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A review of supervised learning methods for classifying animal behavioural states from environmental features

Accurately predicting behavioural modes of animals in response to environmental features is important for ecology and conservation. Supervised learning (SL) methods are increasingly common in animal movement ecology for classifying behavioural modes. However, few examples exist of applying SL to classify polytomous animal behaviour from environmental features especially in the context of millions of animal observations. We review SL methods (weighted k -nearest neighbours; neural nets; random forests; and boosted classification trees with XGBoost) for classifying polytomous animal behaviour from environmental predictors. We also describe tuning parameter selection and assessment strategies, approaches for visualizing relationships between predictors and class outputs, and computational considerations. We demonstrate these methods by predicting three categories of risk to bald eagles from colliding with wind turbines using, as predictors, 12 environmental state features associated with 1.7 million GPS telemetry data points from 57 eagles. Of the SL methods we considered, XGBoost yielded the most accurate model with 86.2% classification accuracy and pairwise-averaged area under the ROC curve of 90.6. Computational time of XGBoost scaled better to large data than any other SL method. We also show how SHAP values integrated in the R package ( xgboost ) facilitate investigation of variable relationships and importance. For big data applications, XGBoost appears to provide superior classification accuracy and computational efficiency. Our results suggest XGBoost should be considered as an early modelling option in situations where the intent is to classify millions of animal behaviour observations from environmental predictors and to understand relationships between those predictors and movement behaviours. We also offer a tutorial to assist researchers in implementing this method.

Methods in Ecology and Evolution

Global positioning system and associated technologies in animal behaviour and ecological research

Biologists can equip animals with global positioning system (GPS) technology to obtain accurate (less than or equal to 30 m) locations that can be combined with sensor data to study animal behaviour and ecology. We provide the background of GPS techniques that have been used to gather data for wildlife studies. We review how GPS has been integrated into functional systems with data storage, data transfer, power supplies, packaging and sensor technologies to collect temperature, activity, proximity and mortality data from terrestrial species and birds. GPS 'rapid fixing' technologies combined with sensors provide location, dive frequency and duration profiles, and underwater acoustic information for the study of marine species. We examine how these rapid fixing technologies may be applied to terrestrial and avian applications. We discuss positional data quality and the capability for high-frequency sampling associated with GPS locations. We present alternatives for storing and retrieving data by using dataloggers (biologging), radio-frequency download systems (e.g. very high frequency, spread spectrum), integration of GPS with other satellite systems (e.g. Argos, Globalstar) and potential new data recovery technologies (e.g. network nodes). GPS is one component among many rapidly evolving technologies. Therefore, we recommend that users and suppliers interact to ensure the availability of appropriate equipment to meet animal research objectives.

Philosophical Transactions of the Royal Society B:

Optimal use of resources structures home ranges and spatial distribution of black bears

Research has shown that territories of animals are economical. Home ranges should be similarly efficient with respect to spatially distributed resources and this should structure their distribution on a landscape, although neither has been demonstrated empirically. To test these hypotheses, we used home range models that optimize resource use according to resource-maximizing and area-minimizing strategies to evaluate the home ranges of female black bears, Ursus americanus, living in the southern Appalachian Mountains. We tested general predictions of our models using 104 home ranges of adult female bears studied in the Pisgah Bear Sanctuary, North Carolina, U.S.A., from 1981 to 2001. We also used our models to estimate home ranges for each real home range under a variety of strategies and constraints and compared similarity of simulated to real home ranges. We found that home ranges of female bears were efficient with respect to the spatial distribution of resources and were best explained by an area-minimizing strategy with moderate resource thresholds and low levels of resource depression. Although resource depression probably influenced the spatial distribution of home ranges on the landscape, levels of resource depression were too low to quantify accurately. Home ranges of lactating females had higher resource thresholds and were more susceptible to resource depression than those of breeding females. We conclude that home ranges of animals, like territories, are economical with respect to resources, and that resource depression may be the mechanism behind ideal free or ideal preemptive distributions on complex, heterogeneous landscapes. ?? 2007 The Association for the Study of Animal Behaviour.

Animal Behaviour

Latitudinal variation in avian incubation attentiveness and a test of the food limitation hypothesis

Avian incubation attentiveness has important fitness consequences through its influence on the number and quality of hatched young and energetic costs imposed on parents. Nest attentiveness is highly variable across species and geographical regions. We reviewed the literature and found a worldwide pattern that nest attentiveness of passerines is generally lower in south temperate and tropical regions than in north temperate regions. We also conducted a food manipulation experiment to assess the extent to which nest attentiveness may reflect proximate responses versus an evolved behaviour. We used the karoo prinia, Prinia maculosa, in South Africa, which has very low nest attentiveness (???49%) compared with that of many passerine birds. We provided supplemental food during early incubation to experimental females and compared nest attentiveness and on- and off-bout lengths of experimental and paired control females.??Nest attentiveness of females at food-provisioned nests was significantly higher than that of control females (57% versus 49%). Food-supplemented females also spent significantly less time off the nest than did control females, whereas mean on-bout lengths did not differ. However, mean nest attentiveness of food-provisioned females was still substantially below that of other similar bird species worldwide. Food can be an important proximate influence on parental care behaviour, but proximate influences of food do not explain broad latitudinal patterns of attentiveness. ?? 2007 The Association for the Study of Animal Behaviour.

Animal Behaviour

Cooperation and competition: nepotistic tolerance and intrasexual aggression in western bluebird winter groups

Two hypothesized benefits of delayed dispersal are access to resources and prolonged brood care (or??parental nepotism). Resource abundance (mistletoe wealth) is a key factor influencing whether sons stay home in western bluebirds, Sialia mexicana, but nepotism is also observed. Western bluebird sons commonly remain in their family groups throughout the winter, whereas daughters usually disperse before winter. Because pairing often takes place in winter groups, with newly formed pairs settling on exclusive all-purpose territories in spring, selection for sexual competition and nepotism co-occur and may simultaneously influence patterns of aggression within groups. We measured aggression at mealworm feeder stations, finding evidence of (1) intrasexual aggression against unrelated group members by experienced breeders of both sexes and (2) nepotism towards sons and daughters by experienced breeder females but not by experienced breeder males. Females showed much higher levels of aggression towards same-sex immigrants than males did. Experienced breeder males did not evict their sons from the natal territory, but they were 12 times more aggressive towards sons than breeder females were towards daughters. They were also equally aggressive towards sons and immigrant males, suggesting that local breeding competition and the benefits of intrasexual dominance counter the benefits of paternal nepotism towards sons. ?? 2009 The Association for the Study of Animal Behaviour.

Animal Behaviour

Impacts of experimentally increased foraging effort on the family: offspring sex matters

We examined how short-term impacts of experimentally increased foraging effort by one parent reverberate around the family in a monomorphic seabird (little auk, Alle alle), and whether these effects depend on offspring sex. In many species, more effort is required to rear sons successfully than daughters. However, undernourishment may have stronger adverse consequences for male offspring, which could result in a lower fitness benefit of additional parental effort when rearing a son. We tested two alternative hypotheses concerning the responses of partners to handicapping parents via feather clipping: partners rearing a son are (1) more willing or able to compensate for the reduced contribution of their mate, or (2) less willing or able to compensate, compared to those rearing a daughter. Hypothesis 1 predicts that sons will be no more adversely affected than daughters, and the impact on parents will be greater when rearing a son. Hypothesis 2 predicts that sons will be more adversely affected than daughters, and parents raising a son less affected. Although experimental chicks of both sexes fledged in poorer condition than controls, sons attained higher mass and more rapid growth than daughters in both groups. Clipped parents lost a similar proportion of their initial mass regardless of chick sex, whereas partners of clipped birds lost more mass when rearing a son. These results support hypothesis 1: impacts of increased foraging effort by one parent were felt by offspring, regardless of their sex, and by the partners of manipulated birds, particularly when the offspring was male. ?? 2009 The Association for the Study of Animal Behaviour.

Animal Behaviour

State‐space modelling of the flight behaviour of a soaring bird provides new insights to migratory strategies

Characterising the spatiotemporal variation of animal behaviour can elucidate the way individuals interact with their environment and allocate energy. Increasing sophistication of tracking technologies paired with novel analytical approaches allows the characterisation of movement dynamics even when an individual is not directly observable. In this study, high‐resolution movement data collected via global positioning system (GPS) tracking in three dimensions were paired with topographical information and used in a Bayesian state‐space model to describe the flight modes of migrating golden eagles ( Aquila chrysaetos ) in eastern North America. Our model identified five functional behavioural states, two of which were previously undescribed variations on thermal soaring. The other states comprised gliding, perching and orographic soaring. States were discriminated by movement features in the horizontal (step length and turning angle) and vertical (change in altitude) planes and by the association with ridgelines promoting wind deflection. Tracked eagles spent 2%, 31%, 38%, 9% and 20% of their daytime in directed thermal soaring, gliding, convoluted thermal soaring, perching and orographic soaring, respectively. The analysis of the relative occurrence of these flight modes highlighted yearly, seasonal, age, individual and sex differences in flight strategy and performance. Particularly, less energy‐efficient orographic soaring was more frequent in autumn, when thermals were less available. Adult birds were also better at optimising energy efficiency than subadults. Our approach represents the first example of a state‐space model for bird flight mode using altitude data in conjunction with horizontal locations and is applicable to other flying organisms where similar data are available. The ability to describe animal movements in a three‐dimensional habitat is critical to advance our understanding of the functional processes driving animals’ decisions.

Functional Ecology

Nest predation research: Recent findings and future perspectives

Nest predation is a key source of selection for birds that has attracted increasing attention from ornithologists. The inclusion of new concepts applicable to nest predation that stem from social information, eavesdropping or physiology has expanded our knowledge considerably. Recent methodological advancements now allow focus on all three players within nest predation interactions: adults, offspring and predators. Indeed, the study of nest predation now forms a vital part of avian research in several fields, including animal behaviour, population ecology, evolution and conservation biology. However, within nest predation research there are important aspects that require further development, such as the comparison between ecological and evolutionary antipredator responses, and the role of anthropogenic change. We hope this review of recent findings and the presentation of new research avenues will encourage researchers to study this important and interesting selective pressure, and ultimately will help us to better understand the biology of birds.

Journal of Ornithology

Climate change as a global amplifier of human–wildlife conflict

Climate change and human–wildlife conflict are both pressing challenges for biodiversity conservation and human well-being in the Anthropocene. Climate change is a critical yet underappreciated amplifier of human–wildlife conflict, as it exacerbates resource scarcity, alters human and animal behaviours and distributions, and increases human–wildlife encounters. We synthesize evidence of climate-driven conflicts occurring among ten taxonomic orders, on six continents and in all five oceans. Such conflicts disrupt both subsistence livelihoods and industrial economies and may accelerate the rate at which human–wildlife conflict drives wildlife declines. We introduce a framework describing distinct environmental, ecological and sociopolitical pathways through which climate variability and change percolate via complex social–ecological systems to influence patterns and outcomes of human–wildlife interactions. Identifying these pathways allows for developing mitigation strategies and proactive policies to limit the impacts of human–wildlife conflict on biodiversity conservation and human well-being in a changing climate.

Nature Climate Change

Fractal structure of sequential behaviour patterns: an indicator of stress

The detection of stress arising from parasitic infection by Sarcoptes scabieis and from pregnancy is explored, using a fractal analysis of head lifting behaviour and feeding–non-feeding activity sequences in female Spanish ibex, Capra pyrenaica , under natural conditions. Because organisms under stress increase their metabolic rate and, in consequence, energy consumption, it follows that stress will, generally, lead to a reduction in complexity (fractal dimension) of exploratory behaviour. In the present study the fractal dimension of the three measures of complexity used declined with stress, both from pregnancy and from parasitic infection. This observation provides a new and effective way to assess the general state of animals’ health in the field, without the need for capture and handling.

Animal Behaviour

Offspring growth in the California gull: Reproductive effort and parental experience hypotheses

Measures of adult feeding and foraging behaviour in the California gull, Larus californicus , were related to the growth of their offspring. Offspring showed significantly higher growth when average feeding interval, a measure of the time interval between feedings, and feeding latency following foraging decreased. The amount of time parents foraged was positively related to offspring growth and negatively correlated with average feeding interval. Either (1) increased foraging efficiency with parental age, or (2) increased reproductive effort with age, could explain age-related differences in patterns of feeding behaviour and their impact on offspring growth. However, data on foraging time support only the hypothesis of increased reproductive effort with parental age.

Wyoming

Hemispheric-scale wind selection facilitates bar-tailed godwit circum-migration of the Pacific

The annual 29 000 km long migration of the bar-tailed godwit, Limosa lapponica baueri, around the Pacific Ocean traverses what is arguably the most complex and seasonally structured atmospheric setting on Earth. Faced with marked variation in wind regimes and storm conditions across oceanic migration corridors, individuals must make critical decisions about when and where to fly during nonstop flights of a week's duration or longer. At a minimum, their decisions will affect wind profitability and thus reduce energetic costs of migration; in the extreme, poor decisions or unpredictable weather events will risk survival. We used satellite telemetry to track the annual migration of 24 bar-tailed godwits and analysed their flight performance relative to wind conditions during three major migration legs between nonbreeding grounds in New Zealand and breeding grounds in Alaska. Because flight altitudes of birds en route were unknown, we modelled flight efficiency at six geopotential heights across each migratory segment. Birds selected departure dates when atmospheric conditions conferred the greatest wind assistance both at departure and throughout their flights. This behaviour suggests that there exists a cognitive mechanism, heretofore unknown among migratory birds, that allows godwits to assess changes in weather conditions that are linked (i.e. teleconnected) across widely separated atmospheric regions. Godwits also showed adaptive flexibility in their response not only to cues related to seasonal changes in macrometeorology, such as spatial shifting of storm tracks and temporal periods of cyclogenesis, but also to cues associated with stochastic events, especially at departure sites. Godwits showed limits to their response behaviours, however, especially relative to rapidly developing stochastic events while en route. We found that flight efficiency depended significantly upon altitude and hypothesize that godwits exhibit further adaptive flexibility by varying flight altitude en route to optimize flight efficiency.

Animal Behaviour

Use of mammal manure by nesting burrowing owls: a test of four functional hypotheses

Animals have evolved an impressive array of behavioural traits to avoid depredation. Olfactory camouflage of conspicuous odours is a strategy to avoid depredation that has been implicated only in a few species of birds. Burrowing owls, Athene cunicularia, routinely collect dried manure from mammals and scatter it in their nest chamber, in the tunnel leading to their nest and at the entrance to their nesting burrow. This unusual behaviour was thought to reduce nest depredation by concealing the scent of adults and juveniles, but a recent study suggests that manure functions to attract arthropod prey. However, burrowing owls routinely scatter other materials in the same way that they scatter manure, and this fact seems to be at odds with both of these hypotheses. Thus, we examined the function of this behaviour by testing four alternative hypotheses. We found no support for the widely cited olfactory-camouflage hypothesis (manure did not lower the probability of depredation), or for the mate-attraction hypothesis (males collected manure after, not before, pair formation). Predictions of the burrow-occupied hypothesis (manure indicates occupancy to conspecifics and thereby reduces agonistic interactions) were supported, but results were not statistically significant. Our results also supported several predictions of the prey-attraction hypothesis. Pitfall traps at sampling sites with manure collected more arthropod biomass (of taxa common in the diet of burrowing owls) than pitfall traps at sampling sites without manure. Scattering behaviour of burrowing owls appears to function to attract arthropod prey, but may also signal occupancy of a burrow to conspecifics. ?? 2006 The Association for the Study of Animal Behaviour.

Animal Behaviour

Changes in vocal repertoire of the Hawaiian crow, Corvus hawaiiensis,from past wild to current captive populations

For most avian species, social behaviou r is critically important for survival and reproductive success. Many social behaviours in birds are culturally transmitted, and as bird populations decline across the globe, important elements of these behaviours may be lost. The Hawaiian crow or 'alalā, Corvus hawaiiensis , is a socially complex avian species that is currently extinct in the wild. As in other oscine passerines, vocalizations in the 'alalā may be culturally transmitted. We compared the vocal repertoire of three of the last four wild 'alalā pairs from the early 1990s to three current captive pairs on the Island of Hawai'i to determine how acoustic behaviour has been affected by changes in their social and physical environment. Over 18 h of recordings from wild breeding pairs were analysed and compared with 44 h from captive breeding pairs. Calls were placed into five putative behavioural categories: (1) alarm, (2) territorial broadcast, (3) aggression, (4) submission and (5) courtship. There was little difference in the overall number and diversity of call types among wild versus captive birds. However, the repertoire was significantly different. Territorial broadcast calls, common components of the wild repertoire, were absent from the captive repertoire. In addition, wild birds had twice the number of alarm calls and had a higher call rate than captive birds. Our results show how socially learned behaviours may change over relatively short periods for an entire species. Understanding how the vocal repertoire and the functional context of vocalizations change may provide useful information for ongoing efforts to reintroduce the 'alalā into the wild.

Hawai'i

Black-tailed prairie dog, Cynomys ludovicianus (Sciuridae), metapopulation response to novel sourced conspecific signals

Aggregation of territorial individuals within a species can be facilitated via conspecific signals, wherein settlement implies habitat suitability, ease of resource acquisition and/or increased predator detection. The black-tailed prairie dog is a colonial small mammal with alarm vocalizations that confer benefits via group vigilance against predators and increased foraging time. Although prairie dog alarm calls are relatively well understood, the information embedded in their jump-yip call, which includes both a distinct cry and a bodily gesture, remains less clear. We evaluated prairie dog behaviour in response to conspecific acoustic signals using playbacks of alarm and jump-yip calls at 26 sites in northeastern Wyoming, U.S.A. Recorded calls from an isolated colony were broadcast to a mean of five individuals per site, and behavioural responses were compared against uninfluenced behaviour and a control playback of ambient sounds. The alarm playback caused prairie dogs to increase vigilance 122% and decrease foraging time 23%, demonstrating prairie dogs will shift behaviour based on signals from individuals of an unfamiliar colony. However, the alarm call playback reduced frequency of the jump-yip behaviour only at colonies nearest the recording source. The jump-yip playback caused unfamiliar prairie dogs to display 339% more jump-yips than uninfluenced behaviour. The jump-yip playback did not alter recipients' foraging or vigilance behaviours relative to control treatments, suggesting that although prairie dogs can understand and reciprocate an unfamiliar, single modality signal, they may not shift other behaviours based on this stimulus. As such, the purpose and benefits of the jump-yip call remain unclear. Playback efficacy also had a nonlinear relationship with distance from recording source. Our work improves understanding of communication at the metapopulation level, examines the potential role of the jump-yip and provides insights for how conspecific signals might be used as a management tool.

Wyoming

[Book review] Cowbirds and Other Brood Parasites by Catherine Ortega. Tucson, Arizona: University of Arizona Press (1998). The Avian Brood Parasites: Deception at the Nest by Paul A. Johnsgard. New York: Oxford University Press (1997) Parasitic Birds and their Hosts: Studies in Coevolution edited by S.I. Rothstein & S.K. Robinson. New York: Oxford University Press (1998)

We are in a golden age for the study of brood parasitism, judging from both the quantity and quality of recent scientific publications on cuckoos, cowbirds and parasitic finches by investigators working in Europe, the Americas, Africa and Asia. As Johnsgard (1997) remarks in his preface, the evolutionary, ecological, and behavioural questions posed by obligate brood parasites are among the most intriguing contemporary ornithological topics. Rothstein & Robinson (1998) explain that brood parasites make ideal subjects for testing the generality of models for the evolution of social and mating behaviour, foraging behaviour, spatial distribution, and vocal development, because the strategy of providing no parental care removes constraints imposed on other birds. Since Aristotle, people have been fascinated by brood parasites, but only in the past two decades has the number of investigators working on this topic reached a critical mass and created momentum that promises many breakthroughs. New studies are being completed so rapidly that a general book is inevitably out of date on some topics by the time it is published. A complete library on brood parasitism should add two recent volumes (Morrison et al. 1999; Smith et al., in press).to the three reviewed here.

Animal Behaviour

Sustained increase in food supplies reduces broodmate aggression in black-legged kittiwakes

The amount of food ingested by chicks has often been suggested as being the main proximate factor controlling broodmate aggression in facultatively siblicidal species. Although several experiments have demonstrated that short-term food deprivation causes a temporary increase in aggression, no study has, to our knowledge, experimentally manipulated overall food supplies and considered long-term effects on chick behaviour and life history traits. We provided supplemental food to breeding pairs of black-legged kittiwakes, Rissa tridactyla , over an entire breeding season and compared the aggressive behaviour of their chicks with that of chicks of control pairs. Control A-chicks (first to hatch) showed more frequent and intense aggression than their experimental counterparts. Furthermore, the more A-chicks begged and the lower their growth rate the more aggressive they were. The consequences of increased aggression for B-chicks (second to hatch) were lower begging rate, lower growth rate and lower survival. We thus provide evidence that a sustained increase in food availability affects broodmate aggression and chick survival at the nest and we discuss the various proximate and ultimate causes involved in the evolution of broodmate aggression.

Alaska

Phenotypic divergence of secondary sexual traits among sage grouse, Centrocercus urophasianus , populations

S age grouse, Centrocercus urophasianus , in an isolated montane basin near Gunnison, Colorado differ in several morphological and behavioural traits from conspecifics studied in other areas of the species' range. Both sexes in Gunnison are smaller than sage grouse elsewhere, and males possess differences in feather morphology as well. The mating behaviour of male sage grouse in three populations was examined to determine whether male strut displays of Gunnison sage grouse were behaviourally distinct. Behavioural analyses revealed Gunnison males perform strut displays at a slower rate than males in the two other sage grouse populations sampled. In addition, Gunnison males' strut displays contain unique visual and acoustical aspects. The most distinguishing attributes of Gunnison sage grouse were male secondary sexual characteristics including traits that correlate with mating success in other populations. Thus, phenotypic differences observed in the Gunnison population represent a divergence in expression of traits that are likely to be influenced by sexual selection. Recent models of speciation suggest that species characterized by intense sexual selection, such as those with lek mating systems, have the potential for rapid inter-populational divergence in male traits and female preferences leading to speciation.

Colorado