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.

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.

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.

Ninja owl; Gerbils over-anticipate an unexpected flying predator.

Foragers make decisions based on cues, information collected from their environment, processed into strategic behaviours. This information, processed in multiple regions of the brain, ultimately result in the production of stress hormones and visible changes in behaviour of animals - both reflexively to avoid depredation and strategically to avoid an encounter with the predator. In a common-garden experiment we tested how imperfect information from visual cues of a predator impacts foraging and apprehension of a desert rodent, the Egyptian gerbil (Gerbillus pyramidum). The gerbils were exposed to predation by barn owls (Tyto alba), one camouflaged on dark nights using black dye. Gerbils' response to the owls was measured using patch-use measured in giving-up densities (GUDs) and time spent in vigilance activity. Owl lethality was extrapolated from mean times spent in attacks and number of attempted strikes. Dyed owls attack-rate was lower and attack duration greater than those of the white owls. During the full moon, when dyed owls were visible, gerbils responded with extreme vigilance and minimal foraging (high GUDs). During the new moon when the owls were most stealthy, the gerbils showed low vigilance coupled with a similar high GUD. The inconsistency between gerbils' foraging and vigilance behaviours, suggest a likely mismatch between perceived risk and actual measurement of predator lethality gathered by the gerbils' observations in real time.

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.

Ecology of Leishmaniasis in an urbanized landscape: Relationship of sand fly densities, and Leishmania tropica infection rates with reservoir host colonies.

Urbanization may influence the transmission of leishmaniasis, which is as a serious public health issue in Palestine. Semi urban environments can provide suitable habitats for the reservoir host species and the vector sand flies to create favorable condition for disease transmission. This study was aimed to evaluating the effect of distance from hyrax (reservoir host) colonies on sand fly (vector) abundance and its relationship to Leishmania infection within a semi urban landscape. In the Aleskan neighborhood the town of Tubas, sand flies were collected in July and September of 2016. Five trapping transects were set running from a rocky area containing hyrax dwelling habitats into an area of inhabited houses. 1051 Phlebotomus sand flies from 9 species were captured. The numbers of Phlebotomus sergenti, the vector species, correlated negatively with the distance from hyrax. Infected, blood engorged female sand flies were captured closer to hyrax colonies than infected, non-fed females. The risk of disease transmission to humans increased with a high density of reservoirs, closer proximity of reservoir hosts, and high densities of sand flies near houses. These results must be taken into account when implementing future interventions to reduce CL in urban environments.

The spatial and temporal distribution, species composition, and host preference of phlebotomine sand flies in the Bethlehem District of Palestine.

In the Palestinian West Bank, leishmaniasis is emerging as a serious public health issue with incidence increasing over time, especially in the western and the northern parts. This study was aimed to evaluating the effect of altitude on sand fly density, temporal and spatial distribution, species composition, and host preference within and between three villages in the Bethlehem District. The three villages occur along an elevation cline, ranging from the disease-free area of Kisan (KIS; 732-782 m ASL), down to the endemic areas of Arab Ar-Rashaiyda (AAR; 522-568 m ASL), and Al'Azazma (AZA; 473-510 m ASL) in the Bethlehem District (southeastern West Bank). Sand flies were trapped monthly from May through October in 2013 in traps located north, south, east, and west of each village. The abundance of sand flies differed among the three villages, with Arab Ar-Rashaiyda (AAR) > Al 'Azazma (AZA) >Kisan (KIS). The sex ratio was even in AAR and AZA, and female biased in KIS. Both male and female Phlebotomus sand fly densities varied with elevation, with greatest densities found at intermediate elevations (AAR). Elevation correlated negatively with the proportion of blood-fed Phlebotomus females. Male Phlebotomus species composition differed among sites, with all the species found in this study present in AZA, while some species were absent from AAR and KIS. The host blood species engorged by P. sergenti were grouped in four categories: human (45.5%), livestock (25%), avian (19.9%), and dog (9.6%). This study provided information about the spatial and temporal distribution, age and species composition, and host preference of sand fly vectors that influence disease transmission. This information will allow us to better target sand flies, to control the disease, and to monitor risk prone areas.

Does intraspecific competition among Allenby's gerbils lead to an Ideal Free Distribution across foraging patches?

Employing the Ideal Free Distribution (IFD) principle as a tool, we investigated how Allenby's gerbils (Gerbillus andersoni allenbyi) utilized food patches within and moved between connected quadrants (i.e., 'habitats') in a large outdoor semi-natural enclosure. These habitats differed in initial forager densities, but provided equal numbers of standardized food patches that provided equal rewards (i.e. food) and costs (i.e. predation risk, metabolic, and missed opportunity). We quantified the gerbils' giving-up-densities (GUDs) within foraging patches and recorded their daily distribution between habitats. Individual gerbils were tagged with unique bar-coded numbers to compare their locations within and across habitats. The mean number of gerbil foragers (9.1 and 8.9 individuals, respectively) and GUDs evened out across habitats over time. Despite this, the distribution of gerbils did not remain static within foraging patches; instead, gerbils altered their use of patches across and within habitats on a nightly basis. This may be due to a combination of factors including, high levels of interference competition between foragers at patches, a lag effect before the gerbils perceived changes in competition intensity with the arrival and departure of individuals, and gerbils having imperfect knowledge of their environment. Furthermore, the pattern of microhabitat (open vs bush patches) use by gerbils differed over time, indicating that despite the distribution of gerbils and their GUDs evening out between habitats, they still preferred foraging from safer bush patches over riskier open patches. This study provides insights into how under low predation risk, strong levels of intraspecific competition can shape the distribution of foragers across and within habitats.

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.

Comparing Plasticity of Response to Perceived Risk in the Textbook Example of Convergent Evolution of Desert Rodents and Their Predators; a Manipulative Study Employing the Landscape of Fear.

Foragers process information they gain from their surroundings to assess the risk from predators and balance it with the resources in their environment. Measuring these perceived risks from the perspective of the forager can produce a heatmap or their "fear" in the environments, a so-called "landscape of fear" (LOF). In an intercontinental comparison of rodents from the Mojave and Negev Deserts, we set to compare families that are used regularly as examples of convergent evolution, heteromyid and gerbilline respectively. Using a LOF spatial-analysis on data collected from common garden experiments in a semi-natural arena we asked: (1) do all four species understand the risk similarly in the exact same physical environment; (2) does relative relation between species affect the way species draw their LOFs, or does the evolutionary niche of a species have a greater impact on its LOF?; and (3) does predator facilitation between vipers and barn owls cause similar changes to the shape of the measured LOFs. For stronger comparative power we mapped the LOF of the rodents under two levels of risk: low risk (snakes only) and high risk (snakes and barn owls). We found concordance in the way all four species assessed risk in the arena. However, the patterns observed in the LOFs of each rodent family were different, and the way the topographic shape of the LOF changed when owls were introduced varied by species. Specifically, gerbils were more sensitive to owl-related risk than snakes and at the opposite correct for heteromyids. Our findings suggest that the community and environment in which a species evolved has a strong impact on the strategies said animals employ. We also conclude, that given the homogenous landscape we provide in our arena and the non- homogenous patterns of LOF maps, risk assessment can be independent of the physical conditions under which the animals find themselves.

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.

Defense by exploitation in Negev gerbils.

In this study, we addressed how frequently a non-traplining animal should visit food patches. More specifically, we investigate if non-traplining animals engage in a behavior called "defense by exploitation", which is characterized by an increase in visitation rates with increased intra-specific competition. We ran four tests with two gerbil species in the Negev Desert. Firstly, we measured patch use of Gerbillus pyramidum and Gerbillus andersoni allenbyi. We assumed that activity and competition would decrease through the night and that patch use would decrease with number of visits. Secondly, we measured how the number of visits to resource patches increased with the addition of individuals. Thirdly, we repeated this experiment, but instead removed individuals. Lastly, we conducted a simulation to compare these results against theoretical expectations. In the first test, we found support for defense by exploitation in G. pyramidum. The second and third test found no support. The fourth test found support for this increase visitation, but only if costs of locomotion are relatively small.

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.

Binary patch assessment by goldfish under safe and dangerous conditions.

Food resources can occur heterogeneously in space or time and differ in their abundances. A forager should be able to determine the value of a patch and choose optimally how to exploit it. However, patch choice and exploitation may be influenced by predation risk. Using the Giving up Densities (GUDs) technique, we evaluated goldfish patch assessment and choice in a binary patch choice experiment. We offered a pair of unequal food patches containing high and low food quantity. We quantified goldfish foraging behavior in the presence and absence of a predator. Goldfish groups equalized the GUDs in the two patches in safe environments but left higher GUDs in the rich patch under predation risk. The results suggest that goldfish can use both "patch assessment rule" and "fixed time rule" to exploit resource patches and trade off food and danger.

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.

A predator equalizes rate of capture of a schooling prey in a patchy environment.

Prey individuals are often distributed heterogeneously in the environment, and their abundances and relative availabilities vary among patches. A foraging predator should maximize energetic gains by selectively choosing patches with higher prey density. However, catching behaviorally responsive and group-forming prey in patchy environments can be a challenge for predators. First, they have to identify the profitable patches, and second, they must manage the prey's sophisticated anti-predator behavior. Thus, the forager and its prey have to continuously adjust their behavior to that of their opponent. Given these conditions, the foraging predator's behavior should be dynamic with time in terms of foraging effort and prey capture rates across different patches. Theoretically, the allocation of its time among patches of behaviorally responsive prey should be such that it equalizes its prey capture rates across patches through time. We tested this prediction in a model system containing a predator (little egret) and group-forming prey (common gold fish) in two sets of experiments in which (1) patches (pools) contained equal numbers of prey, or in which (2) patches contained unequal densities of prey. The egret equalized the prey capture rate through time in both equal and different density experiments.

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.