Trade-offs between maternal foraging and fawn predation risk in an income breeder

The choice of neonatal hiding place is critical for ungulates adopting hiding anti-predator strategies, but the consequences of different decisions have rarely been evaluated with respect to offspring survival. First, we investigated how landscape-scale choices made by roe deer fawns and their mothers affected predation risk by red foxes in a forest–farmland mosaic in southeastern Norway. After, we examined the effect of site-specific characteristics and behaviour (i.e. visibility, mother–fawn distance and abundance of the predator’s main prey item—small rodents) on predation risk. The study of habitat use, selection and habitat-specific mortality revealed that roe deer utilised the landscape matrix in a functional way, with different habitats used for feeding, providing maternal care and as refugia from predation. Mothers faced a trade-off between foraging and offspring survival. At the landscape-scale decisions were primarily determined by maternal energetic constraints and only secondarily by risk avoidance. Indeed, forage-rich habitats were strongly selected notwithstanding the exceptionally high densities of rodents which increased fawn predation. At fine spatial scales, a high visibility of the mother was the major factor determining predation risk; however, mothers adjusted their behaviour to the level of risk at the bed site to minimise predation. Fawns selected both landscape-scale refugia and concealed bed sites, but failure to segregate from the main prey of red foxes led to higher predation. This study provides evidence for the occurrence of spatial heterogeneity in predation risk and shows that energetically stressed individuals can tackle the foraging-safety trade-off by adopting scale-dependent anti-predator responses.     

Meta-analysis of foraging and predation risk trade-offs in terrestrial systems

Although there is ample evidence for the generality of foraging and predation trade-offs in aquatic systems, its application to terrestrial systems is less comprehensive. In this review, meta-analysis was used to analyze experiments on giving-up-densities in terrestrial systems to evaluate the overall magnitude of predation risk on foraging behavior and experimental conditions mediating its effect. Results indicate a large and significant decrease in foraging effort as a consequence of increased predation risk. Whether experiments were conducted under natural or artificial conditions produced no change in the overall effect predation had on foraging. Odor and live predators as a correlate of predation risk had weaker and nonsignificant effects compared to habitat characteristics. The meta-analysis suggests that the effect of predation risk on foraging behavior in terrestrial systems is strongly dependent on the type of predation risk being utilized.     

Trade-offs, temporal variation, and species coexistence in communities with intraguild predation

Intraguild predation/parasitism (IGP: competing species preying on or parasitizing each other) is widespread in nature, but the mechanisms by which intraguild prey and predators coexist remain elusive. Theory predicts that a trade-off between resource competition and IGP should allow local niche partitioning, but such trade-offs are expressed only at intermediate resource productivity and cannot explain observations of stable coexistence at high productivity. Coexistence must therefore involve additional mechanisms beside the trade-off, but very little is known about the operation of such mechanisms in nature. Here I present the first experimental test of multiple coexistence mechanisms in a natural community exhibiting IGP. The results suggest that, when resource productivity constrains the competition-IGP trade-off, a temporal refuge for the intraguild prey can not only promote coexistence, but also change species abundances to a pattern qualitatively different from that expected based on the trade-off or a refuge alone. This is the first empirical study to demonstrate a mechanism for why communities with IGP do not lose species diversity in highly productive environments. These results have implications for diversity maintenance in multi-trophic communities, and the use of multiple natural enemies in biological control.     

The establishment of foraging flocks in house sparrows: risk of predation and daily temperature

Summary The foraging decisions of animals often reflect a trade-off between the risk of predation and efficient foraging. One way an animal may reduce the risk of predation, and hence exploit a resource patch in relative safety, is by foraging in a group. Solitary pioneer sparrows often recruit others to a food source by making chirrup calls in order to establish foraging flocks. This study describes the decisions of house sparrows that arrive at food resources of different risks of predation. Four feeding sites at different distances from a perching site and from an observer were presented to sparrows. When the feeder was adjacent to the perching site and far from the observer, the pioneers chirruped less frequently and were more likely to forage alone than when the feeder was in the other three positions. There were differences in the scanning behaviour of sparrows at these sites, suggesting that they were responding to different risks of predation. Furthermore, the chirrup rates of pioneer sparrows in this study and a previous study were found to be negatively correlated with maximum daily temperature. This is consistent with the hypothesis that energy requirements may affect the flock establishment decisions of sparrows, and that the benefits of foraging in flocks may be greater at lower temperatures.     

The effects of variable predation risk on foraging and growth: less risk is not necessarily better

There is strong evidence that the way prey respond to predation risk can be fundamentally important to the structuring and functioning of natural ecosystems. The majority of work on such nonconsumptive predator effects (NCEs) has examined prey responses under constant risk or constant safety. Hence, the importance of temporal variation in predation risk, which is ubiquitous in natural systems, has received limited empirical attention. In addition, tests of theory (e.g., the risk allocation hypothesis) on how prey allocate risk have relied almost exclusively on the behavioral responses of prey to variation in risk. In this study, we examined how temporal variation in predation risk affected NCEs on prey foraging and growth. We found that high risk, when predictable, was just as energetically favorable to prey as safe environments that are occasionally pulsed by risk. This pattern emerged because even episodic pulses of risk in otherwise safe environments led to strong NCEs on both foraging and growth. However, NCEs more strongly affected growth than foraging, and we suggest that such effects on growth are most important to how prey ultimately allocate risk. Hence, exclusive focus on behavioral responses to risk will likely provide an incomplete understanding of how NCEs shape individual fitness and the dynamics of ecological communities.     

Hunger-dependent predator inspection and foraging behaviours in the threespine stickleback (Gasterosteus aculeatus) under predation risk

Individual fish commonly leave the relative safety of the shoal to approach potential predators at a distance. Not all members of a shoal are equally likely to initiate such predator inspection visits. Here, we show for the first time that the current hunger state of individual fish strongly influences their predator inspection behaviour, as well as their foraging rate, in the face of predation hazard. When all members of threespine stickleback (Gasterosteus aculeatus) test shoals were in a similar hunger state, they were equally likely to inspect a trout predator model alone and did not differ in the frequency of their inspection visits or foraging rate. However, when individual sticklebacks in a shoal differed in their hunger state, the food-deprived (i.e. hungrier) member of the shoal fed at a higher rate, was significantly more likely to initiate solitary predator inspection visits, and inspected the predator model significantly more often than its less hungry (i.e. well-fed) shoal mates. Individual fish which inspected the predator model more frequently also tended to have higher feeding rates. The results indicate that the hungrier fish in a shoal are more willing to take greater risks to inspect a potential threat at a distance, compared with their well-fed shoal mates, and suggest that they may gain a foraging benefit in doing so. If marked asymmetries in hunger state exist among members of fish shoals, then mutual cooperation during predator inspection visits may be difficult to achieve because well-fed individuals are not as likely to initiate or participate in inspection visits as are hungry individuals.Correspondence to: J.-G.J. Godin     

Within-group spatial position in ring-tailed coatis: balancing predation, feeding competition, and social competition

A variety of factors can influence an individual’s choice of within-group spatial position. For terrestrial social animals, predation, feeding success, and social competition are thought to be three of the most important variables. The relative importance of these three factors was investigated in groups of ring-tailed coatis (Nasua nasua) in Iguazú, Argentina. Different age/sex classes responded differently to these three variables. Coatis were found in close proximity to their own age/sex class more often than random, and three out of four age/sex classes were found to exhibit within-group spatial position preferences which differed from random. Juveniles were located more often at the front edge and were rarely found at the back of the group. Juveniles appeared to choose spatial locations based on feeding success and not predation avoidance. Since juveniles are the most susceptible to predation and presumably have less prior knowledge of food source location, these results have important implications in relation to predator-sensitive foraging and models of democratic group leadership. Subadults were subordinate to adult females, and their relationships were characterized by high levels of aggression. This aggression was especially common during the first half of the coati year (Nov–April), and subadults were more peripheralized during this time period. Subadults likely chose spatial positions to avoid aggression and were actively excluded from the center of the group by adult females. In the Iguazú coati groups, it appeared that food acquisition and social agonism were the major determinants driving spatial choice, while predation played little or no role. This paper demonstrates that within-group spatial structure can be a complex process shaped by differences in body size and nutritional requirements, food patch size and depletion rate, and social dominance status. How and why these factors interact is important to understanding the costs and benefits of sociality and emergent properties of animal group formation.     

Trade-offs between time, predation risk and life history, and their implications for biogeography: A systems modelling approach with a primate case study

Group sizes are often considered to be the result of a trade-off between predation risk and the costs of feeding competition. We develop a model to explore the interaction between different ecological constraints on group sizes, using a primate (baboons) case study. The model uses climatic correlates of time budgets to predict maximum ecologically tolerable group size, and climatic predictors of predation risk (reflected mainly in predator density and female body mass) to predict minimum tolerable group size for any given habitat. As well as defining the range of sustainable group sizes for a given habitat, the model also allows us to reliably predict our exemplar taxon's biogeographical distribution across Africa. We also explore the life history implications of the model to ask whether baboons form group sizes which maximise survival or fecundity in the classic trade off between these two key life history variables. Our results indicate that, within the range of study sites in our sample, baboons prefer to maximise fecundity. However, the data indicate that in higher predation risk habitats they would switch to maximising survival at the expense of fecundity. We argue that this is due to the fact that interbirth interval and developmental rates have a ceiling that cannot be breached. Thus, while females can shorten interbirth intervals to compensate for increased predation risk, there is a limit to how much these life history variables can be altered, and when this is reached the best strategy is to maximise survivorship.     

Assessment of predation risk via illumination level: facultative central place foraging in the cricetid rodent Phyllotis darwini

It is well known that the risk of predation affects prey decision making. However, few studies have been concerned with the cues used by prey to assess this risk. Prey animals may use indirect environmental cues to assess predation hazard since direct evaluation may be dangerous. I studied the assessment of predation risk, manipulated via environmental illumination level, and the trade-off between foraging and predation hazard avoidance in the nocturnal rodentPhyllotis darwini (Rodentia: Cricetidae). In experimental arenas I simulated dark and full moon nights (which in nature correlate with low and high predation risk, respectively) and measured the immediate responses of animals to flyovers of a raptor model. Second, varying illumination only, I evaluated patch use, food consumption, central place foraging, and nocturnal variation of body weight. During flyover experiments, animals showed significantly more evasive reactions under full moon illumination than in moonless conditions. In the patch use experiments, rodents significantly increased their giving-up density and decreased their total food consumption under moonlight. On dark nights, rodents normally fed in the food patch, but when illumination was high they became central place foragers in large proportion. Moreover, the body weight of individuals decreased proportionately more during bright nights. These results strongly suggest thatP. darwini uses the level of environmental illumination as a cue to the risk of being preyed upon and may sacrifice part of its energy return to avoid risky situations.     

Spatial position and feeding success in ring-tailed coatis

The location of an animal within a social group has important effects on feeding success. When animals consume quickly eaten food items, individuals located at the front edge of a group typically have greater foraging success. When groups feed at large clumped resources, dominant individuals can often monopolize the resource, leading to higher feeding success in the center of the group. In order to test these predictions, behavioral data relating foraging success to within-group spatial position were recorded from two habituated groups of ring-tailed coatis (Nasua nasua) in Iguazu, Argentina. Foraging success did not fit expected patterns. When feeding on small ground litter invertebrates, coatis had the same foraging success at all spatial positions. This pattern likely resulted from an abundance of invertebrates in the ground litter. When feeding on fruit, individuals in the front of the group had greater feeding success, which was driven by the relatively quick depletion of fruit trees. Dominant juveniles were often located in the front of the group which led to increased access to food. This resulted in higher feeding success on fruits but simultaneously increased their risk of predation. Although groups typically became more elongated and traveled faster when feeding on fruit, it did not appear that the coatis were drastically changing their spacing strategies when switching between the two food types. Paradoxically, spatial position preferences during invertebrate foraging appeared to be driven by fruit trees. Because fruit trees were encountered so frequently, juveniles ranging at the front edge of the group during invertebrate foraging were the first to arrive at fruit trees and thus had higher foraging success. This study demonstrates the importance of how food patch size and depletion rate affect the spatial preferences of individuals.     

A risk-balancing trade off between foraging rewards and predation hazard in a shoaling fish

Summary In controlled experiments, shoaling European minnows fed in equal numbers on two equally-rewarded food patches, and likewise on unequal patches the numbers feeding reflected food levels. For equal food, minnows did not feed at the patch where they had encountered a simulated diving avian predator, whereas they chose to feed at this risky patch when it was more valuable. By avoiding hazard for equal food, but accepting predator risk for higher food rewards, the minnows performed a risk-balancing trade-off.     

Immune function, dominance and mating success in drumming male wolf spiders Hygrolycosa rubrofasciata

In this study, we provide a piece of experimental evidence that immune function is related to dominance and mating success in wild caught male wolf spiders, Hygrolycosa rubrofasciata. In the mating season, H. rubrofasciata males are actively searching for receptive females, and while searching males often engage in agonistic behavior (i.e., agonistic drumming signals, chases, and fights) with each other. The present results demonstrate that dominant males had higher lytic activities in their hemolymph than subordinates. Lytic activity estimates the concentration of antimicrobial peptides with lysozyme-like activity in hemolymph, which have been shown to play an important role in defense against bacteria, viruses, and fungi. Dominants also had higher courtship drumming rates than subordinates. Moreover, winners in mating competition had higher lytic activities than losers, but this was measured nonindependently of dominance status. Among males with mating failure, there was a moderate negative correlation between encapsulation rate and courtship drumming rate, suggesting that low quality males might not be able to bear the immunological costs of courtship behavior. These results suggest that females might gain immunological benefits by preferring vigorous males.     

Uniform predation risk in nature: common,inconspicuous, and a source of error to predation risk experiments

Previous studies indicate that when predation risk is uniform across habitats, foragers concentrate their exploitation in fewer patches. Although uniform predation risk may seem rare in nature, some scenarios might cause it. Testing all scenarios in a single experiment is unfeasible; therefore, we developed a model that points whether concentration of exploitation in specific habitats due to uniform risk requires parameter values similar to what is found in literature. This model was based on Brown’s (Behav Ecol Sociobiol 22:37–47, 1988) fitness function but rescaled to multiple habitats and predators, including uniform risk predators. Deriving function’s maximum allowed comparisons with giving-up density studies. Results showed that uniform predation risk had a u-shaped effect in habitat exploitation, causing a concentration of habitat exploitation at probabilities of survival from 0.2 to 0.8. However, the length of this interval and degree of concentration depended on the value of safety to forager fitness. Heterogeneous, nonuniform, predation risk decreases habitat exploitation where it was higher, therefore suppressing the effect of uniform risk on prey behavior. Time spent in the focal habitat and metabolic costs reduced the detectability of habitat concentration, while total time did not. We also found that uniform risk reduced accuracy of heterogeneous risk measurements. Future studies should aim to control all possible predators, as even the mild ones can induce complex behavior.     

18S rRNA phylogeny of sea spiders with emphasis on the position of Rhynchothoracidae

The phylogenetic relationships among all living families of sea spiders (Arthropoda: Pycnogonida) are investigated using nearly complete 18S rRNA sequences from 57 ingroup species and five chelicerates under the Bayesian and maximum likelihood methods. Monophyly of Colossendeidae, Pycnogonidae, Phoxichilidiidae, Endeidae and Pallenopsidae is consistently supported. However, the genera formerly classified in the family Ammotheidae are split up into two distantly related groups. The genera Ascorhynchus and Eurycyde (here recognized as Ascorhynchidae) are possibly an early offshoot of sea spiders, whereas other ammotheids constitute a robust terminal clade with Pallenopsidae, Phoxichilidiidae and Endeidae. This topology also opposes the prevalent assumption of successive losses and simplification of three kinds of cephalic appendages like in a previous cladistic analysis. At least three independent losses are suggested for palps by the inferred topology, and both chelifores and female ovigers may have been lost twice. Our knowledge of early ontogeny and internal anatomy is more congruent with the present 18S rRNA data. The families Callipallenidae and Nymphonidae with unique “attaching larvae” are grouped together in present molecular trees, suggesting that extended paternal care of offspring evolved only once in Pycnogonida. Confident clustering of Pycnogonidae and Rhynchothoracidae indicates that the number of female genital pores is an evolutionary conservative character.     

Minimizing predation risk in a landscape of multiple predators: effects on the spatial distribution of African ungulates

Studies that focus on single predator-prey interactions can be inadequate for understanding antipredator responses in multi-predator systems. Yet there is still a general lack of information about the strategies of prey to minimize predation risk from multiple predators at the landscape level. Here we examined the distribution of seven African ungulate species in the fenced Karongwe Game Reserve (KGR), South Africa, as a function of predation risk from all large carnivore species (lion, leopard, cheetah, African wild dog, and spotted hyena). Using observed kill data, we generated ungulate-specific predictions of relative predation risk and of riskiness of habitats. To determine how ungulates minimize predation risk at the landscape level, we explicitly tested five hypotheses consisting of strategies that reduce the probability of encountering predators, and the probability of being killed. All ungulate species avoided risky habitats, and most selected safer habitats, thus reducing their probability of being killed. To reduce the probability of encountering predators, most of the smaller prey species (impala, warthog, waterbuck, kudu) avoided the space use of all predators, while the larger species (wildebeest, zebra, giraffe) only avoided areas where lion and leopard space use were high. The strength of avoidance for the space use of predators generally did not correspond to the relative predation threat from those predators. Instead, ungulates used a simpler behavioral rule of avoiding the activity areas of sit-and-pursue predators (lion and leopard), but not those of cursorial predators (cheetah and African wild dog). In general, selection and avoidance of habitats was stronger than avoidance of the predator activity areas. We expect similar decision rules to drive the distribution pattern of ungulates in other African savannas and in other multi-predator systems, especially where predators differ in their hunting modes.     

Climate warming and predation risk during herbivore ontogeny

Phenological effects of climate change are expected to differ among species, altering interactions within ecological communities. However, the nature and strength of these effects can vary during ontogeny, so the net community-level effects will be the result of integration over an individual's lifetime. I resolved the mechanism driving the effects of warming and spider predation risk on a generalist grasshopper herbivore at each ontogenetic stage and quantified the treatment effects on a measure of reproductive fitness. Spiders caused nymphal grasshoppers to increase the proportion of herbs in their diet, thus having a positive indirect effect on grasses and a negative indirect effect on herbs. Warming strengthened the top-down effect by affecting spiders and grasshoppers differently. In cooler, ambient conditions, grasshoppers and spiders had a high degree of spatial overlap within the plant canopy. Grasshopper position was unaffected by temperature, but spiders moved lower in the canopy in response to warming. This decreased the spatial overlap between predator and prey, allowing nymphal grasshoppers to increase daily feeding time. While spiders decreased grasshopper growth and reproductive fitness in ambient conditions, spiders had no effect on grasshopper fitness in warmed treatments. The study demonstrates the importance of considering the ontogeny of behavior when examining the effects of climate change on trophic interactions.     

Female reproductive success and nest predation in polyterritorial wood warblers (Phylloscopus sibilatrix)

Summary Polyterritorial polygyny in passerine birds, i.e., when already-paired males attract females in secondary territories, has been explained by male deception. Secondary females are assumed to make a poor choice, because they lack information about males' pairing status. To date, the deception hypothesis has focused mainly on the hole-nesting pied flycatcher. In this study of polyterritorial wood warblers, an open-nesting species, secondary females did not differ in number of fledged young compared with females of monogamous males, and they fledged even more young than primary females. Nest predation influenced the allocation of paternal care. Almost half of the secondary females had exclusive male assistance because nests of primary females were preyed upon.     

Predator foraging behavior in response to perception and learning by its prey: interactions between orb-spinning spiders and stingless bees

Although rewarded bees learn and remember colors and patterns, they have difficulty in learning to avoid negative stimuli such as decorated spider webs spun by Argiope argentata. A. argentata decorates its web with silk patterns that vary unpredictably (Fig. 1) and thus foraging insects that return to sites where spiders are found encounter new visual cues daily. Stingless bees can learn to avoid spider webs but avoidance-learning is slowed or inhibited by daily variation in web decorations (Figs. 3,4; Tables 1,2). In addition, even if bees learn to avoid decorated webs found in one location, they are unable to generalize learned-avoidance responses to similarly decorated webs found at other sites. A. argentata seems to have evolved a foraging behavior that is tied to the ways insects perceive and process information about their environment. Because of the evolutionary importance of bee-flower interdependence, the predatory behavior of web-decorating spiders may be difficult for natural selection to act against.     

Trade-offs in designing markets with multiple objectives

This paper explores some of the problems involved in designing markets with multiple objectives. The first part of the paper considers the issue of how such markets are designed in theory while the second part reviews some evidence on actual applications in the field of air pollution control.     

Linking movement, diving, and habitat to foraging success in a large marine predator

Establishing where and when predators forage is essential to understanding trophic interactions, yet foraging behavior remains poorly understood in large marine carnivores. We investigated the factors leading to foraging success in gray seals (Halichoerus grypus) in the Northwest Atlantic in the first study to use simultaneous deployments of satellite transmitters, time depth recorders, and stomach-temperature loggers on a free-ranging marine mammal. Thirty-two seals were each fitted with the three types of instrumentation; however, complete records from all three instruments were obtained from only 13 individuals, underscoring the difficulty of such a multi-instrument approach. Our goal was to determine the characteristics of diving, habitat, and movement that predict feeding. We linked diving behavior to foraging success at two temporal scales: trips (days) and bouts (hours) to test models of optimal diving, which indicate that feeding can be predicted by time spent at the bottom of a dive. Using an information-theoretic approach, a Generalized Linear Mixed Model with trip duration and accumulated bottom time per day best explained the number of feeding events per trip, whereas the best predictor of the number of feeding events per bout was accumulated bottom time. We then tested whether characteristics of movement were predictive of feeding. Significant predictors of the number of feeding events per trip were angular variance (i.e., path tortuosity) and distance traveled per day. Finally, we integrated measures of diving, movement, and habitat at four temporal scales to determine overall predictors of feeding. At the 3-h scale, mean bottom time and distance traveled were the most important predictors of feeding frequency, whereas at the 6-h and 24-h time scales, distance traveled alone was most important. Bathymetry was the most significant predictor of feeding at the 12-h interval, with feeding more likely to occur at deeper depths. Our findings indicate that several factors predict feeding in gray seals, but predictor variables differ across temporal scales such that environmental variation becomes important at some scales and not others. Overall, our results illustrate the value of simultaneously recording and integrating multiple types of information to better understand the circumstances leading to foraging success.