Foraging patterns of yellow-bellied marmosts: role of kinship and individual variability

Summary Two colonies of yellow-bellied marmots (Marmota flaviventris) at an elevation of 2900 m in Colorado were studied to elucidate the role of various behavioral and ecological factors as determinants of spatial foraging patterns. The locations of known individuals were periodically recorded. These locality data were plotted as three-dimensional block diagrams, the peak heights representing the frequency of observation. Predation risk and vegetation distribution influenced the location of foraging areas; kinship was an important factor in the determination of the amount of foraging area shared between individual marmots. Spatial overlap tended to be greater among close kin, but this was modified by individual behavioral characteristics, reproductive state, the existence of separate burrow systems within a colony, and the age of the animal. Mothers and juveniles, and littermates as young and resident yearlings, had nearly identical foraging areas.     

Predation risk and foraging behavior of the hoary marmot in Alaska

Summary I observed hoary marmots for three field seasons to determine how the distribution of food and the risk of predation influenced marmots' foraging behavior. I quantified the amount of time Marmota caligata foraged in different patches of alpine meadows and assessed the distribution and abundance of vegetation eaten by marmots in these meadows. Because marmots dig burrows and run to them when attacked by predators, marmot-toburrow distance provided an index of predation risk that could be specified for different meadow patches.Patch use correlated positively with food abundance and negatively with predation risk. However, these significant relationships disappeared when partial correlations were calculated because food abundance and risk were intercorrelated. Using multiple regression, 77.0% of the variance in patch use was explained by a combination of food abundance, refuge burrow density, and a patch's distance from the talus where sleeping burrows were located. Variations in vigilance behavior (look-ups to search for predators while feeding) according to marmots' ages, the presence of other conspecifics, and animals' proximity to their sleeping burrows all indicated that predation risk influenced foraging.In a forage-manipulation experiment, the use of forage-enhanced patches increased six-fold, verifying directly the role of food availability on patch used. Concomitant with increased feeding, however, was the intense construction of refuge burrows in experimental patches that presumably reduced the risk of feeding. Thus, I suggest that food and predation risk jointly influence patch use by hoary marmots and that both factors must be considered when modeling the foraging behavior of species that can be predator and prey simultaneously.     

The influence of reproductive status on foraging by hoary marmots (Marmota caligata)

Summary Predictions were made and tested, comparing the foraging behavior of reproductive (rf) and nonreproductive (nrf) female hoary marmots, with the following findings: In June, no differences occur between rf's and nrf's, regarding daytime foraging. However, rf's forage more in the evening and during inclement weather, suggesting that greater nutritional needs and higher reproductive value select for the assumption of more risk while foraging. These differences disappear by August, when nutritional needs and reproductive values of rf's and nrf's are comparable. Finally, rf's reduce their near-burrow foraging relative to nrf's, which minimizes competition with their own young.     

Social dynamics of juvenile marmots: Role of kinship and individual variability

Summary A population of eight juvenile female yellow-bellied marmots (Marmota flaviventris) was introduced into a marmot locality from which all other marmots were removed. Social interactions were monitored in the field and the individual behavioral profile of each animal was determined by mirror image stimulation. Social interactions were unequally distributed among the eight juveniles. Neither body size nor kinship were significantly related to frequencies of social interactions. Social interactions were significantly related to individual differences.     

Effect of disturbance on foraging: whelk activity on wave-exposed rocky shores with minimal tidal range

For slow-moving rocky intertidal predators such as whelks, frequent stress can be detrimental. Most studies on the foraging behavior of whelks have been conducted in regions where tidal amplitude is >1 m and on relatively small species. We studied the effects of wave action, desiccation, and water temperature on the foraging behavior of a large (approximately 80 mm) rocky shore whelk, Stramonita haemastoma, at the small-tide (<40 cm) but wave-exposed Israeli Mediterranean coast. We hypothesized that in such conditions foraging activity of this large predator will be greatly limited. Field observations show that when wave height exceeds 0.5 m, activity of whelks decreases by at least threefold relative to that seen under calm-sea conditions, and most whelks remain inside shelters. Wave height data from offshore moorings demonstrate that such conditions occur along the coast >85% of the time. Whelks move into shelters or completely disappear when exposed to prolonged desiccation conditions that can last for days along the shore during spring and autumn. Foraging activity is greater at night than in daytime and might be related to lighter winds and calmer sea conditions at night. Laboratory experiments show that elevated water temperatures during winter do not result in increased predation rates relative to those measured during spring. This indicates that a seasonal endogenous biological rhythm may exist. Our findings demonstrate that the foraging activity of large whelks can be extremely constrained by high rates of disturbance, that is, frequent wave action, and less frequent desiccation. We claim that high rates of disturbance in the eastern Mediterranean explain why large whelks are scarce in intertidal habitats where food is plentiful but suitable shelter is rare.Communicated by G.F. Humphrey, Sydney     

Antipredator strategies of house finches: are urban habitats safe spots from predators even when humans are around?

Urbanization decreases species diversity, but it increases the abundance of certain species with high tolerance to human activities. The safe-habitat hypothesis explains this pattern through a decrease in the abundance of native predators, which reduces predation risk in urban habitats. However, this hypothesis does not consider the potential negative effects of human-associated disturbance (e.g., pedestrians, dogs, cats). Our goal was to assess the degree of perceived predation risk in house finches (Carpodacus mexicanus) through field studies and semi-natural experiments in areas with different levels of urbanization using multiple indicators of risk (flock size, flight initiation distance, vigilance, and foraging behavior). Field studies showed that house finches in more urbanized habitats had a greater tendency to flock with an increase in population density and flushed at larger distances than in less urbanized habitats. In the semi-natural experiment, we found that individuals spent a greater proportion of time in the refuge patch and increased the instantaneous pecking rate in the more urbanized habitat with pedestrians probably to compensate for the lower amount of foraging time. Vigilance parameters were influenced in different ways depending on habitat type and distance to flock mates. Our results suggest that house finches may perceive highly urbanized habitats as more dangerous, despite the lower number of native predators. This could be due to the presence of human activities, which could increase risk or modify the ability to detect predators. House finches seem to adapt to the urban environment through different behavioral strategies that minimize risk.     

Demographic Consequences of Changed Pupping and Hauling Sites of the Hawaiian Monk Seal

Abstract: During the last 30 years, changes in the size of Hawaiian monk seal populations at several locations have been associated with the amount and type of human disturbance. Recreational beach activities caused monk seals to alter their pupping and hauling patterns. Survival of pups in suboptimal habitats was low, leading to gradual population declines. During the last decade at Kure Atoll, the process has been reversed human disturbance on beaches has decreased and traditional pupping and hauling sites have been reestablished Subsequently, high survival rates of young seals, coupled with two successful enhancement programs for female pups, have led to dramatic changes in the age and sex composition of the population. Based on these changes, the monk seal population at Kure Atoll soon should begin to increase. Apparently small behavioral changes in such vital activities as feeding and reproduction can have large demographic consequences. Therefore, monitoring of endangered species should include data on habitat use and age and sex composition, as well as estimates of abundance.     

Relationships between Human Disturbance and Wildlife Land Use in Urban Habitat Fragments

Abstract: Habitat remnants in urbanized areas typically conserve biodiversity and serve the recreation and urban open‐space needs of human populations. Nevertheless, these goals can be in conflict if human activity negatively affects wildlife. Hence, when considering habitat remnants as conservation refuges it is crucial to understand how human activities and land uses affect wildlife use of those and adjacent areas. We used tracking data (animal tracks and den or bed sites) on 10 animal species and information on human activity and environmental factors associated with anthropogenic disturbance in 12 habitat fragments across San Diego County, California, to examine the relationships among habitat fragment characteristics, human activity, and wildlife presence. There were no significant correlations of species presence and abundance with percent plant cover for all species or with different land‐use intensities for all species, except the opossum (Didelphis virginiana), which preferred areas with intensive development. Woodrats (Neotoma spp.) and cougars (Puma concolor) were associated significantly and positively and significantly and negatively, respectively, with the presence and prominence of utilities. Woodrats were also negatively associated with the presence of horses. Raccoons (Procyon lotor) and coyotes (Canis latrans) were associated significantly and negatively and significantly and positively, respectively, with plant bulk and permanence. Cougars and gray foxes (Urocyon cinereoargenteus) were negatively associated with the presence of roads. Roadrunners (Geococcyx californianus) were positively associated with litter. The only species that had no significant correlations with any of the environmental variables were black‐tailed jackrabbits (Lepus californicus) and mule deer (Odocoileus hemionus). Bobcat tracks were observed more often than gray foxes in the study area and bobcats correlated significantly only with water availability, contrasting with results from other studies. Our results appear to indicate that maintenance of habitat fragments in urban areas is of conservation benefit to some animal species, despite human activity and disturbance, as long as the fragments are large.     

Use of Acoustic Tools to Reveal Otherwise Cryptic Responses of Forest Elephants to Oil Exploration

Abstract: Most evaluations of the effects of human activities on wild animals have focused on estimating changes in abundance and distribution of threatened species; however, ecosystem disturbances also affect aspects of animal behavior such as short‐term movement, activity budgets, and reproduction. It may take a long time for changes in behavior to manifest as changes in abundance or distribution. Therefore, it is important to have methods with which to detect short‐term behavioral responses to human activity. We used continuous acoustic and seismic monitoring to evaluate the short‐term effects of seismic prospecting for oil on forest elephants (Loxodonta cyclotis) in Gabon, Central Africa. We monitored changes in elephant abundance and activity as a function of the frequency and intensity of acoustic and seismic signals from dynamite detonation and human activity. Elephants did not flee the area being explored; the relative number of elephants increased in a seasonal pattern typical of elsewhere in the ecosystem. In the exploration area, however, they became more nocturnal. Neither the intensity nor the frequency of dynamite blasts affected the frequency of calling or the daily pattern of elephant activity. Nevertheless, the shift of activity to nocturnal hours became more pronounced as human activity neared each monitored area of forest. This change in activity pattern and its likely causes would not have been detected through standard monitoring methods, which are not sensitive to behavioral changes over short time scales (e.g., dung transects, point counts) or cover a limited area (e.g., camera traps). Simultaneous acoustic monitoring of animal communication, human, and environmental sounds allows the documentation of short‐term behavioral changes in response to human disturbance.     

Consequences of behavioral vs. numerical dominance on foraging activity of desert seed-eating ants

Dominance relationships among species play a major role in the structure of animal communities. Yet, dominant species with different trade-offs in resource exploitation and monopolization could affect community structure in variable ways. In ants, dominant species could be classified into either behavioral dominants that exhibit territorial aggression or numerical dominants that exhibit high biomass or frequency of occurrence. While each class of dominance has generally been found to negatively affect the foraging activity of species in ant communities, the concurrent effect of both classes of species has never been tested. Here, we examined the effects of two behaviorally dominant species, Crematogaster inermis and Monomorium salomonis, and a numerically dominant species, Messor arenarius, on the foraging behavior of seed-eating species in a desert ant assemblage. In a 1-year study, the foraging activity of the ant species was assessed using seed baits, which were sampled during night and day. While the numerically dominant species exhibited high foraging efficiency and negatively affected the ability of other seed-eating species to obtain seeds, significantly more seeds remained at baits that were occupied the previous night by each of the two behaviorally dominant species, possibly due to aggressive exclusion of M. arenarius foragers from the baits. This exclusion also facilitated greater foraging activity of the seed-eating species. Our results demonstrate how these two types of dominance could differently affect the foraging activity of ant species in the community.     

Imperfectly optimal animals

Summary We consider models of behavior that apply to two different problems: when a predator should leave a foraging site and how a female should choose the best available male. In each case we derive rules for an optimal solution to the problem. We also derive models based on very simple, plausible rules of behavior that we suspect animals may actually use. Although the expected payoffs from optimality models always exceed the expected payoffs from our simpler behavioral models, under certain conditions the difference is not large. When good foraging sites last but a short time and when females' mobility in their habitat is limited, the results of simple models and optimal models are very close indeed.Because of the difficulty of distinguishing between the results of each type of model and because natural selection will presumably provide a best mix of solutions to a range of problems rather than a best solution to any one problem, we suggest that behavioral ecologists expend more effort on simple, plausible models of animal behavior. Such models provide ready-made testable hypotheses about the animal's approximation to optimality and about the actual mechanisms of behavior.     

Behavioral resource depression and decaying perceived risk of predation in two species of coexisting gerbils

Summary Behavioral resource depression occurs when the behavior of prey individuals changes in response to the presence of a predator, resulting in a reduction of the encounter rate of the predator with its prey. Here I present experimental evidence on the response of two species of gerbils (Gerbillus allenbyi and G. pyramidum) to the presence of barn owls. I conducted the experiments in a large aviary. Both gerbils responded to the presence of barn owl predators by foraging in fewer resource patches (seed trays) and by quitting foraged resource patches at a higher resource harvest rate (giving-up density of resource; GUD). This reduced the amount of time gerbils were exposed to owl predation, and hence the encounter rate of owls with gerbils, i.e., behavioral resource depression. Thus, the presence of owls imposes a foraging cost on gerbils due to risk of predation, and also on the owls themselves due to resource depression. I then examined how resource depression relaxed over time following exposure to owls. In the days following an encounter with the predator, the reduction in foraging activity for both gerbil species eased. Increasing numbers of trays were foraged each day, and GUDs in seed trays declined. The two gerbils differed in their rate of recovery, with G. pyramidum returning to prepredator levels of foraging after 1 or 2 nights and G. allenbyi taking 5 nights or longer. Interspecific differences in recovery rates may be based on differences between the species in vulnerability to predation and/or ability to detect the presence of predators. The differences in recovery rates may be due to optimal memory windows or decay rates, where differences between species are based on risk of predation or on how perceived risk changes with time since a predator was last encountered. Finally, differences between or among competitors in recovery from resource depression may provide foraging opportunities in time for the species which recover most quickly and may have implications for species coexistence.     

Social attributes and associated performance measures in marmots: bigger male bullies and weakly affiliating females have higher annual reproductive success

Studying the structure of social interactions is fundamental in behavioral ecology as social behavior often influences fitness and thus natural selection. However, social structure is often complex, and determining the most appropriate measures of variation in social behavior among individuals can be difficult. Social network analysis generates numerous, but often correlated, measures of individual connectedness derived from a network of interactions. We used measures of individual connectedness in networks of affiliative and agonistic interactions in yellow-bellied marmots, Marmota flaviventris, to first determine how variance was structured among network measures. Principal component analysis reduced our set of network measures to four “social attributes” (unweighted connectedness, affiliation strength, victimization, and bullying), which revealed differences between patterns of affiliative and agonistic interactions. We then used these extracted social attributes to examine the relationship between an individual’s social attributes and several performance measures: annual reproductive success, parasite infection, and basal stress. In male marmots, bullying was positively associated with annual reproductive success, while in females, affiliation strength was negatively associated with annual reproductive success. No other social attributes were significantly associated with any performance measures. Our study highlights the utility of considering multiple dimensions when measuring the structure and functional consequences of social behavior.     

Modeling high-frequency position data of large herbivores with a phase-state model

Understanding the rules and factors that drive the foraging behavior of large herbivores is important to describe their interaction with the landscape at various spatial scales. Some unresolved questions refer to landscape-behavioral interactions that result in oriented or random search in seasonally changing landscapes. Remotely sensed position data indicate that herbivores select local patches of heterogeneous landscapes depending on a complex host of dynamically varying animal and environmental conditions. Since foraging paths consist in successions of relatively short steps, increasing the frequency at which position information is acquired would contribute to entangle the mechanisms resulting in herbivores’ foraging paths. We addressed the question whether herbivores would obtain information at a patch scale that would modify their distribution at a landscape scale based on directed movement or navigation ability. We considered a set of 100,000 high-frequency (1 min intervals) position data of several free-ranging sheep (Ovis aries) at a seasonal-varying range (Patagonian Monte, Argentina) and observed their movements at landscape and at single vegetation patch scales. At a landscape scale, we inspected the spatial co-variation of seasonally varying forage offer and ewes’ movement speeds. At a patch scale, we developed a phase-state (P-S) model of movement cycles based on the occurrence of behavioral phases along foraging paths, and fitted it to the observed daily time series of ewes’ movement speeds. Ewes were preferentially distributed in areas with high forage offer during periods of low forage availability and the reverse occurred during the season of high forage availability. Parameters of the model of activity cycles amenable to control by ewes (duration of speed phases, time elapsed between speed cycles) did not covariate with forage offer, but varied significantly among ewes. The shape (kurtosis) parameter of the model of movement cycles, one which is unlikely under ewes’ control, co-varied significantly with spatial forage offer but did not differ among ewes. We conclude that ewes allocated foraging time along a series of similar movement efforts irrespective of forage availability at small patches. Average forage scarcity at multi-patch level increases the ratio of searching to feeding time. This results in apparent selective time allocation to richer forage areas but does not imply evidence for oriented movement at a landscape scale. We advance a behavioral-based definition of forage patches and discuss its implications in developing foraging theory and models. The P-S model applied to high-frequency position data of large herbivores substantially improves the interpretation of the factors controlling their time allocation in space with respect to previous models of herbivore spatial behavior by discriminating among behavioral-based and environmentally induced components of their movements.     

Different habitats, different habits? Response to foraging information in the parasitic wasp Venturia canescens

The parasitic wasp, Venturia canescens (Gravenhorst) (Hymenoptera: Ichneumonidae), has two reproductive modes, namely, thelytoky or arrhenotoky, and occurs in habitats with highly variable or relatively stable host abundances, respectively. Since information processing is costly, we expected that information indicating resource availability would be mainly used by the thelytokous wasps and less so by the arrhenotokous type. This idea was explored by two different approaches. In a study on patch-time allocation, we used females from ten populations and measured patch-residence times of individuals that visited multiple patches at different encounter rates. In a more detailed approach, thelytokous and arrhenotokous females from a single location were observed continuously while foraging, and all behaviors were recorded. Wasps of both reproductive modes (i.e., both habitat types) used information for the assessment of habitat quality. However, the way that the information was used differed between them. Whereas thelytokous females used foraging information to maximize their efficiency at high patch-encounter rates, arrhenotokous females merely reduced the number of offspring produced without changing patch times. The behavior of the arrhenotokous females should result in a spreading of offspring across the habitat and, thus, reduced sib-mating. The foraging strategy of these wasps might therefore be an adaptation to reduce costs associated with inbreeding.     

Individual differences in the behavior of juvenile yellow-bellied marmots

Summary Yellow-bellied marmots express considerable individuality as measured by behavior in a maze, mirror-image stimulation (MIS), and social behavior in the field. Maze behavior discriminated between residents and dispersers; residents explored the maze more widely than did dispersers. Males could not be distinguished from females nor survivors from non-survivors by their maze behavior. A group of six yearling females was established to examine the relationship between individual behavioral phenotypes (as determined by MIS) and social behavior in the field. This experiment provided a situation in which social behavior was not influenced by age, sex, or reproduction (female yearlings are non-reproductive). The number of social interactions per individual ranged from 25 to 69. The number of observed interactions per individual differend significantly from the expected for greeting, allogrooming, total amicable, play, and total social interactions. Rankings of greeting, total amicable, and total interactions were directly correlated with rankings on the avoidance axis; play was inversely correlated with the approach axis. These results suggest that marmots have individual behavioral phenotypes that are expressed in their social interactions with their conspecifics.     

A systematic survey of the integration of animal behavior into conservation

The role of behavioral ecology in improving wildlife conservation and management has been the subject of much recent debate. We sought to answer 2 foundational questions about the current use of behavioral knowledge in conservation: To what extent is behavioral knowledge used in wildlife conservation and management, and how does the use of animal behavior differ among conservation fields in both frequency and types of use? We searched the literature for intersections between key fields of animal behavior and conservation and created a systematic heat map (i.e., graphical representation of data where values are represented as colors) to visualize relative efforts. Some behaviors, such as dispersal and foraging, were commonly considered (mean [SE] of 1147.38 [353.11] and 439.44 [108.85] papers per cell, respectively). In contrast, other behaviors, such as learning, social, and antipredatory behaviors were rarely considered (mean [SE] of 33.88 [7.62], 44.81 [10.65], and 22.69 [6.37] papers per cell, respectively). In many cases, awareness of the importance of behavior did not translate into applicable management tools. Our results challenge previous suggestions that there is little association between the fields of behavioral ecology and conservation and reveals tremendous variation in the use of different behaviors in conservation. We recommend that researchers focus on examining underutilized intersections of behavior and conservation themes for which preliminary work shows a potential for improving conservation and management, translating behavioral theory into applicable and testable predictions, and creating systematic reviews to summarize the behavioral evidence within the behavior‐conservation intersections for which many studies exist.     

Limited flexibility in the temporal caste system of the honey bee

Caste theory predicts that social insect colonies are organized into stable groups of workers specialized on particular task sets. Alternative concepts of organization of work suggest that colonies are composed of extremely flexible workers able to perform any task as demand necessitates. I explored the flexibility of workers in temporal castes of the honey bee Apis mellifera by determining the ability of colonies to reorganize labor after a major demographic disturbance. I evaluated the flexibility of temporal castes by comparing the foraging rates of colonies having just lost their foragers with colonies having also lost their foragers but having been given a week to reorganize. The population sizes and contents of the colonies in each group were equalized and foraging rates were recorded for one week. Colonies given a weeks initial recovery time after the loss of their foragers were found to forage at significantly higher rates than those colonies given no initial recovery time. This result was consistent for nectar and pollen foraging. These results suggest that honeybee workers lack sufficient flexibility to reorganize labor without compromising foraging. This finding is consistent with the caste concept model of organization of work in insect societies.     

Optimal movement strategies for social foragers in unpredictable environments

Spatial movement models often base movement decision rules on traditional optimal foraging theories, including ideal free distribution (IFD) theory, more recently generalized as density-dependent habitat selection (DDHS) theory, and the marginal value theorem (MVT). Thus optimal patch departure times are predicted on the basis of the density-dependent resource level in the patch. Recently, alternatives to density as a habitat selection criterion, such as individual knowledge of the resource distribution, conspecific attraction, and site fidelity, have been recognized as important influences on movement behavior in environments with an uncertain resource distribution. For foraging processes incorporating these influences, it is not clear whether simple optimal foraging theories provide a reasonable approximation to animal behavior or whether they may be misleading. This study compares patch departure strategies predicted by DDHS theory and the MVT with evolutionarily optimal patch departure strategies for a wide range of foraging scenarios. The level of accuracy with which individuals can navigate toward local food sources is varied, and individual tendency for conspecific attraction or repulsion is optimized over a continuous spectrum. We find that DDHS theory and the MVT accurately predict the evolutionarily optimal patch departure strategy for foragers with high navigational accuracy for a wide range of resource distributions. As navigational accuracy is reduced, the patch departure strategy cannot be accurately predicted by these theories for environments with a heterogeneous resource distribution. In these situations, social forces improve foraging success and have a strong influence on optimal patch departure strategies, causing individuals to stay longer in patches than the optimal foraging theories predict.     

When rate maximization is impulsive

Although optimal foraging theory predicts that natural selection should favor animal behaviors that maximize long-term rate of gain, behaviors observed in the laboratory tend to be impulsive. In binary-choice experiments, despite the long-term gain of each alternative, animals favor short handling times. Most explanations of this behavior suggest that there is hidden rationality in impulsiveness. Instead, we suggest that simultaneous and mutually exclusive binary-choice encounters are often unnatural and thus immune to the effects of natural selection. Using a simulation of an imperfect forager, we show how a simple strategy (i.e., an intuitive model of animal behavior) that maximizes long-term rate of gain under natural conditions appears to be impulsive under operant laboratory conditions. We then show how the accuracy of this model can be verified in the laboratory by biasing subjects with a short pre-experiment ad libitum high-quality feeding period. We also show a similar behavioral mechanism results in diet preferences that are qualitatively consistent with the digestive rate model of foraging (i.e., foraging under digestive rate constraints).