Determinants of uncertainty in wildlife responses to human disturbance

Outdoor recreation is increasing in intensity and space. Areas previously inaccessible are now being visited by ever‐growing numbers of people, which increases human–wildlife encounters across habitats. This has raised concern among researchers and conservationists as, even in non‐aggressive encounters, animals often perceive humans as predators and mount physiological and behavioural responses that can have negative consequences. However, despite all the research in recent decades, not many general patterns have emerged, especially at the level of populations, and many studies have yielded seemingly contradictory or inconclusive results. We argue that this is partly due to incomplete knowledge of the number and complexity of factors that may modulate the responses of animals. Thus, we aim to provide a conceptual approach intended to highlight the reasons that make it difficult to detect general patterns. We present a comprehensive compilation of factors modulating animal responses to humans at increasing levels (from sensory detection and immediate behavioural and physiological reactions, to changes in fitness and population trends), which may help understanding the uncertainty in the patterns. We observed that there are many modulating factors, which can be categorized as reflecting characteristics of the recreational activity itself (e.g. intensity of human presence), of the animals concerned (e.g. age or antipredatory strategy), and of the spatio‐temporal context (e.g. habitat or timing of the encounter). Some factors appear to have non‐linear and complex effects, which, if not considered, may lead to erroneous conclusions. Finally, we conclude that the difficulty in finding general patterns will be amplified at higher levels (i.e. at the level of populations), since as we proceed from one level to the next, the number of potential modulating factors accumulates, adding noise and obscuring direct associations between recreation and wildlife. More comprehensive knowledge about which (and how) factors affect animal responses across levels will certainly improve future research design and interpretation, and thus, our understanding of human recreational impacts on wildlife.     

Managing human disturbance: factors influencing flight-initiation distance of birds in a West African nature reserve

Escape behaviour in response to perceived predators can be employed as a guide when designating protected areas around sensitive bird species to minimise the impact of human disturbance. A key measure of escape response is flight-initiation distance (FID), the distance at which a prey animal initiates its escape when approached by a potential predator. We tested the predictions of optimal escape theory by determining the factors that influence FID of bird species in a Nigerian reserved area and its surrounding habitats, and so the potential utility of FID in managing human disturbance on birds, for the first time within a West African context. We tested how FID varied with group size, proximity to vegetation acting as protective cover, levels of human use, and survival rate, and whether these relationships varied by species. We collected 504 FIDs for seven bird species in Amurum Forest Reserve and its surrounding habitats (Jos, Nigeria). The FID was lower in larger groups and when species were closer to protective cover. The FID was lower outside of the protected area because animals in sites with higher levels of human presence and use may become habituated. The FID was higher for species with higher survival, being consistent with predictions from life history theory. Overall, birds perceived humans as a potential threat and responded in accordance to the predictions of optimal escape theory, with FID increasing with increased cost of staying. Reserve managers in Africa could use species- and context-specific FIDs to designate buffer distances for the protection of wildlife from human disturbance.     

Using flight initiation distance to evaluate responses of colonial‐nesting Great Egrets to the approach of an unmanned aerial vehicle

Remote‐controlled, unmanned aerial vehicles (UAVs) can be used to collect information in difficult‐to‐access places while potentially minimizing human disturbance. These devices have been widely used in a variety of ecological and behavioral studies in recent years, but additional study is needed to assess the magnitude of disturbance they cause to birds. We examined the responses of Great Egrets (Ardea alba) to a UAV in a breeding colony in Louisiana in 2016 where isolated patches of common reed (Phragmites australis) were used as nest sites by multiple breeding pairs. We examined the flush responses and flight initiation distances (FIDs) of nesting adults to the direct vertical approach of a UAV. Incubating adults were more likely to flush from nests and flushed at greater distances when approached by a UAV than adults with nestlings, suggesting that adult assessment of risk was based on the greater reproductive value of nestlings. We observed fewer flush responses and calculated lower set‐back distances using a UAV to approach nesting Great Egrets (~50 m) than set‐back distances calculated using traditional methods of approach (e.g., walking or boating; 87–251 m). We found that FIDs were shorter when more adults were present in nesting patches, suggesting that the perception of predation risk may be based in part on the reactions of other birds. Our results suggest that UAVs may be a useful alternative for monitoring colonial‐nesting waterbirds. However, our analyses were based exclusively on behavioral observations. Additional studies of the physiological responses of birds to the approach of UAVs are needed to better understand the stress responses of birds to these devices.     

Importance of juniper to birds nesting in piñon–juniper woodlands in northwest New Mexico

Piñon–juniper (Pinus spp.–Juniperus spp.) woodlands are common throughout western North America, yet relatively little is known about the habitat use and requirements for many members of its avian community. During summer 2005–2007, we assessed avian nesting substrates within piñon (Pinus edulis)–juniper (Juniperus osteosperma) woodlands in northwestern New Mexico. Of all nests in live trees, 86% were in junipers. The selection of juniper as a nest tree was significantly higher than expected from the region's piñon–juniper ratio (1:1.06) for the community as a whole, for both open cup and cavity nesting species, and for 8 species (of which 6 are piñon–juniper obligate or semi-obligate species). Nest survival, however, was not higher in juniper than in piñon for the nesting community as a whole or for chipping sparrows (Spizella passerina), the single species that was well represented nesting in piñon. The high use of juniper as a nesting substrate differs from previous studies, which have suggested that a presence of piñon is among the most important habitat features for many piñon–juniper species. Because of their importance to nesting birds, managers should avoid preferential thinning of junipers within piñon–juniper woodlands. © 2011 The Wildlife Society.     

Evaluation of multiple behavioral responses of sika deer to human hunting pressures

Several ungulate populations have become overabundant worldwide, resulting in ecological and social effects. Wildlife managers must establish effective population control programs to mitigate these negative influences. Hunting is a significant mortality factor for ungulates, which exhibit sensitive behavioral responses toward hunting activities. Wildlife managers need a comprehensive understanding of the ungulate responses to different hunting pressures across seasons. We developed a conceptual method to evaluate multiple behavioral responses to human hunting pressures and applied this to sika deer (Cervus nippon) in Hokkaido, Japan, during August and November in 2015. We measured flight behavior, spatial avoidance, and temporal activity shift during non-hunting and hunting seasons in 4 regions with different hunting pressures. Although we did not observe a clear difference in flight initiation distance among study areas or seasons, sika deer showed significant spatial avoidance during the hunting season in areas with high hunting pressure. Furthermore, sika deer were more active at night in areas with higher hunting pressures, regardless of the season. Collectively, these results suggest that sika deer responded to hunting pressure by changing diel activity to nocturnal throughout the year and avoiding risky areas (i.e., around hunting roads) during hunting season, rather than by increasing flight distance when they encounter humans. Our method can be used for a more efficient population control program for wildlife managers, as it considers the spatiotemporal variations of flexible ungulate behaviors in response to hunting pressures.     

Provision of supplementary food for wild birds may increase the risk of local nest predation

In countries such as the UK, USA and Australia, approximately half of all households provide supplementary food for wild birds, making this the public's most common form of active engagement with nature. Year‐round supplementary feeding is currently encouraged by major conservation charities in the UK as it is thought to be of benefit to bird conservation. However, little is understood about how the provision of supplementary food affects the behaviour and ecology of target and non‐target species. Given the scale of supplementary feeding, any negative effects may have important implications for conservation. Potential nest predators are abundant in urban areas and some species frequently visit supplementary feeding stations. We assess whether providing supplementary food affects the likelihood of nest predation in the vicinity of the feeder, by acting as a point attractant for potential nest predators. We provided feeding stations (empty, peanut feeder, peanut feeder with guard to exclude potential nest predators) in an area of suburban parkland in the UK and monitored the predation rate of eggs placed in artificial nests located at distances that replicated the size of typical suburban gardens. Nest predators (Magpies Pica pica, Grey Squirrels Sciurus carolinensis) were frequent visitors to filled feeders, and predation caused by Magpies, European Jays Garrulus glandarius and Grey Squirrels was significantly higher when nests were adjacent to filled feeders. The presence of a feeder guard did not significantly reduce nest predation. As supplementary feeding is becoming increasingly common during the breeding season in suburban habitats, we suggest that providing point attractants to nest predators at this time may have previously unconsidered consequences for the breeding success of urban birds.     

Variability in the area,energy and time costs of wintering waders responding to disturbance

Birds’ responses to human disturbance are interesting due to their similarities to anti‐predator behaviour, and understanding this behaviour has practical applications for conservation management by informing measures such as buffer zones to protect priority species. To understand better the costs of disturbance and whether it will impact on population size, studies should quantify time‐related responses as well as the more commonly reported flight initiation distance (FID). Using waders wintering on an estuarine area, we experimentally disturbed foraging birds on the Wash Embayment, UK, by walking towards them and recording their responses (FID, alert time, time spent in flight, time taken to resume feeding, and total feeding time lost). We present data for 10 species of conservation concern: Curlew Numenius arquata, Oystercatcher Haematopus ostralegus, Bar‐tailed Godwit Limosa lapponica, Grey Plover Pluvialis squatarola, Redshank Tringa totanus, Knot Calidris canutus, Turnstone Arenaria interpres, Ringed Plover Charadrius hiaticula, Sanderling Calidris alba and Dunlin Calidris alpina. Larger species responded more strongly, response magnitude was greater under milder environmental conditions, and responses varied over both small and large spatial scales. The energetic costs of individual responses, however, were low relative to daily requirements and disturbance events were unlikely to be frequent enough to seriously limit foraging time. We suggest, therefore, that wintering wader populations on the Wash are not currently significantly negatively impacted by human disturbance during the intertidal foraging period. This is also likely to be the case at other estuarine sites with comparable access levels, visitor patterns, invertebrate food availability and environmental conditions.     

Personality and fitness consequences of flight initiation distance and mating behavior in subdominant male reindeer (Rangifer tarandus)

Animal personality has been studied extensively in recent years, yet multidimensionality in tendencies of risk‐related behavior, and the role of such consistency from a mating tactics perspective, is yet to be investigated. We used a semi‐domesticated herd of reindeer (Rangifer tarandus) to examine individual subdominant male propensity to risk mating attempts on guarded females, as well as flight initiation distance (FID), within the personality paradigm to elucidate potential fitness consequences of consistency from an adaptive perspective. Data were collected at the Kutuharju Reindeer Research Station in Kaamanen, Finland, where measures of personality were generated using field observation data based on the relative frequency of dominant male–subdominant male agonistic interactions over 4 years and subdominant males' FID measured over 1 year. Individual propensity for transient mating attempts was not significantly repeatable and did not significantly predict reproductive success or somatic cost during the mating season. Individuals varied consistently in FID, and although repeatable, FID was not related to reproductive success or somatic cost. Proximate state‐dependent or social mechanisms may be driving decision‐making with respect to mating effort, whereas consistent between‐individual differences in FID may be maintained by mechanisms unrelated to life‐history trade‐offs involving productivity.     

Effect of Approaching Boats on Nesting Black Skimmers: Using Response Distances to Establish Protective Buffer Zones

ABSTRACT Understanding how birds respond to the activities of people is an important component of conserving wildlife. We measured responses of nesting black skimmers (Rynchops niger) to an approaching boat in Barnegat Bay, New Jersey, USA, by examining distance to first respond, distance to flush, and time to return to the colony. Our objective was to determine if response distances of skimmers changed as a function of year, reproductive stage, direction of approach (direct or tangential), or number of birds nesting in the colony. Generally, reproductive stage had the greatest effect on all responses, followed by direction of approach, number of adults present at the colony, number of nests, and year, which also explained variation in behavioral responses. The distance at which skimmers first flew when a boat approached decreased from the pre-egg-laying period to hatching, and then increased slightly later in the season. Time (x̄± SE) for skimmers to return to the nesting colony varied seasonally, with birds taking longer to return during the pre-egg period (9.5 ± min) than during hatching (0.7 ± 0.1 min). The decision process for determining set-back distances to protect nesting skimmers should involve selecting 1) behavioral response of highest concern, 2) reproductive stage of highest concern, and 3) an appropriate level of response at which to establish the buffer area. We recommend that managers use a set-back distance of ± 118 m from the perimeter of the colony for black skimmers, which is the 95% percentile of the distance that skimmers first flew in response to approaching boats. Managers can use these data to set buffer distances for skimmers and other colonial birds.     

Behavioral responses of a sex-role reversed pipefish to a gradient of perceived predation risk

Conspicuous behaviors such as courtship and mating often makeanimals susceptible to predation. When perceiving themselvesat an elevated level of risk, animals frequently reduce conspicuousbehaviors in tradeoff for a decrease in probability of beingpreyed upon. In the present study, we used two experiments toexamine the effect of perceived predation risk from cod (Gadusmorhud) on nonreproductive and reproductive behaviors in thesex-role reversed pipefish (Syngnathus typhle). In the firstexperiment, no differences due to predation risk were detectedin the nonreproductive behaviors of either males or females.In the second experiment, predation risk had significant effectson reproductive behaviors. Pipefish were allowed to court andcopulate at four different predation levels. We created predationlevels differing in perceived predation risk by controllingthe number of sensory modes through which pipefish could detectthe presence of a cod. As predation risk increased, pipefishcopulated and courted less frequently, swam alone (displayedand searched for conspecifics) less often, and waited longerbefore commencing courtship. These changes in behavior minimizedthe amount of time spent above the eelgrass and presumably reducedconspicuousness to visual predators. Pipefish also copulatedafter a smaller amount of courtship as predation risk increased,indicating that they may trade information concerning mate qualityfor a reduction in predation risk. No differences were foundin any response variable between males and females. The roleof operational sex ratios and intersexual competition in determiningwhich sex assumes greater costs in mate acquisition is questioned.     

安邦河自然保护区繁殖期骨顶鸡对游憩干扰的行为反应

随着湿地生态旅游的发展,水禽面临着越来越多的游憩干扰。骨顶鸡在我国北方大部分地区的湖泡沼泽繁殖,可作为湿地质量的指示物种,探讨该物种对游憩干扰的反应很有意义。在黑龙江省安邦河自然保护区的游憩区和对照区进行了繁殖期骨顶鸡日行为观察,比较分析结果显示:繁殖前期游憩区骨顶鸡的躲避行为显著高于对照区(F_(1,18)=62.364,P0.01);孵卵期骨顶鸡对游憩干扰的反应比繁殖前期更强烈,除了躲避行为显著增加(雄性F_(1,8)=40.653,P0.01;雌性F_(1,8)=32.028,P0.01),还主要表现在雌骨顶鸡孵卵时间减少(F_(1,8)=13.521,P0.01),持续孵卵时间缩短;雄骨顶鸡取食时间峰值增加,取食中断不连续;雌雄骨顶鸡繁殖期行为及对游憩干扰反应有所不同。建议通过改善游憩区的隐蔽条件,以提供躲避空间,提高生境质量,减少游憩干扰的影响。     

骨顶鸡等游禽对不同人为干扰方式的响应

分别于2008年4月至6月和2009 年4月至6月, 采用目标动物取样法在黑龙江省安邦河湿地和大庆龙凤湿地研究了骨顶鸡等水鸟对人为干扰的行为响应。结果表明:骨顶鸡对行人和机动车辆两种干扰的反应距离类似,但耐受程度有所不同,骨顶鸡对机动车辆干扰的耐受性要好于行人干扰。在以游客等行人干扰为主的安邦河湿地,骨顶鸡以及其他游禽对干扰产生行为反应的比例要高于以机动车辆干扰为主的龙凤湿地,说明相对于行人干扰骨顶鸡对机动车辆更容易耐受;在安邦河湿地,骨顶鸡对划船的反应距离以及反应程度要大于人行走,说明骨顶鸡对于侵入性的干扰更为敏感。此外,对凤头(Podiceps cristatus)、黒颈(Podiceps nigricollis)、小(Tachybaptus ruficollis)、黑水鸡(Gallinula chloropus)、红头潜鸭(Aythya ferina)、赤膀鸭(Anas strepera)、绿头鸭(Anas platyrhynchos)、斑嘴鸭(Anas poecilorhyncha)、绿翅鸭(Anas crecca)、白眉鸭(Anas querquedula)、赤颈鸭(Anas penelope)、琵嘴鸭(Anas clypeata)等游禽对人为干扰的反应距离、耐受距离以及遭受干扰时的反应比例进行了研究,结果显示3种对干扰的耐受距离差异不显著,12种鸭类中红头潜鸭对人为干扰的敏感性要小于其他鸭类,斑嘴鸭和绿头鸭则相对敏感。     

Flight responses of eastern gray kangaroos to benign or harmful human behavior

Globally, wilderness is being converted for rural and agricultural land use. In countryside landscapes, many habitat structures remain intact, providing suitable habitat for wildlife species that can accurately assess novel risks and develop tolerance to benign disturbances. Associative learning that promotes avoidance and also facilitates desensitization to benign disturbance is key to persisting in these landscapes. Conversely, learning to distinguish and avoid negative interactions with humans, like hunting, is vital. To determine if eastern gray kangaroos are capable of learning from previous interactions with humans, we tested the flight responses of wild kangaroos which have previously experienced either low or high frequencies of harmful and benign encounters with humans. We found that eastern gray kangaroos rapidly habituated to benign disturbance as there was no significant difference in assessment distance between groups that previously experienced low or high frequencies of disturbance. The threat of harmful disturbances was not as quickly learnt, as groups that experienced low frequencies of harmful disturbance delayed flight longer than those experiencing frequent harm. We found that the influence of environmental and group parameters on a kangaroo's decision to flee depended on the intent and frequency of previous interactions with humans. Our study indicates that kangaroos are learning from previous encounters with humans, correctly assessing novel risks which may be contributing to their persistence in countryside landscapes.     

Costs of fear: behavioural and life‐history responses to risk and their demographic consequences vary across species

Behavioural responses to reduce predation risk might cause demographic ‘costs of fear’. Costs differ among species, but a conceptual framework to understand this variation is lacking. We use a life‐history framework to tie together diverse traits and life stages to better understand interspecific variation in responses and costs. We used natural and experimental variation in predation risk to test phenotypic responses and associated demographic costs for 10 songbird species. Responses such as increased parental attentiveness yielded reduced development time and created benefits such as reduced predation probability. Yet, responses to increased risk also created demographic costs by reducing offspring production in the absence of direct predation. This cost of fear varied widely across species, but predictably with the probability of repeat breeding. Use of a life‐history framework can aid our understanding of potential demographic costs from predation, both from responses to perceived risk and from direct predation mortality.     

Generalists are the most urban‐tolerant of birds: a phylogenetically controlled analysis of ecological and life history traits using a novel continuous measure of bird responses to urbanization

Identifying which ecological and life history traits influence a species’ tolerance to urbanization is critical to understanding the trajectory of biodiversity in an increasingly urbanizing world. There is evidence for a wide array of contrasting patterns for single trait associations with urbanization. In a continental‐scale analysis, incorporating 477 species and >5 000 000 bird observations, we developed a novel and scalable methodology that evaluated the ecological and life history traits which most influence a species’ adaptability to persist in urban environments. Specifically, we assigned species‐specific scores based on continuous measures of response to urbanization, using VIIRS night‐time light values (i.e. radiance) as a proxy for urbanization. We identified generalized, phylogenetically controlled patterns: bird species which are generalists (i.e. large niche breadth), with large clutch size, and large residual brain size are among the most urban‐tolerant bird species. Conversely, specialized feeding strategies (i.e. insectivores and granivores) were negatively associated with urbanization. Enhancement and persistence of avian biodiversity in urban environments probably relies on protecting, maintaining and restoring diverse habitats serving a range of life history strategies.