Immune deployment increases larval vulnerability to predators and inhibits adult life‐history traits in a dragonfly

While deploying immune defences early in ontogeny can trade‐off with the production and maintenance of other important traits across the entire life cycle, it remains largely unexplored how features of the environment shape the magnitude or presence of these lifetime costs. Greater predation risk during the juvenile stage may particularly influence such costs by (1) magnifying the survival costs that arise from any handicap of juvenile avoidance traits and/or (2) intensifying allocation trade‐offs with important adult traits. Here, we tested for predator‐dependent costs of immune deployment within and across life stages using the dragonfly, Pachydiplax longipennis. We first examined how larval immune deployment affected two traits associated with larval vulnerability to predators: escape distance and foraging under predation risk. Larvae that were induced to mount an immune response had shorter escape distances but lower foraging activity in the presence of predator cues. We also induced immune responses in larvae and reared them through emergence in mesocosms that differed in the presence of large predatory dragonfly larvae (Aeshnidae spp.). Immune‐challenged larvae had later emergence overall and lower survival in pools with predators. Immune‐challenged males were also smaller at emergence and developed less sexually selected melanin wing coloration, but these effects were independent of predator treatment. Overall, these results highlight how mounting an immune defence early in ontogeny can have substantial ecological and physiological costs that manifest both within and across life stages.     

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

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The evolution of costly acquired immune memory

A key feature of the vertebrate adaptive immune system is acquired immune memory, whereby hosts launch a faster and heightened response when challenged by previously encountered pathogens, preventing full infection. Here, we use a mathematical model to explore the role of ecological and epidemiological processes in shaping selection for costly acquired immune memory. Applying the framework of adaptive dynamics to the classic SIR (Susceptible‐Infected‐Recovered) epidemiological model, we focus on the conditions that may lead hosts to evolve high levels of immunity. Linking our work to previous theory, we show how investment in immune memory may be greatest at long or intermediate host lifespans depending on whether immunity is long lasting. High initial costs to gain immunity are also found to be essential for a highly effective immune memory. We also find that high disease infectivity and sterility, but intermediate virulence and immune period, increase selection for immunity. Diversity in host populations through evolutionary branching is found to be possible but only for a limited range of parameter space. Our model suggests that specific ecological and epidemiological conditions have to be met for acquired immune memory to evolve.     

Fear and lethality in snowshoe hares: the deadly effects of non‐consumptive predation risk

Predators play a critical, top–down role in shaping ecosystems, driving prey population and community dynamics. Traditionally, studies of predator‐prey interactions have focused on direct effects of predators, namely the killing of prey. More recently, the non‐consumptive effects of predation risk are being appreciated; e.g. the ‘ecology of fear’. Prey responses to predation risk can be morphological, behavioural, and physiological, and are assumed to come at a cost to prey fitness. However, few studies have examined the relationship between predation risk and survival in wild animals. We tested the hypothesis that predation risk itself could reduce survival in wild‐caught snowshoe hares. We exposed female snowshoe hares to a simulated predator (a trained dog) during gestation only, and measured adult survival and, in surviving females, their ability to successfully wean offspring. We show for the first time in a wild mammal that the risk of predation can itself be lethal. Predation risk reduced adult female survival by 30%, and had trans‐generational effects, reducing offspring survival to weaning by over 85% – even though the period of risk ended at birth. As a consequence of these effects the predator‐exposed group experienced a decrease in number, while the control group substantially increased. Challenges remain in determining the importance of risk‐induced mortality in natural field settings; however, our findings show that non‐lethal predator encounters can influence survival of both adults and offspring. Future work is needed to test these effects in free‐living animals.     

A tradeoff between perceived predation risk and energy conservation revealed by an immune challenge experiment

Energy is typically a limiting factor for animals during boreal winters, when low temperatures increase the cost of thermoregulation at the same times as short day‐lengths and snow cover constrain foraging opportunities. Under these circumstances animals use a suite of behavioural and physiological adaptations to avoid overnight starvation. However, it is poorly understood how such strategies are affected by increased energy demands from other physiological systems. Thus, we used free‐ranging blue tits, Cyanistes caeruleus, to test if competing demands for energy (here induced by a non‐inflammatory, antibody‐mediated immune challenge) would affect nocturnal body temperature (a predictor of energy expenditure in small animals) and energy‐saving nest box roosting behaviour. We also assessed if the immune challenge incurred long‐term survival costs. We found no evidence that body temperature regulation differed between immune‐challenged and saline‐injected birds. Nor did the immune challenge reduce survival to the next breeding season. However, old (second winter or older) immune‐challenged birds continued roosting in nest boxes to a larger extent at the peak immune response, despite increased perceived predation risk induced by the preceding capture and immunization. In contrast, old control birds were less prone to roost in nest boxes after capture and saline injection. This difference was less pronounced in young (first winter) birds. We interpret the increased risk‐taking behaviour in immune‐challenged birds as a consequence of a higher need for exploiting the thermal benefits of nest box roosting to reduce energy loss. This suggests that resource deficiency might be a stronger predictor of overnight survival than the threat of nocturnal predation in this system. As such, our study provides insights into the classic tradeoff between starvation and predation risk, in suggesting that priority is given to minimizing the risk of starvation in situations where both starvation and predation risks increase during cold winter nights.     

Interactive effects of productivity and predation on zooplankton diversity

Recent studies suggest the necessity of understanding the interactive effects of predation and productivity on species coexistence and prey diversity. Models predict that coexistence of prey species with different competitive abilities can be achieved if inferior resource competitors are less susceptible to predation and if productivity and/or predation pressure are at intermediate levels. Hence, predator effects on prey diversity are predicted to be highly context dependent: enhancing diversity from low to intermediate levels of productivity or predation and reducing diversity of prey at high levels of productivity or predation. While several studies have examined the interactive effects of herbivory and productivity on primary producer diversity, experimental studies of such effects in predator‐prey systems are rare. We tested these predictions using an aquatic field mesocosm experiment in which initial density of the zooplankton predator Notonecta undulata and productivity were manipulated to test their interactive effects on diversity of seven zooplankton, cladoceran species that were common in surrounding ponds. Two productivity levels were imposed via phosphorus enrichment at levels comparable to low and intermediate levels found within neighboring natural ponds. We used open systems to allow for natural dispersal and behaviorally‐mediated numerical responses by the flight‐capable predator. Effects of predators on zooplankton diversity depended on productivity level. At low and high productivity, prey species richness declined while at high productivity it showed a unimodal relationship with increasing the predator density. Effects of treatments were weaker when using Pielou's evenness index or the inverse Simpson index as measures of prey diversity. Our findings are generally consistent with model predictions in which predators can facilitate prey coexistence and diversity at intermediate levels of productivity and predation intensity. Our work also shows that the functional form of the relationship between prey diversity and predation intensity can be complex and highly dependent on environmental context.     

Immunosenescence in wild animals: meta‐analysis and outlook

Immunosenescence, the decline in immune defense with age, is an important mortality source in elderly humans but little is known of immunosenescence in wild animals. We systematically reviewed and meta‐analysed evidence for age‐related changes in immunity in captive and free‐living populations of wild species (321 effect sizes in 62 studies across 44 species of mammals, birds and reptiles). As in humans, senescence was more evident in adaptive (acquired) than innate immune functions. Declines were evident for cell function (antibody response), the relative abundance of naïve immune cells and an in vivo measure of overall immune responsiveness (local response to phytohaemagglutinin injection). Inflammatory markers increased with age, similar to chronic inflammation associated with human immunosenescence. Comparisons across taxa and captive vs free‐living animals were difficult due to lack of overlap in parameters and species measured. Most studies are cross‐sectional, which yields biased estimates of age‐effects when immune function co‐varies with survival. We therefore suggest longitudinal sampling approaches, and highlight techniques from human cohort studies that can be incorporated into ecological research. We also identify avenues to address predictions from evolutionary theory and the contribution of immunosenescence to age‐related increases in disease susceptibility and mortality.     

Novel molecular approach demonstrates that turbid river plumes reduce predation mortality on larval fish

Turbidity associated with river plumes is known to affect the search ability of visual predators and thus can drive ‘top‐down’ impacts on prey populations in complex ecosystems; however, traditional quantification of predator–prey relationships (i.e. stomach content analysis) often fails with larval fish due to rapid digestion rates. Herein, we use novel molecular genetic methods to quantify larval yellow perch (YP) in predator stomachs in western Lake Erie to test the hypothesis that turbidity drives variation in larval predation. We characterize predator stomach content DNA to first identify YP DNA (single nucleotide polymorphism) and then quantify larval YP predation (microsatellite allele counting) in two river plumes differing in turbidity. Our results showed elevated larval YP predation in the less turbid river plume, consistent with a top‐down impact of turbidity on larval survival. Our analyses highlight novel ecological hypothesis testing using the power of innovative molecular genetic approaches.     

Brain size affects female but not male survival under predation threat

There is remarkable diversity in brain size among vertebrates, but surprisingly little is known about how ecological species interactions impact the evolution of brain size. Using guppies, artificially selected for large and small brains, we determined how brain size affects survival under predation threat in a naturalistic environment. We cohoused mixed groups of small‐ and large‐brained individuals in six semi‐natural streams with their natural predator, the pike cichlid, and monitored survival in weekly censuses over 5 months. We found that large‐brained females had 13.5% higher survival compared to small‐brained females, whereas the brain size had no discernible effect on male survival. We suggest that large‐brained females have a cognitive advantage that allows them to better evade predation, whereas large‐brained males are more colourful, which may counteract any potential benefits of brain size. Our study provides the first experimental evidence that trophic interactions can affect the evolution of brain size.     

Predation risk affects the levels of maternal immune factors in avian eggs

Predation risk is an environmental stressor that can induce changes in prey behavior and physiology. Perception of predation risk may indirectly affect offspring traits and future fitness prospects via impacts on the condition of parents. Females may influence the survival of their offspring via maternal effects, especially when breeding in stressful conditions. We investigated the effects of continuous predation risk perceived by mothers on the maternal allocation of immune factors and carotenoids in eggs of the pied flycatcher Ficedula hypoleuca. We collected eggs from wild pied flycatchers that bred in the vicinity of a predator nest (pygmy owl Glaucidium passerinum), were exposed to cues of a mammalian nest predator (urine of least weasel Mustela nivalis), or received appropriate controls for these two groups. Pied flycatchers transferred more immunoglobulin in eggs under high predation risk in both owl and mammalian predator treatments. The presence of owl nests also lowered the level of lysozyme transferred in the eggs in one of the two study years. Predation risk did not modify egg size or overall carotenoid levels. Our results show that continuous predation risk perceived by females during egg‐laying affects egg composition. This different allocation of maternal immune factors may be an adaptive response evolved to increase the probability of offspring survival.     

SURVIVAL COST OF AN EARLY IMMUNE SOLICITING IN NATURE

If immune functions confer obvious benefits to hosts, life-history theory assumes that they also induce costs, leading to trade-offs between immunity and other fitness components. However, whether substantial fitness costs are associated with immune systems in the wild is debatable, as numerous factors may influence the costs and benefits associated with immune activation. Here, we explore the survival cost of immune deployment in postfledging birds. We injected Eurasian collared dove nestlings ( Streptopelia decaocto ) with antigens from Escherichia coli , and examined whether this immune challenge affected survival after fledging. To assess survival, birds were fitted with radiotags and the fate of each individual was monitored regularly. Our results show that mimicking a bacterial infection in nestlings lowered their survival prospects after fledging, in comparison to controls. The main identified cause of mortality (by examination of dead birds) was presumed to be predation. This study provides experimental evidence that immune activation may entail dramatic survival costs in a free-ranging vertebrate, and emphasizes the potential role that environmental factors such as predation may play in this interaction.     

Examining costs of induced and constitutive immune investment in Tenebrio molitor

Central to the conceptual basis of ecological immunity is the notion that immune effector systems are costly to produce, run, and/or maintain. Using the mealworm beetle, Tenebrio molitor, as a model we investigated two aspects of the costs of innate immunity. We conducted an experiment designed to identify the cost of an induced immune response, and the cost of constitutive investment in immunity, as well as potential interactions. The immune traits under consideration were the encapsulation response and prophylactic cuticular melanization, which are mechanistically linked by the melanin-producing phenoloxidase cascade. If immunity is costly, we predicted reduced longevity and/or fecundity as a consequence of investment in either immune trait. We found a measurable longevity cost associated with producing an inducible immune response (encapsulation). In contrast to other studies, this cost was expressed under ad libitum feeding conditions. We found no measurable costs for constitutive investment in immunity (prophylactic investment in cuticular colour).     

Density‐independent predation affects migrants and residents equally in a declining partially migratory elk population

Migration is expected to benefit individuals through exposure to higher quality forage and reducing predation rates more than non‐migratory conspecifics. Previous studies of partially migratory ungulates (with migrant and resident individuals) have focused on bottom–up factors regulating resident and migrant segments, yet differential predation between strategies could also be a density‐dependent regulatory mechanism. Our study tested for density‐dependence in mortality, as well as mechanisms of ­bottom–up or top–down regulation in the resident and migrant portions of the partially migratory Ya Ha Tinda elk population. We tested for density dependence in adult female and juvenile survival rates, and then discriminated between predator‐ and food‐regulation hypotheses by testing for density‐dependence amongst mortality causes for adult female elk. Notably, the population declined almost 70% from near previously published estimates of carrying capacity over 10 years, providing ideal conditions to test for density dependence. In contrast to predictions, we found only weak support for density dependence in adult survival and juvenile survival. We also found few differences between migrant and resident elk in adult or juvenile survival, though juvenile survival differences were biologically significant. Predation by humans and grizzly bears was density dependent, but similar between migratory strategies. Predation by wolves was the leading known cause of mortality, yet remained constant with declining elk density equally for both migrant and resident elk, indicating wolf predation was density‐independent. Instead of being strongly regulated by food or predation, we found adult female survival was driven by density‐independent predation and climatic factors. The few differences between migratory strategies suggest equivalent fitness payoffs for migrants and residents. This population is being limited by density‐independent predation leading to declines of both migratory strategies. Our results challenge classical predator–prey theory, and call for better integration between predator–prey and migration theory.     

Longevity differs among sexes but is not affected by repeated immune activation in voles (Microtus arvalis)

Investment of resources in immune defences, despite obvious short-term benefits, may be detrimental to long-term maintenance and thus decrease longevity in absence of parasites. In addition, females and males may differ in immune investment and intrinsic longevity because they are subjected to different degrees of sexual competition and extrinsic mortality. In order to test if sex-specific investment in mounting an immune response reduced longevity, we compared the longevity of captive male and female common voles Microtus arvalis regularly challenged with keyhole limpet haemocyanin, an antigen which elicits the production of antibodies, to the longevity of voles injected with the corresponding antigen-free buffer (phosphate-buffered saline). Injections were repeated every 28 days to mimic a chronic infection. The magnitude of immune response did not vary between males and females and did not affect longevity. Overall, females lived longer than males, independently of the immune challenge. Thus, the long-term costs of immunity seem small in voles. The longevity pattern is consistent with the prediction that male-biased predation or parasitism in the wild causes reduced intrinsic lifespan, but this reduction is not mediated by a decrease in male immunity.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 328–333.     

Predation selects for increased immune function in male damselflies, Calopteryx splendens

Predation selects for numerous traits in many animal species, with sick or parasitized prey often being at high risk. When challenged by parasites and pathogens, prey with poor immune functions are thus likely to be at a selective disadvantage. We tested the hypothesis that predation by birds selects for increased immune function in a wild population of male damselflies Calopteryx splendens, while controlling for a trait known to be under selection by bird predation, dark wing-spots. We found that selection on both immune function and wing-spot size was significantly positive, and that selection on either trait was independent of selection on the other. We found no evidence of nonlinear quadratic or correlational selection. In contrast to previous studies, we found no phenotypic correlation between immune function and wing-spot size. There was also no difference in immune response between territorial and non-territorial males. Our study suggests that predation may be an important agent of selection on the immune systems of prey, and because the selection we detected was directional, has the potential to cause phenotypic change in populations.     

Nest Predation Deviates from Nest Predator Abundance in an Ecologically Trapped Bird

In human-modified environments, ecological traps may result from a preference for low-quality habitat where survival or reproductive success is lower than in high-quality habitat. It has often been shown that low reproductive success for birds in preferred habitat types was due to higher nest predator abundance. However, between-habitat differences in nest predation may only weakly correlate with differences in nest predator abundance. An ecological trap is at work in a farmland bird (Lanius collurio) that recently expanded its breeding habitat into open areas in plantation forests. This passerine bird shows a strong preference for forest habitat, but it has a higher nest success in farmland. We tested whether higher abundance of nest predators in the preferred habitat or, alternatively, a decoupling of nest predator abundance and nest predation explained this observed pattern of maladaptive habitat selection. More than 90% of brood failures were attributed to nest predation. Nest predator abundance was more than 50% higher in farmland, but nest predation was 17% higher in forest. Differences between nest predation on actual shrike nests and on artificial nests suggested that parent shrikes may facilitate nest disclosure for predators in forest more than they do in farmland. The level of caution by parent shrikes when visiting their nest during a simulated nest predator intrusion was the same in the two habitats, but nest concealment was considerably lower in forest, which contributes to explaining the higher nest predation in this habitat. We conclude that a decoupling of nest predator abundance and nest predation may create ecological traps in human-modified environments.     

Shaped by the past,acting in the present: transgenerational plasticity of anti‐predatory traits

Phenotypic expression can be altered by direct perception of environmental cues (within‐generation phenotypic plasticity) and by the environmental cues experienced by previous generations (transgenerational plasticity). Few studies, however, have investigated how the characteristics of phenotypic traits affect their propensity to exhibit plasticity within and across generations. We tested whether plasticity differed within and across generations between morphological and behavioral anti‐predator traits of Physa acuta, a freshwater snail. We reared 18 maternal lineages of P. acuta snails over two generations using a full factorial design of exposure to predator or control cues and quantified adult F₂ shell size, shape, crush resistance, and anti‐predator behavior – all traits which potentially affect their ability to avoid or survive predation attempts. We found that most morphological traits exhibited transgenerational plasticity, with parental exposure to predator cues resulting in larger and more crush‐resistant offspring, but shell shape demonstrated within‐generation plasticity. In contrast, we found that anti‐predator behavior expressed only within‐generation plasticity such that offspring reared in predator cues responded less to the threat of predation than control offspring. We discuss the consequences of this variation in plasticity for trait evolution and ecological dynamics. Overall, our study suggests that further empirical and theoretical investigation is needed in what types of traits are more likely to be affected by within‐generational and transgenerational plasticity.     

Prey: predator ratio dependence in the functional response of a freshwater amphipod

1. First known for their shredding activity, freshwater amphipods also behave as active predators with consequences for prey population regulation and amphipod coexistence in the context of biological invasions. 2. A way to quantify predation is to determine the average consumption rate per predator, also known as its functional response (FR). 3. Although amphipods are gregarious and can display social interactions that can alter per capita consumption rates, previous studies using the FR approach to investigate amphipod predation ignored such potential mutual interference because they did not consider variations in predator density. 4. We investigated the FR of Echinogammarus berilloni feeding on dipteran larvae with joint variations in prey and predator densities. This bivariate experimental design allowed us to estimate interference and to compare the fits of the three main classes of theoretical FR models, in which the predation rate is a function of prey density alone (prey‐dependent models), of both prey and predator densities (predator‐dependent models) or of the prey‐to‐predator ratio (ratio‐dependent models). 5. The Arditi–Ginzburg ratio‐dependent FR model provided the best representation of the FR of E. berilloni, whose predation rate showed a decelerating rise to a horizontal asymptote as prey abundance increased. 6. Ratio dependence means that mutual interference between amphipods leads to prey sharing. Mutual interference is likely to vary between amphipod species, depending on their level of aggressiveness.     

Nest survival rates of Red‐crested Cardinals increase with nest age in south‐temperate forests of Argentina

ABSTRACT The main cause of nest mortality for most bird species is predation and nest survival rates often vary in relation to time‐specific variables. Few investigators have examined time‐specific patterns of nest survival in Neotropical birds, and most such studies have focused on tropical and subtropical species. To better understand age‐related patterns of nest survival, we studied nest survival of Red‐crested Cardinals (Paroaria coronata, Thraupidae) in a south‐temperate forest in Argentina. We modeled daily nest survival rates (DSR) using program MARK. We examined the relationship between nest age and nest survival rate, controlling for the effects of physical characteristics of nest sites and progression of the breeding season. We monitored 367 nests for a total of 4018 exposure days. We found that DSR increased with nest age and was higher in small isolated patches than in large continuous patches of forests. The increase of DSR with nest age could be a consequence of more vulnerable nests being predated early in the nesting cycle or a result of parents defending nests more vigorously as nestlings age because of their increasing reproductive value. Open areas of grassland that surrounded the small isolated patches of forests in our study may have been a barrier to predator movements, possibly explaining the lower predation rates. Nest survival rates in our study were lower than those reported for tropical or Nearctic temperate birds, but similar to those reported in other studies of Neotropical temperate birds. Reasons for the low nest survival rates of Neotropical temperate birds remain unclear, and additional studies of predator communities are needed to help elucidate this topic.     

Immune system activation interacts with territory-holding potential and increases predation of the damselfly Calopteryx splendens by birds

Activation of the immune system in insects has been shown to be costly in the laboratory setting, but experimental studies in the field are lacking. The costs of immunity in the wild may be different to those in the laboratory because animals in the wild are simultaneously subjected to a suite of selective agents. We have measured the costs of immune system activation in a wild population of the territorial damselfly Calopteryx splendens. Immune-challenged males were found to be less likely to be territorial and had lower overall survival rates than control or sham-manipulated males. Because territorial males have a higher mating success than nonterritorial males, this result suggests that immune-challenged males are also likely to suffer reduced mating success. However, the activation of the immune system as such did not increase predation risk; this occurred due to a combination of the former with a reduced territory-holding potential. As such, immune-challenged males not holding a territory were most susceptible to predation by birds. The size of the wing spots, a known sexually selected male trait, predicted territorial behaviour in control and sham-manipulated males, but not in immune-challenged males. Our data show that immune system activation can have several costs acting in unison and that ubiquitous ecological interactions, such as predation, may affect trade-offs between immunity and other life history traits.