Responses of larval dragonflies to conspecific and heterospecific predator cues

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1 Ecological Entomology (2007), 32, Responses of larval dragonflies to conspecific and heterospecific predator cues GAVIN FERRIS 1,2 and VOLKER H. W. RUDOLF 1,3 1 Mountain Lake Biological Station, Pembroke, VA, U.S.A., 2 Clarion University of Pennsylvania, Biology Department, Clarion, PA, U.S.A., and 3 Department of Biology, University of Virginia, Charlottesville, VA, U.S.A. Abstract. 1. In cannibalistic populations, smaller individuals are subject to predation by larger conspecifics, and small individuals commonly alter their behaviour in response to cannibals. Little is known, however, about the underlying cues that trigger such responses and how the behavioural responses to conspecific cannibals differ from heterospecific predators. 2. This study tests which cues are used for the detection of conspecific predators in the larva of the dragonfly Plathemis lydia and how the behavioural response to cannibals differed from the response to heterospecific predators. 3. Individuals were exposed to chemical cues, visual cues, and a combination of both cues from conspecifics as well as no predator and heterospecific predator controls during which their activity and feeding rates were observed. 4. Individuals increased their activity, spatial movement and feeding behaviour in response to either visual or chemical cues from conspecific predators, which was opposite to responses displayed with cues from heterospecific predators. Interestingly, the responses to visual and chemical cues from conspecifics combined were weaker than to either cue in isolation and similar to the no cue control. 5. The results clearly indicate that individuals are able to use chemical and visual cues to detect even very subtle differences in phenotype of conspecific predators. 6. The opposite response in behaviour when exposed to conspecific cannibals vs. heterospecific predators suggests that the presence of cannibals will increase the mortality risk of small individuals due to heterospecific predation. This risk-enhancement is likely to have important consequences for the dynamics of predator prey interactions. Key words. Anti-predator behaviour, cannibalism, community ecology, competition, dragonfly larvae, intra-specific predation, predator detection, stage interaction. Introduction Cannibalism, the active killing and consumption of a conspecific individual, is a common phenomenon in the animal kingdom ( Fox, 1975; Polis, 1981 ). It represents a unique evolutionary and ecological scenario in predator prey systems because individuals of a single species function as either predator or prey depending on their relative size to other conspecifics. Correspondence: Volker H. W. Rudolf, Department of Biology, University of Virginia, 243, Gilmer Hall, Charlottesville, VA 22904, U.S.A. vrudolf@virginia.edu Cannibalism is generally size-structured, with larger individuals consuming smaller conspecific ones ( Polis, 1981 ). Thus an individual typically begins life as potential prey and then undergoes a size-based niche shift to a potential cannibal during its ontogeny. Owing to the risk asymmetry between cannibals and conspecific prey, cannibalism affects the behavioural interaction between different size classes, which in turn has important consequences for predator prey dynamics ( Sih, 1981, 1982; Rudolf, 2006 ). The proximate causes underlying these behavioural interactions between cannibalistic predator and their conspecific prey, however, are not well understood. Cannibalism is a major mortality factor in many species ( Fox, 1975; Polis, 1981 ). In any system in which predation provides a Journal compilation 2007 The Royal Entomological Society 283

2 284 Gavin Ferris and Volker H. W. Rudolf significant source of mortality, there is a strong selection pressure for prey to display anti-predator behaviour in the presence of predators ( Lima & Dill, 1990 ). These behaviours often include a decrease in activity or an increase in refuge use, which in many instances can reduce feeding rates ( Koperski, 1997; Rudolf, 2006; Sih, 1982; Werner & Anholt, 1996 ). Because of this trade-off, in which a beneficial activity (feeding) is sacrificed to reduce the risk of predation, an individual s fitness level is maximised if this anti-predator behaviour is only exhibited in the presence of a predator ( Ball & Baker, 1996; Lima, 1998; Turner, 2004 ). Thus, the more costly the anti-predator response, the more it should only be displayed if the cues are sufficiently reliable. Such anti-predator behaviour often alters foraging rates, which can result in behaviourally mediated trophic cascades and thereby also have strong effects on the entire community ( Preisser et al., 2005; Schmitz et al., 1997 ). Given this trade-off, the key for successfully maximizing fitness is the reliable identification of the predator. In most systems, prey individuals detect predator species by chemical or visual cues or a combination of both ( Peckarsky, 1982 ). While similar cues could be used in cannibalistic interactions, predator and prey are members of the same species, and differences in phenotype are generally much smaller than across species. The few existing studies have mostly focused on systems in which cannibals and conspecific prey have very different phenotypes (i.e. adults vs. larvae, cannibalistic morph vs. normal larva) and diets ( Kats et al., 1994; Hoffman & Pfennig, 1999; Qureshi et al., 2000; Mathis, 2003 ), either of which can facilitate the recognition of conspecific predators. In many systems, however, the cannibal and prey are very similar in phenotype and ecology, and the differences between the morphology and chemicals produced by cannibal and prey may be less pronounced, if a difference exists at all. In systems where similar sized individuals attack each other, the same cues simultaneously indicate a potential prey or predator. This raises the question of how individuals detect cannibals that are so similar in phenotype to themselves. Furthermore, although cannibalism is an important mortality factor in many insects ( Fox, 1975; Polis, 1981; Crowley et al., 1987; Van Buskirk, 1989 ) to the best of the authors knowledge there has been no previous study on the cues that determine the interaction between conspecific prey and cannibals in insects. This study determines which cues or combinations of cues are used to detect cannibals that are similar in phenotype and life-history stage in larval dragonflies. Victims could recognise conspecific predators by means of various sensory cues and react by exhibiting marked differences in behaviour and in some cases morphology. Larval long-toed salamanders, for example, develop more slowly and become less active when exposed to the scent of cannibalistic adults ( Mathis, 2003 ). Juvenile perch, although unable to discern the scent of an adult conspecific from that of a fellow juvenile, react to the scent of an injured conspecific with increased refuge use and altered foraging behaviour (Harvey & Brown, 2004 ). Tactile cues, although used for prey detection in some species ( Peckarsky, 1982 ) are probably not the primary mode of detecting cannibals or predators in general, as getting close enough to detect a tactile cue nearly ensures that a predation event will occur. Visual and tactile cues can also trigger development of cannibal morphs and anti-predator behaviour in larval tiger salamanders ( Hoffman & Pfennig, 1999 ). Dragonfly larvae are among the most common predators in ponds ( McPeek, 1990 ) and play an important role in determining the structure of aquatic food webs ( McPeek, 1990; Fauth & Resetarits, 1991; McPeek & Peckarsky, 1998; Fauth, 1999 ). In many species, breeding and emergence patterns result in overlapping cohorts, often with a wide size distribution between the oldest and youngest individuals ( Wissinger, 1992 ). Although dragonfly larvae appear not to be limited by alternative food (Johnson et al., 1985, 1987 ), cannibalism can be responsible for up to 97% of the total mortality in some species ( Anholt, 1994 ), making it one of the primary mechanism that regulate odonate population densities next to intra-guild predation ( Anholt, 1994; Crowley et al., 1987; Johnson et al., 1985, 1987 ). Such high occurrences of cannibalism should pose a strong selection pressure for anti-predator behaviour in response to larger cannibalistic conspecifics. Although some species are known to exhibit anti-predator responses in the presence of large conspecifics ( ClausWalker et al., 1997; Van Buskirk, 1992 ) the cue responsible for triggering this behaviour has not yet been identified. Dragonfly larvae present an excellent combination of sensory traits for such a study as these predators have been shown to have both keen eyesight ( Rebora et al., 2004 ) and sensitivity to chemical cues ( Hopper, 2001 ). This study tests which cues are used to recognise large conspecific cannibals and how small individuals alter their behaviour to reduce the risk of cannibalism, through an experiment with the larvae of the common whitetail dragonfly Plathemis lydia. In particular, the study asks whether visual, chemical, or a combination of visual and chemical cues is used for detection of potential cannibals and how those respective cues affect different behavioural aspects of the conspecific prey in relation to heterospecific predators. This study also addresses a community level aspect by testing whether the anti-predator behaviour in response to conspecific predators affects the consumption rates of small dragonfly larvae. Methods Study species Plathemis lydia is an abundant species distributed over most of North America that breeds continuously throughout the summer, resulting in a wide size distribution of larvae from final instars to hatchlings at any given time ( Wissinger, 1989 ). In P. lydia cannibalism commonly occurs over a size difference of as little as one or two instars, and cannibalism rates increase with size differences ( Wissinger, 1988 ). These life history characteristics make P. lydia an excellent focus for studying behaviour related to cannibalism between large cannibals and small prey. Individuals were collected in the last 2 weeks of June 2005 from Sylvatica pond at Mountain Lake Biological Station, Virginia, and housed in separate plastic cups with pond water in a climate-controlled room at 22 C and on a LD 13:11 h photoperiod until the beginning of the experiment on 1 July.

3 Detection of conspecifi c predators 285 Experimental design The behavioural response of small P. lydia larva [size range = mm head width, instar range = F4 F3 after Wissinger (1992) ] to five different treatments was observed, each representing a different combination of visual and chemical cues. Small P. lydia larvae were individually tested in an experimental chamber (30 cm 16 cm 10 cm), filled with dechlorinated tap water to a depth of 5 cm. Each chamber contained two artificial refuges in diagonal opposite corners of the container and a plastic cylinder (diameter = 8 cm) in the centre. Each of the two refuges consisted of three pieces of tile (2.8 cm 5.8 cm) supported 5 mm from the bottom by means of steel hex nuts. The cylinder was either empty for the control, or contained a stimulus individual. Fibreglass window screening covered the bottom of the container to facilitate movement of the focus individual. Experimental chambers were visually separated with a cardboard divider between boxes to prevent crosscontamination of visual cues. For the control treatment, the cylinder was clear, perforated and filled with water. To test the response to visual cues from a larger conspecific, the cylinder contained a stimulus individual at least two instars larger than the focus animal and was left clear and was not perforated, preventing the exchange or chemicals between cylinder interior and container. The same procedure was conducted with a perforated container wrapped in non-reflective aluminium foil (opaque cylinder) to test the response to chemical cues in the absence of visual cues. Aluminium foil has been used successfully in previous studies without triggering a behavioural response ( Hoffman & Pfennig, 1999 ), and preliminary studies showed that the sole presence of aluminium foil did not alter the behaviour (Ferris unpubl. data). Thus, foil was not included in the control experiment. To test for responses to both chemical and visual cues the cylinder with the stimulus animal was perforated and clear. To compare the results from the conspecific predator treatments to the reaction to a heterospecific predator, a large Anax junius larva (head width = mm; instar = F1) served as a stimulus animal in the perforated clear cylinder to expose the focus animal to both chemical and visual cues. This heterospecific predator was fed one P. lydia larvae similar in size to the focus animals to provide the visual and chemical cues associated with predation events as well. Only one replication of each treatment was run per day to reduce variation in activity during the course of the day. Each focus animal was used only once to eliminate any learning response. Each treatment was replicated 20 times. Each focus animal was fed ad libitum for 6 h before being introduced to the experimental chamber. Individuals showing abnormal feeding behaviour (i.e. not eating) during this period were not used as this was observed to be a sign that moulting was imminent. Previous studies have shown that moulting affects the foraging behaviour of odonates (Johnson, 1973 ). Prior to introducing the stimulus animals, focus individuals were allowed to acclimatise for 42 h in experimental chambers with an empty stimulus bottle. Individuals were starved during this period to standardise the hunger level. This starvation period is relatively small for dragonfly given that they can be starved for several weeks ( Corbet, 1999, Rudolf unpubl. data). Experiments were started at 09:00 h and were terminated after 24 h. Stimulus animals were introduced 15 min prior to any observations. To measure predation rates and to provide a stimulus for movement, 15 mosquito larvae were added to the experimental chamber 15 min prior to observations. Following the 15-min acclimation period, the focus individuals were observed for 105 min. Every 5 min the location of each focus individual was recorded by means of an 8 4 grid marked on the bottom of the experimental chamber. Refuge use, i.e. hiding under the refuge, was also recorded every 5 min. Activity was monitored by watching each focus animal one at a time continuously for 5 min, recording all movements. This procedure was repeated for each treatment every 25 min, resulting in 20 min of total observation time. A movement that lasted less than 1 s was considered a single movement. For longer movements, each second of sustained activity was considered a movement. The number of mosquito larvae remaining in the experimental chamber was determined after 24 h. For the analysis, activity rate was calculated as the total number of movements per individual per 20-min observation period. The number of different squares each individual occupied during the 105-min observation period was used to quantify the range of spatial movement. The predation rate was calculated as the number of prey consumed after 24 h. Refuge use was recorded by totalling the number of observations during which the individual was hiding under the refuge, but this variable was not included in the analysis because there were too few observation of refuge use for statistical analysis. All data were square root transformed to meet normality assumptions. Data were analysed using a General Linear Model (Proc GENMOD, SAS 9.1.3) with treatments as the main effect and day as a block effect. If the General Linear Model showed a significant treatment effect, post- hoc multiple comparisons with a sequential Dunn Sidak adjustment were used to test for significant differences between treatments. Results The analysis showed a significant treatment effect for all three variables: The number of squares occupied (c 2 = 11.86, P = 24, ), activity rate (c 2 = 15.64, P = ), and the predation rate (c 2 = , P = ). The number of prey 24,72 24,68 consumed had fewer degrees of freedom than the other variables because the number of prey remaining after 24 h was not measured for one of the replicates due to a logistic mistake. There was also a significant day (block) effect for the number of squares occupied (c 2 = 47.18, P = ), activity rate 19,72 (c 2 = 35.95, P = ), and the number of prey 19,72 consumed (c 2 = 85.57, P < ). 18,68 In general, individuals showed a larger spatial movement when exposed to conspecific cues ( Fig. 1). The number of squares occupied was highest in the treatment with visual cues only, followed by the chemical cues treatment, but only the visual treatment remained significant from both the no cue and predator control (c 2 = 7.84, P = 0.005, and c 2 = 9.65, P = respectively) after Dunn Sidak correction. The response

4 286 Gavin Ferris and Volker H. W. Rudolf b # Squares occupied a ac c ac a Activity (movements/min) b c 0 Control Chem. Visual Both Heter.Pred Treatment 0.0 Control Chem. Visual Both Heter. Pred Treatment Fig. 1. Mean number of squares occupied by small P. lydia larva for each treatment displayed after correcting for the significant day (block) effect. Control = no predator, Chem = chemical cue, Visual = visual cue, Both = chemical + visual cues from conspecific cannibals respectively, Heter. Pred = chemical and visual cues from the heterospecific predator A. junius. Treatments with different letters are significantly different after Dunn Sidak correction ( P < 0.05). Fig. 2. Mean activity rate of small P. lydia larva for each treatment displayed after correcting for the significant day (block) effect. Activity rate was calculated as the total number of movements per minute observed over a 20-min period. For treatment descriptions see Fig. 1. Treatments with different letters are significantly different after Dunn Sidak correction ( P < 0.05). of individuals exposed to both chemical and visual cues was not different from the control. Individuals showed the highest activity rate again when confronted with visual cues from conspecifics, followed by the treatment with both cues. Both activities were significantly higher than the heterospecific control (c 2 = 15.50, P < , c 2 = 8.99, P = respectively) ( Fig. 2). Individuals were least active with heterospecific predators present, but this did not remain significantly lower then the control (c 2 = 4.92, P = 0.026) after Dunn Sidak correction. There was no significant difference in activity between chemical cues from the control (c 2 = 2.85, P > 0.091). Individuals exposed to heterospecific predators had the lowest predation rate that was significantly different from the highest predation rate recorded in treatments with the chemical cue only (c 2 = 13.23, P = 0.003) ( Fig. 3), but did not remain significantly different from treatments with no cue and or combined chemical and visual cues (c 2 = 7.17, P = 0.007, c 2 = 6.89, P = respectively) after Dunn Sidak correction. The response to the combined visual and chemical cues was identical to the control without predators. Discussion This study is the first to demonstrate that even if cannibals are phenotypically similar they can be recognised by their conspecific prey. Results show that dragonfly larvae can use both visual and chemical cues to identify larger conspecific larva that represent conspecific predators, and alter their behaviour accordingly. Contrary to previous expectations, however, individuals showed an increase in activity in response to conspecific cannibals, while they decreased activity when confronted with a heterospecific predation event. Furthermore, the results show that although individuals will change their behaviour in response to either visual or chemical cues, the response to both cues combined was generally weaker and more similar to the no predator control. The conspecific size difference between stimulus and test individual were chosen based on field and laboratory experiments where similar size differences result in cannibalism ( Wissinger, Consumption rate [indiv/h] ab Control Chem. Visual Both Heter. Pred Treatment Fig. 3. Mean per capita consumption rate of small P. lydia larva displayed after correcting for the significant day (block) effect. Consumption rates were calculated as the number of prey consumed during a 24-h period. For treatment descriptions see Fig. 1. Treatments with different letters are significantly different after Dunn Sidak correction ( P < 0.05). c

5 Detection of conspecifi c predators ; Rudolf unpubl. data). The results showed that small larvae of P. lydia increased activity and spatial movement when confronted with either visual or chemical cues from larger conspecifics. This increase in activity from conspecific predators is opposite of what would be expected in an anti-predator response ( Werner & Anholt, 1996 ) which was observed when individuals were confronted with cues from heterospecific predation. Furthermore, anti-predator responses generally decrease an organism s feeding rate ( Werner & Anholt, 1996 ), while these individuals showed a tendency to increase their feeding rate when exposed to conspecific predators. There are at least two possible explanations. Dragonfly larvae differ in their feeding strategy across species. P. lydia belong to the bottom sprawlers, which are mostly sit-and-wait predators that ambush their prey ( Corbet, 1999 ). When taking up the cue of such a predator, the optimal strategy to avoid the risk of predation would be to leave the immediate area around the source of that cue. Individuals that follow such a strategy would show a higher spatial movement, and therefore necessarily a higher activity, especially if the individual is confined within a box without escape possibility. In contrast to P. lydia, A. junius is a very active predator ( Corbet, 1999 ), and behavioural observations showed that A. junius is also more likely to notice and hunt a prey that moves (Rudolf unpubl. data). When faced with such a predator, decreasing activity might reduce the risk of predation. Both predictions would be consistent with the observed pattern in our experiments when exposed to conspecific and heterospecific predator cues. A second possibility would be that the increase in activity and feeding is in relation to a competitive response (Relyea, 2004 ). This would suggest, however, that competition from larger conspecifics poses a greater cost to an individual s fitness than does the threat of cannibalism. Although this has been suggested for starved salamander larvae ( Wildy & Blaustein, 2001 ), it seems unlikely in dragonfly larvae that are usually not food limited in natural habitats ( Johnson et al., 1985, 1987 ), and can endure long time periods without food ( Corbet, 1999 ). It is also possible that the actual predation event provided some additional cue that could affect the behavioural response. Observations in the laboratory suggest that there are no obvious changes in behaviour when individuals were in containers where conspecific predation occurred (Rudolf, pers. obs.). To completely resolve this issue, however, further research especially in terms of resource limitation and response to alarm signals in P. lydia is needed. In any case, our results clearly show that the response to conspecifics cannibals and heterospecific predation is opposite in this scenario. This means cannibals could increase the predation risk of small conspecifics by increasing their activity and thus their visibility for A. junius. This would suggest that the combined effect of both conspecific and heterospecific predators (i.e. multiple predator effect) is likely to be more than additive, resulting in higher mortality rates of small P. lydia than expected from their individual effects (i.e. risk enhancement) ( Sih et al., 1998 ). Such non-additive interactions between conspecific and heterospecific predators are likely to be present in many food webs, and are likely to have important consequences for predator prey dynamics. It is important to point out, however, that in this study, both species have different predation strategies. There are several species that commonly coexist with P. lydia that are also bottom sprawlers. When interacting with these predators, the behavioural responses to conspecifics and heterospecific predators are likely to be similar. In such a scenario, the interactions between predators and cannibals might be additive. Future studies that investigate such interaction effects will provide important insight on how intra- and inter-specific processes shape community dynamics. The reduced or lack of response in activity when visual and chemical cues were combined was unexpected. It is possible that being able to more reliably detect and monitor a larger conspecific might remove the incentive to increase their behaviour. In an anti-predator response this could be explained because complete detection of a predator by multiple cues might allow an individual to more accurately keep track of a predator s location and the threat posed. Only when a predator is partially detected or when the predator is attacking drastic behavioural changes are needed. This explanation would fit well with the hypothesis that the response observed is an anti-predator response, but would be inconsistent with a competitive response. Future research into the ecology of this species and the morphology governing detection of cues may help to generate a theoretical mechanism for this response pattern. The experiment was designed to identify the cues used for detection of potential harmful conspecifics. Now that cues are known, the remaining question is whether the behavioural response to large cannibalistic conspecifics differs from a response to harmless, smaller conspecifics that also represent potential prey. Future studies will investigate size-specific differences in the behavioural response towards conspecifics to answer this question. In conclusion, P. lydia is capable of using both chemical cues and visual cues to detect conspecific predators that are very similar in morphology, developmental state and ecology. Individuals did not alter their behaviour, however, if both cues are present, suggesting an interaction effect of both cue types. Furthermore our results indicated that individuals respond very differently to conspecific cannibals and heterospecific predators, which could lead to non-linear interaction effects between cannibals and heterospecific predators. Such interactions are likely to be common in many communities and could have a strong impact on predator prey dynamics. Acknowledgements We are grateful for comments from H. M. Wilbur for discussion about experimental setup and A. Taylor and A. M. Turner for helpful comments on earlier versions of the manuscript. Mountain Lake Biological Station and the University of Virginia provided logistic support. This material is based upon work supported by the National Science Foundation under grant no. DBI

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