Increased susceptibility to predation and altered anti-predator behaviour in an acanthocephalan-infected amphipod

According to the 'parasitic manipulation hypothesis', phenotypic changes induced by parasites in their intermediate hosts are effective means of increasing trophic transmission to final hosts. One obvious prediction, although seldom tested, is that increased vulnerability of infected prey to an appropriate predator should be achieved by the parasite altering the anti-predator behaviour of its intermediate host. In this study, we tested this prediction using the fish acanthocephalan Pomphorhynchus tereticollis and the freshwater amphipod Gammarus pulex. Firstly, we estimated the relative vulnerability of infected and uninfected gammarids to predation by the bullhead Cottus gobio in the field. Second, we investigated under experimental conditions how two common anti-predator behaviours of aquatic invertebrates, refuge use and short-distance reaction to predator chemical cues, were affected by infection status. We found that the prevalence of infection in the field was 10 times higher among gammarids collected from the stomach contents of bullheads compared with free-ranging individuals collected in the same river. In a microcosm uninfected gammarids, but not infected ones, increased the use of refuge in the presence of a bullhead. Finally, a behavioural experiment using an Y-maze olfactometer showed opposite reactions to predator odour. Whereas uninfected gammarids were significantly repulsed by the chemical cues originating from bullheads, infected ones were significantly attracted to the odour of the predator. Taken together, our results suggest that the alteration of anti-predator behaviour in infected G. pulex might enhance predation by bullheads in the field. Reversing anti-predator behaviour might thus be an efficient device by which parasites with complex life-cycles increase their trophic transmission to final hosts. Further studies should pay more attention to both the increased vulnerability of infected prey to an appropriate predator in the field and the influence of parasitic infection on the anti-predator behaviour of intermediate hosts.     

Parasite-induced changes in nitrogen isotope signatures of host tissues

To estimate isotopic changes caused by trematode parasites within a host, we investigated changes in the carbon and nitrogen isotope ratios of the freshwater snail Lymnaea stagnalis infected by trematode larvae. We measured carbon and nitrogen stable isotopes within the foot, gonad, and hepatopancreas of both infected and uninfected snails. There was no significant difference in the delta13C and delta15N values of foot and gonad between infected and uninfected snails; thus, trematode parasite infections may not cause changes in snail diets. However, in the hepatopancreas, delta15N values were significantly higher in infected than in uninfected snails. The 15N enrichment in the hepatopancreas of infected snails is caused by the higher 15N ratio in parasite tissues. Using an isotope-mixing model, we roughly estimated that the parasites in the hepatopancreas represented from 0.8 to 3.4% of the total snail biomass, including the shell.     

Specificity of the Toxoplasma gondii-altered behaviour to definitive versus non-definitive host predation risk

The hypothesis that the parasite Toxoplasma gondii manipulates the behaviour of its intermediate rat host in order to increase its chance of being predated specifically by its feline definitive host, rather than a non-definitive host predator species, was tested. The impact of a range of therapeutic drugs, previously demonstrated to be effective in preventing the development of T. gondii-associated behavioural and cognitive alterations in rats, on definitive-host predator specificity was also tested. Using a Y-shaped maze design, we demonstrated that T. gondii-associated behavioural changes, apparently aimed to increase predation rate, do appear to be specific to that of the feline definitive host--there were significant and consistent differences between the (untreated) infected and uninfected rats groups where T. gondii-infected rats tended to choose the definitive host feline-predator-associated maze arm and nest-box significantly more often than a maze arm or nest-box treated with non-definitive host predator (mink) odour. Drug treatment of infected rats prevented any such host-specificity from being displayed. We discuss our results in terms of their potential implications both for T. gondii epidemiology and the evolution of parasite-altered behaviour.     

Synchrony between parasite development and host behaviour change

Teleost fish are commonly used as model species in laboratory studies of behaviour and ecology. In comparison to other groups of vertebrates used routinely in such studies, however, relatively little attention has been paid to their environmental requirements from a welfare perspective. Fish naturally inhabit a wide variety of aquatic habitats that differ enormously in the range of light environments they provide, and light regime has enormous potential to affect behaviour. Yet the level and quality of illumination (in terms of intensity and wavelength spectrum) provided in experimental studies of fish behaviour is generally designed to maximize ease of recording by the observer. In addition, display or home aquaria provide illumination that maximizes the 'viewing pleasure' of the observer, and specialist lighting tubes are available to stimulate rapid plant growth and to 'show off' the colours of fish, rather than to provide 'natural' light environments. Here we present the results of three studies designed to examine the effects of light intensity, wavelength spectrum and their interactions on the behaviour of a model species commonly used in behavioural studies, the three‐spined stickleback Gasterosteus aculeatus . Our aims are to determine whether unnatural light environments, generated by manipulating light intensity and wavelength spectrum, affect behaviour in ways that may lead to concern for the welfare of fish as research animals or pets.     

Parasite-induced variation in host morphology: brain-encysting trematodes in fathead minnows

Metacercariae of the trematode Ornithodiplostomum ptychocheilus cause a conspicuous enlargement of the cranium of juvenile fathead minnows (Pimephales promelas). Minnows sampled from 2 naturally infected ponds in northern Alberta, Canada, had 12% higher and 7% wider craniums compared to fish from an adjacent, uninfected pond. We tested the prediction that cranial distortion was caused by encystment of metacercariae on the brains of slow-growing minnows in a factorial experiment. Juvenile fish were either exposed once to 120 cercariae or 3 times to 40 cercariae; they were then fed either a low- or high-quantity diet for 8 wk. Results showed that after controlling for host size, cranial heights were affected by infection regime and host diet but not by the infection x diet interaction. Cranial distortion was most prominent in minnows exposed once to cercariae, showing that the rapid, simultaneous growth of metacercariae interfered with the normal development of the cranium. Thus, the expression of the parasite-induced phenotype was context dependent, the result of factors associated with the dynamics of cercariae transmission and host growth rate.     

Genotype and sex-based host variation in behaviour and susceptibility drives population disease dynamics

Host heterogeneity in pathogen transmission is widespread and presents a major hurdle to predicting and minimizing disease outbreaks. Using Drosophila melanogaster infected with Drosophila C virus as a model system, we integrated experimental measurements of social aggregation, virus shedding, and disease-induced mortality from different genetic lines and sexes into a disease modelling framework. The experimentally measured host heterogeneity produced substantial differences in simulated disease outbreaks, providing evidence for genetic and sex-specific effects on disease dynamics at a population level. While this was true for homogeneous populations of single sex/genetic line, the genetic background or sex of the index case did not alter outbreak dynamics in simulated, heterogeneous populations. Finally, to explore the relative effects of social aggregation, viral shedding and mortality, we compared simulations where we allowed these traits to vary, as measured experimentally, to simulations where we constrained variation in these traits to the population mean. In this context, variation in infectiousness, followed by social aggregation, was the most influential component of transmission. Overall, we show that host heterogeneity in three host traits dramatically affects population-level transmission, but the relative impact of this variation depends on both the susceptible population diversity and the distribution of population-level variation.     

Intraguild predation and species exclusions in amphipods: the interaction of behaviour, physiology and environment

1. Data from field surveys, laboratory experiments and computer simulations of community dynamics revealed that a novel interaction among intraguild predation, physiological adaptation and environment may explain the complex distributions of two putatively competing aquatic amphipods. 2. Gammarus pulex and G. tigrinus both thrive in fresh and oligohaline waters in western Europe. However, the native European G. pulex excludes the invading North American G. tigrinus from freshwaters of relatively low conductivity, whereas the reverse occurs at higher conductivities. Additionally, there is much spatio-temporal fluctuation in the patterns of coexistence of these species. 3. Laboratory experiments in The Netherlands and Ireland revealed that mutual predation of moulting individuals occurred frequently between these species. However, predation frequencies were differentially in favour of G. pulex under the ionic conditions to which this species is physiologically adapted (freshwater). On the other hand, predation was not differential under the ionic conditions to which G. tigrinus is physiologically adapted (oligohaline water). 4. A mathematical model, which extends the logistic equation to include mutual intraguild predation, simulated interactions over a range of values of relevant population parameters. This indicated that G. pulex would be excluded when balanced instantaneous rates of mutual predation were combined with the known greater reproductive output of G. tigrinus. However, this reproductive advantage is overcome by any relatively small bias in the instantaneous rate of predation favouring G. pulex, leading to the exclusion of G. tigrinus. This occurs even when the reproductive advantage to G. tigrinus is relatively large. Moreover, the model generated ‘switches’ in species dominance that are determined by the relative values of reproductive rate and mutual predation. The time taken to ‘switch’ may explain the transient periods of apparent coexistence of these species observed in the field. 5. The complex community dynamics of such species may thus be understood in terms of variation in the intensity of species interactions mediated by behavioural, physiological and environmental factors.     

Threat-sensitive anti-intraguild predation behaviour: maternal strategies to reduce offspring predation risk in mites

Predation is a major selective force for the evolution of behavioural characteristics of prey. Predation among consumers competing for food is termed intraguild predation (IGP). From the perspective of individual prey, IGP differs from classical predation in the likelihood of occurrence because IG prey is usually more rarely encountered and less profitable because it is more difficult to handle than classical prey. It is not known whether IGP is a sufficiently strong force to evolve interspecific threat sensitivity in antipredation behaviours, as is known from classical predation, and if so whether such behaviours are innate or learned. We examined interspecific threat sensitivity in antipredation in a guild of predatory mite species differing in adaptation to the shared spider mite prey (i.e. Phytoseiulus persimilis, Neoseiulus californicus and Amblyseius andersoni). We first ranked the players in this guild according to the IGP risk posed to each other: A. andersoni was the strongest IG predator; P. persimilis was the weakest. Then, we assessed the influence of relative IGP risk and experience on maternal strategies to reduce offspring IGP risk: A. andersoni was insensitive to IGP risk. Threat sensitivity in oviposition site selection was induced by experience in P. persimilis but occurred independently of experience in N. californicus. Irrespective of experience, P. persimilis laid fewer eggs in choice situations with the high- rather than low-risk IG predator. Our study suggests that, similar to classical predation, IGP may select for sophisticated innate and learned interspecific threat-sensitive antipredation responses. We argue that such responses may promote the coexistence of IG predators and prey.     

Crawl-out behaviour in response to predation cues in an aquatic gastropod: insights from artificial selection

Local adaptation to predation often occurs in populations experiencing stable predator regimes. Under such conditions, prey species may respond by fine-tuning their behavioural defences towards a local optimum, although it is often difficult to ascertain whether such local adaptation is due to selection on fixed traits, developmental plasticity that is dependent on relatively long term exposure to environmental cues or phenotypic plasticity that can respond rapidly to a changing environment. Here we investigate whether anti-predator behaviour in two populations of the freshwater gastropod Lymnaea stagnalis responded to artificial selection. Previous work had shown that populations of this species showed a higher level of innate avoidance behaviour (crawling above the water line) in the presence of predatory fish compared with sites lacking this predation threat. By selectively breeding from high and low response selection lines, we demonstrated that this crawl-out behaviour responds rapidly to artificial selection: high response selection lines showed a significant increase and low response selection lines a significant decrease in avoidance compared with non-selected control lines. This suggests that the crawl out response in this species is heritable, and that there is potential for a response to selection in natural populations, which may produce the divergence in the plasticity of crawl out behaviour found between gastropod populations experiencing high and low predation intensity.     

Evasive behaviour of a frog in response to bat predation

Chorusing frogs (Physalaemus pustulosus) visually detect hunting bats (Trachops cirrhosus) and models of T. cirrhosus on all but the darkest nights. Detection is apparently communicated rapidly, since all frogs in the area can quit calling withing less than a second of a T. cirrhosus arrival at the pond. Physalaemus pustulosus choruses remain silent longer following trials when a T. cirrhosus model is passed overhead than following normal shutdowns or those caused by a model of a small insectivorous bat. They often do not reduce calling in response to the normal activities of small bats.     

Competition, predation and species responses to environmental change

Despite much effort over the past decade on the ecological consequences of global warming, ecologists still have little understanding of the importance of interspecific interactions in species responses to environmental change. Models predict that predation should mitigate species responses to environmental change, and that interspecific competition should aggravate species responses to environmental change. To test this prediction, we studied how predation and competition affected the responses of two ciliates, Colpidium striatum and Paramecium tetraurelia , to temperature change in laboratory microcosms. We found that neither predation nor competition altered the responses of Colpidium striatum to temperature change, and that competition but not predation altered the responses of Paramecium tetraurelia to temperature change. Asymmetric interactions and temperature-dependent interactions may have contributed to the disparity between model predictions and experimental results. Our results suggest that models ignoring inherent complexities in ecological communities may be inadequate in forecasting species responses to environmental change.     

Rapid growth results in increased susceptibility to predation in Menidia menidia

Abstract Several recent studies have demonstrated that rapid growth early in life leads to decreased physiological performance. Nearly all involved experiments over short time periods (<1 day) to control for potentially confounding effects of size. This approach, however, neglects the benefits an individual accrues by growing. The net effect of growth can only be evaluated over a longer interval in which rapidly growing individuals are allowed the time required to attain the expected benefits of large size. We used two populations of Menidia menidia with disparate intrinsic growth rates to address this issue. We compared growth and survivorship among populations subject to predation in mesocosms under ambient light and temperature conditions for a period of up to 30 days to address two questions: Do the growth rates of fish in these populations respond differently to the presence of predators? Is the previously demonstrated survival cost of growth counterbalanced by the benefits of increased size? We found that growth was insensitive to predation risk: neither population appeared to modify growth rates in response to predation levels. Moreover, the fast‐growing population suffered significantly higher mortality throughout the trials despite being 40% larger than the slow‐growing population at the experiment's end. These results confirm that the costs of rapid growth extend over prolonged intervals and are not ameliorated merely by the attainment of large size.     

Frequency of fault bars in feathers of birds and susceptibility to predation

Fault bars are transparent bands in the feathers of birds produced under stressful and adverse conditions. The frequency of feathers with fault bars is highly heterogeneous among species. We predicted that prey had a higher frequency of fault bars than individuals from the general population, and that a high susceptibility to predation would be associated with a low frequency of fault bars among species of birds because such species would suffer particularly high costs of producing fault bars. The frequency of fault bars in prey was almost three-fold higher than in the general population, based on a database on the frequency of fault bars and susceptibility to predation by the goshawk Accipiter gentilis L., implying intense natural selection against fault bars. A high susceptibility to predation by the sparrowhawk Accipiter nisus L. and the goshawk, relative to what would be expected from their abundance, was associated with a low frequency of fault bars across species, with long distance migration also being negatively associated with frequency of fault bars. Feathers with fault bars were more likely to break than feathers without fault bars, thereby potentially affecting the flight ability of individuals. These findings are consistent with the hypothesis that susceptibility to factors that cause production of fault bars can be modified by natural selection, as illustrated by the impact of predation on the frequency of fault bars.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 334–345.     

The thermal mismatch hypothesis explains host susceptibility to an emerging infectious disease

Parasites typically have broader thermal limits than hosts, so large performance gaps between pathogens and their cold‐ and warm‐adapted hosts should occur at relatively warm and cold temperatures, respectively. We tested this thermal mismatch hypothesis by quantifying the temperature‐dependent susceptibility of cold‐ and warm‐adapted amphibian species to the fungal pathogen Batrachochytrium dendrobatidis (Bd) using laboratory experiments and field prevalence estimates from 15 410 individuals in 598 populations. In both the laboratory and field, we found that the greatest susceptibility of cold‐ and warm‐adapted hosts occurred at relatively warm and cool temperatures, respectively, providing support for the thermal mismatch hypothesis. Our results suggest that as climate change shifts hosts away from their optimal temperatures, the probability of increased host susceptibility to infectious disease might increase, but the effect will depend on the host species and the direction of the climate shift. Our findings help explain the tremendous variation in species responses to Bd across climates and spatial, temporal and species‐level variation in disease outbreaks associated with extreme weather events that are becoming more common with climate change.     

Direct and indirect effects of predation and predation risk in old-field interaction webs

ABSTRACT Indirect effects emerge when a change in the abundance of one species indirectly affects another by changing the abundances of intermediate species-called density-mediated indirect effects-or they arise when one species modifies how two other species interact-called trait-mediated indirect effects. I report on field experiments that evaluated how grass and herb biomass in old-field interaction webs was influenced indirectly by a spider carnivore through its interactions with a generalist and a grass-specialist grasshopper species. I manipulated interaction pathways between the spider and the plants using different combinations of the grasshopper species. I changed the modality of predator-prey interactions to isolate density-mediated from trait-mediated effects using natural spiders (predation spiders) or spiders that were prevented from subduing prey by mouthpart manipulation (risk spiders). I found that indirect effects were stronger in speciose, reticulate food webs than in linear food chains owing to a trait-mediated effect, a diet shift by herbivores in response to predation risk. Spiders alone did not have significant effects on grasshopper densities in the field experiments, removing any possibility of density-mediated indirect effects. The study illustrates that ecologists should not underestimate the importance of behavioral ecology in determining community-level interactions.     

Prey behaviour and size-selective predation by fish

SUMMARY 1. We investigate the role of differential activity of chiro-nomids as an explanation for the size selection of small larvae by fish.
2. In the laboratory, pumpkinseed sunfish (Lepomis gibbosus L.) selectively consumed large larvae of Chironomus tentans Fab. when no tube-building materials were available. Small larvae were selectively consumed when a mud substrate was provided but there was no difference in predation rates on large and small larvae in sand.
3. Small larvae spent more time out of their tubes than large larvae in the presence of fish, which may explain the selection for small larvae in mud. Large larvae apparently compensated for decreased foraging activity in the presence of fish by increasing activity when fish were absent. Visibility of large larvae inside tubes may account for their increased mortality in sand.
4. Our results suggest that differential activity is important in explaining the size-selective mortality observed in the field.     

A small increase in UV-B increases the susceptibility of tadpoles to predation

Increased ultraviolet-B (UV-B) radiation as a consequence of ozone depletion is one of the many potential drivers of ongoing global amphibian declines. Both alone and in combination with other environmental stressors, UV-B is known to have detrimental effects on the early life stages of amphibians, but our understanding of the fitness consequences of these effects remains superficial. We examined the independent and interactive effects of UV-B and predatory chemical cues (PCC) on a suite of traits of Limnodynastes peronii embryos and tadpoles, and assessed tadpole survival time in a predator environment to evaluate the potential fitness consequences. Exposure to a 3 to 6 per cent increase in UV-B, which is comparable to changes in terrestrial UV-B associated with ozone depletion, had no effect on any of the traits measured, except survival time in a predator environment, which was reduced by 22 to 28 per cent. Exposure to PCC caused tadpoles to hatch earlier, have reduced hatching success, have improved locomotor performance and survive for longer in a predator environment, but had no effect on tadpole survival, behaviour or morphology. Simultaneous exposure to UV-B and PCC resulted in no interactive effects. These findings demonstrate that increased UV-B has the potential to reduce tadpole fitness, while exposure to PCCs improves their fitness.