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.

     

Predation risk and habitat complexity modify intermediate predator feeding rates and energetic efficiencies in a tri‐trophic system

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Habitat heterogeneity and intraguild interactions modify distribution and injury rates in two coexisting genera of damselflies

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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.     

The effects of prey density on survival and growth of damselfly larvae

Abstract.

• 1 Instar 10, 11 and 12 Ischnura larvae were maintained throughout the instar on a constant food supply (Daphnia magna of a standard size).
• 2 A very narrow range of prey availability separated cohorts in which all the larvae successfully moulted to the next instar, from those in which all the larvae died (less than one Daphnia per day in the case of instar 10).
• 3 Larvae were able to survive long periods without food at 16°C.
• 4 Prey availability had a marked effect on development rates, which continued to increase at prey densities well in excess of 100% survival by the larvae.
• 5 The data on Ischnura survival and development rates are compared with previously published general models of these two components of the predators' rate of increase.
• 6 We conclude that starvation is very unlikely to be a significant cause of mortality in the field for Ischnura (or indeed most other Odonata larvae), but that prey availability undoubtedly influences development rates. Natural selection should therefore favour larvae that forage optimally to minimize development times.

     

Use of prey and non-prey food by the ladybird beetle Eriopis connexa (Coleoptera: Coccinellidae) under laboratory-rearing conditions

Prey for predators can fluctuate in abundance and in quality over time requiring predator strategies to cope with food shortage. Coccinellinae are often associated with sap-sucking pests that exhibit high population unpredictability such as aphids and psyllids. Eriopis connexa (Germar) (Coleoptera: Coccinellidae) is a predator with potential for biological control, especially a well-studied population which is resistant to pyrethroids used to control insect defoliators. Both larvae and adult E. connexa were provided ad libitum prey and non-prey foods (pollen and honey water solution) at increasing intervals from 1 to 10 days. Neonate larvae of E. connexa required eating prey daily to develop into adults. However, non-prey food such as honey water solution did prolong larval and adult survival but neither fulfilled larval development nor adult reproduction. Honey water solution promoted 100% adult survival up to 25 days in the adult stage without prey with oviposition returning after daily feeding on prey. Females subjected to increased feeding intervals over four days reduced oviposition and lived longer, but 10-day feeding intervals correlated with risk to adult survival. These results indicate the importance of non-food sources in E. connexa maintenance and the ability of larvae and adult females to compensate for prey scarcity.     

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.     

Interspecific crossing between blue‐tailed damselflies Ischnura elegans and I. senegalensis in the laboratory

Ischnura species (Odonata) are among the most common damselflies in the world, which often exhibit female color polymorphisms. One morph, called androchrome, is similar to males in its color pattern, whereas the other morphs, generally referred to as gynochromes, exhibit female‐specific colors. In several Ischnura species, the female polymorphism is heritable, although molecular and genetic mechanisms remain largely unknown. The dominant‐recessive patterns of the female color morphs may differ between species. For example, androchromic females are dominant to gynochromic females in Ischnura elegans, whereas androchromic females are recessive in Ischnura senegalensis. Here we report a case of interspecific hybridization between a gynochrome female of I. elegans and a male of I. senegalensis in the laboratory. We obtained 61 hybrid adult offspring, of which all 31 females were of gynochrome morph. DNA analyses of the hybrids confirmed that nuclear DNA sequences were derived from both parent species, whereas mitochondrial DNA sequences were maternally inherited. In the hybrids, the postocular spots of female heads, the shape of male appendages, and the color of female's cerci resembled those of I. elegans, whereas the size of abdominal blue spots was similar to that of I. senegalensis. The shape of prothorax and basal abdominal markings were intermediate in females. The larval developmental traits and the morphological changes in the final larval instar of the hybrids were similar to those of I. senegalensis. To our knowledge, this is the first report of hybrids between two damselfly species with different dominant‐recessive patterns of female color morphs.     

Alternative growth and energy storage responses to mortality threats in damselflies

The role of physiology in mediating the growth/predation risk trade‐off has been largely ignored. We examined effects of predation risk on relationships between growth and storage molecules in Enallagma aspersum and Ischnura verticalis damselfly larvae that differ in this trade‐off. In laboratory and field experiments, both species had similar growth and mortality rates and similar concentrations of storage molecules in the absence of mortality threats. However, in the presence of dragonfly predators Ischnura larvae had higher mortality rates and grew faster than Enallagma larvae. Consistent with the difference in growth rate, Enallagma's total protein concentrations decreased under predation risk while those of Ischnura did not. Glucose and glycogen concentrations were not affected, while triglyceride concentrations were lower under predation risk in Enallagma but not in Ischnura. Species differences at the physiological level to the presence of mortality threats may be crucial to understanding patterns in metamorphic and post‐metamorphic traits.     

Spatial avoidance of littoral and pelagic invertebrate predators by <Emphasis Type="Italic">Daphnia</Emphasis>

Studies on spatial avoidance behaviour of predators by prey often ignored the fact that prey typically face multiple predators which themselves interact and show a spatial pattern in abundance and predation rates (PRs). In a series of laboratory experiments, we investigated predation risk (PRI) and horizontal migration of the cladoceran Daphnia magna between open water and vegetation in response to two important invertebrate predators with a contrasting spatial distribution: pelagic Choaborus and vegetation-associated Ischnura. As expected, PRI by Chaoborus was higher in open water due to higher numbers and higher PRs of Chaoborus, while for Ischnura, PRI was highest in the vegetation due to higher densities, despite lower PRs of Ischnura. In accordance with this, Daphnia moved into the vegetation in the presence of the pelagic Chaoborus alone. In the presence of Ischnura alone, however, Daphnia showed no response. We hypothesize this may be the result of a constitutive behaviour of Daphnia to avoid pelagic fish, which impedes a response to the open water. In the combined predator treatment, Daphnia migrated to the open water zone. The increased risk of predation in the vegetation, due to a facilitating effect of Chaoborus on Ischnura PRs is believed to have caused this migration of the Daphnia. This response of Daphnia declined through time and Daphnia moved toward the vegetation. A decline in the activity of the Ischnura larvae through time may have switched the risk balance in favour of the vegetation environment.     

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.     

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.     

Sublethal predation on Stylaria lacustris: a study of regenerative capabilities

Research on predator–prey interaction has generally ignored the possibility of prey injury by predator. Although injured prey usually constitute a minor group in a population, sublethal predation can play an important role in some aquatic assemblages. In a laboratory experiment, I tested the effect of attack by larvae of the damselfly Ischnura elegans and tanyponid Clinotanypus nervosus on the oligochaete Stylaria lacustris. Predation by these insect larvae caused damage to the prey which then are able to escape and survive. More than 50% of the worms used in the experiment were damaged by C. nervosus. Results of predation by I. elegans larvae of different lengths showed that the number of damaged worms decreased with the length of predatory larvae. Small predators injured more worms than large ones, which killed and totally consumed most of the prey. Damage to S. lacustris usually involves the loss of anterior, posterior or both these fragments (middle part preserved). An analysis of the survival of worms revealed that individuals which lost anterior, posterior, or both fragments survived equally well as control ones, with the exception of worms that lost 70% of the body length posteriorly amputated. It should be noted that these worms were the least numerous in all worms damaged by predators. The laboratory experiment on the regenerative capability of S. lacustris showed that after amputation, all worms regenerated the lost structures and started to increase in length. The small individuals after amputation of both anterior and posterior fragments achieved their initial length in the course of the experiment. It is likely that the regenerative capability in S. lacustris is an adaptation to sublethal effects of predation, which seems to play an important role in littoral assemblages dominated by oligochaetes.     

Cyclopoids feed selectively on free-living stages of parasites

1. Many aquatic organisms can consume parasite larvae, thus hampering parasite transmission; however, information about feeding on them in the presence of an alternative prey remains scarce. When having a food choice, predators may decrease parasite consumption, therefore, it is important to assess the role of parasites in the diet of predators in natural communities with different types of prey available. Our study aims to test whether common freshwater cyclopoids feed on trematode free-living stages (cercariae) when an alternative food source is present.
2. We experimentally studied ingestion rates of cyclopoids Macrocyclops distinctus fed with cercariae of trematode Diplostomum pseudospathaceum, a common and harmful parasite of freshwater fishes, and ciliates Paramecium caudatum (an alternative prey, known as suitable food for copepods). First, the feeding response of cyclopoids to different densities of each prey was studied. Then, feeding selectivity in the mixtures of cercariae and ciliates was tested.
3. Feeding rates of cyclopoids increased with prey densities (both ciliates and cercariae) but almost stopped growing at high prey densities, which indicated saturation (Holling type II functional response). In most cases, cyclopoids consumed cercariae at higher rates than ciliates. Maximum ingestion rates estimated from the obtained curves were 37 cercariae ind⁻¹ hr⁻¹ and 17 ciliate ind⁻¹ hr⁻¹.
4. When exposed to prey mixtures, cyclopoids fed on cercariae selectively. When cercariae were offered to cyclopoids at concentrations exceeding the saturation level, the ingestion of ciliates remained constantly low at all ciliate densities. In contrast, the ingestion of cercariae increased with rising cercariae densities even when ciliates were presented ad libitum, decreasing only at very high prey densities. Possible reasons of such feeding preferences are discussed.
5. Our study demonstrated that cyclopoids may prefer to feed on cercariae when there is an alternative food choice and can ingest cercariae at high rates. These experimental results could be extended to natural communities, suggesting that cyclopoids can reduce the transmission of parasites and contribute to the incorporation of parasite production in food webs of lentic ecosystems.

     

Predation and disease: understanding the effects of predators at several trophic levels on pathogen transmission

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Trophic relationships: integrating meiofauna into a realistic benthic food web

• 1 This paper summarises the most important contributions on trophic relationships of lotic meiofauna. In contrast to marine research, the few quantitative studies of the freshwater meiobenthos have shown that these invertebrates not only take up particulate/fine organic matter, but also dissolved organic substances attached to organic particles. In lotic ecosystems, further estimates of grazing rate and bacterial/algal ingestion rate are needed, particularly in situ measurements.
• 2 The effects of macroinvertebrate predators upon meiofauna are still under debate. Depending on the type of experiments (laboratory vs. field) it seems that macrofauna may or may not affect meiofauna. Field samples and analyses of gut contents of larval tanypod chironomids have shown that the impact upon meiofauna was low and larvae were nonselective predators. Predation amounted to 2.2% of the combined prey density and prey consumption averaged 1.3 individuals per predator individual per year.
• 3 Adding taxonomic resolution by including the meiofaunal component within lotic food webs distinctly increases the number of total species and, as a consequence, changes food web statistics. Webs that included meiofauna revealed that these metazoans contributed substantially to the percentage of intermediate species (species with predators and prey). The resolution of dietary analyses of major consumers of macro‐ and meiobenthos showed that many stream invertebrates feed on meiofauna.

     

Predation risk affects egg mortality and carry over effects in the larval stages in damselflies

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Prey selection and baculovirus dissemination by carabid predators of Lepidoptera

Abstract.

• 1 The interaction between coleopteran predators and baculovirus-infected larvae was studied in the laboratory and the field in order to assess the potential role of predators in the dissemination of a nucleopolyhedrovirus (NPV).
• 2 Preference tests using three carabid species, Harpalus rufipes De Geer, Pterostichus melanarius Illiger and Agonum dorsale Pont, showed no evidence of discrimination between healthy and diseased larvae of the cabbage moth Mamestra brassicae L. (Lepidoptera: Noctuidae) as prey items.
• 3 Virus infectivity was maintained after passage through the predator's gut. NPV mortality ranged from 97% to 20% when test larvae were exposed to faeces collected immediately after and 15 days post-infected meal respectively.
• 4 The potential for transfer of inoculum in the environment was estimated in the laboratory by soil bioassay. Carabids continuously passed infective virus to the soil for at least 15 days after feeding on infected larvae.
• 5 Field experiments showed that carabids which had previously fed on diseased larvae transferred sufficient virus to the soil to cause low levels of mortality in larval populations of the cabbage moth at different instars.

     

The biology of Chrysopidae and Hemerobiidae (Neuroptera), with reference to their usage as biocontrol agents: a review

• 1 Many regions have well-developed faunas of Chrysopidae and Hemerobiidae, many of which are potential control agents, but only a few widely distributed species have been seriously considered as such.
• 2 Most of the biological information available concerns Chrysopa species in north temperate areas. C.carnea Stephens, in particular, has been utilised in many pest control programmes. Prepupal or adult diapause constitutes a well-defined stage in the life cycles of many temperate species.
• 3 Larval searching behaviour is efficient, and larvae of most species studied can utilise a wide range of prey organisms or sugar-based foods. The quality of the larval food can affect reproduction of the ensuing adults. Cannibalism is frequent, and may serve as the main food supply when other sources are scarce. Artificial diets for mass rearing are outlined.
• 4 Adult Hemerobiidae are predators. Adult Chrysopidae are either predators or honey-dew feeders, the latter possessing symbiotic yeasts which aid amino acid synthesis. Sprays based on sugar and yeast hydrolysates can be applied in the field as (i) attractants and (ii) alternative or additional food.
• 5 A wide range of predators and hymenopterous parasites attack all stages. Many widespread and non-specific parasites may attack lacewings introduced from other areas.
• 6 Potential use of Chrysopidae and Hemerobiidae in integrated control is enhanced by their tolerance to some insecticides.
• 7 Lacewings are potential control agents of pests in greenhouse, field crops, and orchards. Native species should be augmented rather than others introduced. It would probably be wise to encourage only one or few lacewing species against any given pest.

     

Host-plant effects on Parasyrphus melanderi (Diptera: Syrphidae) feeding on a willow leaf beetle Chrysomela aeneicollis (Coleoptera: Chrysomelidae)

Abstract.

• 1 Generalist predators are repelled by chrysomelid (Chrysomela spp., Phratora vitellinue L.) larval defensive secretions that are obtained from salicin in their host plants. But little is known about the effect of these secretions on specialist predators.
• 2 In this study, we describe the feeding behaviour of a fly, Parasyrphus melanderi Curran (Diptera: Syrphidae), which feeds on Chrysomela aeneicollis Schaeffer (Coleoptera: Chrysomelidae). Parasyrphus melanderi lays its eggs on C.aeneicollis egg clutches, and its larvae consume C.aeneicollis eggs and larvae.
• 3 Chrysomela aeneicollis hatching rates were significantly lower (20%) on clutches with fly eggs than on clutches without them (40%). Half of the clutches with one fly egg had survival rates below 5%, and when two fly eggs were present (four clutches), the entire clutch was consumed.
• 4 In nature, P.melanderi eggs were 3 times more abundant on a salicylaterich willow species S.orestera Schneider, than on the medium-salicylate S.geyeriana Anderss. (1.8 v 0.6 eggs per clutch). On 18% of the S.orestera clones, all the beetle clutches contained fly eggs. In laboratory-choice tests, P.melanderi larvae fed equally rapidly on C.aeneicollis larvae that were chemically defended (feeding on S.orestera) as on larvae that produced no secretion (feeding on the salicylate-poor S.lutea Nutt.). This predator does not appear to be deterred by C.aeneicollis's defensive secretion. We discuss the implications of specialist predators on determining host suitability to herbivorous insects.