Food stress and predator-induced stress shape developmental performance in a damselfly

I studied effects of stress factors like food shortage, non-lethal predator presence and autotomy on survival and larval performance (growth rate, development rate and developmental stability) of larvae of the damselfly Lestes sponsa. In a laboratory experiment, larvae were raised during their last two instars at two food levels (high or low) crossed with two levels of autotomy (caudal lamellae present or absent). These treatments were nested within three levels of predation risk (Aeshna cyanea absent, Chironomus-fed caged Aeshna or Lestes-fed caged Aeshna). The diet of the predator had no effects. The low food level and the presence of Aeshna independently increased mortality rates of L. sponsa larvae. The low food level, presence of a caged Aeshna and autotomy all independently reduced growth rate (mass and body size at day 40) and wing size at emergence, and the first two stress factors also reduced development rate. Regardless of predator presence and autotomy, all damselfly larvae consumed the food available. This indicated that the predator-induced stress effects were not due to reduced food uptake, but probably reflected lowered assimilation efficiency and/or a higher metabolic rate. Besides a low food level, the presence of caged Aeshna predator larvae and autotomy also increased hind wing asymmetry. This result demonstrated that predator-induced stress may reduce developmental stability in the prey.     

Effect of lamellae autotomy on survival and foraging success of the damselfly Lestes sponsa (Odonata: Lestidae)

Damselfly larvae can autotomize their caudal lamellae to escape predation. Costs of caudal lamellae autotomy were investigated by directly manipulating lamellae condition of Lestes sponsa in laboratory experiments. Larvae without lamellae had higher predation mortality in the presence of Notonecta. Both lamellae loss and larval density increased the probability of being cannibalized. The results suggest that the increased vulnerability after lamellae loss resulted from a reduced escape performance. Larvae were less mobile after lamellae loss or in the presence of a predator, but the decrease was no longer significant when both factors were combined. This indicates that larvae compensate for the increased predation risk with a fixed response. Both lamellae loss and predator presence reduced hunting success, but the decrease after lamellae loss was only significant in the absence of a predator. The fitness consequences of these effects for both the larval and adult stages are discussed. In general, the data strongly suggest that lamellae autotomy plays a role in population regulation of damselflies. Received: 1 April 1998 / Accepted: 28 August 1998     

Behavioral responses to fish kairomones and autotomy in a damselfly

The threat-sensitivity hypothesis predicts that prey species assess and adjust their behavior in accordance with the magnitude of the threat posed by a predator. A largely overlooked characteristic of a prey that will affect its sensitivity to predators is its history of autotomy. We studied threat-sensitive behavior to fish kairomones in larvae of Ischnura elegans damselflies, which had undergone autotomy, from a fishpond and from a fishless pond. In agreement with their higher perceived risk, larvae from the fishpond showed fewer rigid abdomen bends, foraged less and walked more slowly than larvae from the fishless pond. In line with their higher vulnerability to predators, larvae without lamellae spent less time foraging than larvae with lamellae. There was a decrease in swimming activity in the presence of fish kairomones except for larvae with lamellae from the fishless pond. This may reflect differences in vulnerability of larvae without lamellae between pond types. Such context-dependent responses in activity to kairomones should be kept in mind when evaluating the ability of a prey to recognize kairomones.     

Threat-Sensitive Responses to Predator Attacks in a Damselfly

The threat sensitivity hypothesis predicts that prey species assess and adjust their behavior flexibly 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 damselfly Ischnura elegans. We manipulated the perceived predation threat of the larvae by changing three factors: lamellae autotomy (an escape strategy where animals sacrifice a body part when grasped by a predator; lamellae present or absent), kairomone type (odors released by predators; control, dragonfly kairomones or fish kairomones), and population of origin (fishpond or fishless pond). We demonstrated that thanatosis increased survival both when confronted with dragonfly and fish predators. We could show, for the first time, costs of past autotomy to be predator‐dependent: larvae without lamellae suffered higher predation mortality but only in the presence of a dragonfly predator and not in the presence of a fish predator. This is in accordance with the observed reduced escape speed of larvae after autotomy, which may affect escape probability toward dragonfly predators but not to the very fast fish predators. Unexpectedly, kairomone type did not affect 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 fishpond showed longer thanatosis durations than larvae from the fishless pond. Consistent with the hypothesis, the reaction of the larvae to a simulated attack depended jointly on lamellae status and population. In fishless ponds, larvae with lamellae swam away more frequently than larvae without lamellae; in fishponds both groups almost never swam away and relied mostly upon immobility. Given the obvious benefits 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.     

MEASURING PHENOTYPIC SELECTION ON AN ADAPTATION: LAMELLAE OF DAMSELFLIES EXPERIENCING DRAGONFLY PREDATION

Previous studies suggest that the evolution of increased caudal lamellae size to increase swimming speed was an adaptation of Enallagma damselflies for coexisting with large, predatory dragonflies in fishless lakes. To test whether dragonfly predation still exerts selection pressures for increased lamellae size, I performed a field experiment in which I manipulated the abilities of dragonfly larvae to inflict mortality on Enallagma boreale larvae and compared differences in lamellae size and shape between treatments. In cages where dragonflies were free to forage on damselflies, surviving E. boreale larvae had lamellae that were larger in lateral surface area, and that were wider relative to their length, as compared with larvae recovered from treatments in which dragonflies were not permitted to forage on damselflies. Selection differentials of about 0.25 phenotypic standard deviation units were measured for both of these characters. These results indicate that dragonfly predation still exerts significant selection pressures on damselfly antipredator adaptations. The results of this study are discussed in the context of studies of adaptation.     

Effects of predator-induced thinning and activity changes on life history in a damselfly

We investigated how the lethal and non-lethal presence and absence of a fish predator, perch (Perca fluviatils), influenced behaviour, numbers emerging, size at emergence, and development rate of the damselfly Lestes sponsa. The experiment was carried out in outdoor artificial ponds and spanned from the egg stage to emergence of the damselflies. During the experiment food resources for the damselflies were continuously monitored. Damselflies exposed to a lethal predator showed a significantly lower activity level than those in the absence of predators or subjected to a non-lethal predator. Half-way through the larval stage the reduction in activity level was correlated with the presence of lethal predators, and at the end of the larval stage with higher zooplankton densities. Though larvae decreased activity level, size at emergence was larger and development time faster for individuals in the lethal predator treatment. Since fewer larvae emerged from that treatment we interpret the larger size at emergence to be an effect of a combination of thinning and higher zooplankton densities.     

Invertebrate predation predicts variation in an autotomy-related trait in larval damselfly

Autotomy, the discarding of a prey appendage grasped by a predator, may evolve when the benefits of immediate survival outweigh the costs of appendage loss. In larval damselflies, joints connecting lamellae to the abdomen vary in size and shape within and among taxa suggesting that they may evolve under selection by invertebrate predators, such as dragonfly larvae. Assuming that joint width is proportional to the force required for autotomy, we tested if invertebrate predation favours smaller lamellar joints for autotomy or larger joints for structural support of lamellae for swimming. We compared the maximum joint widths of larval Lestes and Enallagma among ponds that varied in risk of invertebrate predation. Relative predation risk estimated as the frequency of regenerated lamellae within ponds was weakly and positively related to the relative abundance of larval dragonflies. The allometry of lamellar joint size decreased with increasing risk of invertebrate predation across ponds after controlling for variation in body size in Lestes congener but not in Enallagma species. Both species of Lestes had larger joint sizes than the five species of Enallagma, suggesting that the ancestral divergence of lamellar joints between these genera may influence contemporary responses to invertebrate predation.     

Phenotypic shifts caused by predation: selection or life-history shifts?

Predators can impose both selection and life-history shifts in prey populations. Because both processes may affect phenotypic distributions, the estimates of selection differentials may be biased. We carried out two field experiments to disentangle these separate effects. We studied whether dragonfly predation by Aeshna cyanea changes the distributions in body size and lamellae morphology in the damselfly Lestes sponsa. Damselflies have caudal lamellae which are used in escapes by swimming. In a first experiment, we manipulated predator presence (No Aeshna, Encaged Aeshna or Free-ranging Aeshna) and stopped the experiment when all larvae had moulted once. In a second experiment, larvae were confronted with a Free-ranging Aeshna but collected before moulting, and survivors were compared with a control sample taken at the start of the experiment. The presence of Aeshna largely reduced the survival probabilities of the Lestes larvae at a very similar rate in both experiments. Daily survival probabilities did not differ between the No Aeshna and Encaged Aeshna treatments. In the Free-ranging Aeshna treatment of the first experiment, size was reduced compared to the other two treatments, creating a significant apparent selection differential. This was probably mainly due to predator-induced reduced growth because in the second experiment, where growth effects were excluded, size of the survivors did not differ from the control sample. In both experiments there was a significant selection pressure for larger lamellae. Standardized directional selection differentials were similar in both experiments (0.57 and 0.28 phenotypic standard deviation units). No survival selection on lamellae shape was detected. These results are in agreement with previous findings that lamellae size, but not lamellae shape, enhances swimming performance and thereby predator escape in this species. This revised version was published online in July 2006 with corrections to the Cover Date.     

Spatially heterogeneous selection in nature favors phenotypic plasticity in anuran larvae

Theory holds that adaptive phenotypic plasticity evolves under spatial or temporal variation in natural selection. I tested this prediction in a classic system of predator‐induced plasticity: frog tadpoles (Rana temporaria) reacting to predaceous aquatic insects. An outdoor mesocosm experiment manipulating exposure to Aeshna dragonfly larvae revealed plasticity in most characters: growth, development, behavior, and external morphology. I measured selection by placing 1927 tadpoles into enclosures within natural ponds; photographs permitted identification of the survivors six to nine days later. Fitness was defined as a linear combination of growth, development, and survival that correlates with survival to age 2 in another anuran species. In enclosures with many predators, selection‐favored character values similar to those induced by exposure to Aeshna in mesocosms. The shift in selection along the predation gradient was strongest for characters that exhibited high predator‐induced plasticity. A field survey of 50 ponds revealed that predator density changes over a spatial scale relevant for movement of individual adults and larvae: 17% of variation in predation risk was among ponds separated by tens to thousands of meters and 81% was among sites ≤10 m apart within ponds. These results on heterogeneity in the selection regime confirm a key tenant of the standard model for the evolution of plasticity.     

Effects of Metarhizium robertsii on the bloodsucking mosquito Aedes flavescens and non‐target predatory insects (Odonata)

The effects of different concentrations and methods of treatment with Metarhizium robertsii Bisch., Rehner & Humber conidia on the non‐target aquatic dragonfly larvae Lestes sponsa Hansemann, Lestes dryas Kirby and Aeshna affinis Vander Linden and on the target bloodsucking mosquito larvae Aedes (O.) flavescens (Muller) were analysed. We found that dragonflies are significantly less susceptible than mosquitoes to the fungus. Larvae of L. sponsa larvae were more susceptible to wet conidia than dry conidia. However, the mortality of the air‐breathing larvae of A. affinis was significantly higher after treatment with dry conidia relative to aqueous suspension. The results help to minimize the negative effects of entomopathogenic fungi on non‐target predator insects under the control of mosquito larvae.     

Behavioural activity levels and expression of stress proteins under predation risk in two damselfly species

Abstract 1. It has become apparent that predators may strongly decrease prey fitness without direct contact with the prey, as they induce the development of defence systems that limit the availability of energy for growth and reproduction. Recent studies suggest that stress proteins may help prey organisms deal with this stress. The pattern is not general, however, and little is known about species differences in physiological traits in coping with predator stress, and covariation of physiological with other antipredator traits. 2. To explore these issues, we quantified levels of constitutive and fish‐induced stress proteins (Hsp60 and Hsp70) and anti‐predator behaviours in larvae of two damselfly species that differ in lifestyle. Both stress proteins were fixed at higher levels in Erythromma najas, which has a slow lifestyle, than in Lestes sponsa, which has a fast lifestyle. Similarly, anti‐predator behaviours were fixed at safer levels in E. najas than in L. sponsa. 3. These results suggest that stress proteins may be part of anti‐predator syndromes of damselfly larvae, and there may be trait co‐specialisation between stress proteins and behavioural anti‐predator traits. Studies formally testing these hypotheses in more species may prove rewarding in advancing our understanding of the functional integration of physiological anti‐predator traits in relation to the prey’s lifestyle.     

No behavioural compensation for fitness costs of autotomy in a lizard

Abstract Antipredator mechanisms employed by animals are obviously beneficial if they increase survival, but their use may be costly and decrease fitness. Fitness costs of antipredator mechanisms may, in turn, be defrayed by behavioural compensation. We used lizards as a model to measure behavioural fitness costs of the antipredator mechanism, autotomy, as they commonly lose their tails when attacked by predators. In addition, we examined whether male skinks, Carlia jarnoldae (Scincidae), behaviourally compensate for tail loss by comparing the behaviour of tailed and tailless males in experimental enclosures, either alone, with a conspecific male or female, or with a predator. Tailless males experience several costs of autotomy including reduced energy stores, and loss of autotomy as a defence. We identified an additional cost of tail loss: reduced mating success. However, this species did not behaviourally compensate these costs. Instead, characteristics of the ecology of C. jarnoldae may minimize the costs of autotomy. This species experiences an extended breeding season, which means that they experience reduced mating success for only 20% of this breeding season. Additionally, the presence of inguinal fat stores which supply energy in addition to stores in the tail reduce energetic costs.     

Visual cues contribute to predator detection in anuran larvae

The ability of prey to detect predators directly affects their probability of survival. Chemical cues are known to be important for predator detection in aquatic environments, but the role of other potential cues is controversial. We tested for changes in behaviour of Rana temporaria tadpoles in response to chemical, visual, acoustic, and hydraulic cues originating from dragonfly larvae (Aeshna cyanea) and fish (Gasterosteus aculeatus). The greatest reduction in tadpole activity occurred when all cues were available, but activity was also significantly reduced by visual cues only. We did not find evidence for tadpoles lowering their activity in response to acoustic and hydraulic cues. There was no spatial avoidance of predators in our small experimental containers. The results show that anuran larvae indeed use vision for predator detection, while acoustic and hydraulic cues may be less important. Future studies of predator‐induced responses of tadpoles should not only concentrate on chemical cues but also consider visual stimuli. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ??, ??–??.     

The ecological role of caudal lamellae loss in the larval damselfly,Ischnura posita (Hagen) (Odonata: Zygoptera)

Summary Damselfly larvae may autotomize and regenerate any of their 3 caudal lamellae. At least one missing or regenerating lamella was evident in 50.1% of field collected Ischnura posita larvae. Lamellae loss during molting is very infrequent (1 out of 117 recorded molts). Laboratory trials indicate that conspecifics remove lamellae and that this process is density dependent. The percentage of larvae losing lamellae during 24 h trials ranged from 73.5 at the highest density tested to 17.3 at the lowest density. I. posita larvae are cannibalistic. The presence of lamellae reduces an individual's chance of being cannibalized. More than twice as many final instar lamellae-less larvae were cannibalized during 24 h trials than analogous individuals having 3 lamellae at experimental initiation. Costs are also associated with lamellae autotomy. 1) Although individuals without lamellae can swim they are more reluctant to release from a wooden stalk and swim when threatened (9% release) than are larvae with lamellae (29% release). Since swimming is part of their repertoire of anti-predator behaviors this behavioral shift should be detrimental. 2) Caudal lamellae function in O₂ uptake. Trials were conducted with larvae having and not having lamellae in an experimental horizontal oxygen gradient system. Relative to larvae without lamellae, those with lamellae preferred deeper depths at PO₂ values greater than 70 torr. Many lamellae-less larvae distributed themselves at the water surface throughout the range of PO₂ values tested. Differential depth distribution between larvae with and without lamellae is highly significant (P < 0.01).     

The larval diet of three anisopteran (Odonata) species

SUMMARY.

• 1 Comparisons between larval diets of three anisopteran species (Anax imperator, Aeshna cyanea and Libellula depressa) showed that their food intake changed depending on: (1) predator species, (2) time of year, and (3) developmental stage.
• 2 Although this last factor is not so important, the mean size of prey items and the range of prey species eaten by Auax imperator and Aeshna cyanea larvae increased with predator size.
• 3 Comparisons between prey availability and diets indicated differential selectivity by these predators.

     

Interspecific differences in movement and hunting success in damselfly larvae (Zygoptera: Insecta): responses to prey availability and predation threat

SUMMARY. 1. Freshwater invertebrate predators can alter their hunting behaviour in response to prey availability and threat from their own enemies. Movement patterns and hunting success of the larvae of two species of damselfly (Zygoptera: Insecta), Enallagma cyathigerum (L.) and L. sponsa (Hansemann), were monitored in four combinations of prey availability and enemy threat. Aeshna juncea (L.) (Anisoptera: Insecta) larvae acted as predator and Daphnia magna Straus (Cladocera: Crustacea) as prey in the combinations: no predator/no prey; one Aeshna present/no prey; no predator/thirty Daphnia present; one Aeshna present/ thirty Daphnia present.
2. E. cyathigerum showed significantly reduced movement in the +Aeshna/no prey treatment but hunting success was not significantly affected. No other treatment effects were noted. L. sponsa movement patterns differed significantly across all four treatments and hunting success was significantly reduced in the presence of Aeshna .
Interspecifically, movement patterns of the two species differed markedly in all four treatments. L. sponsa larvae were much more active, and caught many more prey. Despite their activity L. sponsa larvae did not appear markedly more vulnerable than the immobile E. cyathigerum .
3. The interspecific differences between the two damselflies reflect predictions based on larval life-history. Activity patterns and ability to capture adequate prey under varying levels of predation may be important in the ecology of damselfly species.     

Evolution of antipredator behavior in an island lizard species,Podarcis erhardii (Reptilia: Lacertidae): The sum of all fears?

Organisms generally have many defenses against predation, yet may lack effective defenses if from populations without predators. Evolutionary theory predicts that “costly” antipredator behaviors will be selected against when predation risk diminishes. We examined antipredator behaviors in Aegean wall lizards, Podarcis erhardii, across an archipelago of land-bridge islands that vary in predator diversity and period of isolation. We examined two defenses, flight initiation distance and tail autotomy. Flight initiation distance generally decreased with declining predator diversity. All predator types had distinctive effects on flight initiation distance with mammals and birds having the largest estimated effects. Rates of autotomy observed in the field were highest on predator-free islands, yet laboratory-induced autotomy increased linearly with overall predator diversity. Against expectation from previous work, tail autotomy was not explained solely by the presence of vipers. Analyses of populations directly isolated from rich predator communities revealed that flight initiation distance decreased with increased duration of isolation in addition to the effects of current predator diversity, whereas tail autotomy could be explained simply by current predator diversity. Although selection against costly defenses should depend on time with reduced threats, different defenses may diminish along different trajectories even within the same predator–prey system.     

Interactions between fish and salamander larvae

Summary Two species of salamander larvae (Ambystoma talpoideum and A. maculatum) were reared separately in the presence and absence of a fish (Lepomis macrochirus) in artificial ponds to measure the effects of a predator on the growth, survival, diet, and activity of larvae. The presence of L. macrochirus reduced body sizes of larvae by 18% in A. talpoideum and by 16% in A. maculatum. L. macrochirus apparently preyed on the smallest individuals. Survival in the presence of L. macrochirus decreased by 61% in A. talpoideum and by 97% in A. maculatum compared with larvae reared alone. Species identity did not significantly effect body size or survival, but an interaction effect suggested that A. maculatum was more severely affected by predators than was A. talpodeum. Activity of larvae in the water column was dramatically reduced in the presence of L. macrochirus, when larvae were restricted to the leaf litter of the benthic zone. There was overlap in the diets of fish and salamander larvae. Larvae reared in the presence of fish, however, consumed different taxa of prey as well as reduced number of prey compared to larvae reared alone. A. talpoideum larvae were more nocturnal than diurnal in the absence of fish, whereas A. maculatum larvae were equally active day and night. This experiment suggests that predator-prey relationships can change with shifts in species attributes and potentially confound apparent costs of predator avoidance with competition. Measuring the long-term dynamics of the cost-benefit relationship will help elucidate how prey balance the demands of their life history with the demands of predators.     

Effects of alternative food on cannibalism and herbivore suppression by carabid larvae

1. Predator and alternative food density are important factors influencing herbivore suppression by generalist predators. Herbivore suppression can be reduced if predators forage preferentially on alternative foods. Cannibalism can increase at high predator densities, further reducing herbivore suppression. However, complex interactions are possible, as alternative food can increase predator abundance and survival restoring top‐down effects on herbivores. 2. In two species of carabid larvae (Poecilus chalcites and Anisodactylus ovularis), we studied how alternative foods (fly pupae and grass seeds) and predator density affect predation of black cutworm larvae and how alternative foods affect cannibalism among carabid larvae. 3. Adding alternative food to microcosms generally reduced total predation of cutworms. However, the strength of this effect was dependent on carabid species, larval density, and food type. 4. Increasing larval density from one to three per microcosm reduced per‐capita predation by both species irrespective of alternative food treatment. 5. Alternative food reduced cannibalism in both carabid species and increased survival of carabid larvae in field plots, such that twice as many were captured in plots subsidised with pupae than plots with no alternative food. 6. These results provide new insight into the complex interactions that influence predator survival and herbivore suppression in resource diverse habitats by demonstrating the primacy of intraguild interactions among carabid larvae.     

Life history and host specificity ofAltica cyanea [Coleoptera: Chrysomelidae], a potential biological control agent for water primrose,Ludwigia adscendens

The life history and host-specificity of the flea beetle,Altica cyanea (Weber) [Coleoptera: Chrysomelidae], were studied to determine its potential value as a biological control agent for water primrose,Ludwigia adscendens (Onagraceae). Females laid a mean of 146 yellowish eggs in masses on this weed and larvae passed through 3 instars. This multivoltine insect completed a generation in 80–84 days. In preliminary host-specificity trials, larvae and adults fed slightly on 2 varieties ofTrapanatans, but they caused considerable damage toLudwigia spp.; no feeding occurred on rice. In host plant choice tests, larvae and adults preferred to feed onL. adscendens andL. prostata toT. natans. In these same tests, onlyLudwigia spp. supported complete development, but it was fastest onL. adscendens. Adults that were reared onL. adscendens lived longer and laid more eggs than those reared onL. prostata, suggesting thatA. cyanea may be a promising biological control agent forL. adscendens growing in rice-paddies. AdultZicrona coerulea L. [Hemiptera: Pentatomidae] preyed upon 3rd instarA. cyanea larvae in the laboratory.