Large Size As an Antipredator Defense in an Insect

DOUGLAS W. WHITMAN ANDJournal SHAWN of VINCENTOrthoptera Research 2008,17(2): 353-371353

Large size as an antipredator defense in an insect

Accepted December 8, 2008

DOUGLAS W. WHITMAN AND SHAWN VINCENT

[DWW]4120 Department of Biological Sciences, Illinois State University, Normal, IL 61790, USA. Email: [email protected] [SV]Department of Natural, Information, and Mathematical Sciences, University of Indiana Kokomo, IN 46902, USA. E-mail: [email protected] Abstract and are often more difficult to catch. Small insects generally have faster population growth rates than larger insects, and vertebrate Although large size is considered an evolved antipredator defense predators generally prefer larger insect prey over smaller. In fact, for some vertebrates and shellfish, large size is generally not considered size-selective vertebrate predation may be one evolutionary factor an adaptive defensive trait in insects. Here we propose that large size in that explains why insects as a group remain small in body size. chemically defended grasshoppers has evolved as a beneficial antipredator In contrast to the idea that small size aids insect defense, there trait. The lubber grasshoppers Romalea microptera and Taeniopoda eques are has been little discussion of the possibility of large size serving an the largest grasshoppers in North America north of Mexico. These closely antipredator function in insects. For example, neither Edmunds related species escape most vertebrate predation by possessing powerful predator-deterrent toxins and by nocturnal roosting. We hypothesize that (1974), Harvey & Greenwood (1978), Cloudsley-Thompson (1980), escape from vertebrate predation allowed lubbers to evolve a larger body size, Hermann (1984), Endler (1986, 1991), Evans & Schmidt (1990), increased fecundity and provided many other benefits, including defense New (1991) nor Ruxton et al. (2004), discuss large size as an evolved against invertebrate predators. To test the hypotheses that large lubber size antipredator mechanism in insects. However, we believe that under reduces predation, we conducted feeding trials with wolf spiders (Honga certain circumstances, large body size can greatly enhance insect carolinensis), assassin bugs (Arilus cristatus), preying mantids (Tenodera survival against both invertebrate and vertebrate predators, and aridifolia), fire ants Solenopsis( invicta), frogs (Rana pipiens), and birds (Sturnus therefore may be under positive directional selection. vulgaris and Passer domesticus). Our results show that larger lubber instars In this paper, we argue that large size serves as an antipredator enjoyed a highly significant advantagevis-à-vis predators, demonstrating the defense in two species of lubber grasshopper (Romalea microptera adaptive value of large size against both vertebrate and invertebrate predators. (Beauvois) and Taeniopoda eques (Burmeister), family Romaleidae)1. Adult lubbers were generally immune from predation. It appears that lubbers have evolved to occupy a relatively predator-free ecological space: they are too We provide evidence to support five points: 1) Vertebrate predation large to be attacked by most invertebrate predators and too toxic for most typically selects against large size in insects. 2) Lubber grasshoppers vertebrate predators. We propose an evolutionary scenario whereby a change are chemically and behaviorally defended against most vertebrate in feeding behavior toward vertebrate-toxic plants served as an evolutionary predators. 3) Escape from vertebrate predation has released lub- breakthrough, setting in motion the subsequent evolution of increased chemical bers from predatory small-size selection, allowing them to evolve a defense and large body size in lubbers. To determine if large size is associated larger size. 4) Large size is highly beneficial to lubber grasshoppers with chemical defense in grasshoppers in general, we compared body sizes vis-à-vis both invertebrate and vertebrate predators, and as such, of ~ 40 toxic vs ~ 3,000 nontoxic grasshopper species. Our results show that is evolutionarily favored as an adaptive antipredator trait. 5) This chemically defended species tend to be larger than nondefended grasshoppers, syndrome is common among chemically defended grasshoppers, supporting an association between chemical defense and large size in insects. which tend to be larger than palatable grasshoppers. Large size may be favored in insects when vertebrate predation is removed as a strong selective factor. Results and Discussion Key words 1) Vertebrate predation selects against large size in insects.—Insect antipredator defense, body size, size refuge, predator-free space, de- predator-prey interactions are extremely diverse and complicated fense mechanism, chemical defense, allomone, grasshopper, lubber, (Evans & Schmidt 1990, New 1991, Woodward et al. 2005), and Acrididae, Romaleidae, Romalea microptera, Taeniopoda eques nearly all types of interactions are possible. However in general, larger arthropod prey are more conspicuous to vertebrate predators than Introduction are smaller arthropod prey (Curio 1976, Winfield & Townsend 1983, Schülert & Dicke 2002, Shine & Thomas 2005). This is partly because Insects have evolved an impressive arsenal of antipredator de- the probability of encountering/detecting a prey item increases as fenses, including, rapid escape, crypsis, anachoretes (hiding in holes), prey size increases (Maly 1970, Ware 1972, Curio 1976, Maiorana mechanical and chemical defenses, startle and threat behaviors, 1981, Bell 1990, Goerlitz & Siemers 2007, Troost et al.). In addition, hard exoskeletons, mimicry, deimatic behavior, shelter-building, small insects can more easily hide behind small objects or enter group and symbiotic defenses, and rapid reproduction, which out- small cavities inaccessible to large predators, such as under bark or paces that of associated predators (Edmunds 1974, Blum 1981, rocks, or between tight-fitting plant parts (Edmunds 1974). Although Evans & Schmidt 1990, Salazar & Whitman 2001). Small size is a maximum running and flying speeds in insects scale positively with key component of many of these defensive strategies. Small insect 1We will refer to R. microptera and T. eques as “lubbers,” although that term prey are less conspicuous to vertebrate predators than large prey is often applied to all members of the family Romaleidae.

JOURNAL OF ORTHOPTERA RESEARCH 2008, 17(2) se 354 DOUGLAS W. WHITMAN AND SHAWN VINCENT DOUGLAS W. WHITMAN AND SHAWN VINCENT 355 body size (Dudley 2000, 2002; Bonner 2006), flying insects usu- community (e.g., Pearson 1985). As such, insects generally cannot ally escape flying predators not by speed, but by maneuverability escape vertebrate predation by evolving a larger body size. (Cloudsley-Thompson 1980) and acceleration, both of which are In contrast, insects can escape vertebrate predation by evolving inversely proportional to body size (Dudley 2000, 2002) (e.g., smaller size. Arthropod size decreases by an order of magnitude syrphid fliesvs large beetles, dobsonflies, mantids,etc. : McLachlan below the small-size limit for acceptance by most vertebrate preda- et al. 2003). Likewise, small insect species typically exhibit greater tors (except small fish and larval amphibians). Indeed, mites, Col- burst-acceleration during escape-jumping than large species (e.g., lembola, thrips, Psocoptera, Zoraptera, aphids, whiteflies, lice, fleas, fleas, flea beetles, and leaf hoppersvs crickets) (see Alexander 1985), and many scale insects, beetles, Diptera, Hymenoptera, and early and smaller individuals are theoretically more maneuverable than instars of many insects are simply below the acceptable prey-size larger ones when running (Full et al. 2002). These size-relationships range of most vertebrate predators. Hence, vertebrates are a strong imply that larger insects may be under greater threat than small selective force against large insect size, but not against small insect insects from vertebrate predators. body size (Nylin & Gotthard 1998). Both optimal foraging theory (Stephens & Krebs 1986) and empirical evidence (Prop 1960, Tinbergen 1960, Mattson et al. 1968, 2) Lubber grasshoppers are chemically and behaviorally defended against Curio 1976, Churchfield et al. 1991, Schülert & Dicke 2002), sug- most vertebrate predators.— The lubber grasshoppers Romalea microp- gest that when all other things are equal, vertebrate predators prefer tera and Taeniopoda eques are closely-related species from North larger over smaller insect prey items, because large insect prey are America. R. microptera inhabits the southeastern portion of the USA, energetically more nutritious and are often easier to capture (O’Brien whereas T. eques survives primarily in the Chihuahuan Desert of et al. 1976, Morin 1984, Chen et al. 2004, McCracken et al. 2004; the southwestern USA and northern Mexico (Rehn & Grant 1959, but see Shine & Thomas 2005). For example, broad-headed skinks, 1961). Their morphologies, behaviors and antipredator defenses are Eumeces laticeps, selected large crickets and ignored small crickets similar to each other, and different from all other North American when offered both simultaneously (Cooper et al. 2007), and all of grasshoppers (Stuaffer & Whitman 2007). These two species are so six species of insectivorous mammals tested by Dickman (1988) closely-related that they can interbreed and produce fertile offspring preferred large vs small cockroaches. Field studies show that large in the laboratory (Whitman unpub.). Because of their close related- insects are more susceptible to vertebrate predation than small insects (Exnerova et al. 2003). For example, larger insects comprised only 2% of “available” prey, but 28% of all prey items fed by water pipits, Anthus spinoletta, to nestlings (Brodmann & Reyer 1999). Likewise, sphingid caterpillars represent 70% of the biomass fed by trogons, Trogon elegans, to their nestlings, and 98% of the sphingid prey were the last (largest) instar (Janzen 1993). Finally, many field studies show that birds, which in some communities consume enormous numbers of grasshoppers (Bryant 1912; Smith & Popov 1953; Greathead 1966; Joern 1986, 1992; Johnson et al. 1987; Fowler et al. 1991; Bock et al. 1992; Ji et al. 2008), prefer large, over small grasshoppers (Stower & Greathead 1969, Belovsky 1990, Belovsky et al. 1990, Belovsky & Slade 1993, Gardner & Thompson 1998). On a community scale, each vertebrate predator species restricts itself to a specific range of prey sizes (Sinclairet al. 2003, Radloff & Du Toit 2004, Churchfield & Rychlik 2006, Montoya & Burns 2007, Whiting et al. 2007, Owen-Smith & Mills 2008). This range very often exceeds the largest, but not the smallest insect size – i.e., many vertebrate predators can take prey several orders of magnitude larger than the largest insects, but cannot successfully prey on the smallest insects (Wilson 1975, Sinclair et al. 2003). This is seen with large alligators (pers. obs.), owls (Craighead & Craighead 1956, Salvati et al. 2001), hawks (Craighead & Craighead 1956, Johnson et al. 1987), storks (Smith & Popov 1953, Falk et al. 2006), fox (Aranda 1995), coyotes (Fichter et al. 1955, Ortega 1987), hyenas (Kingdom 1997), bears (Chapman & Feldhamer 1982) and African leopards (Ray & Sunquist 2001), all of which take both insects and much larger vertebrate prey. In contrast, some very large insects can escape predation by the smallest vertebrates (salamanders, tiny frogs, small birds); however, many small vertebrates can handle large insect prey by ingesting them in pieces (birds, mice, some lizards) (Kaspari 1990) or by having exceptionally large mouths or expandable gullets (Emerson et al. 1994). In addition, even if an insect species did gain protection against small vertebrates by evolving a larger size, that would presumably make that insect prey even more conspicuous and at- Fig. 1. R. microptera grasshopper expelling odorous, frothy tractive to the numerous larger vertebrate predators in that same defensive secretion from metathoracic spiracles. See Plate VI.

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Fig. 2. T. eques defensive display in response to inquisitive mouse. Display includes visual (aposematic colors, twisting abdominal tip and antennae, elevated wings, jumping and thrusting hind legs), acoustic (auditory discharge of defensive secretion and sometimes wing stridulation), mechanical (spiny hind legs and biting), and chemical (defensive secretion, regurgitation, defecation, and toxic blood) elements. Note defensive secretion emerging from metathoracic spiracles. See Plate VII.

ness and similarity in defense traits, we will combine the results bers is an internal toxin, apparently synthesized by, and present from both species, in this paper. in, all lubber instars (Whitman 1990). It is relatively potent, and These two grasshopper species are chemically defended by two, consumption of a single 2nd instar lubber can induce vomiting in nearly identical, two-component antipredator mechanisms. The first an inexperienced bird or lizard (Fig. 4). Often a naïve vertebrate mechanism is a secretory defense derived from the respiratory system, predator will attack the first few lubbers it encounters, then after and unique among arthropods. In both species, the spiracular tracheal experiencing the negative effects (Figs 3-5), will refuse to attack trunks of the metathorax produce and store an odorous, noxious subsequent offerings. Such food-aversion conditioning is probably secretion that is sprayed out at attacking predators. This defensive highly adaptive to predators, because consumption of lubbers can be secretion emerges from the metathoracic spiracles first as a dispersive lethal (Whitman unpub.). The internal toxin has not been chemi- spray, and then as an adherent froth (Fig. 1) (Whitman et al. 1991, cally identified, but is present even in first-instar nymphs fed lettuce 1992). It contains a witches' brew of low-weight phenolics, quinones, (Whitman & Orsak 1985). aldehydes, ketones, alcohols, organic acids, terpenoids, and miscel- Dual-mechanism chemical defenses are common in insects, laneous other substances (Jones et al. 1988, Polanowski et al. 1997). where a volatile secretion often serves both a rapid warning or Some of the secretion components are synthesized by the insect alerting function for naïve predators, and a memory-eliciting func- itself, whereas others are derived from its diet. Lubbers are poison- tion for experienced predators (Whitman et al. 1985, 1986, 1990, plant generalists, and they sequester many plant toxins into their 1991). A second substance, held in the blood or body tissues, then tracheal defense glands. For example, lubbers that feed on onion or poisons the predator, inducing food-aversion conditioning and garlic secrete a variety of plant-derived sulfur compounds character- a lasting learned association to the first defense (Whitman et al. istic of those plants (Jones et al. 1987, 1988, 1989). Lubbers that 1990). feed on catnip sequester and secrete terpenoid lactones (Blum et al. In lubbers, these two defenses have different effects on preda- 1990), and those that feed on diets high in catechol or hydroquinone, tors. The secretion alone can deter some invertebrate and vertebrate sequester and release large amounts of these substances (Snook et predators outright (Eisner et al. 1971, Jones et al. 1989, Blum et al. al. 1993). As such, this unique defense gland serves as a toxic waste 1990), but seems to have less effect against others, such as preying dump for potentially harmful, plant secondary compounds. When mantids, wheel bugs, large spiders, centipedes, toads, and some ejected, these low-weight substances quickly volatize, enveloping mammals.2 By contrast, the internal defense is highly toxic to birds the grasshopper in a noxious chemical cloud, deterrent to many and lizards, partially toxic to toads and mammals, and only mildly vertebrate predators (Fig. 2). We have observed naïve lizards and birds violently fling lubbers from their mouths after secretion ejec- 2To understand lubber defense ecology, we tested lubbers against 112 species tion. Some predators gagged or wiped their mouths or snouts on of various predator taxa. Given the two separate defense mechanisms and the substrate after encountering this pungent and irritating exudate the great physiological, morphological, and behavioral diversity among grasshopper predators, it is not surprising that we observed virtually every (Fig. 3) (Whitman et al. 1985, Yosef & Whitman 1992). type of predator response against lubbers. The results of these trials will be The second mechanism of the chemical defense system of lub- published elsewhere.

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Fig. 3. Grasshopper mouse Onychomyes torridus, rubbing face and paws in dirt, after becoming contaminated with blood and defensive secretion of T. eques grasshopper. See Plate VII. Slatkin 1984, Schluter et al. 1991, Mayhew 2006). This is certainly deterrent to invertebrate predators (see below). the case for body size (Roff 1981, 2002; Nylin & Gotthard 1998; Strong chemical defenses explain why lubbers can afford to be Blanckenhorn 2005; Lomolino 2005; Mänd et al. 2007), where flightless, lumbering, brightly colored, large, gregarious, and often any number of factors could select for large size (e.g., fecundity, extremely abundant in nature: we have recorded > 900 individuals sexual selection, surface-volume relationships, desiccation resistance, per 100 m2 (Lamb et al. 1999). Despite their abundance, conspicu- thermal inertia, lowered mass-specific metabolic rates, increased ous appearance and sluggish nature, lubbers seem to suffer little strength, ability to consume tough food, locomotion, and increased vertebrate predation. Indeed, during 38 h of field observations of food and water reserves, etc.) (Peters 1983, Schmidt-Nielsen 1984, large and dense populations of active and conspicuous lubber grass- Hon k 1993, Roff 2002, Chown & Nicolson 2004, Makarieva et hoppers inhabiting natural and old-field habitats, we recorded 102 ě al. 2005, Vincent 2006, Vincent & Herrel 2007, Whitman 2008). individual insectivorous birds from 17 species foraging among the Likewise, any number of factors might select for small size, the most grasshoppers, and only observed one bird attack a lubber, despite important being viability selection from either time constraints observing constant bird attacks on other insect species (Whitman, or predative pressures (Stearns 1992, Blanckenhorn 2000, Roff unpubl.).3 2002). As previously discussed, vertebrate predation may select Although some mammals (mice, rats, raccoons, opossums) and for small size in insect prey, and this may be a contributing reason toads will occasionally consume a few lubbers, these predators are to why most grasshoppers and most insects are relatively small in generally not a threat because they hunt at night, and lubbers roost comparison to vertebrates. at the tops of vegetation from dusk to dawn (Whitman 1987). In Hence, for most species, there are probably manifold environ- summary, lubbers are generally immune to vertebrate predation, mental factors selecting for both large and small body size, during due to a combination of toxins and nocturnal roosting. each generation; and for many populations, body-size evolution may have already reached relative equilibrium under a balance of 3) Escape from vertebrate predation releases lubbers from small-size conflicting selective pressures (Thompson & Fincke 2002). However, selection, allowing them to evolve large size.— Most organismal traits when specific selective factors change in strength, we would expect are thought to be under conflicting selection pressures (Mayr 1956, natural selection to alter mean population trait values, given addi- 3In a different study, we observed loggerhead shrikes, Lanius ludovicians, tive genetic variance and heritability in these traits. We suggest that capture R. microptera grasshoppers and impale them on barbwire fences, this occurred in lubber grasshoppers. possibly as a sexual or territorial display. We did not observe consumption We hypothesize that the ancestors of lubber grasshoppers began of the fresh-caught grasshoppers (Yosef & Whitman 1992). feeding on vertebrate-toxic plants, which imbued them with chemi-

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Fig. 4. Anolis carolinensis lizard that has just vomited after swallowing a toxic R. microptera grasshopper nymph. This predator refused to attack subsequent lubbers. See Plate VIII.

cal defenses against many vertebrates. We further hypothesize that al. 2005, Okuyama 2007, Sloggett 2008). For example, hunting escape from vertebrate predation, due to the continued evolution spiders and other invertebrate predators favor small over large of ever more potent chemical defenses, altered the balance of size- grasshopper prey (Belovsky et al 1990, Ovadia & Schmitz 2002). selective forces, allowing lubbers to reach a new equilibrium for This is partially because capture efficiency declines and danger to body size. The reduction of a powerful selective force (vertebrate the predator increases, as prey size and strength increase beyond the predation) destabilized the previous balance between competing optimal prey-size range (Dixon 1959, Morris 1963, Stortenbeker selective forces, allowing lubber body size to increase over evolu- 1967, Dixon & Russell 1972, Wilson 1975, Griffiths 1980, Vermeij tionary time until directional selection for small size (Blanckenhorn 1982, Bailey 1986, Iwasaki 1991, New 1991, Reavy 1993, Cogni et 2000, Thompson & Fincke 2002) once again approximated that for al. 2002, Okuyama 2007). large size. Except in certain cases (such as in social or trapping predators A similar ecological release from predation is thought to be a – e.g., Enders 1975, Hölldobler & Wilson 1990, Kim et al. 2005, major factor favoring island gigantism in a wide range of taxa (Foster Souza et al. 2007), the vast majority of predaceous arthropods will 1964, Case 1978, Smith 1992, Lomolino 2005, but see Meiri et al. not, or cannot, successfully attack prey much larger than themselves 2006, Raia & Meiri 2006), including many island insects (Brindle (Shelly & Pearson 1980, Nentwig & Wissel 1986, Wheater 1988, 1970, Gibbs 1998, Priddel et al. 2003, Evenhuis & Eldredge 2004, Sabelis 1992, Cohen et al. 1993, Montllor & Bernays 1993, Matlock Bell et al. 2007). Population decline or extinction of these island 2005, Olberg et al. 2005). As Warren & Lawton (1978) suggest, giants, following introduction of new predators to their habitats, “Invertebrate predators usually eat prey of about their own size or support the hypotheses that, for invertebrate prey, large size is at a smaller . . .”. Those that occasionally attempt to capture large prey distinct disadvantage against vertebrate predators, and that lack of usually fail (Dixon & Russell 1972, New 1991), such as when ants predators can favor the evolution of large size (Brindle 1970, Gibbs attack large vertebrates, which simply move away. One might expect 1998, Priddel et al. 2003, Jones et al. 2005). Similar decreases in large predaceous arthropods to evolve larger sizes to make use of large zooplankters are seen when vertebrate predators (fish) are introduced prey; however, arthropod predators are under the same vertebrate to ponds (Roff 2002), reconfirming that vertebrate predators are predator-enforced small-size selection as other arthropods. generally a selective force for small size in invertebrate prey. The inability of predacious arthropods to take large prey is a Did acquisition of chemical defense in lubbers allow the evolu- weakness that can be exploited by any invertebrate prey species tion of large size? R. microptera and T. eques are perhaps the most that can evolve large body size. Insects are normally constrained poisonous grasshoppers in the USA (Whitman 1990), and are also from evolving large size, in part by increased liability to vertebrate the largest (Rehn & Grant 1959, 1961; Whitman 1988). Although predators. However, insect prey with effective antivertebrate predator correlation does not prove cause, our data (below) provide experi- defenses are released from this constraint, allowing them to evolve mental evidence to support our hypothesis linking large size with larger body size, which then reduces invertebrate predation. escape from vertebrate predators, as a consequence of chemical We tested the hypothesis that large size is an advantageous an- defense. tipredator trait in lubber grasshoppers. A full accounting of these experiments will be presented elsewhere, but we will provide a brief 4) Large body size is a highly beneficial antipredator trait in lubber description of the methods and results here. We tested wild ants grasshoppers.—Each invertebrate predator species generally attacks and birds in the field. For spiders, preying mantids, wheel bugs, prey within a certain size range (Holling et al. 1976, Pearson & and frogs, we used naive predators collected from the wild, and Mury 1979, Scarborough 1978, Dennis & Lavigne 1985, Warren then acclimated to laboratory conditions for several days. Trials & Lawton 1987, New 1991, Dixon & Hemptinne 2001, Olberg et JOURNAL OF ORTHOPTERA RESEARCH 2008, 17(2) JOURNAL OF ORTHOPTERA RESEARCH 2008, 17(2)

Fig. 5. Left: A naive Didelphis marsupialis opossum eating a toxic R. microptera grasshopper. Right: Same opossum vomiting after consum- ing several R. microptera grasshoppers. This predator refused all subsequent lubbers offered. Photos by Larry Orsak. See Plate VIII. began only after the predator routinely attacked and ate edible prey Table 2. Attack rate of Honga carolinensis wolf spiders on R. microptera (Acheta domestica crickets, Tenebrio molitor mealworms, Galleria mel- grasshoppers of different sizes and instars. Seven different spiders lonella wax-moth caterpillars, Musca domestica house flies,etc. ) that tested for each grasshopper size class; each spider tested once. were offered. In each laboratory trial, a single predator individual was allowed to acclimate to a single cage or arena. We then gently Grasshopper instar 1 2 3 4 5 Adult female introduced a single R. microptera grasshopper of a specific size, and N attacked 5 6 4 1 0 0 recorded if the grasshopper was or was not attacked. Table 1 shows size and mass for various R. microptera instars. classes. Mantids were not allowed to consume captured lubbers. We collected 42 wolf spiders, Hogna carolinensis (Lycosidae), by The results show that the mantids attacked significantly more of headlamps at night near Tifton, Georgia, and divided them into six the small grasshopper size classes than the large size classes (Table treatment groups, each balanced for body mass, which ranged from 3), and that larger mantids attacked larger lubbers (Spearman’s 0.30 to 1.72 g. Spiders were maintained in individual 1-L plastic rho = 0.675, df = 21, p < 0.001; Fig. 6) . Male and female mantids containers and given an adult cricket on the day of capture, and differed in the mean size of prey taken. Female mantids are larger water thereafter. Four days later, we introduced a single R. microp- (mean + SD: mass = 2.14 + 0.35 g; body length = 8.95 + 0.56 cm, tera grasshopper into the container and recorded if the spider did n=11) than males (mass = 1.38 + 0.19 g; body length 7.95 + 0.32 or did not attack the grasshopper during the next 15 min. Here, cm, n=10), and attacked larger prey than males (Mann Whitney U attack is defined as lunging at and covering prey with the fore-legs = 26.5, df = 20, p < 0.05). Male mantids refused to attack adult and anterior body. Each spider was tested once. Table 2 shows that lubbers, whereas female mantids attacked four lubber adults (Table the spiders refused to attack large, late-instar grasshoppers. In fact, 3). Some mantids exhibited threat or defensive behavior, but only spiders often fled from th5 -instar and adult grasshoppers. against large grasshoppers. We collected adult Chinese preying mantids, Tenodera aridifolia Two male mantids backed away from 5th instar lubbers, four near Normal, Illinois. Mantids were maintained in 4-L containers backed away or performed defense/threat displays to adult male lub- and fed various insects until testing began. Each of the 21 mantids bers, and four to adult female lubbers. In two cases, male mantids was tested with seven size classes of R. microptera over the course of attempted to fly away from approaching adult grasshoppers. Female 13 d. Mantids were offered grasshoppers on odd days and allowed mantids displayed defense/threat against one 5th instar, four adult to consume crickets, mealworms, wax-moth larvae or house flies males, and three adult female lubbers. Table 3 shows attacks; how- on even days. Each test consisted of introducing a R. microptera of ever, not all attacks were successful and larger-sized lubbers tended one of seven sizes (see Table 3) into the mantid’s container for 1 to escape mantid attacks more often. One male mantid dropped a h. Each mantid received a different sequence of grasshopper size captured 4th instar after the grasshopper raked its hind tibial spines

Table 1. Approximate body lengths (frons to abdomen tip) and Table 3. Attack rate by adult male and female T. aridifolia preying mass of various R. microptera instars. Note that both length and mantids against various sizes and stages of R. microptera grasshoppers. mass increase within each individual stadium. Eleven female and ten male mantids were offered all size classes of grasshopper, individually on different days. Mantids attacked Instar Body length (mm) Mass (g) significantly more of the small grasshopper-size classes than the large 1 11 0.07 size classes, and larger mantids attacked larger lubbers (Spearman’s 2 17 0.16 rho = 0.675, df = 21, p < 0.001; Fig. 6). 3 24 0.40 4 32 0.95 Grasshopper instar 1 2 3 4 5 Adult 5 40 1.95 No. prey attacked male female Adult male 48 2.33 Male mantids (N=10) 9 9 9 4 1 0 0 Adult female 58 4.88 Female mantids (N=11) 10 10 11 10 8 2 2

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Downloaded From: https://bioone.org/journals/Journal-of-Orthoptera-Research on 04 May 2020 Terms of Use: https://bioone.org/terms-of-use 358 DOUGLAS W. WHITMAN AND SHAWN VINCENT DOUGLAS W. WHITMAN AND SHAWN VINCENT 359 Table 4. Predation by 23 adult Arilus cristatus wheel bugs (Reduvi- Table 5. Ability of R. microptera grasshoppers of different sizes to idae) on R. microptera grasshoppers. Each bug was offered a 1st, 3rd, escape from disturbed fire ant (Solenopsis invicta) mounds. Ten and a 5th -instar grasshopper, at 3 to 6-d intervals, in a balanced grasshoppers tested for each instar. presentation. Bugs consumed significantly more of the smaller Instar 1 2 3 4 5 Adult male sized grasshoppers (1st and 3rd instars) than the larger, 5th instars No. escape 2 1 5 8 10 10 (χ2 = 19.7, df = 2, p < 0.001). Grasshopper instar 1 3 5 legs and head, rearing back, walking backwards or flying away from st No. prey consumed 18 12 0 an approaching grasshopper) to 1 instar lubbers, but eight bugs did to the approach of 5th instar lubbers. across the face of the mantid. The same result occurred with an We tested red imported fire ants, Solenopsis invicta (= wagneri), adult female mantid and an adult male lubber. Interestingly, only during a succession of sunny days in a pasture near Tifton, Georgia. two of the four attacks by female mantids on adult lubbers resulted Prior to the tests, we clipped (to within ~ 2 cm height) any weedy in capture; in two cases, the female’s raptorial legs bounced off of vegetation within 50 cm of the centers of the elevated, dome-shaped the hard cuticle of the grasshopper’s prothoacic shield. In other mounds, in order to remove visual obstructions. We started each unpublished tests, we have observed large captured lubbers struggle test by scraping off the top of a fire-ant mound, exposing a flat wildly, pulling, pushing, twisting, or kicking themselves free of a area of ~ 14 cm diameter. After ~ 10 s, when hundreds of ants had mantid grasp. In such cases, the mantid did not re-attack. moved to the exposed top of the mound, we then dropped three We tested 23 adult wheel bugs, Arilus cristatus, against three lubber R. microptera individuals of different instars onto the center of the size classes. Bugs (mean + SD body length and mass, female : 3.1 nest. This was repeated at different mounds until 10 grasshoppers + 0.14 cm, 0.83 + 0.16 g; male: 2.7 + 0.10 cm, 0.36 + 0.033 g) were of each of six size classes (five instars and adult males) were tested. captured in McLean Co., Illinois, and thereafter maintained in clear We recorded as “escape” those grasshoppers that were able to move 500-ml ventilated plastic containers and fed a variety of palatable at least 50 cm from the center of the hive, whether or not they still insects. Each bug was tested against three different R. microptera had ants on their bodies. Grasshoppers unable to move 50 cm were instars: 1st, 3rd, and 5th at three- to six-day intervals in a balanced recorded as “dead.” The results (Table 5) show that larger lubbers presentation sequence. Bugs were fed a cricket or wax moth larvae escaped more often from predaceous ants. then starved for 3 to 5 d, then tested. Each test consisted of placing We tested 22 northern leopard frogs, Rana pipiens, obtained one lubber in the bug’s container for 24 h. After the test, the bugs from a biological supply company, against various R. microptera were fed a palatable insect and starved again for 3 to 6 d prior to the instars and sizes. Frogs were maintained in individual 4-L plastic next round of testing. After each 24-h test, we recorded which bugs jars with water, during which they were fed crickets, then starved had eaten lubbers. Previous unpublished tests had demonstrated for two days prior to testing. Trials ran for 10 d. Each frog was of- that this species does not develop food-aversion conditioning fered a single R. microptera grasshopper on odd days and an adult toward lubber grasshoppers. The results (Table 4) show that the cricket on even days. Each frog received a different size-sequence bugs fed only on smaller-sized grasshoppers (χ2 = 19.7, df = 2, p < of grasshoppers, such that the presentation sequence of lubbers of 0.001). None of the 23 bugs consumed a 5th instar lubber, whereas various sizes was balanced. Previous work suggests that frogs do 18 consumed a 1st instar lubber. During our observations, no bugs not readily develop food-aversion conditioning to lubbers (Hatle performed threat or defensive displays (elevating fore body, front & Faragher 1998), and indeed, attack rates did not decline between

Fig. 6. Adult mantid (Tenodera aridifolia) body mass vs largest lubber size class (instars 1 to 5 or adult male or adult female) attacked. Mantids attacked significantly more of the small grasshopper size classes than the large-size classes, and larger mantids attacked larger lubbers (Spearman’s rho = 0.675, df = 21, p < 0.001). Open circles indicate male mantids and closed circles indicate female mantids. See Table 3.

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Table 6. Predation rate by northern leopard frogs, Rana pipiens on Table 7. Predation rate on various-sized R. microptera by wild, naive various sizes and stages of R. microptera grasshoppers. Twenty-two starlings and house sparrows at feeders. Four of each prey size of- frogs tested individually, each against five grasshopper size classes, fered. See text for additional methods. with each grasshopper offered individually, on alternative days, in Adult a balanced sequence. Grasshopper instar 1 2 3 4 5 male female Adult N prey attacked 4 4 3 1 0 0 0 Grasshopper instar 1 3 5 male female and removed as soon as feeding had occurred (13 min to 2.2 h). No. prey consumed 12 8 2 0 0 Overall, we tested at four locations, each at least 1.2 km from the others. We assume that each test involved a different flock of birds. the 1st and the last days of testing. The results (Table 6) show that, We tested at each site only once. In some cases we do not know which against frog predators, large lubbers enjoyed a significant survival species of bird ate or attacked lubbers, and so we have combined advantage over small lubbers. Over half of the 22 frogs attacked 1st the response for the two bird species. instar lubbers, but no frogs attacked adult lubbers and only two Table 7 gives the number of grasshoppers attacked (defined as frogs attacked 5th instar lubbers. wounded, missing body parts, gone from the feeder, or observed We tested wild, naive starlings, Sturnus vulgaris, and house spar- to be taken by a bird). The results show that large lubbers were not rows, Passer domesticus against R. microptera grasshoppers in Normal, attacked. Indeed, not a single 5th instar, adult male, or adult female Illinois. We first trained these birds to feed at a feeder on frozen- R. microptera was damaged. In contrast, nearly all small individuals then-thawed crickets, wax-moth larvae and mealworms, and 0.5-g were damaged, killed, or missing from the feeders during each of pieces of moist cat food. After two or three days, when the birds the four tests. These wild birds had probably never encountered repeatedly and aggressively fed at the feeder, we placed out three these grasshoppers, because lubbers do not exist in the midwest feeders, each separated by ~ 60 cm. One feeder contained one each of the USA. These, presumably naive, birds sampled lubbers, even of a living 1st, 2nd and 3rd-instar R. microptera, tied to the feeder by though this prey is warningly colored and chemically defended. thin strings. The 2nd feeder contained a live 4th and a live 5th-instar In all of our experiments, testing seven different predator species grasshopper, and the 3rd feeder contained a live-tethered adult male from different taxa (spider, preying mantid, wheel bug, ant, frog, and adult female grasshopper. We separated the lubber size classes starling and sparrow), large lubber instars enjoyed a highly significant onto different feeders because trials a year earlier showed that the advantage against predation: predators tended to attack or overcome birds were hesitant to approach the feeders containing adult grass- smaller size classes of lubber grasshoppers, but refused to attack or hoppers. Wariness in birds increases with prey size (Gamberale & failed to overcome large-sized lubbers. These data demonstrate a Tullberg 1998). The feeders were placed out at dawn and inspected strong advantage for large body size for lubber grasshoppers against

Fig. 7. Adult R. microptera grasshoppers are simply too large for some small vertebrate predators to attack. See cover.

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Fig. 8. Body length distributions for grasshopper species (females only) from various geographic areas. See Table 8 for sources of data. “Southern Africa & Madagascar” includes Congo, Angola, and Madagascar. Among the ~13,000 species of grasshopper (Orthoptera Species predators. Most surprising is that larger lubber body size decreased File), adult body mass ranges across three orders of magnitude, both invertebrate and vertebrate predation. As such, our results suggest length by 1.5 orders of magnitude: from ~ 15 mg and 5 mm for that large size in an insect can be an antipredator defense, against tiny adult male Illapelia penai from South America (Carbonell & both vertebrate and invertebrate predators (Fig. 7). Mesa 1972), to 30,000 mg and ~ 120 mm (head to tip of abdomen, and 145 mm (to wing tip) for the largest female individuals of 5) Chemically defended grasshoppers are generally larger than their non- Tropidacris cristata from Central and South America (Uvarov 1966, chemically defended relatives.—We wanted to know if large body size was associated with chemical defense in other grasshopper spe- 4We tabulated “body length” from various sources. However, different authors cies, and therefore we compared body sizes of chemically defended recorded body length in different ways (i.e., fastigium to tip of abdomen vs fastigium to tip of hind femora vs fastigium to wing tip), and it is not grasshoppers to those of grasshopper species that lack chemical always clear which method they used. Most measurements are probably defenses. We obtained body-size data for female grasshoppers from based on dried museum specimens, which are shorter than live specimens. various faunal monographs and field guides, and present the data In addition, grasshopper masses and lengths vary widely geographically, here as geographic or taxonomic summaries (Figs 8-10, Table 8). annually, seasonally, with local environmental conditions, and in females, We also list all the grasshopper species known or suspected by us during the gonotrophic cycle. Also, nomenclature changes over time, and the taxonomic designation for many of the early descriptions for size or to be chemically defended (see Whitman 1990), and provide size chemical defense are questionable. Hence, our data can only be considered and mass data when available (Table 9).4 as the best current estimate of the situation.

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Downloaded From: https://bioone.org/journals/Journal-of-Orthoptera-Research on 04 May 2020 Terms of Use: https://bioone.org/terms-of-use 362 DOUGLAS W. WHITMAN AND SHAWN VINCENT DOUGLAS W. WHITMAN AND SHAWN VINCENT 363 all grasshopper species are under 1 g and 4 cm (Table 8, Figs 8-10). By comparison, the females of most of the ~ 40 known chemically defended species of grasshopper (from among seven subfamilies) are heavier than 2 g and longer than 4 cm (Fig. 9, Table 9). Figure 9 gives female body sizes for some pyrgomorphids from Africa and Thailand, and also for USA Melanoplinae; chemically defended species are designated in grey. Note that in each case, the chemically defended species sort to the larger-sized classes. Thus, chemically defended grasshoppers tend to be larger than nonchemically defended grasshoppers. A problem in our analysis is that many palatable grass-mimicking grasshoppers are very long, thus weakening the correlation between chemical defense and body length. However, such grasshoppers weigh substantially less than chemically defended grasshoppers, which tend to be robust and heavy. Mass is a better metric than length for predicting ecological interactions, in part because mass scales as the cube of length for isometric bodies (Peters 1983, Calder 1996). Hence, a doubling of body length would increase volume and mass by eight times, for individuals with the same relative dimensions. Although chemically defended grasshoppers may be only somewhat larger than palatable grasshoppers, they are substantially heavier. Unfortunately, grasshopper fresh-body masses are difficult to come by. However, Pfadt (1994) gives fresh adult mass for 30 common Western USA species (Fig. 10). Of these, the greatest mean female mass was 1.65 g, and females of only three species exceeded 1.0 g. In comparison, median wet masses for females of chemically defended grasshoppers center around 4 to 5 g (Table 9). Another problem is our incomplete knowledge of chemical defenses among grasshoppers. Many chemically defended species are yet to be discovered, and in many cases we only have strong, not conclusive, evidence for chemical defense. For example, the largest grasshopper known, T. cristata (see above), is probably chemically Fig. 9. Top: body-length distributions for grasshopper species (fe- defended, as they (and some other Romaleinae – including Tropid- males only) for African and Thai Pyrgomorphidae, including from acris, Chromacris, and Taeniopoda; see Table 9) possess many of the North Africa (Chopard 1943), Congo (Dirsh 1970), Angola (Dirsh traits characteristic of the chemical defense syndrome (Whitman et 1966), Madagascar (Dirsh 1963), and Thailand (Roffey 1979). Bot- al. 1985): they feed on toxic plants, and the nymphs aggregate and tom: female body-length distribution for USA Melanoplinae from flaunt bright (presumably warning) colors (Rowell 1983, Carbonell Capinera et al. 2004. In each case, known chemically defended 1986, Whitman unpub.). Locust species, two of which have been species are designated in grey, and nonchemically defended spe- found to be chemically defended when in the gregarious, swarm- cies in white. ing, phase (Sword 1999, Despland & Simpson 2005, Simpson & Sword 2009), also tend to be large and heavy (Uvarov 1966, 1977). Rowell 1983, Carbonell 1986). In general, grasshopper mass, shape, Some larger-bodied locust species, Proscopiidae, Pyrgomorphidae, and length vary with family, latitude, and life form, with the largest Pamphagidae and Romaleinae may likewise be chemically defended species usually inhabiting warmer climates (Uvarov 1966, 1977). (Schultz 1981, López et al. 2007), but we will not know until careful Ground-dwelling, “terricolis” grasshoppers tend to be robust and predator-feeding trials are completed. heavy, and grass-mimicking species (e.g., Acrida, Achurum) tend to In summary, large size appears to be correlated with chemical be long, thin and light. defense in grasshoppers. And, as our results demonstrate, large However, even with such wide background variability in size, size in an insect can deter invertebrate predation. This supports shape, and mass among grasshoppers, there are striking trends the hypotheses that large size is beneficial for chemically defended related to chemical defense. First is that the majority of females of Table 8. Percentage of grasshopper species with females under 4-cm body length for different geographic regions. Location N Percentage of Reference females < 4.0 cm Europe 332 90 Harz 1975 USA & Canada 233 88 Capinera et al. 2004, Vickery & Kevan 1985 New Zealand 15 87 Bigelow 1967 USSR & adjacent areas 977 85 Bei-Bienko & Mishchenko 1963, 1964 Japan 119 84 Ichikawa et al. 2006 North Africa 205 75 Chopard 1943 Southern Africa & Madagascar 751 73 Dirsh 1962, 1963ab, 1966, 1970 Thailand 56 71 Roffey 1979 JOURNAL OF ORTHOPTERA RESEARCH 2008, 17(2) JOURNAL OF ORTHOPTERA RESEARCH 2008, 17(2)

Downloaded From: https://bioone.org/journals/Journal-of-Orthoptera-Research on 04 May 2020 Terms of Use: https://bioone.org/terms-of-use 362 DOUGLAS W. WHITMAN AND SHAWN VINCENT DOUGLAS W. WHITMAN AND SHAWN VINCENT 363 We further propose that large size is a common antipredator trait among chemically defended insects. Chemically defended insects often possess a suite of characteristics that are diametrically oppo- site to those of nonchemically defended insects (Salazar & Whit- man 2001). This ensemble of traits has been named the Chemical Defense Syndrome (CDS), and includes chemical defense, visual, chemical, and/or mechanical (tactile or auditory) warning signals (aposematism) and threat displays, aggregation, exposed diurnal behavior, flightlessness, sluggishness, and large size (Whitmanet al. 1985, Yosef & Whitman 1992, Salazar & Whitman 2001). Not all chemically defended insects exhibit all of these traits, but enough do to validate the principle. Various components of the CDS have been thoroughly examined (Ruxton et al., 2004), such as chemical defense (Blum 1981, Whit- man et al. 1990, Eisner et al. 2005), aposematism (Guilford 1990, Prudic et al. 2007), aggregation (Vulinec 1990, Costa 2006), and sluggishness (Hatle & Whitman 2001, Hatle et al. 2002). However, large size as a component of the CDS has received little attention, despite its apparent common association with chemical defense across numerous insect orders (Pasteeles et al. 1983), and the fact that the efficacy of warning coloration increases with body size (Nilsson & Forsman 2003). The consequences of this association are not trivial: the presence or absence of chemical defense may be an important factor in body size evolution in insect prey (Forsman & Merilaita 1999). In fact, just the presumption of chemical defense may be enough to influence body-size evolution, such as in those Batesian mimics that lack chemical defenses, but mimic large insects that do. An example may be seen in the barklice (Psocoptera), nearly all of which are cryptic and < 5 mm long (Mockford 1993), except for a group of giant-bodied (up to 11.5-mm long) Psocoptera from Central America that apparently mimic assassin bugs and wasps (Mockford 1992). Fig. 10. Body-mass distribution for 31 species of grasshopper from Whether these giant barklice are actually chemically defended or the western USA. Top: males. Bottom: females. Nearly all are <1g. are only mimics is unknown. However, the important ecological Data from Pfadt 1994. and evolutionary reality is that they appear to be defended, and as grasshoppers and that escape from vertebrate predation (via chemi- a result presumably suffer less predation and less selection for small cal defense) allows some grasshoppers to evolve large size. size. Another feature of many species of chemically defended grasshop- General discussion pers is that (like lubbers), their chemical defenses often work better against vertebrate predators than invertebrate predators (Whitman Copious evidence suggests that predation can be a strong se- 1990). For example, both birds (Descamps & Wintrebert 1966) lective force on prey morphology (Kittlewell 1973, Swain 1992, and humans (Steyn 1962) have died after eating toxic Phymateus Heinrich 1993). Although large size is perhaps the most successful grasshoppers. Euw and coworkers (1967) calculated that a single defence in vertebrates (e.g., elephants and rhinos), large body size Poekilocerus bufonius contained enough cardenolide to kill a cat. has seldom been considered as an antipredator defense in insects. Greg Sword experienced golf-ball sized lymph nodes after consum- However, our results show that large lubber size is highly beneficial ing a single Schistocerca emarginata grasshopper (Sword 2000), and against both invertebrate and vertebrate predators, and thus serves we thank him for his personal commitment to understanding the as a defensive trait. dynamics of chemical defense in Orthoptera. In our trials, the largest lubber grasshoppers were relatively im- Of course, there is great variability among the interactions of mune to predation. Note that we selected as test predators, the largest the ~ 40 known chemically defended grasshopper species and their wolf spider (Honga carolinensis), largest mantid (Tenodera aridifolia), > 200,000 species of potential predators. However, for those pro- and the largest reduviid species (Arilus cristatus) in the USA, as well tected species that have been thoroughly studied, there are usually as a very aggressive ant species (Solenopsis invicta). Presumably, lub- several species of invertebrate predator that are not deterred by the bers would enjoy even greater protection against the more common chemical defenses of the grasshopper (Whitman 1990, Sword 2000). smaller and less aggressive invertebrate predators that share their Insect chemical defenses may have evolved primarily against birds habitats. In addition to size-escape from invertebrate predation, our (Pasteels et al. 1983, Brower 1984, Rothschild 1985), and chemical results show that large lubber size can deter vertebrate predators as defense in grasshoppers may have evolved primarily against verte- well (Tables 6, 7). As such, lubbers have come to occupy a relatively brate predation. predator-free niche. Our results suggest a broader evolutionary theme. The evolu- We suggest that large size in lubber grasshoppers evolved as a tionary path of a species is guided by phylogenetic and ecological direct consequence of chemical defense against vertebrate predators. constraints. Major evolutionary changes and rapid speciation and

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Table 9. Body sizes of chemically defended grasshoppers. Note that females of most species >2g and 4 cm. * no sex specified.

SUPERFAMILY Body mass (g) Body length (mm) Reference Family male female male female Subfamily species PAMPHAGOIDEA Pyrgomorphidae Orthacridinae Colemania sphenarioides – – 39 36 Coleman 1911 Pyrgomorphinae Attractomorpha crenulata – – 16-19 23-26 Roffey 1979 Aularches milliaris (=punctus, scabiosus) – – 37-55 47-69 Katiyar 1955, Roffey 1979 Dictyophorus griesus (=laticincta, oberthuri, productus) 4.1* 39-52 41-65 Bateman & Fleming 2008 Dictyophorus spumans – – 47-49 48-70 Johnsen 1990 Maura rubroornata (=rugulosa) – – 22-24 34-38 Dirsh 1966 Monistria concinna – – <28 <47 Key 1985, Groeters & Strong 1993 Monistria discrepans – – <20 <41 Key 1985 Monistria pustulifera – – <30 <53 Key 1985 Petasida ephippigera – – <53 <60 Key 1985 Phymateus baccatus – – 44-57 65-80 Johnsen 1990 Phymateus iris – – 42-46 60-70 Dirsh 1970 Phymateus aegrotus (=hildebrandti) – – – – Phymateus leprosus – – 70* Bishop 1940, M. Samways, pers. comm. Phymateus madagassus – – 43-51 55-75 Dirsh 1963 Phymateus morbillosus 3.6 12.3 55 77 Gäde 2002 Phymateus saxosus – – 43-55 64-73 Dirsh 1963 Phymateus viridipes – – 50-61 62-85 Johnsen 1990 Physemophorus socotranus – – Phyteumas (Phymateus) purpurascens – – – < 90 Rowell 1967 Poekilocerus bufonius – – 33-40 44-68 Fishelson 1960 Poekilocerus hieroglyphicus – – 41-43 55-60 Chopard 1943 Poekilocerus pictus 2.1 4.1 43-50* Delvi & Pandian 1979 Pyrgomorpha conica – – 15-18 22-30 Chopard 1943 Rubellia nigrosignata – – 18-25 27-28 Dirsh 1963 Taphronota calliparea (=cincta) – – 23-40 34-51 Johnsen 1990 Taphronota occidentalis – – – – Zonocerus elegans 1.6* 32-45 38-51 Dirsh 1966, Bateman & Fleming 2008 Zonocerus variegatus 1.0 1.8 28-37 33-47 Phipps 1962, Kaufmann 1965, Dirsh 1966 Pamphagidae Pamphaginae Eunapiodes granosus – – 33-44 50-60 Chopard 1943 ACRIDOIDEA Romaleidae Romaleinae Chromacris colorata – – – – Chromacris pedes – – – – Chromacris speciosa – – 31 – Radclyffe Roberts & Carbonell 1982 Romalea microptera 1.5-6.9 2.1-18.5 41-70 50-90 Rehn & Grant 1961, Whitman, unpubl. Taeniopoda eques 0.8-2.8 2.3-8.3 33-58 40-71 Hebard 1925, Whitman, unpubl. Taeniopoda reticulate – – 43-52 54-70 Hebard 1925 Tropadacris cristata < 30..0* 60 83 Uvarov 1966, Rowell 1983, Carbonell 1986 Tropadacris collaris (=grandis) – – 72 89 Carbonell 1986 Acrididae Catantopinae Eupropacris cylindricollis (=ornate) – – 23-26 30-39 Dirsh 1966, Preston-Mafham 1990 Melanoplinae Dactylotum bicolor – – 21 32 Capinera et al. 2004 Dactylotum variegatum – – 22 32 Capinera et al. 2004 Cyrtacanthacridinae Schistocerca emarginata (=lineate) – – 23-35 30-50 Helfer 1953 Schistocerca gregaria 1.5-2.3 1.9-3.6 42-50 48-58 Dudley 1961, Dirsh 1966

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Downloaded From: https://bioone.org/journals/Journal-of-Orthoptera-Research on 04 May 2020 Terms of Use: https://bioone.org/terms-of-use 364 DOUGLAS W. WHITMAN AND SHAWN VINCENT DOUGLAS W. WHITMAN AND SHAWN VINCENT 365 diversification follow those rare breakthroughs when a taxon al. 2007), larger species or instars can often generate strong forces eliminates a constraint. Body size, as all organismal traits, is under during defensive kicking or biting behaviors. For example, another conflicting selection pressures, with some factors selecting for small large bodied lubber grasshopper, Brachystola magna, can bite through and others for large size. A change in strength or direction in any human skin, and can employ its spiked hindlegs during defensive one factor can alter the overall balance between these competing kicking bouts to generate upwards of 25 Newtons of force, enough selective forces, pushing (or allowing) the population to evolve to pierce the integument of some vertebrate and invertebrate preda- until a new equilibrium body size is reached. Such a process might tors (Vincent, pers. obs.). All of these factors should select for larger explain some cases of island gigantism (Evenhuis & Eldredge 2004, insect size. However, the fact that insects as a group remain small Lomolino 2005, Bell et al. 2007), the loss of pigment and eyes in (Blanckenhorn 2000, Whitman 2008) suggests that the disadvan- cave-dwelling species (Culver 1982), the loss of flight and defensive tages of increasing size generally outweigh the advantages. behavior in island-dwelling birds (MacArthur & Wilson 1967) and In this paper we propose that lubber grasshoppers evolved chemi- the correlation of defense mechanisms with predator sympatry, but cal defense prior to large size. However there are other scenarios not allopatry (Jones et al. 1978, Endler 1985). for the evolution of size and defense in lubbers. Perhaps lubbers In some cases, ecological or behavioral change stimulates a ben- evolved large size first, which exposed them to increasing predation eficial evolutionary breakthrough, which then alters overall selection from vertebrates and placed them under strong selection to develop dynamics, releasing a cascade of new evolutionary events. Such an antivertebrate chemical defense. Hence, maybe chemical defense is “accidental” or serendipitous evolutionary breakthrough may lead to a result of large size and not vice-versa. rapid increases in population density and range, speciation and radia- Our results also confirm that predator threat changes with prey tion. Examples might include the evolution of lungs, flight, sociality, ontogeny, as in other insects (Dempster 1967, Stortenbeker 1967, or chemical defense – all presumably beneficial traits that dramati- Feeny et al. 1985, Dixon & Baker 1988, Belovsky et al. 1990, Medina cally alter overall selection dynamics, leading to multiple changes in & Barbosa 2002). For many insect prey, invertebrate predators numerous other traits (e.g., Schmidt 1990). For example, chemical attack the smallest instars or species, and vertebrate predators the defense may be a prerequisite for the evolution of insect sociality larger instars or species (Watanabe 1976, 1981, Montllor & Bernays (Starr 1985, Kukuk et al. 1989), or the many components of the CDS. 1993). This is well documented in grasshoppers (Stower & Greathead Perhaps the evolution of chemical defense in lubber grasshop- 1969, Chapman & Page 1979, Belovsky et al 1990, Belovsky & Slade pers was a breakthrough adaptation that sent them down a different 1993), where smaller instars usually suffer higher rates of predative evolutionary pathway, and set in motion a series of subsequent mortality than later (larger) instars (Stortenbeker 1967, Cherrill & evolutionary events that profoundly altered their physiology, mor- Begon 1989, Danner & Joern 2003), and where predator species phology, behavior, life-history, and ecology. This could have started change with grasshopper growth (Stortenbeker 1967; Belovsky et when their cryptic and palatable ancestors encountered and fed on al. 1990; Danner & Joern 2003, 2004). In lubbers, if the smaller, a vertebrate-toxic plant, which filled the insect’s gut and oral and earlier instars suffer higher predation rates than the larger, later anal discharges with deterrent substances, causing reduced predation instars, then we might expect selection for large egg size and rapid on that population (e.g., Jones et al. 1988, Sword 2001, Calcagno et growth (Paine 1976, Arendt 1997) of the small early stages. This al. 2004). Continued directional selection by predators could have may be the case for lubbers, which have one of the largest egg sizes then selected for specialization on toxin-providing food plants, and known for grasshoppers (1 cm long and up to 43 mg fresh mass), greater defensive capabilities (e.g., Jones et al. 1988, Dopman 2002), and which are black as nymphs, which aids solar heating, growth, including all the traits of the Chemical Defense Syndrome (Whitman and development (Whitman 1987, 1988). et al. 1985), such as aposematism, threat displays, gregariousness, Lastly, we previously mentioned that predator-prey interac- flightlessness, sluggishness, and large size. Similar arguments have tions are exceedingly complex. Because of such complexity, there been made for other chemically defended groups (e.g., Schmidt are exceptions to nearly every generality that we have discussed. 1990 for Hymenoptera). Hence, some small invertebrate prey are more conspicuous, more Hence, the key evolutionary event for lubber grasshoppers may nutritious, and less agile than some large invertebrate prey species. have been feeding on toxic plants, which increased defense against Some vertebrates prefer smaller invertebrate prey, some invertebrate vertebrate predators, thus favoring the evolution of stronger chemi- predators can capture large prey (Lorenz 2007), some chemically cal defenses. Escape from vertebrate predation (via toxins), released defended prey are quite small (Pasteeles et al. 1983), and some lubbers to evolve large body size, which then allowed them to escape palatable insect prey are large. Furthermore, previous authors have from invertebrate predation via mechanical defense (large size). As anecdotally noted the defensive benefits of large body size in inver- such, the size difference between chemically defended lubber grass- tebrates, such as shellfish (Roff 2002), or documented the associa- hoppers and their palatable relatives, represents the magnitude of the tion between chemical defense and large size in insects (Pasteeles evolutionary force of vertebrate predation on grasshopper body size. et al. 1983). However, we believe that overall, the generalities and Of course large size has many benefits, including perhaps greater principles proposed here are valid. mating success, fecundity, homeostasis, an ability to consume tough food, dominate intraspecific competitors, and for grasshoppers, to Acknowledgements lay egg pods deeper to thwart egg predators and parasitoids (Peters 1983, Andersson 1994, Calder 1996, Vincent 2006, Stauffer & Whit- We thank Shin-Ichi Akimoto, Robert Alexander, Corey Baze- man 2007, Whitman 2008). Another reason large body size may be let, Murray Blum, Clive Jones, Robert Dudley, David Eades, Jahir advantageous as an antipredator mechanism in insects is because it Hussain, Shajahan Johny, Michel Lecoq, Daniel Otte, My Hanh strongly covaries with the strength of mechanical defenses such as Luong-Skovmand, Michael Samways, Melissa Stauffer, Tim Stauffer, biting or kicking (Norman 1995, Burrows & Morris 2003, Vincent Yoshikazu Sugano, and Gregory Sword for providing data, advice, 2006, Vincent & Lailvaux 2008). Whereas small insects must rely or assistance. on crypsis or rapid-escape behaviors to avoid predation (Dangles et

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