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 Ó 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