Giving-up Densities Research Articles

Similarities in perceived predation risk prevent temporal partitioning of food by rodents in an African grassland

Abstract One way in which animals coexist is through temporal separation of feeding activities. This separation directly reduces interference competition, but potentially not exploitive competition. To reduce exploitive competition, coexisting species tend to utilize different microhabitats and/or achieve different feeding efforts across microhabitats. However, 1 factor that has generally not been considered with regards to its impacts on competition, and thus coexistence, is predation risk. As different predators are active during the day and at night, the location of safe areas across the landscape can vary temporally. If so, then temporally separated prey species would likely forage in different areas thus reducing exploitive competition. However, if predation risk across the landscape is similar for nocturnal and diurnal species, then both could restrict their foraging to the same microhabitats, thus increasing exploitive competition. To explore these alternative possibilities, we manipulated grass height in an African grassland to create microhabitats that varied in predation risk. We then estimated perceived predation risk of both nocturnal and diurnal rodents in these microhabitats by recording giving-up densities (GUDs) in artificial resource patches. We found that despite differences in predators, both nocturnal and diurnal rodents preferred feeding in the same microhabitats, and they achieved similar feeding efforts within these microhabitats. This suggests that despite the prevention of interference competition through temporal partitioning, the spatial similarities in perceived predation risk in relation to cover likely increase exploitive competition between these rodents. However, as both nocturnal and diurnal rodents were present in the study area, it is likely that some other mechanism (e.g., varied diets) allows them to coexist.

Naiveté is not forever: responses of a vulnerable native rodent to its long term alien predators

Alien predators have wreaked havoc on isolated endemic and island fauna worldwide, a phenomenon generally attributed to prey naiveté, or a failure to display effective antipredator behaviour due to a lack of experience. While the failure to recognise and/or respond to a novel predator has devastating impacts in the short term after predators are introduced, few studies have asked whether medium to long term experience with alien predators enables native species to overcome their naiveté. In Australia, introduced dogs Canis lupus familiaris, foxes Vulpes vulpes and cats Felis catus have caused rapid extinctions and declines in small–medium sized native mammals since they were introduced ∼150 years ago. However, native wildlife have had ∼4000 years experience with another dog – the dingo Canis lupus dingo. Native bush rats Rattus fuscipes remain common despite predation from these predators. We predicted that prior experience with dingoes would mean that bush rats recognise and respond to dogs, but suspect that hundreds of years experience may not be enough for effective responses to cats and foxes. To test these predictions, we combined the giving‐up density (GUD) with analysis of remote camera footage to measure bush rat foraging and behavioural responses to body odour from dogs, foxes, cats and native spotted‐tail quolls Dasyurus maculatus. Bush rats responded strongly to dogs with increased GUDs, increased vigilance and decreased foraging. However, mixed responses to foxes and cats suggest that at least some individuals remain naïve towards these predators. Naiveté is not necessarily forever: alien predators devastate many native prey species, but others may learn or adapt to the new threat.

Foraging decisions in wild versus domestic Mus musculus: What does life in the lab select for?

What does domestication select for in terms of foraging and anti-predator behaviors? We applied principles of patch use and foraging theory to test foraging strategies and fear responses of three strains of Mus musculus: wild-caught, control laboratory, and genetically modified strains. Foraging choices were quantified using giving-up densities (GUDs) under three foraging scenarios: (1) patches varying in microhabitat (covered versus open), and initial resource density (low versus high); (2) daily variation in auditory cues (aerial predators and control calls); (3) patches with varying seed aggregations. Overall, both domestic strains harvested significantly more food than wild mice. Each strain revealed a significant preference for foraging under cover compared to the open, and predator calls had no detectable effects on foraging. Both domestic strains biased their harvest toward high quality patches; wild mice did not. In terms of exploiting favorable and avoiding unfavorable distributions of seeds within patches, the lab strain performed best, the wild strain worst, and the mutant strain in between. Our study provides support for hypothesis that domestic animals have more energy-efficient foraging strategies than their wild counterparts, but retain residual fear responses. Furthermore, patch-use studies can reveal the aptitudes and priorities of both domestic and wild animals.

Fight for Life

Optimal foraging theory explains that organisms whose foraging is as energetically efficient as possible should be favored by natural selection. However, many individuals must exhibit trade-offs between foraging and other factors in their environment (i.e., predation risk, competitive interactions). We present a hands-on activity for undergraduates using just a deck of cards, bingo chips, and dice to introduce ecological concepts of foraging theory, predator–prey interactions, and energy trade-offs. Specifically, this activity will focus on optimal foraging theory and giving-up density. Students should gain an understanding of how organisms balance predation risk and competitive interactions with energetic demands. Further, this activity can be scaled for nonmajors and introductory courses to introduce general ecological concepts, or for upper-division courses to explore advanced topics in foraging theory.

Do individual differences in behavior influence wild rodents more than predation risk?

Prey can enhance their survival by eliciting an appropriate response to predators. Theoretically, prey should distinguish odors of predators and nonpredators. The manifestation of defensive antipredator behaviors has been extensively researched in domestic species (i.e., the relationship between laboratory-bred rats and domestic cats). However, little is known about the expression of these behaviors in wild rodents. Studies have so far focused on quantitative assessments of cost–benefit trade-offs or giving-up densities. We examined the expression of fine-scale defensive behaviors in Arnhem rock rats (Zyzomys maini) in response to fecal cues from 2 predators (the northern quoll [Dasyurus hallucatus] and the dingo [Canis dingo]), a nonpredator (the short-eared rock-wallaby [Petrogale brachyotis]), and a control (water). We adapted a predator-odor avoidance apparatus that has been widely used for domestic rodent studies to film the behavior of wild rock rats in a captive environment. Rock rats did not alter their behavior in the presence of odors of nonpredators, predators, or controls. In the current study, individual rock rats behaved in a consistent manner across time, and we identified 3 individually consistent behaviors which may suggest the existence of personality traits in this species. We suggest that these individual differences may influence wild rock rat behavior more than predation risk. These differences should therefore be taken into consideration when investigating behavioral responses to predators in wild populations.

Foraging behaviour of a desert rodent community: habitat or moon – which is more influential?

In this field study, we questioned how diverging vegetal coverage, temperature and moonlight influence the patch use indicated by the giving-up density (GUD) of a nocturnal small mammal community in sheltered and non-sheltered food patches. We investigated the foraging strategy of a widely spread community consisting of Desert hamsters (Phodopus roborovskii), Midday gerbils (Meriones meridianus), Northern three-toed jerboas (Dipus sagitta) and Long-eared hedgehogs (Hemiechinus auritus) in the Alashan Desert, China. The aim was to analyse foraging as a result of biotic and abiotic factors in undisturbed habitats, i.e. we did not manipulate any surrounding conditions and all animals were free ranging. Three habitats were investigated, named after the dominant species: Ammopiptanthus mongolicus, Corispermum sp. and Zygophyllum pterocarpum. The following results can be summarised: (1) we found no or only slight differences for the GUD within the habitats between open and sheltered places; (2) lunar illumination affected foraging during waxing and waning moon phases within the first part of the night; (3) ambient temperature and the presence of moonlight resulted in changes in the interspecific competition that impacted the GUD; and (4) we determined prominent differences amongst habitats within the four moon phases, especially between the more covered habitats Ammopiptanthus and Zygophyllum, in contrast to the Corispermum habitat with its sparse coverage ratio. In general, foraging effort was elevated in the more covered habitats. We found a preferred foraging activity in warm and dark parts of the night which may lead to elevated inter-individual competition resulting in higher GUDs. Warmer periods were preferred in nights with constant light conditions, although resource competition was again elevated. We concluded that the foraging strategy was mainly affected by habitat, whereas moonlight and temperature modulate the resulting GUD in undisturbed environments. The availability of vegetal shelters influences foraging only in detail.

Increases in food availability can tempt oribi antelope into taking greater risks at both large and small spatial scales

Differences in food availability and predation risk can influence how herbivores use landscapes. As a result, trade-offs between costs and benefits can influence habitat and patch selection. To determine how oribi antelope, Ourebia ourebi, weigh up costs and benefits when making habitat and patch level foraging decisions, we measured giving-up densities in artificial patches. First, we determined large-scale habitat use, and then explored how different variables explained patch use within habitats. When the availability of food within patches across the different habitats was equal, oribi preferred to feed in short and tall grasslands and avoided woodlands. Furthermore, the avoidance of woodlands extended into the surrounding grasslands, resulting in oribi feeding less intensively in grassland areas within 15 m of the woodlands. Within the safe grassland habitats, oribi preferred to feed in patches close to tall grass (i.e. escape cover), and where they could see beyond 2 m. These results suggest that oribi select habitats and patches in relation to perceived predation risk (i.e. predation costs outweigh potential food intake benefits). However, when we increased food availability within woodlands, oribi increased their large-scale risk-taking behaviour and fed in these woodlands. Furthermore, this increased risk taking extended to small-scale foraging decisions whereby an increase in food availability within woodlands caused oribi to increase their relative usage of patches that had sight lines as well as patches that were closer to potential ambush sites. Ultimately, these results highlight how changes in food availability can determine the degree to which herbivores are willing to increase their risk-taking behaviour, and how these changes can affect overall landscape use.

Interference competition: odours of an apex predator and conspecifics influence resource acquisition by red foxes.

Apex predators can impact smaller predators via lethal effects that occur through direct killing, and non-lethal effects that arise when fear-induced behavioural and physiological changes reduce the fitness of smaller predators. A general outcome of asymmetrical competition between co-existing predator species is that larger predators tend to suppress the abundances of smaller predators. Here, we investigate interference effects that an apex predator, the dingo (Canis dingo), has on the acquisition of food and water by the smaller red fox (Vulpes vulpes), by exposing free-ranging foxes to the odour of dingoes and conspecifics in an arid environment. Using giving-up densities we show that foxes foraged more apprehensively at predator-odour treatments than unscented controls, but their food intake did not differ between dingo- and fox-odour treatments. Using video analysis of fox behaviour at experimental water stations we show that foxes spent more time engaged in exploration behaviour at stations scented with fox odour and spent more time drinking at water stations scented with dingo odour. Our results provide support for the idea that dingo odour exerts a stronger interference effect on foxes than conspecific odour, but suggest that the odours of both larger dingoes and unfamiliar conspecifics curtailed foxes' acquisition of food resources.

Risk perception by endangered European bison Bison bonasus is context (condition) dependent

Patch use can illustrate the contributions that forage quality and foraging risk make in shaping foraging decisions made under the risk of being killed. We aimed to determine whether forage selection by European bison Bison bonasus was state-dependent in being shaped by risk (wolf predation or human poaching/culling avoidance) or nutrient quality at two time periods—early winter (when resources are abundant) and at the end of winter (when resources are scarce)—in Białowieża Primeval Forest (Poland). We used a giving-up density framework using the proportional consumption of hay provided by humans to measure the perceptions of risk in European bison. European bison resource selection was primarily driven by minimising the distance they travel over open ground in early winter (i.e. avoiding humans), however by the end of winter, when resources are scarce, bison selected haystacks for their nutrient quality (low fibre, high Mg and energy). This study illustrates how resource selection varies according to the condition of animals (i.e. state-dependency affects the marginal value theorem). It also indicates conservation managers using hay quality may actively manage human–bison conflicts in trouble spots and that bison are currently free from top-down limitation in Białowieża as they do not perceive wolves as threatening enough to alter their foraging behaviour.

Relaxation of risk-sensitive behaviour of prey following disease-induced decline of an apex predator, the Tasmanian devil.

Apex predators structure ecosystems through lethal and non-lethal interactions with prey, and their global decline is causing loss of ecological function. Behavioural changes of prey are some of the most rapid responses to predator decline and may act as an early indicator of cascading effects. The Tasmanian devil (Sarcophilus harrisii), an apex predator, is undergoing progressive and extensive population decline, of more than 90% in long-diseased areas, caused by a novel disease. Time since local disease outbreak correlates with devil population declines and thus predation risk. We used hair traps and giving-up densities (GUDs) in food patches to test whether a major prey species of devils, the arboreal common brushtail possum (Trichosurus vulpecula), is responsive to the changing risk of predation when they forage on the ground. Possums spend more time on the ground, discover food patches faster and forage more to a lower GUD with increasing years since disease outbreak and greater devil population decline. Loss of top-down effects of devils with respect to predation risk was evident at 90% devil population decline, with possum behaviour indistinguishable from a devil-free island. Alternative predators may help to maintain risk-sensitive anti-predator behaviours in possums while devil populations remain low.

Scatterhoarding rodents favor higher predation risks for cache sites: The potential for predators to influence the seed dispersal process

Scatterhoarding rodents often place caches in the open where pilferage rates are reduced, suggesting that they tradeoff higher risks of predation for more secure cache sites. We tested this hypothesis in two study systems by measuring predation risks inferred from measures of giving-up densities (GUDs) at known cache sites and other sites for comparison. Rodent GUDs were measured with small trays containing 3 L of fine sand mixed with sunflower seeds. In the first experiment, we relied on a 2-year seed dispersal study in a natural forest to identify caches of eastern gray squirrels (Sciurus carolinensis) and then measured GUDs at: (i) these caches; (ii) comparable points along logs and rocks where rodent activity was assumed highest; and (iii) a set of random points. We found that GUDs and, presumably, predation risks, were higher at both cache and random points than those with cover. At the second site, we measured GUDs of eastern gray squirrels in an open park system and found that GUDs were consistently lowest at the base of the tree compared to more open sites, where previous studies show caching by squirrels to be highest and pilferage rates by naïve competitors to be lowest. These results confirm that predation risks can influence scatterhoarding decisions but that they are also highly context dependent, and that the landscape of fear, now so well documented in the literature, could potentially shape the temporal and spatial patterns of seedling establishment and forest regeneration in systems where scatterhoarding is common.

Foraging and habitat use of eastern cottontails (Sylvilagus floridanus) in an urban landscape

Urban landscapes such as college campuses, arboretums, and backyards provide excellent habitats for education and research into animal behavior. We investigated aspects of the foraging activity of free-ranging Eastern cottontails (Sylvilagus floridanus) on the campuses of the University of Illinois at Chicago and Lawrence University. We used giving-up densities (GUD) to test for habitat selection and patch-use behavior by cottontails inhabiting an urban landscape with a gradient of shrub and tree cover. In addition, we used small garden fences around feeding trays to test their effect as obstacles to the foraging of cottontails. Foraging activity was significantly higher under cover than in the open. GUDs were significantly lower in proximity to cover; in addition, shrubs were preferred over low-laying trees as the source of cover. Camera trap photos revealed solitary foraging, highest in the late afternoon and early morning. We demonstrated that surrounding a food patch with 3 or 4 fences increased the cottontails’ GUDs. Similar to natural habitats, urban landscapes offer heterogeneous environments that force their inhabitants to allocate their foraging activity according to their perceived stresses. Studying effect of habitat complexity on foraging responses provides useful tools to study ecological interactions and can help minimize the damage that cottontails cause within urban environments such as city parks and private gardens.

A game of cat-and-mouse: microhabitat influences rodent foraging in recently burnt but not long unburnt shrublands

We investigated the influence of vegetation structure and fire history on the foraging behavior of small rodents (Notomys mitchellii, Pseudomys hermannsburgensis, and Mus musculus) by conducting giving-up density (GUD) experiments in recently burnt (9–13 years since last fire) and long unburnt shrublands (> 40 years), and open and sheltered microhabitats, in a semiarid region of Western Australia. We predicted that rodents would spend less time foraging in recently burnt shrublands and open microhabitat and that the influence of microhabitat would be weaker in long unburnt compared to more recently burnt vegetation. Our findings show that fire history and microhabitat structure influence the foraging behavior of the study species and that the influence of microhabitat varies between fire histories. GUDs were higher in long unburnt vegetation and in open microhabitats. There was a microhabitat effect in recently burnt vegetation, but not in long unburnt. Rodents foraged more in sheltered microhabitats probably because predator encounters are less likely to occur there and it provides them with greater refuge from predation. The presence of a microhabitat effect in recently burnt, but not long unburnt vegetation suggests that understory vegetation density is more important in mediating predation risk than canopy density. Future studies of small mammal responses to land management actions should include behavioral, as well as population-level responses to differing fire regimes.

Foraging in groups affects giving-up densities: solo foragers quit sooner

The giving-up density framework is an elegant and widely adopted mathematical approach to measuring animals' foraging decisions at non-replenishing artificial resource patches. Under this framework, an animal should "give up" when the benefits of foraging are outweighed by the costs (e.g., predation risk, energetic, and/or missed opportunity costs). However, animals of many species may forage in groups, and group size is expected to alter perceived predation risk and hence influence quitting decisions. Yet, most giving-up density studies assume either that individuals forage alone or that giving-up densities are not affected by group foraging. For animals that forage both alone and in groups, differences in giving-up densities due to group foraging rather than experimental variables may substantially alter interpretation. However, no research to date has directly investigated how group foraging affects the giving-up density. We used remote-sensing cameras to identify instances of group foraging in two species of Rattus across three giving-up density experiments to determine whether group foraging influences giving-up densities. Both Rattus species have been observed to vary between foraging alone and in groups. In all three experiments, solo foragers left higher giving-up densities on average than did group foragers. This result has important implications for studies using giving-up densities to investigate perceived risk, the energetic costs of searching, handling time, digestion, and missed opportunity costs, particularly if groups of animals are more likely to experience certain experimental treatments. It is critically important that future giving-up density studies consider the effects of group foraging.

Divergent foraging behaviour of a desert rodent, Notomys fuscus, in covered and open microhabitats revealed using giving up densities and video analysis

We used a combination of giving up densities (GUD) and behavioural analysis from video footage to test the response of an Australian desert rodent, Notomys fuscus, to the experimental provision of cover microhabitat in the Strzelecki Desert, Australia. In many ecosystems, cover microhabitats are considered to be safe foraging locations for rodents. The response of bipedal desert rodents to cover microhabitats is less certain, with varied findings, due to their use of open habitats for fast travel. Notomys fuscus returned lower GUDs in cover than in open microhabitats and moved slowly for a greater amount of time under cover than in the open. These results suggest that N. fuscus has a preference for foraging under cover, where predation risk is lower, and under these conditions took longer to assess the cover microhabitat before foraging. This was distinctly different to the ‘get in, get out’ behaviour associated with foraging in open habitats. We advocate for the combined measurement of GUD and behavioural analysis using video footage as a way to improve understanding of rodents’ foraging behaviour.

Hypoxic refuges, predator-prey interactions and habitat selection by fishes.

Localized hypoxic habitats were created in Delta Marsh, Manitoba, Canada to determine the potential of regions of moderate hypoxia to act as refuges for forage fishes from piscine predators. Minnow traps and giving-up density (GUD) plates (plexiglas plates covered with trout crumble and fine gravel) were used to assess habitat use and perceived habitat quality for forage fishes, respectively, while passive integrated transponder tags provided data on habitat use by predator species to assess the level of predation risk. Data were collected both before and after a hypoxia manipulation (2-3 mg l(-1) dissolved oxygen, DO) to create a before-after control-effect style experiment. Fathead minnows Pimephales promelas were more abundant and consumed more food from GUD plates in hypoxic bays after the DO manipulation, indicating hypoxic locations were perceived as higher quality, lower-risk habitats. The frequency of predator visits was not consistently affected. The duration of visits, and therefore the total time spent in these habitats, however, was significantly shorter. These predator data, combined with the prey information, are consistent with the hypothesis that hypoxic regions function as predator refuges. The refuge effect is not the result of predator exclusion, however; instead predators are rendered less capable of foraging and pose less of a threat in hypoxic locations.

Morphological and physiological responses of seagrasses (Alismatales) to grazers (Testudines: Cheloniidae) and the role of these responses as grazing patch abandonment cues.

Green sea turtles, Chelonia mydas, are grazers influencing the distribution of seagrass within shallow coastal ecosystems, yet the drivers behind C. mydas patch use within seagrass beds are largely unknown. Current theories center on food quality (nutrient content) as the plant responds to grazing disturbances; however, no study has monitored these parameters in a natural setting without grazer manipulation. To determine the morphological and physiological responses potentially influencing seagrass recovery from grazing disturbances, seagrasses were monitored for one year under three different grazing scenarios (turtle grazed, fish grazed and ungrazed) in a tropical ecosystem in Akumal Bay, Quintana Roo, Mexico. Significantly less soluble carbohydrates and increased nitrogen and phosphorus content in Thalassia testudinum were indicative of the stresses placed on seagrasses during herbivory. To determine if these physiological responses were the drivers of the heterogeneous grazing behavior by C. mydas recorded in Akumal Bay, patches were mapped and monitored over a six-month interval. The abandoned patches had the lowest standing crop rather than leaf nutrient or rhi- zome soluble carbohydrate content. This suggests a modified Giving Up Density (GUD) behavior: the critical threshold where cost of continued grazing does not provide minimum nutrients, therefore, new patches must be utilized, explains resource abandonment and mechanism behind C. mydas grazing. This study is the first to apply GUD theory, often applied in terrestrial literature, to explain marine herbivore grazing behavior.

Personality affects the foraging response of a mammalian herbivore to the dual costs of food and fear

Predators attack and plants defend, so herbivores face the dilemma of how to eat enough without being eaten. But do differences in the personality of herbivores affect the foraging choices of individuals? We explored the ecological impact of personality in a generalist herbivore, the brushtail possum (Trichosurus vulpecula). After quantifying personality traits in wild individuals brought temporarily into captivity, we tested how these traits altered foraging by individuals when free-ranging in their natural habitat. To measure their responses to the dual costs of predation risk and plant toxin, we varied the toxin concentration of food in safe foraging patches against paired, non-toxic risky patches, and used a novel synthesis of a manipulative Giving-Up-Density (GUD) experiment and video behavioural analysis. At the population level, the cost of safe patches pivoted around that of risky patches depending on food toxin concentration. At the individual level, boldness affected foraging at risky high-quality food patches (as behavioural differences between bold and shy), and at safe patches only when food toxin concentration was low (as differences in foraging outcome). Our results ecologically validate the personality trait of boldness, in brushtail possums. They also reveal, for the first time, a nuanced link between personality and the way in which individuals balance the costs of food and fear. Importantly, they suggest that high plant defence effectively attenuates differences in foraging behaviour arising from variation in personality, but poorly defended plants in safe areas should be differentially subject to herbivory depending on the personality of the herbivore.

Uniform predation risk in nature: common, inconspicuous, and a source of error to predation risk experiments

Previous studies indicate that when predation risk is uniform across habitats, foragers concentrate their exploitation in fewer patches. Although uniform predation risk may seem rare in nature, some scenarios might cause it. Testing all scenarios in a single experiment is unfeasible; therefore, we developed a model that points whether concentration of exploitation in specific habitats due to uniform risk requires parameter values similar to what is found in literature. This model was based on Brown’s (Behav Ecol Sociobiol 22:37–47, 1988) fitness function but rescaled to multiple habitats and predators, including uniform risk predators. Deriving function’s maximum allowed comparisons with giving-up density studies. Results showed that uniform predation risk had a u-shaped effect in habitat exploitation, causing a concentration of habitat exploitation at probabilities of survival from 0.2 to 0.8. However, the length of this interval and degree of concentration depended on the value of safety to forager fitness. Heterogeneous, nonuniform, predation risk decreases habitat exploitation where it was higher, therefore suppressing the effect of uniform risk on prey behavior. Time spent in the focal habitat and metabolic costs reduced the detectability of habitat concentration, while total time did not. We also found that uniform risk reduced accuracy of heterogeneous risk measurements. Future studies should aim to control all possible predators, as even the mild ones can induce complex behavior.

Giving-up densities and foraging behaviour indicate possible effects of shrub encroachment on arctic ground squirrels

Behavioural responses of prey to predation risk are often mediated by vegetation structure. Erect woody shrubs are increasing in many arctic and alpine environments, and this change in habitat structure has the potential to alter perception of risk and fear for foraging herbivores. To assess the role of shrub cover in determining behavioural responses to foraging under predation risk, we used measurements of giving-up density (GUD) and video recordings of vigilance behaviour of individual Arctic ground squirrels, Urocitellus parryii, across an alpine tundra to shrub ecotone. Dense shrub habitat was associated with higher GUDs, implying that foraging costs were higher in dense shrub than in less shrub-dominated habitats. Foraging strategies differed between habitats, with a negative relationship between visibility and GUD in high-visibility, open-tundra habitats and a positive relationship between visibility and GUD in low-visibility, shrub-dominated habitats, which may be indicative of alternative foraging strategies in different habitats. Squirrels initially made a high investment in vigilance, which was independent of patch residence time. This presumably increases the costs of quitting patches earlier. In shrub-dominated habitat, erect bipedal forms of vigilance were also observed more frequently. Our results indicate that shrub encroachment into northern and alpine tundra may impose costs on foraging arctic ground squirrels and alter foraging strategies.