The context dependence of non-consumptive predator effects.

Non-consumptive predator effects (NCEs) are now widely recognised for their capacity to shape ecosystem structure and function. Yet, forecasting the propagation of these predator-induced trait changes through particular communities remains a challenge. Accordingly, focusing on plasticity in prey anti-predator behaviours, we conceptualise the multi-stage process by which predators trigger direct and indirect NCEs, review and distil potential drivers of contingencies into three key categories (properties of the prey, predator and setting), and then provide a general framework for predicting both the nature and strength of direct NCEs. Our review underscores the myriad factors that can generate NCE contingencies while guiding how research might better anticipate and account for them. Moreover, our synthesis highlights the value of mapping both habitat domains and prey-specific patterns of evasion success ('evasion landscapes') as the basis for predicting how direct NCEs are likely to manifest in any particular community. Looking ahead, we highlight two key knowledge gaps that continue to impede a comprehensive understanding of non-consumptive predator-prey interactions and their ecosystem consequences; namely, insufficient empirical exploration of (1) context-dependent indirect NCEs and (2) the ways in which direct and indirect NCEs are shaped interactively by multiple drivers of context dependence.

The Enemy Within: How Does a Bacterium Inhibit the Foraging Aptitude and Risk Management Behavior of Allenby's Gerbils?

AbstractMicrobes inhabiting multicellular organisms have complex, often subtle effects on their hosts. Gerbillus andersoni allenbyi are commonly infected with Mycoplasma haemomuris-like bacteria, which may cause mild nutrient (choline, arginine) deficiencies. However, are there more serious ecological consequences of infection, such as effects on foraging aptitudes and risk management? We tested two alternatives: the nutrient compensation hypothesis (does nutrient deficiency induce infected gerbils to make up for the shortfall by foraging more and taking greater risks?) and (2) the lethargy hypothesis (do sick gerbils forage less, and are they compromised in their ability to detect predators or risky microhabitats?). We compared the foraging and risk management behavior of infected and noninfected gerbils. We experimentally infected gerbils with the bacteria, which allowed us to compare between noninfected, acutely infected (peak infection loads), and chronically infected (low infection loads) individuals. Our findings supported the lethargy hypothesis over the nutrient compensation hypothesis. Infected individuals incurred dramatically elevated foraging costs, including less efficient foraging, diminished "quality" of time spent vigilant, and increased owl predation. Interestingly, gerbils that were chronically infected (lower bacteria load) experienced larger ecological costs than acutely infected individuals (i.e., peak infection loads). This suggests that the debilitating effects of infection occur gradually, with a progressive decline in the quality of time gerbils allocated to foraging and managing risk. These increased long-term costs of infection demonstrate how small direct physiological costs of infection can lead to large indirect ecological costs. The indirect ecological costs of this parasite appear to be much greater than the direct physiological costs.

Cancer Community Ecology.

Here we advocate Cancer Community Ecology as a valuable focus of study in Cancer Biology. We hypothesize that the heterogeneity and characteristics of cancer cells within tumors should vary systematically in space and time and that cancer cells form local ecological communities within tumors. These communities possess limited numbers of species determined by local conditions, with each species in a community possessing predictable traits that enable them to cope with their particular environment and coexist with each other. We start with a discussion of concepts and assumptions that ecologists use to study closely related species. We then discuss the competitive exclusion principle as a means for knowing when two species should not coexist, and as an opening towards understanding how they can. We present the five major categories of mechanisms of coexistence that operate in nature and suggest that the same mechanisms apply towards understanding the diversification and coexistence of cancer cell species. They are: Food-Safety Tradeoffs, Diet Choice, Habitat Selection, Variance Partitioning, and Competition-Colonization Tradeoffs. For each mechanism, we discuss how it works in nature, how it might work in cancers, and its implications for therapy.

Intercontinental test of constraint-breaking adaptations: Testing behavioural plasticity in the face of a predator with novel hunting strategies.

Constraint-breaking adaptations are evolutionary tools that provide a mechanism for incumbent-replacement between species filling similar ecological roles. In common-garden experiments, we exposed populations of two desert rodents to two different viper species, testing their ability to adjust to novel predators that use different hunting strategies. We aimed to understand whether both predators and prey with constraint-breaking adaptations actually manifest comparative advantage over their counterparts. We used convergent species from desert dunes in the Mojave Desert in North America, Merriam's kangaroo rat Dipodomys merriami and the sidewinder rattlesnake Crotalus cerastes, and from the Negev Desert in the Middle East, the greater Egyptian gerbil Gerbillus pyramidum and the Saharan horned viper Cerastes cerastes. Both Mojave species hold constraint-breaking adaptations in relation to their counterparts from the Negev. The rattlesnakes have heat sensing organs (pits) and the kangaroo rats have fur-lined cheek pouches that allow for greater foraging efficiency and food preservation. Using patch-use theory, we evaluated the rodents' risk-assessment from each snake-separately, together and in combination with barn owls. Initially each rodent species foraged less in the presence of its familiar snake, but within a month both foraged less in the presence of the pit-viper (sidewinder). Our findings indicate a level of learning, and behavioural plasticity, in both rodents and ability to assess the risk from novel predators. The kangaroo rats were capable of harvesting far greater amounts of resources under the same conditions of elevated risk. However, the reason for their advantage may lie in bi-pedal agility and not only their ability collect food more efficiently.

Individual willingness to leave a safe refuge and the trade-off between food and safety: a test with social fish.

Refuges offer prey animals protection from predation, but increased time spent hiding can reduce foraging opportunities. Within social groups, individuals vary in their refuge use and willingness to forage in the presence of a predator. Here, we examine the relative foraging benefits and mortality costs associated with individual refuge use and foraging behaviour within groups of goldfish (Carassius auratus) under predation risk from an avian predator (little egret-Egretta garzetta). We assessed individual order of emergence from the refuge and participation over 15 group foraging outings, and assigned each fish a daily outing index score. The individual fish that emerged from the refuge earlier than the other group members and that participated in more outings received high outing index scores and consumed more food compared with fish that tended to emerge in posterior positions and participate in fewer outings. However, individual fish that attained high outing index scores suffered a higher risk of predation. Furthermore, the amount of time the egret spent at the pool affected group foraging behaviour: as predation risk increased, groups of fish consumed significantly less food. Our results exemplify the trade-off between foraging success and safety from predation that prey species regularly experience.

State-dependent foraging among social fish in a risky environment.

In the presence of a predator, foraging is a dangerous task. Social individuals can respond to risk by forming groups, benefiting from enhanced collective anti-predator behavior but suffering from increased conspicuousness to predators. Within groups, individuals exhibit variable foraging behavior. One important factor influencing risky foraging behaviour is current energetic state, and individuals must trade off food and safety by deciding when to leave a protected refuge in order to find food. We generated mixed groups of goldfish (Carassius auratus) containing equal numbers of underfed and well-fed individuals and examined individual refuge use and willingness to take risks venturing into risky foraging areas in the presence of an avian predator (little egret-Egretta garzetta). Underfed fish exhibited higher levels of risky behaviour by participating in more foraging outings and emerging from the refuge in frontal group positions, compared with well-fed individuals. As expected, underfed fish benefitted by consuming more food, but surprisingly did not experience higher rates of mortality. This may be due to the fact that the egret predator rarely captured the first fish to emerge from the refuge, preferentially attacked groups of three or more fish, and often captured fish in the chaotic period following a failed initial strike. We demonstrate how differences in energetic condition can influence risk-taking behaviours among social individuals that subsequently influence relative levels of foraging success and group fission-fusion dynamics. Moreover, our results illustrate the risk associated with foraging in larger groups.

Can we predict the success of a parasite to colonise an invasive host?

To understand whether a parasite can exploit a novel invasive host species, we measured reproductive performance (number of eggs per female per day, egg size, development rate and size of new imagoes) of fleas from the Negev desert in Israel (two host generalists, Synosternus cleopatrae and Xenopsylla ramesis, and a host specialist, Parapulex chephrenis) when they exploited either a local murid host (Gerbillus andersoni, Meriones crassus and Acomys cahirinus) or two alien hosts (North American heteromyids, Chaetodipus penicillatus and Dipodomys merriami). We asked whether (1) reproductive performance of a flea differs between an alien and a characteristic hosts and (2) this difference is greater in a host specialist than in host generalists. The three fleas performed poorly on alien hosts as compared to local hosts, but the pattern of performance differed both among fleas and within fleas between alien hosts. The response to alien hosts did not depend on the degree of host specificity of a flea. We conclude that successful parasite colonisation of an invasive host is determined by some physiological, immunological and/or behavioural compatibility between a host and a parasite. This compatibility is unique for each host-parasite association, so that the success of a parasite to colonise an invasive host is unpredictable.

How does the presence of a conspecific individual change the behavioral game that a predator plays with its prey?

Behavioral games predators play among themselves may have profound effects on behavioral games predators play with their prey. We studied the behavioral game between predators and prey within the framework of social foraging among predators. We tested how conspecific interactions among predators (little egret) change the predator-prey behavioral game and foraging success. To do so, we examined foraging behavior of egrets alone and in pairs (male and female) in a specially designed aviary consisting of three equally spaced pools with identical initial prey (comet goldfish) densities. Each pool was comprised of a risky microhabitat, rich with food, and a safe microhabitat with no food, forcing the fish to trade off food and safety. When faced with two versus one egret, we found that fish significantly reduced activity in the risky habitat. Egrets in pairs suffered reduced foraging success (negative intraspecific density dependence) and responded to fish behavior and to their conspecific by changing their visiting regime at the different pools-having shorter, more frequent visits. The time egret spent on each visit allowed them to match their long-term capture success rate across the environment to their capture success rate in the pool, which satisfies one aspect of optimality. Overall, egrets in pairs allocated more time for foraging and changed their foraging tactics to focus more on fish under cover and fish 'peeping' out from their shelter. These results suggest that both prey and predator show behavioral flexibility and can adjust to changing conditions as needed in this foraging game.

Everybody loses: intraspecific competition induces tragedy of the commons in Allenby's gerbils.

Interference competition may lead to a tragedy of the commons in which individuals driven by self-interest reduce the fitness of the entire group. We investigated this hypothesis in Allenby's gerbils, Gerbillus andersoni allenbyi, by comparing foraging behaviors of single vs. pairs of gerbils. We recorded strong interference competition within the foraging pairs. Competition reduced the amount of time the gerbils spent foraging, as well as foraging efficiency since part of the foragers' attention was directed toward detecting competitors (apparent predation risk). Single gerbils harvested significantly more food than the combined efforts of two gerbils foraging together. Competition reduced the success of both individuals within a pair by more than 50%, making this a case of the tragedy of the commons where each individual's investment in competition reduces the success of all individuals within the group, including its own. Despite their great costs, competitive behaviors will be selected for as long as one individual achieves higher fitness than the other. In nature, interspecific interactions, such as predation risk, may act to reduce and regulate the deleterious effects of intraspecific competition.

What do predators really want? The role of gerbil energetic state in determining prey choice by Barn Owls.

In predator-prey foraging games, predators should respond to variations in prey state. The value of energy for the prey changes depending on season. Prey in a low energetic state and/or in a reproductive state should invest more in foraging and tolerate higher predation risk. This should make the prey more catchable, and thereby, more preferable to predators. We ask, can predators respond to prey state? How does season and state affect the foraging game from the predator's perspective? By letting owls choose between gerbils whose states we experimentally manipulated, we could demonstrate predator sensitivity to prey state and predator selectivity that otherwise may be obscured by the foraging game. During spring, owls invested more time and attacks in the patch with well-fed gerbils. During summer, owls attacked both patches equally, yet allocated more time to the patch with hungry gerbils. Energetic state per se does not seem to be the basis of owl choice. The owls strongly responded to these subtle differences. In summer, gerbils managed their behavior primarily for survival, and the owls equalized capture opportunities by attacking both patches equally.

Ectoparasitism and stress hormones: strategy of host exploitation, common host-parasite history and energetics matter.

Parasites are thought to have numerous negative effects on their hosts. These negative effects may be associated with stress in a host. We evaluated the effects of four species of flea ectoparasites (Parapulex chephrenis, Synosternus cleopatrae, Xenopsylla conformis and Xenopsylla ramesis) on non-specific responses of eight species of rodents (Meriones crassus, Gerbillus dasyurus, Gerbillus andersoni, Gerbillus pyramidum, Gerbillus nanus, Acomys cahirinus, Acomys russatus and Mesocricetus auratus) and measured faecal glucocorticoid metabolites concentrations (FGMC) produced by the hosts. We found no effect of body mass of an individual rodent on FGMCs. Parasitism by fleas with a 'stay on the host body' exploitation strategy was associated with higher host FGMCs than parasitism by fleas that spent most of their life 'off-host'. FGMCs among rodents infested by the same flea species were correlated positively with the phylogenetic distance of a given rodent from the principal host of this flea; changes in FGMCs were lower in the host species more closely related to the flea's principal host. Changes in FMGCs of a host while parasitized were correlated with a host's change in body mass, where hosts that lost more body mass had higher FGMCs. Our results suggest that ectoparasitism can be stressful to their hosts. However, the occurrence of parasite-induced stress seems to depend on the identity of both host and parasite species and the evolutionary history of a host-parasite association. To our knowledge, this is the first multispecies study to evaluate the effect of ectoparasites on glucocorticoid hormones in small mammals.

To dare or not to dare? Risk management by owls in a predator-prey foraging game.

In a foraging game, predators must catch elusive prey while avoiding injury. Predators manage their hunting success with behavioral tools such as habitat selection, time allocation, and perhaps daring-the willingness to risk injury to increase hunting success. A predator's level of daring should be state dependent: the hungrier it is, the more it should be willing to risk injury to better capture prey. We ask, in a foraging game, will a hungry predator be more willing to risk injury while hunting? We performed an experiment in an outdoor vivarium in which barn owls (Tyto alba) were allowed to hunt Allenby's gerbils (Gerbillus andersoni allenbyi) from a choice of safe and risky patches. Owls were either well fed or hungry, representing the high and low state, respectively. We quantified the owls' patch use behavior. We predicted that hungry owls would be more daring and allocate more time to the risky patches. Owls preferred to hunt in the safe patches. This indicates that owls manage risk of injury by avoiding the risky patches. Hungry owls doubled their attacks on gerbils, but directed the added effort mostly toward the safe patch and the safer, open areas in the risky patch. Thus, owls dared by performing a risky action-the attack maneuver-more times, but only in the safest places-the open areas. We conclude that daring can be used to manage risk of injury and owls implement it strategically, in ways we did not foresee, to minimize risk of injury while maximizing hunting success.

Predator facilitation or interference: a game of vipers and owls.

In predator-prey foraging games, the prey's reaction to one type of predator may either facilitate or hinder the success of another predator. We ask, do different predator species affect each other's patch selection? If the predators facilitate each other, they should prefer to hunt in the same patch; if they interfere, they should prefer to hunt alone. We performed an experiment in a large outdoor vivarium where we presented barn owls (Tyto alba) with a choice of hunting greater Egyptian gerbils (Gerbillus pyramidum) in patches with or without Saharan horned vipers (Cerastes cerastes). Gerbils foraged on feeding trays set under bushes or in the open. We monitored owl location, activity, and hunting attempts, viper activity and ambush site location, and the foraging behavior of the gerbils in bush and open microhabitats. Owls directed more attacks towards patches with vipers, and vipers were more active in the presence of owls. Owls and vipers facilitated each other's hunting through their combined effect on gerbil behavior, especially on full moon nights when vipers are more active. Owls forced gerbils into the bushes where vipers preferred to ambush, while viper presence chased gerbils into the open where they were exposed to owls. Owls and vipers took advantage of their indirect positive effect on each other. In the foraging game context, they improve each other's patch quality and hunting success.

Free-living gerbils with higher testosterone take fewer risks.

Among the physiological differences between the sexes are circulating androgen levels. Testosterone (T) is an androgen that has been linked to aggression and risk-taking in male vertebrates, so that males with higher T are generally more aggressive and take more risks. In females, T is not often measured, and its relationship with behaviour has been less studied. The costs of elevated T are assumed to be higher for reproductive females, while the benefits higher for males. Here, we tested the association between endogenous T and risk-taking behaviours in both males and females under well-studied experimental settings in free-living Baluchistan gerbils (Gerbillus nanus; Gn). In addition, we experimentally elevated Gn T levels using implants and measured risk-taking behaviour. Surprisingly, we found that there were no differences in the association between T and risk-taking behaviours between males and females, and that in both sexes, Gn with higher T levels took fewer risks. We also found that Gn spent equal time foraging between risky (open habitat) and safe (under a bush) experimental food patches. We expected Gn, which are nocturnal, to take fewer risks during full moon nights, but found that Gn were more active during moon lit nights than during dark (new moon) nights. This study demonstrates that T has many functions, and that its effects are complex and often unpredictable. It also shows that hypotheses regarding the propensity to take risks under specific coverage and light regimes are not universal, and likely include variables such as species, environment, context, and predator-specific behavioural strategies.

Driven to distraction: detecting the hidden costs of flea parasitism through foraging behaviour in gerbils.

Gerbilline rodents such as Allenby's gerbils (Gerbillus andersoni allenbyi), when parasitized by fleas such as Synosternus cleopatrae pyramidis, devote long hours of grooming to remove the ectoparasites. Yet no detrimental energetic or immunological effects of the ectoparasites have been found in adult Allenby's gerbil. Why should gerbils go to such trouble? We tested for the various ways that fleas can negatively affect gerbils by manipulating flea infestation on gerbils and the presence of a fox. We demonstrate that gerbils responded to fleas by leaving resource patches at higher giving-up densities. Furthermore, they stayed in those resource patches less time and left them at higher quitting harvest rates so long as a fox was also present. When flea-ridden, gerbils also abandoned using vigilance to manage risk and relied mainly on time allocation. Thus, having fleas imposed a foraging cost similar in nature to that arising from the risk of predation from foxes and may be even larger in magnitude. More than that, the presence of fleas acted as a magnifier of foraging costs, especially those arising from the risk of predation. The fleas reduced the gerbils' foraging aptitude and altered how they went about managing risk of predation. We hypothesize that fleas reduce the attention that gerbils otherwise have for foraging and predator detection. We suggest that this is the major cost of ectoparasitism.

Social behaviour and foraging success of little egrets (Egretta garzetta).

Intraspecific interactions among predators can change the game between a predator and its prey. Individuals of different size or sex can differ in their responses to conspecific competitors. We studied intraspecific interactions among pairs of little egrets (Egretta garzetta) while foraging on responsive prey (comet goldfish, Carassius auratus). Testing little egrets in an artificial patchy environment both singly and while engaged in social forging in pairs (male & female) at two prey densities, allowed us to explore individual differences in foraging success. We found sexual dimorphism with males being bigger and more aggressive than females. However, female foraging success was positively affected by the time they spent foraging with a conspecific male, suggesting they might be able to mitigate male aggressiveness with an indirect positive interaction. Despite the presence of direct interactions between individuals in the pair, egret foraging success was not affected by such interactions, nor by prey density. Our results demonstrate the importance of sex and an individual's ability to adjust its social behaviour based on the behaviour of others in this predator-prey foraging game.

Complex state-dependent games between owls and gerbils.

Predator-prey interactions are often behaviourally sophisticated games in which the predator and prey are players. Past studies teach us that hungrier prey take higher risks when foraging and that hungrier predators increase their foraging activity and are willing to take higher risks of injury. Yet no study has looked at the simultaneous responses of predator and prey to their own and each other's hunger levels in a controlled environment. We looked for evidence of a state-dependent game between predators and their prey by simultaneously manipulating the hunger state of barn owls, and Allenby's gerbils as prey. The owls significantly increased their activity when hungry. However, they did not appear to respond to changes in the hunger state of the gerbils. The gerbils reacted strongly to the owls' state, as well as to their own state when the risk was perceived as high. Our study shows that predator-prey interactions give rise to a complex state-dependent game.

Moonlight avoidance in gerbils reveals a sophisticated interplay among time allocation, vigilance and state-dependent foraging.

Foraging animals have several tools for managing the risk of predation, and the foraging games between them and their predators. Among these, time allocation is foremost, followed by vigilance and apprehension. Together, their use influences a forager's time allocation and giving-up density (GUD) in depletable resource patches. We examined Allenby's gerbils (Gerbilus andersoni allenbyi) exploiting seed resource patches in a large vivarium under varying moon phases in the presence of a red fox (Vulpes vulpes). We measured time allocated to foraging patches electronically and GUDs from seeds left behind in resource patches. From these, we estimated handling times, attack rates and quitting harvest rates (QHRs). Gerbils displayed greater vigilance (lower attack rates) at brighter moon phases (full < wane < wax < new). Similarly, they displayed higher GUDs at brighter moon phases (wax > full > new > wane). Finally, gerbils displayed higher QHRs at new and waxing moon phases. Differences across moon phases not only reflect changing time allocation and vigilance, but changes in the state of the foragers and their marginal value of energy. Early in the lunar cycle, gerbils rely on vigilance and sacrifice state to avoid risk; later they defend state at the cost of increased time allocation; finally their state can recover as safe opportunities expand. In the predator-prey foraging game, foxes may contribute to these patterns of behaviours by modulating their own activity in response to the opportunities presented in each moon phase.

State of emergency: behavior of gerbils is affected by the hunger state of their predators.

Predator-prey interactions are usually composed of behaviorally sophisticated games in which the values of the strategies of foraging prey individuals may depend on those of their predators, and vice versa. Therefore, any change in the behavior of the predator should result in changes to the behavior of the prey. However, this key prediction has rarely been tested. To examine the effects of the predator state on prey behavior, we manipulated the state of captive Barn Owls, Tyto alba, and released them into an enclosure containing Allenby's gerbils, Gerbillus andersoni allenbyi, a common prey of the owls. The owls were significantly more active when hungry. In response, the gerbils altered their behavior according to the state of the owl. When the owl was hungry, the gerbils visited fewer food patches, foraged in fewer patches, and harvested less food from each patch. Moreover, the gerbils kept their foraging bouts closer to their burrow, which reduced the overlap among foraging ranges of individual gerbils. Thus, changes in the state of the predator affect the foraging behavior of its prey and can also mediate competition among prey individuals.

Foraging behavior of an urban bird species: molt gaps, distance to shelter, and predation risk.

Predation cost (Pc) is often regarded as a pivotal component determining foraging behavior. We hypothesized that variations in two of its major constituents, predation risk (mu) and the marginal value of energy ([see text for symbol]Fs/ [see text for symbol]e, where Fs is the survivor's fitness and e represents the amount of acquired energy), will translate into variations in patch use behavior of ground-foraging birds. We studied patch use behavior of House Sparrows (Passer domesticus), as affected by the proximity to shelter, in two large outdoor aviaries. Proximity to shelter should affect mu. We manipulated the birds' flight performance by clipping primary flight feathers from their wings to increase mu, but the clipping may also increase [see text for symbol]Fs/ [see text for symbol]e. To help distinguish between the birds' response to these confounding effects, we further augmented food in the aviaries to reduce [see text for symbol]Fs/ [see text for symbol]e. Patch use, as measured by giving-up densities (GUD, the amount of food left behind in a resource patch following exploitation) was affected by distance from shelter only slightly and mainly when the birds were feather-clipped and food was not augmented. Food augmentation had a homogenizing effect on foraging costs by increasing GUDs and washing out the effects of distance and feather clipping. We argue that mu increases with distance from shelter but that, for the highly urban House Sparrow, this increase is only slight. Feather clipping then increased mu further to the point at which patch use discernibly decreased with distance from shelter. Our experimental manipulation of feather clipping also acted to increase [see text for symbol]Fs/ [see text for symbol]e and resulted in an overall lowering of GUDs. The seed augmentation counteracted the effect of feather clipping on [see text for symbol]Fs/ [see text for symbol]e, allowing the birds to reduce their foraging efforts and washing out the qualitative effect of mu with respect to distance from shelter.