Interspecific infanticide deters predators

It is well known that young, small predator stages are vulnerable to predation by conspecifics, intra-guild competitors or hyperpredators. It is less known that prey can also kill vulnerable predator stages that present no danger to the prey. Since adult predators are expected to avoid places where their offspring would run a high predation risk, this opens the way for potential prey to deter dangerous predator stages by killing vulnerable predator stages. We present an example of such a complex predator–prey interaction. We show that (1) the vulnerable stage of an omnivorous arthropod prey discriminates between eggs of a harmless predator species and eggs of a dangerous species, killing more eggs of the latter; (2) prey suffer a minor predation risk from newly hatched predators; (3) adult predators avoid ovipositing near killed predator eggs, and (4) vulnerable prey near killed predator eggs experience an almost fourfold reduction of predation. Hence, by attacking the vulnerable stage of their predator, prey deter adult predators and thus reduce their own predation risk. This provides a novel explanation for the killing of vulnerable stages of predators by prey and adds a new dimension to anti-predator behaviour.     

Predator avoidance by the freshwater snailPhysella virgata in response to the crayfishProcambarus simulans

Summary We examined predator avoidance behavior of the freshwater snailPhysella (=Physa) virgata in response to the crayfishProcambarus simulans. In both laboratory and field enclosure experiments snails crawled above the waterline for 2 h or longer, then returned to the water.Physella virgata react to chemical signals given off by crayfish actively foraging on conspecific snails; they do not react to inactive crayfish. Low dissolved oxygen, crowding, and disturbance of the sediments did not elicit crawlout behavior. Crawling above the waterline, by reducing the probability of encounter between vulnerable, thin-shelled snails and crayfish, is an adaptive response to predation.     

Zooplankton spine induces aversion in small fish predators

Summary The spined cladoceran Bythotrephes cederstroemi is protected from small fish predators due to the difficulty small fish have in ingesting the spine. Juvenile yellow perch (Perca flavescens) 50–60 mm in length were offered Bythotrephes with alternative prey available in two experiments. First, perch were observed as they gained experience with Bythotrephes and developed aversion to the zooplankter. Perch initially attacked and captured Bythotrephes. However, they struggled to ingest the spined zooplankter, rejected and recaptured it many times, and finally ceased to attack it. Second, perch were offered Bythotrephes with varying portions of the spine removed to clarify the spine's role in inducing such behaviors. Perch showed greater preference to attack nospine and half-spine Bythotrephes, and were less likely to reject and more likely to ingest Bythotrephes with the spine removed. For small or young fish that forage on zooplankton in lakes where Bythotrephes is present, aversion is an efficient response to the conspicuous but unpalatable spined cladoceran. However, aversion allows Bythotrephes, also a predator on zooplankton, to more effectively compete with young fish without an increase in predation risk.     

Habitat partitioning of native and exotic Daphnia in gradients of temperature and food: mesocosm experiments

1. Invasion of tropical zooplankton into temperate lakes provides an interesting opportunity to explore habitat segregation in a thermal gradient. 2. We explored differing vertical positioning of native and exotic Daphnia (Daphnia mendotae and Daphnia lumholtzi) in a large indoor mesocosm system (Plön plankton towers) during 2 month‐long experiments. The two towers were manipulated to provide gradients of both temperature (15–29 °C) and algal food (0.05–0.58 mg C L^?1) and a day–night cycle. 3. Both juvenile and adult D. lumholtzi showed a ‘typical’ vertical migration pattern, with higher densities in the epilimnion at night than during the day. They avoided the food‐poor middle layer. In contrast, D. mendotae adults showed little tendency to migrate into the epilimnion at night, remaining in the cooler hypolimnion while juveniles migrated. The vertical distribution of D. mendotae appeared unaffected by the presence of D. lumholtzi. 4. The strong migration behaviour of D. lumholtzi in the absence of fish cues suggests that this behaviour may be a constitutive trait. Habitat partitioning of the two species is probably the result of different thermal tolerances, with D. mendotae constrained to remaining in deeper water by high temperatures in the epilimnion and the tropical D. lumholtzi able to use the warm epilimnion at night.     

A mechanism for interference between stream predators: responses of the stonefly Agnetina capitata to the presence of sculpins

Summary Mottled sculpins (Cottus bairdi) have a strong negative effect on the ability of the stonefly Agnetina capitata to capture some types of mayfly prey. To determine the mechanism for this interference effect, behavior of Agnetina in the presence and absence of sculpins was observed over 24 h periods (12 h light, 12 h dark), using an infra-red sensitive camera and a time-lapse video recorder. Agnetina larvae reacted to the presence of sculpins by significantly reducing the time they spent off the bottom of the substrate, and by significantly decreasing the amount of time spent moving on the substrate. These experiments suggest that in the presence of fish, stonefly diets may contain a smaller proportion of prey that tend to frequent tops and sides of stones. This behavioral flexibility may be important in streams in that it allows stoneflies to advantageously shift their diets when fish population densities are low.     

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     

The rules of engagement: how to defend against combinations of predators

Studies of inducible defenses have traditionally examined prey responses to one predator at a time. However, prey in nature encounter combinations of predators that should force them to produce phenotypic compromises. We examined how snails (Helisoma trivolvis) alter their phenotype in the presence of three different predator species that were presented alone and in pairwise combinations. When snails were exposed to each predator alone, they formed predator-specific defenses that reflected the differences in each predator’s foraging mode. When snails were exposed to pairwise combinations of predators, their phenotype was dependent on their ability to detect each predator, the risk posed by each predator, and the effectiveness of a given defense against each predator. Consequently, responses to combined predators were typically biased towards one of the predators in the pair. This suggests that prey facing combined predators do not form simple intermediate defenses and, as a result, may experience enhanced mortality risk when they encounter natural predator regimes.     

Why do shallow-water predators migrate? Strategic models and empirical evidence from an estuarine mysid

We investigated factors potentially affecting tidal migrations over the littoral zone by invertebrate predators via a combination of strategic modelling, field observations and laboratory experiments using the mysid Neomysis integer. The models predict the distribution of individuals over the immersed intertidal region under the three different scenarios of diffusive movement, movement up a gradient of prey abundance, and movement towards a specific water depth. We reject the diffusive spread hypothesis since the predicted changes in spatial patterns are qualitatively inconsistent with those of density estimates over the tidal cycle in the field. The foraging hypothesis was consistent with the field samples only if there was a consistent upshore food gradient. Gut contents analysis showed meiofaunal prey were rare, but that organic detritus was the main dietary component. Sediment samples indicated some evidence of an organic matter gradient, but in the laboratory, Neomysis showed no preference for sediment with high organic content. We therefore rejected the foraging hypothesis. The depth-seeking model was not rejected, but laboratory experiments involving responses to various predators of Neomysis provided only weak evidence that depth-seeking was a result of predator avoidance. We hypothesise that the proximate mechanism is most likely to involve behavioural responses to flow conditions.     

The outcome of the invasion of Florida lakes by Daphnia lumholtzi

1. We examined 7–12 years of monthly to quarterly historical data from 15 lakes in FL, U.S.A. to determine the extent and outcome of invasion by the alien cladoceran Daphnia lumholtzi Sars. 2. The alien species was found in 10 of the 15 lakes, including Florida’s three largest lakes: Okeechobee, George and Apopka. All the surveyed lakes had resident populations of the smaller native species Daphnia ambigua Scourfield. 3. In most of the lakes, D. ambigua occurred seven to ninefold more often in plankton samples than D. lumholtzi, and at 10‐ to 100‐fold higher maximal densities. One exception was a small lake in central Florida (Lake Jesup), where D. lumholtzi attained high densities on several occasions in the 10 years of sampling. 4. In Lake Okeechobee, where data were of sufficient quality and quantity to perform statistical analyses, the results of canonical correlation analysis indicated that high densities of D. lumholtzi were correlated with lower concentrations of suspended solids, high algal biomass and higher temperature, whereas the opposite conditions were correlated with high densities of D. ambigua. 5. Based on the majority of data, D. lumholtzi has successfully invaded many lakes in Florida, yet it has not become a substantive component of the zooplankton. Additional research is needed to determine whether resources, fish predation or some other factor is responsible for this outcome of invasion.     

Differing effects of suspended sediments on the performance of native and exotic Daphnia

1. Although large cladocerans are usually uncommon in large rivers, Daphnia lumholtzi (an exotic species in North America) is widespread and occasionally abundant. We collected zooplankton on the Illinois River (Illinois, U.S.A.) in 1995 and 1996 and found that the peak density of D. lumholtzi (25 L⁻¹) typically exceeded that of all native species combined. Maximum density occurred during warm periods (up to 27 °C) when concentrations of inorganic suspended sediments were high (>50 mg L⁻¹).
2. Using a life table experiment, we examined the effects of variation in suspended sediment (0 and 80 mg L⁻¹) and food (10⁴ and 10⁵ Ankistrodesmus cells mL⁻¹) on fitness of D. lumholtzi and the native Daphnia parvula. Daphnia lumholtzi had greater survivorship than D. parvula in most treatments and higher life-time fertility than D. parvula in all treatments. Both species achieved their fastest intrinsic rates of growth in treatments with high food, but their responses to suspended solids differed. The growth rate of D. lumholtzi in high food was slightly increased by higher turbidity, whereas that of D. parvula was depressed.
3. Results suggest that the ability of D. lumholtzi to tolerate suspended solids is an important factor contributing to its success in invading North American rivers.     

Flight morphology of Neotropical butterflies: palatability and distribution of mass to the thorax and abdomen

Summary We test whether palatability of Neotropical butterflies is associated with distribution of mass to the thorax and abdomen. Thoracic mass is predominantly muscle mass, whereas abdominal mass includes organs of digestion, food storage, and reproduction. To escape from predation, butterflies palatable to the rufous-tailed jacamar (Galbula ruficauda) use fast, erratic flight, whereas unpalatable butterflies have defensive chemicals and slow, regular flight patterns. We adjusted for effects of phylogeny and report partial correlations for two levels of analysis: 1) comparisons among-lineage means, which test for correlations between traits of distantly related lineages, and 2) comparisons among deviations from lineage means (or within lineages), which test for correlations between traits of more closely related species.Among lineages for both males (n=10 lineages) and females (n=9), palatability and thoracic mass were positively correlated, whereas palatability and abdominal mass were negatively correlated. An inverse correlation between thoracic and abdominal mass is a consequence of the two segments composing 75% of the total body mass. Predation, indexed by palatability, may select for increased flight speed and thoracic mass at the expense of the abdomen, but relative flight speed and thoracic mass were not significantly correlated.Within lineages (n=45 species for each sex), thoracic mass was uncorrelated with palatability in both sexes. Relative flight speed correlated positively with thoracic mass and negatively with body mass. Palatability and abdominal mass were negatively correlated for males but not females. Hence differences between the sexes in mass distribution suggest differences in reproductive constraints and predation stress.     

Waterborne metals impair inducible defences in Daphnia pulex: morphology, life-history traits and encounters with predators

1.  Inducible defences may be temporary and favoured where predation is intermittent and have been demonstrated in several invertebrates and vertebrates when prey detect chemical cues (kairomones) released by predators. Daphnia pulex (a water flea) exposed to Chaoborus (midge larvae) kairomones produce small neckteeth on the dorsal surface of the head as a defence against this gape-limited predator and survive better in the presence of Chaoborus . Recent studies have shown that waterborne copper (Cu) impairs the induction of neckteeth which could lead to lower survival.
2.  Here, we examined the effects of Cu on morphological changes and shifts in life-history traits in D. pulex exposed to kairomone from Chaoborus americanus . We exposed D. pulex mothers to chemical cues of C. americanus fed on either D. pulex neonates or on brine shrimp Artemia salina , the same Chaoborus cues combined with an environmentally relevant concentration of copper (10 μg L⁻¹), or dechlorinated tap water. We examined several morphological characteristics of neonates and life-historical characteristics of adults as well as assessing survival of neonates by staging encounters with predators.
3.  Neonates from mothers exposed to kairomone plus copper had fewer and shorter neckteeth than neonates from mothers exposed to kairomone alone. Moreover, neonates exposed to Cu had lower survival during encounters with predators than neonates exposed to kairomone without Cu.
4.  Adult female Daphnia exposed to kairomones released more neonates within the first 24 h of brood release and emptied their brood pouches quicker than mothers not exposed to kairomones, irrespective of the presence of Cu.
5.  Impairment by metals of morphological defences in zooplankton could lead to a decline in population density and alter community structure.     

Balancing risks? Responses and non-responses of mayfly larvae to fish and stonefly predators

Summary In a series of laboratory experiments we examined the hypothesis that larvae of stream mayflies would respond to the presence of two different types of predators in such a way as to minimize their risk of being consumed by each. Positioning of larvae (whether they frequent the top, sides, or bottom of stones) of Baetis tricaudatus and Ephemerella subvaria was altered by the presence of predaceous stoneflies (Agnetina capitata) with a larger proportion of the population occurring on the upper surfaces, where the probability of encountering the predator was lowest. The presence of a benthivorous fish (Cottus bairdi) had no significant effects on positioning of the mayfly larvae. Lack of fish effects may reflect an inability of the mayflies to detect or respond to sculpins, or alternately may indicate that sculpins do not normally present a important predation risk for these mayflies. Failure of mayfly prey to account for fish predators when responding to the presence of stoneflies appcars to explain facilitation previously observed between stoneflies and sculpins.     

Invasibility of a reservoir to exotic Daphnia lumholtzi: experimental assessment of diet selection and life history responses to cyanobacteria

SUMMARY 1. In reservoirs of the south-central United States, the exotic cladoceran Daphnia lumholtzi is common during warm midsummer conditions, when cyanobacteria are abundant and native Daphnia are rare. In the current study, we employed surveys, field experiments, and a life table experiment to investigate the role of food quality in explaining the distribution and phenology of D. lumholtzi , relative to two native species ( Daphnia parvula and Daphnia mendotae ).
2. During May–September 2000 in eutrophic McDaniel Lake, Missouri U.S.A., cyanobacteria (primarily Oscillatoria ) first appeared at 6-m depth and then became abundant throughout the epilimnion.
3. During the May field experiment, D. lumholtzi , D. parvula and D. mendotae all consumed a similar diet of algae, showing positive selection for small greens (chlorophytes and cryptophytes <20 μm). During the July experiment, when the epilimnion exceeded 25 °C and cyanobacteria were common in the lake, D. lumholtzi consumed significantly more total algae and more cyanobacteria than the two native species. Although the Daphnia selected against cyanobacteria, all three species consumed about 25% of this food in their diet.
4. A life table experiment compared the responses of D. lumholtzi and D. parvula with variation in density of high-quality food ( Ankistrodesmus ) and concentration of a toxic strain of cyanobacteria ( Anabaena flos-aquae ). Both Daphnia species showed reduced survivorship, fertility and intrinsic rates of increase in response to elevated concentrations of cyanobacteria, particularly at the higher food level.
5. The results suggest that D. lumholtzi shows similar inhibition from cyanobacteria as does the native Daphnia . However, their continued high in situ feeding rates imply that D. lumholtzi is less affected by midsummer conditions in warm-water reservoirs than are native Daphnia .     

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.     

A growth/mortality trade-off in larval salamanders and the coexistence of intraguild predators and prey

Behavioral and morphological traits often influence a key trade-off between resource acquisition and vulnerability to predation, and understanding trait differences between species can provide critical insight into their interactions with other species and their distributions. Such an approach should enhance our understanding of the criteria for coexistence between species that can interact through both competition and predation (i.e. intraguild predators and prey). I conducted a common garden experiment that revealed strong differences between three guild members (larval salamanders Ambystoma laterale, A. maculatum, and A. tigrinum) in behavior, morphology, and growth in the presence and absence of a shared top predator (the larval dragonfly Anax longipes). All three species also reduced their activity and modified their tail fin depth, tail muscle length, and body length in response to non-lethal Anax. Species that act as intraguild predators were more active and could grow faster than their intraguild prey species, but they also suffered higher mortality in laboratory predation trials with Anax. I also used survey data from natural communities to compare the distribution of Ambystoma species between ponds differing in abiotic characteristics and predatory invertebrate assemblages. An intraguild prey species (A. maculatum) was found more reliably, occurred at higher densities, and was more likely to persist late into the larval period in ponds with more diverse invertebrate predator assemblages. Taken together, these results indicate that top predators such as Anax may play an important role in influencing intraguild interactions among Ambystoma and ultimately their local distribution patterns.     

The influence of prey abundance on the feeding ecology of two piscivorous species of coral reef fish

Despite the potential importance of predation as a process structuring coral reef fish communities, few studies have examined how the diet of piscivorous fish responds to fluctuations in the abundance of their prey. This study focused on two species of rock-cod, Cephalopholis cyanostigma (Valenciennes, 1828) and Cephalopholis boenak (Bloch, 1790) (Serranidae), and monitored their diet in two different habitats (patch and contiguous reef) at Lizard Island on the northern Great Barrier Reef, Australia, over a 2-year period. The abundance of the rock-cods and the abundance and family composition of their prey were monitored at the same time. Dietary information was largely collected from regurgitated samples, which represented approximately 60% of the prey consumed and were unbiased in composition. A laboratory experiment showed that fish were digested approximately four times faster than crustaceans, leading to gross overestimation of the importance of crustaceans in the diet. When this was taken into account fish were found to make up over 90% of the diet of both species. Prey fish of the family Apogonidae, followed by Pomacentridae and Clupeidae, dominated the diet of both species of rock-cod. The interacting effect of fluctuations in prey abundance and patterns of prey selection caused dietary composition to vary both temporally and spatially. Mid-water schooling prey belonging to the families Clupeidae and to a lesser extent Caesionidae were selected for over other families. In the absence of these types of prey, apogonids were selected for over the more reef-associated pomacentrids. A laboratory experiment supported the hypothesis that such patterns were mainly due to prey behaviour. Feeding rates of both species of rock-cod were much higher in summer than in winter, and in summer they concentrated on small recruit sized fish. However, there was little variation in feeding rates between habitats, despite apparent differences in prey abundance. In summary, our observations of how the feeding ecology of predatory fish responded to variation in prey abundance provide potential mechanisms for how predation may affect the community structure of coral reef fishes.     

Impact of predation by spiders on a territorial damselfly (Odonata: Calopterygidae)

Summary Predation by orb-weaving spiders and crab spiders on the damselfly Calopteryx haemorrhoidalis was studied at a small stream in Southern France. One species of orb-weaving spider, Larinioides folium, caught 76% of the damselflies which fell prey to spiders. Displacement experiments on spiders on sections of bank and the positioning of webs in male territories show that the density and distribution of damselflies is not influenced by orbweb density or by the position of webs. Predation rates corresponded to orb-web density, but neither for sex nor for stage was there a relationship with damselfly density. Mean daily predation rates ranged between 0.9% for females and 4.1% for adult males. Predation risk to adult damselflies by orb-weaving spiders was male biased, whereas among tenerals there was no bias. Males were captured more frequently at territories near the water. Captures show a maximum at noon when territorial disputes of adult males were most frequent. After orbwebs were placed within territories predation rate of males was strongly increased. Predation risk to adult females in the direct vicinity of the stream was less than in the bank vegetation where they perch close to orbwebs. The risk of predation by crab spiders, which catch damselflies at their perching sites, was not sex-biased.     

Predator-induced phenotypic plasticity in the exotic cladoceran Daphnia lumholtzi

1. The exotic cladoceran Daphnia lumholtzi has recently invaded freshwater systems throughout the United States. Daphnia lumholtzi possesses extravagant head spines that are longer than those found on any other North American Daphnia. These spines are effective at reducing predation from many of the predators that are native to newly invaded habitats; however, they are plastic both in nature and in laboratory cultures. The purpose of this experiment was to better understand what environmental cues induce and maintain these effective predator‐deterrent spines. We conducted life‐table experiments on individual D. lumholtzi grown in water conditioned with an invertebrate insect predator, Chaoborus punctipennis, and water conditioned with a vertebrate fish predator, Lepomis macrochirus. 2. Daphnia lumholtzi exhibited morphological plasticity in response to kairomones released by both predators. However, direct exposure to predator kairomones during postembryonic development did not induce long spines in D. lumholtzi. In contrast, neonates produced from individuals exposed to Lepomis kairomones had significantly longer head and tail spines than neonates produced from control and Chaoborus individuals. These results suggest that there may be a maternal, or pre‐embryonic, effect of kairomone exposure on spine development in D. lumholtzi. 3. Independent of these morphological shifts, D. lumholtzi also exhibited plasticity in life history characteristics in response to predator kairomones. For example, D. lumholtzi exhibited delayed reproduction in response to Chaoborus kairomones, and significantly more individuals produced resting eggs, or ephippia, in the presence of Lepomis kairomones.