Grooming decisions by damselflies, age-specific colonisation by water mites, and the probability of successful parasitism.

We examined whether host damselflies (Ischnura verticalis) in different stages of development were differentially susceptible to parasitism by larval water mites (Arrenurus pseudosuperior). We found that mites were successful in reaching the parasitic phase more often if they colonised hosts closer to emergence. Thus, we predicted that more mites should colonise damselflies closer to emergence and damselflies closer to emergence should spend more time defending against mites. We found that mites colonised damselflies closer to emergence in one of two experiments, but that damselflies in different stages of development did not differ in time spent defending against mites.     

Aggressive Interactions and Risk of Fish Predation for Larval Damselflies

Larval damselflies frequently engage in aggressive interactions that may increase their risk of fish predation. To test this we analyzed the behavior of larval Ischnura verticalis exposed to both conspecifics and fish predators. Larvae in the presence of conspecifics oriented, struck, and swam more but crawled less compared to solitary larvae; the presence of fish reduced, or tended to reduce, all behaviors. Fish struck more at interacting larvae compared to noninteracting larvae. Increased attack rate by fish likely reflects the increase in the very active swimming behavior by larvae and suggests a conflict between antipredator behaviors. Swimming is an appropriate response to avoid predation by odonate larvae which normally ambush prey but is clearly dangerous when fast-swimming fish that cue in on movement are nearby.     

Do Larval Damselflies make Adaptive Choices When Exposed to Both Parasites and Predators?

The importance of multiple enemies from different trophic levels on investment in defence by prey has, with some exceptions, received little attention. Some defences may make the victim more susceptible to other enemies; this latter situation applies to predators and parasites of larval damselflies. Baker and Smith [Oecologia 109 (1997) 622) showed that larval damselflies were as active in the presence of both mites and fish as they were when only mites were present, an apparently maladaptive behaviour that results in higher fish predation. In this paper, we further examine this maladaptive behavioural response to multiple enemies (fish predators and mite parasites) and test whether their defence responses are a result of the order in which they experience the parasite or predator, and/or if behavioural ‘personalities’ exist, such that some individuals show anti‐predator behaviours and other show anti‐parasite behaviours. Order of experience did not affect the four main behaviours (groom, crawl, turn and swim) exhibited when larval damselflies were simultaneously exposed to fish and mites. Grooming levels increased in response to mites, decreased in response to fish and when exposed to both mites and fish were similar to when they were exposed to mites alone. Duration of the other three behaviours was lower in the presence of both mites and fish. The crawling ‘personalities’ were evident. The apparently maladaptive response of high grooming levels in the presence of mites and fish is not a result of order of experience or ‘personalities’. It may be a result of relatively high encounter rates with mite parasites, compared with the encounter rates with fish. Lower encounter rates can result in diminishing investment in defence against an enemy.     

Larval Ischnura verticalis (Odonata: Coenagrionidae) Respond to Visual Cues of Predator Presence

Larvae of some species of damselflies respond to chemical cues of fish predators but, while larvae of many species are thought to detect prey through vision, there is little evidence that larvae respond to visual cues of predator presence. This laboratory study indicated larval Ischnura verticalis behaviours are affected by visual cues and, to a much lesser extent, chemical cues of fish; there was no significant interaction between the effects of visual and chemical cues. Responses to chemical cues of fish did not depend on whether fish were fed I. verticalis larvae versus commercial fish food. Larvae were more active in the spring than the fall when they were likely in diapause. Results suggest larvae can use vision to detect large, active predators but can also detect predators through olfaction when visual cues are unreliable.     

Effects of size on predation risk,behavioural response to fish,and cost of reduced feeding in larval Ischnura verticalis (Coenagrionidae: Odonata)

Summary We used laboratory studies to examine the role of predation risk and cost of anti-predator behaviour in determining the behavioural response of several larval instars of Ischnura verticalis to a fish predator (Lepomis gibbosus). Smaller larvae were less susceptible to fish predation than larger larvae. Smaller larvae depressed movement to a greater degree in the presence of fish than did larger larvae; large larvae were generally less active than small larvae regardless of fish presence. Reduced feeding resulted in smaller larvae suffering more in terms of reduced growth than did large larvae. In general, our results tend to support the hypothesis that individuals that suffer high costs of anti-predator behaviour but little risk of predation may only exhibit anti-predator behaviours in the presence of predators, whereas individuals with a higher risk of predation and a lower cost of anti-predator behaviour may evolve anti-predator mechanisms that are in effect even in the absence of predators.     

Loss of larval parasitism in parasitengonine mites

Larval Parasitengona are typically parasites, yet at least 29 species of water mites and one species of Trombidiidae forgo larval feeding and any association with a host. Species with non-feeding larvae are isolated cases within species groups or genera where the remaining species have parasitic larvae. Species without larval parasitism occur in at least 14 genera, eight families and four superfamilies of water mites; the loss of larval parasitism is presumably polyphyletic, having occurred at least 21 times. Lineages of water mites with non-feeding larvae frequently exist in parallel with almost identical populations or species that have parasitic larvae. Thus, there is tremendous potential for studies comparing the relative merits of the two life history strategies. Comparisons indicate that adults from lineages with non-parasitic larvae produce smaller numbers of larger eggs; the extra nutrition included in larger eggs permits the larvae to forgo feeding. Non-feeding larvae frequently have wider dorsal plates but reduced leg length, setal length and sclerotization when compared to parasitic larvae from sister lineages. The adults of lineages with non-feeding larvae are frequently smaller in comparison to adults of sister lineages with parasitic larvae. There is no apparent pattern in relation to habitat: lineages lacking larval parasitism occur in streams, temporary ponds and the littoral and planktonic regions of permanent lakes. © Rapid Science Ltd. 1998     

The effect of invertebrate and vertebrate predators on the foraging movements of Ischnura elegans larvae (Odonata: Zygoptera)

SUMMARY.

• 1 The foraging movements of late instar Ischnura elegans larvae were monitored in laboratory experiments to study the effects of predators on larval feeding behaviour.
• 2 Ischnura larvae are sit-atid-wait, or ambush, foragers, moving occasionally between perches in search of profitable feeding sites. Larval foraging movements, monitored at different densities of Daphnia prey, increased significantly when prey were absent.
• 3 In experiments without prey, larval movement was inhibited by the presence of fish predators, as well as by invertebrate predators (Notonecta glauca), but not by closely related, non-predatory invertebrates (Corixa punctata) or physical disturbance of the water (intermittent air bubbles).
• 4 Further experiments varied Ischnura hunger levels (0–8 days without food) and illumination (light or dark) with and without notonectid predators. Hunger had no consistent effect on penultimate instar behaviour but final instar foraging activity was significantly modified: movements increased after 4 days starvation and decreased again after 8 days. This response was suppressed by the presence of predators. Both larval instars moved significantly less often in the light, even when predators were absent.
• 5 These phenotypically flexible predator-avoidance responses are likely to decrease the risk of predation by both visual and tactile predators. However, predators clearly have an important influence on the feeding niche of Ischnura larvae, and may decrease the overall feeding efficiency, growth rate, and survival of larvae by constraining their movement in search of profitable feeding sites.

     

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.     

Hunger‐dependent and sex‐specific antipredator behaviour of larvae of a size‐dimorphic mosquito

1. Modification of behaviours in the presence of predators or predation cues is widespread among animals. The costs of a behavioural change in the presence of predators or predation cues depend on fitness effects of lost feeding opportunities and, especially when organisms are sexually dimorphic in size or timing of maturation, these costs are expected to differ between the sexes. 2. Larval Aedes triseriatus (Say) (Diptera: Culicidae) were used to test the hypothesis that behavioural responses of the sexes to predation cues have been selected differently due to different energy demands. 3. Even in the absence of water‐borne predation cues, hungry females (the larger sex) spent more time browsing than did males, indicating a difference in energy needs. 4. In the presence of predation cues, well‐fed larvae of both sexes reduced their activity more than did hungry larvae, and males shifted away from high‐risk behaviours to a greater degree than did females, providing the first evidence of sex‐specific antipredator behaviour in foraging mosquito larvae. 5. Because sexual size dimorphism is common across taxa, and energetic demands are probably correlated with size dimorphism, this research demonstrates the importance of investigating sex‐specific behaviour and behavioural responses to enemies, and cautions against generalising results between sexes.     

Wetland type differentially affects ectoparasitic mites and their damselfly hosts

The effect of artificial habitat in altered landscapes on species interactions and their suite of enemies is largely unknown. Water mites have been associated with reduced fitness of model damselflies. Mite parasitism was variable, but higher for Ischnura verticalis damselflies from natural, than from artificial, wetlands in the same region. There were no differences in timing of sampling, temperature during sampling, or host age or sex composition of samples between wetland types. Landscape structure might constrain mite presence or abundance at wetland sites or wetland type might be a better predictor of mites, based on factors such as prey abundance. Fewer mites on damselflies from numerous artificial wetlands means that the strength of parasite-mediated selection is likely less than would be inferred if only natural wetlands were surveyed. Such effects of human changes in habitats on host species probably occur often.     

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.     

Behavioural and life history effects of predator diet cues during ontogeny in damselfly larvae

A central issue in predator–prey interactions is how predator associated chemical cues affect the behaviour and life history of prey. In this study, we investigated how growth and behaviour during ontogeny of a damselfly larva (Coenagrion hastulatum) in high and low food environments was affected by the diet of a predator (Aeshna juncea). We reared larvae in three different predator treatments; no predator, predator feeding on conspecifics and predator feeding on heterospecifics. We found that, independent of food availability, larvae displayed the strongest anti-predator behaviours where predators consumed prey conspecifics. Interestingly, the effect of predator diet on prey activity was only present early in ontogeny, whereas late in ontogeny no difference in prey activity between treatments could be found. In contrast, the significant effect of predator diet on prey spatial distribution was unaffected by time. Larval size was affected by both food availability and predator diet. Larvae reared in the high food treatment grew larger than larvae in the low food treatment. Mean larval size was smallest in the treatment where predators consumed prey conspecifics, intermediate where predators consumed heterospecifics and largest in the treatment without predators. The difference in mean larval size between treatments is probably an effect of reduced larval feeding, due to behavioural responses to chemical cues associated with predator diet. Our study suggests that anti-predator responses can be specific for certain stages in ontogeny. This finding shows the importance of considering where in its ontogeny a study organism is before results are interpreted and generalisations are made. Furthermore, this finding accentuates the importance of long-term studies and may have implications for how results generated by short-term studies can be used.     

Effects of predators and food availability on activity and growth of Chironomus tentans (Chironomidae: Diptera)

1. Larvae of Chironomus tentans Fab, decreased the amount of time they spent outside their tubes as the presence of predatory pumpkinseed sunfish (Lepomis gibbosus L.) increased. Greatest reductions in activity occurred at low levels of fish presence; above a certain level further increases in fish presence had little effect on activity. 2. Whether the pattern of predator presence was ordered or random had no effect on larval behaviour. Larvae did not habituate to short- or long-term predator presence. 3. Larvae were less active when more food was available and predator-induced reductions in activity were negatively related to food availability. Larval activity was much higher in the dark than it was in the light. 4. Over 7 days, presence of fish reduced the proportion of third-instar larvae that moulted but did not affect head width or dry mass; low food availability reduced the number of larvae that moulted as well as head width and dry mass of larvae in the fourth instar. 5. Results indicate that the behavioural response of larval chironomids to predator presence depends strongly on environmental conditions and that estimating the developmental costs of these behavioural responses under field conditions will be complicated.     

Interactions between adult and larval bluegill sunfish: positive and negative effects

Adult fish may affect the growth and survival of conspecific larvae through a variety of pathways, including negative interactions via competition for shared limiting resources or via predation (i.e., cannibalism), and positive interactions due to the consumption of larval predators and via resource enhancement (i.e., presence of adults increases availability of larval prey). To examine the overall effect of adult bluegill sunfish (Lepomis macrochirus) on larval bluegill, we conducted a field experiment in which we manipulated adult densities and quantified larval growth and survival, prey abundance, invertebrate predator abundance, and cannibalism. The presence of adult bluegill had a negative effect on final larval mass. This response was consistent with competition for zooplankton prey. Adult bluegill reduced the abundance of large zooplankton (e.g., Chaoborus and Daphnia), which were the dominant prey of bluegill larvae in the absence of adults. Larvae in the no-adult treatment also had significantly more prey in their stomachs compared to larvae in the presence of adults. Larval survival was maximized at intermediate adult densities and the overall production of larvae peaked at intermediate adult densities. The higher larval survival at intermediate adult densities is attributed to a reduction in invertebrate predators in treatments with adult bluegill; invertebrate predators experienced an 80% reduction in the presence of adult fish. Decreased larval survival at the highest adult density was not due to resource limitation and may be due to cannibalism, which was not directly observed in our study, but has been observed in other studies.     

Parasite-host associations and life cycles of spring-living water mites (Hydrachnidia, Acari) from Luxembourg

Larval water mites are parasites of various insect species. The main aim of the present study was to analyse the host range of spring dwelling water mites. The investigation focuses on seven spring sites in Luxembourg. Some 24 water mite species were recorded either from the benthos or as parasites attached to flying insects captured in emergence traps. For 20 mite species 35 host species from four Nematocera (Diptera) families were recorded. About 80% of the host species and over 90% of the host individuals were Chironomidae, the others were Limoniidae, Dixidae and Simuliidae. For all water mite species recorded we present the observed host spectrum and/or potential hosts as well as the intensity of parasitism and the phenology of the mites. For 10 mite species the hosts were previously unknown. For another ten species the known host spectrum can be confirmed and extended. The host spectrum ranged from one host species (e.g. for Sperchon insignis) to at least 10 host species (for Sperchon thienemanni, Ljania bipapillata), but the effective host range could not be definitively estimated due to the lack of corresponding data. The hypothesised host preference of the water mites, of which most are strictly confined to spring habitats, for similarly spring-preferring hosts could not be proven. The mean intensity of parasitism was highest for Thyas palustris (10.8 larvae/host) and lowest for Sperchon insignis and Hygrobates norvegicus (1.2 larvae per host for each). The hydryphantid mite Thyas palustris occurred at maximal intensity (41 larvae per host) and the two abdominal parasites Ljania bipapillata and Arrenurus fontinalis showed higher mean intensities than the thoracic parasites did. Larval water mites parasitising chironomids did not exhibit a preference for host sex. The phenology of the larval mite species was varied, some species were only present in samples early in the year and others exclusively in the summer. Another species showed two peaks of occurrence, springtime/early summer and late summer/autumn. In conclusion, the water mite larvae in the studied springs showed differences in host spectra and phenology but there are no clear evidences in both for host partitioning. Maybe, the relative low species diversity of water mites in individual springs and the low inter-specific competition for suitable hosts in combination with the high host abundances and species richness makes springs such favourable habitats for the mites.     

Are behavioural traits in prey sensitive to the risk imposed by predatory fish?

1. Behavioural differences among prey species may result from evolutionary adaptations that facilitate coexistence with different predators and influence vulnerability to predators. It has been hypothesised that prey species modify their behaviour in relation to the risk posed by particular predators. 2. We examined the relationship between anti‐predator behaviour and predation risk in five species of larval odonates in combination with three predatory fish species (perch, gudgeon and rudd) that differ in foraging behaviour. The odonates, Platycnemis pennipes, Coenagrion puella, Lestes sponsa, Sympetrum striolatum and Libellula depressa, differ with regard to their life cycle and habitat, including water depth, occurrence in temporary ponds and co‐existence with fish. 3. The odonate species differed in their response to fish: (i) Two species showed a flexible response. Larval C. puella reduced activity in the presence of fish, regardless of species, whereas L. depressa altered their activity only in the presence of gudgeon. (ii) Independent of fish species, all odonates except L. depressa exhibited spatial avoidance of fish. This was interpreted as a more general anti‐predator response. (iii) In some cases the odonates showed no response to predators and their behaviour was thus independent of predation risk. 4. Our results confirm that all odonates responded to the presence of at least some predatory fish, and that some odonate species discriminated between fish species. However, we found no significant correlation between behavioural modifications and predation risk, indicating that anti‐predator responses and predation risk depend on the particular predator and the species being preyed on.     

Effect of group size on parasitism in a natural population of the Baltimore checkerspot Euphydryas phaeton

Summary The effect of group size of early instars on parasitism of Euphydryas phaeton (Nymphalidae) was examined. Different numbers of larvae were stocked per web to determine the effect of group size on parasitism. Larval aggregations of moderate size (the size occurring naturally) had the least parasitism. Larger larval groups had a disproportionately high rate of parasitism. The major larval parasitoids located vulnerable larvae within webs, instead of attacking larvae available on the outside of webs. Parasitism rates were similar for larvae of damaged and undamaged webs, a consequence of the behavior and location of larvae in the webs. Lower limit to group size was a function of facilitation of larval numbers in reaching the first feeding site, the top of the host plant. Feeding facilitation by larval aggregations was not a factor in larval survival or growth.     

Are behavioural responses to predation cues linked across life cycle stages?

1. Prey organisms can perceive cues to predation hazard and adopt low‐risk behaviours to increase survival. Animals with complex life cycles, such as insects, can exhibit such anti‐predatory behaviours in multiple life stages. 2. Cues to predation risk may induce ovipositing females to choose habitats with low predation risk. Cues to predation risk may also induce larvae to adopt facultative behaviours that reduce risk of predation. 3. One hypothesis postulates that anti‐predation behaviours across adult and larval stages may be negatively associated because selection for effective anti‐predator behaviour in one stage leads to reduced selection for avoidance of predators in other stages. An alternative hypothesis suggests that selection by predation favours multi‐component defences, with both avoidance of oviposition and facultative adoption of low‐risk behaviours by larvae. 4. Laboratory and field experiments were used to determine whether defensive responses of adult and larval mosquitoes are positively or negatively associated. The study tested effects of waterborne cues from predatory Toxorhynchites theobaldi on oviposition choices and larval behaviours of three of its common prey: Culex mollis, Limatus durhamii and Aedes albopictus. 5. Culex mollis shows strong anti‐predator responses in both life stages, consistent with the hypothesis of a multi‐component behavioural defence. The other two species showed no detectable responses to waterborne predator cues in either adult or larval stages. Larvae of these unresponsive species were significantly more vulnerable to this predator than was C. mollis. 6. For these mosquitoes, species appear either to have been selected for multi‐component defences against predation or to act in ways that could be called predator‐naïve.     

Condition and fecundity of the damselfly,Enallagma ebrium (Hagen): the importance of ectoparasites

Summary The extent, magnitude, and cause of natural covariation between degree of parasitism and other variables known or suspected of influencing host fitness (such as host age or body size) has been understudied. We demonstrate that degree of parasitism by larval water mites (Arrenurus spp.) was associated with reduced condition of males and with lowered fecundity of young females of the damselfly, Enallagma ebrium (Hagen) (Odonata: Coenagrionidae). We also demonstrate that degree of parasitism can covary with both age and size of host damselflies. We explain the putative causes of such natural covariation, and we suggest that degree of parasitism, host age, and host size can all interact to determine damselfly fitness. We expect that natural covariation between the host's phenotype and degree of parasitism will be frequently observed. Studies of such natural covariation will help researchers to assess better the importance of several variables on host reproductive success and to understand better the dynamics of host-parasite interactions.     

Host-plant effects on larval survival of a salicin-using leaf beetle Chrysomela aeneicollis Schaeffer (Coleoptera: Chrysomelidae)

Several species of willow leaf beetles use hostplant salicin to produce a defensive secretion that consists of salicylaldehyde. Generalist arthropod predators such as ants, ladybird beetles, and spiders are repelled by this secretion. The beetle larvae produce very little secretion when they feed on willows that lack salicylates, and salicin-using beetles prefer salicylate-rich willows over salicylate-poor ones. This preference may exist because the larvae are better defended against natural enemies on salicylate-rich willows. If this is true, the larvae should survive longer on those willows in nature. However, this prediction has not been tested. I determined the larval growth and survival of Chrysomela aeneicollis (Coleoptera: Chrysomelidae) on five willow species (Salix boothi, S. drummondiana, S. geyeriana, S. lutea, and S. orestera). These species differed in their salicylate chemistries and in leaf toughness but not in water content. The water content varied among the individual plants. Larval growth of C. aeneicollis did not differ among the five species in the laboratory, but it varied among the individual plants and it was related to the water content. In the field, C. aeneicollis larvae developed equally rapidly on the salicylate-poor S. lutea and on the salicylate-rich S. orestera. Larval survival was greater on S. orestera than on S. lutea in one year (1986), but there was no difference between them during three succeeding years. In another survivorship experiment, larval survival was low on the medium-salicylate S. geyeriana, but high on the salicylate-poor S. boothi and on S. orestera. Larval survival in the field was related to the larval growth and water content that had been previously measured in the laboratory. These results showed that the predicted relationship between the host plant chemistry and larval survival did not usually exist for C. aeneicollis. One possible reason for this was that the most important natural enemies were specialist predators that were unaffected by the host-derived defensive secretion. One specialist predator, Symmorphus cristatus (Hymenoptera: Eumenidae), probably caused much of the mortality observed in this study. I discuss the importance of other specialist predators to salicin-using leaf beetles.