exapodsstand out among all other invertebratesfor being far and away the most diverse group of animals on Earth, the only inverte- bratesto fly, and the only terrestrial invertebratesto undergo indirect developmentor completemetamorphosis. The arthropod subphylum Hexapoda comprisesthe classInsecta and three other small, closelyrelated, wingless, insect-likegroups: Collembola, protura, and Diplura. The Hexapodaare united on the basisof a distinct body plan of a head,3-segmented thorax, and 11-segmentedabdomery 3 pairs of thoricic legs, a single pair of antennae,3 setsof "jaws" (mandibles,maxillae, and labium), an aerial gasexchange system composed of tracheaeand spiracles,Malpighian tubules formed as proctodeal (ectodermal)evaginations, and, among the Pterygota, wings (Box 22A). The presence of a tho- rax fixed at 3 segments, each with a pair of walking legs, is a unique slmapomorphy for the Hexapoda. Classificationof The Animal Other synapomorphies include the presence of a Kingdom(Metazoa) large fat body (mainly concentrated in the abdo- men), and fusion of the second maxillae to form a Non-Bilateria* Lophophorata' lowerlip (thelabium). (a.k.a.the diploblasts) PHYLUM PHORONIDA PHYLUM PORIFERA PHYLUM BRYOZOA Hexapods evolved on land; groups inhabit- pHYrDv pLAcozoA PHYLUM BRACHIOPODA ing aquatic environments today have secondarily PHYLUM CNIDARIA EcpysozoA invaded those habitats through behavioral adap- PHYLUM CTENOPHORA Nematoida tations and modifications of their aerial gas ex- PHYLUM Bilateria NEMATODA change systems. The earliest undisputed fossils of PHYLUM NEMATOMORPHA (a.k.a.the triploblasts) hexapods are early Devonian (412Ma). However, Scalidophora PHYLUM XENACOELOMORPHA PHYLUM KINORHYNCHr'. there are Silurian trace fossils that are very hexa- Protostomia PHYLUM PRIAPULA pod-like, and molecular clock data suggest an PHYLUM CHAETOGNATHA PHYLUM LOBICIFERA Early Ordovician origin for Hexapods at about Sptneura Panarthropoda 479 millionyears ago and PHYLUM PLATYHELMINTHES an early Silurian origin PHYLUM TARDIGRADA PHYLUM GASTROTRICHA about M7 million years ago for Insecta. PHYLUM ONYCHOPHORA PHYLUM RHOMBOZOA The most spectacular evolutionary PHYLUM ARTHROPODA radiation PHYLUM ORTHONECTIDA suBpHvLUMcRusrncen* among the Hexapoda (in fact among all eukary- PHYLUM NEMERTEA SUAPHYLUMH€XAPObA otic life) has, of course, been within the insects, PHYLUM MOLLUSCA SUBPHYLUM MYRIAPODA which inhabit nearly every PHYLUM ANNELIDA conceivable terrestrial SUBPHYLUM CHELICERATA PHYLUM ENTOPROCTA and freshwater habitat and, less commonly, even Deuterostomia PHYLUM CYCLIOPHORA the sea surface and the marine littoral iegion. PHYLUM ECHINODERMATA Gnathifera PHYLUM HEMICHORDATA lnsects are also found in such unlikely places as oil PHYLUM GNATHOSTOMULIDA PHYLUM CHORDATA swamps and seeps, sulfur springs, glacial streams, PHYLUM MICROGNATHOZOA and brine ponds. They often live where few other PHYLUM ROTIFERA "Paraphyletic group

This chapterhas been revised by Wendy Moore. 844 Chapter Twenty-Two

Insects are not only diverse, but also incredibly BOX22A Characteristicsof the abundant. For every human alive, there are an estimat- SubphylumHexapoda ed 200 million insects. Howard Ensign Evans estimat- ed that an acre of ordinary English pasture supports (plus 1. Body composed of 20 true somites acron) an astonishin g 248,375,000 springtails and 17,825,000 organized as a head (6 somites), thorax (3 somites) beetles. In tropical rain forests, insects can constitute and abdomerl (11 sopites). Due to fusion of (dry somites, these body segments are not always 40% of the total animal biomass weight), and the externallyobvious. biomass of the ants can be far greater than that of the 2. Head segments bear the following structures (from combined mammal fauna (up to 75"/" of the total ani- anterior to posterior):compound eyes and ocelli; mal biomass). A single colony of the African driver ant antennae; clypeolabrum; mandibles; maxillae,labi- Anomma wilaerthi may contain as many as 22 million um (fused second maxillae).Ocelli (and compound workers. Based on his research in the tropics, biodi- eyes) are secondarily lost in some groups. versitv sleuth Terrv Erwin has calculated that there 3. Legs uniramous; present on the three thoracic seg- are about 3.2 x 108individual arthropods per hectare, ments of adults; legs composed of 6 articles: coxa, representing more than 60,000 species, in the west- pretarsus; trochanter, femur, tibia, tarsus, tarsus ern Amazon. In Maryland, a single population of the often subdivided; pretarsus typically clawed mound-building ant Formicn exsectoidescomprised 73 4. Gas exchange by spiracles and tracheae nests covering an area of 10 acres and containing ap- 5. Gut with gastric (digestive)ceca proximately 12 million workers. Termites have colo- 6. With large fat body (mainlyconcentrated in nies of similar magnitudes. E. O. Wilson has calculated abdomen) that, at any given time, 101s(a million billion) ants are 7. Fused exoskeleton of head forms unique internal alive on Earth! tentorium In most parts of the world, insects are among the B. With ectodermally derived Malpighiantubules (proc- principal predators of other invertebrates. Insects are todeal evaginations) also key items in the diets of many terrestrial verte- 9. Gonopores open on the last abdominal segment, brates, and they play a major role as reducer-level or- or on abdominalsegment 7, B, or I ganisms (detritovores and decomposers) in food webs. 10. Gonochoristic; direct or indirect development Due to their sheer numbers, they constitute much of the matrix of terrestrial food webs. Their biomass and energy consumption exceed those of vertebrates in most terrestrial habitats. In deserts and in the tropics, animals or plants can exist. It is no exaggeration to say ants replace earthworms as the most abundant earth that insects rule the land. Their diversity and abun- movers (ants are nearly as important as earthworms dance defy imagination (Figures 22.1,-22.7). even in temperate regions). Termites are among the We do not know how many species of insects there chief decomposers of dead wood and leaf litter around are, or even how many have been described. Published the world, and without dung beetles African savan- estimates of the number of described species range nahs would be buried under the excrement of the tens from 890,000 to well over a million (we calculate of thousands of large grazingmammals. about926,990). An average of about 3,500 new species Without insects, life as we know it would ceaseto have been described annually since the publication exist. In fact,E. O. Wilson has stated, "so important of Linnaeus's SystemaNsturne in1758, although in re- are insects and other land-dwelling arthropods that if cent years the average has climbed to 7,000 new spe- all were to disappear, humanity probably could not cies annually. Estimates of the number of insect species last more than a few months." Eighty percent of the remaining to be described range from 3 million to 100 world's crop species, including food, medicine, and million. The Coleoptera (beetles), with an estimated fiber crops, rely on animal pollinators, nearly all of 380,000described species,is far and away the largest which are insects. Insects also play key roles in pol- insect order (more than a quarter of all animal species linating wild, native plants. Beekeeping began long are beetles). The beetle family Curculionidae (the wee- ago/ at least by 600 BC in the Nile Valley and prob- vils) contains about 65,000 described species (nearly ably well before that. The first migratory beekeep- 5% of all described animal species).The rich diversity ers were Egyptians who floated hives up and down of insects seems to have come about through a combi- the Nile to provide pollination services to floodplain nation of advantageous features, including the evolu- farmers while simultaneously producing a honey tionary exploitation of developmental genes working crop. Domestic honeybees (Apis mellifera),introduced on segmented and compartmen talize d bodies, coevo- to North America from Europe in the mid-1600s, are lution with plants (particularly the flowering plants), now the dominant pollinators of most food crops miniaturization, and the invention of flight. grown around the world, and they play some role PHYLUMARTHROPODA The Hexaooda:Insects and Their Kin 845

Figure 22.1 Representatives of the three orders of entognathous (noninsect) hexapods. (A) Anurida grana- na, a springtail (order Collembola). (B) Ptenothrix sp., a resulted in flowers with anatomy and scentsthat are springlail showing entognathous mouthparts. (C) A diplu- finely tuned to their insect partners. In exchangefor ran from New Zealand (order Diplura). (D) A proturan from pollination services,flowers provide insects with British Columbia (order Protura). food (nectar, pollen), shelter, and chemicals used by the insectsto produce such things as pheromones.In general,insect pollination is accomplishedcoinciden- in pollinatingS}% of the crop varieties grown in the tally, as the pollinators visit flowers for other reasons. United States(they are estimated to be directly re- But in a few cases,such as that of the yucca moths of sponsiblefor $10to $20billion in crops annually).l the American Southwesl (Tegiticulaspp.), the insects Interactions between insects and flowering plants actually gather up pollen and force it into the recep- have been going on for a very long time, beginning tive stigma of the flower, initiating pollination. The over 100 million years ago with the origin of the an- moth's goal is to assurea supply of yucca seedfor its giosperms and acceleratingwith the ascendancyof larvae,which develop within the yucca's fruits. Some these flowering plants during the early Cenozoic. insectsalso play important roles as seeddispersers, Millions of years of plant-insect coevolution have especiallyants. More than 3,000plant species(in 60 families) are known to rely on ants for the dispersal of their seeds. lThe study of beesis called "melittophily." The study of honey- bees(Apis spp.) and their managementis called "apiculture." Like all other animals on Earth, insects are facing The managementof bumblebees(Bombus spp.) is "bombiculture." enormous threats of extinction. Certainly many thou- The ritualized keeping of stinglessbees is "meliponiculture." sands of specieshave becomeextinct over the past The Asian honeybee,Apis dorsata,not yet introduced to the U.S.,is a giant reaching an inch in length. Its droppings are quite notice- century as a result of rampant land use changeand able, and the massdefecations of thesebees at sunsetcreate a deforestation.With acceleratingbiodiversity losses "golden shower" that provides significant nutrient enrichment worldwide, estimatesof the number of insect species to tropical soils. Their droppings were once confusedwith the dreaded "yellow rain," a deadly form of biochemicalwarfare that that have already gone extinct range into the millions. poisoned thousandsof villagers during the Vietnam War. Further, widespread and often inappropriate use of 846 Chapter Twentv-Two pesticides has created a "pollination crisis" in many ability to fly, the ability to fold back their wings, and the parts of the world, as pollinating insects are locally evolution of holometabolous development (= indirect extirpated and native plant and domestic crop pollina- development, = complete metamorphosis). The persis- tionplummets. tence of the main lineages of insects since the Devonian As valuable as insects are to human life, some spe- and their ecological and morphological versatility have cies seem to cons,pire to give the whole group a bad undoubtedly contributed to making Hexapoda the name. Some insect species are pests and consume dominant group in extant terrestrial ecosystems, with about a third of our potential annual harvest, and respect to species diversity, functional diversity, and some other species transmit many major human dis- overall biomass. Obviously, the subject of insect biol- eases.Every year we spend billions of dollars on insect ogy, or entomology, is a discipline in its own right, and control. Malaria, transmitted by mosquitoes, kills 1 to a multitude of books and college courses on the subject 3 million people annually (mostly children), and each exists. If we apportioned pages to animal groups on the year nearly 500 million people contract the disease.It basis of numbers of species, overall abundance, or eco- is the leading cause of death from infectious disease, nomic importance, insect chapters could easily fill 90% and it has plagued humans for at least 3,000 years of this textbook. The Selected References at the end of (Egyptian mummies have been found with malaria this chapter provide entry into some of the current lit- antigens in their blood). One of the most widespread erature on insects. and fastest spreading human viral diseases, dengue, is Becausethe Hexapoda comprises such a large and transmitted by mosquitoes of the genus Aedes.Dengue diverse assemblage of arthropods, we first present is essentially an urban disease, almost entirely as- a brief classification of the 31 recognized orders, fol- sociated with anthropogenic environments because lowed by more detailed synopses, brief diagnoses, and its main vectors, A. albopictus and A. aegypti, breed comments, on each order. These two sections serve as primarily in artificial containers (e.g., flower vases, a preface to the body plan discussion that follows, and discarded tires, water tanks). In recent years, these also provide a reference that the reader can turn to as species have spread throughout the tropics, often fol- needed. lowing the international trade in used tires. Although these mosquitoes have not penetrated very far into the temperate zorres, they have become established in the CLASSIFICATION OF THE southern United States. A varietv of mosquitoes trans- SUBPHYLUM HEXAPODA mits the filarial nematode Wu-chereriabancrofti, the causative agent of lymphatic filariasis ("elephantia- Our classification scheme recognizes 31 orders of sis") throughout the world's tropics. Chagas' disease living hexapods. Three entognathous, or non-insect (American trypanosomiasis) is transmitted by certain hexapod orders (the Entognatha), are basal to the hemipteran bugs in the subfamily Triatominae (family monophyletic class Insecta. The Insecta comprise Reduviidae), and causes chronic degenerative disease two monophyletic sister groups, the order Archae- of the heart and intestine. The species of triatomine ognatha (with monocondylic mandibles) and all the bugs that occur in the southwestein United States tend others (with dicondylic mandibles). The subclass not to defecate when they feed, greatly reducing the Pterygota, or flying insects, comprise two groups: possibility of humans contracting Chagas' disease in the Palaeoptera (Ephemeroptera, Odonata), which that area. However, global warming is now increas- may be a paraphyletic group, and the monophyletic ing the spread of Aedes, Culex, triatomines, and other infraclass Neoptera. We recognize three superor- tropical disease vectors. ders within the modern winged insects, or Neoptera: The natural history writer David Quammen, the Polyneoptera (Plecoptera, Zoraplera, Blattodea, speaking of the blood-sucking varieties of mosqui- Mantodea, Dermaptera, Orthoptera, Phasmida, Gr- toes, notes that the average blood meal of a female ylloblattodea, Embioptera, Mantophasmatodea), the (the only sex that feeds on blood) amounts to 2.5 times Acercaria (Psocodea,Thysanoptera, Hemiptera), and the original weight of the insect-the equivalent, the Holometabola (all the remaining orders). Within Quammen notes, "of Audrey Hepburn sitting down the Holometabola we recognize four well supported, to dinner and getting up from the table weighting but unranked clades:Coleopetrida (Coleoptera, Strep- 380 pounds, then, for that matter, flying away." But siptera), Neuropterida (Neuroptera, Megaloptera, as Quammen also points out, mosquitoes have made Rhapidioptera), Antliophora (Mecoptera, Siphonap- tropical rain forests (the most diverse ecosystems on tera. Diptera), and Amphiesmenoptera (Trichoptera, Earth) Iargely uninhabitable to humans, thus helping Lepidoptera). With nearly a million named species of to preserve them! Hexapoda, we have opted to include representative The enormous diversification of Hexapoda is often families of only the most diverse and common orders attributed to the evolution of three key innovations: the in the taxonomic synopses. I PHYLUM ARTHROPODA The Hexapoda:lnsects and Their Kin 847

SUBPHYLUM HEXAPODA Amphiesmenoptera (Note:"Entognatha" and "Palaeoptera" are likely paraphy- OrderTrichoptera: Caddisf lies leticgroups) OrderLepidoptera: Butterflies, moths Entognatha OrderCollembola: Springtails OrderPrgtura: P,rotu rans Hexapod Classification OrderDiplura: Diplurans Subphylum Hexapoda CLASS INSECTA (= ECTOGNATHA) Body differentiated into head (acron + 6 segments), thorax (3 segments), and abdomen (11 or fewer seg- OrderArchaeognatha: Jumping bristletails ments); cephalon with one pair lateral compound eyes Dicondylia and often with a triad or pair of medial ocelli; with one OrderThysanura (= Zygentoma): Silverfish pair of uniramous multiarticulate antennae, mandibles, SubclassPterygota: Winged insects and maxillae; second pair of maxillae fused to form a Palaeoptera:Ancient winged insects complex labium; each thoracic segment with one pair of uniramous legs; wings often present on second and OrderEphemeroptera: Mayflies third thoracic segments (inpterygote insects); abdomen OrderOdonata: Dragonflies and damselflies without fully developed legs, but "prolegs" (presum- Infraclass Neoptera: Modern, wing-folding ably homologous to the ancestral arthropod abdominal insects appendages) occur in at least seven orders (in adults SuperorderPolyneoptera of some Diplura, Thysanura, and Archaeognatha; in OrderPlecoptera: Stoneflies larvae of some Diptera, Trichoptera, Lepidoptera, and OrderBlattodea: Cockroaches and termites Hymenoptera); abdomen with a large fat body; gono- OrderMantodea: Mantises pores open on the last abdominal segment or on the OrderPhasmida (= Phasmatodea):Stick and seventh, eighth, or ninth abdominal segmenf paired leafinsects cerci often present; males commonly with intromittent OrderGrylloblattodea: Rock crawlers and clasping structures; development direct, involving OrderDermaptera: Earwigs relatively slight changes in body form (ametabolous OrderOrthoptera: Locusts, katydids, crickets, or hemimetabolous), or indirect with striking changes grassnoppers (holometabolous). OrderMantophasmatodea: Heel-walkers or gladiators Entognatha OrderEmbioptera (= Embiidina):Web-spinners Mouthparts with bases hidden within the head cap- OrderZoraptera: Zorapterans sule (ento-gnathous); mandibles with single articula- SuperorderAcercaria (= Paraneoptera) tion; most or all antennal articles with intrinsic mus- OrderThysanoptera: Thrips culature; wingless; without, or with poorly developed, OrderHemiptera: True bugs Malpighian tubules; legs with one (undivided) tarsus. OrderPsocodea: Book lice, bark lice, The three orders of entognathous hexapods do not truelice ' form a monophyletic group. While the entognathous SuperorderHolometabola conditions of Collembola and Protura appear to be ho- OrderHymenoptera: Ants, bees, wasps mologous (these two orders are often placed together Coleopterida in the class Ellipura), entognathy in the Diplura may OrderColeootera: Beetles be a product of convergent evolution. Recent data from OrderStrepsiptera: Twisted-wing parasites paleontology, comparative anatomy, and molecular phylogenetics suggest that the Diplura are the sister Neuropterida group of the Insecta, and are therefore more closely OrderMegaloptera: Alderllies, dobsonflies, related to the Insecta than they are to the other ento- fishflies gnathous orders. OrderRaphidioptera: Snakeflies OrderNeuroptera: Lacewings, ant lions, Order Collembola Approximately 6,000 described mantisflies,owlflies species (Figure 22.1.A,8). Small (most less than 6 mm); Antliophora biting-chewing mouthparts; with or without small OrderMecoptera: Scorpionflies, hangingflies, compound eyes; ocelli vestigial; anterrnae 4-articulate, snowscorpionflies first 3 articles with intrinsic muscles; tarsus of legs OrderSiphonaptera: Fleas indistinct (perhaps fused with tibia); pretarsus of legs OrderDiptera: True flies, mosquitoes, gnats with single claw; abdomen with a reduced number of 848 Chaoter Twentv-Two

I I segments (six); first abdominal segment with ventral article with intrinsic musculature; simple develop- tube (collophore) of unknown function; third abdomi- ment. Most specieslive in mesic habitats beneath rocks, nal segment with small process (retinaculum); a forked rotting logs, leaf littel, humus, and soil. tail-like appendage on fourth or fifth abdominal seg- ment (furcula); without cerci; with gonopores on last Class lnsecta abdominal segmenf without Malpighian tubules; often Mouth appendages ectognathous (exposed and pro- without spiracles or traeheae. jecting from the head capsule); mandibles with two The earliest known hexapods in the fossil record points of articulation (except Archaeognatha); intrinsic are collembolans. Rhynietla ptorrurto, and other spe- musculature of antennal articles greatly reduced; an- cies from the Lower Devonian closely resemble some tennal pedicel with a mechanoreceptor that perceives modern collembolan families. Unlike other hexapods, the movement of the flagellum, called the johnston's which breathe using internal tubes called trachea, organ; head with a tentorialbridge connecting the pos- springtails breathe air directly through their cuticle terior tentorial arms; tarsi subdivided into tarsomeres; and epidermis. Their cuticle repels water, allowing with well-developed Malpighian tubules; ovipositor them to live in moist environments without suffocat- formed from modifications of the appendages of ab- ing. They also have a remarkable system for escaping dominal segments 8 and 9. The Insecta comprise two predators. \Atrhileat rest, the furcula is retracted under clades, the order Archaeognatha (with monocondylic the abdomen and held in place bv the retinaculum. mandibles) and all other insects (the clade Dicondylia, When the furcula and retinaculum disassociate, the with dicondylic mandibles). Dicondylia also comprise furcula swings downwards with such force that it hits two clades, the order Thysanura and the subclass Pter- the substrate, and quickly propels the collembolan ygota (winged insects). high into the air. Many workers believe that springtails evolved via neoteny. Order Archaeognatha Approximately 390 described species (Figure 22.2A,8). Small (to 15 mm), wingless Order Protura Approximately 200 described species (perhaps secondarily), resembling silverfish but body (Figure 22.1D). Minute (smaller than2 mm); whitish; more cylindrical; ocelli present; compound eyes large without eyes, abdominal spiracles, hypopharynx, or and contiguous; body usually covered with scales; cerci; Malpighian tubules are small papillae; sucking mandibles biting-chewing; with a single condyle mouthparts; stylet-like mandibles; vestigial antennae; (articulation point); maxillary palp large and leglike; first pair of legs carried in an elevated position and tarsi 3-articulate; middle and hind coxae usually with used as surrogate " antenrrae"; pretarsus of legs with exites ("styli"); abdomen 11-segmented, with 3 to 8 single claw; abdomen 11-segmented,with a telson (per- pairs of lateral leglets ("slyli") and 3 caudal filaments; haps reminiscent of their crustacean ancestors);the seg- simple development. ]umping bristletails are usually mental nature of this telson or twelfth "segment" has found in grassy or wooded areas under leaves, bark, not been confirmed; first 3 abdominal segments with or stones. small appendages; without external genitalia, but male gonopores on protrusible phallic complex; gonopores Dicondylia on last abdominal segment; with or without tracheae; Includes Thysaura and the Pterygota. These insects simple development. have mandibles with a two condvles (articulation Proturans are the only hexapods with andmor- points). phic development, a type of development in which a new abdominal segment is added with each instar (or Order Thysanura Approximately 450 described molt). AII other insects have epimorphic development, species (Figure 22.2C,D). Small, wingless, resembling in which segmentation is complete before hatching. Archaeognatha but with flattened body; with or with- Proturans are tate, and live in leaf litter, moist soils, out ocelli; compound eyes reduced, not contiguous; and rotting vegetation. body usually covered with scales;mandibles biting- chewing; antennae multiarticulate, but only basal arti- Order Diplura Approximately 800 described spe- cle with musculature; tarsi 3- to S-articulate; abdomen cies (Figure 22.1C); fossils date to the Carboniferous. 11-segmented, with lateral leglets (often called styli) on Small (less than 4 mm); whitish; without eyes, ocelli, segments 2-9,7-9, or 8-9;3 caudal cerci; female gono- external genitalia or Malpighian tubules; chewing pores on eighth abdominal segment, male gonopores mouthparts; abdomen 11-segmented,but embryonic on tenth; without copulatory organs; with tracheae; segments 10 and 11 fuse before hatching; gonopores on simple development. Silverfish occur in leaf litter or ninth abdominal segment;7 pairs of lateral abdominal under bark or stones, or in buildings, where they may leglets; 2 caudal cerci; with tracheae and up to 7 pairs feed on wallpaper paste, bookbindings, and the starch of abdominal spiracles; antennae multiarticulate, each sizing of some fabrics. PHYLUM ARTHROPODA The Hexaooda: lnsects and Their Kin 849

Figure 2ff Representatives of the two orders of wingless Insecta.(A) Jumping bris- tletail(order Archaeognatha) and (B) Close-up of jumping bristletailhead, note the eyes are contiguous.(G) A silverfish(order Thysanura). (D)Glose-up of sliverfishhead. Note that eyes are not contiguous,but set wide apart, and that the bodiesof both of these groups are coveredwith scales.

Subclass Pterygota cordion-like; antennaehighly reduced or vestigial in The winged insects (with a pair of wings on the sec- adults; hemimetabolousdevelopmenf larvae aquatic. ond and third thoracic segments),the forewings (front Two extant orders;many extinct groups. wings) and hindwings; wings maybe secondarilylost in one or both sexes,or modified for functions other Order Ephemeroptera Approximately 2,500 than flight; adults without abdominalleglets except on describedspecies (Figure 22.3A). Adults with vestigial genital segments;female gonopores on eighth abdomi- mouthparts, minute antennae,and soft'bodies;wings nal segment,male on tenth; femaleoften with oviposi- held vertically over body when at res! forewings pres- tor; molting ceasesat maturity. ent; hindwings absent or present but much smaller than forewings; long, articulated cerci, usually with Palaeoptera medial caudal filament; male with first pair of legs Wings cannot be folded, and when at rest wings are elongated for clasping female in flight; second and either held straight out to the side or vertically above third legs of male, and all legs of female,may be vesti- the abdomen (with dorsal surfacespressed together); gial or absent(Polymitarcyidae); abdomen 10-segment- wings always membranous, with many longitudinal ed; larvae aquatic;young (nymphs) with paired articu- veins and cross veins; wings tend to be fluted, 6r ac- lated lateral gills, caudalfilaments, and well developed

Figure 22.3 Representatives of the two orders of Palaeoptera. (A) A mayfly (order Ephemeroptera).(B) A damselfly(order Odonata). (C)A dragonfly(order Odonata). Note all of these insectshold their wings eitherout flat or straight up, but they cannotfold their wings over their back. 850 Chapter Twentv-Two mouthparts; adults preceded by winged subimago Order Pfecoptera Approximately L,700 deserlbed stage. The mayfly subimago (subadult) is the only species (Figure 22.4A). Adults with reduced mouth- winged insect known to undergo an additional molt. parts, elongate antennae, (usually) long articulated It is the one exception to the rule, that an insect with cerci, soft bodies, and a 10-segmented abdomen; with- wings is a mature adult insect and will never undergo out ovipositor; wings membranous, pleated, folded another molt. over and around abdomen when at rest; wings with Mayflies are |rimitive winged insects in which the primitive venation; nymphs aquatic (naiads), with gills. aquatic nymphal stage dominates the life cycle. Larvae Stonefly nymphs live in well-oxygenated lakes and hatch in fresh water and become long-lived nymphs, streams where they are either herbivores, feeding on passing through many instars. Mayfly nymphs are im- submerged leaves and benthic algae, or predators of portant food for many stream and lake fishes. Adults other aquatic arthropods. They are an important food eclose in synchrony and live only a few hours or days resource for fish. Plecopteran nymphs are intolerant of (hence the name, "ephemeral winged"), do not feed, water pollution, and their presence is often used as a and copulate in the air, sometimes in large nuptial bioindicator of high water quality. Adults of most spe- swarms. cies are shortlived and die soon after mating.

Order Odonata Approximately 6,000 described spe- Order Bfattodea Approximately 7,000 described cies (Figure 22.38,C).Adults with small filiform anten- species(Figure 22.48,C).TWo major body forms: cock- nae, large compound eyes, and chewing mouthparts roaches and termites. Cockroaches have a dorsoven- with massive mandibles;larval labium modified into trally flattened body; large pronotum, with expanded prehensile organ; two pairs of large wings, held out- margins extending over head; forewings (when pres- stretched (dragonflies) or straight up over body (dam- ent) leathery; hindwings expansive and fanlike; ovi- selflies) when at rest; abdomen slender and elongate, positor reduced; cerci multiarticulate; legs adapted 10-segmented; male with accessory genitalia on second for running; eggs laid in cases (ootheca). Termites are and third abdominal sternites; eggs and larvae aquatic, small; soft-bodied; wings equal-sized, elongate, mem- with caudal or rectal gills. branous, dehiscent (shed by breaking at basal line of Dragonflies and damselflies are spectacular insects weakness); antennae short, filamentous, with 11-33 with broad public appeal, not only for their beauty articles; cerci small to minute; ovipositor reduced or but because they are fast flyers and consume large absent; many with rudimentary or no external genita- numbers of insect pests, including mosquitoes, on the lia; marked polymorphism. wing. Larvae and adults are both highly active preda- Of the 4,000 described species of cockroaches, tors, with larvae consuming various invertebrates and fewer than 40 are domestic (household inhabitants). adults capturing other flying insects. Many species are Some species are omnivores, while others are restrict- 7-8 cmlong, while some extinct forms had a wingspan ed in diet. Most species are tropical, but some live in of over 70 cm. temperate habitats, caves, deserts, and ant and bird nests. Some live in and feed on wood and have intes- Infraclass Neoptera tinal flora that aid in cellulose digestion (Cryptocercus). The modern, wing-folding insects. Modificationr-of tn" These wood-feeding cockroaches gave rise to the ter- sclerites and an associated muscle at the base of the rnites (infraorder Isoptera), a skictly social group of in- wings, allow neopterans to rotate their wing joint and sects, usually with three distinct types of individuals, fold back their wings when they are not flying. This is or castes,in a species: workers, soldiers, and alates (re- one of the most important evolutionary innovations in productive individuals). Workers are generally sterile, hexapods. Wing folding allows insects to protect their blind individuals with normal mandibles; they are re- fragile wings, especially from abrasion, thereby allow- sponsible for foraging, nest construction, and caring for ing them to live in tight spaces such as crevices under members of the other castes.Soldiers are blind, usually bark, under rocks, in burrows, nests, and tunnels. sterile, wingless forms with powerful enlarged man- dibles used to defend the colony. Alates have wings Superorder Polyneoptera and fully formed compound eyes. They are produced Polyneopterans are a morphologically diverse group of in large numbers at certain times of the year, where- insects with biting-chewing mouthparts and hemime- upon they emerge from the colony in swarms. Mating tabolous development. The phylogenetic.relationships occurs at this time, and individual pairs start new colo- among the orders within Polyneoptera, and the mono- nies. Wings are shed after copulation. Colonies form phyly of the group itself have long been controversial. nests (termitaria) in wood that is in or on the ground. However, recent phylogenomic work based upon1478 Workers harbor a variety of symbiotic cellulose-digest- single-copy nuclear genes, recovered strong support ing flagellate pfotists in special chambers in the hind- that the 10 polyneopteran orders form a monophyletic gut. Some families contain symbiotic bacteria that serve group (Misof et aI.2014). the same purpose. Termites often occur in enormous PHYLUMARTHROPODA The Hexapoda:Insects and TheirKin 851

(B) (c)

Figure 22.4 Representatives of the ten orders of Polyneoptera. (A) A stonefly (order Plecoptera). (B) A cockroach (order Blattodea). (C) Termites (order Blattodea, infraorder lsoptera). (D) A mantid (order Mantodea). (E) A molecular evidence that order Blattodea is the sis- stick insect (order Phasmida). (F) A rock crawler (order ter group of the order Mantodea. Together these two Grylloblattodea). (G) Earwigs (order Dermaptera). (H) A groups are referred to asthe Dictyoptera. horse lubber grasshopper (order Ofthoptera). (l) A heel- walker (order Mantophasmatodea), inset SEM of the Order Mantodea Approximately 2,400 described tarsus of a heelwalker showing enlarged arolium. (J) A species(Figure 22.4D). First pair of legs large and rap- (order (K) (order webspinner Embioptera). A zorapteran torial; prothorax elongate;head highly mobile due to Zoraptera). cervical scleritepthat lend structural and musculature support, with very large compound eyes,not covered numbers; one spectacularestimate suggests that there by the pronotum; forewings thickened, hindwings are about three-quartersof a ton of termites for every membranous;abdomen 11-segmented,10 visible seg- person on Earth! There is strong morphological and ments and the fragmentedepiproct (which is made \ 852 Chapter Twenty-Two up of a median and two lateral components); reduced Order Grylloblattodea Approximately 30 species ovipositor made up of three valvular structures; male (Figure 22.4F).Slender, elongate, cylindrical, wingless genitalia made up of three phallomeric lobes; one pair insects,usually 15-30 mm long. Body usually pale or multiarticulate cerci; styli sometimes present in males. golden and finely pubescenf compound eyessmall or Mantises are obligate predators, mostly on insects absent;no ocelli; mouthparts mandibulate; antennae and spiders. While many species are highly cryptic in long and filiform, of 2345 antennomeres,cerci long, both color and st'ructurhl morphology, some species 8-segmented;terminal sword-shaped ovipositor of feature brightly colored patches on the anteroventral similar length as cerci. surface of their forecoxae to use in threat displays or Rock crawlers were not discovered until 191,4,and courtship displays. They have very good eyesight, today 33 speciesare known, roughly half of which are which they use to locate and track prey before striking from North America.They inhabit cold, rocky habitats, with their raptorial forelegs, using either an ambush or including snow fields below glaciersand ice caves. cursorial hunting strategy. Females lay many eggs to- Most speciescannot tolerate warm temperatures,but gether in an ootheca, a protective matrix of hardened thrive at below freezing temperatures.Due to the cold foam, which is characteristic of this order. Mantises temperature at which they live, growth and develop- are distributed around the world, with their greatest ment are very slow. Rock crawlers may require up to diversity in the Indo-Malaysian, tropical African, and sevenyears to complete a single generation.They are Neotropical regions. nocturnal scavengerson dead insectsand other organ- ic matter. Order Phasmida Approximately 3,000 described spe- cies (Figure 22.4E). Body cylindrical or markedly flat- Order Dermaptera Approximately 1,800described tened dorsoventrally, usually elongate; biting-chewing species(Figure 22.4G).Cerci usually form heavily mouthpartsi prothorax short, with specialized glands sclerotizedposterior forceps; forewings (when present) for the excretion of noxious chemicals when disturbed; form short, leathery tegmina, without veins and serv- meso- and metathorax greatly elongate; forewings ing as covers for the semicircular,membranous hind- absent or forming small to moderately elongate, leath- wings (when present);ovipositor reduced or absent. ery tegmina; hindwings absent, reduced to leathery Earwigs are common in urban environments.Most tegmina, or fanlike; tarsomeres with ventral adhesive appeatto be nocturnal scavengingomnivores. The for- pads (euplantulae); short, unsegmented cerci; male cepsare used in predation, for defense,to hold a mate with vomer-a specialized sclerite on venter of abdom- during courtship, for grooming the body, and for fold- inal segment 10; ovipositor of female weak. ing the hindwings under leathery forewings. Some Stick and leaf insects ("walking sticks"), and other specieseject a foul-smelling liquid from abdominal phasmids are large, tropical, predominantly noctur- glandswhen disturbed.Most speciesare tropical, al- nal herbivores and are some of the most spectacular though many alsoinhabit temperateregions. and oddest of all the insects. Although resembling or- thopterans in basic form, they are clearly a distinct ra- Order Orthoptera Approximately 23,000described diation. Their ability to mimic plant parts is legendary, species(Figure 22.4H). Pronotum unusually large, and many have evolved as perfect mimics of twigs, eltending posteriorly over mesonotum; forewings with leaves, bark, broken branches, moss or lichens. Stick thickened and leathery region (tegmina),occasionally and leaf insects are the only hexapods that can regener- modified for stridulation or cambuflage; hindwings ate lost limbs (e.g., due to predation) like their crusta- membranous, fanlike; hindlegs often large, adapted cean ancestors; regeneration occurs during molts, with for jumping; auditory tympana present on forelegs the new legs markedly smaller than original limbs but and abdomen;tarsomeres with ventral adhesivepads increasing in relative size with each successive molt (euplantulae);ovipositor large;male genitalia.o-ple"; (as in Crustacea). Phasmids are the only insect order cerci distinct, short, and jointed. with species-specific egg morphology across the en- Grasshoppersand their kin are conunon and abun- tire order. The eggs of some species even mimic an- dant insectsat all but the coldest latitudes. This order giosperm seeds and are spread via ant-mediated dis- includes some of the largestliving insects.Most are persal. The order includes the longest extant insects on herbivores, but many are omnivorous, and some are Earth, including the worlds longest at just over 56 cm predatory. Stridulation, which is common among in length, though some are less than 4 cm. Sexual di- males,is usually accomplishedby rubbing the special- morphism is so striking that males and females have ly modified forewings (tegmina) together, or by rub- often mistakenly been given different species names. bing a ridge on the inside of the hind femur against a Phasmids are facultatively parthenogenetic; in the ab- specialvein of the tegmen.No orthopteransstridulate sence of males, females can produce viable eggs that by rubbing the hindlegs together, as is often thought. are genetic clones of their mother. Common families include Acrididae (short-horned PHYLUMARTHROPODA The Hexaooda:Insects and TheirKin 853 grasshoppers), Gryllotalpidae (mole crickets), Grylla- blood sinuses in both pairs of wings. They feed mostly cridadae (Jerusalem crickets), Tetrigidae (pygmy grass- on dead plant material and also graze on the outer bark hoppers); Tridactylidae (pygmy mole crickets); Grylla- of trees. and on mosses and lichens. cridadae (cave crickets); Cryllidae (crickets); Tetti- goniidae (long-horned grasshoppers, katydids). Order Zoraptera Approximately 40 species (Figure 22.4K). Minute (to 3 mm); termite-like; colonial; wing- Order Mantophasmatod6a Approximately 20 spe- less or with wings; wings eventually shed; antennae cies (Figure 22.4I). Head hypognathous, with general- moniliform, 9-articulate; abdomen short, oval, 10-seg- ized mouthparts; anternae long, filiform; ocelli absen! mented; chewing mouthparts; simple development. wings entirely lacking; coxae elongate; tarsi with 5 tar- These uncommon insects are usually found in gre- someres, pretarsus of all legs with an unusually large garious colonies in dead wood, but they do not have arolium; cerci short, one-segmented. a division of labor or polymorphism (as in termites The Mantophasmatodea is the most recently de- and ants). They feed chiefly on mites and other small scribed order of insects (2002) and the only new insect arthropods. All extant species are classified in the sin- order described since 1914. The order includes several gle genus Zorotypus. The sister group relationship of living species (from Namibia, South Africa, Tattzania, this order remains controversial and elusive. and Malawi) and six fossil species (5 from Baltic amber and one fossil from China). They resemble a mix be- SuperorderAcercaria tween praying mantises and phasmids, but molecular The supeforder Acercaria is sometimes referred to evidence indicates that they are most closely related to as the Paraneoptera or the "hemipteroids." These in- the Grylloblattodea. sects are characterized by (usually) short antennae, Mantophasmatodeans have several distinct char- enlarged cibarial (feeding) muscles, visible externally acteristics, including a hypognathous head and, most as an enlarged portion of the head; lacinia slender strikingly, when walking all species keep the fifth tar- and elongate; sucking mouthparts, tarsi with three or somere and pretarsus (a greatly enlarged arolium plus fewer tarsomeres, absence of cerci, lack of true male two tarsal claws) of each leg turned upwards and off gonopods, wings (when present) with reduced vena- the substrate, giving them the appearance of "walking tion, and hemimetabolous development (although life on their heels." Both sexes are wingless.Th"y are high- cycles in several groups includes one or two inactive ly flexible along their longitudinal body axis enabling pupa-like stages). them to clean their extemal genitalia with their mouth- parts. During the day they hide in bushes, rock crevices OrderThysanoptera Approximately 5,000described or clumps of grass and prey on spiders and insects at species (Figure 22.5D). Slender, minute (0.5-1.5 mm) night. Males and females produce percussive signals by insects with long, narrow wings (when present) bear- tapping their abdomens on the substrate to locate mates. ing long marginal setal fringes; mouthparts form a con- ical, asymmetrical sucking beak; left mandible a stylet, Order Embioptera (Embiidina) Approximately 400 right mandible vestigial; with compound eyes; anten- described species (Figure 22.41). Males somewhat nae with 4-10 flagellomeres; abdomen 10-segmented; flattened; females and young cylindrical. Most about without cerci; tarsi 1-2 segmented, with an eversible, 10 mm long, however Southeast Asian species in the pretarsal eversible adhesive sac, or arolium. Thrips are genus Ptilocerembia arc approximately 20 mm long. mostly herbivores or predators, and many pollinate Antennae filiform; ocelli lacking; chewing mouthparts; flowers. They are known to transmit plant viruses and head prognathous; legs short and stout; tarsi 3-articu- fungal spores. "Thrips" is both singular and plural. late; hind femora greatly enlarged. The basal article of the front tarsus is enlarged and contains glands that Order Hemiptera Approximately 85,000 species produce silk, which is spun from a dense field of hol- (Figure 22.54,8). Piercing-sucking mouthparts form low hairlike structures on the ventral surface. Males an articulated beak, mandibles and first maxillae sty- of most species are winged, but some are wingless; let-like, lying in dorsally grooved labium; forewings females and nymphs are always wingless. Abdomen either completely membranous, or hardened basally 1O-segmented, with rudiments of the eleventh seg- and membranous only distally; hindwings membra- ment, and a pair of short cerci. nousi pronotum large. Webspinners are small, slender, chiefly tropical Hemipterans occur worldwide and in virtually all insects. They live gregariously in silken galleries that habitats. Hemipterans are liquid feeders. Most feed on they construct in leaf litter, under or on stones, in soil the xylem or phloem of plants, although many feed on cracks, inbark crevices, and in epiphytic plants. Wings the hemolymph of arthropods or blood of vertebrates are made rigid for flight and flexible in galleries, by and some are specialized ectoparasites. They are of regulating the hemocoelic fluid pressure in the radial considerable economic importance because many 854 Chapter Twenty-Two

Figure22.5 Representatives of the three orders of Acercaria. (A) A true bug (order Hemiptera). (B) A cicada (order Hemiptera). (C) Two bark lice (order Psocodea). (D) A thrips (order Thysanoptera). Note that "thrips" is both singular and plural.

are serious crop pests. Members of one subfamily of were classified in two separate orders: the Psocoptera Reduviidae (Triatominae, the assassin or kissing bugs) (the book and bark lice) and the Phthiraptera (the true transmit Chagas disease. Others have more positive lice). Psocopterans are small (1-10 mm long); with economic importance to humans, such as the cochineal long, filiform, multiarticulate antennae; short pro- bugs (Dactylopiidae), from which a safe red dye (cochi- thorax; meso- and metathorax often fused; chewing neal) is extracted for use in the food industry. Shellac is mouthparts; abdomen 9-segmented; without cerci. made from lac, a chemical produced bv members of the Phthirapterans are even smaller (less than 5 mm), family Kerriidae (lac insecls). One of ihe most famous wingless, blood-sucking, obligate ectoparasites of hemipterans are the 17-year cicadas (genus Magiciada), birds and mammals; thoracic segments completely which have a very long life cycle and synchronized fused; cuticle largely membranous and expandable development and can reach plague-like levels of abun- to permit engorgement; compound. eyes abient or of dance (to 3.7 million individuals per hectare). Common 1-2 ommatidia; ocelli absent; piercing-sucking mouth- predacious hemipteran families include Nepidae parts retractable into a buccal pouch; antennae short (water scorpions), Belostomatidae (giant water bugs or (5 or fewer flagellomeres), exposed or concealed in "toe biters"), Corixidae (water boatmen), Notonectidae grooves beneath the head; with 1 pair dorsal thoracic (backswimmers), Gerridae (water striders), Saldidae spiracles and 6 or fewer abdominal spiracles; without (shore bugs), Cimicidae ftedbugs), and Reduviidae (as- cerci; females lack ovipositor. sassinbugs). Psocids-the book and bark lice-generally feed on Many others are plant feeders (hence the common algae and fungi, and occur in suitably moist areas (e.g., name "plant bugs"). Heavy infestations of these insects under bark, in leaf litter, under stones, in human habi- on plants may cause wilting, stunting, or even death, tations where humid climates prevail). They are often and some are vectors of important plant diseases. pests that get into various stored food products or con- Common herbivorous families include the Cicadidae sume insect and plant collections; some species live in (cicadas), Cicadellidae (leafhoppers), Fulgoridae (p1- books and eat the bindings. Commonly called sucking anthoppers), Membracidae (treehoppers), Cercopidae lice ( "Anoplura") and biting lice ("Mallophaga"), phthi- (spittle bugs and froghoppers), Aleyrodidae (white- rapterans spend their entire life on one host. Eggs (nits) flies), and Aphidae (aphids), as well as members of the are usually attached to the hair or feathers of the host, large superfamily Coccoidea (coccoids, scale insects, although the human body louse (a "sucking louse") mealybugs, and many others). may attach eggs to clothing. No biting lice are known to infest humans. Posthatching development comprises Order Psocodea Approximately 8,500 described spe- three nymphal instars. Some species that infest domes- cies (Figure 22.5C). Until recently, species in this order tic birds and mammals are of economic significance. PHYLUMARTHROPODA The Hexapoda:Insects and TheirKin 855

Superorder Holometabola Coleopterida Holometabola is a monophyletic group strongly sup- The Coleopterida includes two orders the Coleoptera ported by both morphological and molecular data. (beetles) and the Strepsiptera (twisted wing parasites). One of its key synapomorphies is indirect (holome- This clade includes the most diverse order of insects tabolous) development, with distinct egg, larval, (Coleoptera) and one with the most highly modified pupal, and adult states.During the pupal stage, most and morphologically and developmentally aberrant tissues undergo a tomplete reorganization (e.g., lar- groups of parasites (Strepsiptera). Largely due to their val eyes [stemmata] disintegrate and adult compound bizate combination of morphological characters, and eyes and ocelli form de noao).Another key apomorphy the high rate of molecular evolution in many strep- is the presence of internal wing buds (imaginal discs) sipteran genes, the sister group relationship of the in the larval stage, these clusters of early embryonic Strepsiptera eluded researchers until very recently. In cells arise from localized invaginations of the ecto- the past, Strepsiptera were considered at various times derm in the early embryo and form adult structures to be close relatives of either Hymenoptera, Diptera, during pupation. or Coleoptera. Recent genome-wide analyses and new morphological evidence strongly suggests that they are Order Hymenoptera Approximately 115,000 de- in fact the sister group to the Coleoptera. scribed species (Figure 22.6A). Mouthparts often elongate and modified for ingesting floral nectar, Order Coleoptera Approximately 380,000 described although mandibles usually remain functional; labi- species (Figure 22.68). Body usually heavily sclero- um often (bees) distally expanded as paired lobe- tized; forewings sclerotized and modified as rigid like structures called glossae and paraglossae; three covers (elytra) over hindwings and body; membra- ocelli; usually with two pairs of membranous wings; nous hindwings fold both transversely and longitudi- hindwings small, coupled to forewings by hooks nally, and are often reduced or absent; biting-chewing (hamuli); wing venation highly reduced; antennae mouthparts; antennae usually with 8-11 flagellomeres; well developed, of various forms and with 3-70 flag- prothorax large and mobile; mesothorax reduced; ellomeres, reduced metathorax usually fused to first abdomen fypically of 5 (or up to 8) segments; without abdominal segment; males with complex genitalia; ovipositor; male genitalia retractable. females with ovipositor (in most), modified for saw- Coleoptera is the largest order of insects. Many hy- ing, piercing, or stinging. potheses have been proposed to explain the extraordi- The earliest fossil Hymenoptera date from the nary diversity of beetles, including: (1) their age, the Triassic (220-207 Ma). Ants, bees, wasps, sawflies, and oldest fossils date to the early Permian but they most their relatives are all active insects with a tendency probably arose in the late Carboniferous (300 Ma); (2) to form polymorphic social communities. Two sub- their heavily sclerotized bodies, including their protec- orders are generally recognized. Suborder Symphyta tive elytra, and general lack of exposed membranous contains the primitive, wasplike, "thick-waisted" hy- surfaces facilitates their adaptation to a wide variety menopterans (sawflies, horntails, and their kin). They of tight narrow spaces and reduced their risk of preda- rarely show conspicuous sexual dimorphism and are tion; and (3) the their co-evolution with the great an- always fully winged. The first and second abdomi- giosperm radiation in the Cretaceous period. Today, nal segments are broadly joined. Larvae are mostly beetles range from minute (0.35 mm, Nanosellafungi) caterpillar-like, with a well-developed head capsule, to very large (20 crr.,Titanus giganteus) and occur in all true legs, and often also with abdominal prolegs. the world's environments (except the open sea). Some Suborder Apocrita contains the "narrow-waisted" of the world's strongest animals are beetles: rhinocer- hymenopterans (true wasps, bees, and ants), in which os beetles can carry up to 100 times their own weight the first and second abdominal segments are joined for short distances, and 30 times their weight indefi- by a distinct and often elongate constriction. Adults nitely (equivalent to a 150-pound man walking with a tend to be strongly social and display marked poly- Cadillac on his head-without tiring). Humans have morphism. Social communities often include distinct had a long fascination with beetles, and beetle worship castes of queens, haploid males, parthenogenetic fe- can be traced back to at least 2500 BC. (The venerated males, and individuals with other sex-related special- scarab of early Egyptians was actually a dung beetle.) izations, as well as non-reproducing worker and sol- Some common coleopteran families include dier forms. Common families of Hymenoptera include Carabidae (ground beetles), Dytiscidae (preda- the Apidae (bumblebees and honeybees), Formicidae ceous diving beetles), Gyrinidae (whirligig beetles), (ants), Vespidae (yellow jackets, hornets, paper wasps/ Hydrophilidae (water scavenger beetles), Staphylinidae and potter wasps, Halictidae (sweat bees), Sphecidae (rove beetles), Cantharidae (soldier beetles), (sand wasps, digger wasps, and mud-daubers), and Lampyridae (fireflies and lightrring bugs), Phengodidae three large groups of parasitic wasps (Ichneumonidae, (glowworms), Elateridae (click beetles), Buprestidae Braconidae, Chalcidoidea). (metallic wood-boring beetles), Coccinellidae (ladybird 856 Chapter Twentv-Two

beetles), Meloidae (blister beetles), Tenebrionidae Order Raphidioptera Approximat ely 260 described (darkling beetles), Scarabaeidae(scarab beetles, dung species (Figure 22.6E). Snakeflies strongly resemble beetles, June "bugs"), Cerambycidae (long-horned neuropterans (and are often regarded as a suborder), beetles), Chrysomelidae (leaf beetles), Curculionidae but are unique in having the prothorax elongate (as in (weevils), Brentidae (primitive weevils), and Ptiliidae the mantises), but the forelegs similar to the other legs. (featherwinged begtles, the smallest of all beetles, some The head can be raised above the rest of the body, as with body lengths bf just 0.35 mm). in a snake preparing to strike. Adults and larvae are predators on small insect prey. Order Strepsiptera Approximately 600 described species (Figure 22.6C). Extreme sexual dimorphism; Order Neuroptera Approximately 6,000 described males freeJiving and winged; females wingless, usu- species (Figure 22.6F). Adults soft-bodied; with two ally parasitic. Females of free-living species with dis- pairs of similar, highly veined wings held tent-like tinct head, simple antennae, chewing mouthparts, and over the abdomen when at rest; with biting-chewing compound eyes. Females of parasitic speciesneoten- mouthparts; abdomen 1O-segmented;without cerci; ous, larviform, usually without eyes, antennae, and larvae with mandibles and maxillae co-adapted to legs; with indistinct body segmentation. Male anten- create a sucking tube; mouth closed off by modified nae often with elongate processes on flagellomeres; labrum and labium; well developed legs; larval midgut forewings reduced to club-like structures resembling is closed off posteriorly, larval waste accumulates until halteres of Diptera; hindwings large and membranous, the adult emerges; Malpighian tubules secrete silk, via with reduced venation; raspberry-like eyes. the anus, to construct the pupal cocoon. Most of these minute insects are parasitic on other The'lacewings, ant lions, mantisflies, spongilla- insects. Adult females of parasitic species are larviform flies, and owlflies form a complex group, the adults and most commonly live between the abdominal scler- of which are often important predators of insect pests ites of flying insects that pollinate flowers, such as bees (e.g., aphids). The larvae of many species have pierc- and wasps. Winged males find the females on the bee ing-sucking mouthparts, and those of other species are or wasp abdomen and mate with her. The fertilized predaceous and have biting mouthparts. The pupae eggs hatch into first instar larvae inside their mother's are often unusual in possessing free appendages and body. These larvae, called triungulins, have well devel- functional mandibles used for defense; they may ac- oped eyes and legs and they actively crawl out of their tively walk about prior to the adult molt, but do not mother to invade the soil and vegetation. The triun- feed. Common families include Chrysopidae (green gulins eventually locate a new host insect and enter it, lacewings), Myrmeleontidae (ant lions); Ascalaphidae wherein they molt into a legless wormlike larval stage (owlflies); Mantispidae (mantidflies). that feeds in the host's body cavity. Pupation also takes place within the host's body, where the females re- Antliophora main for the rest of their lives and the freeliving males The Antliophora include three orders, the Mecoptera, emerge as fully formed adults. Siphonaptera, and Diptera. There is strong molecular and morphological support for the monophyly of this Neuropterida group. The males of all members of Antliophora have The three orders of Neuropterida have always been a sperm pump, a structure that aids in sperm transfer considered close relatives. Some workers subsume the during copulation. Many other more characters also Megaloptera and Raphidioptera within the Neurop- define this grouping, most of which have to do with tera, but all three groups are monophyletic making relatively subtle aspects of the adult mouthparts. such a taxonomic decision arbitrary. These three orders have two pairs of membranous wings with many cross Order Mecoptera Approximately 600 described spe- veins, S-segmented tarsi, adults with mandibles, and cies (Figure 22.6G). TWo pairs of similar, narrow mem- decticous pupae (with articulated mandibles). branous wings, held horizontally from sides of body when at rest; antennae long, slender, and of many Order Megaloptera Approximately 300 described flagellomeres (about half the body length); head with species (Figure 22.6D). Ocelli present or absent; larvae ventral rostrum and reduced biting mouthparts; long, aquatic, with lateral abdominal gills. Megalopterans slender legs; mesothorax, metathorax, and first abdom- (alderflies, dobsonflies, fishflies) strongly resemble inal tergum fused; abdomen 1l-segmented; female neuropterans (and are often regarded as a suborder), with two cerci; male genitalia prominent and com- but their hindwings are broader at the base than the plex, at apex of attenuate abdomen and often resem- forewings, and the longitudinal veins do not have bling a scorpion's stinger. The larvae of some species branches near the wing margin. Larvae of some mega- are remarkable in having compound eyes, a condition lopterans (hellgrammites) are commonly used as fish unknown among larvae of other insects having com- bait. plete metamorphosis. PHYLUMARTHROPODA The Hexapoda:Insects and Their Kin 857

Figure 22.6 Representatives of the eleven orders of Megaloptera). (E) A snakefly (order Raphidioptera). (F) A Holometabola. (A) A paper wasp (order Hymenoptera). green lacewing (order Neuroptera). (G) A scorpionfly (order (B) A pleasing fungus beetle, Gibbifer californicus (order Mecoptera). (H) A adult mde Oropsylla montana flea Coleoptera). (C) Female twisted wing parasites (order (order Siphonaptera). (l) A golden dung fly (Scathophaga Strepsiptera) visible between the abdominal sclerites stercoraria) (order Diptera). (J) A caddisfly (order of a wasp (order Hymenoptera). (D) An alderfly (order Trichoptera). (K) A luna moth (order Lepidoptera).

Mecopterans are usually found in moist places, Order Siphonaptera Approximately 3,000described often in forests, where most are diumal flyers. They are species(Figure 22.6H). Small (less than 3 mm long); best representedin the Holarctic region. Somefeed on wingless;body laterally compressedand heavily scler- nectar; others prey on insectsor are scavengers.There otized; short antennaelie in deep grooves on sides of are several families, including Panorpidae (scorpion- head; mouthparts piercing-sucking; compound eyes flies), Bittacidae(hangingflies), and Boreidae(snow often absen! legsmodified for clinging and (especially scorpionflies). hindlegs)jumping; abdomen11-segmented; abdominal 858 Chapter Twentv-Two

segment 10 with distinct dorsal pincushion-like sensil- in extreme environments, such as hot springs, saline lum, containing a number of sensory organsi without desert lakes, oil seeps, tundra pools, and even shallow ovipositor; pupal stage passed in a cocoon. benthic marine habitats. Adult fleas are ectoparasites on mammals and birds. Some common dipteran families include Asilidae from which they take blood meals. They occur wher- (robber flies), Bombyliidae (bee flies), Calliphoridae ever suitable hosts are found, including the Arctic and (blowflies, bluebottles, greenbottles, screwworm Antarctic. Larvab usually feed on organic debris in flies, etc.), Chironomidae (midges), Coelopidae (kelp the nest or dwelling place of the host. Host specific- flies), Culicidae (mosquitoes: Culex, Anopheles, etc.), ity is often weak, particularly among the parasites of Drosophilidae (pomace or vinegar flies; often also mammals, and fleas regularly commute from one host called "fruit flies"), Ephydridae (shore flies and brine species to another. Fleas act as intermediate hosts and flies), Glossinidae (tsetse flies), Halictidae (sweat vectors for organisms such as plague bacteria, dog and bees), Muscidae (houseflies, stable flies, etc.), Otitidae cat tapeworms, and various nematodes. Commonly (picture-winged flies), Sarcophagidae (flesh flies), encountered species include Ctenocephalidesfelis (cat Scatophagidae (dung flies), Simuliidae (blackflies and flea), C. canis (dog flea), Pulex irritans (domestic flea), buffalo gnats), Syrphidae (hover flies and flower flies), andDiamus montanus (western squirrel flea). Tabanidae (horseflies, deerflies, and clegs), Tachinidae (tachinid flies), Tephritidae (fruit flies), and Tipulidae Order Diptera Approximately 135,000described spe- (crane flies). cies (Figure 22.6I). Adults with one pair of membra- nous mesothoracic forewings and a metathoracic pair Amphiesmenoptera of clublike halteres (organs ofbalance); head large and The Amphiesmenoptera contains the orders Trichop- mobile; compound eyes large; antennae primitively tera and Lepidoptera. Some characteristics that unite filiform, witlnT to 16 flagellomeres and often second- these two groups include the presence of hairy wings arily annulated (reduced to only a few articles in some (the hairs are modified into scales in Lepidoptera), groups); mouthparts adapted for sponging, sucking, the females are the heterogametic sex, and the larval or lapping; mandibles of blood-sucking females devel- labium and hypopharynx are fused into a composite oped as piercing stylets; hypopharynx, laciniae, galeae, lobe with the opening of an associated silk gland at and mandibles variouslv modified as stvlets in para- its apex. sitic and predatory gtonpr; labium forms a proboscis ("tongue"), consisting of distinct basal and distal por- Order Trichoptera Approximately 12,000described tions, the latter in higher families forming a sponge- species (Figure 22.6D. Adults resemble small moths, like pad (labellum) with absolptive canals; mesothorax but with body and wings covered with short hairs; greatly enlarged; abdomen primitively 11-segmented, two pairs of wings, tented in oblique vertical plane but reduced or fused in many higher forms; male geni- (rooflike) over abdomen when at rest; compound eyes talia complex; females without true ovipositor, but present; mandibles minute or absent; antennae usually many with secondary ovipositor composed of tele- as long or longer than body, setaceous; legs long and scoping posterior abdominal segments; larvae lack slender; larvae and pupae mainly in fresh wate1, adults true legs, although ambulatory structures (prolegs and terrestrial; larvae with abdominal prolegs on terminal "pseudopods") occur in many. segment. The true flies (which include mosquitoes and gnats) The freshwater larvae of caddisflies construct fixed are a large and ecologically diverse group, notable for or portable "houses" (cases)made of sand grains, their excellent vision and aeronautic capabilities. The wood fragments, or other material bound together by mouthparts and digestive system are modified for a silk emitted through the labium. Larvae are primar- fluid diet, and several groups feed on blood or plant ily herbivorous scavengersi some use silk to produce juice. Dipterans are vastly important carriers of human food-filtering devices. Most larvae inhabit benthic hab- diseases, such as sleeping sickness, yellow fever, itats in temperate streams, ponds, and lakes. Adults are African river blindness, and various enteric diseases. strictly terrestrial and have liquid diets. It has been said that mosquitoes (and the diseases they carry) prevented Genghis Khan from conquering Order Lepidoptera Approximately 720,000 Russia, killed Alexander the Great, and played pivotal described species (Figure 22.6K). Minute to large; suck- roles in both world wars. Myiasis-the infestation of ing mouthparts; mandibles usually vestigial; maxillae living tissue by dipteran larvae-is often a problem for coupled, forming a tubular sucking proboscis, coiled livestock and occasionally for humans. Many dipterans between labial palps when not in use; head, body, are also beneficial to humans as parasites or predators wings, and legs usually densely scaled; compound of other insects and as pollinators of flowering plants. eyes well developed; usually with two pairs of large Dipterans occur worldwide and in virtually every and colorfully scaled wings, coupled to one another major environment (except the open sea). Some breed by various mechanisms) protibia with epiphysis used Figure 22.7 Defense, warning coloration, and camouflage in insects. (A) A leaf-mimicking katy- did (Orthoptera: Tettigoniidae) from Ecuador is perfectly camouflaged. (B) The bright coloration of the silkmoth caterpillar (Lepidoptera: Saturniidae: Hyalophora eu ryal us), warns potential predators of the defensive hairs on its back. (C) A bombardier beetle (Coleoptera: Carabidae: Brachinus) sprays nox- ious benzoquinones in defense while being "attacked" by for- ceps. (D) Close-up of an "eye spot" on a luna moth (see Figure 22.6K) (Lepidoptera: Saturniidae). Eyespots attract predators away from the moth's head and body and encourage predators to focus on their wings. Since butterflies and moths can fly even with slight wing damage, eyespots are a commonly used defense mecha- nism. (E)A spittlebug (Hemiptera: Cercopoidea) produces a cover of frothed-up plant sap resembling saliva which hides the nymph from the view of predators and parasites.

for cleaning antennae; male genitalia complex; females The Hexapod Body Plan with ovipositors. Butterflies and moths are among the best known General Morphology and most colorful of all the insects. The adults are pri- In Chapter 20 we briefly discussed the various advan- marily nectar feeders, and many are important polli- tages and constraints imposed by the phenomenon of nators, some of the best known being the large hawk, arthropodization, including those associated with the or sphinx, moths (Sphingidae). A few tropical species establishment of a terrestrial lifestyle. Departure from are known to feed on animal blood, and some even the ancestral aquatic environment necessitated the evo- drink the tears of mammals. The larvae (caterpillars) lution of stronger and more efficient support and loco- feed on green plants. Caterpillars have three pairs of motory appendages, special adaptations to withstand thoracic legs and a pair of soft prolegs on each of ab- osmotic and ionic stress, and aerial gas exchange struc- dominal segments 3-6; the anal segment bears a pair tures. The basic arthropod body plan included many of prolegs or claspers. Butterflies can be distinguished preadaptations to life in a "dry" world. As we have from moths by two features: their antennae are always seen, the arthropod exoskeleton inherently provides long and slender, ending in a knob (moth antennae are physical support and protection from predators, and never knobbed), and their wings are typically held to- gether above the body at rest (moths never hold their 2One of the best known butterfly taxonomists was the great wings in this position). Over 80% of the described Russian novelist Vladimir Nabokov (Lolita, Pale Fire, The Gift), Lepidoptera are moths. who left Saint PetersburginL9lT to travel around Europe and (first Other common families include Psychidae (bag eventually settled in the United States working at the American Museum of Natural History in New York, then at worms); Cossidae (carpenter worms); Pyralidae (snout Cornell University). Nabokov was a specialist on the blue but- moths); Saturniidae (silk moths); Sphingidae (hawk terflies (Polyommatini) of the New World and a pioneer anato- moths); Hesperiidae (skippers); Ceometridae (inch mist, coining such alliterative anatomical terms as "alula" and "bullula." Butterflies, real and imaginary, flit through 60 years worms); Arctiidae (tiger moths); Noctuidae (owlet of Nabokov's fiction, and many lepidopterists have named but- moths); Papillionidae (swallowtails); Nymphalidae terflies after characters in his life and writings (e.g., species epi- (brush-footed butterflies); Pieridae (whites and sul- thets include lolita, humbert, ada, zembla, and aokoban-a reversal of Nabokov). Nabokov's descriptions of Lolita were patterned phurs); Lycaenidae (gossamer-winged butterflies); and after his species descriptions of butterflies (e.g., "her fine downy Riodinidae (metalmarks).2 limbs"). 860 Chapter Twentv-Two

(A) by incorporating waxes into the epicuticle, the insects, like the arachnids, acquired an effective barrier to water loss. Similarly, within the Hexapoda, the highly adapt- able, serially arranged arthropod limbs evolved into a variety of specialized locomotory and food-capturing appendages. Reproductive behavior became increas- ingly complex, aril in many cases highly evolved so- cial systems developed. Within the class Insecta, many (B) taxa underwent intimate coevolution with land plants, particularly angiosperms. The adaptive potential of in- sects is evident in the many species that have evolved striking camouflage, warning coloratior; and chemical defense (Figure22.7). Non-insect hexapods (proturans, collembolans, and diplurans-the entognathous hexapods) differ from insects in several important ways. The mouthparts are not fully exposed (i.e., they are entognathous), the (c) mandibles have a single point of articulation, develop- ment is always simple, the abdomen may have a re- duced number of segments, and they never developed flight. Insects are primitively composed of 20 somites (as in the Eumalacostraca; Chapter 21), although these are Figure 22.8 The principal body regions of hexapods, not always obvious. The consolidation and specializa- illustrated by three kinds of insects. (A) A grqsshopper tion of these body segments (i.e.,tagmosis) has played (wings removed). (B) A beetle. (C) An ant. In each case, a key role in hexapod evolution and has opened the the stippled region is the head; the white region is the tho- way for further adaptive radiation. The body is always rax; the black region is the abdomen. organized into a head, thorax, and abdomen (Figures 22.8and22.9), comprising6,3, and 11 segmentsrespec- tively. In contrast to marine arthropods, a true cara- labium) (Figure 22.11). Compound eyes, as well as pace never develops in hexapods. In the head, all body three simple eyes (ocelli) are typically present in adult sclerites are more or less fused as a solid head capsule. hexapods. The median (anterior) ocellus is thought to In the thorax and abdomen, the adult sclerites usually have arisen through the fusion of two separate ocelli. develop embryologically such that they overlap the The internal manifestation of the fused exoskeleton primary segment articulations, forming secondary seg- of the head forms a variety of apodemes, braces, and ments, and these are the "segments" we typically see struts collectively called the tentorium. Externally, when we examine an insect extemally (e.g., the tergum the head may also bear lines that may demarcate its and sternum of each adult abdominal secondary seg- original segmental divisions, and others that represent ment actually overlap its adjacent anterior primary the dorsal (and ventral) ecdysial lines, where the head segment) (Figure 22.10). The primitive (primary) body capsule splits in immature insects and which persist as segmentation can be seen in unsclerotized larvae by unpigmented lines in some adults. Still other lines rep- the insertions of the segmental muscles and transverse resent inflections of the surface associated with internal grooves on the body surface. apodemes. Most insects are small, between 0.5 and 3.0 cm in The antennae (Figure 22.12) arc composed of three length. The smallest are the thrips, feather-winged bee- regions: the scape, pedicel, and multijointed sensory tles, and certain parasitic wasps, which are all nearly flagellum. The scape and pedicel constitute the proto- microscopic. The largest are certain beetles, orthopter- pod; the flagellum represents the telopod. Among the ans, and stick insects, the latter attaining lengths great- entognathous insects, muscles intrinsic to the scape, er than 56 cm. However, certain Paleozoic species grew pedicel and flagellum are retained. But in the class to twice that size. To familiarize you with the hexapod Insecta, the intrinsic muscles of the antennae have been body plan and its terminology, we briefly discuss each lost except for those in the scape. In addition, in many of the main body regions (tagmata) below. insects the joints, or flagellomeres, of the flagellum may have been secondarily subdivided (or annulated) The hexapod head The hexapod head comprises to produce additional unmuscled joints, and increasing an acron and six segments, bearing (from anterior to the length and flexibility of the antenna. posterior) the eyes, antennae, clypeolabrum, and three The mouth is bordered anteriorly by the clypeola- pairs of mouth appendages (mandibles, maxillae, brum, posteriorly by the labium, and on the sides by PHYLUMARTHROPODA The Hexaooda:Insects and Their Kin 861

Abdomen

Forewing ["*r-'n-*Metathorax Hindwing Antennae Compound eye Mesothorax

Prothorax------l Tergites

Cercus

Ovipositor

Tibia

Femur Tympanum Sternites Post-tarsus Arolium

\Tarsal claw

(B) (c) Antenna Frons Compound Clypeus Mandible Prothorax Labrum Mesothorax Labial palp Maxillary palp Metathorax

Forewing Coxa Prothoracicleg 'Femur Trochanter Hindwing

Mesothoracicleg Tibia Abdomen S-jointed tarsus

Metathoracicleg Sgl. d Ceicus Figure 22.9 Generalbody anatomy of insects.(A) A grasshopper(order Orthoptera).(B,C) Dorsal and ventralviews of a cockroach(order Blattodea).

(A) Posterior Anterior

tl tl II i-Primary segment--|

Figure22.10 The ontogenesisof insect body segments. (A) Primarysegmentation. (B) Simple secondary segmenta- tion. (C)More advancedsecondary segmentation. 862 ChapterTwenty-Two

(A) Front vlew

Frons

Clypeus

Labrum Labrum fll f,l t: ..,1 X-J ft ,J Maxillary palp w klft( wr'd'/ r Mandible Labial palp ffil Hypopharynx Head

Cardo Submentum

Stipes Palpiger

Lacinia

Palp

( Glottu/ Lieula{ Labial palp " ^raragrossa I Labium (first maxilla) (secondmaxilla)

Figure 22.11 The mouth appendages of a typical biting-chewing insect: a grasshopper (order Orthoptera). (A) Front view. (B) Side view. the mandibles and maxillae. In the entognathans, the prognathous (projecting anteriorly) or opisthogna- mouthparts are sunk within the head capsule and thous (projectingposteri orly ; Figarc 22.73). largely hidden from view. In contrast, the mouthparts The labrum is a movable plate attachedto the mar- of insects are exposed (ectognathous) and ventrally gin of the clypeus(a projectingfrontal head piece),and projecting (hypognathous). However, in some insects, together they form the clypeolabrum. Some work- the orientation of the head has changed so that they are ers regard the clypeolabrumto be an independently

(A) (F) % E{

0) Figure 22.12 A variety of insect antennae and the ter- minology generally applied to them. (A) Setaceous. (B) .7YX Filiform. (C) Moniliform. (D,E) Clavate. (F) Capitate. (G) Serrate. (H) Pectinate. (l) Plumose. (J) Aristate. (K) Stytate. \**dz (L) Flabellate. (M) Lamellate. (N) Genicutate.

(K) A -=:-_=.=.z:$, PHYLUMARTHROPODA The Hexapoda:Insects and TheirKin 863

(A) (B)

Mandible Maxillary ial Maxillary palp PAlP PAIP

Labial palp

Prothoracic leg

Figure 2213 Different positions of head and mouth- parts relative to the rest of the body. (A) Hypognathous some insects (e.g., Hemiptera), the labium is draum out condition (grasshopper). (B) Prognathous condition (beetle into an elongate trough to hold the other mouthparts, larva). (C) Opisthorhynchous condition (aphid). and its palps may be absent; in others (e.g., Diptera), it is modified distally into a pair of fleshy porous lobes derived structure of the exoskeleton; others believe it called labellae. could be the fused appendagesof the first or third head segment.The mandibles (Figure 22.1,4)are strongly The hexapod thorax The three segments of the tho- sclerotized,usually toothed,and lack a palp. In most rax are the prothorax, mesothorax, and metathorax insectsthe mandible is of one article,but in someprim- (Figure 22.9). Their tergites carry the same prefixes: itive groups (and fossil taxa) it is composedof several pronotum, mesonotum, metanotum. In the winged articles.However, the geneDistal-less (Dll) is apparent- insects (Pterygota), the mesothorax and metathorax ly never expressedin the embryogenyof hexapodan are enlarged and closely united to form a rigid ptero- mandibles, suggestingthat they are fully gnathobasic thorax. Wings, when present, are bome on these two (i.e.,protopodal). The maxillae are generally multi- segments and articulate with processes on the tergite articulateand bear a palp of 1.-7articles. The labium (notum) and pleura of the somites. The prothorax is comprises the fused secondmaxillae and typically sometimes greatly reduced, but in some insects it is bearstwo palps.In addition to theseappendages, there greatly enlarged (e.g., beetles) or even expanded into is a median, unpaired, tonguelike organ called the hy- a large shield (e.g., cockroaches).The lateral, pleural popharynx that projects forward from the back of the sclerites are complex and thought to be derived, at preoral cavity. The salivary glands open through the least in part, from subcoxal (protopodal) elements of hypopharynx.' the ancestral legs thatbecame incorporated into the lat- In the past variations in feeding appendageswere eral body wall. The stemites may be simple, or may be often used to define the major insect clades,and more divided into multiple sclerites on each segment. recentmolecular phylogeneticwork has largely cor- Each of the three thoracic somites bears a pair of legs roborated thoseideas although a number of casesof (Figure 22.9), composed of two parts, a proximal pro- convergentevolution in mouthparts have also been topod and a distal telopod. The protopod (sometimes revealed.In sucking insectsboth mandiblesand maxil- lae may be transformed into spear-likestructures (sty- lets),or the mandiblesmaybe absentaltogether (Figure Adductor 22.15and22.24).In most Lepidoptera,the maxillae muscle form an elongatecoiled sucking tube, the proboscis.In Abductor muscle 3Study of the Dll gene reveals that it was probably primitively expressed in the distal parts of all arthropod appendages. It is also expressed in the endites, or inner lobes, of arthropod limbs (e.g., Double in the phyllopodous limbs of Branchiopoda and in the maxillae of articulation Malacostraca). In crustaceans and myriapods there is an initial Dll expression in the mandibular limb buds that is displaced laterally and continues in the mandibular palp in crustaceans. In insects, no Dll expression at all is seen in the mandibles-it has appar- ently been completely lost. Thus, the mandibles of all three groups are gnathobasic. The palp of the crustacean mandible represents the distal portion of the mandibular limb, altogether lost in hexa- pods and myriapods. The only real "wholelimb jaws" among the Mandible artfuopods are those of onychophorans. Dll is also expressed in the coxal endites of chelicerates and the pedipalp endites of arach- nids. The complete loss of Dll expression in hexapod mandibles may be a synapomorphy for the group. Figure 22.14 The musculature of an insect mandible. 864 ChapterTwenty-Two I

Figure 22.15 A variety of insect mouth appendages, specialized for different types of feeding habits. (A,B) Piercing-sucking Maxillary mouthparts of a mosquito (Diptera). Note the naln r ^-r complex stylet structure in (B). (C) Sucking Labrum mouthparts of a honeybee (Hymenoptera). Labium epipharynx (D) Sucking mouthparts of a butterfly Food channel (Lepidoptera). (E) Sponging mouthparts of a false blackfly (Diptera). (For an illustration Hypopharynx of biting-chewing mouthparts, see Figure Salivary duct 22.1't.)

Mandible Maxilla Labrum epipharynx

Mandible ypopharynx Labellum (c) Compound eye

Clypeus Maxillary

YAIY Labrum Mandible

Maxilla Epipharynx Mandible Maxilla Hypopharynx Labellum Glossa

called a "coxopodite"by entomologists)is composed occurs in them, and they are thus viewed as subdivi- of two articles (coxa,trochanter), and the telopod is sions of a single original article. The whole length of composedof four articles (femur, tibia, tarsusrpretar- the tarsus is crossed by the tendon of the flexor muscle sus) (Figure22.1,6). The tarsusis often subdivided into of the pretarsus, whose fibers usually arise on the tibia additional pseudoarticlescalled tarsomeres.The basal (Figure 22.77). The pretarsus is a minute article that hexapodshave a single tarsus(Protura and Diplura) or usually bears a pair of lateral claws. The pretarsus in an indistinct tarsus(Collembola;probably fused with Collembola and Protura bears a single median claw. A the tibia). In the Archaeognatha the tarsus is usually single claw also occurs in many holometabolous larvae composedof three tarsomeres,and in the Pterygotait is and some pterygote adults. But in most hexapods, the composedof one, three, or five tarsomeres.aWhatever pretarsus bears a pair of lateral claws, and many also the number of tarsal articles,no intrinsic musculature have a median arolium (which functions as an adhe- sive pad on smooth surfaces), unguitractor plate, or alt medianclaw. is unclear whether having one or several tarsomeres is the In insects, many adult organs derive primitive condition for the Ilexapoda. Homologization of the leg from clusters - articles among the various arthropod groups is a popular and of early embryonic cells called imaginal discs, which often rancorous pastime. The issue is further confused when the arise from localized invaginations of the ectoderm in number of articles differs from the norm (e.g., some insects have the early embryo. The embryonic thorax two trochanters, the number of tarsi varies from one to five, etc.). contains three The protopods of myriapods, chelicerates, and trilobites all seem pairs of leg discs, and as development proceeds, these to consist of a single basal article (usually called the coxa). In the discs develop a series of concentric rings, which are the latter case, KukalovS-Peck hypothesizes that three "missing,, pro- presumptive leg articles. The center topodal articles were lost by fusion among themselves andwith of the disc corre- the pleural region. See Chapter 20 for a discussion of ancestral sponds to the distalmost articles (tarsus and pretarsus) arthropod legs. of the future leg, while the peripheral rings correspond PHYLUMARTHROPODA The Hexaooda:Insects and Their Kin 865

(c)

Coxa Pollen basket Rake Pollen Press Basitarsus

'k,

Notch for antennal groorning nsec,sA The hindleg of a grasshopper (Orthoptera), modified for iumping. (B) The raptorial foreleg of a mantid (Mantodea), modified for prey capture. (C) The hindleg of a honeybee (Hymenoptera), modified for collecting and holding pollen (anatomy diagram and photograph). (D) The foreleg of a worker honeybee has a notch for antennal grooming. (E) The foreleg of a mole cricket (Orthoptera), modified for digging. (F) The hindleg of a backswimmer (Hemiptera), modified for swimming (anatomy diagram and photo- Pretarsus graph). (G) Close-up of insect tarsus with 5 tarsomeres Tarsomeres and a pretarsus with 2lateral claws flanking an arolium.

to its proximal region (coxa, trochanter). During em- Most workers use a consistent naming system that bryogenesis, the leg telescopes out as it subdivides into recognizes six major veins: costa (C), subcosta (SC), ra- the component articles. The gene Distal-less (Dll) is ex- dius (R),media (M), cubitus (CU), and anal (A) (Figure pressed in the presumptive distal region of the limb, 22.18).Areas in the wings that are enclosedby longi- while the gene Extradenticle (Exd) is necessary for the tudinal and crossveins are called cells, and thesetoo development of the proximal portion of the limb. Thus the protopod and telopod of the legs are each under Trochanter their own genetic control. Trochanter depressor levator Within the Pterygota, most species also have a pair muscle muscle of wings on the second and third thoracic segments. Wing morphology has been more extensively used in insect classification than any other single structure. Articulation Wings are often the only remains of insects preserved Femoral reductor Tibial depressor Pretarsal muscle muscle in fossils. The wings of modern insects develop as depressor evaginations of the integument, with thin cuticular Tarsal depressor muscles membranes forming the upper and lower surfaces muscle of each wing. Wing veins, which contain circulating Tarsal levator hemolymph, anastomose and eventually open into muscle the body. The arrangement of veins in insect wings provides important diagnostic characters at all taxo- nomic levels. The origin and homologization of wing venation has been heavily debated over the decades. Figure 2217 The musculature of an insect leg. 866 Chapter Twenty-Two I

Figure 22.18 The nomenclature of basic wing venation in insects. Although the cells formed within the veins also have names, only the names of the veins are given here. Longitudinal veins are coded R3 with capital letters, cross veins with low- ercase letters. Longitudinal veins: costa (C); subcosta (SC); fadius (El);radial sec- tor (RS); media (M); cubitus (CU); anat (A). Cross veins: humeral (h); radial (r); sectorial (s);radiomedial (rm); medial (m); mediocu- bital (m-cu); cubitoanal (cu-a).

CUz cUru have a somewhat complex nomenclature. In some insects, however, the intromittent organ develops late groups (e.g., Orthoptera, Dermaptera) the forewings in embryogeny by fusion of the genital papillae to form develop heavily sclerotized regions called tegmina a median, tubular, often eversible endophallus, with (sing. tegmin), used for protection, stridulation, or the joined ejaculatory ducts opening at a gonopore at other purposes. In many sedentary, cryptic, parasitic, its base. The external walls may be sclerotized or modi- and insular lineages the wings have become shortened fied in a wide variety of ways, and the whole organ is (brachypterous) or lost (apterous). Insects often couple known as the aedeagus. Some workers consider the their wings together for flight by means of hook{ike aedeagus to be derived from segment 9; others regard devices along the margin between the posterior border it as belonging to segment 10. A pair of sensory cerci of the forewings and the anterior margin of the hind- (sing. cercus) often project from the last abdominal wings (e.9., hamuli in Hymenoptera; frenula in many segment. Lepidoptera). In these insects the coupled wings func- tion together as a single unit. Locomotion Walking Hexapods rely on their sclerotized exo- The hexapod abdomen The abdomen primitively skeleton for support on land. Their limbs provide the comprises 11 segments, although the first is often physical support needed to lift the body clear of the reduced or incorporated into the thorax, and the ground during locomotion. In order to accomplish this, last may be vestigial. Abdominal pleura are greatly the limbs must be long enough to hold the body high reduced or absent. The occurrence of true (though min- off the ground, but not so high as to endanger stability. ute) abdominal leglets (sometimes called "prolegs" ot Most hexapods maintain stability by having the legs "styli") on the pregenital segments is commonplace in positions that suspend the body in a sling{ike fash- among the apterygotes and also occurs in the larvae of ion and keep the overall center of gravity low (Figure many pterygotes (e.g., the legs of caterpillars). In addi- 20.19). tion, transitory limb buds or rudiments appear fleet- The basic structure of arthropod limbs was described ingly in the early embryos of some species,presumably in Chapter 20. In hexapods (and crustaceans) the ante- harking back to the deep evolutionary past. Abdominal rior-posterior limb movements take place between the segments 8-9 (or 7-9) are typically modified as the ano- coxae and the body proper (in contrast to most arach- genital tagmata, or terminalia, the exposed parts being nids, in which the coxae are immovably fixed to the the genitalia. The female median gonopore occurs body and limb movement occurs at more distal ioints). behind sternum 7 in Ephemeroptera and Dermaptera, Like the power controlled by the range of gears in an and behind sternum 8 or 9 in all other orders. The anus automobile, the power exerted by a limb is greatest at is always on segment 11 (which may be fused with seg- low speeds and least at higher speeds. At lower speeds ment 10). the legs are in contact with the ground for longer pe- There is enormous complexity in both clasping and riods of time, thus increasing the power, or force, that intromittent organs among the Hexapoda, and a cor- can be exerted during locomotion. In burrowing forms respondingly sharp disagreement over the homologi- the legs are short, and the gait is slow and powerful as zation and terminology of these structures. In gener- the animal forces its way through soil, rotting wood, al, females discriminate among males on the basis of or other material. Longer limbs reduce the force, but sensory stimuli produced by the male genitalia; hence increase the speed of a running gait, as do limbs capa- selection pressure has been a powerful force in the ble of swinging through a greater angle. Limbs long in evolution of these structures (inboth sexes).The most length and stride are typical features of the fastest-run- primitive male architecture can be seen in apterygotes ning insects (e.g.,tiger beetles, Carabidae). and Ephemeroptera, in which the penes are paired One of the principal problems associated with in- and contain separate ejaculatory ducts. In most other creased limb length is that the field of movement of one PHYLUMARTHROPODA The Hexaooda:Insects and Their Kin 867

predator,generates 400 g of force,with a peak decel- eration of 2,300g.

Flight Among the many remarkable advancesof insects,flight is perhaps the most impressive. Insects were the first flying animals, and throughout the histo- ry of life on Earth no other invertebrateshave learned the art of true flight. The wingless insectsbelong either OrJ to groups that have secondarilylost the wings (e.g., fleas,lice, certain scaleinsects) or to primitive taxa (the I apterygotes)that aroseprior to the evolution of wings. In three orders, the wings are effectively reduced to a single pair. In beetles,the forewings are modified as a protectivedorsal shield (elytra).In dipterans,the hind- wings aremodified asorgans of balance(halteres). The halteresbeat with the samefrequency as the forewings, functioning as gyroscopesto assist in flight perfor- (': manceand stability-flies fly very well. Compared with an insect,an airplane is a simple study in aerodymamics.Planes fly by moving air over Figure 22.19 A beetle walking. The alternating tripod a fixed wing surface,the leading edgeof which is tilted gait consists of alternate stepping with two sets of three upward, forcing the air to travel farther (thus faster) legs; thus the body is always suppoded by a triad of legs. over the top of the wing than the bottom, resulting in Here, three legs (Ll , R2, and L3) are moving forward while a vortex that createsa lift. But conventionalfixed-wing the other three (Rl , L2, and R3) are on the ground. aerodynamic theory is insufficient to understand insect flight. Insect wings are anything but fixed. Insects,of course, fly by flapping their wings to createvortices, limb may overlap that of adjacentlimbs. Interference from which they gain lift, but thesevortices slip off the is prevented by the placement of the tips of adjacent wings with eachbeat, and new vortices are formed legsat different distancesfrom the body (Figure22.19). with eachalternate stroke. Beating insect wings trace Thus fast-running insectsusually have legs of slightly a figure eight pattern, and they also rotate at certain different lengths. Insectsusually move their legs in an crucial moments. Thus, each cycle of flapping creates alternating tripod sequence.Balance is maintained by dynamic forces that fluctuate drastically. By complex always having three legs in contact with the ground. actions of wing orientation, insectscan hover, fly for- Like many spiders,some insects can walk on water, ward, backward, and sideways,negotiate highly so- and they do so in much the sameway-by balancing phisticated aerial maneuvers,and land in any posi- the pull of gravity on their featherweight bodies with tion. To complicate matters even more, in the caseof the physical principles of buoyancy and surface ten- small insects (and most are small, the average size of sion. Insects(and spiders)that walk on water don't get all insectsbeing just 3-4 mm), the complex mechanics wet becausetheir exoskeletonsare coatedwith waxes of flight take place at very low Reynoldsnumbers (see that repel water molecules.The water surface,held taut Chapter 4), such that the insectis essentially"flying by surfacetension, bends under eachleg to createa de- through molasses."As a result of thesecomplex me- pressioryor dimple, that works to push the animal up- chanics,insect flight is energetically costly, requiring ward in support. Water walking occursin many insect metabolicrates as high as 100times the resting rate. groups, notably the Hemiptera (e.9.,water striders), Each wing articulates with the edge of the notum Coleoptera(e.g., whirligig beetles),and Collembola (thoracic tergite), but its proximal end rests on a dor- (somespringtails).5 solateralpleural processthat actsas a fulcrum (Figure Many insectsare good jumpers (e.g.,fleas, spring- 22.20).The wing hinge itself is composedin large part tails, most orthopterans),but the click beetles of resilin, a highly elasticprotein that allows for rapid, (Elateridae)are probably the champions.It has been sustainedmovement. The complex wing movements calculatedthat a tlpical click beetle (e.9.,Athous haem- are made possible by the flexibility of the wing itself orrhoidalis),when jackknifing into the air to escapea and by the action of a number of different muscle sets that run from the baseof the wing to the inside walls of the thoracic segmenton which it is borne. Thesedi- 5On an undisturbed surface, water molecules are attracted to their rect flight musclesserve to raise and lower the wings neighbors beside and below, resulting in a flat skin of molecules that exerts only horizontal tensile forces; it is this "elasticity" of and to tilt their plane at different angles (somewhat the surface that we call surface tension. like altering the blade angles on a helicopter) (Figure 868 ChapterTwenty-Two

Figure 22.20 A typical insect wing hinge arrangement. A) (B) Resilin plus This transverse section through the thoracic wall of a Pure resilin chitin lamellae grasshopper shows the base of the wing and the wing hinge. (A) Entire hinge area. (B) Enlargement of hinge section.

22.27). However, dxceptin palaeopterans (Odonata and Ephemeroptera), the direct flight muscles are not the main source of power for insect wing movements. Most of the fti force comes from two sets of indirect flight muscles, which neither originate nor insert on the Wing hinge \% wings themselves (Figures 22.21 and 22.22). Pleuron Fibrous Dorsal longitudinal muscles run between apodemes protein at the anterior and posterior ends of each winged Epidermis segment. When these muscles contract, the seg- Endocuticle ment is shortened, which results in a dorsal arching of the segment roof and a downstroke of the wings. Dorsoventral muscles, which extend from the notum to of the mesothorax and metathorax. Other, smaller tho- the sternum (or to basal leg joints) in each wing-bear- racic muscle sets serve to make minor adiustments to ing segment, are antagonistic to the longitudinal mus- this basic operation. cles. Contraction of the dorsoventral muscles lowers Insects with low wing-flapping rates (e.g., dragon- the roof of the segment. ln doing so, it raises the wings. flies, orthopterans, mayflies, and lepidopterans) are Thus, wing flapping in most insects is primarily gener- limited by the rate at which neurons can repeatedly ated by rapid changes in the walls and overall shape fire and muscles can execute contractions. However, in insects with high wing-flapping rates (e.g., dipterans, hymenopterans, and some coleopterans), an entirely (B) different regulatory mechanism has evolved. Once

muscle: contracted

Figure 22.21 Wing movements of a primitive insect such as a dragonfly, in which direct wing muscles cause depression of the wings. Dots represent pivot points, and arrows indicate the direction of wing movement. (A) The dorsoventral muscles contract to depress the notum as the basalar muscles relax, a combination forcing the wings into an upstroke. (B) The dorso- ventral muscles relax as the basalar muscles contract, a com- bination pulling the wings into a downstroke and relaxing (and raising) the notum. (C) Thorax of a dragonfly showing wing attachment to the notum of thoracic segments 2 and 3. PHYLUMARTHROPODA The Hexapoda:Insects and TheirKin 869

(B) Dorsal longitudinal Nofum: muscles: arched contracted

Pivot (fulcrum) on pleural process

3li'.",J,i"$xl".,.0 Figure 22.22 Wing movements of an insect such as a thoracictergites (paranotal lobes), which eventually downward fly or hemipteran, in whieh both upward and becamearticulated and muscledto form wings. The movements of the wings are produced by indirect flight hypothesizesthat wings evolved from pre-exist- muscles. In these transverse sections of a thoracic seg- latter ment, dots represent pivot points, and arrows indicate the ing articulated structureson the thoracic appendages, direction of wing movement. Only two sets of muscles are such as gills or protopodal exites on the legs. There is shown. (A) The dorsoventral muscles contract, depressing also tantalizing evidencefrom the fossil record sug- the thoracic notum and forcing the wings into upstroke. gestingthat the first pterygote insectspossessed ap- (B) The dorsoventral muscles relax as the dorsal longitu- pendageson the prothorax,called "winglets," that may the notum, elevating it dinal muscles contract to "pop up" have been serially homologous to modern wings, im- and forcing the wings into a downstroke. plying that the loss of prothoracic proto-wings might have taken place in the early evolutionary history of flight has been initiated and a high wing-flapping rate the Hexapoda. attained (up to 100 beats/second), myogenic control The paranotallobe hypothesiswas first proposedby takes over. This mechanism exploits the elastic-me- Mtiller in1,873,saw a resurgenceof popularity in the chanical properties of the exoskeleton. When one set middle of the twentieth century, and has lost favor in of indirect muscles contracts, the thorax is deformed. recentyears. It suggeststhat wings originated aslateral Upon relaxation of the muscles, there is an elastic re- aerodynamicflaps of the thoracic nota that enabled bound of the thoracic exoskeleton, which stretches the insectsto alight right side up when jumping or when second set of indirect muscles and thus directly stimu- blown about by the wind. Thesestabilizing Parano- lates their contraction. This contraction establishes a tal lobes later evolved hinged structures and muscles second deformation, which in turn stretches and stim- at their bases.The occurrenceof fixed paranotal lobes ulates the first muscle group. Once initiated, this mech- in certain ancient fossil insectshas been cited in sup- anism is nearly self-perpetuating, and the nonsynchro- port of the paranotal lobe hypothesis (Figure22.23). nous firing of neurons serves only to keep it in action. However, recent studies suggestthat these primitive Not all insects utilize wings to travel through the air. paranotallobes might have been used for other pur- Many small and immature insects are effectively dis- poses,such ascovering the spiracularopenings or gills persed by wind power alone. Some first-instar lepidop- in amphibious insects,protecting or concealingthe terans use silk threads for dispersal (as do spiders and insectsfrom predators,courtship displays, or thermo- mites). Tiny scale insects are commonly collected in regulationby absorptionof solar radiation. aerial nets. In fact, studies have revealed the existence The appendagehypothesis (alsoknown as the "gill of " aerial plankton" consisting of insects and other or branchial theory," "exite theoryi' or "leg theory") minute arthropods, extending to altitudes as high as also datesback to the nineteenthcentury, but was res- 14,000 feet. Most are minute winged forms, but wing- urrectedby the great entomologistV. B. Wigglesworth less species are also common. in the 7970s,and was championed by f. Kukalov6- Peck sincethe 1980s.It is the more favored hypoth- The Origin of Insect Flight esisof wing origin today, basedon recentpaleonto- For many decades, two competing views of insect wing logical work, microscopic anatomy, and molecular origin have dominated. In general, these views can be developmental biology. It suggeststhat insect wings termed the paranotal lobe hypothesis and the append- are derived from thoracic appendages-from pro- age hypothesis. The former holds that wings evolved topodal exites,in Wigglesworth and Kukalov6-Peck's by way of a gradual expansion of lateral folds of the view. Theseproto-wing appendagesmight have first 870 ChapterTwenty-Two

(A) Dorann+ar r^l form the leg primordium, from which they segregate, migrating dorsally to a position below the tergum. Forewing Recent studies on gene expression also support the ori- gin of wings from legs. The genes pdm and apterousarc expressed in the wing (and leg) primordia of all insects. Expression of both genes appears to be necessary for normal wing formation. In malacostracan crustaceans (but not in branchiopod crustaceans) these same genes are expressed, in a similar manner, in the formation of Hindwing the leg rami (the exopod and endopod).

Feeding and Digestion Feeding Every conceivable kind of diet is exploited (B) by species within the Hexapoda, whose feeding strate- gies include herbivory, carnivory, and scavenging, as lobe well as a magnificent array of commensalism and par- asitism. This "nutritional Forewing radiation" has played a key role in the phenomenal evolution among the Insecta. A comprehensive survey of insect feeding biology alone Hindwing could easily fill a book this size. Setting aside symbiotic relationships for a moment, in the most general sense insects can be classified as (1) biters-chewers, (2) suck- ers/ or (3) spongers (Figure 22.24). Biters-chewers, such as the grasshoppers, have the least modified mouthparts, so we describe them first. The maxillae and labium of these insects have well de- veloped leglike palps (Figure22.24A) that help them hold food in place, while powerful mandibles cut off Figure 22.23 Fossil insects with paranotal lobes on the and chew bite-sized prothorax. (A) Stenodictya lobata. (B) Lemmatophora typa. pieces. The mandibles lack palps (C) Nymphal stage of Rochdalia parkeri, a Paleozoic ter- (in all insects) and typicallybear small, sharp teeth that restrial palaeodictyopteran. In this species, all three tho- work in opposition as the appendages slide against racic segments appear to have had "articulated" thoracic each other in the transverse (side to side) fashion char- lobes. acteristic of most arthropod jaws. Biting-chewing in- sects may be carnivores, herbivores, or scavengers. In functioned as aquatic gills or paddles, or as terrestrial many plant eaters, the labrum bears a notch or cleft in gliding structures. The paired abdominal gills of may- which a leaf edge may be lodged while being eaten. flies have been suggested as serial homologues of such Some of the best examples of this feeding strategy are "proto-wings." In KukalovS-Peck's version of this hy- seen among the Orthoptera (locusts, grasshoppers, pothesis, the first protopodal leg article (the epicoxa) crickets), and most people have witnessed the efficient fused with the thoracic pleural membrane early in the fashion in which these insects consume their garden evolution of the Arthropoda, as did the second article plants! Equally impressive are the famous leafcutter (the precoxa) in the ancient hexapods, with both mi- ants of the Neotropics, which can denude an entire tree grating dorsally off the leg and onto the body proper. in a few days. Leafcutter ants have a notable feeding In insects, the epicoxa eventually fused with the tergite, adaptation: when cutting leaf fragments, they produce its exite enlarging to form the proto-wing, and even- high-frequency vibrations with an abdominal stridu- tually the true wing. The precoxa formed the pleural latory organ. This stridulation is synchronized with sclerite providing the ventral articulation of the wing. movements of the mandible, generating complex vi- Wing veins might have evolved from cuticular ridges brations. The high vibrational acceleration of the man- that served to strengthen these structures, and eventu- dible appears to stiffen the material being cut, just as ally to circulate blood through them.6 soft material is stiffened with a vibratome for section- Kukalovd-Peck's theory of wing evolution finds ing in a laboratory. Leafcutters don't eat the leaves they support in molecular developmental studies, which cuf instead, they carry them into an underground nes! have shown that the cells that give rise to the wing where they use them to grow a fungus on which they primordium derive from the same cluster of cells that feed. Several other insect groups have evolved associa- tions with fungi, and in almost every case these rela- bUnspecialized coxal exites can be seen on the legs of some living tionships are obligate and mutualistic-neither parbter archaeognathans (bristletails) and in numerous eltinct hexapodsl can live without the other. PHYLUMARTHROPODA The Hexaooda:Insects and Their Kin 871

Figure 22.24 Mouthparts specialized for different modes of feeding. (A) Biting-chewing mouthparts of a often barbed to tear the prey's tissuesand enlarge the grasshopper. Note the well developed leglike palps. (B) wound. The labrum is in the form of a small flap cov- Sponging mouthparts of a fly. (G) Sucking mouthparts of a ering the base of the grooved labium. When piercer- (D) Piercing mouthparts of a true bug. butterfly. suckersfeed, the labium remains stationary, and the stylets do the work of puncturing the plant (or animal) In sucking insects the mouthparts are markedly and drawing out the liquid meal. modified for the consumption of liquid foods, gener- Different variations of piercing-sucking mouthparts ally plant sapsor nectarsor animal blood or cell fluids are found in other insect taxa. In mosquitoes,midges, (Figure 22.24D).Sucking mouthparts and liquid diets and certainbiting flies (e.g.,horseflies) there are six have clearly evolved many times in different insect long, slender stylets, which include the labrum-epi- lines-further testimony to the frequency of evolution- pharynx and the hypopharynx as well as the man- ary convergencein arthropods and the developmental dibles and first maxillae (Figure 22.15A).Other biting adaptability of their appendages.In some sucking in- flies, such as the stable fly, have mosquitoJike mouth- sects,such as mosquitoes,feeding is initiated by pierc- parts but lack mandibles and maxillae altogether. Fleas ing the victim's epidermal tissue;this mode of feeding (Siphonaptera)have three stylets: the labrum-epi- is referred to as piercing-sucking. Other insects,such pharynx and the two mandibles.Thrips have unusual asbutterflies and moths that feed on flower nectar,do mouthparts: the right mandible is greatly reduced, not pierce anything and are merely suckers. making the head somewhat asymmetrical, and the left In all sucking insectsthe mouth itself is very small mandible, first maxillae, and hypopharynx make up and hidden. The mouthparts,instead of being adapted the stylets. for handling and chewing solid piecesof food, are elon- Lepidopterans are nonpiercing sucking insects gated into a needle-likebeak adapted for a liquid diet. in which the paired first maxillae are enormously Different combinations of mouth appendagesconsti- elongated, coiled, and fused to form a tube through tute the beak in different taxa.True bugs (Hemiptera), which flower nectar is sucked (Figure 22,24C);the which are piercer-suckers, have a beak composed mandibles are vestigial or absent(Figure 22.15D).The of five elements:an outer troughlike element (the la- mouthparts of beesare similar: the first maxillae and bium) and, Iying in the trougtu four very sharp stylets labium are modified together to form a nectar-suck- (the two mandibles and two maxillae). The stylets are ing tube, but the mandibles are retained and used for 872 Chapter Twenty-Two

(B)

Dilator muscle Dilator muscle of cibarium of pharynx

Pharynx

Mouth Cibarium Salivary duct Salivary pump Clypeus lea (lobe of maxilla)

Labium

Mandible Figure 22.25 Feeding pump of a cicada (Hemiptera). (A) Close-up head showing dilated cibarial pump for feeding on xylem. (B) Diagram- matic vedical cross section of the head and cibarium. Note the enlarge- Maxilla ment of the cibarial dilator muscles, which activate the feeding pump. wax manipulation during hive construction (Figure exposing the blood and cellular fluids to be sponged 22.15C). The collected nectar is stored in a special "sac" up by the labellae. in the foregut and carried back to the hive where it is Many insects are scatophagous, feeding on animal converted into honey, which is stored as a food reserve. feces. Most of these groups have biting mouthparts, Bees in an average hive consume about 500 pounds of but some (such as certain flies) have sucking mouth- honey per year-we humans get the leftovers. parts. Perhaps the most famous of the scatophagous in- Associated with sucking mouthparts are various sects are the dung beetles, or tumblebugs (certain bee- mechanisms for drawing liquid food into the mouth. tles in the families Scarabaeidae and Histeridae). These Most piercer-suckers rely largely on capillary action, remarkable insects harvest animal dung by biting or but others have developed feeding "purrlps." Often the slicing off pieces with specialized head or leg struc- pump is developed through elongation of the preoral tures and working them into a ball. They may roll the cavity, or cibarium, which by extension of the cuticle dung ball a considerable distance, and eventually bury around the mouth becomes a semi-closed chamber it in the soil, whereupon females deposit eggs within it. connecting with the alimentary canal (Figure 22.25). Larvae are thus assured of a ready food supply. Dung In these cases,cibarial muscles from the clypeus are balls may even be maneuvered by apair of dung bee- enlarged to make a powerful pump. In lepidopterans, tles pushing and pulling in a cooperative effort. dipterans, and hymenopterans the cibarial pump is There are many symbiotic insects, and two orders combined with a pharyngeal pump, which operates are composed entirely of wingless parasites, most by means of muscles arising on the front of the head. of which spend their entire lives on their host: some Specialized salivary glands are also often associated Psocodea (lice) and Siphonaptera (fleas). Bird lice are with sucking mouthparts. In some hemipterans a sali- common, and lice are also found on dogs/ cats, hors- vary pump forces saliva through the feeding tube and es, cattle, and other mammals. Biting lice have broad into the prey, softening tissues and predigesting the heads and biting mouthparts used to chew epithelial liquid food. In mosquitoes, saliva carries blood thin- cells and other structures on the host's skin. Sucking ners and anticoagulants (and often parasites such as lice have narrow heads and piercing-sucking mouth- Plasmodium,which causes malaria). parts, which they use to suck blood and tissue fluids In spongers, such as most flies (order Diptera), the from their host, always a mammal. Unlike most ar- labium is typically expanded distally into a labellum thropod parasites, lice (of both types) spend their en- (Figures 22.75E and25.24B). Fluid nutrients are trans- tire lives on the bodies of their hosts, and transmission ported by capillary action along minute surface chan- to new hosts is by direct contact. For this reason most nels from the labellae to the mouth. In many spongers, lice show a high degree of host specificity. Eggs, or nits, such as houseflies, saliva is exuded onto the food to are attached by the female to the feathers or hair of partly liquefy it. In strict spongers, the mandibles are the host, where they develop without a marked meta- absent. ln biting spongers, such as horseflies, the man- morphosis. Many lice, particularly those whose diet is dibles serve to slice open a wound in the flesh. thus chiefly keratin, possess symbiotic intracellular bacteria PHYLUMARTHROPODA The Hexapoda:Insects and Their Kin 873 that appear to aid in the digestion of their food. These adobe house). Mosquitoes (family Culicidae), on the bacteria are passed to the offspring by way of the in- other hand, are vectors for a large number of disease- sects' eggs. Similar bacteria occur in ticks, mites, bed- causing microorganisms, including Plasmodium (re- bugs, and some blood-sucking dipterans. sponsible for malaria; Figure 3.16), yellow fever, viral None of the biting lice are known to infest people or encephalitis, dengue, and lymphatic filariasis (with its to transmit human disease microorganisms, although gross symptom, elephantiasis, resulting from blockage one species acts as an intermediate host for certain of lymph ducts). Kissingbugs (Hemiptera, Reduviidae, dog tapeworms. The sucking lice, on the other hand, Triatominae) also have a casual host relationship. Thuy include two genera that commonly infest humans live in all kinds of environments, but often inhabit the (Pediculus and Phthirus). The latter genus includes burrows or nests of mammals, especially rodents and the notorious P. pubis, the human pubic "crab" Iouse armadillos, as well as birds and lizards. They feed on (which often occurs on other parts of the body as well). the blood of these and other vertebrates, including A number of sucking lice are vectors for human disease dogs, cats, and people. Their host specificity is low. organisms. The most common reaction to infestation Several species are vectors of mammalian trypano- with lice-a condition known as pediculosis, or being somiasis (Trypanosomacruzi, the causative agent of lousy-is simple irritation and itching caused by the Chagas' disease). The tendency of some species to bite anticoagulant injected by the parasite during feeding. on the face (where the skin is thin) has resulted in the Chronic infestation with lice among certain footloose commonname. travelers is manifested by leathery, darkened skin-a In the dipteran family Calliphoridae, larvae are sa- condition known as vagabond's disease. prophagous, coprophagous, wound feeding, or para- Fleas (order Siphonaptera) are perhaps the best sitic. The parasitic species include earthworms, locust known of all insect parasites. Nearly 1,500species from egg cases, termite colonies, and nestling birds among birds and mammals have been described. Unlike lice, their hosts, and several parasitize humans and do- fleas are holometabolous, passing through egg,larval, mestic stock (e.9., Gochliomyiaamericana, the tropical pupal, and adult stages. Some species of fleas live their American scren worm). entire lives on their host, although eggs are generally Many insect parasites of plants cause an abnor- deposited in the host's environment and larvae feed on mal growth of plant tissues, called a gall. Some fungi local organic debris. Larvae of domestic fleas, includ- and nematodes also produce plant galls, but most are ing the rare human flea (Pulex irritans), feed on virtu- caused by mites and insects (especially hymenopter- ally any organic crumbs they find in the household ans and dipterans). Parasitic adults may bore into the furniture or carpet. Upon metamorphosis to the adult host plant or, more commonly, deposit eggs in plant stage, fleas may undergo a quiescent period until an tissues, where they undergo larval development. The appropriate host appears. A number of serious disease presence of the insect or its larva stimulates the plant organisms are transmitted by fleas, and at least 8 of tissues to grow rapidly, forming a gall. The adaptive the 60 or so species of fleas associated with household significance (for insects) of galls remains unclear, but rodents are capable of acting as vectors for bubonic one popular theory is that their production interferes plague bacteria. with the production of defensive chemicals by the Other insect orders contain primarily free-living in- plant, thus rendering gall tissues more palatable. A sects,but include various families of parasitic or micro- somewhat similar strategy is used by leaf miners, spe- predatory forms, or groups in which the larval stage cialized larvae from several orders (e.g., Coleoptera, is parasitic but the adults are free-living. Most of these Diptera, Hymenoptera) that live entirely within the tis- "parasites" do not live continuously on a host and have sues of leaves, burrowing through and consuming the feeding behaviors that fall into a gray zone between most digestible tissues. true obligate parasitism and predation. Such insects are An interesting predatory strategy is that of New sometimes classed as intermittent parasites, or micro- Zealand glowworms (Ar achnocampaluminosa), which predators. Bedbugs (Hemiptera, Cimicidae), for exam- live in caves and in bushes along riverbeds. These lar- ple, are minute flattened insects that feed on birds and vae of small flies produce a bright bioluminescence mammals. However, most live in the nest or sleeping in the distal ends of the Malpighian tubules, which area of their host, emerging only periodically to feed. lights up the posterior end of the body. (The light The common human bedbugs (Cimex lectularius and peaks at 485 nm wavelength.) Each larva constructs a C. hemipterus)hide in bedding, in cracks, in thatched horizontal web from which up to 30 vertical "fishing roofs, or under rugs by day and feed on their host's lines" descend, each with a regularly spaced series of blood at night. They are piercer-suckers, much like sticky droplets. Small invertebrates (e.g., flies, spiders, the sucking lice. Bedbugs are not known to transmit small beetles, hymenopterans) attracted to the light any human diseases,although when present in large are caught by the fishing lines, hauled up, and eaten. numbers they can be troublesome (in South America, Harvestmen (Opiliones), the main predators of glow- as many as 8,500 bugs have been found in a single worms, use the light to locate their prey! 874 Chapter Twenty-Two

(A) Hindgut

Pylorus (B) Invagination of stomodeum

Malpighian Gastric cecum tubule

Figure 22.26 Main subdivisions of an insect gut. (A) The entire alimentary canal. (B) The junction of the foregut and midgut in a dipteran. Note the origin of the Foregut- peritrophic membrane and the fold formed by the stomo- deal invaginationand the midgut wall. Cells secreting peritrophic membrane

Secretioncoalescing Digestive system Like the guts of all arthropods,the to membrane long, usually straight hexapod gut is divisible into a stomodealforegut, endodermalmidgut, and proctode- Perihophic membrane al hindgut (Figwe22.26).Salivary glands are associated with one or severalof the mouth appendages(Figure 22.27).The salivary secretionssoften and lubricate chitinous material may line the midgut or pull free to solid food, and in some speciescontain enzymesthat envelop and coat the food particles as-Ul"ypus through initiate chemical digestion. In larval moths (caterpil- the gut. The peritrophic membrane servesto protect the lars), and in larval beesand wasps,the salivary glands delicatemidgut epithelium from abrasion.It is perme- secretesilk used to make pupal cells. ated by microscopicpores that allow passageof en- All hexapods,as well asmost other arthropods that zpes and digested nutrients. Lr many species,produc- consume solid foods, produce a peritrophic mem- tion of this membranealso takesplace in the hindgut, brane in the midgut (Figure 22.268).This sheetof thin where it encapsulatesthe fecesas discrete pellets.

(A)

Salivary gland Figure 22.27 Internal anatomy of Salivary bladder two common insects. (A) Cockroach. Prothoracic ganglion (B) Grasshopper. Mesothoracicganglion e Metathoracic ganglion I Crop frr First abdominal ganglion Proventriculus t_fI I Salivary gland ! l.drntesnne - $ Gastric ceca f vtatpigtrtan I tubules ( L LHindgut I Clypeus Labrum Ovipositor Malpighian tubules Maxillary palp PHYLUM ARTHROPODA The Hexaooda:Insects and TheirKin 875

lral slnus

diaphragm Gut Segmental Perivisceral sinus vessel Ventral diaphragm Heart

Nerve cord (B) Dorsal diaphragm Dorsal Pulsatile organ diaphragm ergosternal Aorta muscle Antennal pulsatile organ Segmental vesicle rebral ganglion Aliform muscle

Septa Figure 22.28 The circulatory system of insects. (A) An insect abdomen (cross section). Note the division of the hindgut serves primarily to regulate the composition hemocoel into three chambers (a dorsal pericardial sinus, a ventral perineural sinus, and a central perivisceral sinus). of the feces and perhaps to absorb some nutrients. These chambers are separated by diaphragms lying on Digestion of cellulase by termites and certain wood- frontal planes. (B) Blood circulationin an insect with a eating roaches is made possible by enzymes produced fully developed circulatory system (longitudinal section). by protists and bacteria that inhabit the hindgut. Arrows indicate the circulatory course. (C) A cockroach Clusters of fat cells create a fat body in the hemocoel (ventral dissection). Note the dorsal and segmental ves- of many insects, which is most conspicuous in the ab- sels. The dorsal diaphragm and aliform (heart) muscles are domen but also extends into the thorax and head. The continuous over the ventral wall of the heart and vessels, but they are omitted from the diagram for clarity. fat body is a unique organ to the insects and is often likened to the vertebrate liver and the chlorogogen tissue in annelids. The fat body not only stores lipids, proteins and carbohydrates, but also slmthesizes pro- Along with their vast range of feeding habits, in- teins. Many insects do not feed during their adult life; sects have evolved a number of specialized digestive instead, they rely on stored nutrients accumulated in structures. The foregut is typically divided into a well the larval or juvenile stages and stored in the fatbody. defined pharynx, esophagus, crop, and proventriculus (Figures 22.26 and22.27). The pharynx is muscular, Circulation and Gas Exchange particularly in the sucking insects, in which it com- The hexapod circulatory system includes a dorsal tu- monly forms a pharyngeal pump.The crop is a storage bular heart that pumps the hemocoelic fluid (blood) center whose walls are highly extensible in species that toward the head. The heart narrows anteriorly into a consume large but infrequent meals. The proventricu- vessel-like aorta, from which blood enters the large he- lus regulates food passage into the midgut, either as a mocoelic chambers, through which it flows posteriorly, simple valve that strains the semifluid foods of suck- eventually retuming to the pericardial sinus and then ing insects or as a grinding organ, called a gizzard or to the heart via paired lateral ostia (Figure 22.28).In gastric mill, that masticates the chunks ingested by bit- most insects the heart extends through the first nine ing insects. Well-developed gastric mills have strong abdominal segments; the number of ostia is variable. cuticular teeth and grinding surfaces that are gnashed Accessory pumping organs, or pulsatile organs, often together by powerful proventricular muscles. occur at the bases of wings and of especially long ap- The midgut (= stomach) of most insects bears gastric pendages, such as the hindlegs of grasshoppers, to as- ceca that lie near the midgut-foregut junction and re- sist in circulation and maintenance of blood pressure. semble those of crustaceans. These evaginations serve The heart is a rather weak pumping organ, and to increase the surface area available for digestion and blood is moved primarilv bv routine muscular activ- absorption. In some casesthe cecaalso house mutual- ity of the body and appendiges. Hence, circulation is istic microorganisms (bacteria and protists). The insect slow and system pressure is relatively low. Like many 876 ChapterTwenty-Two

(A) (c) Fluid in tracheole Trichomes

Tracheole

Taerfdium

Tracheolar cell body

Figure 22.29 The tracheal system of insects. (A) Tracheoles and flight muscle cells. Note the region where the trachioles become functionally intracellular within the muscle fibers. The upper figure depicts a situation in which the muscle cells are well oxygenated, oxygen demand is low, and fluid accumulates in the trachioles. The lower figure depicts muscle cells that are oxygen- deficient. Decreased fluid volumes in the tracheoles allow the tissues increased access to oxygen. (B) A tracheole end cell. The taenidia are rings that serve to keep the lumen of the trachioles open. (C) A generalized insect spir- acle (longitudinal section). Note the dust-catching spines (trichomes) within the atrium. (D) View inside a prothoracic trachea of the honeybee, Apis mellifera. (960x) (E) SEM of trachea and tracheoles of a carabid beetle. (F) Dragonfly nymph molting into an adult. Note the long white tracheae being pulled arachnids,some hexapodsuse the hydraulic pressure out of the exuvia by the emerging adult. of the hemocoelic system in lieu of extensormuscles. In this way, for example,butterflies and moths unroll their maxillary feeding tubes. in wound healing and clotting. Nutrients, wastes,and Many types of hemocyteshave been reported from hormones can be efficiently carded by this system, but the blood of insects. None functions in oxygen stor- respiratory oxygen cannot (some CO, does diffuse age or transport, but severalare apparently important into the blood). The active lifestyles of theseterrestrial PHYLUMARTHROPODA The Hexapoda:Insects and TheirKin 877 animals require special structures to carry out the tasks and gas exchange takes place directly between the body of respiratory gas exchange and excretion. These struc- cells and the tracheoles. Unlike tracheae, tracheoles are tures are the tracheal system and the Malpighian tu- not shed during ecdysis. The tracheoles are so minute bules, described below. (0.2-1.0 pm) that ventilation is impossible, and gas trans- Desiccation is one of the principal dangers faced by port here relies on aqueous diffusion. This ultimate con- terrestrial invertehrates. Adaptations to terrestrial life straint on the rate of gas exchange may be the primary always involve so'medegree of compromise between reason terrestrial arthropods never achieved extremely water loss and gas exchange with the atmosphere. large sizes. Even though the general body surface of insects may In aquatic insects the spiracles are usually nonfunc- be largely waterproof, the gas exchange surfaces can- tional, and gases simply diffuse across the body wall not be. directly to the tracheae. A few species retain functional In some minute hexapods, such as Collembola, gas spiracles; they hold an air bubble over each opening, exchange occurs by direct diffusion across the body through which oxygen from the surrounding water surface. However, the vast majority of hexapods rely diffuses. The air bubbles are held in place by secreted on a tracheal system (Figure 22.29). As explained in waxes and by patches of hydrophobic hairs in densities Chapter 20, tracheae are extensive tubular invagina- that may exceed 2 million per square millimeter. Most tions of the body wall, opening through the cuticle by aquatic insects, particularly larval stages, have gills- pores called spiracles. Up to ten pairs of spiracles can external projections of the body wall that are covered occur on the pleural walls of the thorax and abdomen. by thin, unsclerotized cuticle and contain blood, tra- Since tracheae are epidermal in origin, their linings are cheae, or air bubbles (Figure 22.30).The gills contain shed with each molt. The cuticular wall of each trachea channels that lead to the main tracheal system. In some is sclerotized and usually strengthened by rings or spi- aquatic insects, such as dragonfly nymphs, the rectum ral thickenings called taenidia, which keep the tube bears tiny branched tubules called rectal accessory from collapsing but allow for changes in length that gills. By pumping water in and out of the anus, these may accompany body movements. The tracheae origi- insects exchange gases across the increased surface nating at one spiracle commonly anastomose with oth- area of the thin gutwall. There are analogous examples ers to form branching networks penetrating most of the of hindgut respiratory irrigation in other, unrelated in- body. In some insects it appears that air is taken into vertebrate groups (e.g., echiurids, holothurians). the body through the thoracic spiracles and released Excretion and Osmoregulation through the abdominal spiracles, thus creating a flow- through system. The problem of water conservation and the nature of Each spiracle is usually recessed in an atrium, the circulatory and gas exchange systems in terrestrial whose walls are lined with setae or spines (trichomes) arthropods necessitated the evolution of entirely new that prevent dust, debris, and parasites from entering structures to remove metabolic wastes. Like the gas the tracheal tubes. A muscular valve or other closing exchange surfaces, the excretory system is a site of device is often present and is under control of internal potential water loss, because nitrogenous wastes ini- partial pressures of O, and COr. In resting insects most tially occur in a dissolved state. These problems are of the spiracles are generally closed. Ventilation of the tracheal system is accomplished by simple diffusion gradients, as well as by pressure changes induced by the animal itself. Almost any movement of the body or gut causes air to move in and out of some tracheae. *i Telescopic elongation of the abdomen is used by some Gills insects to move air in and out of the tracheal tubes. Many insects have expanded tracheal regions called tracheal pouches, which function as sacsfor air storage. Becausethe blood of hexapods does not transport ox- ygen, the tracheae must extend directly to each organ of the body, where their ends actually penetrate the tissues. Oxygen and CO, thus are exchanged directly between cells and the small ends of the kacheae, the tracheoles.hr the case of flight muscles, where oxygen demand is high, the tracheal tubes invade the muscle fibers themselves. Caudai fili"inents Tracheoles, the innermost parts of the tracheal system, are thin-walled, fluid-filled channels that end as a sin- Figure 22.30 Aquatic nymph ot a maylly, Para- gle cell, the tracheole end cell (= tracheolar cell) (Figure leptophlebia (Ephemeroptera), with lateral abdominal 22.29).The tracheoles penetrate every organ in the body, gills. 878 ChapterTwenty-Two Malpighian tubule

Figure 22.31 A single Malpighian tubule opening into the hindgut at its junction with the midgut. Arrows indi- cate the flow of materials.

r(-,+ , urate, Water, K- solutes

compounded in small terrestrial organisms, such as environments. In many terrestrial arthropods (includ- many hexapods, because of their large surface area- ing primitive insects) an eversible coxal sac (not to be to-volume ratios. And water loss problems are even confused with the coxal glands of arachnids) proj- more severe in flying insects, because flight is prob- ects from the body wall near the base of each leg. It is ably the most metabolically demanding of all locomo- thought that the coxal sacs assist in maintaining body tor activities. hydration by taking up water from the environment In most terrestrial arthropods, the solution to these (e.g., dewdrops). Many insects collect environmental problems is Malpighian tubules. In the Hexapoda, water by various other devices. Some desert beetles these unbranched outgrowths of the gut arise near (Tenebrionidae) collect atmospheric water by "stand- the junction of the midgut and hindgut (Figures22.26, ing on their heads" and holding their bodies up to the 22.27, and 22.31).Their blind distal ends extend into moving air so that humidity can condense on the abdo- the hemocoel and lie among various organs and tis- men and be channeled to the mouth for consumption. sues. Up to several hundred Malpighian tubules may Insects that inhabit desert environments have a be present. much greater tolerance of high temperatures and body In the absence of sufficient blood pressure for typi- water loss than do insects in mesic environments, and cal excretory filtration, hexapods use osmotic pressure they are particularly good at water conservation and to achieve the same result. Various ions, especially po- producing insoluble nitrogenous waste products. They tassium, are actively transported across the Malpighian also have behavioral traits, such as nocturnal activity tubule epithelium from the blood into the tubule lumen cycles and dormancy periods that enhance water con- (Figure 22.37).The osmotic gradient maintained by this servation. Upper lethal temperatures for desert species ion transport mechanism enables water and solutes to commonly range to 50'C. The spiracles are often cov- move from the body cavity into the tubules, and thence ered by setae or depressed below the cuticular surface. into the gut. Water and other metabolically valuable Many xeric insects also undergo periods of dormancy materials are selectively reabsorbed into the blood (i.e., diapause or aestivation) during some stage of the across the wall of the hindgut, while the Malpighian fil- life cycle, characterized by a lowering of the basal met- trate left behind is mixed with the other gut contents. abolic rate and cessation of movement, which allow Reabsorption of water, amino acids, salts, and other nu- them to withstand prolonged periods of temperature trients may be enhanced by the action of special cells in and moisture extremes. Some even utilize evaporative thickened regions called rectal glands. The soluble po- cooling to reduce body temperatures. The long-chain tassium urate from the Malpighian tubules has, at this hydrocarbons that waterproof the epicuticle also are point in the gut, been precipitated out as solid uric acid more abundant in xeric insects. as a result of the low pH of the hindgut (pH 4-5). Uric acid crystals cannot be reabsorbed into the blood, hence Nervous System and Sense Organs they pass out the gut with the feces.Insects also possess The hexapod nervous system conforms to the basic ar- special cells called nephrocytes or pericardial cells that thropod plan described in Chapter 20 (Figures 22.32 move about in certain areas of the hemocoel, engulfing and22.33). The two ventral nerve cords, as well as the and digesting particulate or complex waste products. segmental ganglia, are often largely fused. In dipterans, The hexapod cuticle is sclerotized or tanned to vari- for example, even the three thoracic ganglia are fused ous degrees, adding a small measure of waterproof- into a single mass. The largest number of free ganglia ing. But more importantly, a waxy layer occurs with- occurs in the primitive wingless insects, which have as in the epicuticle, which greatly increases resistance many as eight unfused abdominal ganglia. Giant fibers to desiccation and frees insects to fully exploit dry have also been reported from several insect orders. PHYLUMARTHROPODA The Hexaooda:Insects and Their Kin 879

Segmental ganglia Optic Protocerebrum lobe (B)

Segmental Antennal nerve nerves Median ocellus Hypocerebral Opticlobe Deutocerebrum ganglion Figure22.32 (A)The insectcentral nervous system. Tritocerebrum (B)Frontolateral view of the brainof a locust(Orthoptera). Recurrent nerve Frontal Circumesophageal Labral connective Like the "brains" of other arthropods, the cerebral Frontal ganglion ganglia of insectscomprise three distinct regions: the protocerebrum, the deutocerebrum,and the tritocere- brum. The subesophagealganglion is composedof the fused ganglia of the fourth, fifth, and perhaps the sixth almost all directions. Compound eyes are greatly re- head segmentsand controls the mouthparts, salivary duced or absentin parasitic groups and in many cave- glands,and someother local musculature. dwelling forms. The general anatomy of the arthropod hrsectspossess a hypocerebralganglionbetween the compound eyewas describedin Chapter 20,but sever- cerebralganglion and the foregut. Associatedwith this al distinct structural trends are found in hexapod eyes, ganglion are two pairs of glandular bodies called the as we describebelow. corpora cardiacaand the corpora allata (Figure22.33). The number of ommatidia apparently determines Thesetwo organswork in concertwith the prothoracic the overall visual acuity of a compound eye; hence glands and certainneurosecretory cells in the protocer- large eyes are typically found on active, predatory ebrum. The whole complexis a major endocrinecenter insects such as dragonflies and damselflies (order that regulates growth, metamorphosis, and other func- Odonata), which may have over 10,000ommatidia in tions (seeChapter 20). eacheye. On the other hand, workers of some ant spe- Hexapods typically possesssimple ocelli in the lar- cieshave but a single ommatidium per eye (ants live in val, juvenile, and often adult stages.When present in a world of chemicalcommunication)! Similarly,larger adults, they usually form a triad or a pair on the an- facetscapture more light and are typical of nocturnal terodorsalsurface of the head.The compound eyesare insects.In all cases,a single ommatidium consists of well developed,resembling those of Crustaceil,and are two functional elements:an outer light-gathering part image-forming. Most adult insectshave a pair of com- composed of a lens and a crystalline cone, and an inner pound eyes (Figure 22.34),which bulge out to some sensorypart composedof a rhabdome and sensory extent, giving these animals a wide field of vision in cells(Figure 22.34).

Neurosecretorycells

Optic lobes

Protocerebrum

Aorta Antennal i..-cut Deutocerebrum Prothoracicgland

Tritocerebrum Prothoracic ganglion Figure 22.33 Endocrine organs Subesophageal and central nervous system in ganglion the head and thorax of a general- Lug ized insect. These organs all play roles in the control of moltino and metamorohosis. 880 Chapter Twenty-Two

Figure 22.34 Compound eyes Corneal lens facets of insects. (A) Close-up of the compound eyes of a tachinid fly Retinular (Diptera) with many ommatidia. cells (B) A generalized insect com- pound (cross (C) eye section). A Pigment single ommatidium from a eucone cells compound eye. Nerve fiber bundle

Basementmembrane

lens Corneagencell (primary pigment cell) Sempercells (crystalline cone cells) In some insects the outer surface of the cornea (lens) is covered with minute conical tubercles about 0.2 pm tall and arranged in a hexagonal pattern. It is thought that these projections decrease reflection from the sur- Secondary pigment cell face of the lens, thus increasing the proportion of light transmitted through the facet. Insect eyes in which the crystalline cone is present are called eucone eyes Retinular cell (Figure 22.348). Immediately behind the crystalline (sensorynerve cell) cone (in eucone eyes) are the elongate sensory neurons, Rhabdome or retinular cells. Primitively, each ommatidium prob- ably contained eight retinular cells arising from three successive divisions of a single cell. This number is Basementmembrane found in some insects today, but in most it is reduced Optic nerve axons to six or seven, with the other one or two persisting as short basal cells in the proximal region of each omma- tidium. Arising from each retinular cell is a neuronal axon that passes out through the basement membrane at the back of the eye into the optic lobe. There is no true optic nerve in insects; the eyes connect directly with are surroundedby 12 to 78 secondarypigment cells, the optic lobe of the brain. The rhabdomeres consist of which isolateeach ommatidium from its neighbors. tightly packed microvilli that are about 50 nm in diam- The generalbody surfaceof hexapods,like that of eter and hexagonal in cross section. The retinular cells other arthropods, bearsa greatvariety of microscopic

Processes of chemoreceptor cells

ticle

Epidermis

Protective cell cell bodies

Figure 22.35 Chemosensory peg organs. (A) SEM of a peg organ from an antenna of a beetle. (B) Diagram of a peg organ in cross section from the antenna of a grasshopper. PHYLUMARTHROPODA The Hexapoda:Insects and TheirKin 881

(c)

Tympanum

Tympanic membrane (= tympanum)

Figure 22.36 lnsect "ears." Insect auditory organs (phonorecep- tors) differ widely in their anatomy and location. (A) The "ear" of noctuid moths (Lepidoptera) is a pressure receiver used to detect the ultrasonic cries of hunting bats. lt is similar to most insect "ears" in comprising a tympanic membrane backed by a tracheal air . space. Two receptor cells attach to the tympanum. (B) ln Drosophila (Diptera), a feathery seta called an arista arises on the third anten- nal segment. The arista detects air movements, thus responding to sound through interaction with vibrating air particles. lt is used to detect the calling song of the species. (C) In the "ear" of a water boatman (Hemiptera), the tympanum is covered by the base of a club-shaped cuticular body that protrudes outside the body. The club performs rocking movements that allow some frequency analysis of the songs of other water boatmen. (D) Tympani (arrows) on the tibiae of katydid forelegs.

sensory hairs and setae, known collectively as sensil- (generally above the range of human ears), will fold la (sing., sensillum). The incredible diversity of these their wings and suddeniy drop groundward as Erneva- cuticular surface structures has only begun to be ex- sive maneuver. Praying mantises/ whose sonar detec- plored, primarily by scanning electron microscopy. tion device is buried in a groove on the ventral side of Sensilla are most heavily concentrated on the antennae, the abdomen, throw out the raptorial forelimbs and el- mouthparts, and legs. Most appear to be tactile or che- evate the abdomen. These movements cause the insect mosensory. Club-shaped or peg-shaped chemosensory to "stall" and go into a steep roll, which it pulls out of setae, usually called peg organs and resembling the at the last minute with a "power dive" that effectively aesthetascsof crustaceans, are particularly common on avoids bat predators. the antennae of hexapods (Figure 22.35). Sound communication in insects, like light commu- Insects have internal proprioceptors called chor- nication in fireflies (and some ostracods), is a species- dotonal organs. These structures stretch across joints specific means of mate communication. Several insect and monitor the movement and position of various groups (e.g., some orthopterans, coleopterans, dipter- body parts. Phonoreceptors also occur in most insect ans, and hemipterans) possess sound-producing struc- orders. These structures may be simple modified body tures. Male flies of the genus Drosophila create species- or appendage setae/or antennae, or complex strucfures specific mating songs by rapidly vibrating the wings called tympanic organs (Figure 22.36). Tympanic or- or abdomen. These "love songs" attract conspecific fe- gans generally develop from the fusion of parts of a males for copulation. It has been demonstrated that the tracheal dilation and the body wall, which form a thin rhythm of the male's song is encoded in genes inher- tympanic membrane (= tympanum). Receptor cells in ited from his mother, on the X chromosome, whereas an underlying air sac, or attached directly to the tym- the song's "pulse interval" is controlled by genes on panic membrane, respond to vibrations in much the autosomal chromosomes. same fashion as they do in the cochlea of the human Cicadas may possess the most complex sound-pro- inner ear. Many insects can discriminate among dif- ducing organs in the animal kingdom (Figure 22.37). ferent sound frequencies, but others may be tone-deaf. The ventral metathoracic region of male cicadas bears Tympanic organs may occur on the abdomen, the two large plates, or opercula, that cover a complex sys- thorax, or the forelegs. Several insects that are prey tem of vibratory membranes and resonating chambers. to bats have the ability to hear the high frequencies of One membrane, the tymbal, is set vibrating by special bat echolocation devices, and they have evolved flight muscles, and other membranes in the resonating cham- behaviors to avoid these flying mammals. For exam- bers amplify its vibrations. The sound leaves the cica- ple, some moths, when they hear a bat's echolocation da's body through the metathoracic spiracle. 882 ChaoterTwentv-Two Tergum Viscera Rim of tymbal Tymbal cover Tymbal Figure 22.37 Sound production structure in Air sacs cicadas (Hemiptera) from the first abdominal seg- Apodeme(strut) ment (section). is produced by buckling Sound Tymbal muscle of the tymbal, a thin disc of cuticle. The tymbal muscle is connected to the tymbal by a strut. Rim of tymbal Contraction of this muscle causes the tymbal to Tensor muscle buckle inward, thereby producing a click that is amplified by resonanie in th6 underlying air sacs. Air sac On relaxation, the elasticity of the muscle causes um the tymbal to buckle out again. On the underside of this abdominal segment, a folded membrane can membrane be stretched to tune the air sacs to the resonant frequency of the tymbal.

Numerous families of beetles and bugs utilize water feeding ground. The foragerbee also carries food odors surfaces as a substratum both for locomotion and for (nectar samples), pollen, and various other odors cling- communication by waves or ripples. Such insects pro- ing to the hairs on her body. She can also mark the food duce a signal with simultaneous vertical oscillations source with a pheromone produced in a special gland, of one or more pairs of legs, and sometimes also with called the Nasanov gland. All of these clues help her distinct vertical body motions. The wave pattems pro- hive-mates find the new food source. Karl von Frisch duced are species-specific. Potential prey trapped on a was the first person to document all these attributes of surface film may also be recognized in this fashiorg just bee foraging early in the twentieth century. as spiders recognize prey by web vibrations. Limited A large body of research on bee navigation has ac- data suggest that the receptor organs for ripple com- cumulated since the pioneering "dancing bee stud- munication are either specialized sensilla on the legs ies" of von Frisch. We now know that honeybees (and or special proprioceptors between joints of the legs or solitary bees) have outstanding vision. Much of the antennae, perhaps similar to the tarsal organs of scor- bee's daily activity, including navigation and flower pions (Chapter24). recognition, relies strongly on ultraviolet vision. Bees A number of insects are bioluminescent, the most fa- appear to utilize a hierarchical series of flight orienta- miliar being beetles of the family Lampyridae, known tion mechanisms; when the primary mechanism is as lightning bugs or fireflies. In the tropics, where they blocked, a bee can switch to a secondary system. The are especially abundant, fireflies are sometimes kept in primary navigation system utilizes the pattern of po- containers and used as natural flashlights, and women larized ultraviolet sunlight in the sky. This pattern may wrap them in gauzebags worn as glowing hair or- depends on the location of the sun as determined by naments. The light of luminescent insects ranges from two coordinates, the azimuth and the elevation. Bees green through red and orange, depending on the spe- and many other animals that orient to the sun have a cies and the precise chemical nature of the luciferin-lu- built-in ability to compensate for both hourly changes ciferase system involved. Light-producing organs are (elevation) and seasonal changes (azimuth) in the sun's typically composed of clusters of light-producing cells, position with time. On cloudy days, when the sun's or photocytes, backed by alayer of reflecting cells and light is largely depolarized, bees cannot rely on their covered with a thin, transparent epidermis. The photo- ultraviolet celestial navigation mechanism and thus cytes are richly supplied with tracheae, oxygen being may switch to their second-order navigational system: necessary for the chemical reaction. Each species of navigation by landmarks (foliage, rocks, and so on) hrefly, and of most other glowing insects, has a distinct thatwere imprinted during the most recentflight to the flash pattem, or code, to facilitate mate recognition and food source. Limited evidence suggests that some form communication. of tertiary backup system may also exist. One of the most sophisticated communication be- Thus, if the honeybee dance model is correct,T hon- haviors among insects may be the famous honeybee eybees must simultaneously process information "waggle dance." Each day forager bees leave their concerning time, the direction of flight relative to the colony to locate new food sources (e.9., fresh flower sun's azimuth, the movement of the sun, the distance blooms). They fly meandering search forays until a flown, and local landmarks (not to mention complica- good source is located. Then they return to the hive tions due to other factors, such as crosswinds), and in along a straight flight path (a "bee line"); while doing doing so reconstruct a straightJine heading to inform so, they are thought to imprint a navigational"rnap" from the colony to the food source. Most behavior- TThe ists believe that this information is communicated to honeybee dance hypothesis is not without its detractors, and some workers doubt its existence altogether; see the General hive-mates in a complex tail-wagging dance that al- References section of this chapter for a glimpse at the history of lows other bees from the hive to flv directlv to the new the honeybee dance controversy. PHYLUMARTHROPODA The Hexapoda:Insects and TheirKin 883

their hive-mates. If recent evidence is correct, bees (like tubular ovarioles (Figure 2238A). The oviducts unite homing pigeons) may also detect Earth's magnetic as a common duct before entering a genital chamber. fields with iron compounds (magnetite) located in their Seminal receptacles (spermathecae) and accessory abdomens. Bands of cells in each abdominal segment glands also empty into the genital chamber. The genital of the honeybee contain iron-rich granules, and nerve chamber opens, via a short copulatory bursa (= y6gi- branches from each segmental ganglion appear to in- na)/ on the sternum of the eighth, or occasionally the nervate these tissu'es.8 seventh or ninth, abdominal segment. The male repro- In some insects the ocelli are the principal naviga- ductive system is similar, with a pair of testes, each tion receptors. Some locusts and dragonflies and at formed by a number of sperm tubes (Figure 22.388). least one ant species utilize the ocelli to read compass Paired sperm ducts dilate into seminal vesicles (where information from the blue skv. As in bees, the pattern sperm are stored) and then unite as a single ejaculatory of polarized light in the sky r""-t to be the .orn- duct. Near this duct, accessory glands discharge semi- pass cue. In some species,both ocelli and compound-uirl nal fluids into the reproductive tract. The lower end of eyes may function in this fashion. Many (probably the ejaculatory duct is housed within a penis, which most) insects also see ultraviolet light. extends posteroventrally from the ninth abdominal Perhaps the most famous insect navigators are sternite. North America's monarch butterflies (Dannus plexip- Courtship behaviors in insects are extremely di- pus).Each autumn, monarchs migrate up to 4,000 km verse and often quite elaborate, and each species has from breeding grounds in the eastern United States its own recognition methods. Courtship may consist of and Canada to over-wintering sites in the mountains simple chemical or visual attractiory but more typically of Michoacdn, in central Mexico. They make this re- it involves pheromone release, followed by a variety markable journey by orienting with a Sun compass, of displays, tactile stimulation, songs, flashing lights, using the Sun's changing azimuth (and knowledge or other rituals that may last for hours. The subject of of the relative time of day) to direct their movements. insect courtship is a large and fascinating study of its On cloudy days, when a precise solar azimuth is un- own. Although the field of pheromone biology is still obtainable, monarchs still manage to orient towards in its infancy, sexual attractant or aggregation phero- the south-southwest, suggesting that they also have a mones have been identified from about 500 different backup mechanism of orientation, such as a geomag- insect species (about half of which are synthesized and netic compass. Monarchs are one of a small group of sold commercially for pest control purposes). animal species for which a sun compass orientation Most insects transfer sperm directly as the male in- mechanism has been shown to exist. serts either his aedeagus (Figure 22.388,D) or a gono- Many insects release noxious quinone compounds pod into the genital chamber of the female. Special to repel attacks. Perhaps best known in this regard are abdominal claspers, or other articulated cuticular certain Tenebrionidae, many of which stand on their structures on the male, often augment his copulatory heads to do so. But the champions of this chemical grip. Such morphological modifications are species warfare strategy are definitely the bombardier beetles, specific and thus serve as valuable recognition char- members of the carabid subfamilies Brachininae and acters, both for insect mates and insect taxonomists. Paussinae, which expel quinone compounds at tem- Copulation often takes place in mid-flight. In some of peratures reaching 100"C (Figur e 22.7C). the primitive wingless insects, and in the odonatans, sperm transfer is indirect. In these cases, a male may Reproduction and Development deposit his sperm on specialized regions of his body to Reproduction Hexapods are dioecious, and most are be picked up by the female; or he may simply leave the oviparous. A few insects are ovoviviparous, and many sperm on the ground, where they are found and taken can reproduce parthenogenetically. Most insects rely up by females. In bedbugs (order Hemiptera, family on direct copulation and insemination. Reproductively Cimicidae) males use the swollen penis to pierce a spe- mature insects are termed adults or imagos. Female cial region of the female's body wall; sperm are then imagos have one pair of ovaries, formed of clusters of deposited directly into an internal organ (the organ of Berlese). From there they migrate to the ovaries, where 6Many fertilization takes place as eggs are released. animals possess magnetotactic capabilities, including some molluscs, hornets, salmon, tuna, turtles, salamanders, homing Sperm may be suspended in an accessory gland pigeons, cetaceans, and even bacteria and humans. Magnetotactic secretion, or, more commonly/ the secretion hard- bacteria swim to the north in the Northern Hemisphere, to the ens around the sperm to produce a spermatophore. south in the Southern Hemisphere, and in both diiections at the geomagnetic equator. In all these cases, iron oxide crystals in Females of many insect species store large quantities of the form of magnetite have been shown to underlie the primary sperm within the spermathecae. In some cases sperm detection devices. However, in honeybees, the iron-contiining- from a single mating is sufficient to fertilize a female's structures are trophocytes that contain paramagnetic magnetite. These magnetotactic trophocytes surround each abdominal seg- eggs for her entire reproductive lifetime, which may ment and are innervated by the central nervous system. last a few days to several years. Sperm tubes 884 Chapter Twenty-Two rian ligament Testis Ovarioles Figure 22.38 Insect reproductive Sperm duct systems. (A)Female system. (B) Male (=vas deferens) system.(C) The posteriorend of the abdomenof a maturefemale insect. (D)The posteriorend of the abdomen Accessory of a maturemale insect glands

Lateral Spermathecal (c) Seminal oviduct gland Tergum vesicle Calyx Spermathecae Common Ejaculatory duct oviduct

Aedeagus Accessorygland Genital chamber Copulatory bursa Gonopore

species, Wolbachiainfections eliminate males altogether Gonopore by disrupting the first cell division of the egg, resulting in diploid eggs that can develop only as females-thus (D) Cercus creating parthenogenetic strains of normally sexual wasps. Such asexual strains of wasps will revert back Accessoryglanc Anus to dioecy if the Wolbachiadies out.' Sperm duct Aedeagus (=vas deferens) Embryology As discussed in Chapter 20, the large centrolecithal eggs of arthropods are often very yolky, a condition resulting in modifications of the cleavage pat- Ejaculatory duct tern. Although vestiges of what have been interpreted as holoblastic spiral cleavage are still discemible in some crustaceans,the hexapods show almost no trace of spiral Insect eggs are protected by a thick membrane (the cleavage at all. Instead, most undergo meroblastic cleav- chorion) produced within the ovary. Fertilization oc- age by way of intralecithal nuclear divisions, followed curs as the eggs pass through the oviduct to be depos- by migration of the daughter nuclei to the peripheral ited. Accessory glands contribute adhesives or secre- cytoplasm (= periplasm). Cytokinesis does not occur tions that harden over the zygotes. In many species, during these early nuclear divisions (up to 13 cycles), cuticular extensions around the gonopore of the female which thus generate a slmcytium, or plasmodial phase form an ovipositor (Figure 22.38C), with which she of embryogenesis. The nuclei continue to divide until places the eggs in a brooding site that will afford suit- the periplasm is dense with nuclei, whereupon a syncy- able conditions for the young once they hatch (such as tial blastoderm exists. Eventually, cell membranes begin in a shallow underground chamber, in a plant stem, or to form, partitioning uninucleate cells from one another. within the body of a host insect). Although 50-100 eggs At this point the embryo is a periblastula, comprising a are usually laid at a time, as few as one and as many as yolky sphere containing a few scattered nuclei and cov- several thousand are deposited by some species. Some ered by a thin cellular layer (Figure 22.39). insects, such as cockroaches/enclose several eggs at a Along one side of the blastula a patch of columnar time in a protective egg case. cells forms a germinal disc, sharply marked off from Parthenogenesis is common in a variety of insect the thin cuboidal cells of the remaining blastoderm groups. It is used as an alternative form of reproduc- (Figure 22.39A). From specific regions of this disc, pre- tion seasonally by a number of insect taxa, particu- sumptive endodermal and mesodermal cells begin to larly those living in unstable environments. In the proliferate as germinal centers. These cells migrate in- Hymenoptera (bees,wasps, ants), it is also used as a ward during gastrulation to lie beneath their parental mechanism for sex determination. In these cases, dip- cells, which now form the ectoderm. The mesoderm loid fertilized eggs become females, and haploid un- proliferates inward as a longitudinal gastral groove fertilized eggs develop into males. Infections by the bacterium Wolbachia,a frequent parasite of arthropod reproductive systems, are known to affect reproduc- vW olbachiapipientis are maternally transmitted, gram-negative, tion in many insect species.In some cases,infections obligate intracellular bacteria found in filariai nematodes, crus- taceans, arachnids, and at ieast 20% of ail insect species. Many result in infertility, whereas in others they transform Wolbachin increase their prevalence in populations by manipulat- males into functional females. But in some wasp ing host reproductive systems. PHYLUMARTHROPODA The Hexapoda:Insects and Their Kin 885

Figure 22.39 Early stages of insect development. (A) The blastoderm (blas- tula) of a generalized insect, subsequent to cytokinesis (cross section). Note the thickened germinal disc. (B) An early gastrula of a honeybee (cross section). Note the gastral groove and the prolif- eration of mesoderm.

Mesoderm

Germinal disc

(Figure 22.398). The cells of the developing gut usually Polyembryony occursin a number of insect taxa, par- surround and gradually begin absorbing the central ticularly parasiticHymenoptera. In this form of devel- yolky mass of the embryo, and paired coelomic spaces opment the early embryo splits to give rise to more than appear in the mesoderm. one developing embryo. Thus, from two to thousandsof As segments begin to demarcate and proliferate, larvae may result from a single fertilized egg,which is each receives one pair of mesodermal pouches and often depositedin the body of another(host) insect. eventually develops appendage buds. As the meso- derm contributes to various organs and tissues, the Post-embryonic development Within Hexapoda paired coelomic spaces merge with the small blastocoel there are three main types of development: ametabo- to produce the hemocoelic space. The mouth and anus lous (direct, or u*orphic develophent), hemime- arise by ingrowths of the ectoderm that form the proc- tabolous, and holometabolous (indirect, or complete todeal foregut and hindgut, which eventually establish development).Figure 22.40 depicts these development contact with the developing endodermal midgut. types. Speciesin the most primitive wingless hexapod

(A) (B) (C) n Figure 22.4O Side- by-side comparison o @ J * of the three main I types of development N + 4:-- y,p,\n Hq=o"SR found in hexapods.(A) "6W,"-' Y Ametabolousdevelop- IJ'frW Y ment, (B) hemimetabo- I Xi& lous development,and (c) holometabolous rV I $,ffi" N\\ ' n^ develoPment' W tW

,t Wba' + cW/@- ] ^q $'ffi"ffi I E Psqg rt YJ,M ffit Wl\\ (WW@-- +^^ + / \- zG" | ffi + {,ilffil J n"p" '"-*-----tt hw F*- Y W .t tI \k4l ,rffi (i lt\ ffie4 () 886 ChapterTwentY-Two

Compound eye

Pronotum Forewing Mesonotum Pad Metanotum

Abdomen ------>

Second instar Third instar

Metanotum Forewing

Hindwing pads

Figure22.41 lllustrationsand photo of the life stages of milkweed bugs (Hemiptera),illustrating the main life stages of hemimetabolousdevelopment. Note the wing oads in instars3-5.

However functional wings and sexual structures are always lacking, although juveniles have wing rudi- ments called wing pads or wing buds, and the wings themselves become exposed for the first time during the preadult molt. Holometabolous insects hatch as vermiform lar- vae that bear no resemblance whatsoever to the adult forms. These larvae are so different from adults that they are often given separate vernacular names; for example/ butterfly larvae are called caterpillars, fly lar- vae maggots, andbeetle larvae grubs. Holometabolous larvae lack compound eyes (and often antennae), and orders undergo ametabolousdevelopment. The young their natural history differs markedly from that of hatch out as juveniles closely resemblingthe adult, or adults. Their mouthparts may be wholly unlike those imago, condition but the overall body size increases of adults, and external wing buds are never present. with each successivemolt. Winged insectsundergo Often the greater part of a holometabolous insect's either hemimetabolous development (Figures 22.408 lifetime is spent in a series of larval instars. Larvae and 22.41)or holometabolous develoPment (Figures typically consume vast quantities of food and attain a 22.40Cand22.42). larger size than adults. Termination of the larval stage In hemimetabolousdevelopment, principal changes is accompanied by pupation, during which (in a single during growth are in body sizeand proportions and in molt) the pupal stage is entered (Figure 22.43). Pupae the development of wings and sexual structures.The do not feed or move about very much. They often re- juveniles of hemimetabolousinsects are callednymphs side in protective niches in the ground, within plant (terrestrial juveniles) or naiads (aquatic juveniles, tissues, or housed in a cocoon. Energy reserves stored such as mayflies, dragonflies,damselflies)' Nymphs during the long larval life are utilized by the pupa to and adults often live in the same general habitat; na- undergo whole scale body transformation. Many lar- iads and their respective adults do not. Nymphs and val tissues are broken down and reorganized to attain naiads possesscompound eyes,antennae, and feeding the adult form; external wings and sexual organs are and walking appendagessirnilar to thoseof the adults' formed. The remarkable transformation from larval PHYLUMARTHROPODA The Hexapoda:Insects and TheirKin 887

Dorsal process Figure 22.42 Life stages of a butterfly Lateral Head (Lepidoptera), illustrating the main life ocelli stages of holometabolous development.

Mouthparts Thoracic^legs Anal proleg Hexapod Evolution Larva The hexapods were among the first animals to + colonize and exploit terrestrial and freshwater eco- Legs systems. The fossil record is good, with about 1,263 recognized families (by comparison, there are 825 Proboscis recognized fossil families of tetrapod vertebrates). Antenna The oldest known fossil insects are from the Early Line of weakness Devonian, which has led to the hypothesis that hexapods originated in the late Silurian with Wing the earliest terrestrial Abdomen ecosystems. The remarkable di- versification of insects is undoubtedly related to the evolution of wings, and insects are the only group of invertebrates with the ability to fly. Fossil Pupa winged insects exist from the Late Mississippian (-324Ma), which suggests a pre-Carboniferous I Forewing origin of insect flight. However, the description of Rhyniognntha (-412Ma) from a mandible, po- tentially indicative of a winged insect, suggests a Antenna late Silurian to Early Devonian origin of winged Compound eye insects. Divergence time estimates based on a mo- lecular phylogenetic analysis of many nuclear, Head protein-coding genes (Misof et aL.2014)corrobo- Thorax rate an origin of winged insect lineages during this Abdomen time period, which implies that the ability to fly Hindwing emerged after the establishment of complex terres- trial ecosystems. Since then, insects have shaped Earth's terrestrial ecosystems, coevolving with an- other hyperdiverse terrestrial group, the flowering stage to adult stage in holometabolous insects is one of plants, ultimately qualifying the Cenozoic to be called the most impressive achievements of animal evolution "the age of insects." (Figure 22.42), and it is on par with the transformation By the Carboniferous, various modem insect orders of crustaceans through a series of larval stages to adult- were flourishing, although many were quite unlike to- hood (Figure21.33). day's fauna. Some Carboniferous hexapods are notable The role of ecdysone in initiating molting is de- for their gigantic size, such as silverfish (Thysanura) scribed in Chapter 20. This hormone works in conjunc- that reached 6 cm in length and dragonflies with wing- tion with a second endocrine product in controlling the spans of about 70 cm. In addition to the living orders sequence of events in insect metamorphosis. This sec- of insects, at least ten other orders arose and radiated ond product, juvenile hormone, is manufactured and in late Paleozoic and early Mesozoic times, then went released by the corpora aITata,apair of glandlike struc- extinct. tures associated with the brain (Figure22.33). When ec- The Permian saw an explosive radiation of holome- dysone initiates a molt in an early larval instar, the ac- tabolous insects, although many groups went extinct companying concentration of juvenile hormone in the in the great end-Permian extinction event (Chapter 1). hemolymph is high. A high concentration of juvenile In fact, relatively few groups of Paleozoic insects sur- hormone ensures a larva-to-larva molt. After the last vived into the Mesozoic, and many recent families first - Iarval instar is reached, the corpora allata ceasesto se- appeared in the jurassic. By the Cretaceous, most mod- crete juvenile hormone. Low concentrations of juvenile ern families were extant, insect sociality had evolved, hormone result in a larva-to-pupa molt. Finally, when and many insect families had begun their intimate re- the pupa is ready to molt, juvenile hormone is absent lationships with angiosperms. Tertiary insects were es- from the hemolymph altogether; this deficiency leads sentially modern and included many genera indistin- to a pupa-to-adult molt. guishable from the Recent (Holocene) fauna. 888 Chapter Twenty-Two

Figure 22.43 Four different types of insect pupae. (A) Chrysalis of a monarch butterfly (Lepidoptera: Nymphalidae'. Danaus plexip- pus). (B) Pupa of a longhorn beetle (Coleoptera: Cerambycidae: Xylotrechus nauticus). (C) Cocoon of a silkworm moth (Lepidoptera: Saturniidae: Bombyx mon) sliced open to reveal the pupa inside. The shed skin (exuviae) of the final larval instar is visible to the right of the pupa inside the cocoon. (D) Pupa of a mosquito (Diptera:Culicidae).

Our current view of the evolutionary relationships wa11).In addition, the Malpighian tubules and com- of hexapod orders is presentedin Figure 22.44.This pound eyesare reduced--compound eyesare degener- tree is basedon a recentpublication (Misof et aI.20L4) ate in Collembolaand absentin the extant Diplura and presenting a molecular phylogenetic analysisof 1.,478 Protura. However. thesereductions could be conver- single-copynuclear, protein-coding genes (see Chapter gencesresulting from small body size.Our evolution- 2 for detailed treewith divergencetime estimates.)This ary tree thus depicts an unresolved trichotomy at the is by far the most data rich analysisof the hexapods baseof the Hexapoda, and we treat the entognathous conducted to date. The results of this analysissupport hexapods as a potentially paraphyletic group in our many of the long held views of hexapod evolution but classification. also provide novel support for some parts of the tree The monophyly of the Insecta (Archaeognatha, that had been difficult to resolvebased on smallermo- Thysanura,and Pterygota)(Figure 22.448)is undis- lecular setsand by analysesof morphological charac- puted. The principal synapomorphiesof this group ters alone. include the structure of the antenna, with its lack of The hexapods are divided between three entogna- musclesbeyond the first segment (scape);the pres- thous orders and the Insecta.The three entognathous enceof a group of special chordotonal organs (vibra- orders (the Collembola,Protura, and Diplura) all tion sensors)in the secondantennal segment(pedicel) have internalized mouthparts. Most current workers called the Johnston's organ; a well developed poste- regard the Collembola + Protura to be a monophy- rior tentorium (forming a transversebar); subdivision letic group (called the Ellipura), and this relationship of the tarsus into tarsomeres;females with ovipositor is strongly supported by the most recent analyses. formed by gonapophyses(limb-base endites) on seg- Flowever, whether the Diplura are more closely re- ments 8 and9; and long, annulated,posterior terminal lated to the Collembola + Protura, or to the Insecta(a filaments (cerci). view persuasivelyargued by Kukalov6-Peck)remains The Insectahave traditionally been divided into hot$ debatedand unresolved.Thus, the entognathous the wingless insects (Archaeognathaand Thysanura) hexapodsmay or may not form a monophyletic group. and the winged insects (Pterygota).Flowever, on the Among the potential synapomorphiesthat may unite basis of molecular studies and the presenceof a di- all three orders is entognathyitself (the overgrowth of condylic mandible, the Thysanura (silverfish) are the mouthparts by oral folds from the lateral cranial now thought to be the sister group of the Pterygota. pHyLUM ARTHROPODA The Hexapoda:lnsects and Their Kin 889

) "C.rrrtac"u" )

Collembola

Protura

Diplura Archaeognatha Thysanura Ephemeroptera Odonata Dermaptera Zoraplera Plecoptera Orthoptera g Blattodea fi I Mantodea "g

Phasmida *r

Embioptera !,

Grylloblattodea A) Mantophasmatodea @ - t) ) Thysanoptera o IP q l3 z Hemiptera 6 lp Psocodea )e o Hymenoptera x

Coleoptera* Strepsiptera Neuroptera |'r Raphidioptera

Megaloptera o Lepidoptera * Trichoptera

Diptera * Mecoptera Siphonaptera

the evolution of dicondylic mandibles (an apomorphy of Figure 22.44 Phylogeny of the 31 orders of Hexapoda' the Dicondylia) (D) the evolution of wings (an apomorprhy Major clades are indicated to the right of the tree' The of Pterygota); (E) the evolution of wing folding (an apo- most recent common ancestor of extant taxa with traits morphy of Neoptera); (F) the evolution of holometabolous that led to the success of the Hexapods are denoted with development (= indirect development, or complete meta- circled letters to the left of the tree. These key innovations morphosis; an apomorphy of the Holometabola)' The most include: (A) arthropod body subdivided into three tagmata: diverse insect orders, commonly known as the "big four," the head, 3-segmented thorax with one pair of uniramous with asterisks. Crustacea, a paraphyletic each segment, and an 11-segmented abdomen are denoted legs on is shown at (B) evolution of exter- group due to its exclusion of the Hexapoda, lsynapomorphies of Hexapoda); the (C) the base of the tree. nal mouthparts (an apomorphy of the class lnsecta);

once in Hexapoda along the branch leading to They are classified together in a lineage known as the only (Figure 22.44D). However, the Pterygota Dicondylia (seeFigure 22.44C). the Pterygota Palaeoptera and Neoptera, with The Fterygota are,of course,distinguished by the compdse two groups, wing types. The Palaeoptera presenceoiwings on the mesothoraxand metathorax fundamentally different include the Odonata (dragonflies of udnltt. Thereis wide agreementthat wings evolved ("ancient wings") 890 ChaoterTwentv-Two and damselflies) and Ephemeroptera (mayflies), which characters, the monophyly of this group is likely (but are characterizedby many-veined, netlike wings that controversial), since Misof et al. (2014) found evi- cannot be folded over the back. It is still unclear wheth- dence that the Psocodea may be the sister group to er or not the two palaeopterous orders, Ephemeroptera Holometabola. Although this relationship appears to and Odonata, form a monophyletic group and they be well-supported by their analyses (see Figure 2.6) are therefore depicled in a trichotomy with Neoptera with high bootstrap support values, this measure of in our summary trbe (Fig'ure 22.44D). The Neoptera statistical support is of controversial utility for such ("modern wings") have reduced wing venation, but large molecular data sets. more importantly, they can rotate their wing joint and The monophyly of the Holometabola is well es- fold back their wings when they are not flying (Figure tablished. The eleven orders placed together in the 22.44E). This is one of the most important evolutionary Holometabola are united on the basis of holometabo- innovations in hexapods. Wing folding allows insects lous development (Figure 22.44F). The eminent suc- to protect their fragile wings, especially from abrasion, cess of the holometabolous lifestyle is demonstrated thereby allowing them to live in tight spaces such as by the fact that their species outnumber hemimetabo- crevices under bark, under rocks, in burrows, nests, lous species ten to one. The most species rich insect and tunnels. orders (Hymenoptera, Coleoptera, Lepidoptera, and The Neoptera is divided into three broad groups: Diptera), commonly known as the "bigfour" all un- Polyneoptera (10 orders); Acercaria, or Paraneoptera (3 dergo complete metamorphosis. There is a popular orders); and the Holometabola, or Endopterygota (11 theory among evolutionary biologists that views in- orders). Polyneopterans are a morphologically diverse direct development, including holometabolous de- group of insects with biting-chewing mouthparts and velopment in insects, as selectively advantageous be- hemimetabolous development. The phylogenetic re- cause it results in the ecological segregation of adults lationships among the orders within Polyneoptera, from young, thus avoiding intraspecific competition and the monophyly of the group itself have long been and allowing each stage to develop its own suite of controversial. However, recent phylogenomic work re- specific survival strategies. We have seen that such covered strong support that the polyneopteran orders transformations in development are common in ma- form a monophyletic group. rine and some freshwater invertebrates, but only the The Acercaria includes the Thysanoptera, Hemi- insects have managed to exploit this strategy so suc- ptera, and the Psocodea.Supported by many derived cessfully on land.

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