The combined effects of hypoxia and fish kairomones on several physiological and life history traits of Daphnia

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Reinforcing effects of non-pathogenic bacteria and predation risk: from physiology to life history

The important ecological role of predation risk in shaping populations, communities and ecosystems is becoming increasingly clear. In this context, synergistic effects between predation risk and other natural stressors on prey organisms are gaining attention. Although non-pathogenic bacteria can be widespread in aquatic ecosystems, their role in mediating effects of predation risk has been ignored. We here address the hypothesis that non-pathogenic bacteria may reinforce the negative effects of predation risk in larvae of the damselfly Coenagrion puella. We found synergistic effects for all three life history variables studied: mortality increased, growth reductions were magnified and bacterial load was higher when both non-lethal stressors were combined. The combined exposure to the bacterium and predation risk considerably impaired the two key antipredator mechanisms of the damselfly larvae: they no longer reduced their food intake under predation risk and showed a synergistic reduction in escape swimming speed. The reinforcing negative effects on the fitness-related traits could be explained by the observed synergistic effects on food intake, swimming muscle mass, immune function and oxidative damage. These are likely widespread consequences of energetic constraints and increased metabolic rates associated with the fight-or-flight response. We therefore hypothesize that the here documented synergistic interactions with non-pathogenic bacteria may be widespread. Our results highlight the ignored ecological role of non-pathogenic bacteria in reinforcing the negative effects of predation risk on prey organisms.     

No evidence for a cost of selection by carbaryl exposure in terms of vulnerability to fish predation in <Emphasis Type="Italic">Daphnia magna</Emphasis>

Natural populations are exposed to multiple stressors. These stressors may interact, leading to synergistic or antagonistic responses. In addition to these direct interaction effects, there may also be an interaction between stressors through a selection effect: as the population genetically responds to one stressor, it may become more vulnerable to another one, for instance because of an associated reduction in genetic variation. We here capitalized on a selection experiment involving the exposure of Daphnia populations to carbaryl pulses to test the hypothesis that selection imposed by this pesticide may increase vulnerability to fish predation in the resulting population. A direct predation experiment with individuals isolated from carbaryl-exposed and non-exposed populations revealed no effect of prior selection by carbaryl exposure on mortality due to stickleback predation.     

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.     

Two stressors are far deadlier than one

Natural organisms often face a barrage of stressors, both natural and human induced. Two known stressors that impact amphibian populations are pesticides and predators. Recent work by Relyea and by Mills and Relyea reveals strikingly strong, synergistic negative effects of these two factors on amphibian larvae. Adding predation risk on top of supposedly sublethal concentrations of a common pesticide caused a massive increase in larval mortality. Interestingly, the increased mortality did not require exposure to actual predation. That is, simply the 'smell of danger' (predator chemical cues) caused 80-90% of larvae that were held in otherwise 'safe' levels of the pesticide to die. Notably, this effect occurred in some species, but not in others. These new studies highlight the need for further interdisciplinary work on the conditions under which combinations of stressors have particularly strong negative effects on natural organisms.     

Biotic interactions govern genetic adaptation to toxicants

The genetic recovery of resistant populations released from pesticide exposure is accelerated by the presence of environmental stressors. By contrast, the relevance of environmental stressors for the spread of resistance during pesticide exposure has not been studied. Moreover, the consequences of interactions between different stressors have not been considered. Here we show that stress through intraspecific competition accelerates microevolution, because it enhances fitness differences between adapted and non-adapted individuals. By contrast, stress through interspecific competition or predation reduces intraspecific competition and thereby delays microevolution. This was demonstrated in mosquito populations (Culex quinquefasciatus) that were exposed to the pesticide chlorpyrifos. Non-selective predation through harvesting and interspecific competition with Daphnia magna delayed the selection for individuals carrying the ace-1^R resistance allele. Under non-toxic conditions, susceptible individuals without ace-1^R prevailed. Likewise, predation delayed the reverse adaptation of the populations to a non-toxic environment, while the effect of interspecific competition was not significant. Applying a simulation model, we further identified how microevolution is generally determined by the type and degree of competition and predation. We infer that interactions with other species—especially strong in ecosystems with high biodiversity—can delay the development of pesticide resistance.     

Chemical cues from multiple predator-prey interactions induce changes in behavior and growth of anuran larvae

Chemical signals are used as information by prey to assess predation risk in their environment. To evaluate the effects of multiple predators on prey growth, mediated by a change in prey activity, I exposed small and large bullfrog (Rana catesbeiana) larvae (tadpoles) to chemical cues from different combinations of bluegill sunfish (Lepomis macrochirus) and larval dragonfly (Anax junius) predators. Water was regularly transferred from predation trials (outdoor experiment) to aquaria (indoor experiment) in which activity and growth of tadpoles was measured. The highest predation mortality of small bullfrog larvae in the outdoor experiment was due to Anax, and it was slightly lower in the presence of both predators, probably resulting from interactions between predators. There was almost no mortality of prey with bluegill. The activity and growth of small bullfrog larvae was highest in the absence of predators and lowest in the presence of Anax. In the presence of bluegill only, or with both predators, the activity and growth of small bullfrog tadpoles was intermediate. Predators did not affect large tadpole activity and growth. Regressing mortality of small bullfrog tadpoles against activity and growth of bullfrog tadpoles revealed a significant effect for small bullfrog larvae but a non-significant effect for large bullfrog larvae. This shows that the response of bullfrog tadpoles to predators is related to their own body size. The experiment demonstrates that chemical cues are released both as predator odor and as alarm substances and both have the potential to strongly alter the activity and growth of prey. Different mechanisms by which chemical cues may be transmitted to species interactions in the food web are discussed. Received: 28 June 1999 / Accepted: 15 November 1999     

Associational resistance or susceptibility: the indirect interaction between chemically‐defended and non‐defended herbivore prey via a shared predator

Many organisms possess chemical defences against their natural enemies, which render them unpalatable or toxic when attacked or consumed. These chemically‐defended organisms commonly occur in communities with non‐ or less‐defended prey, leading to indirect interactions between prey species, mediated by natural enemies. Although the importance of enemy‐mediated indirect interactions have been well documented (e.g. apparent competition), how the presence of prey chemical defences may affect predation of non‐defended prey in terrestrial communities remains unclear. Here, an experimental approach was used to study the predator‐mediated indirect interaction between a chemically‐defended and non‐defended pest aphid species. Using laboratory‐based mesocosms, aphid community composition was manipulated to include chemically‐defended (CD) aphids Brevicoryne brassicae, non‐defended (ND) aphids Myzus persicae or a mixed assemblage of both species, on Brassica oleracea cabbage plants, in the presence or absence of a shared predator (Chrysoperla carnea larvae). Aphid population growth rates, aphid distributions on host plants and predator growth rates were measured. In single‐species treatments, C. carnea reduced M. persicae population growth rate, but had no significant impact on B. brassicae population growth rate, suggesting B. brassicae chemical defences are effective against C. carnea. Chrysoperla carnea had no significant impact on either aphid species population growth rate in mixed‐species treatments. Myzus persicae (ND) therefore experienced reduced predation in the presence of B. brassicae (CD) through a predator‐mediated indirect effect. Moreover, predator growth rates were significantly higher in the M. persicae‐only treatments than in either the B. brassicae‐only or mixed‐species treatments, suggesting predation was impaired in the presence of B. brassicae (CD). A trait‐mediated indirect interaction is proposed, consistent with associational resistance, in which the predator, upon incidental consumption of chemically‐defended aphids is deterred from feeding, releasing non‐defended aphids from predatory control.     

Complex interactions between native and invasive fish: the simultaneous effects of multiple negative interactions

We suggest that the ultimate outcome of interactions between native species and invasive species (extinction or coexistence) depends on the number of simultaneous negative interactions (competition and predation), which depends on relative body sizes of the species. Multiple simultaneous interactions may constrain the ability of native species to trade fitness components (i.e., reduced growth for reduced risk of predation) causing a spiral to extinction. We found evidence for five types of interactions between the adults and juveniles of introduced western mosquitofish (Gambusia affinis) and the juveniles of native least chub (Iotichthys phlegethontis). We added ten large (23–28 mm) and seven small (9–13 mm) young-of-the-year (YOY) least chub to replicate enclosures with zero, low, and high densities of mosquitofish in a desert spring ecosystem. Treatments with mosquitofish reduced the average survival of least chub by one-third. No small YOY least chub survived in enclosures with high mosquitofish densities. We also performed two laboratory experiments to determine mortality to predation, aggressiveness, and habitat selection of least chub in the presence of mosquitofish. Mean mortality of least chub due to predation by large mosquitofish was 69.7% over a 3-h trial. Least chub were less aggressive, selected protected habitats (Potamogeton spp.), and were more stationary in the presence of mosquitofish where the dominance hierarchy was large mosquitofish>>large least chubsmall mosquitofish>>small least chub. Least chub juveniles appear to be figuratively caught in a vice. Rapid growth to a size refuge could reduce the risk of predation, but the simultaneous effects of competition decreased least chub growth and prolonged the period when juveniles were vulnerable to mosquitofish predation.     

Interacting environmental mosaics drive geographic variation in mussel performance and predation vulnerability

Although theory suggests geographic variation in species' performance is determined by multiple niche parameters, little consideration has been given to the spatial structure of interacting stressors that may shape local and regional vulnerability to global change. Here, we use spatially explicit mosaics of carbonate chemistry, food availability and temperature spanning 1280 km of coastline to test whether persistent, overlapping environmental mosaics mediate the growth and predation vulnerability of a critical foundation species, the mussel Mytilus californianus. We find growth was highest and predation vulnerability was lowest in dynamic environments with frequent exposure to low pH seawater and consistent food. In contrast, growth was lowest and predation vulnerability highest when exposure to low pH seawater was decoupled from high food availability, or in exceptionally warm locations. These results illustrate how interactions among multiple drivers can cause unexpected, yet persistent geographic mosaics of species performance, interactions and vulnerability to environmental change.     

Intraguild predation among larval plethodontid salamanders: a field experiment in artificial stream pools

Intraguild predation can be important in determining community structure and dynamics. Artificial stream pools were used to test for the impacts of intraguild predation among three species of larval plethodontid salamanders. Intraguild predators (large Gyrinophilus porphyriticus and Pseudotriton ruber) significantly decreased the survival of small Pseudotriton ruber. There was a trend toward reduced growth of Pseudotriton and Eurycea cirrigera in the presence of intraguild predators. The presence of large Gyrinophilus significantly reduced the growth rate of large Pseudotriton, both in the absence and presence of intraguild prey. The presence of intraguild prey did not significantly increase the growth rates of the intraguild predators. Intraguild predation is likely to be an important force shaping the evolution and ecology of these salamanders.     

Interactions Between Competition and Predation Shape Early Growth and Survival of Two Neotropical Hylid Tadpoles

Experimental studies in temperate regions have revealed that competition and predation interact to shape aquatic communities. Predators typically reduce the effect of competition on growth and competitors provide alternative prey subjects, which may also alter predation. Here, we examine the independent and combined effects of competition and predation on the survival and growth of hatchling tadpoles of two widespread co‐occurring Neotropical hylid frogs (Agalychnis callidryas and Dendropsophus ebraccatus). Using 400 L mesocosms, we used a 2 × 3 factorial substitutive design, which crossed tadpole species composition with the presence or absence of a free‐roaming predator (Anax amazili dragonfly larva). Dragonflies were effective predators of both species, but had larger effects on A. callidryas survival. Both species had similar growth rates when alone, whereas A. callidryas grew 30 percent faster than D. ebraccatus when they co‐occurred, suggesting interspecific rather than intraspecific competition had relatively stronger effects on D. ebraccatus growth, while the opposite was true for A. callidryas. Predator presence dramatically reduced growth rates of both species and erased this asymmetry. Results suggest that the effects of predator induction (i.e., nonconsumptive effects) on growth were larger than both consumptive and competitive effects. Our study demonstrates that predators have strong effects on both survival and growth of prey, highlighting the potential importance of predators in shaping prey populations and tropical aquatic food web interactions. Abstract in Spanish is available at http://www.blackwell‐synergy.com/loi/btp .     

Impact of intraguild predation on parasitoid foraging behaviour

1. Trophic interactions between predators and parasitoids can be described as intraguild predation (IGP) and are often asymmetric. Parasitoids (typically the IG prey) may respond to the threat of IGP by mitigating the predation risk for their offspring. 2. We used a system with a facultative predator Macrolophus caliginosus, the parasitoid Aphidius colemani, and their shared prey, the aphid Myzus persicae. We examined the functional responses of the parasitoid in the presence/absence of the predator on two host plants (aubergine and sweet pepper) with differing IGP risk. 3. Estimated model parameters such as parasitoid handling time increased on both plants where the predator was present, but impact of the predator varied with plant species. The predator, which could feed herbivorously on aubergine, had a reduced impact on parasitoid foraging on that plant. IG predator presence could reduce the searching effort of the IG prey depending on the plant, and on likely predation risk. 4. The results are discussed with regard to individual parasitoid's foraging behaviour and population stability; it is suggested that the presence of the predator can contribute to the stabilisation of host–parasitoid dynamics     

Non‐pathogenic aquatic bacteria activate the immune system and increase predation risk in damselfly larvae

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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.     

Effects of predation risk and plant resistance on Manduca sexta caterpillar feeding behaviour and physiology

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Habitat complexity and sex-dependent predation of mosquito larvae in containers

Studies in aquatic systems have shown that habitat complexity may provide refuge or reduce the number of encounters prey have with actively searching predators. For ambush predators, habitat complexity may enhance or have no effect on predation rates because it conceals predators, reduces prey detection by predators, or visually impairs both predators and prey. We investigated the effects of habitat complexity and predation by the ambush predators Toxorhynchites rutilus and Corethrella appendiculata on their mosquito prey Aedes albopictus and Ochlerotatus triseriatus in container analogs of treeholes. As in other ambush predator-prey systems, habitat complexity did not alter the effects of T. rutilus or C. appendiculata whose presence decreased prey survivorship, shortened development time, and increased adult size compared to treatments where predators were absent. Faster growth and larger size were due to predator-mediated release from competition among surviving prey. Male and female prey survivorship were similar in the absence of predators, however when predators were present, survivorship of both prey species was skewed in favor of males. We conclude that habitat complexity is relatively unimportant in shaping predator-prey interactions in this treehole community, where predation risk differs between prey sexes.     

Density is more important than predation risk for predicting growth and developmental outcomes in tadpoles of spotted tree frog,Litoria spenceri (Dubois 1984)

The diverse benefits of group living include protection against predators through dilution effects and greater group vigilance. However, intraspecific aggregation can decrease developmental rates and survival in prey species. We investigated the impact on tadpole development and behaviour of the interaction between population density and predation risk. Spotted tree frog (Litoria spenceri: Hylidae, Dubois 1984) tadpoles were kept at one of three different densities (two tadpoles per litre, five tadpoles per litre or 10 tadpoles per litre) until metamorphosis in the presence or absence of predatory cues. We aimed to determine the influence of population density, predation and the interaction of both factors in determining growth rates in tadpoles. Tadpoles were measured weekly to assess growth and development and filmed to quantify differences in activity and feeding frequency between groups. Generally, tadpoles housed without predators had longer developmental periods when housed with a predator, but there was no effect on tail length or total length. There was no effect of either predation cues or density on percentage of individuals feeding or moving. Although the effects of the presence of predators alone may appear to be less than the effects of the presence of competitors, the prioritisation of competitiveness over predator avoidance may increase vulnerability of tadpoles to the lethal threat of predators. This is particularly important in species such as L. spenceri, which is at risk from introduced fish predators.     

Influence of substrate preference and complexity on co-existence of two non-native gammarideans (Crustacea: Amphipoda)

Substrate choice, swimming activity and risk to predation by burbot (Lota lota) of the well established Gammarus roeselii and the invader Dikerogammarus villosus were studied in mixed and single-species aquarium experiments. We used stones, gravel and aquatic weeds (Elodea, Chara) as substrates. We hypothesized that both species have different substrate preferences and that substrate affects the predation risk. We also assumed that presence of D. villosus influences substrate preference and predation risk of G. roeselii since the invader is known to affect the behavior of other gammarids. Adults of D. villosus in single species experiments and juveniles in mixed and single species experiments were evenly distributed over the different substrates but adults in mixed species experiments were more likely to prefer stone substrate. In contrast, adults and juveniles of G. roeselii clearly preferred aquatic weeds independent of the presence/absence of the invader. Both species preferred substrates with fissured surface over substrates with smooth surface. Gammarus roeselii was observed swimming more often than D. villosus in the open water but its swimming activity was lower when its preferred substrate was present compared with its swimming activity if non-preferred substrates were present. Predation rate of burbot on D. villosus was comparatively low and independent of the substrate. Burbot consumed many more G. roeselii than D. villosus, both in mixed and single species experiments. But when the preferred substrate of G. roeselii (weeds) was used in the experiments, predation rate of burbot on G. roeselii was somewhat lower than that when non-preferred substrates were present. The results of the experiments support our hypothesis that the gammarids studied here have different substrate preferences and that presence of the preferred substrate can affect predation risk. However, there is no evidence that presence of D. villosus affected substrate choice or predation risk in G. roeselii. We consider that differences in use of spatial niches permit co-existence of G. roeselii and D. villosus in the wild when substrates are diverse. The fact that G. roeselii than D. villosus is more often observed swimming in the open water may explain its higher risk of being captured by fish.     

Behavioural responses to predation may explain shifts in community structure

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