Ethology 111, 411423 (2005) 2005 Blackwell Verlag, Berlin

Threat-Sensitive Responses to Predator Attacks in a Damsely

Freya G. M. Gyssels & Robby Stoks Laboratory of Aquatic Ecology, University of Leuven, Leuven, Belgium Abstract The threat sensitivity hypothesis predicts that prey species assess and adjust their behavior exibly in accordance with the magnitude of the threat imposed by a predator. We tested this hypothesis with regard to escape behavior and thanatosis (feigning of death to escape predation) in larvae of the damsely Ischnura elegans. We manipulated the perceived predation threat of the larvae by changing three factors: lamellae autotomy (an escape strategy where animals sacrice a body part when grasped by a predator; lamellae present or absent), kairomone type (odors released by predators; control, dragony kairomones or sh kairomones), and population of origin (shpond or shless pond). We demonstrated that thanatosis increased survival both when confronted with dragony and sh predators. We could show, for the rst time, costs of past autotomy to be predator-dependent: larvae without lamellae suered higher predation mortality but only in the presence of a dragony predator and not in the presence of a sh predator. This is in accordance with the observed reduced escape speed of larvae after autotomy, which may aect escape probability toward dragony predators but not to the very fast sh predators. Unexpectedly, kairomone type did not aect the escape response of the larvae. In accordance with the threat sensitivity hypothesis, after an unsuccessful attack, larvae without lamellae had a higher frequency to enter thanatosis than larvae with lamellae and larvae from the shpond showed longer thanatosis durations than larvae from the shless pond. Consistent with the hypothesis, the reaction of the larvae to a simulated attack depended jointly on lamellae status and population. In shless ponds, larvae with lamellae swam away more frequently than larvae without lamellae; in shponds both groups almost never swam away and relied mostly upon immobility. Given the obvious benets of adaptively varying escape responses we hypothesize this threat sensitivity to be widespread. Moreover, we argue that former inconsistencies between studies with regard to escape behavior may have been partly because of such adaptive variation. Correspondence: R. Stoks, Laboratory of Aquatic Ecology, University of Leuven, Ch. de Beriotstraat 32, B-3000 Leuven, Belgium. E-mail: robby. stoks@bio.kuleuven.ac.be

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Introduction The hypothesis that prey species assess and adjust their behavior exibly in accordance with the magnitude of the threat imposed by a predator is known as the threat sensitivity hypothesis (Sih 1986). Almost all studies to date consider threat sensitivity in foraging activity or predator inspection behavior. Far fewer studies deal with threat sensitivity with regard to responses to predator attacks (e.g. Martin & Lopez 2003). Most prey respond to attacks with typical escape behavior, which mostly takes the form of eeing. As a response to an unsuccessful attack, prey may also rely on thanatosis. This feigning of death to escape predation has been observed in several taxa, including Coleoptera (e.g. Acheampong & Mitchell 1997; Miyatake 2001a,b) and Phasmida (Carlberg 1986). However, threat sensitivity to thanatosis has received little attention and very few studies address its context dependency (but see Acheampong & Mitchell 1997; Miyatake 2001a,b). It is plausible to expect that prey with a lower relative escape speed, and therefore with a higher threat when attacked, will rely less upon eeing, and more upon immobility or thanatosis. An intriguing aspect here is that former antipredator behavior may aect escape speed of the prey and therefore shape future threat-sensitive escape decisions. This has been shown for autotomy, a widespread behavior where prey sacrices a body part when grasped by a predator. Autotomy has been shown to reduce escape speed, accompanied with a reduced tendency to ee (Robinson et al. 1991a,b). However, relative escape speed of the prey also depends upon the absolute attack speed of the predator. As far as we know, no studies looked at the combined situation, namely how predators with dierent attack speeds dierently shaped the threat-sensitive escape behavior of prey with dierent escape speed. In this study, we test the threat sensitivity hypothesis with regard to behavioral responses to predator attacks in larvae of the damsely Ischnura elegans. Besides typical escape behavior, we also focus on thanatosis and test the additional hypothesis that thanatosis increases survival after an unsuccessful attack. We manipulated the perceived predation threat of the larvae by changing three factors: lamellae status, kairomones (odors released by predators), and population of origin. We hypothesize that larvae will perceive a higher threat after autotomy, and in the presence of predator kairomones. Moreover, we expect the threat to be higher when exposed to sh kairomones than to kairomones from dragony predators as sh have a much higher attack speed than dragony larvae (Stoks & De Block 2000). As a result, it is also plausible to expect that larvae from a shpond perceive a higher threat than larvae from a shless pond. We expect that larvae which experience a higher threat of being caught when they ee, rely more upon thanatosis or immobility. Finally, we hypothesize that the survival cost of autotomy in later predator attacks depends upon the attack speed of the predator. More specically, we expect no dierential vulnerability between larvae with and without caudal lamellae to the very fast sh predators, but a higher vulnerability in larvae without lamellae to dragony predators.

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Methods
Collection and Housing

Larvae of the damsely I. elegans were collected throughout the winter of 200102 and immediately brought to the laboratory. This continuous collection procedure reduced the amount of time between capturing and testing the larvae and kept this time lag similar for all larvae (about 3 d). Half of the larvae were collected in a shpond dominated by the top predator pumpkinseed sunsh (Lepomis gibbosus) in the nature reserve De Maten in Genk (Belgium). This pond also has low densities of Anax dragony larvae. The other damsely larvae were collected in a small shless pond dominated by Anax dragony larvae in Overijse (Belgium). In such shless water bodies Anax are the top predators (e.g. McPeek 1990). We only collected nal instar larvae with three complete, unregenerated lamellae. Larvae were kept individually in plastic holding containers (10 8 4 cm) in a walk-in climate room with a constant temperature of 21C and a photoperiod of L:D 16:8 h. Damsely larvae were fed ad libitum with Daphnia and mayy larvae. Containers were lled with water containing the kairomones of the top predators of the respective ponds of origin of the larvae. Because kairomones of pumpkinseed have a behavioral lifetime of 41 h to snails (Turner & Montgomery 2003), we refreshed the water daily. Medium with kairomones was made by keeping eight nal instar Anax larvae or two pumpkinseeds (standard length 6 cm) in a 16-l bucket lled with 8 l of aged tap water. Predators were fed with Daphnia and mayy larvae. We lled the holding containers to a height of 3 cm with this medium. During the acclimation period of the larvae we manipulated their lamellae status. We randomly assigned larvae of each population to one of two groups: no lamellae or three lamellae. All three caudal lamellae were removed by gently pulling them with two ngers until the animals autotomized these appendages at the specialized breaking joints (as in Stoks 1998, 1999a,b). The other half of the larvae underwent a sham operation without removing the lamellae. All larvae underwent autotomy or the sham operation at least 1 d before their use in experiments.
Experiment 1: Survival Value of Thanatosis

In this experiment, we explicitly tested the survival value of thanatosis when larvae were confronted with their top predator (sh or dragony larvae). We randomly selected 20 larvae with lamellae from the shless pond to test with dragony larvae, and 20 larvae with lamellae from the shpond to test with sh. Preliminary trials showed that when we induced thanatosis it sometimes only lasted for a very short period of time. To avoid early cessation of thanatosis by the larva before the predator attacked, we mimicked thanatosis by freezing half of the larvae for 20 min at )20C. Larvae were exposed in pairs, one unfrozen and one frozen, to the predators and we noted which larva was attacked and eaten rst.

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Preliminary trials showed that predators did not dislike frozen larvae: they attacked and ate them readily when we simulated movements by holding the frozen larva with a forceps. For the 10 trials with the dragony predator, we used plastic aquaria (16 11 8 cm) lled to a height of 4 cm with aged tap water. For the 10 trials with the sh predator, we used aquaria (48 23 26.5 cm) lled to a height of 20 cm with aged tap water. We divided the aquaria in two halves with an untransparent screen. We introduced the two larvae at one side of an aquarium and the predator at the opposite side. We took care that the larvae were both at a similar distance from the predator. This way we prevented any bias of the predator toward the treatment condition (frozen/unfrozen) of the rst larva it would encounter. Directly after introducing larvae and predator in their compartments, thereby avoiding any position changes of the unfrozen larva, we removed the screen and noted which larva was detected and eaten rst. We separately analyzed the trials with the dragony and sh predators using binomial tests (Sokal & Rohlf 1995) assuming an equal probability of being attacked for both larvae in each trial.
Experiment 2: Threat Sensitivity of Thanatosis

In this experiment, we tested to see whether kairomones, lamellae status and population aected the frequency and duration of thanatosis after a simulated unsuccessful attack. Therefore, we set up a full factorial 3 2 2 experiment with three levels of kairomone type (control, dragony medium, and sh medium), two levels of lamellae status (three lamellae, and no lamellae), and two populations (shless pond, and shpond). We tested 10 larvae (replicates) per treatment combination (total of 120 larvae). Kairomone treatments were set up as explained above for the holding containers. Each trial started with carefully placing a larva into an experimental container identical to the holding containers. After a 5-min acclimation period we simulated an unsuccessful predator attack by rmly grabbing the thorax of a larva with a forceps and turning the larva on its back (as in Wildermuth 2000). For each attack we scored whether the larva entered thanatosis or not and the duration of thanatosis to the nearest second with a chronometer. Thanatosis durations longer than 20 min were set to 20 min. Thanatosis could easily be scored because when entering thanatosis larvae adopted a typical position with bended legs kept close to the abdomen while they stayed motionless on their back. We dened a thanatosis bout as nished when the larva had turned back on its legs, which was within seconds after it made rst leg movements again. We performed a loglinear analysis (Sokal & Rohlf 1995) to analyze the number of larvae that entered thanatosis as a function of the treatments: kairomones, lamellae status, and population. For those larvae that entered thanatosis, we tested for treatment eects on its duration using an anova. We started with a full factorial model including all interactions, but removed nonsignicant interactions from the nal model (Crawley 1993).

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Experiment 3: Survival Value of Lamellae Status

In this experiment, we tested how lamellae status aected the survival probability of larvae when attacked by one of the two top predators (sh and dragony larvae). We exposed sets of 10 larvae, all with lamellae or all without lamellae, to a single predator. We tested larvae from the shless pond with dragony larvae, and larvae from the shpond with sh. For the trials with the dragony predator, we used circular plastic dishes (diameter 22.6 cm, height 4.5 cm) as experimental arenas and lled them to a height of 3.5 cm with tap water. We placed 10 larvae in a dish and let them acclimate for 30 min. Then we introduced one Anax in the center of the dish. Each time the dragony attacked, i.e. when it struck its labium to a damsely larva, we noted whether the larva could escape or not. Attacked larvae were replaced by new ones. These new larvae were rst acclimated in a similar dish and with a spoon we gently placed them in the test dish behind the Anax. Each trial was ended after 10 attacks or after 30 min. Larvae and predators were used in only one trial. For the trials with the sh predator, we used similar plastic aquaria with a dividing screen as in expt 1. Ten larvae were placed in one compartment and one sh in the other compartment. After an acclimation period of 30 min the trial started by removing the screen. Again, we noted the survival success of the damsely larvae when attacked by the sh. The trial ended when all 10 larvae were eaten or when 20 min had passed. We did not put new larvae in the aquarium during the experiment because the sh would learn to attack those larvae immediately. Again, both damsely larvae and sh were used in only one trial. We performed six trials for each combination of lamellae status and predator (total 24). Because of the small number of attacks during each trial (usually 68), we pooled observations across all trials of the same treatment combination. We performed Fisher Exact tests (Sokal & Rohlf 1995) to analyze the eect of lamellae status on the success of escaping a predator attack separately for each predator.
Experiment 4: Threat Sensitivity of Escape Behavior

In this experiment, we tested for eects of kairomone type, lamellae status and population on the escape response of damsely larvae to a simulated predator attack. We observed 10 larvae (replicates) for each treatment combination of the complete 3 (kairomones type) 2 (lamellae status) 2 (population) design (total of 120 larvae). We simulated an unsuccessful attack by tapping each larva with a blunt probe on the thorax. This resembles an unsuccessful attack from a dragony larva or foraging sh (Hopper 2001). Each larva was placed individually in a circular plastic dish (diameter 48 cm, depth 6 cm) lled to a height of 5.5 cm. After 5 min we scored its escape response (not moving, walking or swimming away) to the simulated attack. Additionally, when a larva moved, we quantied the duration of the escape response to the

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nearest second using a chronometer, and the distance to the nearest centimeter using a ruler. The kairomone treatments were installed by adding control water, water with dragony medium, or water with sh medium in the experimental dishes as in expt 2. A loglinear analysis was performed to test the eect of kairomone type, lamellae status and population on the frequencies of the three dierent escape responses (not moving, walking, and swimming). For those larvae that did move when attacked, we analyzed the eect of kairomone type, lamellae status, and population on the duration and the distance traveled during the escape in a manova. Both duration and distance were log transformed to meet assumptions of manova. To interpret the signicant eects we performed separate anovas. We started with a full factorial model including all interactions, but removed nonsignicant interactions from the nal model (Crawley 1993). Results
Experiment 1: Survival Value of Thanatosis

In all 10 trials with the dragony predator and all 10 trials with the sh predator, the unfrozen larva was attacked rst. The probability of being attacked was therefore signicantly lower when the larva was frozen, our condition mimicking thanatosis, than when the larva was unfrozen (binomial test: p < 0.001).
Experiment 2: Threat Sensitivity of Thanatosis

Larvae without lamellae entered thanatosis (85.0%) more frequently than larvae with lamellae (53.3%) (df 1; v2 4.09; p 0.043; Fig. 1a). There was no eect of kairomone type (df 1; v2 0.71; p 0.70), population (df 1; v2 1.43; p 0.23), or any of their interactions (all p > 0.20) on the percentage of larvae that entered thanatosis. Larvae from the shpond population stayed in thanatosis longer than those of the shless pond (F 37.17; df 1.77; p < 0.0001; Fig. 1b). There was no eect of kairomone type (F 0.23; df 2.77; p 0.79), lamellae status (F 0.13; df 1.77; p 0.72), or any of their interactions (all p > 0.085).
Experiment 3: Survival Value of Lamellae Status

When confronted with the dragony predator, the lamellae status of a damsely larva had a signicant eect on its survival probability (Fisher Exact, p < 0.001). Larvae with lamellae had higher survival (67.4%) than larvae without lamellae (25.6%). With the sh predator, there was no eect of lamellae status (Fisher Exact, p 0.20). When attacked by a sh, both larvae with lamellae (2.4%) and larvae without lamellae (11.6%) had a low survival probability.

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(a) Larvae that entered thanatosis (%) 100

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0 (b) 1400 1200 1000 Time (s) 800 600 400 200 0 No lamellae Lamellae Fishless pond No lamellae Lamellae Fish pond

Fig. 1: (a) Percentage of the larvae that entered thanatosis and (b)  (+1SE) duration of thanatosis as x a function of kairomone type, lamellae status and population. For the duration, only larvae that entered thanatosis are included

Experiment 4: Threat Sensitivity of Escape Behavior

The escape behavior toward a simulated attack was jointly inuenced by lamellae status and population (Loglinear analysis: lamellae status population escape behavior; df 2; v2 5.97; p 0.050; Fig. 2). In the shless pond, larvae with lamellae were more inclined to swim than the larvae without lamellae (56.7% vs. 3.3%). Larvae without lamellae most often (80%) did not move when attacked, while this was much less frequent in larvae with lamellae (40%). In the shpond, larvae with and without lamellae most often did not move when

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Not moving Walking Swimming (a) 10 8 Frequency 6 4 2 0 (b) 10 8 Frequency 6 4 2 0 (c) 10 8 Frequency 6 4 2 0 No lamellae Lamellae No lamellae Lamellae Fishless pond Fish pond

Fig. 2: Frequency of three escape behaviors (not moving, walking and swimming) to a simulated predator attack as a function of lamellae status and population for several kairomone types: (a) control, (b) dragony kairomones, and (c) sh kairomones

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attacked (with lamellae: 77.8%, without lamellae: 80%). Kairomone type did not aect the escape behavior (df 2; v2 0.00; p 0.97). The manova revealed that lamellae status had an eect on the duration and the distance of the escape response (F 13.62; df 2, 31; p < 0.0001; Fig. 3a). Kairomone type (F 0.34; df 4, 62; p 0.85), population (F 0.30; df 2, 31; p 0.74), or their interactions (all p > 0.27) had no eect. Univariate anovas showed that lamellae status only had an eect on the time (F 13.96; df 1, 32; p 0.00073), and not on distance traveled (F 0.07; df 1, 32; p 0.79). The

60 (a) 50
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Fig. 3: Mean (+1SE) duration (a) and distance (b) of the escape response to a simulated attack as a function of kairomone type, lamellae status and population. Only larvae that moved are included

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duration of the escape response was about six times longer in larvae without lamellae compared with larvae with lamellae (Fig. 3b). Discussion Our results show that both escape responses, thanatosis and moving away, were to some extent threat sensitive. Thanatosis did increase the survival of larvae and depended upon lamellae status and population. Lamellae status inuenced the survival value of the larvae and escape behavior also depended upon lamellae status and population. Larvae did not change their escape behavior as a function of the added kairomones. However, this would be adaptive, because swimming away is benecial when confronted with dragony predators but not when confronted with sh (Stoks & De Block 2000, see also expt 3). The few studies that looked at a response of damsely larvae to kairomones found mixed support. Only Chivers et al. (1996) and Wisenden et al. (1997) showed a short-term decrease in foraging activity in Enallagma larvae confronted with sh kairomones. Heads (1985) reported a decrease in movements of I. elegans during the night in the presence of Notonecta but this could be caused by a response to kairomones or to mechanical stimuli from the predator. In accordance with our present ndings, two other studies on I. elegans failed to nd a reduction in foraging activity to predator kairomones (Schaner & Anholt 1998; F. Gyssels and R. Stoks, unpubl. data). Any breakdown of kairomones is unlikely to cause these negative results as in the study of Schaner & Anholt (1998) a caged Anax was present throughout the experiment. Further work is needed to see whether responses to predator kairomones are species-specic in damsely larvae and to unravel the underlying logic. The results of our rst experiment supported our hypothesis that thanatosis increases survival. By mimicking thanatosis we demonstrated that larvae in thanatosis were less frequently attacked than larvae not in thanatosis. Surprisingly, this survival benet has only been shown in two other studies, namely in the walking stick Baculum (Carlberg 1986), and in several mantid species (Reitze & Nentwig 1991). This advantage of thanatosis is logical because many predators, including sh and dragony larvae only or mainly react to moving prey. Larvae without lamellae entered thanatosis more frequently than larvae with lamellae after a general, simulated unsuccessful attack. This agrees with the lower survival probability of larvae without lamellae when attacked by a dragony predator (expt 3), and therefore is consistent with our hypothesis of threatsensitive thanatosis. In addition, the longer thanatosis duration of larvae from the shpond population is consistent with a threat-sensitive scenario. In shponds the overall predation risk is not only assumed to be higher, but also the main predation risk is qualitatively dierent: sh are the top predators, while large dragony predators, which are themselves prey for sh are less active and threatening (Wellborn et al. 1996). After an unsuccessful attack or after having shortly observed a moving larva, a dragony predator often lost interest when the larva entered thanatosis. A sh, on the contrary, seemed to remember where he had last seen the larva and swam regularly back to that place to look for the larva

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even when it was in thanatosis (F. Gyssels and R. Stoks, pers. obs.). Therefore, longer thanatosis times in a shpond population compared with a shless pond population may be adaptive and are consistent with a higher predation threat in the former. A higher benet of thanatosis is also suggested by the nding of Wildermuth (1999, 2000) that odonate species typical for shponds almost always enter thanatosis after a simulated attack, while species of shless ponds do not. However, in our study at the intraspecic level, this did not lead to dierences in the frequency to enter thanatosis but in longer thanatosis times. One reason for this may be that the tendency to enter thanatosis was already overall high in our study species (Fig. 1a). To our knowledge, there are no other studies, which tested the threat sensitivity of thanatosis. Moreover, very few studies looked for variables aecting thanatosis. Two studies on beetles showed that animals are less willing to enter thanatosis and show shorter thanatosis times when starved (Acheampong & Mitchell 1997; Miyatake 2001a), and another study showed that at night fewer animals entered thanatosis and did so for shorter times (Miyatake 2001b). The latter was interpreted by the conicting need to reproduce at night. These studies suggest that animals may adaptively vary thanatosis. Given the obvious costs of thanatosis in terms of lost foraging time, it is to be expected that ne-tuning of thanatosis with regard to predation risk, as we found, may be widespread. As far as we know, our study is the rst to demonstrate predator-dependent predation costs of past autotomy. As expected, lamellae autotomy only reduced survival when confronted with dragony predators and not with sh (expt 3). After lamellae loss, larvae can no longer use autotomy to escape, moreover their escape speed is reduced as indicated by similar escape distances but longer escape times (expt 4). Similar reductions in escape speed after autotomy have been shown in other damsely larvae (Robinson et al. 1991a; Burnside & Robinson 1995; Stoks 1999a) and lizards (Daniels 1983; Formanowicz et al. 1990). This can generate the observed dierential survival with regard to predator type because autotomy and speed are important in escaping dragony attacks but not sh attacks (Stoks & De Block 2000). Analogously, after autotomy Lestes damsely larvae have been shown to be more vulnerable to cannibalism and predation by Notonecta backswimmers (Stoks 1998) and Aeshna dragony larvae (Stoks 1999a). Some other studies have also shown increased mortality by predation after autotomy (e.g. Wilson 1992); however, others found no eect or even a decreased mortality, which was explained by compensatory behavioral mechanisms (e.g. Niewiarowski et al. 1997 and references herein). Our results illustrate that dierences in predator type may also partly explain these inconsistent ndings. The reaction to a simulated attack (expt 4) depended on both lamellae status and population in a way consistent with an adaptive scenario. Larvae of the shless pond with lamellae swam more frequently away after a simulated attack than those without lamellae, which relied more upon immobility. This may be adaptive as larvae with lamellae have a fair chance of surviving a dragony attack by swimming away or by autotomizing lamellae when grasped (Stoks & De Block 2000), while larvae without lamellae have a much lower chance of escape. The

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latter may benet by relying upon immobility as the predator may lose interest in the prey after an unsuccessful attack (see above). A decreased tendency to move away after autotomy has been shown before in damsely larvae (Robinson et al. 1991b). In contrast, all larvae of the shpond, irrespective of their lamellae status, most often did not move. This is consistent with the fact that even larvae with lamellae are unable to out-swim a sh predator while also autotomy is not eective (Stoks & De Block 2000). The higher tendency to swim away when attacked in larvae from shless ponds compared with larvae from shponds has been found in other studies at the species level (McPeek 1990; Stoks & McPeek 2003) and at the population level (Hopper 2001). But as far as we know, no other studies looked at dierences in escape response of animals after autotomy with respect to their natural predator environment. To conclude, escape responses of damsely larvae depended on lamellae status and population consistent with a threat-sensitive scenario. While such intraspecic threat sensitivity has often been reported for behaviors that reduced the probability of being detected by a predator (e.g. Sih 1986), empirical evidence for escape behavior is rare. Given the obvious benets of also adaptively varying escape responses we hypothesize this threat sensitivity to be widespread. Moreover, former inconsistencies between studies with regard to escape behavior may have been partly due to such adaptive variation. Studying such adaptive inter- and intrapopulation dierences in escape behavior may enlarge our insights in the evolution of these behaviors at a macro-evolutionary level because at the intraspecic level intrinsic dierences among species can be avoided. Acknowledgements
We appreciate the help in the eld and in the laboratory of Karen Coeckelbergs and Bastiaan Jansen, and Frank Van de Meutter who also gave constructive comments on the manuscript. RS beneted from a post-doctoral fellowship and a research grant from the Fund for Scientic ResearchFlanders (FWO).

Literature Cited
Acheampong, S. & Mitchell, B. K. 1997: Quiescence in the Colorado potato beetle, Leptinotarsa decemlineata. Ent. Exp. Appl. 82, 8389. Burnside, C. A. & Robinson, J. V. 1995: The functional morphology of caudal lamellae in Coenagrionid (Odonata, Zygoptera) damsely larvae. Zool. J. Linn. Soc. Lond. 114, 155171. Carlberg, U. 1986: Thanatosis and autotomy as defence in Baculum sp.1 (Insecta: Phasmida). Zool. Anz. 21, 1933. Chivers, D. P., Wisenden, B. D. & Smith, R. J. F. 1996: Damsely larvae learn to recognize predators from chemical cues in the predators diet. Anim. Behav. 52, 315320. Crawley, P. 1993. GLIM for Ecologists. Blackwell Science, Oxford. Daniels, C. B. 1983: Running an escape strategy enhanced by autotomy. Herpetologica 39, 162165. Formanowicz, D. R., Brodie, E. D. & Bradley, P. J. 1990: Behavioral compensation for tail loss in the ground skink, Scincella lateralis. Anim. Behav. 40, 782784. Heads, P. A. 1985: The eect of invertebrate and vertebrate predators on the foraging movements of Ischnura elegans larvae (Odonata: Zygoptera). Freshw. Biol. 15, 559571. Hopper, K. R. 2001: Flexible antipredator behavior in a dragony species that coexists with dierent predator types. Oikos 93, 470476.

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Martin, J. & Lopez, P. 2003: Changes in the escape responses of the lizard Acanthodactylus erythrurus under persistent predatory attacks. Copeia 2003, 408413. McPeek, M. A. 1990: Behavioral dierences between Enallagma species (Odonata) inuencing dierential vulnerability to predators. Ecology 71, 17141726. Miyatake, T. 2001a: Eects of starvation on death-feigning in adults of Cylas formicarius (Coleoptera: Brentidae). J. Insect Behav. 14, 421432. Miyatake, T. 2001b: Diurnal periodicity of death-feigning in Cylas formicarius (Coleoptera: Brentidae). Ann. Entomol. Soc. Am. 94, 612616. Niewiarowski, P. H., Congdon, J. D., Dunham, A. E., Vitt, L. J. & Tinkle, D. W. 1997: Tales of lizard tails: eects of tail autotomy on subsequent survival and growth of free-ranging hatchling Uta stansburiana. Can. J. Zool. 75, 542548. Reitze, M. & Nentwig, W. 1991: Comparative investigations into the feeding ecology of six Mantodea species. Oecologia 86, 568574. Robinson, J. V., Hayworth, D. A. & Harvey, M. B. 1991a: The eect of caudal lamellae loss on swimming speed of the damsely Argia moesta (Hagen) (Odonata, Coenagrionidae). Am. Midl. Nat. 125, 240244. Robinson, J. V., Shaer, L. R., Hagemeier, D. D. & Smatresk, N. J. 1991b: The ecological role of caudal lamellae loss in the larval damsely, Ischnura posita (Hagen) (Odonata, Zygoptera). Oecologia 87, 17. Schaner, A. K. & Anholt, B. R. 1998: Inuence of predator presence and prey density on behavior and growth of damsely larvae (Ischnura elegans) (Odonata: Zygoptera). J. Insect Behav. 11, 793809. Sih, A. 1986: Antipredator responses and the perception of danger by mosquito larvae. Ecology 67, 434441. Sokal, R. R. & Rohlf, F. J. 1995: Biometry. W.H. Freeman and Co., New York. Stoks, R. 1998: Eect of lamellae autotomy on survival and foraging success of the damsely Lestes sponsa (Odonata: Lestidae). Oecologia 117, 443448. Stoks, R. 1999a: Autotomy shapes the trade-o between seeking cover and foraging in larval damselies. Behav. Ecol. Sociobiol. 47, 7075. Stoks, R. 1999b: The eect of lamellae autotomy and sexual size dimorphism on startle-response performance in larvae of a lestid damsely (Odonata). J. Zool. 247, 269273. Stoks, R. & De Block, M. 2000: The inuence of predator species and prey age on the immediate survival value of antipredator behaviours in a damsely. Arch. Hydrobiol. 147, 417430. Stoks, R. & McPeek, M. A. 2003: Predators and life histories shape Lestes damsely assemblages along a freshwater habitat gradient. Ecology 84, 15761587. Turner, A. M. & Montgomery, S. L. 2003: Spatial and temporal scales of predator avoidance: experiments with sh and snails. Ecology 84, 616622. Wellborn, G. A., Skelly, D. K. & Werner, E. E. 1996: Mechanisms creating community structure across a freshwater habitat gradient. Annu. Rev. Ecol. Syst. 27, 337363. Wildermuth, H. 1999: Somatochlora alpestris (Selys 1840) in den Schweizer Alpen eine Verbreitungsund Habitatanalyse (Anisoptera: Corduliidae). Odonatologica 28, 399416. Wildermuth, H. 2000: Totstellreex bei Grolibellenlarven (Odonata). Libellula 19, 1739. Wilson, B. S. 1992: Tail injuries increase the risk of mortality in free-living lizards (Uta stansburiana). Oecologia 92, 145152. Wisenden, B. D., Chivers, D. P. & Smith, R. J. F. 1997: Learned recognition of predation risk by Enallagma damsely larvae (Odonata, Zygoptera) on the basis of chemical cues. J. Chem. Ecol. 23, 137151. Received: May 26, 2004 Initial acceptance: September 19, 2004 Final acceptance: November 18, 2004 (B. Kempenaers)