Order Hemiptera

Chapter 37

Order Hemiptera David A. Lytle Department of Integrative Biology, Oregon State University, Corvallis, OR, USA

Chapter Outline Introduction951 Distribution, Diversity, and Phylogenetic Relationships951 General Biology 953 External Anatomy 953 Locomotion953 Aquatic Locomotion 953 Flight955 Physiology956 Respiration956 Physiological Traits as Predators 956 Osmoregulation956

INTRODUCTION The insect order Hemiptera is a group that evolved terrestrially and invaded aquatic habitats secondarily. Respiration, mating behavior, and general physiology are therefore built on a terrestrial ground plan and secondarily adapted to aquatic life. The aquatic Hemiptera are composed of semi-aquatic bugs (Gerromorpha) that live primarily on the water’s surface and aquatic bugs (Nepomorpha) that live submerged beneath the water, along with several other mostly terrestrial groups that live near aquatic habitats. Nearly all aquatic Hemiptera species depend on atmospheric air for respiration, and most taxa can walk or fly in the terrestrial environment as adults. Aquatic Hemiptera occupy a diverse array of habitats, ranging from stable spring-fed systems to temporary rain pools. Several lineages have invaded near-shore and open water marine habitats. Most aquatic Hemiptera are predatory, using a piercing rostrum to subdue and feed on invertebrates, as well as fish and frogs in some cases. The aquatic Hemiptera contain a number of superlatives, including the largest aquatic insect (Lethocerus maximus), which can exceed 11 cm in length. The group also exhibits a diverse array of

Life Cycle and Reproduction 956 Life Cycle 956 Reproduction957 Ecology and Behavior 957 Feeding957 Mating958 Body Size and Evolution of Paternal Care 958 Flood Survival 959 Importance to Humans 959 Conservation of Hemiptera 960 Collecting, Culturing, and Preparing Specimens 960 References961

mating behaviors, including rare examples of male parental care (Figure 37.1) and the elaboration of unusual morphologies owing to sexual conflict.

Distribution, Diversity, and Phylogenetic Relationships Aquatic Hemiptera occur in the suborder Heteroptera, which represents the most successful radiation of non-­ holometabolous insects with over 40,000 known species (Weirauch and Schuh, 2011). Heteroptera, or “true bugs,” are united by the presence of metathoracic glands in adults, dorsal abdominal glands in immatures, and a labium inserted anteriorly on the head (Carver et al., 1991; Wheeler et al., 1993). The presence of a hemelytron, the subdivision of the forewing into a proximal coriaceous and distal membranous region, is also typical of the group but is derived within the Heteroptera ­(Andersen and Weir, 2004). Although some Homoptera may be viewed as associating with aquatic habitats (Polhemus, 2008), they possess no true adaptations to aquatic life and are not treated here. “Aquatic Hemiptera” is therefore synonymous with “aquatic Heteroptera.” Aquatic and semiaquatic species

Thorp and Covich’s Freshwater Invertebrates. http://dx.doi.org/10.1016/B978-0-12-385026-3.00037-1 Copyright © 2015 Elsevier Inc. All rights reserved.

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FIGURE 37.1  A male giant water bug Abedus herberti (Belostomatidae) brooding eggs on its back. The eggs will be kept partially submerged near the water’s surface until they hatch. Photograph courtesy of Ivan Phillipsen.

are restricted to three of the seven Heteroptera infraorders: Gerromorpha, Nepomorpha, and Leptopodomorpha ­(Figure 37.2). Whereas placement of these infraorders within Heteroptera differs among authors (Andersen, 1982; Mahner, 1993; Wheeler et al., 1993; Xie et al.,

SECTION | VI  Phylum Arthropoda

2008), monophyly of each suborder is generally well supported. Gerromorpha, or semiaquatic bugs, consist of eight families that reside primarily on the water’s surface. These families include Gerridae (waterstriders), Veliidae (riffle bugs), Mesoveliidae (water treaders), and Hydrometridae (water measurers), all of which skate or walk on the surface of freshwater habitats. The coral treaders, family Hermatobatidae, are a small group of marine species associated with Indo-Pacific coral reefs. The remaining three families, Hebridae, Macroveliidae, and ­Paraphrynoveliidae, are found on shorelines. Nepomorpha, or aquatic bugs, are represented by 11 families that live in or near water. These families range from active ­swimmers such as the Corixidae (water boatman), Notonectidae (backswimmers), and Naucoridae (creeping water bugs) to more sedentary predators such as the Belostomatidae (giant water bugs) and Nepidae (water scorpions). Pleidae (pygmy backswimmers) and the related Helotrephidae are small, convex bugs found in slower waters. Two families, the Gelastocoridae (toad bugs) and Ochteridae (velvety shore bugs), inhabit the land–water transitional zone. The naucorid-like Aphelocheiridae inhabit lakes and streams, and little is known about the small (eight species in two

FIGURE 37.2  Diversity of form in the aquatic Hemiptera (not drawn to scale). Top row, left to right—Nepomorpha: Nepidae (Ranatra), Belostomatidae (Lethocerus), Gelastocoridae (Nerthra), and Corixidae (Hesperocorixa). Bottom row, left to right—Gerromorpha: Hydrometridae (Hydrometra) and Gerridae (Aquarius); Leptopodomorpha: Saldidae (Micracanthia). Line drawings by Arthur Smith, British Museum (Natural History), in Usinger (1956).

Chapter | 37  Order Hemiptera

genera) related group Potamocoridae. Finally, Leptopodomorpha encompass just four families, two inhabiting shorelines (Saldidae and Leptopodidae) and two occupying the marine intertidal (Omaniidae and Aepophilidae). Aquatic Hemiptera are nearly global in extent, with taxa occupying all continents except Antarctica. Polhemus and Polhemus (2008) reviewed the global diversity of aquatic Hemiptera and tallied 23 families, 343 genera, and over 4811 valid species. The inclusion of several minor marine groups brings the species count to 4820 (Table 37.1). About 97% of this diversity is associated with freshwater habitats, with the remainder occupying the marine intertidal or pelagic zone. Although the North American, European, and Australian faunas have been reasonably well-described, portions of Africa, the Malay Archipelago, interior Indochina, the southeastern margin of the Himalayan plateau, and the Atlantic coastal rainforest of Brazil are likely under-collected. High degrees of endemicity appear to occur in Madagascar, New Guinea, Indochina, the Malay Archipelago, and the tropics of Africa and South America. In general, diversity of most aquatic Hemiptera groups is highest in tropical regions, although both Corixidae and Saldidae show the reverse pattern, with higher species richness in the Northern Hemisphere compared with the tropics. Aquatic bugs occupy a wide variety of habitats, including flowing rivers and streams, lakes, and temporary pool habitats. Several groups have invaded marine habitats, including Halobates (Gerridae), which occupy the open ocean far from any land masses. Hermatobatid coral treaders live in air-filled rocky crevices on shorelines, from which they emerge to forage during low tides (Foster, 1989), a habitat preference also shared by the Omaniidae and Aepophilidae. The invasion of marine habitats is a novel trait likely derived from freshwater ancestors. The most diverse families are the gerromorphs Veliidae and Gerridae and nepomorphs Notonectidae and Corixidae, and species in these groups are distributed across a diverse array of habitats, ranging from lakes to temporary rain pools, and large rivers to small riffly streams. Some of the “shore bug” groups verge on terrestrial habitats, with some members of Mesoveliidae, Hebridae, Gelastocoridae, and Ochteridae occurring far from surface water in damp habitats. Habitat requirements range from thermal spring systems with near-constant flow and temperature (some naucorids in Ambrysus) to extremely variable temporary rain pools that persist for short time periods (notonectid and corixid taxa that may be considered “fugitive species” adept at moving to new habitats; Hutchinson, 1951). Unlike many aquatic insect taxa in which the adult stage is primarily focused on mating and dispersal (e.g., Ephemeroptera, Trichoptera, and Plecoptera), adult Hemiptera are relatively long-lived, which enables adults to move easily among habitats as conditions change.

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GENERAL BIOLOGY External Anatomy Aquatic Hemiptera are hemimetabolous, typically with five instars (nymphs) that resemble adults in general morphology. In taxa that possess wings as adults, developing wingpads are visible in at least the fourth and fifth instars, which can be a useful trait for determining the stage of a specimen. An important difference between nymphs and adults is the presence of two-segmented tarsi on at least some legs of adults, versus one-segmented tarsi on nymphs. This character is useful for separating nymphs from adults in taxa that are facultatively or obligately apterous, which occurs in several gerromorphan families. The number of instars is fixed at five for most Hemiptera, with few exceptions (Esperk et al., 2007). This apparent phylogenetic constraint has implications for the evolution of body size, egg morphology, and egglaying behavior, discussed subsequently. Aquatic Hemiptera possess a piercing mouthpart, the rostrum, which is three- or four-segmented and directed posteriorly beneath the head. The rostrum is generally adapted to predation by piercing and feeding on digested fluids, except in the Corixidae, where it has been modified into a blunt cone-shaped structure for feeding on detritus and plant material. The hindwings of adults are membranous as with other insect orders, but the forewings consist of a leathery hemelytra plus a thin membranous margin (hence the Latin name “half-wing”). The aquatic Hemiptera span nearly two orders of magnitude in body size. The largest aquatic hemipteran is the South American belostomatid Lethocerus maximus De Carlo 1938, which may attain 11 cm in length, whereas adults of some pygmy backswimmers are only 1.5 mm (Schuh and Slater, 1995).

Locomotion Aquatic Locomotion Legs of aquatic Hemiptera are broadly adapted to skating on the water surface in the Gerromorpha and swimming and grasping in the Nepomorpha. Hydrofuge hairs located on the legs and body surface allow gerromorphans to move without breaking the surface tension of water, instead forming trough-shaped depressions at the surface. Andersen (1982) described three kinds of water surface locomotion in the Gerromorpha: walking, in which the three pairs of legs are moved as alternating tripods; rowing, in which the middle legs move simultaneously while the hind legs slide on the water surface; and skating, in which powerful strokes from the middle legs allow the bug to leave the water surface in a jump-and-slide movement. Most gerromorphans are able to walk on land or on the water surface. Rowing is most typical of the Veliidae, which have elaborate swimming fans in their middle tarsi, and skating is common in

TABLE 37.1  Global Species Richness of Aquatic Hemiptera by Region NA

NT

AT

IM

OC

AU

World

954

PA Gerromorpha-Semi-Aquatic Bugs Gerridae

Water striders

51

47

141

66

287

8

113

713

Hebridae

Velvet shore bugs

16

15

31

77

76

0

8

223

Hermatobatidae (1)

Coral treaders

0

0

1

1

2

4

4

12

Hydrometridae

Water measurers

6

6

37

31

30

4

15

129

Macroveliidae

Macroveliid shore bugs

0

2

1

0

0

0

0

3

Mesoveliidae

Water treaders

2

3

15

5

9

2

13

49

0

0

0

2

0

0

0

2

44

31

290

158

199

5

176

903

119

104

516

340

603

23

329

2034

Paraphrynoveliidae Veliidae

Riffle bugs

Total Leptopodomorpha-Shore Bugs Aepophilidae (2)

Marine bug

1

0

0

0

0

0

0

1

Leptopodidae

Spiny-legged bugs

7

1

1

13

6

0

4

32

Omaniidae (3)

Intertidal dwarf bugs

2

0

0

0

0

2

1

5

Saldidae

Shore bugs

147

70

41

28

22

13

23

344

157

71

42

41

28

15

28

382

19

0

0

6

47

0

6

78

4

17

111

23

9

0

5

169

140

136

152

111

77

0

46

662

2

7

48

2

9

1

47

116

0

0

10

31

111

0

12

164

Total Nepomorpha-Aquatic Bugs Aphelocheiridae Belostomatidae

Giant water bugs

Corixidae

Water boatmen

Gelastocoridae

Toad bugs

Naucoridae

Creeping water bugs

6

29

186

67

74

0

36

398

Nepidae

Water scorpions

7

13

93

84

48

0

23

268

Notonectidae

Backswimmers

36

35

96

85

75

3

92

422

Ochteridae

Velvety shore bugs

3

6

16

6

15

0

29

75

Pleidae

Pygmy backswimmers

6

6

12

4

9

1

6

44

0

0

8

0

0

0

0

8

Total

223

249

732

419

474

5

302

2404

Total species richness by region

499

424

1290

800

1105

43

659

4820

Potamocoridae

PA - Palaearctic, NA - Nearctic, NT - Neotropical, AT - Afrotropical, IM - Indomalayan, OC - Oceana, and AU – Australasian. Redrawn from Polhemus and Polhemus, 2008 with additional data from: Cobben, 1970; Schuh and Slater, 1995; and Polhemus and Polhemus, 2012.

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Helotrephidae

Chapter | 37  Order Hemiptera

the Gerridae. Some Veliidae also use “expansion skating” to move quickly, in which a small amount of saliva acts as a surfactant that breaks the surface tension of the water in front of the bug, thereby propelling it forward (­Andersen and Weir, 2004). Within the Nepomorpha, locomotion occurs either by synchronous strokes of the middle and hind legs (Belostomatidae and Nepidae) or with oar-like movement of the hind legs (Corixidae, Naucoridae, Notonectidae, and Pleidae). Swimming is also aided by long fringes of hair on the tibiae and tarsi of belostomatids, corixids, naucorids, and notonectids (Figure 37.3). The aquatic Hemiptera exhibit a wide range of swimming abilities. The Naucoridae, Corixidae, and Notonectidae are strong swimmers capable of fast movement in the pelagic zones of ponds and even swiftly moving streams, whereas the Gerridae and Veliidae are agile denizens of the water’s surface. Nepid water scorpions, on the other hand, are slow-moving creatures more suited to clinging on emergent vegetation, although they can swim (albeit awkwardly) when dislodged. Similarly, the hydrometrid water measurers often go unnoticed owing to their small size and slow movement across the surface of ponds.

Flight Flight ability ranges widely across the aquatic Hemiptera. One the one hand, some groups are strong fliers capable of long-distance dispersal to new habitats (most Belostomatidae, Corixidae, and Notonectidae; some Gerridae), whereas other taxa lack functional wings (some Gerridae, including the marine water strider Halobates) or functional flight muscles (some Belostomatidae, Naucoridae, and Notonectidae). In general, the Gerromorpha exhibit wing polymorphism, whereas the Nepomorpha exhibit flight muscle polymorphism; the latter likely retain functional or near-functional wings because they are involved in holding

FIGURE 37.3  A backswimmer (Notonecta) showing its ventral surface, with piercing rostrum and oar-like hind legs fringed with swimming hairs. Photograph courtesy of Mike Bogan.

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a subelytral air store for respiration (Andersen and Weir, 2004). Aquatic Hemiptera provide a compelling example of what C.G. Johnson (1969) termed the “oogenesis-flight syndrome,” in which there is a direct tradeoff between investment in egg production and investment in wings or wing musculature for flight dispersal. Unlike terrestrial insects for which flight is a daily component of foraging or escape from predators, most aquatic Hemiptera use flight primarily as a mechanism to disperse or migrate from one habitat to another. For some taxa, migratory flight is an activity that occurs once or twice in a lifetime, and flight is not required during the remaining parts of the life cycle. The expression of functional wings or flight muscles can thus be understood as the outcome of tradeoffs between egg production and dispersal to new habitats—tradeoffs that may change seasonally and across different ecological settings. Wing polymorphism can occur among successive generations within a single population, in which individuals produced during one part of the year develop functional wings whereas individuals produced later are apterous (Brinkhurst, 1959; Andersen, 1973). This may occur in response to proximate seasonal cues such as changing day length or pond drying (Andersen, 1973; Spence and ­Anderson, 1994). In the waterstrider Gerris, wing expression is correlated with habitat stability, with populations inhabiting large continuous rivers being apterous (wingless) and populations in smaller, more isolated habitats being macropterous (functional wings) (Järvinen and Vepsäläinen, 1976; Andersen and Weir, 1997). Flight muscle polymorphism can also occur across populations or species, or seasonally within a single taxon. Lack of flight musculature has been noted in the Corixidae, Gelastocoridae, and Notonectidae (Andersen and Weir, 2004). Some species in the belostomatid Abedus also lack wing musculature (Menke, 1979b), as do some members of the naucorid Ambrysus, which are endemic to remote desert springs (Whiteman and Sites, 2008). In the case of Abedus herberti Hidalgo 1935, wings are present but wing venation and flight musculature is much reduced (Lytle and Smith, 2004) and population genetic structure suggests that dispersal among adjacent populations is infrequent (Finn et al., 2007; Phillipsen and Lytle, 2013). Some belostomatids also exhibit flight muscle polymorphism on a seasonal basis. Adult Lethocerus spend the dry season in perennial lakes or streams. Heavy rainfall is a proximate cue that seasonal habitats, such as vernal pools, are becoming available for reproduction; these seasonal habitats are rich in food and largely devoid of predators that might feed on young (Lytle and Smith, 2004). After experiencing a sufficiently long rainfall cue, individuals exit the water, warm their flight muscles, and wait until dark to fly in search of vernal pools. In at least some cases, the flight muscles are then resorbed to provide nutrition for egg production (Cullen, 1969), a clear example of the tradeoff between flight ability

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and oogenesis. The “cryptic flightlessness” produced by a lack of wing musculature is underappreciated and in need of further study from both a morphological and a population genetic perspective, because it likely contributes to the high degree of endemism that has been documented in some aquatic Hemiptera groups.

Physiology Respiration Aquatic Hemiptera rely on atmospheric oxygen for respiration, and this physiological fact sets the stage for many of the behavioral and life history traits exhibited by this group. Gas exchange occurs via paired spiracles on the thorax and abdomen, which are in continuous contact with the atmosphere for taxa that live on or near water. For taxa that live submerged beneath the water surface, respiration is facilitated by a diverse array of siphons (Nepidae), air straps (Belostomatidae), and subalar air storage structures associated with the wings and hemelytron (Corixidae, Naucoridae, Notonectidae, and Pleidae). These submerged taxa hold an air store, a bubble or thin layer of air, between the wings and the abdomen with the aid of specialized hydrofuge hairs. Although they ultimately depend on atmospheric air for respiration, the submersed air stores can act as a physical gill while underwater. As oxygen is consumed from the air store by the respiring bug, new oxygen passively diffuses into the air store from the surrounding water. Similarly, as carbon dioxide waste builds up in the air store, it passively diffuses out to the environment. This gas exchange would occur indefinitely except that nitrogen eventually diffuses out as well, reducing the size of the air store and thus its ability to facilitate gas exchange. One exception to this is found in Aphelocheirus (Aphelocheiridae), in which a rigid plastron of fine hydrofuge hairs creates a permanent air store that does not require replenishment at the surface (Thorpe and Crisp, 1947). The ability of bugs to stay submerged will depend on the availability of oxygen in the water and the amount of activity of the bug. Some taxa may regulate these dynamics behaviorally by physically exposing the subalar bubble to facilitate gas exchange (Goforth and Smith, 2012). Although most aquatic bugs are slightly heavier than water, even a small air store causes positive buoyancy, requiring individuals to cling to vegetation or swim to remain submerged. As the air store become depleted, negative buoyancy results, which requires active swimming to the water’s surface to replenish air stores. This constant change in buoyancy likely explains why some groups (e.g., Belostomatidae) are typically found near the water’s surface or clinging to benthic substrates, but seldom moving freely in the pelagic zone. Some notonectids have solved the buoyancy problem by using hemoglobin to facilitate oxygen exchange, which makes them one of only three

insect families known to produce this oxygen-binding protein (along with Chironomidae and Oestridae; Weber and Vinogradov, 2001). Hemoglobin is produced in specialized fat-body cells within the abdomen, and these cells are extensively tracheated to facilitate gas exchange (Matthews and Seymour, 2008). The efficient oxygen-binding ability of hemoglobin allows notonectids to regulate bubble size to achieve neutral buoyancy at a variety of water depths, allowing them to occupy the pelagic zone of lakes, ponds, and large rivers.

Physiological Traits as Predators Most aquatic Hemiptera are predators, and for this reason they possess a physiology that is broadly adapted to consuming and processing other animals. In at least one instance, the ingestion of vertebrate prey is required for the production of steroids, which may serve as an anti-predator defense (Lokensgard et al., 1993). In belostomatine giant water bugs, vertebrate prey supply the precursor cholesterol, which is then converted to a variety of pregnanes. When agitated or threatened, the bugs emit copious amounts of these distasteful bluish-white compounds from cephalic glands at the base of the rostrum.

Osmoregulation Aquatic Hemiptera taxa vary in their ability to tolerate salinity, eutrophication, and pH, although the physiological basis for this variation is not well understood. Within the Corixidae in particular, there is great variation among species in nutrient and pH tolerance, and this has spurred the development of species-based indices to monitor changes in lake pollution (Jansson, 1987). The North American corixid Trichocorixa verticalis (Fieber 1851), on the other hand, is exceptionally tolerant to salinity, and may be found in habitats ranging from low-salinity marshes to hypersaline ponds. In a congeneric species, salinity tolerance was achieved by maintaining hemolymph Na+, Cl−, Mg2+, and K+ hyperosmotic to the medium at low salinities and hyposmotic at high salinities, which suggests a strong ability to osmoregulate across a variety of environments (Jang and Tullis, 1980). The ability to persist in a wide range of salinities may have facilitated T. verticalis’ ability to invade and establish in habitats throughout Europe, Africa, and Australia, although other factors such as anthropogenic disturbance may have had a role (Rodríguez-Peréz et al., 2009; Van De Meutter et al., 2010).

Life Cycle and Reproduction Life Cycle Most aquatic Hemiptera in temperate zones appear to have a univoltine life cycle, in which eggs are laid in the spring,

Chapter | 37  Order Hemiptera

larvae develop during summer and fall, and individuals overwinter as adults. Some taxa, especially smaller-bodied water striders, water boatmen, and backswimmers, produce multiple generations per year; at the other end of the spectrum, the large-bodied belostomatid Abedus can live for over 2 years and produce multiple clutches of eggs (Lytle, 2011). The number of generations per year can also change with latitude; Barahona et al. (2005) reported that the widespread corixid Sigara selecta (Fieber, 1848) produces as many as four cohorts annually at the warm southern edge of its European distribution. Although there is some evidence that species occurring in the tropics can breed nearly year round (Peters and Ulbrich, 1973), tropical taxa are likely constrained by other seasonal factors such as the timing of rainy and dry seasons (Lytle and Smith, 2004).

Reproduction Eggs of aquatic Hemiptera are highly variable in structure, size, color, and location of oviposition, but can usually be recognized as hemipteran by the presence of a tough, hexagonally reticulate chorion and button-like or peg-like micropylar processes (Menke, 1979a). Eggs can be ovoid (Notonectidae) or elongate (Mesoveliidae and Macroveliidae), with threadlike respiratory horns (Nepidae), or they can be attached to a stalk (Hydrometridae). The diversity of form allows the ready identification of the eggs of most groups to genus (Andersen, 1982). Most aquatic Hemiptera lay their eggs in or slightly above the water, with the exception of the shore-dwelling gelastocorids and ochterids and Hydrometra, which deposit eggs terrestrially. Eggs are attached to mineral substrates, plant material, or in some cases to the backs of males (belostomatine giant water bugs). Even the pelagic marine waterstrider Halobates must find floating detritus such as driftwood, animal carcasses, or plastic bottles on which to oviposit.

ECOLOGY AND BEHAVIOR Feeding Most aquatic Hemiptera are predators and feed using their piercing rostrum. The rostrum is indented medially and forms a groove enclosing two pairs of stylets. The mandibular pair of stylets possesses errations that serve to “harpoon” prey, whereas the maxillary pair of stylets is inserted deeper to deliver digestive enzymes that quickly paralyze and digest prey (Andersen and Weir, 2004). These enzymes can be a mixture of proteolytic, hemolytic, and neurotoxic enzymes that are potent and capable of subduing prey items many times larger than the bug itself (Dan et al., 1993). Digested prey fluids are then drawn up via the maxillary stylets. The larger-bodied members of the Belostomatidae are legendary for their predatory abilities (Figure 37.4); incidences of predation on fish,

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FIGURE 37.4 A Lethocerus medius (Guérin, 1856) (Belostomatidae) feeding on a Mexican stoneroller (Campostoma ornatum) in a southern Arizona (USA) stream. Lethocerine belostomatids are the largest of the aquatic Hemiptera, capable of subduing vertebrate prey such as fish, frogs, and snakes. Photograph courtesy of Mike Bogan.

frogs, snakes, and even birds have been recorded (Menke, 1979b). Because of the piercing mode of feeding, prey size is somewhat decoupled from the body size of the predator, although there are limits imposed by the ability of the bug to handle prey items that are too large or too small. Some groups are equipped with raptorial forelegs that are used to grasp prey while the digestive enzymes take effect (most notably Naucoridae, Belostomatidae, Nepidae, and Gerridae). An exception to predatory feeding is found in the Corixidae, which possess a blunt, modified rostrum adapted to feeding on detritus. Inflated, scoop-like fore tarsi are used to direct detritus toward the rostrum. Although their diet may include significant amounts of plant material, animal food (protozoans and microscopic invertebrates) may be a common or even necessary part of the corixid diet (Jansson, 1986). Water striders in the Gerridae and Veliidae are sensitive to surface vibrations and can locate prey struggling on the water’s surface. Nepid water scorpions and belostomatid giant water bugs can be found in vegetation or along the rocky edges of pools, peering facedown into the water with raptorial legs spread apart, waiting for prey. These taxa often leave their respiratory siphons or air straps in continuous contact with atmospheric air at the surface. Notonectid backswimmers can float neutrally in the pelagic zone of ponds and rivers, waiting for small prey such as cladocerans and copepods. Although aquatic Hemiptera are often the predator, and are sometimes the apex predator in their ecosystem (Boersma et al., 2014), they are sometimes the prey. For example, Corbet (1959) reported that large water bugs (Belostomatidae and Naucoridae) are the primary food for young Nile crocodiles in Uganda.

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Mating The mating behaviors of aquatic Hemiptera are diverse, and numerous taxa have been studied because behaviors are readily observable in the laboratory and field. The ability of females to store viable sperm internally in a spermatheca has been demonstrated for several aquatic Hemiptera groups (Belostomatidae: Smith, 1979; Gerridae: Rubenstein, 1989) and has undoubtedly influenced the evolution of mating behaviors and morphologies. Courtship behavior in the Gerridae involves the production of low-frequency surface waves by males (Wilcox and Spence, 1986). Audible sound production by stridulation is known in the Veliidae and a few Gerridae, but is most widespread throughout the Nepomorpha (Polhemus, 1994). The corixids are well known for producing a variety of courtship sounds, some of which are audible to the human ear. The diminutive Micronecta scholtzi (Fieber, 1860) has the distinction of being the loudest stridulating animal after accounting for its 2-mm body size (Sueur et al., 2011); stridulations can reach 99.2 dB, which is equivalent to hearing a loud orchestra from a frontrow seat. Mating in the gerrids and veliids involves both behavioral and morphological strategies for achieving copulation, or for preventing unwanted copulations. Male gerrid waterstriders are often observed mate-guarding females by grasping them dorsally, and females are often seen dislodging the smaller-bodied males. The sexual conflict that arises from the fitness benefits that males receive from multiple copulations versus the costs that females incur from unnecessary matings (risk of predation and loss of time spent feeding) has driven the evolution of a variety of morphological strategies and counterstrategies for facilitating or preventing matings. Arnqvist and Rowe (2002) described an example of a morphological “arms race” resulting from sexual conflict in 15 species of Gerris waterstriders. In species where females have evolved features for dislodging males, such as erect abdominal spines and a less accessible genital tip, males have simultaneously evolved exaggerated grasping appendages such as prolonged genital and pregenital segments and a flattened distal portion of the abdomen (Figure 37.5). By contrast, other species show little differentiation between male and female morphologies. Similarly to the situation in Gerris, males in the gerrid Rheumatobates possess legs and antennae that are highly modified for grasping females. Phoreticovelia species (Veliidae) exhibit what appears to be a less conflict-ridden approach to mating, in which pairs remain in tandem for extended periods of time, during which the smaller male feeds on a glandular secretion produced by the female (Arnqvist et al., 2007). A rare example of paternal care of eggs can be found in the giant water bugs. Whereas exclusive paternal care has evolved in only a handful of arthropod lineages (Tallamy, 2001), a major radiation of this behavior has occurred in the Belostomatidae. Male giant water bugs in the subfamily

FIGURE 37.5  Examples of sexual dimorphism in Gerris water striders. At one extreme, males of G. incognitus (a) have an elongated pregenital segment and flattened abdomen whereas female G. incognitus (b) possess an erect abdominal spine for dislodging males. At the other extreme, males (c) and females (d) of G. thoracicus exhibit little sexual dimorphism. Image from Arnqvist and Rowe, 2002.

Belostomatinae care for offspring by brooding them on their backs until they hatch, a period that can last over a month (Figure 37.1). During this time, males provide care by keeping the eggs at the water’s surface, where they remain moist yet also have contact with atmospheric oxygen. The lethocerine belostomatids exhibit a similar behavior in which males guard eggs laid on emergent vegetation by females, occasionally bringing water to moisten the eggs and assuming a defensive posture when disturbed (Ichikawa, 1988; Smith and Larsen, 1993). Parental care appears to be required to ensure the survival of eggs, which will desiccate if left terrestrially or drown if left submerged in standing water (Smith, 1976).

Body Size and Evolution of Paternal Care The large body size of some Nepomorpha may have implications for the evolution of paternal care also observed in the group. Smith (1997) noted that a large adult body size

Chapter | 37  Order Hemiptera

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necessitates large eggs. The dual constraints of Dyar’s rule (which states that intermolt body size is constrained to an upper limit; Dyar, 1890; Cole, 1980; Klingenberg and Zimmermann, 1992) and Hemiptera molt number (constrained to five molts) dictate this to be so. Selection for large body size, presumably to exploit large anuran prey, appears to have occurred early in the evolution of belostomatids (the fossil Mesobelostomum deperditum (Germar, 1839) from the 150 million–year-old Solnhofen formation is nearly 6 cm in length). These large eggs face respiratory challenges underwater owing to the allometry of egg size. As egg size increases, the volume of oxygen-requiring tissue increases by the cube of egg diameter while the surface area (where oxygen diffusion takes place) increases by only the square. Smith suggested that one solution to this problem is parental care, in which eggs are kept moist above or near the water’s surface to prevent desiccation. Under this scenario, emergent brooding evolved first in the lethocerines, followed by a transition to back brooding in the belostomatines (Figure 37.6). Interestingly, the Nepidae appear to have solved the same physiological problem of large eggs with a different mechanism; nepid eggs have evolved elongate respiratory horns, which effectively increase the surface area of the eggs to allow adequate oxygen diffusion.

use intense rainfall from thunderstorms as a cue to crawl out of streams, thereby escaping the flash floods that follow soon after (Lytle, 1999; Lytle et al., 2008). Laboratory experiments using artificial rainfall confirm that the impact of water droplets on the stream surface is sufficient to trigger the behavior. Similar, though not necessarily homologous, behaviors are documented in the water strider Aquarius, the naucorid Ambrysus, and the nepids Ranatra and Curicta (Lytle and White, 2007). Comparative data from other taxa in the Nepoidea suggest that “rainfall response behavior” may have originally evolved to trigger migration from dry season habitats (perennial lakes and streams) to rainy season habitats (i.e., vernal pools that are used for breeding), and has been secondarily exapted to allow the escape of flash floods (Lytle and Smith, 2004). In general, it is likely that the amphibious lifestyle of most aquatic Hemiptera adults predisposes them to respond behaviorally to disturbances. Because they are air-breathers, they can easily crawl or fly to new habitats as conditions deteriorate. By contrast, other aquatic insect groups such as the Trichoptera and Ephemeroptera must rely on life history strategies (e.g., timing of emergence, diapauses) to survive these same disturbances (Lytle, 2008).

Flood Survival

In pre-Hispanic times, the Aztecs of Central Mexico harvested water boatmen eggs, known as ahuauhtli, in large numbers from lakes (Alcocer-Durand and Escobar-Briones, 2010; Figure 37.7). Bundles of reeds were placed below the water surface and would soon become covered in eggs from

Several groups possess adaptations that allow them to occupy habitats prone to disturbances such as floods. ­Desert-dwelling belostomatids in Abedus and Lethocerus

Importance to Humans

FIGURE 37.6  Evolution of male brooding behavior in the giant water bugs. Parental care compensates for the respiratory demands required by large-volume eggs in the Belostomatidae; respiratory horns on eggs in the Nepidae appear to serve the same purpose. Reproduced from Smith, 1997.

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FIGURE 37.7  Drawing from Book 11 of the Florentine Codex (Sahagun, 1577) depicting corixids (axayacatl) laying eggs (ahuauhtli) on submerged bundles of reeds. The eggs were harvested for food by Aztecs in pre-Hispanic Mexico. Image retrieved from an article by Dr. Matthew McDavitt, http://www.mexicolore.co.uk/aztecs/flora-and-fauna/astonishing-axayacatl and also available from a scanned historical version of the Codex at http://www.wdl.org/en/item/10622/view/1/137/.

the abundant corixids. The eggs, valued as a delicacy, were dried, pressed into bricks, and used in cooking. The large belostomatid Lethocerus is eaten in Southeast Asia, and the scent glands of males are also harvested to produce a highly valued extract for seasoning food. Belostomatids and naucorids have been implicated in the transmission of buruli ulcer disease, a necrotizing cutaneous infection caused by Mycobacterium ulcerans, although the role of aquatic bugs may involve passive dissemination of the disease rather than active transfer via bites (Merritt et al., 2010). Although the piercing mouthparts of many aquatic Hemiptera, primarily the nepomorphs, can inflict a painful bite (e.g., Haddad et al., 2010), most species will not do so unless carelessly handled; the unfortunate common name of “toe biters” for belostomatids is something of a misnomer. Because of their ecological role as predators, aquatic bugs also show promise for controlling diseases and agricultural pests. The veliid Microvelia can be an effective predator on the brown planthopper (Nilaparvata lugens), a major rice field pest in Southeast Asia (Nakasuji and Dyck, 1984). A large number of aquatic bug species are known to feed on mosquito larvae and adults (Chapman, 1974) and show promise for controlling the mosquito vectors of yellow fever, dengue, malaria, and encephalitis (Shaalan and Canyon, 2009). Because some nepomorphs feed on snails, they may be useful in regulating human pathogens that have snails as intermediate hosts, such as schistosomes (Kesler and Munns, 1989).

Conservation of Hemiptera Three features of aquatic Hemiptera biology seem to pose a conservation problem for the group. First, aquatic habitats are disproportionately imperiled relative to terrestrial

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habitats. Rivers, streams, wetlands, and lakes cover less than 0.02% of the earth’s surface, and these habitats face a barrage of conservation threats including damming of rivers, drainage of wetlands, and groundwater pumping for agricultural and municipal uses. This is a problem common to all aquatic taxa, vertebrate and invertebrate, and it is becoming increasingly recognized by the conservation community (Stein and Kutner, 2000). Second, a number of aquatic Hemiptera taxa are endemic to small areas, sometimes to a single spring or drainage complex. This may be result from the tendency in the group to evolve flightlessness, to biogeographic history, to the disjunct nature of suitable aquatic habitat, or to a combination of factors. Nonetheless, the degree of endemicity across the landscape is striking in some cases, particularly in arid land regions where surface water is already a scarce commodity (Polhemus and Polhemus, 2002). Third, most aquatic Hemiptera are predators, and some may be considered the apex predator in their habitat. A number of characteristics predispose apex predators to extinction, including ecological dependence on prey species, small population size, large body size, and relatively low fecundity (Boersma et al., 2014). Although these factors clearly do not apply to all aquatic Hemiptera, many taxa likely fit the “endangerment profile” of (relatively) large-bodied, effectively flightless predators restricted to specific microhabitats in geographically isolated aquatic ecosystems. Overall, we do not currently have an accurate picture of the conservation status of aquatic Hemiptera. Polhemus (1993) examined the status of all aquatic insects and determined that whereas there is no clear evidence that aquatic insects as a group are imperiled, we simply lack enough distributional information on most groups to provide an accurate assessment. In some cases, the situation is clear-cut; the first aquatic insect to be listed under the US. Endangered Species Act was the Ash Meadows naucorid (Ambrysus amargosus La Rivers, 1953), which received this status because of imminent threats to its only remaining desert oasis habitat. However, there exist many other aquatic Hemiptera taxa with equally restricted distributions that receive little or no formal protection (Whiteman and Sites, 2008). The situation is likely compounded in other parts of the world with high endemism and little or no information on current distribution and conservation status of species.

COLLECTING, CULTURING, AND PREPARING SPECIMENS Despite abundant collections from the twentieth century, recent specimens of aquatic Hemiptera are less well represented in museum collections. This is likely because of reluctance on the part of many collectors to kill largebodied taxa, and a general feeling that new specimens are

Chapter | 37  Order Hemiptera

not needed. This is unfortunate, because our understanding of how species distributions are changing owing to natural and anthropogenic causes depends directly on properly collected and curated specimens. Furthermore, modern molecular techniques enable the amplification of fragments and even entire sequences of DNA from museum specimens (Thomsen et al., 2009), which makes repeated collections of common species important for understanding ecological and evolutionary processes. Most aquatic Hemiptera can be collected effectively with a standard D-frame net, although in practice nearly any net with the proper mesh size will suffice (500 μm will catch most specimens without clogging too quickly from detritus). Taxa in the pelagic zone such as notonectids and corixids can be obtained by sweeping, whereas others may be found by working submerged vegetation (nepid water scorpions and belostomatids). Surface-dwellers such as gerrids and veliids are often visually wary, and so must be targeted directly with the net. Bugs that crawl among the interstices of rocks in streams (naucorids and some belostomatids) can be obtained by kick-netting, where rocks are disturbed with the net placed immediately downstream. Giant water bugs in Abedus and Lethocerus can be collected by “grabbling,” which involves reaching under rocky stream banks and pinning the bugs by hand when encountered (the author has captured hundreds if not thousands this way, without enduring a single bite). Shore bugs are usually collected by hand, by overturning rocks and debris near the water’s edge. Specimens can be preserved in ethyl alcohol (at least 70%) or pinned. To preserve DNA as well as the morphological specimen, it is important to keep the water content of specimens as low as possible. Preservation in 95% ethanol followed by a complete change to fresh 95% ethanol within 24 h produces good results, although the effectiveness will ultimately depend on the ratio of tissue to preservative in the vial. Insects initially preserved in ethanol can be pinned later or stored in ethanol. Pinned, dried specimens can be a good way to preserve DNA as long as they are kept in a low-humidity environment. For DNA preservation of large-bodied species, it may be necessary to remove sample tissue (e.g., all or part of a leg) into a separate vial containing absolute ethanol (or alternatively, anhydrous calcium sulfate, which serves as a desiccant). Because aquatic Hemiptera breathe air, they should not be transported in water if they are to be kept alive. Moist paper towels in plastic containers (perforated to allow air exchange) work well, as long as the bugs are kept cool during transport. Many taxa can be maintained in aquaria, but predator taxa will require a constant supply of prey items, ranging from fruit flies for small taxa and early instars, crickets, or mealworms for larger individuals, and tadpoles or fish for the largest belostomatids.

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