral through which parts together form a “rostrum,” which in the the saliva flows. The labium is transformed into resting state is usually directed toward the back Mouthparts of Hexapods M 2501

Gena Clypeus

Labrum Mandible

Cardo

Lorum

Submentum

Mentum

Hypopharynx

Stipes Maxillary palpus

Paraglossa

Labial palpus Glossa

Flabellum

Mouthparts of Hexapods, Figure 105 Front and side view of chewing-sucking mouthparts (Hymenoptera: Apidae).

(opisthognathous condition). Although anatomi- which the mandibles and maxillae are short struc- cally the hypopharynx does not constitute a tures, which are finely toothed apically, and rudi- mouthpart, in hemipterans its distal part appears mentary labellar structures can be seen (Fig. 110). as a small lobe between the stylets. In the same way, the labrum (and its ventral epipharyngeal part) are situated in the anterior part (dorsal) of Sucking Mouthparts the same mouthpart (Figs. 106–109). In hematophagous Diptera, piercing-sucking This type of mouthpart is seen in Diptera, Cyclor- mouthparts are developed, with the mouthparts rhapha. All the mouthparts contribute, to a greater transformed into stylets, except the palps and labium. or lesser degree, to the formation of a proboscis, In addition, the females exhibit well developed man- whose interpretation is difficult due to the reduc- dibles, contrary to the males, in which they are usu- tion of the maxillae and to the great develop- ally atrophied. Also forming part of the “labial ment of membranous areas. Following the current complex” are the labrum, which has a channeled nomenclature accepted by the majority of authors, form, and the hypopharynx, which is flattened in the this proboscis consists of two morphologically and form of a lamella, also channeled, and in whose base functionally different zones: one in the basal posi- runs the salivary canal. Both structures are superim- tion, named rostrum or buccal cone, and the other posed and form a canal through which flows the distal, named haustellum, which ends in an oral blood collected from the wound produced by the disc (Fig. 111). injuring organs (mandibular and maxillary stylets). The rostrum morphologically pertains to the One variation of this type of mouthparts (named head capsule and dorsally carries the palps and a cutting-sucking) is found in Diptera, Tabanidae, in naturally cuticular structure named the fulcrum. 2502 M Mouthparts of Hexapods

Flagellum Antenna Pedicel

Clypeus Maxillary palpi

Labellum Compound eye Stylets Labium

Stylets Mouthparts of Hexapods, Figure 106 Mouthpart components and their placement in a piercing-sucking insect (Diptera: Culicidae).

Maxillary rod 1

Maxillary Labium 2 palpus Maxillary Labial groove stylet

Mandible Mandible Labellum Mouthparts of Hexapods, Figure 107 Components of mosquito mouthparts (Diptera: Culicidae).

In the base of this fulcrum is situated a small for- labella (lobes). These labella form an oral disc in mation in the form of a “U,” named the hyoid scler- their apical part, constituted by a series of canals ite, which serves to maintain the lumen of the for taking in fluids, named pseudotracheae. The cibarium. pseudotracheae maintain their light by a series of The haustellum is formed in the dorsal zone incompletely sclerotized and bifurcated rings in (anterior) by the labrum (and its ventral epipha- their apex, which give them an appearance of tra- ryngeal face) and the hypopharynx, being reinforced cheae, from which originates their name. The fluid in its ventral face (posterior) by the prementum, passes through the interbifid spaces, acting as a fil- which articulates with a labial rod like a furca, ter for the solid particles. When the proboscis whose branches form the endoskeleton of the begins to function, the rostrum is distended by Mouthparts of Hexapods M 2503 aerial sacs in its base and the haustellum through free part formed by the galeae. The apical part of extensor muscles. In addition, the labella become the stipes bears a palpifer prolonged into a gener- swollen through the internal pressure from the ally reduced maxillary palp, except in primitive circulatory liquid. The retraction of the proboscis families like Tineidae in which the palp is well is carried out by the appropriate muscles. developed and consists of five to six segments. The distal parts of the galeae, which are channeled in their internal side, are united by a system of hooks Siphoning-Sucking Mouthparts and spines. A suction tube for feeding named the spiritrompe or haustellum is thus formed. The This type of mouthpart is seen in Lepidoptera. The labium is greatly reduced and is partly membra- mandibles are generally vestigial or non-existent, nous, the same occurring with the hypopharynx, except that in some families of moths like Tinei- which is normally found fused to the internal side dae they are evident, although small. The maxillae of the labium. A nerve, a trachea, and two oblique comprise a basal part (formed by the cardo and muscular bundles run internally along the entire stipes) that is incorporated into the head, and one length of each half of the proboscis (Fig. 122). When the proboscis is at rest, it folds back in Mandible a spiral below the thorax. This coiling is possible Labial groove Hemocoel because although normally each part of the spiri- Hemocoel of mandible trompe is surrounded by incomplete sclerotized of maxilla rings, among them exist ample membranous Food channel Labium zones; in addition, the spiritrompe is very elastic. When the proboscis begins to function, it Salivary channel Hemocoel stretches so that circulatory liquid, whose pres- of labium sure is regulated by a valve situated in the stipes, penetrates its interior. A wide variation in the length of the spiritrompe exists, reaching the Mouthparts of Hexapods, Figure 108 Cross-section maximum in Sphingidae, in which in some indi- of piercing-sucking mouthparts (Hemiptera: viduals it can measure four times the length of Cicadidae). the body.

Compound eye

Antenna

Anterior tentorial pit Clypeus Base of mandible Mentum Unsclerotized labrum Sclerotized labrum Maxillary palpus Labellum of labium Maxilla

Mouthparts of Hexapods, Figure 109 Cutting-sucking mouthparts (Diptera: Tabanidae). 2504 M Mouthparts of Hexapods In addition to the basic models of mouthparts References mentioned, others exist that are highly specialized to different ways of life, those related to parasitism Bitsch J (1973) Morphologie de la tête des insects. Partie standing out, such as the case of the mouthparts of Générale. In Grassé, PP (Dir.) Traité de Zoologie VIII (I):3–100 Siphunculata and Siphonaptera. Koch M (2001) Mandibular mechanisms and the evolution of hexapods. Annales de la Societé Entomologique de France (N.S.) 37:129–174 Matsuda R (1965) Morphology and evolution of the insect head. Mem Am Entomol Inst 4:1–334 Quénnec E (2001) Insights into arthropod head evolution. Two heads in one: the end of the “endless dispute”? Ann Soc Entomol Fr 37:51–70 Snodgrass RE (1951) Comparative studies on the head of mandibulate arthropods. Comstock, Ithaca, New York, NY

Mud Daubers

Sceliphron spp. (Hymenoptera: Sphecidae) solitary wasps that create mud nests and provision them with spiders as a food supply for their young.  Wasps, Bees, Ants and Sawflies

Mulch

A layer of material placed on the soil to retard growth of weeds. In commercial crop production plastic is often used, whereas in the home garden organic materials such as leaves, straw, wood chips, Mouthparts of Hexapods, Figure 110 Sucking and pine needles are often used. mouthparts (Diptera: Muscidae).

Antenna

Ocellus Compound eye

Clypeus

Epipharynx

Labrum Galea Labial palpus

Mouthparts of Hexapods, Figure 111 Siphoning-sucking mouthparts (Lepidoptera: Sphingidae). Mulsant, Etienne M 2505 Müller, Johann Friedrich Theodor Venezia Giulia” and monographic works on ants, beetles, reptiles, etc. Müller led several expedi- “Fritz” Müller was born at Windischholzhausen, tions to Ethiopia and the Red Sea. He retired as Germany, on March 31, 1822. He entered the Uni- the director in 1941, but in 1953 published a versity of Berlin in 1841 with the intent of becom- large work on phytophagous beetles. Müller was ing a teacher, received his doctorate in 1844, and an eminent European entomologist during the commenced teaching in a gymnasium at Erfurt. In 1920s and 1930s, and he published 243 papers, 1852, Müller traveled to a German colony in Bra- mostly on Coleoptera. He died at Trieste on Sep- zil. Though it was a primitive existence, Müller tember 21, 1964. enjoyed his life in the colony, and again became a teacher, then a public officer, and finally a naturalist with the National Museum of Rio de Janeiro. In Reference 1863 Müller published “Für Darwin,” a treatise of support for Charles Darwin’s ideas. His studies on Herman LH (2001) Müller, Josef. Bull Am Mus Nat Hist insect coloration, published in 1879, became 265:112–113 famous and served as the basis for the concept of Müllerian mimicry. Müllerian Mimicry Reference Mimicry in which several distasteful organisms share a common appearance. Mutual aposematism. Papavero N (1971, 1973) Essays on the history of Neotropical Dipterology with special reference to collectors  Mimicry (1750–1905). Museu de Zoologia, Universidade de São Paulo Mulluscicide

Müller, Josef A pesticide used to kill slugs and snails.

Josef (Giuseppe) Müller was born at Zara, Dal- matia (now Croatia) on April 24, 1880. He Mulsant, Etienne obtained a degree in philosophy from Graz Uni- versity in 1902, and moved to Trieste, Italy. There, Etienne Mulsant was born at Mornant, France, on Müller joined the Società Adriatica and estab- March 2, 1797. He received his education at col- lished an entomological section of the society. leges in Belley, Roanne, and Tournon. He worked He intended, with the cooperation of others, to as a curator of the city library in Lyon, and as a complete an entomological survey of the area. professor of natural history at the Lyceum in Lyon, However, World War I broke out, and Müller was France. He worked at these two posts his entire drafted, and he worked on the biology of human life, and became a noted coleopterist who is lice, a vector of typhus. Müller returned to Tri- remembered as one of the world’s greatest authori- este after the war, and became conservator and ties on Coccinellidae. In addition to a monograph then director of the Trister Naturhistorisches on Coccinellidae (in 1866 and 1867), a most Museum. The museum flourished under his important publication was “The natural history of direction, particularly the entomology depart- Coleoptera of France” published in 37 parts from ment. Müller published many encyclopedic 1839 to 1884. His work was meticulous, and this works, such as “Catalogo dei Coleotteri della became a standard reference for many years. His 2506 M Multifunctional Semiochemicals publication list totals nearly 250 items. He died at vital – additional functions as chemical regula- Lyon, France, on November 4, 1880. tors of a large diversity of behaviors. Ultimately, this phenomenon has been described as “semiochemical parsimony” as a reflection of the great References adaptiveness of insects manipulating their exocrine products in the biological milieu. As will Essig EO (1931) A history of entomology. The Macmillan be described subsequently, the ability of insects Company, New York, 1029 pp Herman LH (2001) Mulsant, Etienne. Bull Am Mus Nat Hist to exploit a number of habitats is in no small way 265:114 correlated with the use of external secretions as multifunctional regulators of both intra- and interspecific interactions. Multifunctional Semiochemicals

Murray S. Blum The Parsimonious Activities of University of Georgia, Athens, GA, USA Eclectic Alarm Pheromones

A diversity of factors is undoubtedly correlated Alarm pheromones, which are used by both with the pronounced success of insects in both eusocial and solitary species, are generally terrestrial and aquatic environments. Signifi- produced during traumatic interactions that cantly, in the last several decades, identification result in dispersion or defense of the alarm pher- of a great variety of natural products (chemical omone producers. These pheromones, which are compounds) has resulted in an awareness of generally produced in much greater quantities the remarkable versatility with which insects use than other classes of pheromones, appear to be the products of their exocrine glands (external highly adaptive to function multifunctionally. secretions) to manipulate intra- and interrela- Because the pheromones are secreted in adver- tionships. A multitude of research investigations sarial confrontations, they possess some of the has demonstrated that insects and related arthro- same properties as defensive allomones, and pods have converted exocrine products to serve indeed, are believed to be derived from these multiple functions in diverse contexts. In addi- widespread defensive products. Alarm phero- tion, it has become clear that exocrine secretions mones can be visualized as an evolutionary or their individual compounds, which previously development from defensive compounds, the had been identified with a single function, often latter already being programmed for responses possess several roles which are highly adaptive to environmental perturbations. for their producers. In short, insects may exploit the secretions of a single gland for unrelated diverse roles which can include defense, sexual Activity Inhibitors attraction, and communication. The multifunctional compounds secreted by Some eusocial species have adapted their alarm insects are termed semiochemicals and primar- pheromones to regulate important social activi- ily include pheromones (communication chemi- ties in a variety of specific contexts. Honey bee cals) and allomones (defensive chemicals). These workers, Apis mellifera, suppress visitations of compounds, which have been identified in insect workers to nectar-depleted flowers by marking species in at least six orders, had previously been these flowers with 2-heptanone, an alarm pher- assigned single functions, but it is now evident omone produced in the capacious mandibular that they possess a variety of unsuspected – and glands. 2-Heptanone, along with isopentyl Multifunctional Semiochemicals M 2507 acetate (a sting-shaft compound), inhibit the exaggerated alarm response, resulting in disper- secretion of the worker Nasavov gland, an organ sion of the ants and rapid avoidance behavior by that plays a role in colony fission and swarming. the mutillids. The Nasanov secretion is highly attractive to Other ketones, regarded as highly stimulatory queens and workers in reproductive swarms but olfactants, have also been evolved by cock- in its absence foreign queens can be rejected. roaches to function as cryptic alarm pheromones. 4-Methyl-3-heptanone, the alarm phero- 2-Heptanone, a characteristic alarm pheromone mone of the fungus-growing ant Atta texana, of a variety of dolichoderine ant species, is pro- can be used to disrupt foraging on well-marked duced by both cockroaches (Platyzosteria spp.) trails in the presence of high concentrations of and beetles (Dyschirus spp.) and these rapidly the alarm pheromone. The ants cut leaf frag- moving solitary insects can escape the predatory ments that are normally carried to the nest to ants whose attack behavior is severely disrupted generate a fungal food source. Exposure to the by the cryptic pheromone 2-heptanone. 6-Methyl- alarm pheromone results in the workers drop- 5-hepten-2-one, another widespread alarm phero- ping their leaves and moving rapidly to the nest. mone of dolichoderine ants, is produced by the This behavior could be very beneficial if a pred- cockroach Neostylopyga rhombifolia, as further ator attacked the ants on their crowded foraging testimony of the frequent structural congruency trails. of the cryptic alarm pheromones of solitary insects and their ant predators.

Cryptic Alarm Pheromones in Solitary Insects Robbing Agents

Many species of solitary insects, when moving A robbing modus operandi, predicated on the uti- over the ground surface, are exposed to aggres- lization of idiosyncratic natural products, charac- sive ants that are capable of rapidly recruiting terizes the aggressive behavior of a variety of ants additional workers for en masse attacks. Some and tropical bees. These lifestyles, when analyzed, species of beetles, cockroaches, and mutillid have been demonstrated to be possible because wasps, as well as non-insect arthropods that the chemical agents secreted by these attacking have frequent encounters with these formicids, hymenopterans effectively disarm the host species. have evolved escape behaviors which are highly In all cases in which the disarming chemicals have adaptive as survival mechanisms. Indeed, it been identified, they have proven to be alarm appears that the basis for avoiding attacking pheromones. ants is identified with the use of cryptic alarm Workers of Lestrimelitta limao, a stingless bee pheromones by these solitary insect species. that constitutes a major raiding species in the Neo- 4-Methyl-3-heptanone, a characteristic alarm tropics, subdue other species of stingless bees by pheromone of aggressive ants in five subfamilies, secreting copious amounts of mandibular gland has been exploited by female mutillid wasps as a secretions on the raided nest. The secretion, domi- disruptive cryptic alarm pheromone that blunts nated by the powerful lemon-smelling compound the attacks of the formicids. The wasps are wing- citral, serves to disorient the host workers while less and they undoubtedly encounter foraging simultaneously attracting additional workers of ants with some frequency as they move over the L. limao. Resistance by workers of the host species ground with great cursorial speed. The wasps rapidly ceases and nest plundering is pronounced. secrete copious amounts of the pheromone from Citral proves to be the magic bullet for slaying cephalic glands and this compound causes an vulnerable species. 2508 M Multifunctional Semiochemicals At least two species in the ant genus Formica is widely distributed in myrmicine species. This use Dufour’s gland constituents to perform alarm pheromone initiates digging behavior in slave raids on susceptible species. The attack- the sandy soil in which these ants nest. Workers ing workers secrete alkyl acetates from their may be buried by cave-ins in the sand and their hypertrophied Dufour’s glands and these sim- pheromonal signals may be of great importance ple esters function to disarm the host workers, in signaling their dilemma to other workers. who become disorganized and incapable of organized resistance. Antimicrobial Alarm Pheromones

Alarm Pheromones as Trail Pheromones Insect species often develop in environments that are highly suitable for the proliferation of diverse Multifunctional parsimony characterizes the man- bacterial and fungal microorganisms. Inhibition dibular gland secretions of a variety of stingless of pathogenic growth is a sine qua non for insect bees in the American tropics. When examined in survival in environments that readily support detail, there is strong evidence that the secretions virulent bacteria and fungi. This is particularly of these bees are at least trifunctional. true of ground-dwelling ants, bees, and wasps, Citral is a major constituent in the mandibu- whose subterranean nests possess the high ambi- lar gland secretion of the bee Trigona subterranea. ent temperatures and relative humidities favored This compound, the dominant compound in the by microorganisms. exudates, generates well-developed trails when The southern green stink bug, Nezara viridula, deposited by workers. On the other hand, if the co-habits plants that contain the fungus Metarrhiz- secretion is deposited near the nest, intense alarm ium anisopliae, a particularly virulent insect pathogen. activity is released. Pure citral produces the same The alarm pheromones of N. virudula, (E)-2-hexenal response. Identical responses were obtained with and (E)-2-decenal, inhibit spore germination of this another Trigona species. entomopathogenic fungus, and this fungistatic activity is critical to maintenance of viable populations of the stink bug. Releasers of Digging Behavior Several alarm pheromones of ants have been demonstrated to be potently fungistatic. Citral, a Displacement behavior by some species of ants monoterpene produced by Atta spp., was as active results when workers undertake digging after against dermatophytes as some commercial fun- exposure to high concentrations of their alarm gicides but was not as active against insect and pheromones. The behavior may be highly adaptive plant pathogens. Two other characteristic ant for selected species. alarm pheromones derived from species in the The dolichoderine ant Conomyrma pyramicus subfamilies Myrmicinae and Dolichoderinae, releases alarm behavior in sister workers with a 4-methyl-3-heptanone and 2-heptanone, were pygidial gland product, 2-heptanone. Burial of also fungistatic but did not possess the inhibitory objects treated with high concentrations of this activity of the aldehyde citral. ketone result in workers rapidly burying them. Such behavior effectively removes a highly excitatory and disruptive stimulus from the ground surface. Alarm Pheromones as Attractants Another ant species, the myrmicine Pogono- myrmex badius, generates an alarm signal with Workers of ants and eusocial species of bees and 4-methyl-3-heptanone, a minty compound that wasps may mark assailants with alarm pheromones Multifunctional Semiochemicals M 2509 that function to attract additional workers to the in considerably greater quantities than other labeled individual. This attraction results in form- classes of pheromones, further emphasizing their ing aggregations around marked adversaries and is suitability as defensive allomones. Indeed, defen- highly adaptive in terms of developing a force of sive allomones and alarm pheromones share many combatants. Alarm pheromones have thus been common properties, a fact consistent with the sug- converted to recruitment stimuli whose binary gestion that the latter were derived from the for- functions – alarm and recruitment – interact effec- mer. This evolutionary scenario is predicated on a tively to develop group behavior as a first line of species’ preprogrammed behavioral response to a defense against adversaries, and prey as well. defensive compound to which it already has an Although alarm pheromones may certainly adaptive traumatic response. function as traumatic stimuli, these compounds Ants provide persuasive examples of how at low concentrations may also be used to pro- compounds demonstrated to be alarm phero- mote the formation of both combative and non- mones have been exploited by nonsocial insects as combative aggregations. For example, workers of defensive allomones. For example, 6-methyl-5- the ant Camponotus pennsylvanicus use the hydro- hepten-2-one, a typical alarm pheromone of carbon n-undecane, a defensive compound, to dolichoderine ants, is used by cockroaches in the orient excited workers to sources marked by their genus Neostylopyga as an effective deterrent. major alarm pheromone, formic acid. By contrast, Multifunctional alarm pheromones are wide- low concentrations of n-undecane can produce spread in eusocial insects, particularly species of long-term aggregations of workers. Similarly, low Hymenoptera and Isoptera. In ants and termites, concentrations of 2-heptanone, the alarm phero- characteristic monoterpenes such as limonene, mone of the dolichoderine ant Iridomyrmex pru- pinene, citral, citronellal, and 6-methyl-5-hepten- inosus, label the habitual feeding aggregations of 2-one function as effective chemical deterrents the workers. and, in addition, releasers of alarm behavior. In While aggregative agents such as n-undecane ants and bees, 2-heptanone is utilized as an allo- and 2-heptanone are at least bifunctional alarm mone-pheromone, as are 4-methyl-3-heptanone pheromones, it is certainly recognized that these and 3-octanone in many ants. compounds are, in reality, trifunctional pheromones, as are a wide variety of additional compounds. These pheromones are of great parsimoni- Sex Pheromones as Parsimonious Agents ous use as defensive compounds, in addition to their known roles as aggregative and alarm phero- A variety of insect species have adapted secre- mones. In essence, these semiochemicals clearly tory compounds with clearly established defen- possess diverse functions that reflect their adap- sive functions that also serve as sex pheromones. tive value in the social milieu. In addition to defensive compounds, in some hymenopterous species these sexual pheromones constitute versatile releasers and primers of Defensive Allomones as Alarm social behavior that are essential to colonial Pheromones organization.

If the defensive allomones of solitary insects are remarkably eclectic, it is also rather significant that Pheromonal Parsimony in the Honey Bee many of these compounds are structurally con- gruent with the alarm pheromones of eusocial A mandibular gland product of the queen honey bee, insects. Alarm pheromones are generally secreted Apis mellifera, has been demonstrated to possess a 2510 M Multifunctional Semiochemicals remarkable variety of functions both in the hive (about 70%) of 9-ODA in conjunction with sev- and outside the hive. (E)-9-oxo-2-decenoic acid eral other mandibular products of the queen. (9-ODA), designated as queen substance, is used Swarming of honey bee colonies is regulated by the queen as both a releaser (rapid-active by a potpourri of compounds produced by both behavioral modification) and a primer pheromone the queen and the workers. Swarm formation and (slow acting physiological modification). 9-ODA movement are regulated by monoterpenes gener- is distinctive in manifesting pheromonal activity ated in the Nasanov gland secretion of workers. with workers, virgin queens, and drones. In some Cavities marked with this secretion are highly cases, the pheromonal activity of 9-ODA is syner- attractive to the swarming workers, which attracts gized by additional compounds in the queen’s other workers for possible nest-site selection. mandibular gland secretion, and in some cases Swarm movement is enhanced by 9-ODA from these synergists are chemically related to 9-ODA. the queen, which functions as a short-range attrac- Queen cell construction is inhibited by the tant. By itself, 9-ODA has no swarm-orienting queens’ workers in the presence of 9-ODA and, in activity. addition, other mandibular gland constituents The parsimonious activity of 9-ODA is - fur including (E)-9-hydroxy-2-decenoic acid (9-HDA), ther revealed by its activity as a sex pheromone for an acid related to 9-ODA. Together, these two flying drones in pursuit of queens. Large clusters acids function as primer pheromones that inhibit of drones are attracted to single queens and queen cell construction, but neither acid is active multiple copulations are characteristic of the mat- alone. This inhibition is also expressed in workers ing behavior of queens. Unlike other pheromonal by immature queens in queen cells. In all cases, the contexts, 9-ODA, by itself, is highly attractive to workers must have contact with the queen in order drones in the aerial milieu. for her primer activity to be expressed. Several species of Heteroptera (Hemiptera) In addition to inhibiting queen cell construc- have been shown to produce sex pheromones tion, 9-ODA possesses another important primer in glands clearly identified as defensive organs. function. This acid, along with 9-HDA and other Females of the mullein bug, Campylomma ver- mandibular gland products of the queen, inhibits basci, produce sex pheromones in the metatho- ovarian development of workers, provided that racic scent glands, characteristic heteropterous they have physical contact with the queen. In addi- defensive organs. (E)-crotyl butyrate and butyl tion to these important roles as primer phero- butyrate, typical defensive constituents of true mones, the queen also regulates colonial functions bugs, function as highly active sex pheromones for by utilizing 9-ODA as a releaser pheromone for males. In contrast, males of the alydid Riptortus both workers and drones. 9-ODA is obviously a clavatus have adapted metathoracic gland constit- powerful mandibular gland product of the queen. uents to function as sexual attractants for females. Honey bee queens produce an olfactory Three esters, (E)-2-hexenyl-(E)-2-hexenoate, (E)- attractant for workers, signaling her presence to 2-hexenyl (Z)-3-hexenoate, and myristyl isobu- them. In essence, for worker honey bees this acid tyrate, are clearly bifunctional, possessing activities is both a powerful olfactant and a tactile stimulant. both as sex pheromones and defensive allomones. The versatility of 9-ODA as a chemical releaser of social behavior is demonstrated by its critical roles in the hive and in the exterior. Defensive Secretions as Sexual The formation of retinues, the attraction of Pheromones workers to the queen in the milieu of the hive, is mediated by 9-ODA. Maximum retinue develop- A variety of insects have adapted defensive exu- ment occurs in the presence of high concentrations dates to function as either female or male sex Multifunctional Semiochemicals M 2511 attractants. Since these sexual secretions still product is distinctive in being both a very rare exo- possess their original repellent functions, the crine compound and, in addition, a singular terpene evolution of these systems clearly constitutes whose toxicological effects are more pathological extreme semiochemical parsimony. The use of than any known compound produced by insects. characteristic defensive allomones as sex pher- Beetles in the family Meloidae, the major omones by species in at least four orders family producing cantharidin, are frequently emphasizes the widespread exploitation of insect referred to as “blister beetles” because of the pro- chemical defenses as sexual communicants. nounced lesions that result from dermal contact Both sexes of the staphylinid beetle Aleochara of these insects with human beings. While can- curtula produce an effective insect repellent in the tharidin (or a meloid) can constitute a powerful hypertrophied tergal gland. The glandular secretion external vesicant, its pathogenicity upon inges- is fortified with 1,4-benzoquinones, hydrocarbons, tion can be particularly devastating, usually and aliphatic aldehydes, a formidable mixture of resulting in the lining of the tongue, throat, and defensive allomones. Three compounds – (Z)-4- palate peeling away. Internal injuries can rapidly tridecene, dodecanal, and (Z)-5-tetradecenal – are eventuate in death as the corrosive effects of can- powerful male attractants and release strong cop- tharidin are manifested. Unlike most corrosive ulatory behavior in these insects. A female aphro- poisons, the deleterious effects of cantharidin are disiac sex pheromone from the epicuticular lipids not instantaneous, and the lag in apparent poi- acts synergistically with the tergal gland secretion. soning is a prelude to detecting the pathological On the other hand, high concentrations of the ter- action of the ingested terpene. gal gland secretion function as a repellent for the Cantharidin is released from the beetles sus- beetles, the secretion thus acting as a repellent. pended in blood by a process referred to as reflex The defensive secretion of the grasshopper bleeding. Weakened cuticular areas in the legs Taeniopoda eques has been adapted to function as “bleed,” and accumulated droplets of cantharidin- a sex pheromone with an important temporal com- fortified blood from the stimulated leg can be wiped ponent. The secretion is synthesized in glands sur- on adversaries with effective repellent results. This rounding the metathoracic tracheal trunks and is defensive method is not harmful to the beetles stored in the tracheal lumina. The odoriferous unless inordinate amounts of blood are lost as a defensive exudate is produced from the third instar consequence of extensive reflex bleeding. Clearly, on and constitutes the primary deterrent for a vari- the vesicatory properties of the anhydride make it ety of vertebrate and invertebrate predators. Signifi- a powerful vertebrate repellent. On the other hand, cantly, 16–18 days after adult eclosion the female of cantharidin, topically applied to pigs and humans, T. eques produces a potent sex pheromone in the effected remission of epidermal cancer. This - ter tracheal defensive secretion. Sexual synchrony is pene also is an effective feeding deterrent for insects, achieved because the males respond to the sex and its functional parsimony is further demon- pheromone about 16 days after adult eclosion. strated by the fact that it is a selective herbicide. Invasive fungi such as Trichophyton and Microsporum species are inhibited by cantharidin, A Highly Toxic Anhydride with and it has been suggested that this anhydride plays Pronounced Vesicatory Parsimony an important role in protecting meloid eggs, which are incubated in fungal-rich moist environments. Cantharidin, the anhydride of cantharidic acid, is a The egg of a meloid beetle is fortified with enough well-recognized toxin that is only known to be pro- cantharidin to act as a vesicant, a fact that is consistent duced by beetles in the families Meloidae and with its suggested role as a fungicide. Significantly, Oedemeridae. Thus, this relatively simple natural the cantharidin with which the female treats the 2512 M Multifunctional Semiochemicals eggs is a copulatory bonus, derived from the semi- Injection of the venom by stinging ant work- nal ejaculate of the male, delivered at copulation. ers results in rapid dermal necrosis, accompanied The adult female does not synthesize cantharidin, by the development of pruritic and sterile pustules. and the male ejaculatory contribution is not only These reactions to the venomous alkaloids are also critical reproductively, in terms of spermatozoa, but accompanied by considerable algogenicity, as a defensively as both a predator deterrent and an consequence of the liberation of histamine from antifungal agent applied to the eggs as an inhibitor mast cells. The alkaloids also have a rapid lytic of entomopathogenic fungi. effect on rabbit erythrocytes, instantly hemolyzing these cells. In addition, the piperidines possess considerable pharmacological activities that fur- Multifunctional Venom Alkaloids ther emphasize their parsimonious toxicological functions. These include the inhibition of ATPases, Insect venoms are generally endowed with high uncoupling of oxidative phosphorylation, reduc- concentrations of proteins that are often identified tion of mitochondrial respiration, and blocking of with allergic reactions in individuals that have been neuromuscular junctions. These activities, directed stung. On the other hand, hymenopterous species against vertebrates, demonstrate that these ven- in a variety of genera produce venoms that are omous constituents target a considerable variety thoroughly dominated by non-proteinaceous com- of biochemical systems in implementing their pounds that often possess diverse biological activi- toxicity. However, the semiochemical parsimony ties. Recent studies have demonstrated that these of these cyclic compounds is further demonstrated venomous constituents are often identified with by their toxic activities against a variety of micro- considerable multifunctionality. In essence, their organisms, fungi, and insects. poison gland products have been evolved to dem- The alkaloids possess well developed antifun- onstrate great parsimony in the biological milieu. gal and antibacterial activities and, in addition, Ants in the genus Solenopsis synthesize mix- these cyclic compounds are phytotoxic and strongly tures of 2,6-dialkylpiperidines, and in general, the insecticidal. The antifungal activities of the alkaloids venom composition may constitute 95% of these are very adaptive, since the interior of Solenopsis distinctive nitrogenous compounds. The major con- colonies is both humid and warm, environmental stituents in these venoms are alkaloids that are conditions that are very conducive to the growth of related to coniine, the hemlock-derived alkaloid that entomopathogenic fungi. Workers treat their larvae was drunk by Socrates as an imposed suicide. with alkaloids, and fire ant queens apply venom to 2,6-Dialkylpiperidines are found in the venoms of their eggs, and in both cases the antifungal activities species in several genera and, in the case of species of the alkaloids are of great significance. in a single genus such as Solenopsis, these alkaloids The insecticidal activities of the alkaloids are are qualitatively distinctive. These alkaloids are pres- quite pronounced, and in the case of termites these ent as cis-trans-mixtures with one or the other iso- venomous constituents are comparable in toxicity mers invariably predominating. A variety of alkaloids to some commercial insecticides. The alkaloids are are present due to the fact that the 6-alkyl group on very repellent to other species of ants; ant-ant

the piperidine ring may be C9, C11, C13, C13:1, C15, C15:1, competition for resources should strongly favor

and C17:1. In all cases, these alkaloidal venoms are the piperidine secretors. In addition, the workers products of ant species in the subfamily Myrmici- can discharge venom through the air by a phenom- nae, which includes the aggressive fire ants, whose enon known as gaster flagging, a highly adaptive common name refers to the reaction of humans to mechanism for repelling heterospecifics. The diverse the “hot” stings delivered by the workers attacking pharmacological activities of the Solenopsis en masse. alkaloids, in combination with the insecticidal Muscid Flies M 2513 and antifungal properties of these cyclic piperi- Murine Typhus dines, further emphasizes the great semiochemical parsimony of these compounds. A rickettsial disease (Rickettsia typhi) affecting  Allelochemicals primarily rats, but sometimes transmitted from  Alarm Pheromones rats to humans by fleas and rat lice through their  Pheromones feces. The insects are not affected, and the mortal-  Sex Attractant Pheromones ity rate is low in humans less than 50 years old. It is  Social Insect Pheromones also known as “endemic typhus.”  Lice References

Blum MS (1981) Chemical defenses of arthropods. Academic Murray Valley Encephalitis Press, New York, NY, 232 pp Blum MS (1996) Semiochemical parsimony in the Arthro- An arbovirus transmitted by mosquitoes and indig- poda. Annu Rev Entomol 41:353–374 enous to Australia and Papua New Guinea. It also is Buschinger A (1972) Giftdrussensekret als sexual pheromon bei der ameise Harpagoxenus sublaevis. 313–314 known as Australian encephalitis, and is harbored Koch RB, Dessaiah D, Ahmed K (1977) Effect of piperi- in wading birds. It is caused by a virus in the family dines and fire ant venom on ATPase activities from Flaviviridae. It causes fever, nausea, seizure, diar- brain homogenate fractions and characterization of Na + -K + ATPase inhibition. Biochem Pharmacol rhea, lethargy and confusion. Most victims do not 26:983–985 suffer significant symptomology, but of those that Schmidt JO, Slessor KN, Winston WL (1993) Roles of Nasanov do, severe neurological damage may occur. and queen pheromones in attraction of honeybee  Mosquitoes swarms. Naturwissenschaften 80:573–575  Mosquitoes as Vectors of Viral Pathogens Multiparasitism Musapsocidae Attack of an insect by two or more species of parasitoids (multiple parasitism). A family of psocids (order Psocoptera).  Bark-Lice, Book-Lice or Psocids Multiple Resistance (to pesticides)

The resistance of an organism to a number of dif- Muscardine ferent pesticides, requiring different mechanisms of counteracting their effects. A term used generally in connection with those mycoses of insects in which the fruiting of the Multivoltine pathogenic fungi arise on the exterior of the insect. A number of fungi are capable of causing this condition. Having several generations per year.  Fungal Pathogens of Insects Mummy Muscid Flies The remains of an aphid whose insides have been consumed by a parasitoid. A dried, shriveled fruit Members of the family Muscidae (order Diptera). or nut.  Flies 2514 M Muscidae Muscidae Department of Agriculture provided funds for the Commonwealth Institute of Biological Control A family of flies (order Diptera). They commonly (now CABI Bioscience) to extend the search across are known as muscid flies. Europe from western France to Austria. As a result  Flies of this search, selected insects were imported and screened under quarantine to determine their development and feeding range (host specificity). Muscoid Larva Two imported weevils that passed the screening tests were subsequently released and have become A larval body form that is headless, and spindle- well established in North America for musk thistle shaped or cylindrical and truncate. It occurs in control. most Diptera.

Rhinocyllus conicus Froel (Coleoptera: Mushroom Bodies Curculionidae)

Fiber tracts within the protocerebrum, also known This was the first insect released in North America as the corpora pendunculata, that are major inte- for musk thistle control. It was collected from the grative centers. Rhine Valley in France and released in Canada in  Nervous System 1968. In 1969, it was introduced into California, Virginia and Montana, and subsequently relocated to many of the other contiguous states in the Musk Thistle Suppression Using United States. This weevil is a native of southern Weevils for Biological Control and central Europe, North Africa, and western Asia between latitude 30 and 52 north. The adults L. T. Kok are dark brown in color and 10–15 mm long. Virginia Polytechnic Institute and The adult hibernates in winter and becomes active State University, Blacksburg, VA, USA again in mid to late April. Soon after emerging in spring, the female starts to lay eggs on the Musk thistle, Carduus thoermeri Weinmann = bract leaves of thistle heads. Each female lays Carduus nutans L. (Campanulatae: Asteraceae) is about 100–200 eggs. The eggs are brown specks an invasive Eurasian weed that has become wide- 0.5–1 mm in diameter, and hatch in 6–9 days. spread in the contiguous United States. It repro- Newly hatched grubs (larvae) feed through the duces by seed and was first reported in the United bracts and into the base of the developing thistle States in 1953 in Harrisburg, Pennsylvania. Being bud. Thus, it is often referred to as the thistle head a highly competitive weed, it has replaced much of weevil. Feeding by the weevil grubs prevents the the native vegetation in pastures, rangelands, crop- production of viable thistle seeds. Many grubs lands, and along state highways in many parts of feed and complete development to the quiescent the USA and Canada. Its success is due to its pro- (pupa) stage in about 6 weeks within a thistle lific seed production, seed longevity, and lack of head. It is during this feeding stage that the thistle natural enemies to suppress it. As it spread rapidly heads are destroyed and fail to produce the usual in the absence of any native insects capable of sup- number of seeds. The quiescent stage is spent pressing it, the United States Department of Agri- inside the thistle head, where many pupation culture started a program in search of its natural chambers are formed. Each full-grown grub forms enemies in Italy in the early 1960s. The Canada a pupation chamber for its development into a Musk Thistle Suppression Using Weevils for Biological Control M 2515 pupa. The quiescent stage lasts for 7–10 days plants. It was officially approved for field release before emergence of the next generation adult in Virginia in June 1974. It became established in weevil. The new adults emerge in July/August and Virginia in 1977 and has since been relocated to do not stay on the plants for very long. They seek many of the mainland states. This weevil passes shelter from the summer heat and pass the sum- the winter in the adult, egg, and grub stages. The mer in one place in a state of torpor or inactiv- adult is about 10 mm long and emerges in late ity, and then hibernate in the winter to emerge in winter and early spring. It lays eggs within the the spring at the time of thistle elongation. There mid-rib on the underside of the leaves, usually is usually one generation a year. Once it has in clusters of two or three. The eggs hatch in become successfully established, this thistle head 10–12 days and the young grubs feed within the weevil can suppress musk thistle stands in 5–6 mid-rib towards the center growth point of the years (Fig. 112). thistle rosette. The grubs reach the thistle crown in about 7 days and continue feeding within the same place causing localized death of the crown tissues. Trichosirocalus horridus (Panzer) On completion of feeding in 6–8 weeks, the full- (Coleoptera: Curculionidae) grown grub leaves the plant and changes into the pupa in the soil within a chamber made from soil This was the second weevil released for thistle particles and organic matter. The quiescent (pupa) control in North America. It is native to south and stage lasts for 12–20 days. The newly emerged central Europe. Unlike the first weevil, this insect weevil is reddish in color, and it changes to dark feeds on the crown tissues of thistles in the rosette brown and black with time. The new generation of stage, before plant elongation. This crown or adults appears in May and June, and goes into heat rosette weevil was imported from Rome, Italy, into induced inactivity in July until the fall, when they the USA in 1970–1972 for quarantine tests to emerge to feed. Some females begin to lay eggs determine what type of plants it would feed on. until the first frost. There is usually one generation Thirty-five species of plants from seven families, per year. Successful suppression of musk thistle by including 12 economically important crop plants this weevil takes 4–6 years (Fig. 113). were tested. After undergoing 3 years of intensive testing, it was found to feed only on a narrow range of plants and would not be a threat to non-target

Musk Thistle Suppression Using Weevils for Musk Thistle Suppression Using Weevils for Biological Control, Figure 112 Thistle head weevil, Biological Control, Figure 113 Thistle rosette Rhinocyllus conicus adult. weevil, Trichosirocalus horridus adult. 2516 M Mutagen With the successful field establishment of Kok (1986) Impact of Trichosirocalus horridus (Coleoptera: these two weevils, thistle reductions exceeding Curculionidae) on Carduus thistles in pastures. Crop Prot 5:214–217 90% of the original density have been achieved in Kok LT (1998) Biological control of musk and plumeless many of the release sites. Because they attack dif- thistles. Recent Res Dev Entomol 2:33–45 ferent growth stages of the thistle plant, these two Sieburth PJ, Kok LT, Lentner M (1983) Factors influencing the weevils complement each other. Successful bio- effectiveness of Trichosirocalus horridus (Coleoptera: Curculionidae) in the control of Carduus thistles. Crop logical control of musk thistle is partly due to the Prot 2:143–151 good synchronization of plant growth and insect activity. Long term trend lines of musk thistles at sites under study have shown distinct declines in Mutagen thistle populations despite some occasional spikes due to resurgence of the weed population. Factors A chemical or physical agent able to induce a that cause resurgence of thistles include: (i) dump- mutation in a DNA molecule. ing soil with thistle seeds into the site, (ii) exposing soil when trenches are dug in the field, (iii) overgrazing leading to bare patches of soil where Mutant thistle seeds can germinate, or (iv) frequent sharp temperature fluctuations during the winter that An organism expressing the effects of a mutated result in high mortality of the weevils during win- gene in its phenotype. ter. Also, cool temperatures which favor thistle growth in spring, but inhibit weevil activity, could lessen sustained pressure on the weed. Despite Mutation such occurrences that cause temporary resurgence of thistles, the established weevils eventually regain A change in the nucleotide sequence of a DNA control. Both weevils are highly successful in con- molecule. Mutations can involve duplications, dele- trolling musk thistle. Their impact is evident after tions, inversions, translocations, and substitutions. 5 or 6 years of establishment. In places where the weevils multiply rapidly, a dramatic decline in musk thistle is possible after 2 or 3 years. Thistle Mutillidae suppression also is enhanced by planting tall fescue grass in thistle-infested land or pastures in A family of wasps (order Hymenoptera). They conjunction with the use of weevils. The fescue commonly are known as velvet ants. grass is able to effectively compete against thistles,  Wasps, Ants, Bees and Sawflies especially when the latter is weakened by the weevils. Mutual Interference

References Interference among predators leading to a reduced consumption rate by individual predators.

Kok LT, Surles WW (1975) Successful biocontrol of musk thistle by an introduced weevil, Rhinocyllus conicus. Environ Entomol 4:1025–1027 Mutualism Kok LT, Ward RH, Grills CC (1975) Biological studies of Ceuthorhynchidius horridus (Panzer), an introduced weevil for thistle control. Ann Entomol Soc Am An association between different types of organ- 68:503–505 isms that benefits both. Myiasis M 2517 Mycangium Mycotoxin

In bark beetles, a pocket-shaped receptacle used to A toxin produced by fungi. carry symbiotic fungi. Mycteridae Mycelium A family of beetles (order Coleoptera). They com- The hypha or mass of hyphae that constitutes the monly are known as palm beetles. body of a fungus.  Beetles

Mycetocyte Mydas Flies

A cell containing intracellular mutualistic and Members of the family Mydidae (order Diptera). commensalistic microsymbiotes; one of many cells  Flies making up the mycetome. Mydidae Mycetome A family of flies (order Diptera). They commonly In various invertebrate animals, the structure or are known as mydas flies. organ which houses symbiotes; the cells making  Flies up the mycetome and containing the symbiotes are known as mycetocytes. Myerslopiidae

Mycetophagidae A family of bugs (order Hemiptera, suborder Cicadomorpha). A family of beetles (order Coleoptera). They com-  Bugs monly are known as hairy fungus beetles.  Beetles Myiasis

Mycetophilidae M. D. Soler Cruz University of Granada, Granada, Spain A family of flies (order Diptera). They commonly are known as fungus gnats. This term was first used in 1840 to refer to  Flies human diseases originating from dipterous (fly)  Fungal Gnats larvae. More recently, it has been described as the infestation of live vertebrate animals with fly larvae, which, at least for a certain period, Mycosis feed on the host’s dead or living tissue, liquid body substances, or ingested food. Myiasis Any disease caused by the presence of fungi. begins when gravid female flies are attracted by 2518 M Myiasis the odors of infested wounds, decaying organic without being digested, and cause abnormal diges- matter, feces, urine, and human food, where they tive reactions in hypersensitive hosts. They also can deposit larvae or eggs. There are two principal develop directly in feces or urine-impregnated ways to classify myiasis: entomologically and materials, or badly stored food. Accidental myiasis anatomically. is usually caused by flies in the family Muscidae. It is important to be able to distinguish these larvae because in sensitive hosts, they can produce An Entomological Classification of digestive disorders, causing symptoms similar to Myiasis food poisoning. Also, larvae can be found in feces or improperly washed clothing of babies, and produce Myiasis can be classified according to the relation- cases of false parasitism. ship or level of dependence between the larvae and the host: An Anatomical Classification of Myiasis Specific or Obligatory Myiasis Myiasis also can be classified according to ana- This is caused by flies that can develop only on live tomical position, or location, in and on the host. hosts. Included in this group are members of Oestridae and Sarcophagidae. Dermal or Subdermal Myiasis

Semi-Specific or Facultative Myiasis In this condition, larvae are found between the epidermis and dermis. Invasion of animal or This is caused by facultative or opportunistic para- human skin tissues by the larvae causes tun- sitic flies with larvae that usually develop on decay- nels or boils in the dermal layers, and the flies ing organic matter, but with adults that also may may invade and enlarge existing wounds, or deposit their larvae or eggs in live tissues. There even form wounds themselves. This condition are two levels: primary myiasis, wherein the flies has also been called foruncular, traumatic or are able to initiate myiasis (they attack living tis- cutaneous myiasis. Flies in the families Calli- sues) or they can invade living tissue after other phoridae and Sarcophagidae produce dermal species have initiated the myiasis; and secondary and subdermal myiasis, particularly Cochlio- and tertiary myiasis, which occurs when the host myia hominivorax, Chrysomya bezziana, Ch. is nearly dead. Flies in this category include mem- albiceps, Lucilia sericata, Calliphora vicina, bers of Calliphoridae and Phoridae. Phormia regina, Protophormia terraenovae and Wohlfahrtia magnifica. Also, the fly Megaselia ruficeps (Phoridae) is a facultative parasite Accidental, Pseudomyiasis or False with larvae that can invade wounds or foul- Myiasis smelling sores.

Larvae of these species are normally free-living and non-parasitic, but may be ingested accidentally. This Intermedia Anatomical Position Myiasis happens when flies deposit eggs on food with pun- gent odors, eggs hatch, and larvae are ingested. Once Some species of Oestridae cause myiasis of ingested, they can pass through the digestive tract rodents, lagomorphs, and also humans in North Myiasis M 2519 America. Larvae create boil-like swellings on the Migratory Myiasis skin. The most important isDermatobia hominis. It is an important cattle pest in Central and This condition is displayed by Hypoderma spp., South America, and also affects humans. In the larvae of which migrate from oviposition sites Africa, Cordylobia anthropophaga (Calliphori- by subcutaneous routes and in nerve tissues to the dae) causes African foruncular myiasis, a condi- back, where they develop into “warbles” which tion very similar to that caused by Dermatobia spoil the host’s hide. hominis in the western hemisphere, in dogs, other domestic animals, and humans. Intestinal Myiasis

Creeping Myiasis This is caused by Gasterophilus spp. developing in the digestive tract of horses. This condition can be Larvae of Oestridae also can create a condition found worldwide. called creeping myiasis. These are able to move long distances within the host’s body, and typically are found in different anatomical positions. The Atypical Sanguinivorous Myiasis following arrangement has the fly species sorted by site of larval development: This unusual condition is caused by the ectoparasitic African fly Auchmeromyia luteola (Calliphori- dae). Larvae do not live on, or in, the host because Ocular Myiasis the female deposits her eggs on the soil floor of primitive huts. There, larvae suck the blood of sleep- The eye is invaded by Oestrus ovis, Rhinoestrus ing humans. They also feed on burrow-dwelling purpureus, Megaselia scalaria, Wolfahrtia mag- animals. After feeding, the larva returns to the soil. nifica and Sarcophaga carnaria. Diagnosis Aural Myiasis Diagnosis of myiasis is normally based on larval The ear is invaded by O. ovis and W. magnifica. characteristics, though it may be possible to raise the adults. Females deposit eggs (oviparous species) or larvae (larviparous). They may select organic matter Nasal Fossae (nostrils), Mouth, Frontal for oviposition (accidental parasites) or a wound, Sinuses Myiasis and Surface of Brain mucous membrane or natural body opening (obligate parasites). Larvae immediately begin to feed by Flies associated with these tissues are W. magnifica, burrowing into the tissues (obligate parasites) or in S. carnaria, Calliphora vomitoria, O. ovis and the soil (accidental parasites). When they feed in the R. purpureus, Cephalopina titillator. tissues, the wounds are enlarged and deepened, resulting in extensive tissue destruction. The larvae lack legs (a), and are pointed at the anterior (head) Urogenital, Anal and Vaginal Myiasis end, and broader and truncate at the posterior end. The larvae molt twice, resulting in three instars. At Flies associated with these tissues are W. magnifica, the end of the third instar, the mature larva leaves S. carnaria and Sarcophaga haemorrhoidalis. the tissues, falls to the ground, and burrows into the 2520 M Myiasis ground to pupate. Flies pupate within the old cuticle A. bequaerti of the third instar larva, a structure called a pupar- A. choerophaga ium. Adult flies emerge from the puparium, feed and A. luteola (Congo Floor Maggot) mate, and commence reproducing. A. redi The head of larvae of cyclorraphous flies The Auchmeromyia species are African, with (infraorder Cyclorrapha, the “higher” flies) is greatly A. bequaerti and A. luteola distributed in the Congo, reduced; the antennae, palpi maxillae, and labium and A. redi present in the Sudan. The adults are are scarcely visible. A cephalopharyngeal skeleton is 8–13 mm in length, with a yellow-brown or orange evident (b) in developing larvae, and sometimes body and legs. The distal part of abdomen is black. varies among species. It consists of the anterior- The diet of the adults appears to be human feces and most mouth hooks or mandibular sclerite, which fermented vegetables. Females also are attracted to articulates with the hypostomal or intermediate wild animal feces. There are three larval stages. All sclerite, behind which is the much larger basal or they are blood-sucking. The red ingested blood pharyngeal sclerite. In carnivorous species, other shines through the body-well. Under normal condi- small accessory oral sclerites are present (Fig. 114). tions a meal is taken every night. Auchmeroyia cho- For a specific diagnosis, the posterior spira- erophaga and A. redi do not normally enter human cles, found in the last abdominal segment of the habitations and live in association with wild animals, third instar (c), should be used. This segment though A. luteola attacks humans. The mature larvae should be removed with a scalpel under a stereo- attain a length of 18 mm, with 12 body segments. microscope. The spiracles should be removed from Laterally, they each bear two or more protuberances the cavity, and excess tissue removed. They should with a spine directed posteriorly and a small pit. The be placed on a slide with a drop of water and ventral portion of the body is flattened. The last body examined with a light microscope. The following segment bears five pairs of finger-like protuberances. structures should be examined in order to make a In the posterior spiracle region, the two small correct diagnosis: the ecdysial scar, interspiracular perimetral plates are widely separated (e). processes, peritremal ring, spiracular plate, and Genus Calliphora Rob-Desvoidy (Bluebottle spiracular openings (d) (Fig. 114). Flies) (D; AT/F; UO) C. albifrontalis C. augur The Taxa Responsible for Myiasis C. croceipalpis C. erythrocepala Following is a list of the principal families, genera, C. hilli and species of flies known to cause myiasis. After C. hortona each genus, the tissue of the host affected by the C. icela flies is designated as AT/F = alimentary tract/ C. nociva excreted with the feces; BS = blood-sucking; C. nothocalliphoralis D = dermal layers; HC = head cavities; UO = uro- C. quadrimaculata genital organs. C. stygia C. vicina C. vomitoria Family Calliphoridae – Blowflies or TheCalliphora species are cosmopolitan. Callipora Bluebottle Flies icela and C. nothocalliphoralis are present in New Zealand sheep; C. nociva, C. quadrimaculata and Genus Auchmeromyia Brauer and Bergen- C. stygia are found in Australian sheep. There are cer- stamm (BS) tain similarities among the species: C. albifrontalis Myiasis M 2521

a ps b ms

hs or

c Interspiracular d processes Peritremal ring

Spiracular openings Pharyngeal sclerite Spiracular plate Ecdysial scar

e fgh

i jkl

m nop

q rst

Myiasis, Figure 114 Characters used to identify fly larvae causing myiasis: (a) typical maggot, with the anterior end pointed and the posterior end blunt; (b) cephalopharyngeal skeleton (ms, mandibular sclerite; ps, pharyngeal sclerite; hs, hypostomal sclerite; os, oral sclerite); (c) view of the posterior end of a cyclorraphous maggot; (d) close-up of posterior spiracle; (e) spiracle of Auchmeromyia sp.; (f) spiracle of Calliphora sp.; (g) spiracle of Chrysomya sp.; (h) spiracle of Cochliomyia sp.; (i) spiracle of Cordylobia sp.; (j) spiracle of Lucillia sp.; (k) spiracle of Prophormia sp.; (l) spiracle of Musca sp.; (m) spiracle of Cuterebra (Dermatobia) sp.; (n) spiracle of Gasterophilus sp.; (o) spiracle of Hypoderma sp.; (p) spiracle of Cephalopina (Oestrus) sp.; (q) spiracle of Pharyngomyia sp.; (r) spiracle of Rhinoestrus sp.; (s) spiracle of Sarcophaga sp.; (t) spiracle of Wohlfahrtia sp. 2522 M Myiasis is similar to C. hilli and C. stygia; C. augur is simi- equivalent of Cochliomyia in the New World. There lar to C. nociva; C. croceipalpis is similar to C. are some similarities among species: C. mallochi is vicina; C. hortena is similar to C. quadrimaculata. similar to C. megacephala and C. putoria is close to C. The adults are 5–12 mm in length, with a black tho- chloropyga and C. rufifacies. The adults are 5–10 mm rax and legs. The abdomen is a dark metallic blue in length. They possess a metallic green body, with color. The female’s eyes are further separated than blackish bands in the posterior margin of the abdom- that of the male. In both sexes, the buccae are yellow inal segments, and with reddish-brown to blackish or orange, darkened posteriorly. The females are legs. The buccae are partially yellow. Chrysomya albi- attracted to decaying matter for oviposition. Most ceps is a facultative species, normally laying eggs on species are oviparous, but some deposit larvae, and carcasses, but the adult can deposit larvae on wounds. others deposit eggs if the weather is cool and larvae It is involved in secondary myiasis of sheep. Chry- during hot months. Calliphora vicina may be a pri- somya bezzina is an obligate parasite in wounds. mary invader, though C. vomitoria is involved only Females oviposit on live mammals, in wounds or in secondary myiasis. There are three larval instars. body orifices (ear, nose or urogenital orifices). The mature larvae are about 19 mm in length, with The mature larva is about 18 mm in length, twelve body segments, and with spinose bands and possesses long processes on the dorsal and lat- characteristically arranged according to species. eral sides of the body. The ventral processes are The cephaloskeleton bears an accessory oral scler- shorter. Chrysomya albiceps and C. rufifacies have ite. Each posterior spiracle is in a closed peritreme fleshy body projections; those of C. varipes are which shows an ecdysial scar and three slits (f). smaller. In the posterior spiracle region the peritre- Genus Chrysomya Rob-Desvoidy (Old World mal ring is broadly open (g). The ecdysial scar is Screwworm Fly) (D; AT/F; UO) present or absent according to species. Larvae C. albiceps hatch and molt twice. Larvae then drop to the C. bezziana ground to pupate. Myiasis has been found in C. chloropyga humans, cattle, water-buffalo, sheep, goats, horses, C. inclinata donkeys, dogs, camels and elephants. Chrysomya C. mallochi chloropyga is involved in primary and secondary C. marginalis myiasis; C. inclinata and C. marginalis are common C. megacephala (Oriental Latrine Fly) in carrion, but rarely have been found in wound C. putoria myiasis. Chrysomya putoria has been involved in C. rufifacies primary and secondary myiasis; C. putoria was C. varipes reported in Guinea in a case of traumatic myiasis. The Chrysomya species are restricted to Europe, Chrysomya megacephala has been found in large Africa, Asia, and the Australian region. Chrysomya numbers around latrines because they breed in albicens is present in northern Africa, southern feces and other decomposing organic matter. They Europe and northwestern India; C. chloropyga is an also are present near slaughter-houses, and open- African species; C. inclinata is found in Africa; and air meat and fish markets. They can accidentally C. mallochi occurs in Australia and New Guinea. produce human and animal wound myiasis in Chrysomya marginalis is common in human and Africa. Chrysomya varipes is a carrion-breeder, and animal wound myiasis in Kenya and Madagascar; also is temporarily predatory on other fly larvae. C. megacephala is a Chinese, Japanese and Austra- Genus Cochliomyia Townsend (New World lian species; C. putoria was reported in Guinea Screwworm Flies) (D) (Africa); C. rufifacies is a species of Australasia and C. americana the Orient; and C. varipes is an Australian species. C. hominivorax Chrysomya in the Old World is the ecological C. macellaria Myiasis M 2523 This genus is the New World equivalent of the and New Zealand. Lucilia cuprina is responsible of genus Chrysomyia in the Old World. Cochliomyia wound myiasis in South Africa and Australia, and homnivorax, formerly found in the United States, L. illustris in North America. Lucilia porphyrin has Mexico, and northern Africa, it is now restricted to been found in India; L. richardsi is common in portions of Central and South America. It was Great Britain, Finland and France and L. sericata eradicated from most of North America and from occurs in Europe and North America. Lucilia Africa by continuous release of sterile male flies. ampullacea and L. illustris have been confused Cochliomyia hominivorax females lay their eggs on with L. caesar. Lucilia porphyrin is similar to the wounds of humans and animals. In contrast, L. ampullacea, and L. richardsi to L. sericata. Adults C. macellaria is a secondary invader, and generally are 5–10 mm in length. The adult fly is metallic- is present only in carrion. The posterior spiracle coppery green. Females lay their eggs on carcasses, can be seen in (h). in neglected, suppurating wounds, and in sheep Genus Cordylobia Grünberg (African Tumbu wool soiled by urine, feces or blood, in which the Fly) (D) larvae can complete its development. Other ani- C. anthropophaga mals affected are horses, cattle and humans.Lucilia C. rodhain ampullacea, L. caesar and L. illustris breed in car- C. ruandae rion. The adults are diurnal. Females need a pro- Cordylobia anthropophaga is found in Africa south tein-containing meal for the eggs to mature. Lucilia of the Sahara. It is a myiasis-causing fly similar to bufonivora is an obligatory parasite of amphibians. Dermatobia hominis from the Americas. The adult The mature larva attains a body length of up to measures 6–12 mm in length. It is a stout, yellow- 16 mm. The posterior spiracles possess a narrow brown fly bearing black, undefined bands on the peritreme which, in fully sclerotized specimens, thorax and abdomen. The legs and face are yellow. shows inner tubercles on the upper margin of the The mature larva is 13–15 mm in length, with a posterior cavity approximately equal to the dis- cephaloskeleton bearing two projecting, hook- tance between the inner and median ones (j). shaped labial sclerites. The posterior spiracles consist Genus Phormia Rob-Desvoidy (D) of three sinuous slits situated on a weakly sclero- Ph. regina tized peritreme (i). Larvae cause foruncular (cuta- Ph. terraenovae neous) myiasis in dogs, rats and humans. Cordylobia Phormia species occur in the New World. Phormia rodhain parasitize wild animals and humans. The regina is present in the southern United States, pupae of C. ruandae are found in tree-nests of the whereas Phormia terraenovae is common in north- rodent Grammomys dolichurus (Forest Mouse). ern Canada. Phormia regina usually breeds in car- Genus Lucilia Rob-Desvoidy (Greenbottle rion, and possibly can be found in wounds. Flies) (D) Phormia terranovae is saprophagous, and prefers L. ampullaceal low temperatures and high altitudes for breeding. L. bufonivor The adults possess a black or bluish-green thorax L. caesar and abdomen. L. cuprina Genus Protophormia Townsend (D) L. illustris Pr. terraenovae L. porphyrin Protophormia terranovae is found in the cooler parts L. richardsi of the Holarctic region, and is involved in wound L. sericata myiasis in Europe and North America. It breeds in L. silvarum carrion or wounds, attacking cattle, sheep and rein- The Lucilia species are widespread. Lucilia caesar deer. Pr. terranovae appears in the early sprints. Sev- is found in North and South America, Australia eral samples also have been found in bird’s nests, 2524 M Myiasis causing myiasis in the nestlings. It has been taken The Cuterebra species, of which there are within 550 miles of the North Pole. Adults are many, occur only in North America. In appearance 6–11 mm in length. They possess a dark metallic and biology, they are very similar to Dermatobia. blue, green or black body with black legs. The mature They are found beneath the skin of rabbits, rodents, larvae are 17 mm in length. The posterior segment cats and dogs, but rarely in humans. bears fairly pointed tubercles. The posterior spiracle Genus Dermatobia Brauer shows a weakly developed ecdysial scar. D. hominis Dermatobia species occur in Central and South America. Only D. hominis is important. The adult Family Muscidae – (Houseflies) is 15–18 mm in length, with a yellow and black face, black and blue thorax, and metallic blue and Genus Musca Linnaeus (D; AT/F; UO) violet abdomen. The larvae are found beneath the M. crassirostris skin, and produce large swellings. The female uses M. domestica blood-feeding arthropods, primarily mosquitoes M. hilli but also ticks, to transfer eggs to the skin of humans The distribution of Musca species is variable, with and other animals, cattle, dogs, pigs, and cats. The M. domestica cosmopolitan in distribution, whereas posterior spiracle can be sen in (m). M. hilli is found in Australia. Musca hilli is similar Genus Gasterophilus Leach (Dark-Winged Horse to M. domestica, and they measure 6–9 mm in Bot Flies) (D; AT/F) length. These species are not involved in traumatic G. equi myiasis cases. Musca crassirostris breeds in cow G. flaviceps and horse dung. Musca domestica can serve as a G. gedoelsti mechanical vector of disease, but the larvae feed G. haemorrhoidalis and molt in decomposing organic matter. Musca G. inermis domestica has a remarkably high reproductive G. intestinalis capacity; it is estimated that (in the absence of G. lativentris mortality) a population of 100 eggs hatching on G. meridionalis the 1st of May could reach 4,000 trillion speci- G. nasalis mens on the 30th of September. The larval length G. nigricornis is about 12 mm, and the larva is creamy white. The G. pecorum posterior spiracle region has three tortuous slits. G. ternicinetus G. veterinus Family Oestridae-(Bot and Warble Flies) Gasterophilus species originally were restricted to the Palearctic regions, but now can be found on The family Oestridae now is considered to contain horses in other parts of the world. There are some a large number of species, including some that for- similarities among the species, with G. equi similar merly comprised the families Cuterebridae, Gas- to G. intestinalis; G. flaviceps similar to G. haemor- terophilidae and Hypodermatidae; these former rhoidalis; G. gedoelsti similar to G. intestinalis; families are now considered to be subfamilies. G. lativentris similar to G. nigronirmus; G. meridi- Genus Cephalopina Strand onalis similar to G. nigronirmus; G. nasalis similar C. titillator (Camel Nasal Bot Fly) to G. veterinus; and G. ternicinetus similar to Cephalopina is a small genus, with only C. titillator G. gedoelsti. The adults are 11–16 mm in length. considered important. It is an obligate parasite, Males possess a black-brown thorax, and a yellow- causing nasal myiasis in camels. brown head and abdomen. The body is covered Genus Cuterebra Clark with yellow hairs, but the thorax shows a transverse Myiasis M 2525 band of dark hairs. The female is darker than the of the larva is strongly reduced, and external mouth- male (especially the abdomen). Both sexes have hooks are not visible. The posterior spiracles are sur- yellow legs. Oviposition occurs in flight. The eggs rounded by minute spines (o). They are more or less are attached along the distal half of the hairs. symmetrical and they show a longer and narrower Eggs are ready to hatch on the fifth day after channel in H. bovis than in H. lineatum, with the deposition, though embryonic development inner margins of the channel divergent. Larvae hatch depends somewhat on temperature. The larvae and crawl down the hairs and penetrate the body penetrate the mouth and the tongue. From time to through an injury of the skin. Larvae migrate below time larvae make small holes to breathe. Second the skin along the nerve, muscle and fat tissues to the and third instars are found in the stomach. Mature skin of the host’s back, and there forms small holes larvae are excreted with the feces and pupate in in the skin. The larvae molt to the second and third the soil. The mature larvae are 16–20 mm in length. instar, remaining stationary in the slowly enlarging They possess rows of spines on each segment, and swellings or “warbles.” They are a subcutaneous par- the shape of the spines varies among species. The asite, with the posterior peritremes located near the region of the posterior spiracles is marked with hole to facilitate obtaining oxygen. From here, the 12–20 transverse bands, with the number varying third instar drops to pupate. among species (n). Larvae can develop only in Genus Oestrus Linnaeus (HC) the alimentary tract of horses, donkeys, zebras O. aureoargentatus and other equids. Gasterophilus haemorrhoidalis, O. caucasicus G. inermis, G. intestinalis, G. nigrocornis, G. peco- O. ovis (Sheep Nasal Bot Fly) rum and G. veterinus are obligate parasites. O. variolosus Genus Hypoderma Latreille (Heel Warble or TheOestrus species are found primarily in the Old Cattle Grub Flies) (D) World: O. aureoargentatus and O. variolosus are H. actaeon distributed throughout Africa south of the Sahara; H. bovis and O. caucasicus is present in domestic and wild H. capreola animals of the Caucasus region and Central Asia. H. diana However, O. ovis is found in all sheep-farming H. lineatum areas of the world. Hypoderma species are found on several continents, The adults ofOestrus species are 10–12 mm in including Europe, Africa, Australia and North and length. They have a yellow-brown head, with small South America. Though commonly associated with black tubercles of equal size on the thorax, and livestock, Hypoderma lineatum has been reported yellow legs. They possess yellow-veined wings. The in a wild host, the North American Bison (Bison abdomen is marked with black, brown, grey or bison). The flies are 13–15 mm in length. They are white, the appearance changing with the light inci- densely clothed with black and yellow hairs, almost dence. Oestrus ovis is an obligate parasite, affecting resembling a bumble bee. Hypoderma actaeon and the ocular, nasal, and frontal sinuses, and causing H. capreola are similar to G. diana. Hypoderma bovis maxillary sinus myiasis in sheep and goats. It is an obligate parasite of cattle, equids and humans; attacks dogs and man occasionally. In this last case, H. diana is parasite of deer and roedeer, and H. lin- the larva can be found in the eye, and the syn- eatum is present in cattle, deer and humans. The drome is diagnosed as an acute catarrhal conjunc- flies are active in bright sunshine, calm weather and tivitis because the young larva cannot develop. The temperatures in excess of 18°C. Eggs are deposited life cycle is dependent on climatic factors: in West on the hairs of their hosts. Texas, with its moderate winters, the flies are These large larvae measure 25–30 mm long at active during almost all months of the year, except maturity, and are yellow-brown. The cephaloskeleton January and February. 2526 M Myiasis The mature larva is about 20 mm in length, These flies are obligate ocular and nasal parasites and brown with transverse, dorsal blackish bands. in bovides and equides. Rhinoestrus purpureus is a The posterior spiracles are circular, with a central parasite found in horses and donkey, and their ecdysial scar, and without a distinct suture (p). cross-breeds. The female is larviparous. The adults are Genus Pharyngomyia Schiner (HC) 8–11 mm long. The eyes in both sexes are widely sepa- Ph. picta rated. The abdomen bears glossy black and brown The Pharyngomyia species are deer parasites. setiferous tubercles. The legs are red and yellow-brown. Pharyngomyia picta is an obligate parasite of red The young larvae are undescribed in many deer (Cervus elaphus), sika deer (Cervus nippon) species. The mature larvae are about 20 mm in and in Europe attacks the fallow deer (Dama length, with anal bulges bearing spines. The poste- dama), elk (Alces alces) and the roe deer (Capreo- rior spiracles are open and a little longer than lus capreolus). The adult is 13–16 mm long. Its broad (r); the channels lie almost opposite one body is densely covered with blackish hairs, and another in R. purpureus. appears black and white, or brown and white, according to the light incidence. The eyes in both sexes are broadly separated. The mature larvae Family Phoridae – (Scuttle or are about 35 mm in length, and have irregular Humpbacked or Phorid Flies) black spots, especially in the posterior part of the body. The posterior spiracles are crescent- Genus Megaselia Rondani (D; AT/F) shaped, with the inner margins of the sinuate part M. rufipes divergent (q). M. scalaria Genus Rhinoestrus Brauer (Horse Nasal Bot The genusMegaselia is important primarily because Fly) (HC) the larvae of M. rufipes produce traumatic myiasis, R. antidorciti boils and borrows. Megaselia scalaria is a second- R. giraffae ary occasional invaders of wounds. These flies are R. hippopotami recorded from humans. Megaselia rufipes is com- R. latifrons mon in North America and Europe. The mature R. nasalis larva is small, measuring about 4 mm in length. It is R. nivarleti small, dirty-white, and slightly flattened. The poste- R. phacochoeri rior spiracles are situated on brown, sclerotized R. purpureus tubercles, each with a narrow opening. R. steyni R. tshernyshevi R. usbekistanicus Family Sarcophagidae – (Flesh Flies) R. vanzyli The Rhinoestrus species vary in their distribu- Genus Sarcophaga Meigen (D; AT/F UO) tion: R. antidorciti, R. steyni and R. vanzyli are S. albiceps present in southwestern Africa; R. giraffae S. argyrostoma occurs in Tanzania (Africa); R. hippopotami in S. carnaria Uganda and Zimbabwe (Africa); R. latifrons is S. crassipalpis present in Russia and China; R. nivarleti is S. exuberans found in Zimbabwe; R. phacochoeri is present S. fertoni in Cameroon (Africa); R. purpureus is a palearc- S. froggatti tic species; R. tshernyshevi is present in Central S. haemorrhoidalis Asia; and R. usbekistanicus occurs in East and S. hirtipes Central Asia. S. misera Mymaridae M 2527 S. nodosa They are similar to Sarcophaga in general appear- S. peregrina ance, but instead of showing an ill-defined chess- S. ruficornis board pattern, the abdomen shows sharply marked S. striata black spots. Body is densely grey pollinose. The S. tibiali dark stripes on the thorax are clearly visible. The TheSarcophaga species are widely distributed: S. albi- legs are black. The mature larva is covered with ceps occurs in the Hawaiian Islands and New Guinea; many irregular rows of small dark-pointed back- S. argyrostoma is found in South America, India, Mar- wardly directed spines that are much larger than shall Islands, Hawaii and Yugoslavia (Europe); S. cras- those of Sarcophaga. The posterior spiracles, how- sipalpis is present in South America and Australia; S. ever, are similar to Sarcophaga (t). exuberans and S. fertoni are present in the Mediterra- Wohlfahrtia magnifica is an obligate parasite nean regions; S. froggatti is an Australian species; S. of warm-blooded vertebrates. It is a larviparous hirtipes is found in both the Ethiopian and Palearctic species. From 150 to 200 larvae are deposited near regions; S. misera is found in the Oriental and Aus- a wound or body openings of humans or other tralasian regions and Pacific Islands;S. nodosa is pres- animals such as sheep, goats, cattle, horses and ent in Zimbabwe; S. peregrina is present in the dogs. Larvae molt twice, then leave the wound of Madagascan and Australasian regions; S. ruficornis is the hosts to drop to the ground, where they pupate. present in Indochina; S. striata is present in Russia; Wohlfahrtia bella is an obligate parasite in wounds and S. tibialis is present in the Ethiopian and Mediter- in sheep, goats and humans; W. nuba is a parasite ranean regions. The thorax of the adult typically bears of both living and dead livestock tissues. In the three broad and black longitudinal stripes. The abdo- case of W. opaca and W. v igil, the larvae penetrate men has a gray and blackish tessellation, a so-called the host skin, producing foruncles. chess-board pattern. The legs are black. The mature larva is densely spinulose. The larval cephaloskeleton has a bifurcated dorsal cornua. The eritremal ring of References the posterior spiracles is open (s). Females of this genus are larviparous, deposit- Beaver PC, Jung RC, Cupp EW (1986) Parasitología Clínica. ing larvae rather than eggs. This species breeds in Salvat Editores. Barcelona, Spain, 882 pp Gállego Berenguer, J (1998) Manual de parasitología. excrement, carrion and other decomposing organic Edicions Universitat de Barcelona, Barcelona, Spain, matter. Adults can be found indoors, and are attracted 491 pp to freshly deposited stools. The larvae of S. carnaria Hall (1991) Screwworm flies as agents of wound myiasis. feed in feces, but accidentally can be involved in World Anim Rev. Special 2:6–17 Richards OW, Davies RG (1977) IMMS general textbook of nose, mouth, anal or vaginal myiasis. Similarly, entomology. Vol. 2. Classification and biology. Wiley, S. haemorrhoidalis larvae breed mainly in feces, but New York, NY, 1354 pp also has been involved in anal and vaginal myiasis. Teskey HJ (1981) Morphology and terminology-larvae. In: Genus Wohlfahrtia Brauer and Bergenstamm MacAlpine JF, Peterson BV, Shewell GE, Teskey GJ, Vockeroth JR, Wood DM (eds) Manual of nearctic (D; UO) Diptera, Vol. 1. Monograph 27. Agriculture Canada W. bella Research Branch, Ottawa, Canada, pp 65–88 W. magnifica Zump F (1965) Myiasis in man and animals in the Old World. Butterworths, London, United Kingdom. 267 pp W. nuba W. opaca W. vigil Wohlfahrtia magnifica is present in the south of Mymaridae Europe, Asia (Russia), and in North Africa. Wohl- fahrtia nuba, W. opaca and W. v igil are North A family of wasps (order Hymenoptera). American species. Adults are 8–14 mm in length.  Wasps, Ants, Bees and Sawflies 2528 M Mymarommatidae Mymarommatidae often paler, with a light green abdomen. Within the geographical range of these planthoppers, A family of wasps (order Hymenoptera). they are common on the foliage of many kinds  Wasps, Ants, Bees and Sawflies of palms. The nymphs feed on the roots of grasses, usually at or near the soil surface. They are tan Myndus crudus Van Duzee to grey colored with a reddish blush on the head (Hemiptera: Cixiidae) and legs. The nymphs are covered with a thin, waxy bloom produced by numerous wax glands Myndus crudus Van Duzee (Fig. 115) is a plan- in the cuticle. The tibiae of the forelegs are flat- thopper whose adults feed on the foliage of vari- tened, a possible adaptation for digging beneath ous species of palms. This insect species is the only the soil surface. Guinea grass (Panicum maxi- known vector of lethal yellowing, a highly destruc- mum Jacquin) and St. Augustine grass (Steno- tive disease of palms in various countries of the taphrum secundatum (Walter) Kuntz) are two Caribbean Basin region. of several grass species that are highly favorable This planthopper is distributed on the hosts of M. crudus nymphs, and both are very mainland of Tropical America from northern common in various localities within the insect’s Brazil to northern Mexico, with its range extend- range. ing to islands of the western Caribbean region (i.e., Cuba, Jamaica, and the Cayman Islands), but it has not been reported in Hispaniola, Damage and Economic Importance Puerto Rico, or other islands of the eastern Caribbean except Trinidad. This distribution Myndus crudus is a vector of lethal yellowing pattern in the Caribbean reflects the invasion disease of palms. As the name implies, “lethal route of its fauna, i.e., mainland species invaded yellowing” is lethal to nearly all of the palms it the westernmost islands from the Yucatan Pen- infects. The disease is caused by a kind of plant- insula, with diminishing numbers of species inhabiting bacterium called a phytoplasma. It is reaching the easternmost islands. From the one of the most devastating diseases of palms south, species crossed the short span to Trini- and has caused serious impacts on the landscape dad, with diminishing numbers reaching islands and the agricultural economies of regions that it to the north. Myndus crudus is present in south- has invaded. ern Florida and is probably present on at least Lethal yellowing has been known in Cuba, some islands of the Bahamas, since these two Jamaica, and the Cayman Islands since the 1800s. political entities are highly similar in climate In the mid-1900s it was first observed in and other geographical considerations, and bor- Hispaniola, the Bahamas, and Florida. Florida was der and share flora and fauna with the Carib- the only locality on the mainland of the Americas bean Basin region. affected by lethal yellowing until the early 1980s, The adult female of M. crudus at rest with when it was reported on the Yucatan Peninsula of posteriorly extended wings is about 5 mm long Mexico. It has since practically eliminated coco- from the vertex of the head to the tip of the wing. nut palms from the Caribbean coast of most of The head and body are straw colored. The wings southern Mexico and much of Central America. are transparent, with brown veins that have More recently, it has been reported on Nevis in numerous pustules bearing setae. The prominent the eastern Caribbean (Fig. 116). ovipositor distinguishes the female. The male is Although it is sometimes suggested that slightly smaller and similarly straw-colored, but additional species of insects may transmit lethal Myndus Crudus Van Duzee (Hemiptera: Cixiidae) M 2529

Myndus Crudus Van Duzee (Hemiptera: Cixiidae), Figure 115 Myndus crudus and damage: (a) female, (b) male, (c) nymph (photo by J.V. DeFilippis), (d) view of Fort Lauderdale, Florida, with initial case of lethal yellowing (center), (e) dead palm trunks in former coconut plantation that was totally destroyed by lethal yellowing, Yucatan State, Mexico. yellowing, researchers have found no evidence diversity tends to increase relative to decreasing that any species other than M. crudus is a vector latitude, and indeed there are more species of of this disease. Transmission experiments have auchenorrhynchous insects on palms in the tropics successfully shown this insect to be a vector in than in Florida. Little is known concerning the Florida, where conditions for conducting this type biology and vector potential of most of these species. of experiment were especially favorable, but Lethal yellowing has been most intensely M. crudus is most probably a vector in all countries studied as a disease of coconut palm because of that of Tropical America where lethal yellowing is species’ economic importance. In fact, the coconut present. It is also recognized, however, that insect palm is considered one of the 20 most important 2530 M Myndus crudus Van Duzee (Hemiptera: Cixiidae)

Myndus Crudus Van Duzee (Hemiptera: Cixiidae), Figure 116 Map showing the distribution of lethal yellowing, 2007. Several cases were also reported on the island of Nevis in the Lesser Antilles (not shown on map).

crop plants in the world, and is a basic element in the prospects for controlling lethal yellowing via agricultural economies of many tropical countries, biological control of the vector are not promis- as well as a source of important products in the ing. As an insect native to the Americas, it is world economy. However, lethal yellowing infects attacked by several natural enemies, but at least and is lethal to at least 35 additional species of palms, in lethal yellowing-affected areas, these do not including the economically important date palm reduce the populations of this insect sufficiently (Phoenix dactylifera L.), as well as many palms that to significantly reduce the spread of the disease. are important as ornamentals or as local sources of Myndus crudus populations can be suppressed food or fiber in tropical countries (Fig. 116). by treating palms with insecticides, and there is a There are several other diseases of coconut slight reduction in the spread of lethal yellowing. palm in various countries that were formerly But chemical control is not a feasible method of thought to be identical to lethal yellowing of the reducing the spread of lethal yellowing over large Caribbean, and thus were referred to as lethal areas for long periods. Insecticide treatments of yellowing. But as knowledge of phytoplasmas palms and grasses have been used as quarantine increased in recent decades, lethal yellowing was treatments to attempt to prevent M. crudus from recognized as a distinct disease of palms in the being transported to new localities. Caribbean region. Similar diseases of palms, most Populations of M. crudus can be reduced by of which are present in various parts of Africa and planting ground covers that do not support Asia, are currently known by other names. development of the immature stages, including various grass species, or legumes such as tropical- kudzu, Pueraria phaseoloides (Roxburgh) Ben- Management tham, or perennial peanut, Arachis pintoi Krapov and W.C. Gregory. The latter legume species are Once M. crudus was implicated as a vector of used as ground cover in coconut plantations for lethal yellowing, interest turned to the possibilities soil improvement and erosion control. Where of managing this insect to achieve a corresponding lethal yellowing-resistant palms are planted, reduction in the spread of lethal yellowing. The the use of leguminous ground covers would Myrmecology M 2531 reduce the vector population and indirectly the Kramer JP (1979) Taxonomic study of the planthopper genus Myndus in the Americas (Homoptera: Fulgoroidea: disease pressure on the palms, thus delaying Cixiidae). Trans Am Entomol Soc 105:301–389 the development of a strain of the pathogen that Oropeza C, Howard FW, Ashburner GR (eds) (1995) Lethal can overcome the defenses of the resistant palm. yellowing: research and practical aspects. Kluwer Academic Publishers, Dordrecht, The Netherlands, This prospective method of managing lethal 250 pp yellowing has been investigated in experiments in small research systems, but not on farms or other large areas. Myofibrils Although managing LY indirectly by controlling M. crudus has been investigated as mentioned The fibers that collectively comprise muscles. above, virtually all management efforts are focused directly on the disease. A therapeutic treatment involving trunk injections of antibiotics active Myopsocidae against phytoplasmas was developed in the 1970s. Although costly, it has been used effectively in A family of psocids (order Psocoptera). preventing the disease in palms in some relatively  Bark-Lice, Book-Lice or Psocids affluent areas, such as Palm Beach, Florida. By far the most common management Myriapods method is the use of resistant palms. Varieties of coconut differ in susceptibility to lethal yellowing, Classes of Phylum Arthropoda, subphylum Ate- and those that are relatively resistant have been locerata (formerly subphylum Myriapoda, the established in large planting programs in lethal basis for this name) that are insect relatives but yellowing-affected areas. In the remaining 35 sus- possessing many legs. The myriapods consist of ceptible species, distinct varieties have not been the centipedes, millipedes, pauropods and sym- distinguished. However, the degree of susceptibil- phylans. There is some question whether this is a ity of many species of palms is roughly known natural group. from observations in lethal yellowing-affected  Phylum urban areas, particularly in Florida, where there is an exceptionally high diversity of palms used in landscaping. For example, in urban areas in Flor- Myrmecodomatia ida where lethal yellowing has killed numerous coconut palms, it has also killed many Adonidia Structures found in higher plants that appear to merrillii (Beccari), while in the same areas a have evolved to serve as dwelling places for similar palm, Ptychosperma elegans (R. Brown) ants. Blume, has not been affected. Landscapers in lethal yellowing-affected areas can select palms that have shown apparent resistance or immunity Myrmecolacidae based on such observations. A family of insects in the order Strepsiptera.  Stylopids References Myrmecology Howard FW, Moore D, Giblin-Davis R, Abad R (2001) Insects on palms. CABI Publications, Wallingford, United King- dom, 400 pp The scientific study of ants. 2532 M Myrmecomorphy Myrmecomorphy and insects, and describe some examples of intraspecific variation. James McIver, Gary Stonedahl USDA Forest Service, Pacific Northwest Experiment Station, La Grande, OR, USA Spiders

Myrmecomorphy, or the morphological and Spiders have a wide variety of body forms, but behavioral mimicry of ants, has evolved at least compared to ants, typically have relatively short, 70 times in the arthropods – 15 times in spiders, hairy bodies. Ants are generally elongate, have a at least 10 times in plant bugs, and seven times medially constricted body with a distinct petiole, in staphylinid beetles. More than 2,000 species elbowed antennae, large compound eyes, and typ- of myrmecomorphic arthropods have been ically a shiny integument. Ant-like spiders on the described thus far, belonging to over 200 genera other hand, are relatively elongate, have a medial in 54 families. Myrmecomorphy forms a subset constriction of the cephalothorax into a head and of ant mimicry, which includes all species that alitrunk, with a narrowing of the posterior cepha- resemble ants through convergence in morpho- lothorax or anterior abdomen to produce a peti- logical, behavioral, chemical, or textural charac- ole and gaster. Ant-like spiders often use the first ters (Fig. 117). The other major group of or second pair of legs as if they were antennae, ant-mimetic species are the myrmecophiles, or have pigmented spots on the cephalothorax that those arthropods that associate closely with resemble large compound eyes, often have shiny ants, but do not necessarily resemble them mor- setae or dense mats of reflective hairs to give a phologically. Although some are also myrmeco- shiny illusion, and can have a transparent cuticle morphic, most myrmecophiles have chemical to give the illusion of a constriction. Many ant- and/or textural characters that facilitate a close like spiders match the color of their ant models relationship with their ant hosts. Here we closely. Populations of the jumping spider Syne- describe signal properties of myrmecomorphic mosyna aurantiaca are color polymorphic, with arthropods, present their taxonomic distribu- yellow morphs resembling the ants Pseudomyrmex tion, and discuss their adaptive significance. flavidulus and P. oculatus, and black morphs resembling P. g ra c i li s . Correspondence in the color of individual structures in not uncommon, Signal Properties of as in the species-specific mimicCastianeira mem- Myrmecomorphic Arthropods nonia, in which the yellow terminal segments of the front legs correspond to the bright yellow Mimicry can be defined as a system that involves antennal apices of its otherwise black ant model, an organism (the mimic) which simulates signal Pachycondyla obscuricornis. The evolution of ant- properties of another organism (the model) so like behaviors in myrmecomorphic spiders is not that the two are confused by a third organism surprising, given that behavior is often identified (the operator) and the mimic gains protection, as the most conspicuous feature of ants. In both food, or a mating advantage as a consequence of clubionid and salticid spiders, the first or second the confusion. Myrmecomorphic species express pair of legs are waved around in front of the spi- a variety of signal properties that enhance their der, contacting the substrate in much the same resemblance to ants, involving shape, pattern, way that ants use their antennae. The antennal texture, color, behavior, and size. In this section, illusion is often supplemented by a zigzag run- we review how mimicry is achieved for a repre- ning gait, and in jumping spiders, there is a general sentative sample of myrmecomorphic spiders reluctance to jump. In general, the spiders that Myrmecomorphy M 2533 are most difficult to distinguish from ants in the field are those that have a combination of morphological and behavioral ant-like features.

Insects

While insects are confronted with many of the same problems as spiders for evolving ant-like form, the possession of a similar body plan requires less profound modification. A major con- straint to myrmecomorphy, however, is the one or two pairs of wings found in most adult insects. Consequently, the loss or reduction of wings in the adult is common in ant-like insect species, often accompanied by a constriction of the posterior thorax and/or anterior abdomen. In those species of myrmecomorphic insects that have retained their wings, oblique or transverse pale marks or bands of pale hairs typically interrupt the otherwise darkened forewings, to produce the illusion of a petiole. Still other species, such as aly- dids and mantids, resemble ants only in the immature form. Compared to many insects, ants have relatively large heads with well developed mandibles. In general, myrmecomorphic insects tend to possess relatively larger heads than their non- Myrmecomorphy, Figure 117 Ants (top), mimetic relatives, and the illusion of large man- myrmecomorphs (mimics; middle), and dibles in many ant-like plant bugs is accomplished non-mimetic relatives (bottom). (a) Formica by enlargement of the ventral region of the head, obscuripes (Formicidae), western North America. which also brings the head forward into a more (b) Coquillettia insignis (Miridae), western North ant-like horizontal position. Many ant-like insects America. (c) Pronotocrepis clavicornis (Miridae), mimic the elbowed antennae of ants through western North America. (d) Pseudomyrmex tenuis differential pigmentation or enlargement of vari- (Formicidae), Central and South America. (e, f) ous antennal segments. Myrmecomorphic insects Synemosyna aurantiaca (Salticidae), Trinidad, often display microstructural and color modifica- Brazil. (g) Habronattus mexicanus (Salticidae), tions that enhance mimicry, including: (i) silvery, southern North America, Central America, reflective hairs to increase body shine, or when Caribbean. arranged in bands, to act as an interruptive agent; (ii) changes in surface texture corresponding with smooth, roughened, or pitted areas on the ant’s As in the spiders, morphological adaptations body; (iii) thoracic or abdominal spines to mimic in ant-like insects are often accompanied by those on the alitrunk and petiole of some ants; resemblance in behavior. Many staphylinid bee- and (iv) color polymorphisms that match avail- tles are difficult to distinguish from their army ant able ant models (Fig. 117). hosts, due to very similar patterns of locomotion. 2534 M Myrmecomorphy Regarding the behavior of alydid bugs, Oliveira Taxonomic and Geographic (1985) remarks, “Nymphs of Hyalymenus have a Distribution of Myrmecomorphy highly differentiated ant-like morphology which is achieved by several structural adaptations. The Myrmecomorphy has been identified in nine fam- similarity is greatly enhance by the nymph’s ant- ilies of spiders and 45 families of insects, repre- like behavior, notably the rapid zig-zag loco- senting 11 different orders. Over 200 spider and motion, the constantly agitated antennae, and insect genera are known to contain myrmeco- the up and down movement of the abdomen morphs, and the number of species involved is cer- (similar to an alarmed ant)”. tainly in the thousands worldwide. Ant-mimicry has arisen at least four times in the spider families Clubionidae and Corinnidae (running spiders), Transformational Mimicry three times in the Salticidae (jumping spiders), and several times each in the Aphantochilidae, Because their ant models are holometabolous, Araneidae (orb-weavers) and Theridiidae (comb- mimic species that develop gradually, like plant foot weavers). In the plant bugs (Heteroptera: Mir- bugs and spiders, tend to resemble a range of idae), morphological resemblance to ants has appropriately sized models, usually representing arisen no fewer than ten times, and this family two or more ant species or genera. This phenom- contains the highest diversity of myrmecomorphic enon is called transformational mimicry, and species among insects. has been described for mantids, plant bugs, aly- Myrmecomorphic arthropods are found in all did bugs, running spiders and jumping spiders. major regions of the world except Antarctica and Species that rely on transformational mimicry the extreme northern Holarctic. The number of are typically genus-specific mimics, presumably species increases toward the tropics, mirroring the because features that provide species-specificity pattern observed for other mimetic species, for on one life-history stage constrain the evolution ants themselves, and for most other plant and ani- of features that promote close correspondence mal groups. to different ants in other stages. Adaptive Significance Sexual Dimorphism The adaptive significance of myrmecomorphy has While not common in ant-mimetic systems, sexual not been clearly established in most cases. The dimorphism has been described in several groups most common mimetic hypotheses to explain of spiders and some Hemiptera/Heteroptera. The myrmecomorphy are Batesian, Wasmannian, and adult males of the jumping spider Zuniga magna aggressive mimicry. are striking mimics of Pseudomyrmex gracilis, while females closely resemble the ponerine Pachy- condyla villosa. In both cases, the species-specific Batesian Mimicry mimicry involves remarkably accurate structural and color correspondence between model and For those ant-like species that do not live with or mimic. Many myrmecomorphic plant bugs are sex- attack ants, the most widely supported hypoth- ually dimorphic; brachypterous or apterous females esis for myrmecomorphy is Batesian mimicry. are among the best morphological mimics of ants, The evolution of Batesian mimicry is presumed to while the macropterous males are comparatively occur within the context of an interactive system poor pattern mimics. involving model, mimic, and a predaceous Myrmecomorphy M 2535 operator(s). The system has four basic features: estimate population sizes of mimics in relation to (i) certain arthropods (models) are unacceptable their models, observational evidence suggests that to predators and advertise this, (ii) predators ants are almost always more common than co- (operators) learn about this unacceptability, occurring mimics. Most evidence suggests that (iii) generalization in predators takes place allowing free-living myrmecomorphs are relatively palat- acceptable species (mimics) to benefit by resem- able – spiders serve as important prey items for blance, and (iv) visual discrimination by preda- birds and lizards, and myrmecomorphs are no tors is sufficient to select for increased mimetic exception to this general rule. resemblance. The behavioral and ecological con- The most likely predators that could serve as ditions presumed to favor the evolution of Bate- operators in Batesian mimicry systems are small sian mimicry include: (i) the model must be an vertebrate predators such as lizards and birds, and unacceptable prey item to at least some predators, arthropod predators such as jumping spiders and (ii) the mimic must be an acceptable prey item, wasps. These predators possess relatively good (iii) the model and mimic must have similar tem- vision, necessary to select for the detailed struc- poral and spatial distributions, (iv) the model tural and behavioral adaptations seen in many must be common relative to the mimic, (vi) the myrmecomorphic species. Vertebrate species are mimic must have signal properties that deceive also well known to be capable of associative learn- visually oriented predators within a community ing, including experimental studies involving of alternate prey, and (vii) predators must be mimetic insects. While associative learning has able to learn. Our discussion on the evidence for been demonstrated in social insects, similar data Batesian mimicry addresses these conditions by on arthropod predators are scanty at best, possibly describing the qualities of species within selected because of the greater difficulty in choosing myrecomorphic systems, and offering observa- meaningful stimuli for arthropods that are soli- tional and experimental evidence of functional tary, more reclusive than bees and ants, or have Batesian mimicry in the field. unknown feeding habits. Nonetheless, a few stud- In the best known myrmecomorphic systems, ies have demonstrated the capacity for associative models, mimics and predators tend to possess eco- learning in arthropod predators, involving wasps, logical and behavioral features consistent with a mantids, crab spiders, and assassin bugs. Batesian mimicry hypothesis. Like bees and wasps, Some of the most convincing observational ants have features that make them ideal models in evidence that supports Batesian mimicry in ant- Batesian mimicry systems. Ants are among the like species comes from the existence of a number most common and conspicuous of insects, and of remarkably close species-specific correspon- workers of many species are aggressive and dis- dences between model and mimic, particularly tasteful. Ants are entirely social, and have alarm among the spiders. For example, the running spi- pheromones used for common defense against der Mazax rettenmeyeri features a unique ridge of enemies. Therefore, small vertebrate and inverte- erect hairs along the midline of the cephalotho- brate predators must hunt them with caution. rax, which closely approximates the thoracic keel Although a variety of small predators attack or of its model Camponotus sericeiventris. Other specialize on ants, these species are comparatively characteristics of the mimic, such as color, shape rare, and typically use special hunting tactics. and behavior, accentuate the resemblance between Myrmecomorphs that do not attack ants are model and mimic. Many other species-specific almost always found in the same microhabitat as pairs of model and ant mimic have been described their models, but do not associate closely with worldwide. ants, and often show avoidance reactions to them. Experimental evidence in support of Batesian Although little quantitative work has been done to mimicry includes feeding trials in which visually 2536 M Myrmecomorphy oriented predators behave similarly toward model consequence of selection by both ants (Wasman- and mimic. For example, in a study on the ant- nian mimicry) and by visually oriented preda- mimetic plant bug Coquillettia insignis in north- tors (Batesian mimicry). eastern Oregon (USA), both the jumping spider Sassacus papenhoei and the assassin bug Sinea diadema accepted non-mimetic plant bug prey Aggressive Mimicry significantly more often than the ant-mimicCoquil - lettia insignis, while their behavior toward the Ants represent an abundant and conspicuous model ant Formica fusca and toward the mimic source of protein for potential predators, and was indistinguishable. In addition, the assassin bug many ant species care for other insect species, Siadema diadema was able to learn and remember from which they extract nutrients. These features unpleasant experiences with the ant model. While attract a considerable diversity of arthropod about half of the field-collected specimens of this predators, and among these predators are some assassin bug attacked the ant-mimic Coquillettia of the more remarkable examples of aggressive insignis, after close confinement with the ant For- ant-mimicry. Aggressive mimicry differs from mica fusca, individual assassin bugs that had previ- Wasmannian mimicry in that aggressive mimics ously attacked C. insiginis were significantly less do not live with their ant models, and typically likely to do so. associate with ants just closely enough to access their resource, either the ants themselves, or their symbiotic associates. Spiders of the genus Wasmannian Mimicry Aphantochilus possess a shiny and granular integument, characters that are thought to facili- Myrmecophilic arthropods that also possess a tate acceptance by their cephalotine ant models, body shape or texture that closely resembles which are their only source of food. The adult their ant models are called Wasmannian mimics. crab spider Amyciaea forticeps attacks workers Some observers have argued that the body shape of the weaver ant Oecophylla smaragdina. Under and texture of ant-like rove beetles that associate normal circumstances, the crab spider does not with army ants evolved as a consequence of closely resemble the weaver ant. While hunting, selection by the ants themselves. This view is however, the spider adopts a behavior in which it consistent with the general observation that looks like a dying or struggling weaver ant, and when encountering one another, doryline army other workers often come nearer to investigate. ants and other swarm raiding species antennate The spider then pounces on its prey and quickly the petiolar area of their nestmates, and that the withdraws to a more remote location. Myrme- same behavior performed by a myrmecomor- comorphic arthropods may also have evolved phic rove beetle allows the mimic to function ant-like morphology and behavior to gain with the colony as if it were an ant. Yet among access to the Hemiptera that some ants tend for the rove beetles that associate with ants (myrme- honeydew. Several authors have noticed a corre- cophiles), most species that do not resemble ants lation between the distribution of ant-tended occur entirely within the nest of their hosts, aphids and various species of the ant-like plant while all known ant-like rove beetles live with bug Pilophorus . It is widely believed that legionary ants, spending the majority of their myrmecomorphy in Pilophorus serves as a tem- adult lives on the surface, exposed to the full porary illusion, allowing the plant bugs to closely range of visually oriented predators that accom- approach and seize their aphid prey. pany the foraging raids. Hence, ant-like body Mimicry is very common in nature, and form in some rove beetles may have evolved as a occurs in a bewildering array of plant and animal Myrmecophiles M 2537 groups. Species that are abundant and ecologically demonstrated that the guests take food from the dominant generally make excellent models in hosts and may even prey upon them. Outstanding mimicry systems, and so it is no surprise that so cases, such as more specialized species, that pass many myrmecomorphic arthropods have evolved the entirety of their life cycle in the nest, may best since ants came on the scene some 100 million illustrate why “nest parasite” is the most com- years ago. Myrmecomorphic species offer abun- monly cited role of social insect symbionts. dant opportunities for exploring ecological and Throughout their lifespan, these myrmecophiles evolutionary aspects of mimicry and can lead to a receive regurgitations from nurse ants tending the deeper understanding of related fields, such as ant ant larvae, and in the process, drain the resources social organization, systematics, and predator-prey that would have otherwise gone to the host ant relationships. larvae. The larval myrmecophile also preys upon  Ants the ant larvae, even in the presence of the nurse  Mimicry ants. Nonetheless, many myrmecophiles may not  Myrmecophiles be solely parasitic on the hosts. More highly adapted species may even provide benefits to their host colonies for at least part of their life cycle, possibly References indicating that they are mutualistic with the hosts. A great number of taxa have evolved Edmunds M (1974) Defence in animals. Longman, Essex, myrmecophilous lineages. Mites (Acarina), beetles United Kingdom, 357 pp (chiefly Staphylinoidea), flies (Phoridae) and a few McIver JD, Stonedahl GM (1993) Myrmecomorphy: morphological and behavioral mimicry of ants. Annu Rev Ento- other soil-dwelling insect species have the most mol 38:351–379 myrmecophilous species and are also the most Oliveira PS (1985) On the mimetic association between abundant. Myrmecophiles are found living in nests nymphs of Hyalymenus spp. (Hemiptera: Alydidae) and of nearly every species of ant. Colonies that are ants. Zool J Linn Soc 83:371–384 Reiskind J (1970) Multiple mimetic forms in an ant-mimicking larger and more persistent at maturity, such as clubionid spider. Science 169:587–588 army and driver ants, have more species and indi- Wickler W (1968) Mimicry in plants and animals. World Uni- viduals of myrmecophiles than smaller mature versity Library, London, England, 255 pp colonies, such as ponerine and dacetine ants. Addi- tionally, the species found in larger colonies tend to be more specialized than are those living with Myrmecophiles ants that have smaller, less permanent colonies. Irrespective of the type of colony, the total relative James A. Danoff-Burg abundance of myrmecophiles is low, often on the Columbia University, New York, NY, USA order of 1:5,000 ants. Myrmecophiles are found in nearly every area of the nest including the refuse One of several types of social insect symbionts, middens, foraging columns, brood chamber and myrmecophiles are animals that live with ants for the queen chamber. A single species typically spe- at least part of their life cycle. Other similar sym- cializes in one of these niches within the nest. bionts are termitophiles (guests of termites), melit- tophiles (guests of bees) and sphecophiles (guests of wasps). Of these, myrmecophiles and termito- Ecological Categories philes are the most abundant, species-rich and morphologically diverse. Myrmecophilous species generally play one of All of these social insect symbionts are thought three consistent roles in the nests of the ants. to be nest parasites. Many previous studies have Symphilic species, the best integrated into the host 2538 M Myrmecophiles nest, are species-specific guests who must live with particular host species, whereas non-integrated a single species and frequently interact with the synecthrans are usually not host-specific. They are, host ants. These species usually obtain all food instead, found with whatever ant species presents from regurgitations or grooming interactions that the necessary ecological resources needed by the they solicit from the hosts. Synoeketes (also called guest. Most species of myrmecophiles are integrated indifferently tolerated guests) are found in ant into the host nest, as this mode of living tends to nests, but do not interact with the host ants. produce a greater number of species through the Instead, these guests use the resources that are processes of resource tracking and coevolution provided by the nest, such as nest materials, frass, with the host ants. Therefore, as host ants speciate, food refuse and other nest detritus. Host ants will any well-integrated, species-specific myrmecophile attack these species if the myrmecophile is too may also speciate and come to specialize on the apparent, forceful, or bothersome. Synecthrans newly evolved host species. Non-integrated species (also called persecuted guests) are only occasion- generally do not have strong parallel evolutionary ally found with ants and may merely raid the nest relationships with their host ants because they for food. This ecological category of myrmeco- generally are not species-specific. philes usually does not live within the nest, instead residing in the surrounding litter or soil. Other ant symphiles often classed as myrmecophiles include Chemical Communication trophobionts (ant-tended phytophagous insects, usually Hemiptera and Lepidoptera) and ant para- Strongly integrated myrmecophiles tend to have a sites (mites, phorid flies, or parasitic wasps). great diversity of adaptations that help to either A simpler organizational scheme to help label mimic or crack the communication code of their those species that fall into more than one of the hosts. These adaptations can include chemical, above three categories classifies myrmecophiles as morphological and behavioral traits. Because they either integrated or non-integrated species. Inte- help to break the code, these adaptations often grated species are those that play a role in the become useful as integrating mechanisms that social life of the colony, including symphiles who enable the myrmecophile to enter and become a occasionally attack the hosts and trophobionts. part of the colony. Non-integrated myrmecophilic The roles played by these species can range from species may have, at most, a single, rudimentarily procuring food (e.g., trophobionts), to grooming developed integrating mechanism. the hosts, and providing what may be psychoac- Presumably because most communication in tive chemicals (e.g., symphiles). Non-integrated the ant colony is done chemically, most well- species normally do not interact with the hosts integrated symphilic myrmecophiles are able and, instead, use the nest or the ants themselves as to chemically communicate with the host ants. an ecological niche to be exploited. This category Myrmecophiles both send and receive chemical includes synoeketes, synecthrans and parasites. messages with the host ants. Typically, communications from the host ants to the myrmecophiles are intercepted signals between nestmate ants, Evolutionary Trends rather than pure, interspecific communications. Species that ancestrally possess extensive glandular Several trends are consistent with these ecological systems, such as staphylinid beetles of the subfamily categories. Obligate, strongly integrated symphiles Aleocharinae, have evolved prominent structures tend to be host-specific and are found with a single associated with the glands, such as trichomes and or a few closely related host species. These species brushes. Complicated processes of chemical exu- are strongly adapted to living in nests of only one dation have evolved in these species such that some Myrmecophiles M 2539 myrmecophilous species use a sequence of three chemicals to first defend against, then appease, and then convince an ant to adopt them and carry them into their nest. These exudates often trigger actions by the ants that mimic the normal brood care behavior of the host ants. Well-integrated, obligate symphiles are frequently able to secrete chemicals that generally resemble the cuticular hydrocarbons of the host. In so doing, they are able to mimic the chemicals that are thought to form the basis of colony odor and nestmate recognition, thereby gaining at least initial entrance to the colony.

Myrmecophiles, Figure 118 Myrmecophiles, Morphological Mimicry particularly well-integrated species such as these Dinardilla mexicana and Sceptobius dispar Morphological adaptations can include similar (Coleoptera: Staphylinidae: Aleocharinae), color patterning to the host, development of promi- frequently interact with their host ants. The nent glandular trichomes and the evolution of spe- obligate symphiles require the presence of the cialized body plans. Myrmecoidy, the most unique hosts to live and are rarely found outside their morphological specialization among myrmeco- company. philes, involves a suite of characteristics including a petiolate abdomen, narrow body, long legs and an expanded basal antennal segment to resemble retaining the ancestral species bauplan. Morpho- geniculate antennae. Typically, well-integrated, logically generalized species tend to be either host-specific symphilic species adopt some aspects synoeketes or synecthrans, and are rarely well of myrmecoidy. In contrast, most synoeketes and integrated into the colony. These species must synecthrans have either retained their generalized instead manipulate the host behavior using either bauplan or have evolved a limuloid, heavily-sclero- chemical or behavioral specializations. tized defensive (or trutztypus) form (Fig. 118). Limuloid species, such as many staphylinid beetles, are characterized by reductions in the Behavioral Traits appendages and head and development of overlapping, sclerotized body regions so that the insects A myrmecophile may have evolved behavioral appear teardrop-shaped. When attacked, species traits that allow it to interact peaceably with the with defensive forms retract their appendages into host ants. These are found in all types of guests, grooves and feign death until the agitated ant irrespective of how well integrated they are. Strigi- departs. Specializations of the cuticle of the guest lation occurs when the myrmecophile either licks so that they resemble their hosts are also common. or scrapes the oily secretions from the surface of For example, host-specific phoretic mites have the ants and serves to acquire what is likely the host cuticular surfaces that so closely mimic those of odor as well as to provide some food to the guest. their hosts that it is hypothesized that the ants are Guests often perform a vigorous bout of strigila- incapable of detecting the presence of the mites. tion when first introduced into a novel nest. This Most species of myrmecophiles have not behavior frequently stops the attacks that invari- evolved any morphological adaptations, instead ably occur when a myrmecophile first enters a new 2540 M Myrmeleontidae colony. Behavioral traits such as episodic walking Mystax that is similar to that of ants, as well as antennation upon greeting, are frequently manifested in well A patch of hair or bristles located above the mouth, integrated guests. Whether these traits are selected especially in robber flies (Diptera: Asilidae). In by the hosts or another species that may be preda- robber flies it is also called a mouth beard. tory on the guests, such as antbirds, is not clear. It is unlikely that the operator of selection is identical in all cases. Mythicomyiidae Most research on myrmecophiles conducted at present focuses on Lycaenidae caterpillars, A family of flies (order Diptera). which are trophobionts and are tended by the  Flies ants for the honeydew and a diversity of chemical exudates by the caterpillars. The caterpillars are frequently studied within the field of myrme- Mythology and Insects cophily, in part because most species are easily accessible on the branches of a plant. The adult Ron Cherry butterflies are not tended nor are they ant asso- University of Florida, Belle Glade, FL, USA ciates. The caterpillars are not, strictly speaking, symphiles because they do not live with the ants, The study of insects and other arthropods in but instead are only tended by the hosts. Most of mythology falls into the realm of cultural ento- the adaptations of these caterpillars involve mology. However, in order to approach this sub- chemical cues, including the secretion of many ject, it is necessary to understand what mythology chemicals from a spectacular diversity of spe- is. Quite simply, mythology is the study of myths. cialized exudatory organs. As an example, the One definition of a myth commonly used in caterpillars often produce an alarm pheromone everyday conversation is that a myth is something used by the host ants, so that if they are attacked, false or imaginary. This definition has nothing to they signal for help from the host ants. do with mythology. As used in mythology, a myth is a story, presented as having actually occurred in References a previous age, explaining the cosmological and supernatural traditions of a people, their gods, heroes, cultural traits, religious beliefs, etc. Mytho Kistner DH (1979) Social and evolutionary significance of social insect symbionts. In: Matthews RW (ed) Social logy is also closely related to religion as exempli- insects, Vol. I. Academic Press, New York, NY, pp fied by the saying, “One man’s religion is another 339–413 man’s mythology.” Hölldobler B, Wilson EO (1990) The ants. Chapter 13.Harvard University Press, Cambridge, MA Myths in general may be categorized into cer- Pierce NE, Braby MF, Heath A, Lohman DJ, Mathew J, Rand tain types such as creation myths, emergence DB, Travassos MA (2002) The ecology and evolution of myths, etc., and this is also true of many insect ant association in the Lycaenidae (Lepidoptera). Annu myths. For example, the creation of the Milky Way Rev Entomol 47:733–771 Galaxy by a beetle is explained in a creation myth of the Cochiti tribe of North America. The Negritos Myrmeleontidae of the Malay peninsula have a diving myth in which a beetle dives into mud and brings up earth A family of insects in the order Neuroptera. They which become land. The Navajo of North America commonly are known as antlions. have an emergence myth in which the origin of  Lacewings, Antlions and Mantidflies the Navajo from the earth is explained in a myth Mythology and Insects M 2541 involving several insects. In a fire theft myth, the popular title of Beelzebub was “lord of flies” and San of Africa say that fire was stolen by the praying he is depicted both in human form as a fallen mantis, an insect widely regarded by Africans as angel and as a demonic-appearing fly. The most sacred. Both bees and ants are totems as the Honey famous of all mythological insects is the sacred Ancestor and Honey Ant Ancestor respectively in scarab of ancient Egypt. The sacred scarab, Scara- the mythology of Australian aborigines. baeus sacer Linn., is a coprophagous scarabaeid Symbols are also closely related to mythology. found around the perimeter of the Mediterra- Myths, spoken or written, are many times extended nean. This dung beetle was of great symbolic symbol systems encapsulating religious, philo- importance in ancient Egypt. The beetle symbol sophical, or psychological beliefs. Of particular known as a scarab became a symbol of rebirth interest to zoologists are animal symbols. Well after death. Scarabs were found in religious rites, known examples of animal symbols are the mag- tomb hieroglyphics, as amulets, and large num- nificent lion for royalty, the bull for masculinity bers of hand-carved scarabs were buried with the and virility, and the dove for peace. However, dead. Numerous other insects have also been used although lesser known, many interesting animal for symbols (Figs. 119 and 120). symbols also occur among invertebrates, espe- On a superficial level, myths provide color- cially insects. For example, the use of ants as sym- ful stories of interactions between gods, god- bols for positive traits is widespread throughout desses, people, and nature. However, beyond various cultures. In many cultures, the humble, providing colorful stories, myths also serve sev- hard working ant is a universal symbol of indus- eral useful functions. One important function of triousness and organization. The Old Testament myths is to explain. How did my people get fire? states, “Go to the ant you sluggard: consider her Why does a zebra have stripes? Why should I be ways and be wise,” and, “There are four things which good? Where will I go when I die? Answering are little upon the earth but they are exceedingly questions such as these is the subject matter of wise: the ants are a people not strong, yet they provide their meat in the summer.” The bee, also considered to be a rich symbol, is an exemplar of ethical virtues. Among qualities attributed to the bee are diligence, organization, sociability, purity and chastity. The bee was associated with Christi- anity, the Virgin Mary, and in ancient Greece, with virgin priestesses or Melissae who were termed “bees.” Also in Greece, the bee was a cult symbol for Artemis, the virgin huntress and goddess of wild nature. In contrast to ants and bees, flies occur as many symbols and almost always with negative connotations. The fly represents feeble- ness and insignificance, but is also associated with evil gods and corruption. In early European Christian art, flies appear as a universal symbol for torment. Similarly, in Zorastrianism, yazads are major demons including the female Nasu, the demoness of dead matter who is depicted as a fly. Mythology and Insects, Figure 119 Ionian coin The best known mythological figure associating showing the bee which was a cult symbol for flies with negative symbolism is Beelzebub. A Artemis, the goddess of wild nature. 2542 M Mythology and Insects pottery and carry tiny pots (vestigial wing covers) on their shoulders. They say that these insects are in league with a monster that breaks the pottery of the dead and that it is this beetle that smashes into small fragments the pottery that is found at ancient village sites. On a larger scale, a Cherokee Indian myth tells of how a water beetle dove into a watery Lower World and brought back mud to make earth from which mountains and valleys were formed. Another function of myths is to provide a basis for social cohesion. A shared mythology is a strong social tie that may be used to justify a social structure such as a religion or government. Myths explaining the common origin of a people provide social cohesion to those people, and insects play important roles in many of these myths. Mythology and Insects, Figure 120 Beelzebub, a According to South African Khoisan traditions, demon known as Lord of the flies, is an example of the first living thing on earth was the tiny praying a dipteran being associated with evil. mantis, and it was he who created the earliest beings, including humans. One of the tribes of Sumatra claims to be descendants of three myths. Many insect myths explain the origin, brothers hatched from eggs laid by a butterfly. In morphology, and behavior of different insects. Madagascar, and among the Naga tribes of The Tlingit Indians of North America explain Manipur, some also trace their ancestry to a the origin of mosquitoes in a story about a butterfly. Among Australian aborigines, insect blood-sucking, carnivorous giant who fed on based totems are found that provide social cohe- humans. This giant is ultimately avenged after sion by offering group identity and even dictate his gruesome death by returning to feed on social restrictions. humans in the form of blood-sucking mosqui- A third function of myths is to provide moral toes. The reason bees, wasps, and hornets have order and many animals including insects fre- stingers is explained in a story by the Algonquin quently occur in myths to show how one should Indians of North America. According to this lead a moral life. Insects also occur in myths as myth, the god Wakonda gave stingers to bees “enforcers” or punishments to guarantee virtuous because the bees were industrious, but needed behavior. Of the ten plagues, which, according to protection. However, since wasps and hornets the Bible, were sent by God to Pharaoh’s Egypt at claimed to be related to bees (which is true), The the instigation of Moses and Aaron, three were Great Spirit benevolently endowed them with actually insect plagues, namely lice, flies and stinging weapons also. locusts. And according to Danish legend the flea Besides explaining different facets of insect was sent to pester mankind as a punishment for biology, insect myths also help explain the world laziness. An interesting insect myth with moral in which we live. Why is ancient pottery almost overtones is also found in Native American always found broken? The Navajo Indians mythology. The Montagnais Indians of eastern observed that beetles of the family Rhipiphori- Canada believed that the overlord of fish, particu- dae wander among scattered heaps of broken larly salmon and cod, was Big Biter (=Tabanus Myxomatosis M 2543 influence natural forces are found in Indian and Australian mythology. In India, the Dravidians practiced conciliatory control. The custom was to catch a locust, decorate it, revere it, and let it go, which, in turn, would cause the swarm to depart. Native bees were important providers of honey to Australian aborigines. Once the nest was found, the “sugar bag” was eagerly devoured – wax, honey, pupae, dead bees, ants and all. The stick which was used to pry the sugar bag from the tree was thrown into a fire. This simple act allowed the spirits of the bees to return to the heavens where they stay until Mayra, the wind of spring, breathes life into the flowers again. Then the bees return to earth, thus providing more honey for mankind. The preceding insect myths clearly show that mythology is more than just entertaining stories. Important questions are also the subject matter of mythology. Myths, including many insect myths, help answer fundamental questions about human existence.

References

Capinera JL (1993) Insects in art and religion: the American Mythology and Insects, Figure 121 Enamel plate Southwest. Am Entomol 39:221–229 from Qul’ at Sharquat, Iraq, representing an Cherry R (1985) Sacred scarabs of ancient Egypt. Bull Ento- Assyrian noble in a locust prayer before the god mol Soc Am 31:14–16 Kritsky G, Cherry R (2000) Insect mythology. Writers Club Ashur. A swarm of locusts may symbolize the Press, New York, NY wrath of god or cosmic disorder. Leach M (1984) Funk and Wagnalls standard dictionary of folklore, mythology, and legend. Harper, San Francisco, CA affinis Kirby). This fly appeared whenever fish were being taken from the water and hovered over the fisherman to see how his subjects were being Myxomatosis treated. Occasionally Big Biter would bite the fisherman to remind him that the fish were in his A viral disease of New World rabbits that is trans- custody and to warn him against wastefulness mitted by mosquitoes, blackflies, fleas, lice and mites. (Fig. 121). It has only mild effects on New World rabbits, but is A fourth important function of myths is to quite deadly to Old World rabbits. In 1950 it was control natural forces. Once one has gods, one introduced to Australia to reduce the population can influence them by making sacrifices, offer- of European rabbits that were deliberately but ing prayers, or performing rituals. Two interest- regrettably introduced to Australia, where they had ing examples of insects being used in myths to few natural enemies. The rabbits in Australia have 2544 M Myxomatosis caused the extinction of numerous animals and was also introduced to France, where it spread rap- plants, and caused extensive soil erosion due to over- idly throughout Europe, causing significant decreases grazing. The virus quickly reduced the population of in rabbit populations, and some of the predators that rabbits from 600 million to 100 million, but the rab- fed upon them. A vaccine is used in Europe to pro- bits have developed resistance. Now another virus, vide protection of domestic rabbits from the virus. rabbit calicivirus, has been introduced to attempt  Mosquitoes population suppression in Australia. Myxomatosis  Mosquitoes as Vectors of Viral Pathogens