Fun and Games: predator–prey foraging games and related interactions

On July 2014, Dr Keren Embar passed away from a Puumala virus infection that she contracted while researching predator–prey interactions in Finland. Keren Embar was an original, from her name, to her dress, to her mastering of martial arts, to her love of fantasy and science fiction. She did what made her happy. And she was always happy, always cheerful, always friendly, always willing to help out friends and colleagues. Although Keren had only just finished her PhD degree, she was already making a worldwide impact (e.g., Embar et al. 2011). While others studied foragers at risk of predation, Keren studied the predators themselves. How do they choose prey (Embar et al. 2014a)? Do they interfere with or facilitate other predators (Embar et al. 2014c)? Do they use daring (Embar et al. 2014b)? How do they manage the fear that they strike in the heart of their prey? What are the consequences of the foraging game that they play among themselves and with their prey? Keren embraced the world with a creative eye all full of wonder. She loved the world in which she lived. We will long remember Keren's broad curiosity about the universe and the enthusiastic commitment to ecology and evolutionary biology that burned within her. She had achieved excellence in her field of interest and was overflowing with promise for greater discoveries to come. Keren died doing what she loved best. Her friends miss her, and so will the scientific community. While the “Fun and Games” in the title may sound flippant, “Fun” best describes her approach to life and her approach to science, and “Games” best describes the game-theoretic approach to ecology that she embraced; nothing could be more fitting. This volume is dedicated to her memory.

Species interactions are often foraging games, with the value of a trait to one player depending on the traits of those with which it interacts. These players may be prey, conspecific competitors, interspecific competitors, or predators. The interaction of clever prey and clever predators takes clever methods and can result in deep and often unexpected insights. Here, we take a deeper look at such interactions.

In the Soapbox Essay that opens this volume, Robert D. Holt (2016, this volume) reflects on our wounded world, in close from our personal, human perspective all the way out to the Earth's biota. How do we deal with the wounds of personal loss? How can we pass a more functional world on to future generations? How are these questions related? How we answer these questions personally and collectively will determine much for our legacies and what the future holds.

Katz and colleagues (2016, this volume) examine the foraging game between little egrets and their goldfish prey. In this game, egrets must allocate time among pools of fish, and fish must allocate time between safe refuges and risky open areas where food is available. To manage risk of predation, the fish need up-to-date information on whether the predator is present at their pool. To get this information, the fish emerge slightly from cover to take a “peep.” The authors varied the number of pools available to the egret as a way of manipulating egret behavior and examined lethal and non-lethal effects on the fish in response to the resulting changing levels of predation risk, including direct mortality and their emergence from cover and their rate of peeping. The use of costly information by the fish helps drive this game.

Just as predators may manage their risk of injury from dangerous prey, herbivores may need to manage both mechanical and chemical plant defenses. Kiekebusch and Kotler (2016, this volume) examine the effect of both types of plant defenses on patch use and seasonal foraging preferences of Nubian ibex. They further examine how the availability of water may affect the efficacy of chemical plant defenses. Overall in this study, mechanical and chemical defense are substitutable and are additive in their effects, but they are also affected by seasonality. Food abundance and the availability of alternative sources of food and water may explain this and explain why some plants rely on both types of defenses.

Different types of species interactions can be complex and often confused with each other. One species may be a competitor with another at one stage in life and an intra-guild predator at another life stage. Tsurim and Silberbush (2016, this volume) examined the interaction of two species of mosquito larvae found in temporary pools in arid regions. What at first appears to be intra-guild predation turns out to be scavenging. This result is consistent with the absence of any anti-predatory behavior on the part of presumed prey species.

All species face tradeoffs and perhaps the most fundamental tradeoff of all is the tradeoff of food and safety. Often, the input of safety is governed by the risk of predation, but other risks can be involved. Top predators, for example, may face different risks of injury associated with different prey species or different capture techniques. Prey inhabiting temporary pools at early stages of their live histories may face threats to their safety based on the likelihood of their pool drying out before they can metamorphose and leave the pool. Female adult mosquitoes carefully choose the pool into which they lay their eggs and take into consideration various factors including food availability, competitor density, and the presence of predators. Such oviposition habitat selection may also be sensitive to desiccation risk, and such risk may be indicated by pool size. Saward-Arav et al. (2016, this volume) examine two species of mosquitoes. They show that while both species are sensitive to the presence of predators, the one whose larvae are more vulnerable to predation is also sensitive to desiccation risk. This suggests that tradeoffs between different mortality risks may be key to their coexistence.

Studying predators, the effects of predators in the foraging behavior of their prey, and predator–prey foraging games experimentally can be challenging. To this end, trained predators can provide a powerful tool for such studies in artificial and natural settings. Subach (2016, this volume) presents the methods by which barn owls can be raised and trained for ecological and behavioral experiments. He also clearly defines the critical stages of growth, the training to take place at each stage, and the characteristic body masses of the growing owls necessary for success.

Just as organisms trade off food and safety, they often trade off mating opportunities and safety. Ylönen and Haapakoski (2016, this volume) examine kinship, mate choice, and inbreeding in bank voles. Females responded most strongly to dominance, but fell back on relatedness when dominance provided little resolution in mate quality. The authors suggest that the mismatch between female mate choice based on dominance and negative effects of inbreeding may reflect sex-biased dispersal.

In the tradeoff of food and safety, risk can come in many forms. The risk allocation hypothesis predicts (Lima and Bednekoff 1999) how organisms should alter risk management as risk and resources vary in time, especially in temporally autocorrelated environments (Higginson et al. 2012). Bannister and Morris (2016, this volume) propose that this same theory can apply to habitat selection for safe and resource poor versus risky and resource rich patches. To test this, they examined risk allocation in response to risk of desiccation for a small soil arthropod whose energetic state had been manipulated by exposure to favorable or unfavorable conditions of different proportions and durations. Risk allocation depended on a threshold value of energetic state, suggesting that state-dependent habitat selection can be used to track changing habitat quality.

Species diversity in ecological communities is supported by mechanisms of species coexistence. Studying mechanisms allows us to identify salient features of the environment and salient features of the organisms that permit diversification (Brown 1989). They further help to identify whether predation is involved. Shuai et al. (2016, this volume) examined coexistence of a pair of desert rodents from the Gobi Desert in Central Asia. This pair included a bipedal jerboa and a quadrupedal jird (gerbil). Results suggest that coexistence is promoted by the anti-predator abilities of the jerboa and the interference abilities of the jird. In this sense, this Gobi Desert community is more similar to tree squirrels in North America than it is to other desert rodent communities.

Foragers must trade off food and safety to make foraging decisions while facing a diversity of predators. The ability to deal with these predators should depend on the capabilities of those predators and the ability of the forager to assess and respond. Bleicher et al. (2016, this volume) studied the foraging Allenby's gerbil in a large outdoor vivarium in which they had to exploit resource patches while facing risk of predation with four species of predators: an owl, a fox, and two species of vipers. Of these, the gerbil has a shared history with the owl (barn owl) and the fox (red fox) and one of the vipers (Saharan horned viper), but not the other viper (sidewinder rattlesnake). Furthermore, the novel viper also possesses the compromise-breaking adaptation of heat-sensitive sensory pits that allow them to “see” in the dark. Although the gerbils “cared” more about the foxes and owls than the snakes, they were still able to recognize the novel snake as presenting a threat similar to that posed by their familiar snake. The gerbils were able to overcome their varying evolutionary histories to appropriately respond to the snakes.

We are all familiar with prey that face mortality risks from predators and how this threat leads to a tradeoff of food and safety. This tradeoff then affects their foraging decisions and risk management, particularly their use of time allocation and vigilance. In turn, risk management has profound, far-reaching effects in the prey's interactions with resources, competitors, predators, and, ultimately, their communities and ecosystems.

Predators, too, face a tradeoff of food and safety, but here the threat comes from risk of injury from dangerous prey. Just as prey manage risk using vigilance, predators may manage risk of injury using derring-do, their willingness to risk using tactics that increase prey capture success. Brown et al. (2016, this volume) explore derring-do theoretically in the context of a predator–prey foraging game in which predators can choose their optimal derring-do and prey can choose their optimal vigilance. They show that although prey respond to predator density and predator lethality by increasing vigilance and predators respond to prey abundance and their own derring-do, at the ESS (i.e., an Evolutionary Stable Strategy, a strategy that when held by most members of a population cannot be invaded by individuals carrying a rare alternative), prey vigilance causes predators to decrease derring-do and thereby make prey individuals safer. Furthermore, feedbacks of vigilance, derring-do, and population dynamics increase intraspecific density dependencies and stabilize the species interaction. Tradeoffs of food and safety are everywhere and affect even predators. Thus they can be expected to have profound, far-reaching effects on the predators’ interactions with prey, competitors, and, ultimately, their communities and ecosystems, too.

Ecologists have long been interested in comparisons between ecological communities from climatically and structurally similar environments across the globe. The hopes of such comparisons include possibly deducing general ecological principles based on intercontinental community convergences. Kotler et al. (2016, this volume) build on the work of Bleicher et al. (2016) by adding three more desert rodents for a comparison of gerbils from the Negev Desert of the Middle East with kangaroos and pocket mice from the Mojave Desert of North America. The comparison has implications for the role of macroevolution in determining microecological interactions. In particular, the rodents of North America possess cheek pouches that the gerbils lack and the sidewinder rattlesnakes that prey on the kangaroo rats and pocket mice possess heat-sensitive sensory pits that the Saharan horned vipers lack. The authors suggest that the limited convergence of these two communities can best be understood in the context of the advanced evolutionary technologies found only in the North American lineages.

The papers that comprise this volume deal with a wide range of issues in predator–prey interactions, explore new dimensions, push the theoretical envelope, and propose bold syntheses, but they cannot replace Keren's creative energy and her unique vision never more to be. We all hope that they form a fitting tribute.

Disclosure statement

No potential conflict of interest was reported by the author.