Shomen Mukherjee

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 foragers time allocation and giving-up density (GUD) in depletable resource patches. We examined Allenbys 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.

Patch use in time and space for a meso-predator in a risky world

Predator–prey studies often assume a three trophic level system where predators forage free from any risk of predation. Since meso-predators themselves are also prospective prey, they too need to trade-off between food and safety. We applied foraging theory to study patch use and habitat selection by a meso-predator, the red fox. We present evidence that foxes use a quitting harvest rate rule when deciding whether or not to abandon a foraging patch, and experience diminishing returns when foraging from a depletable food patch. Furthermore, our data suggest that patch use decisions of red foxes are influenced not just by the availability of food, but also by their perceived risk of predation. Fox behavior was affected by moonlight, with foxes depleting food resources more thoroughly (lower giving-up density) on darker nights compared to moonlit nights. Foxes reduced risk from hyenas by being more active where and when hyena activity was low. While hyenas were least active during moon, and most active during full moon nights, the reverse was true for foxes. Foxes showed twice as much activity during new moon compared to full moon nights, suggesting different costs of predation. Interestingly, resources in patches with cues of another predator (scat of wolf) were depleted to significantly lower levels compared to patches without. Our results emphasize the need for considering risk of predation for intermediate predators, and also shows how patch use theory and experimental food patches can be used for a predator. Taken together, these results may help us better understand trophic interactions.

CAN WE MEASURE CARRYING CAPACITY WITH FORAGING BEHAVIOR

Carrying capacity is one of the most important, yet least understood and rarely estimated, parameters in population management and modeling. A simple behavioral metric of carrying capacity would advance theory, conservation, and management of biological populations. Such a metric should be possible because behavior is finely attuned to variation in environment including population density. We connect optimal foraging theory with population dynamics and life history to develop a simple model that predicts this sort of adaptive density-dependent change in food consumption. We then confirm the models unexpected and manifold predictions with field experiments. The theory predicts reproductive thresholds that alter the marginal value of energy as well as the value of time. Both effects cause a pronounced discontinuity in quitting-harvest rate that we revealed with foraging experiments. Red-backed voles maintained across a range of high densities foraged at a lower density-dependent rate than the same animals exposed to low-density treatments. The change in harvest rate is diagnostic of populations that exceed their carrying capacity. Ecologists, conservation biologists, and wildlife managers may thus be able to use simple and efficient foraging experiments to estimate carrying capacity and habitat quality.

Look before you leap: is risk of injury a foraging cost?

Theory states that an optimal forager should exploit a patch so long as its harvest rate of resources from the patch exceeds its energetic, predation, and missed opportunity costs for foraging. However, for many foragers, predation is not the only source of danger they face while foraging. Foragers also face the risk of injuring themselves. To test whether risk of injury gives rise to a foraging cost, we offered red foxes pairs of depletable resource patches in which they experienced diminishing returns. The resource patches were identical in all respects, save for the risk of injury. In response, the foxes exploited the safe patches more intensively. They foraged for a longer time and also removed more food (i.e., had lower giving up densities) in the safe patches compared to the risky patches. Although they never sustained injury, video footage revealed that the foxes used greater care while foraging from the risky patches and removed food at a slower rate. Furthermore, an increase in their hunger state led foxes to allocate more time to foraging from the risky patches, thereby exposing themselves to higher risks. Our results suggest that foxes treat risk of injury as a foraging cost and use time allocation and daring—the willingness to risk injury—as tools for managing their risk of injury while foraging. This is the first study, to our knowledge, which explicitly tests and shows that risk of injury is indeed a foraging cost. While nearly all foragers may face an injury cost of foraging, we suggest that this cost will be largest and most important for predators.

FORAGING GAMES BETWEEN GERBILS AND THEIR PREDATORS: SEASONAL CHANGES IN SCHEDULES OF ACTIVITY AND APPREHENSION

The interactions between predators and prey often constitute foraging games where prey manage risk and predators manage fear. Tools available to prey to manage risk include time allocation and apprehension. Such a game exists between gerbils and their predators in sandy habitats in the Negev Desert. Pulses of seeds made available daily by wind action result in a tightly choreographed game of changing seed availability and changing gerbil and predator behavior throughout the night. This outcome depends on summer conditions, especially the mobile sandy substrate that allows for daily renewal of resources. But winter conditions are far different: colder temperatures and wet, immobile substrate that stymies seed renewal. Here, we examined nightly patterns of time allocation and apprehension in gerbils in summer and winter. Gerbils showed higher GUDs (giving-up density, a measure of time allocation) and higher selectivity for full resource patches over micropatches (a measure of apprehension) in winter than in summer. Also, gerbils showed stronger responses of GUDs to moon phase and time of night in the summer and stronger responses of selectivity to moon phase and microhabitat in the winter. In summer, gerbils use apprehension and, especially, time allocation to manage risk; in winter, gerbils rely more on apprehension. These results show how a forager’s use of time allocation and apprehension depends on the nature of resource renewal and the cost of thermoregulation while foraging. Such factors can vary greatly across seasons and result in very different tactics for animals managing food and safety through foraging behavior.

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.

Domestic ungulates in protected areas and the potential for indirect interactions via shared predation

Abstract In many parts of the world, protected areas harbour permanent livestock that range freely with native herbivores. These domestic animals are typically an undesirable ecosystem component because they pose a challenge to park managers and biologists who wish to maintain ‘natural’ species interactions and diversity. Studies dealing with livestock in protected areas have primarily focussed on interactions such as competition for food resources with native herbivores, habitat degradation, and human-carnivore conflicts caused by livestock depredation. The negative effects of such interactions are a major threat to the survival of many mammalian prey and predator species. However, the role of indirect interactions between native herbivores and domestic prey, via their common enemy, has received comparatively little attention and poses a significant knowledge gap in understanding the net impacts of domestic prey on native herbivores. We present our perspectives on ignored or missed indirect interactions in livestock–native ungulate systems, and suggest some management actions for understanding these systems and minimising conflicts. A broader understanding of indirect interactions among livestock, native herbivores and their predators will aid in more informed protected-area management.