Behavioral Ecology doi:10.1093/beheco/arr045 Advance Access publication 4 May 2011

Original Article Failure to launch? The influence of limb autotomy on the escape behavior of a semiaquatic grasshopper Paroxya atlantica (Acrididae)

Philip W. Batemana,b,c and Patricia A. Flemingb aDepartment of Zoology and Entomology, University of Pretoria, Pretoria 0002, South Africa, bSchool of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, WA 6150, Australia, and cArchbold Biological Station, Lake Placid, PO Box 2057, Lake Placid, FL 33862, USA Downloaded from Autotomy is an extreme escape tactic where an animal sheds an appendage to escape predation. Many species alter their behavior postautotomy to compensate for this loss. We examined the escape behavior in the field of a semiaquatic grasshopper (Paroxya atlantica) that could escape either by flight and landing in vegetation or flight and landing in water and swimming to safety. We predicted that animals missing a hind limb would be more reactive (i.e., have longer flight initiation distances; FID) and would beheco.oxfordjournals.org prefer to escape to vegetation rather than to water as loss of a limb is likely to reduce swimming ability. However, our predictions were not supported. FID in autotomized animals was not different from that in intact animals. Furthermore, although autotom- ized grasshoppers paused more often and swam slower than intact individuals, autotomized grasshoppers more often escaped to water, reaching it via shorter flights that were lateral to the approach of the observer (intact grasshoppers more often flew directly away from the observer). We also noted differences in behavior before disturbance: Autotomised animals perched lower on emergent vegetation than did intact ones, presumably in readiness for escape via water, and also showed a greater likelihood to at Murdoch University on June 19, 2011 hide (squirreling) from the approaching observer prior to launch into flight. It seems likely that the reduced flight distance and greater propensity to land in water for autotomized P. atlantica may reflect a failure to launch from their perch due to loss of a jumping back leg. Key words: distance fled, escape tactics, escape trajectory, flight initiation distance, Orthoptera, predation risk. [Behav Ecol 22:763–768 (2011)]

INTRODUCTION becoming alert to approaching threats and monitoring them until deciding to retreat to their burrows. Furthermore, Wong here is an extensive and growing body of research on et al. (2005) found that fiddler crabs (U. pugilator) would often predator-induced flight behavior of multiple taxa. At the T retreat to burrows if they saw conspecifics reacting to threats, heart of these studies is the optimal escape theory of Ydenberg and Dill (1986), which predicts that animals should even if they did not see the threat themselves. FID of wolf spi- balance costs and benefits of fleeing from an approaching ders (Hogna carolinensis) is shorter for slower individuals, sug- predator, moving when costs of escaping are equal to costs gesting that slower spiders rely more on crypsis than do faster of not fleeing. Subsequent research on flight optimization individuals (Nelson and Formanowicz 2005). Cooper (2006) behavior has examined the influence of many variables on examined the flight behavior of the acridid grasshopper Dissos- flight initiation distance (FID) (often relying on the observer teira carolina in the field and found that predator approach as the predator), including distance to refuge, distance to speed, directness of approach, and repeated approach influ- conspecifics, sex, sexual, or ontogenetic differences in ence flight behavior. These studies demonstrate that inverte- camouflage, previous experience with predators, speed of brate behavior conforms to antipredator escape decision approach of the predator or number of predators (see theory (Ydenberg and Dill 1986), suggesting a broad applica- Stankowich and Blumstein 2005; Cooper and Frederick bility to invertebrates as well as vertebrates. 2007; Stankowich 2008 for reviews and discussion). Although there is an extensive literature on antipredator es- Although much of the research published on threat reaction cape studies, one aspect that has not received a great deal of and predator escape behavior is biased toward vertebrates, attention to date is the potential effect of compromised state a number of studies have examined invertebrate models. on escape behavior (Stankowich 2009; Cooper and Frederick Hemmi (2005a, 2005b) found that fiddler crabs (Uca vomeris) 2010). Autotomy, the voluntary shedding of a body part, react to threats in much the same way as do vertebrates, usually in response to predation, is observed in a variety of invertebrate and vertebrate (particularly lizard) taxa (Fleming Address correspondence to P.W. Bateman. E-mail: pwbateman@ et al. 2007; Bateman and Fleming 2009). The autotomy of zoology.up.ac.za. a body part allows escape from a predator, but this escape Received 8 April 2010; revised 17 January 2011; accepted 31 comes at a cost, for example, loss of fat stores, locomotory January 2011. ability, intraspecific competitive or mate attraction ability, com- promised foraging, increased vulnerability to attacks, etc. (see The Author 2011. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: [email protected] 764 Behavioral Ecology

Clause and Capaldi 2006; Maginnis 2006; Fleming et al. 2007; MATERIALS AND METHODS Bateman and Fleming 2009 for recent reviews). Autotomy is Populations of P. atlantica were found in isolated patches of a good model mechanism to examine flight decision optimi- reed and long emergent grasses around a small suburban lake zation because comparisons can be made between intact (i.e., (circumference ’1.3 km) in central Florida, USA. The ‘‘unharmed’’) individuals and autotomized animals that have waterside vegetation was fragmented by beaches and mown undergone a nonfatal ‘‘wounding.’’ sections of lawns, but P. atlantica were frequent all around There are 3 reasons to expect that autotomized individu- the lake except on bare sand. als may demonstrate different antipredator behavior com- Grasshoppers were found by listening for stridulation and pared with their intact conspecifics: firstly, once a body part scanning emergent vegetation with binoculars. Once located, has been lost, the animal cannot then use autotomy of that each grasshopper was examined through binoculars to see if body part as a defense in a future encounter (until such it had autotomized a rear hind leg. This method was only time as the body part regenerates, if it does) (Arnold occasionally successful, and so the individual was followed 1988). Secondly, a number of studies have demonstrated that autotomy of a body part (caudal lamellae, limb, or tail) onceithadfledandeithercaughtorexaminedatclose compromises locomotion (reviewed by Fleming et al. 2007; range which had the advantage that the majority of data Bateman and Fleming 2009). For example, in invertebrates, up to that point were collected ‘‘blind’’ to the animals’ con- damselfly nymphs face a significant reduction in swimming dition. Data from any grasshopper that could not be speed after autotomy of a caudal lamella or even experimen- followed and definitively identified as ‘‘intact’’ or tal reduction in lamella size (Robinson, Hayworth, et al. ‘‘autotomized’’ were discarded. Of the 57 individuals exam- 1991; Burnside and Robinson 1995; McPeek et al. 1996; ined, 29.8% (17) were identified as missing a hind limb, but Stoks 1999b; Gyssels and Stoks 2005). Loss of a single leg unlike a field population of G. bimaculatus (Bateman and in some harvestmen and spiders does not reduce sprint Fleming 2005), no grasshoppers were found missing front or middle legs or both hind legs. speed but loss of 3 does (Guffey 1999; Amaya et al. 2001; Downloaded from Brueseke et al. 2001; Apontes and Brown 2005). Loss of The vegetation thinned from the shore into the water, and it a single leg, however, reduces stick insect mobility (Carlberg was difficult to locate and approach grasshoppers in the 1984) or reduces running speed in the gryllid crickets Gryl- thickest parts of the vegetation as the reeds and grasses (which were over 1 m in height) bent toward the focal animal as the lus bimaculatus and Acheta domesticus (Bateman and Fleming beheco.oxfordjournals.org 2005, 2006a) and increases energetic costs of locomotion in observer (P.W.B.) approached, influencing FID. Therefore, G. bimaculatus (Fleming and Bateman 2007). Locusts only grasshoppers in the more sparse emergent vegetation (Schistocerca gregaria) show a 40% decrease in energy re- were approached (a ;10 m band around the shores of the leased when jumping after the loss of a hind leg and lake). This meant that all these grasshoppers were above water a 27% decrease in distance jumped (Norman 1995). but surrounded by vegetation. Following a slightly modified

Thirdly, animals that have lost a body part have already version of Cooper’s (2006) methodology, the observer at Murdoch University on June 19, 2011 experienced an attempted predation event. Autotomy of approached a grasshopper by wading slowly within the a limb can lead to lasting changes in any behavior that vegetation parallel to the open water. At a distance of about may further expose the autotomized individual, as has been 5 m from the grasshopper, the observer stopped, waited for shown for latency to emerge and to resume calling after a few seconds and then approached slowly, taking small, disturbance in G. bimaculatus (Bateman and Fleming shuffling steps so that the water did not surge forward, and 2006b). move the emergent vegetation unduly. No grasshopper was The semiaquatic grasshopper Paroxya atlantica is a com- observed to react to the observer at distances greater than mon acridid in southeastern USA. It is often found in veg- 5 m. Average speed was approximately 0.2 m/s. All ap- etation on the edge of slow-moving water (Capinera et al. proaches took place around midday on sunny days in August 1997). When disturbed it acts much like any other grasshop- and early September to reduce the effect of solar angle and to per species in that it can jump or fly away from the ap- ensure little variation in temperature (range for observation proaching disturbance, or ‘‘squirrel,’’ that is, flip round to days 26–32 C). the other side of the plant stem on which it is perched, away Once a grasshopper was sighted, its perch height above the from the approaching disturbance (Morse 1893). When water surface was noted (and marked with a piece of twine once they then jump or fly, they either land on the ground or the grasshopper had fled and later measured with a meter rule, a plant stem or in water where they swim by kicking vigor- along with stem height: from water surface to tip). Starting ously with their back legs until they reach a plant stem point was recorded to later measure starting distance emerging from the water surface (Bateman PW, personal (distance from focal animal when commencing approach). observation). As the focal animal was approached, some would squirrel The aims of this study were to examine the effects of limb around to the other side of the plant stem; this was noted autotomy on antipredator behavior in a field population of and the distance later measured (squirrel distance: distance P. atlantica. We tested the following predictions: from observer when the grasshopper moved, recorded with 1. Autotomized individuals would perceive greater risk a meter rule). Closer advance initiated flight in all individuals, from an approaching ‘‘predator’’ (the observer) due to and the FID (distance from observer when the grasshopper their compromised locomotory capacity and altered took flight) was recorded by sticking a bamboo pole in the state and would therefore be more reactive (move away ground at that point and later measuring the distance with when the observer was at a greater distance, i.e., longer a tape. Grasshoppers could escape by jumping and flying away FID). from the observer’s approach at any angle. Following Cooper 2. Compromised locomotion of autotomized P. atlantica (2006), angles were recorded using a protractor on a 180 would result in their flying shorter distances than intact scale such that 180 represented directly away from the individuals. observer’s approach (and therefore parallel to the shore 3. Swimming would be compromised by loss of a leg, and on one side and the lake on the other), whereas 90 repre- therefore, autotomized P. atlantica would be less willing sented escape lateral to the observer’s approach. The distance to escape via water and would perch higher in vegetation moved (from initial perch site to estimated point of landing) to allow better launch into flight (to clear the water). and landing location (either in water or on vegetation) were Bateman and Fleming • Autotomy and escape behavior 765 recorded. Any grasshoppers approached where not all these data could be collected were discarded from analyses. To record swimming speed under controlled conditions, 24 intact grasshoppers were captured by hand and netting. Within 2 h of capture, half of the grasshoppers (chosen randomly) had their right rear leg autotomized by briefly pinching it with forceps. All grasshoppers were kept over- night in individual glass jars with perforated lids and given lettuce seedlings for food. At midday the following day, the swimming ability of each grasshopper was tested by placing it at one end of a clean plastic tub (1 3 0.75 m) filled with rainwater. All grasshoppers began to swim immediately. The time taken to swim the length of the tub was recorded along with a number of pauses requiring the experimenter to prompt the grasshopper with the tip of a narrow bamboo pole. All grasshoppers were tested only once and then re- leased at the site of capture. 2 The proportions of individuals were compared by vdf analyses. The proportion of animals that landed on grass or in the water was compared with expected values calculated assuming that the proportion of individuals landing on each substrate was equal between autotomized and intact Figure 1 Although vegetation stems were the same height, intact Paroxya P. atlantica. The proportions of P.atlantica that squirreled was atlantica perched higher on the stems than autotomized animals. Downloaded from similarly analyzed comparing actual numbers with expected Letters link data that are not significantly different from each other values calculated assuming that the proportion of individuals at P , 0.05 (separate analyses were carried out for stem height and squirreling or not was equal between autotomized and intact perch height).

animals. Stem and perch heights, distances moved, and swim- beheco.oxfordjournals.org ming speed were compared between intact and autotomized animals by 1-way analysis of variance (Statistica 8.0; StatSoft to the observer’s path (80–120) compared with those that Inc.). The number of times animals stopped during swimming moved directly away from the approach path (150–180) could not be analyzed by parametric statistics (the data were (F1,38 ¼ 0.93, P ¼ 0.341). not normally distributed continuous data) and were therefore Distance moved was significantly inversely correlated with 2 analyszd with Mann–Whitney U test. Values are presented as FID in intact P. atlantica (r ¼ 0.20, F1,38 ¼ 9.29, P ¼ 0.004) at Murdoch University on June 19, 2011 mean 6 1 standard deviation throughout, and statistical but was not correlated in autotomized animals (r2 ¼ 0.04, significance was considered where a , 0.05. F1,15 ¼ 0.63, P ¼ 0.441) (Figure 4). Intact P. atlantica moved both into the water (37%) or onto another grass stem (63%) (v2 ¼ 3:67, P ¼ 0.055) but RESULTS 1 significantly more of the autotomized individuals landed in Complete data were collected for 57 P. atlantica responding to the water (88%) rather than landing on grass stems (12%) 2 approach by a human; this comprised 40 intact animals and (v1 ¼ 8:64, P ¼ 0.003). 17 missing a hind limb. Starting distances did not differ Under laboratory conditions, autotomized grasshoppers between intact and autotomized animals (5.2 6 0.5 m, swam slower (0.07 6 0.01 ms21) than intact individuals 21 F1,55 ¼ 0.02, P ¼ 0.887). (0.12 6 0.03 ms )(F1,22 ¼ 59.05, P , 0.001) and paused The stems of vegetation on which P. atlantica perched more times (1.4 6 1.47, range 0–3) than intact grasshoppers emerged an average of 1.01 6 0.28 m above the water surface (0.3 6 0.5, range 0–1) (Mann–Whitney U test: Z12,12 ¼22.48, (not different between intact or autotomized animals: F1,55 ¼ P ¼ 0.013). 0.26, P ¼ 0.615) (Figure 1). Intact animals, however, perched significantly higher on the stem (0.76 6 0.18 m) than did DISCUSSION autotomized grasshoppers (0.46 6 0.17 m) (F1,55 ¼ 34.34, P , 0.001) (Figure 1). The literature includes few experimental explorations of 2 In response to approach, over half (59%, v1 ¼ 14:59, P , predator escape behavior in invertebrates (Wong et al. 2005; 0.001) of the autotomized animals ‘‘squirreled’’ (moved away Hemmi 2005a, 2005b; Cooper 2006; Hoover and Richardson to the far side of the stem from the approaching observer) 2010). In the present study, we observed 2 levels of change in 2 compared with only 5% of intact animals (v1 ¼ 6:20, P ¼ antipredator behavior of autotomized P. atlantica. Firstly, prior 0.013). to being approached or moving away in response (therefore As they were approached by the observer, all autotomized before beginning to accrue locomotory costs), autotomized grasshoppers moved away from the approaching observer by animals were perched lower on stems than intact animals, moving laterally (90–110) to his path (Figure 2). Intact and they also appeared to rely more on hiding than intact crickets moved both laterally (80–120) to the approach path animals, more often ‘‘squirreling’’ around the perch stem. as well as directly away from the observer (150–180). The In addition to possible differential survival of intact and distance from the observer when the P. atlantica made their autotomized individuals (e.g., Bateman and Fleming 2006a; escape (their FID) did not differ between intact (3.27 6 0.63 particularly if autotomized individuals are competitively m, n ¼ 40) and autotomized (3.05 6 0.66 m, n ¼ 17) excluded by intact ones), we note that this hiding behavior individuals (F1,55 ¼ 1.38, P ¼ 0.245). Intact animals moved may influence the recorded frequency of autotomized a greater distance (5.4 6 1.4 m) compared with animals that individuals in the population. Secondly, after being disturbed, were missing a hind limb (2.3 6 1.6 m) (F1,55 ¼ 54.78, P , autotomized animals flee a shorter distance and land in water 0.001) (Figure 3). There was no difference in the distance more often (88% of individuals), despite not being able to moved between the intact animals that moved perpendicular swim as well as intact animals. Intact animals would generally 766 Behavioral Ecology

Figure 3 Flight distances of intact and autotomized Paroxya atlantica. Downloaded from

of tail autotomy on FID have been examined in lizards. Figure 2 However, the results of these studies are not consistent, with beheco.oxfordjournals.org All autotomized Paroxya atlantica moved away from the approaching studies finding shorter FID (Formanowicz et al. 1990; Kelt observer by moving perpendicular to his path (shown by the gray et al. 2002; Capizzi et al. 2007), longer FID (Downes and dotted line). Intact P. atlantica (black solid line) moved both laterally to his path as well as directly away from the observer (position Shine 2001; Cooper 2007), or no significant difference in indicated with the arrow). Values shown are the number of FID (Kelt et al. 2002; Cooper 2003; Capizzi et al. 2007). These individuals within each 10 arc. differences may be explained by the efficacy of alternative

antipredator behavior, and a key to these responses will be at Murdoch University on June 19, 2011 flight speed. The effects of autotomy on escape speed can move toward another stem (63%, the remainder landing in vary across lizard species, with some moving faster when water), but autotomized animals may fall short of, or be autotomized, whereas other species appear unaffected or even unable to grasp vegetation, instead landing in the water. move more slowly (see review by Bateman and Fleming 2009) Escaping P. atlantica launch into flight by a jump; loss of which may account for the varied antipredator flight re- a leg may therefore compromise the power of the leap, as it sponses of different lizard species. does in the locust S. gregaria (Norman 1995), and/or influ- Together, these studies suggest that autotomized lizards and ence steering or stability in takeoff. Compromised launch invertebrates may assess the risk of an encounter differently capacity (which was corroborated by the finding that launch from intact animals and can alter their behavior accordingly. distance was significantly shorter for autotomized grasshop- We had predicted that autotomized grasshoppers would be pers; Norman 1995) may therefore be responsible for altered more wary of the observer’s approach and would take flight antipredator behavior in autotomized P. atlantica. earlier compared with intact individuals. The fact that there A somewhat surprising finding of this study was that there was no significant difference in FID, however, masks the result was no difference in FID between intact and autotomized that autotomized individuals tended to move around the stem grasshoppers, despite their compromised locomotion. away from the observer. Autotomized animals used a different However, the relationship between autotomy and antipreda- mechanism to move away from the observer (walking tor behavior is not always a simple one. In invertebrates, rather than immediately taking flight). The observation although FID has rarely been measured, other behavior may points to an interesting difference in the behavior of these be altered in response to autotomy. For example, leg- animals—perhaps hiding is favored when leaping ability is autotomized wolf spider (Schizocosa avida) individuals avoid compromised and trying an unsuccessful leap may draw the olfactory cues associated with scorpion predators (Punzo unwanted attention of the approaching predator. 1997), whereas lamella-less damselfly larvae (various species) The lack of difference in FID and greater incidence of are less mobile, enter thanatosis more frequently, have re- escape to water (despite compromised swimming) suggest that duced swimming speed, show reduced tendency to flee, or the costs of different escape methods open to P. atlantica are only sporadically leave ‘‘safer’’ microhabitat (Robinson, Hay- more complex than we might expect. Although they cannot worth, et al. 1991; Robinson, Shaffer, et al. 1991; Stoks 1998, swim as well as do intact individuals (more than 1.5 times 1999a, 1999b; Gyssels and Stoks 2005). Autotomized male G. slower), autotomized individuals do not have to swim far bimaculatus crickets take longer to recommence singing after before being able to grasp another emergent stem on to subsequent disturbances compared with intact animals which they can climb; therefore, although swimming is likely (Bateman and Fleming 2006b). Stankowich (2009) found to be more energetically expensive for autotomized over in- no differences between autotomized jumping spiders com- tact animals (just as running is for autotomized G. bimaculatus, pared with intact individuals in FID, flight speed, or behavior Fleming and Bateman 2007), the metabolic costs of using (e.g., backing up) in response to a predator model. water to escape may be outweighed by antipredator benefits. Flight response (i.e., FID) has more commonly been Cooper (2006) noted that most D. carolina fled laterally to recorded in vertebrates (than invertebrates), and the effects the observer’s approach rather than directly away. This lateral Bateman and Fleming • Autotomy and escape behavior 767

supported by our data, emphasizing that greater focus on the repertoire of possible escape tactics available to prey species should be considered in future studies. For example, in this study, we did not appreciate that the use of an alternative defensive tactic—squirreling—would allow autotomized individuals to deal with predation risk without having to leap sooner. Alternatively, it would be adaptive for autotomized individuals to use squirreling as leaping sooner might draw attention to their compromised condition.

FUNDING Murdoch University for financial support.

P.W.B. collected this data as a visiting researcher in the Herpetology Laboratory of Archbold Biological Station, Lake Placid, Florida. We thank Dr Betsie Rothermel and the Restoration Ecology and Herpetol- ogy Program for assistance and hospitality. This paper is dedicated to Jamie T. —‘‘where we going, what we doing... .’’

Figure 4 Comparison between distance fled and FID for intact and REFERENCES

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