Keren Embar

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.

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.

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 predators 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.

Intercontinental-wide consequences of compromise-breaking adaptations: the case of desert rodents

Desert rodent assemblages from around the world provide convergent, but independent crucibles for testing theory and deducing general ecological principles. The heteromyid rodents of North America and the gerbils of the Middle East and their predators provide such an example. Both sets of rodents face predation from owls and vipers, but the North American species possess unique traits that may represent macroevolutionary breakthroughs: rattlesnakes have infra-red sensitive sensory pits, and heteromyids have cheek pouches. To test their significance, we brought together two gerbils (Middle East), two heteromyid rodents (a kangaroo rat and a pocket mouse; North America) in a common setting (a vivarium in the Negev Desert), and quantified the “opinions” of the rodents towards the North American sidewinder rattlesnake and the Middle Eastern Saharan horned viper and the foraging behavior of each in the face of these snake predators plus owl predators. Gerbils are fairly evenly matched in their anti-predator ab...

Past experiences and future expectations generate context-dependent costs of foraging

Because environments can vary over space and time in non-predictable ways, foragers must rely on estimates of resource availability and distribution to make decisions. Optimal foraging theory assumes that foraging behavior has evolved to maximize fitness and provides a conceptual framework in which environmental quality is often assumed to be fixed. Another more mechanistic conceptual framework comes from the successive contrast effects (SCE) approach in which the conditions that an individual has experienced in the recent past alter its response to current conditions. By regarding foragers’ estimation of resource patches as subjective future value assessments, SCE may be integrated into an optimal foraging framework to generate novel predictions. We released Allenby’s gerbils (Gerbillus andersoni allenbyi) into an enclosure containing rich patches with equal amounts of food and manipulated the quality of the environment over time by reducing the amount of food in most (but not all) food patches and then increasing it again. We found that, as predicted by optimal foraging models, gerbils increased their foraging activity in the rich patch when the environment became poor. However, when the environment became rich again, the gerbils significantly altered their behavior compared to the first identical rich period. Specifically, in the second rich period, the gerbils spent more time foraging and harvested more food from the patches. Thus, seemingly identical environments can be treated as strikingly different by foragers as a function of their past experiences and future expectations.

Novel predator recognition by Allenby's gerbil (Gerbillus andersoni allenbyi ): do gerbils learn to respond to a snake that can “see” in the dark?

Unlike desert rodents from North America, Allenbys gerbil (Gerbillus andersoni allenbyi) from the Negev Desert, Israel has evolved with snakes that do not have heat-sensitive sensory pits that enhance night vision. Does this history affect their ability to assess and respond to a snake that has this ability? As a test, we exposed gerbils to risk of predation from various predators, including snakes, owls, and foxes. The snakes included the Saharan horned viper (Cerastes cerastes) and the sidewinder rattlesnake (Crotalus cerastes). The former snake lacks sensory pits and shares a common evolutionary history with the gerbil. The latter snake, while convergent evolutionarily on the horned viper, has sensory pits and no prior history with the gerbil. The gerbils exploited depletable resource patches similarly, regardless of snake species and moon phase. While the gerbils did not respond to the novel snake as a greater threat than their familiar horned viper, the gerbils were cognizant that the novel predator...

Predators risk injury too: the evolution of derring-do in a predator–prey foraging game

Derring-do is how aggressive a predator is in stalking and capturing prey. We model predator–prey interactions in which prey adjust vigilance behavior to mitigate risk of predation and predators their derring-do to manage risk of injury from capturing prey. High derring-do increases a predators likelihood of capturing prey, but at higher risk of injury to itself. For fixed predator derring-do, prey increase vigilance in response to predator abundance, predator lethality, and predator encounter probability with prey and decrease vigilance with their own feeding rate; there is a humped-shaped relationship between prey vigilance and effectiveness of vigilance. For fixed prey vigilance, predators increase derring-do with the abundance of prey and predator lethality and decrease it with benefit of vigilance to prey and level of prey vigilance. When both prey and predator are behaviorally flexible, a predator–prey foraging game ensues whose solution represents an evolutionarily stable strategy (ESS). At the ES...

Foraging behaviour in East Asian desert rodents and its implications on coexistence

We studied the foraging behaviour of two sympatric rodents (Meriones meridianus and Dipus sagitta) in the Gobi Desert, Northwestern China. The role of the foraging behaviour in promoting species coexistence was also examined. We used giving-up densities (GUDs) in artificial food patches to measure the patch use of rodents and video trapping to directly record the foraging behaviour, vigilance, and interspecific interactions. Three potential mechanisms of coexistence were evaluated (1) microhabitat partitioning; (2) spatial heterogeneity of resource abundance with a tradeoff in foraging efficiency vs. locomotion; and (3) temporal partitioning on a daily scale. Compared to M. meridianus, D. sagitta generally possessed lower GUDs, spent more time on patches, and conducted more visits per tray per capita, regardless of microhabitat. However, M. meridianus possessed advantages in average harvesting rates and direct interference against D. sagitta. Our results only partly support the third mechanism listed abov...

Divergent behavior amid convergent evolution: A case of four desert rodents learning to respond to known and novel vipers

Desert communities world-wide are used as natural laboratories for the study of convergent evolution, yet inferences drawn from such studies are necessarily indirect. Here, we brought desert organisms together (rodents and vipers) from two deserts (Mojave and Negev). Both predators and prey in the Mojave have adaptations that give them competitive advantage compared to their middle-eastern counterparts. Heteromyid rodents of the Mojave, kangaroo rats and pocket mice, have fur-lined cheek pouches that allow them to carry larger loads of seeds under predation risk compared to gerbilline rodents of the Negev Deserts. Sidewinder rattlesnakes have heat-sensing pits, allowing them to hunt better on moonless nights when their Negev sidewinding counterpart, the Saharan horned vipers, are visually impaired. In behavioral-assays, we used giving-up density (GUD) to gauge how each species of rodent perceived risk posed by known and novel snakes. We repeated this for the same set of rodents at first encounter and again two months later following intensive “natural” exposure to both snake species. Pre-exposure, all rodents identified their evolutionarily familiar snake as a greater risk than the novel one. However, post-exposure all identified the heat-sensing sidewinder rattlesnake as a greater risk. The heteromyids were more likely to avoid encounters with, and discern the behavioral difference among, snakes than their gerbilline counterparts.

Pit fights: predators in evolutionarily independent communities

Sidewinders (Crotalus cerastes) and Saharan horned vipers (Cerastes cerastes) have evolved to hunt desert rodents on different continents in evolutionarily independent communities. These species are remarkably convergent, except that sidewinders possess heat-sensitive pit organs that enable them to “see” in the dark. As a constraintbreaking adaptation, this may give sidewinders an advantage when hunting in the dark. How will introducing a novel predator with a constraint-breaking adaptation affect the local species? We allowed Saharan horned vipers to hunt Allenbys gerbils (Gerbillus andersoni allenbyi) in patches with or without sidewinders at full and new moon. When horned vipers hunted alone, moonlight did not affect their foraging behavior. However, in the presence of sidewinders, horned vipers increased their activity on bright nights, but dramatically decreased it on dark nights. Although gerbils foraged equally when hunted by either snake, the combined effect of the 2 predators synergistically decreased gerbil foraging, especially during full moon when both snakes were most active. Thus, sidewinders facilitated horned vipers in full moon, but interfered on darker nights when possessing pit organs were most advantageous for sidewinders. Gerbils quickly learned and adjusted their behavior to manage risks from the novel predators, but the combined effects of both local and novel predators may prove detrimental in the long run. Comparing convergent species that differ in a constraint-breaking adaptation allows us to study the effectiveness of these key adaptations and their potential roles in biological invasions.