Using global remote camera data of a solitary species complex to evaluate the drivers of group formation.

The social system of animals involves a complex interplay between physiology, natural history, and the environment. Long relied upon discrete categorizations of "social" and "solitary" inhibit our capacity to understand species and their interactions with the world around them. Here, we use a globally distributed camera trapping dataset to test the drivers of aggregating into groups in a species complex (martens and relatives, family Mustelidae, Order Carnivora) assumed to be obligately solitary. We use a simple quantification, the probability of being detected in a group, that was applied across our globally derived camera trap dataset. Using a series of binomial generalized mixed-effects models applied to a dataset of 16,483 independent detections across 17 countries on four continents we test explicit hypotheses about potential drivers of group formation. We observe a wide range of probabilities of being detected in groups within the solitary model system, with the probability of aggregating in groups varying by more than an order of magnitude. We demonstrate that a species' context-dependent proclivity toward aggregating in groups is underpinned by a range of resource-related factors, primarily the distribution of resources, with increasing patchiness of resources facilitating group formation, as well as interactions between environmental conditions (resource constancy/winter severity) and physiology (energy storage capabilities). The wide variation in propensities to aggregate with conspecifics observed here highlights how continued failure to recognize complexities in the social behaviors of apparently solitary species limits our understanding not only of the individual species but also the causes and consequences of group formation.

Small mammal personalities generate context dependence in the seed dispersal mutualism.

Mutualisms are foundational components of ecosystems with the capacity to generate biodiversity through adaptation and coevolution and give rise to essential services such as pollination and seed dispersal. To understand how mutualistic interactions shape communities and ecosystems, we must identify the mechanisms that underlie their functioning. One mechanism that may drive mutualisms to vary in space and time is the unique behavioral types, or personalities, of the individuals involved. Here, our goal was to examine interindividual variation in the seed dispersal mutualism and identify the role that different personalities play. In a field experiment, we observed individual deer mice (Peromyscus maniculatus) with known personality traits predating and dispersing seeds in a natural environment and classified all observed interactions made by individuals as either positive or negative. We then scored mice on a continuum from antagonistic to mutualistic and found that within a population of scatter hoarders, some individuals are more mutualistic than others and that one factor driving this distinction is animal personality. Through this empirical work, we provide a conceptual advancement to the study of mutualism by integrating it with the study of intraspecific behavioral variation. These findings indicate that animal personality is a previously overlooked mechanism generating context dependence in plant­animal interactions and suggest that behavioral diversity may have important consequences for the functioning of mutualisms.

Population genomic structure of a widespread, urban-dwelling mammal: The eastern grey squirrel (Sciurus carolinensis).

Urbanization is a persistent and widespread driver of global environmental change, potentially shaping evolutionary processes due to genetic drift and reduced gene flow in cities induced by habitat fragmentation and small population sizes. We tested this prediction for the eastern grey squirrel (Sciurus carolinensis), a common and conspicuous forest-dwelling rodent, by obtaining 44K SNPs using reduced representation sequencing (ddRAD) for 403 individuals sampled across the species' native range in eastern North America. We observed moderate levels of genetic diversity, low levels of inbreeding, and only a modest signal of isolation-by-distance. Clustering and migration analyses show that estimated levels of migration and genetic connectivity were higher than expected across cities and forested areas, specifically within the eastern portion of the species' range dominated by urbanization, and genetic connectivity was less than expected within the western range where the landscape is fragmented by agriculture. Landscape genetic methods revealed greater gene flow among individual squirrels in forested regions, which likely provide abundant food and shelter for squirrels. Although gene flow appears to be higher in areas with more tree cover, only slight discontinuities in gene flow suggest eastern grey squirrels have maintained connected populations across urban areas in all but the most heavily fragmented agricultural landscapes. Our results suggest urbanization shapes biological evolution in wildlife species depending strongly on the composition and habitability of the landscape matrix surrounding urban areas.

Pilfering personalities: Effects of small mammal personality on cache pilferage.

Small mammals such as mice and voles play a fundamental role in the ecosystem service of seed dispersal by caching seeds in small hoards that germinate under beneficial conditions. Pilferage is a critical step in this process in which animals steal seeds from other individuals' caches. Pilferers often recache stolen seeds, which are often pilfered by new individuals, who may recache again, and so on, potentially leading to compounded increased dispersal distance. However, little research has investigated intraspecific differences in pilfering frequency, despite its importance in better understanding the role of behavioural diversity in the valuable ecosystem service of seed dispersal. We conducted a field experiment in Maine (USA) investigating how intraspecific variation, including personality, influences pilferage effectiveness. Within the context of a long-term capture-mark-recapture study, we measured the unique personality of 3311 individual small mammals of 10 species over a 7-year period. For this experiment, we created artificial caches using eastern white pine (Pinus strobus) seeds monitored with trail cameras and buried antennas for individual identification. Of the 436 caches created, 83.5% were pilfered by 10 species, including deer mice ((Peromyscus maniculatus) and southern red-backed voles (Myodes gapperi). We show how individuals differ in their ability to pilfer seeds and that these differences are driven by personality, body condition and sex. More exploratory deer mice and those with lower body condition were more likely to locate a cache, and female southern red-backed voles were more likely than males to locate caches. Also, caches were more likely to be pilfered in areas of higher small mammal abundance. Because the risk of pilferage drives decisions concerning where an animal chooses to store seeds, pilferage pressure is thought to drive the evolution of food-hoarding behaviour. Our study shows that pilferage ability varies between individuals, meaning that some individuals have a disproportionately strong influence on others' caching decisions and disproportionately contribute to compounded longer-distance seed dispersal facilitated by pilferage. Our results add to a growing body of knowledge showing that the unique personalities of individual small mammals play a critical role in forest regeneration by impacting seed dispersal.

Environmental heterogeneity modifies the link between personality and survival in fluctuating small mammal populations.

Despite numerous studies examining the fitness consequences of animal personalities, predictions concerning the relationship between personality and survival are not consistent with empirical observations. Theory predicts that individuals who are risky (i.e. bold, active and aggressive) should have higher rates of mortality; however, empirical evidence shows high levels of variation in behaviour-survival relationships in wild populations. We suggest that this mismatch between predictions under theory and empirical observations results from environmental contingencies that drive heterogeneity in selection. This uncertainty may constrain any universal directional relationships between personality traits and survival. Specifically, we hypothesize that spatiotemporal fluctuations in perceived risk that arise from variability in refuge abundance and competitor density alter the relationship between personality traits and survival. In a large-scale manipulative experiment, we trapped four small mammal species in five subsequent years across six forest stands treated with different management practices in Maine, United States. Stands all occur within the same experimental forest but contain varying amounts of refuge and small mammal densities fluctuate over time and space. We quantified the effects of habitat structure and competitor density on the relationship between personality traits and survival to assess whether directional relationships differed depending on environmental contingencies. In the two most abundant species, deer mice and southern red-backed voles, risky behaviours (i.e. higher aggression and boldness) predicted apparent monthly survival probability. Mice that were more aggressive (less docile) had higher survival. Voles that were bolder (less timid) had higher survival, but in the risky forest stands only. Additionally, traits associated with stress coping and de-arousal increased survival probability in both species at high small mammal density but decreased survival at low density. In the two less abundant study species, there was no evidence for an effect of personality traits on survival. Our field experiment provides partial support for our hypothesis: that spatiotemporal fluctuations in refuge abundance and competitor density alter the relationship between personality traits and survival. Our findings also suggest that behaviours associated with stress coping and de-arousal may be subject to density-dependent selection and should be further assessed and incorporated into theory.

Land-use change alters associations between personality and microhabitat selection.

Ecologists commonly assess ecological patterns at the population level, focusing on the average response of all individuals within a population, but to predict how populations will respond to land-use change we must understand how changes to habitat differentially affect individuals within a population. For example, forest management is a widespread type of land-use that impacts wildlife through the loss of key habitat features, but individuals within a population may vary in their responses to this loss due to differences in habitat selection among individuals. Specifically, intraspecific variation in habitat selection has been linked to animal personalities (i.e., consistent behavioral differences among conspecifics), but previous research has not examined whether the relationship between personality and habitat selection is influenced by land-use change. To address this knowledge gap, we tested the hypothesis that land-use change alters the association between personality and microhabitat selection in small mammals. Specifically, we investigated two main questions: (1) To what extent are personality type and microhabitat selection correlated among conspecifics? (2) Does land-use change alter individual patterns of microhabitat selection? To answer these questions, we conducted a large-scale field experiment over 4 years, contrasting unmanaged forest (control) with managed forest (two silvicultural treatments) in Maine, USA. We examined the relationships between habitat selection and personality traits in deer mice (Peromyscus maniculatus) and southern red-backed voles (Myodes gapperi). We found that personality traits were correlated with microhabitat selection at multiple spatial scales. Furthermore, land-use change altered these patterns of selection; resulting in either the loss of personality-associated selection or in novel patterns of selection in managed forests. These findings suggest that promoting structural complexity at multiple spatial scales, such as by interspersing stands of mature forest with managed stands, may maintain a variety of intraspecific habitat selection patterns and the associated ecological outcomes.

Environmental heterogeneity and population density affect the functional diversity of personality traits in small mammal populations.

Understanding factors affecting the functional diversity of ecological communities is an important goal for ecologists and conservationists. Previous work has largely been conducted at the community level; however, recent studies have highlighted the critical importance of considering intraspecific functional diversity (i.e. the functional diversity of phenotypic traits among conspecifics). Further, a major limitation of existing literature on this topic is the lack of empirical studies examining functional diversity of behavioural phenotypes-including animal personalities. This is a major shortcoming because personality traits can affect the fitness of individuals, and the composition of personalities in a population can have important ecological consequences. Our study aims to contribute to filling this knowledge gap by investigating factors affecting the functional diversity of personality traits in wild animal populations. Specifically, we predicted that the richness, divergence and evenness associated with personality traits would be impacted by key components of forest structure and would vary between contrasting forest types. To achieve our objective we conducted a fully replicated large-scale field experiment over a 4 year period using small mammal populations as a model system. We found that greater heterogeneity in the cover of shrubs, coarse woody debris and canopy cover was associated with a greater richness, lower divergence and lower evenness in personality traits. Greater population density was associated with greater functional richness and lower functional divergence and evenness of personality traits. To maintain a behaviourally diverse population and its associated functions, managers may promote heterogeneity in vegetation and increased population density, which we found to be the most important determinants driving functional diversity of personality traits.

Land-use change and the ecological consequences of personality in small mammals.

Many plants rely on animals for seed dispersal, but are all individuals equally effective at dispersing seeds? If not, then the loss of certain individual dispersers from populations could have cascade effects on ecosystems. Despite the importance of seed dispersal for forest ecosystems, variation among individual dispersers and whether land-use change interferes with this process remains untested. Through a large-scale field experiment conducted on small mammal seed dispersers, we show that an individual's personality affects its choice of seeds, as well as how distant and where seeds are cached. We also show that anthropogenic habitat modifications shift the distribution of personalities within a population, by increasing the proportion of bold, active, and anxious individuals and in-turn affecting the potential survival and dispersal of seeds. We demonstrate that preserving diverse personality types within a population is critical for maintaining the key ecosystem function of seed dispersal.

Effects of past and present livestock grazing on herpetofauna in a landscape-scale experiment.

Livestock grazing is the most widespread land use on Earth and can have negative effects on biodiversity. Yet, many of the mechanisms by which grazing leads to changes in biodiversity remain unresolved. One reason is that conventional grazing studies often target broad treatments rather than specific parameters of grazing (e.g., intensity, duration, and frequency) or fail to account for historical grazing effects. We conducted a landscape-scale replicated grazing experiment (15,000 km2 , 97 sites) to examine the impact of past grazing management and current grazing regimes (intensity, duration, and frequency) on a community of ground-dwelling herpetofauna (39 species). We analyzed community variables (species richness and composition) for all species and built multiseason patch-occupancy models to predict local colonization and extinction for the 7 most abundant species. Past grazing practices did not influence community richness but did affect community composition and patch colonization and extinction for 4 of 7 species. Present grazing parameters did not influence community richness or composition, but 6 of the 7 target species were affected by at least one grazing parameter. Grazing frequency had the most consistent influence, positively affecting 3 of 7 species (increased colonization or decreased extinction). Past grazing practice affected community composition and population dynamics in some species in different ways, which suggests that conservation planners should examine the different grazing histories of an area. Species responded differently to specific current grazing practices; thus, incentive programs that apply a diversity of approaches rather than focusing on a change such as reduced grazing intensity should be considered. Based on our findings, we suggest that determining fine-scale grazing attributes is essential for advancing grazing as a conservation strategy.

Using empirical models of species colonization under multiple threatening processes to identify complementary threat-mitigation strategies.

Approaches to prioritize conservation actions are gaining popularity. However, limited empirical evidence exists on which species might benefit most from threat mitigation and on what combination of threats, if mitigated simultaneously, would result in the best outcomes for biodiversity. We devised a way to prioritize threat mitigation at a regional scale with empirical evidence based on predicted changes to population dynamics-information that is lacking in most threat-management prioritization frameworks that rely on expert elicitation. We used dynamic occupancy models to investigate the effects of multiple threats (tree cover, grazing, and presence of an hyperaggressive competitor, the Noisy Miner (Manorina melanocephala) on bird-population dynamics in an endangered woodland community in southeastern Australia. The 3 threatening processes had different effects on different species. We used predicted patch-colonization probabilities to estimate the benefit to each species of removing one or more threats. We then determined the complementary set of threat-mitigation strategies that maximized colonization of all species while ensuring that redundant actions with little benefit were avoided. The single action that resulted in the highest colonization was increasing tree cover, which increased patch colonization by 5% and 11% on average across all species and for declining species, respectively. Combining Noisy Miner control with increasing tree cover increased species colonization by 10% and 19% on average for all species and for declining species respectively, and was a higher priority than changing grazing regimes. Guidance for prioritizing threat mitigation is critical in the face of cumulative threatening processes. By incorporating population dynamics in prioritization of threat management, our approach helps ensure funding is not wasted on ineffective management programs that target the wrong threats or species.

Effects of landscape transformation on bird colonization and extinction patterns in a large-scale, long-term natural experiment.

Conversion of agricultural land to forest plantations is a major driver of global change. Studies on the impact of forest plantations on biodiversity in plantations and in the surrounding native vegetation have been inconclusive. Consequently, it is not known how to best manage the extensive areas of the planet currently covered by plantations. We used a novel, long-term (16 years) and large-scale (30,000 ha) landscape transformation natural experiment (the Nanangroe experiment, Australia) to test the effects of land conversion on population dynamics of 64 bird species associated with woodland and forest. A unique aspect of our study is that we focused on the effects of plantations on birds in habitat patches within plantations. Our study design included 56 treatment sites (Eucalyptus patches where the surrounding matrix was converted from grazed land to pine plantations), 55 control sites (Eucalyptus patches surrounded by grazed land), and 20 matrix sites (sites within the pine plantations and grazed land). Bird populations were studied through point counts, and colonization and extinction patterns were inferred through multiple season occupancy models. Large-scale pine plantation establishment affected the colonization or extinction patterns of 89% of studied species and thus led to a comprehensive turnover in bird communities inhabiting Eucalyptus patches embedded within the maturing plantations. Smaller bodied species appeared to respond positively to plantations (i.e., colonization increased and extirpation of these species decreased in patches surrounded by plantations) because they were able to use the newly created surrounding matrix. We found that the effects of forest plantations affected the majority of the bird community, and we believe these effects could lead to the artificial selection of one group of species at the expense of another.

Guidelines for Using Movement Science to Inform Biodiversity Policy.

Substantial advances have been made in our understanding of the movement of species, including processes such as dispersal and migration. This knowledge has the potential to improve decisions about biodiversity policy and management, but it can be difficult for decision makers to readily access and integrate the growing body of movement science. This is, in part, due to a lack of synthesis of information that is sufficiently contextualized for a policy audience. Here, we identify key species movement concepts, including mechanisms, types, and moderators of movement, and review their relevance to (1) national biodiversity policies and strategies, (2) reserve planning and management, (3) threatened species protection and recovery, (4) impact and risk assessments, and (5) the prioritization of restoration actions. Based on the review, and considering recent developments in movement ecology, we provide a new framework that draws links between aspects of movement knowledge that are likely the most relevant to each biodiversity policy category. Our framework also shows that there is substantial opportunity for collaboration between researchers and government decision makers in the use of movement science to promote positive biodiversity outcomes.

The importance of animal behavior for ecosystem services.

Animal behavior plays a critical role in the delivery of ecosystem services, yet the study of animal behavior and ecosystem services rarely intersect. The study of behavior-mediated ecosystem services should be prioritized, focusing on the conditions that allow these critical behaviors to persist and adapt to global change.

Umbrella effect of monitoring protocols for mammals in the Northeast US.

Developing cost-effective monitoring protocols is a priority for wildlife conservation agencies worldwide. In particular, developing protocols that cover a wide range of species is highly desirable. Here we applied the 'umbrella species' concept to the context of ecological monitoring; specifically testing the hypothesis that protocols developed for the American marten would contextually allow detecting occupancy trends for 13 other mammalian species (i.e., an umbrella effect). We conducted a large-scale four-year camera trapping survey across a gradient of forest disturbance in Maine, USA. We sampled 197 sites using a total of 591 cameras and collected over 800,000 photographs to generate detection histories for the most common terrestrial species. By combining multi-season occupancy modelling and power analyses, we estimated the required sampling effort to detect 10%, 25% and 50% declines in the fourteen species. By conducting a spatially explicit comparison of sampling effort, we found evidence that monitoring protocols for American marten would provide an umbrella effect for up to 11 other mammal species. The capacity of the umbrella effect varied among species, with fisher, snowshoe hare, red squirrel, and black bear consistently covered under several scenarios. Our results support the application of the umbrella species concept to monitoring (here defined as 'umbrella monitoring species'), providing empirical evidence for its use by management agencies.

The role of habitat quality in fragmented landscapes: a conceptual overview and prospectus for future research.

There is increasing empirical evidence that the quality of habitat patches (determined by either habitat degradation or natural heterogeneity in the quality of habitat) plays an important role in determining species distribution patterns and in regulating spatial dynamics in fragmented landscapes. However, to date, most of the debate has focused on whether or not to include habitat variables in fragmentation studies, and we still lack general conclusions as well as standard and robust research approaches. In this paper we show how a weak conceptualization of "patch quality" and the inappropriate choice of target surrogate variables (e.g., density is often used as an indicator of patch quality) have mainly produced case-specific results, rather than general conclusions. We then identify weaknesses in the inclusion of habitat quality measurements within fragmentation studies. In particular, we focus on: (1) the lack of appropriate experimental design, outlining how few studies have actually included a gradient of habitat quality in their sample; (2) the lack of fundamental information provided (e.g., lack of standard outputs), which in turn hampers the possibility of carrying out meta-analyses. We finally synthesize available knowledge from empirical studies and highlight the different conceptual frameworks needed for patch occupancy versus patch use studies.

Correction: Effects of trap confinement on personality measurements in two terrestrial rodents.

[This corrects the article DOI: 10.1371/journal.pone.0221136.].

Effects of trap confinement on personality measurements in two terrestrial rodents.

In recent years, consistent individual differences in behavior, or personalities, have been a topic of increasing interest as researchers strive to understand and predict the responses of individuals and populations to anthropogenic changes. Behavioral studies in wild populations often require that animals are live trapped before behavioral observation can occur, and this is especially true in studies investigating animal personalities. However, it is unknown whether the amount of time confined to a live trap may regulate the behavior of trapped individuals. Specifically, if the duration of trap confinement directly influences behavior, then by obtaining wild animals through live trapping we may be confounding the very measurements of greatest interest. To investigate whether the duration of trap confinement influences the behavior of trapped individuals, we performed a study on two small mammal species, focusing specifically on personality traits. We positioned high-definition trail cameras facing Longworth small mammal traps in the field to observe capture events and record the time of capture. We then measured personality in captured deer mice (Peromyscus maniculatus) and southern red-backed voles (Myodes gapperi) using three standardized tests, and through linear and generalized linear models we found that the time an animal had spent confined to a trap before testing did not affect 86% of behaviors exhibited. Our results showed two weak behavioral effects of confinement duration on boldness and docility resulting from an interaction between the duration of confinement and whether or not an individual was naïve to trapping. Our results suggest that behavioral measurements of wild, trapped small mammals are not determined by the time spent confined to a trap. However, researchers should use caution and consider whether an animal is naïve to trapping during analysis since habituation to the live trap may play a role in the effects of confinement duration on behavior.

Assessing arrays of multiple trail cameras to detect North American mammals.

Motion triggered camera traps are an increasingly popular tool for wildlife research and can be used to survey for multiple species simultaneously. As with all survey techniques, it is crucial to conduct camera trapping research following study designs that include adequate spatial and temporal replication, and sufficient probability of detecting species presence. The use and configuration of multiple camera traps within a single survey site are understudied considerations that could have a substantial impact on detection probability. Our objective was to test the role that camera number (one, two or three units), and spacing along a linear transect (100 m or 150 m), have on the probability of detecting a species given it is present. From January to March, 2017 we collected data on six mammal species in Maine, USA: coyote (Canis latrans), fisher (Pekania pennanti), American marten (Martes americana), short-tailed weasel (Mustela erminea), snowshoe hare (Lepus americanus), and American red squirrel (Tamiasciurus hudsonicus). We used multi-scale occupancy modelling to compare pooled detection histories of different configuration of five cameras deployed at the same survey site (n = 32), and how the configuration would influence the probability of detecting a species given it was available at the site. Across all six species, we found substantial increases in probability of detection as the number of cameras increased from one to two (22 to 400 percent increase), regardless of the spacing between cameras. For most species the magnitude of the increase was less substantial when adding a third camera (4 to 85 percent increase), with coyote and snowshoe hare showing a pronounced effect. The influence of survey station features also varied by species. We suggest that using pooled data from two or three cameras at a survey site is a cost effective approach to increase detection success over a single camera.

Managing uncertainty in movement knowledge for environmental decisions.

Species' movements affect their response to environmental change but movement knowledge is often highly uncertain. We now have well-established methods to integrate movement knowledge into conservation practice but still lack a framework to deal with uncertainty in movement knowledge for environmental decisions. We provide a framework that distinguishes two dimensions of species' movement that are heavily influenced by uncertainty: knowledge about movement and relevance of movement to environmental decisions. Management decisions can be informed by their position in this knowledge-relevance space. We then outline a framework to support decisions around (1) increasing understanding of the relevance of movement knowledge, (2) increasing robustness of decisions to uncertainties and (3) improving knowledge on species' movement. Our decision-support framework provides guidance for managing movement-related uncertainty in systematic conservation planning, agri-environment schemes, habitat restoration and international biodiversity policy. It caters to different resource levels (time and funding) so that species' movement knowledge can be more effectively integrated into environmental decisions.

Fine-Scale Habitat Heterogeneity Influences Occupancy in Terrestrial Mammals in a Temperate Region of Australia.

Vegetation heterogeneity is an inherent feature of most ecosystems, characterises the structure of habitat, and is considered an important driver of species distribution patterns. However, quantifying fine-scale heterogeneity of vegetation cover can be time consuming, and therefore it is seldom measured. Here, we determine if heterogeneity is worthwhile measuring, in addition to the amount of cover, when examining species distribution patterns. Further, we investigated the effect of the surrounding landscape heterogeneity on species occupancy. We tested the effect of cover and heterogeneity of trees and shrubs, and the context of the surrounding landscape (number of habitats and distance to an ecotone) on site occupancy of three mammal species (the black wallaby [Wallabia bicolor], the long-nosed bandicoot [Perameles nasuta], and the bush rat [Rattus fuscipes]) within a naturally heterogeneous landscape in a temperate region of Australia. We found that fine-scale heterogeneity of vegetation attributes is an important driver of mammal occurrence of two of these species. Further, we found that, although all three species responded positively to vegetation heterogeneity, different mammals vary in their response to different types of vegetation heterogeneity measurement. For example, the black wallaby responded to the proximity of an ecotone, and the bush rat and the long-nosed bandicoot responded to fine-scale heterogeneity of small tree cover, whereas none of the mammals responded to broad scale heterogeneity (i.e., the number of habitat types). Our results highlight the influence of methodological decisions, such as how heterogeneity vegetation is measured, in quantifying species responses to habitat structures. The findings confirm the importance of choosing meaningful heterogeneity measures when modelling the factors influencing occupancy of the species of interest.