U.S. Fish & Wildlife Service Human Disturbance of Breeding Golden Eagles (Aquila chrysaetos)

Photo credit: Jeremy Buck, USFWS

Human Disturbance of Breeding Golden Eagles (Aquila chrysaetos)

U.S. Fish and Wildlife Service Regions 1, 2, 6, and 8

Front Matter September 18, 2017

Disclaimer The findings and conclusions in this article are those of the author(s) and do not necessarily represent the views of the U.S. Fish and Wildlife Service.

Suggested Citation Hansen, D.L., R.J. Spaul, B. Woodbridge, D. Leal, J.R. Dunk, J.W. Watson, and J. T. Driscoll. 2017. Human disturbance of breeding golden eagles (Aquila chrysaetos). Unpublished report prepared for the Western Golden Eagle Team, U.S. Fish and Wildlife Service. Available online at:. https://ecos.fws.gov/ServCat/Reference/Profile/112570

Acknowledgments This synthesis was authored by Dan L. Hansen, Robert J. Spaul, Brian Woodbridge, David Leal, Jeffrey R. Dunk, James W. Watson, and James T. Driscoll. The authors are grateful to the following reviewers (in alphabetical order): Joseph Buchanan, Michael Collopy, Joel Pagel, Matthew Stuber, and Hillary White.

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Table of Contents

Front Matter ...... i Disclaimer ...... i Suggested Citation ...... i Acknowledgments ...... i Table of Contents ...... ii Introduction ...... 1 Human Disturbance of Golden Eagles and Other Raptors ...... 2 Physiological Responses ...... 3 Behavioral Responses ...... 3 Alertness or Alarm ...... 4 Activity Patterns ...... 7 Habitat Associations, Spatial Relationships, or Distribution ...... 8 Reproduction, Survival, and Population Responses ...... 9 Factors Influencing Responses to Human Disturbance ...... 11 Auditory vs. Visual Stimuli ...... 12 Mode of Human Presence ...... 12 Vegetation and Terrain ...... 13 Proximity and Angle of Approach ...... 14 Nutritional Status...... 14 Reproductive Status and Time of Year...... 15 Previous Experience ...... 15 Protecting Breeding Golden Eagles from Human Disturbance ...... 17 Temporal Buffers ...... 18 Spatial Buffers ...... 18 Buffers Around Used Nests ...... 19 Buffers Based on Spatial Use ...... 21 Adaptation of Spatial Buffers ...... 25 References ...... 25 Appendix 1: Elicitation of Expert Opinion Concerning Human Disturbance of Breeding Golden Eagles ...... 33 Introduction and Methods ...... 33 Results and Discussion ...... 36 Management Considerations ...... 43 Acknowledgments ...... 44 References...... 44

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Introduction

The status of golden eagle (Aquila chrysaetos) populations in the western United States (U.S.) is unclear (USFWS 2009, 2016a). Kochert and Steenhof (2002) reported that some nesting populations in the western U.S. had declined due to human activities. More recently, modeling based on count data indicated that golden eagle populations in the western U.S. were generally stable during the period 1968–2014, while analyses of demographic data suggested that they are gradually declining (Millsap et al. 2013, USFWS 2016a). Regardless, the golden eagle is a protected species in the U.S., and some populations are negatively impacted by human activities (Kochert and Steenhof 2002, Kochert et al. 2002, USFWS 2016a, b). Recognized threats to golden eagles in the U.S. include electrocution by power lines, collisions with automobiles or wind turbines, lead poisoning, intentional shooting, habitat change, prey declines, and human disturbance (Kochert and Steenhof 2002, Kochert et al. 2002, USFWS 2009, 2016a, b). The following document is concerned with human disturbance of golden eagles, as defined below. Other potential threats, such as habitat modification, may also be considered forms of 'disturbance' but are not discussed herein.

Golden eagles are protected by the Bald and Golden Eagle Protection Act (16 U.S.C. 668- 668c; hereafter, Eagle Act), the Migratory Bird Treaty Act (16 U.S.C. 703-712), and various state regulations and guidelines. The Eagle Act is the primary law protecting golden eagles in the U.S. (USFWS 2009). The Eagle Act prohibits unauthorized 'take' of eagles. Take includes to "pursue, shoot, shoot at, poison, wound, kill, capture, trap, collect, destroy, molest or disturb (16 U.S.C. 668c; 50 CFR 22.3)." The U.S. Fish and Wildlife Service (hereafter, Service) defined the word 'disturb', as used in the Eagle Act, to mean "...to agitate or bother a bald or golden eagle to a degree that causes, or is likely to cause, based on the best scientific information available, (1) injury to an eagle, (2) a decrease in its productivity, by substantially interfering with normal breeding, feeding, or sheltering behavior, or (3) nest abandonment, by substantially interfering with normal breeding, feeding, or sheltering behavior (USFWS 2007:2)." In contrast with the Service's definition of disturbance, researchers often simply define human disturbance as activities that disrupt an animal's normal physiology or behavior (Knight and Skagen 1988, Frid and Dill 2002, Romero 2004). Few studies have established a clear link between wildlife species' physiological or behavioral responses to human activities and negative effects on survival, reproduction, or population size (Bowles 1995, Gill et al. 2001, Tarlow and Blumstein 2007).

The following synthesis is an evaluation of human disturbance of golden eagles. The synthesis is presented in three parts: (1) a review of what is currently known about the effects of human activities on the physiology, behavior, fitness, and population biology of golden eagles and other raptors; (2) a discussion of how the responses of golden eagles and other wildlife to human activities may be influenced by characteristics of the animal, human activity, or environment; and (3) an analysis of possible approaches to protecting breeding golden eagles from human disturbance. The purpose of this synthesis is to provide a review of currently available scientific information on these topics, rather than to recommend specific management guidelines or actions.

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Human Disturbance of Golden Eagles and Other Raptors

Disturbance of raptors is frequently evaluated through behavioral metrics; most often, the distance at which birds exhibit alertness or alarm in response to human activity (Knight and Skagen 1988, Taylor and Knight 2003). Fewer studies have used physiological metrics to investigate human disturbance of wild raptors. Disturbance metrics are imperfect in that those that are relatively easy to use can be unreliable measures of impacts on individuals or populations (e.g., stress hormone levels or distances at which birds become alert) while others can be difficult to use in the field (e.g., changes in heart rate). Research on human disturbance of raptors would ideally include direct measures of human activity and evaluation of multiple disturbance metrics, including changes in both fitness and behavior or physiology (Tarlow and Blumstein 2007; e.g., White and Thurow 1985, Fernández and Azkona 1993, Dunk et al. 2011, Spaul and Heath 2016, in press).

Individual disturbance events may often have little or no impact on fitness or population size (Gill et al. 2001, Gill 2007). For example, flushing a bird from its nest once may not negatively affect reproduction if the offspring are adequately thermoregulating or if flushing does not result in prolonged exposure of offspring to heat, cold, or predators (Fyfe and Olendorff 1976). Conversely, disturbance that is subtle or temporary but chronic could have cumulative effects on fitness. For instance, repeated disturbances may result in decreased reproduction through changes in behavior, such as reduced parental care or abandonment of the nest or territory (e.g., White and Thurow 1985). Repeated exposure to stressors can also compromise an animal's reproduction or survival through cumulative negative effects on its physiology (Wingfield 1988, Sapolsky et al. 2000, Busch and Hayward 2009). Some human activities, such as an annual recreational event, may result in infrequent or short-term disturbance of wildlife. Other activities may result in chronic or long-term disturbance. It is also possible for human activities to cause both short- and long- term disturbance; for example, construction of roads or energy developments could lead to short-term disturbance during the construction phase and long-term disturbance during operation and maintenance (e.g., see May 2015).

Responses to human disturbance can vary widely among species (Knight and Cole 1995b, Fletcher et al. 1999, Blumstein et al. 2003). Thus, efforts to reduce or avoid disturbance impacts on golden eagles should be informed by species-specific research to the extent possible. However, because there is relatively little empirical information about the effects of human disturbance on golden eagles it might be useful to review effects of human disturbance on other raptors. Research results for other species in the genus Aquila may be most relevant, followed by those for bald eagles (Haliaeetus leucocephalus), other large raptors, and finally, more distantly related species or those with substantially different natural histories, such as falcons or owls. We generally followed this guideline while selecting literature to include in this synthesis. We also included a smaller number of theoretical or review references that more broadly apply to birds or wildlife. The taxonomic group to which a statement or citation refers is noted in all cases.

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It is illegal to experimentally expose golden eagles to intensive human disturbance. Therefore, much of the available information about the species' responses to human activities is observational. Given the paucity of empirical research of human disturbance of golden eagles, and methodological differences among available studies, we also review expert elicitations on the subject. Expert opinion can provide a valuable supplement to limited empirical information when formulating recommendations for protecting wildlife from human disturbance (Whitfield et al. 2008, Martin et al. 2011, Drescher et al. 2013). Expert elicitation data are clearly denoted as such throughout the document.

Physiological Responses

Physiological measures, such as increases in heart rate or stress hormone levels, can be used to evaluate the effects of human activities on wildlife (Gabrielsen and Smith 1995, Tarlow and Blumstein 2007). For example, Wasser et al. (1997) found significantly higher fecal corticosterone (stress hormone) levels in male northern spotted owls (Strix occidentalis caurina) with home range centers located within 410 meters (m) of timber harvest activity or a major logging road than in male owls located farther away. Northern spotted owls also exhibited higher corticosterone levels in response to acute exposure to motorcycle activity (simulated "enduro" events; Hayward et al. 2011). An acute stress response is adaptive, in that it allows animals to mobilize energy reserves needed for coping with adverse conditions and can suppress behaviors that are not essential to survival (Tarlow and Blumstein 2007). Prolonged adrenocortical stress response, however, can result in physiological problems, including cessation of reproduction, cardiovascular disease, or immune system damage (Wingfield 1988, Sapolsky et al. 2000, Busch and Hayward 2009). Yet, some animals exhibit reduced corticosteroid levels in response to chronic stress or when they are in poor physiological condition (Busch and Hayward 2009, Hayward et al. 2011). Thus, low stress hormone levels do not necessarily indicate low stress levels (e.g., Hayward et al. 2011).

There is currently no published research investigating physiological effects of human disturbance on wild golden eagles. However, researchers found higher fecal glucocorticoid metabolite levels in captive golden eagles injected with adrenocorticotropin hormone (ACTH), which is commonly used to assess physiological stress responses (Staley et al. 2007). This result suggests that noninvasive measurement of physiological stress is a viable method for evaluating human disturbance of wild golden eagles.

Behavioral Responses

Researchers frequently use behavioral metrics to examine human disturbance of wildlife (Knight and Cole 1995a, Frid and Dill 2002, Taylor and Knight 2003). Tarlow and Blumstein (2007:430) noted that, "...ultimately a species' behavioral response to humans will influence its ability to coexist with humans." The 'risk-disturbance hypothesis' (Frid and Dill 2002) provides a theoretical framework for predicting and understanding wildlife behavioral responses to human disturbance. Disturbance by humans resembles predation risk in that it can cause animals to reduce their engagement in fitness-enhancing activities, such as foraging or parental care, in order to minimize their vulnerability to real or perceived threats. The risk-disturbance hypothesis predicts that animals will be more responsive to human activities when they perceive them to be more threatening and when the fitness costs of responding are lower. Thus, a high degree of responsiveness could

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indicate either a high level of perceived threat or a low cost of responding, while a low degree of responsiveness could reflect either a low threat level or high cost of responding (Gill 2007). Examples of the potential relevance of the risk-disturbance hypothesis to evaluating human disturbance of golden eagles and other raptors are discussed below.

Alertness or Alarm

The distances at which individuals exhibit behavioral indicators of alertness or alarm are among the most commonly used metrics for evaluating human disturbance of raptors and other wildlife (Knight and Skagen 1988, Taylor and Knight 2003, Tarlow and Blumstein 2007). These distances are also frequently used to formulate spatial buffers for protecting raptors from human disturbance (Knight and Skagen 1988, Richardson and Miller 1997). Increased vigilance, flight, and distance moved may reflect fitness costs to raptors and other wildlife through wasted energy, lost foraging opportunities, or reduced parental care (Fyfe and Olendorff 1976, Ydenberg and Dill 1986, Knight and Skagen 1988, Tarlow and Blumstein 2007). In addition, flushing an adult raptor from the nest might result in reduced reproductive success due to trampling, ejection, cooling, overheating, or desiccation of eggs or offspring (Fyfe and Olendorff 1976). Many golden eagle nests are exposed to direct sunlight so overheating in particular could be a source of injury or mortality for the species' eggs or young (Fyfe and Olendorff 1976, Brown et al. 2015, Kochert et al. in prep.).

Spaul and Heath (in press; Spaul 2015) provided the only empirical data for distances at which breeding golden eagles flush in response to human activities. Golden eagles in their study (n = 23 territories) nested on canyon cliffs in sagebrush-dominated (Artemisia tridentata) landscapes in southwestern Idaho. Eagles rarely flushed in response to recreationists (pedestrians and various types of OHVs) passing within 1.2 kilometers (km) of nests or perches (14% of 270 passes). Eagles flushed from nests during only 7% of passes (n = 183). Eagles flushed from nests at a mean distance of 449 m (SD = 311 m, range = 110– 1,000 m) from passing recreationists and remained off the nest an average of 57.2 minutes (SD = 86.8 minutes, range = 3.9–286.2 minutes; Spaul 2015). Golden eagles perched away from the nest flushed during 26% of passes and at a mean distance of 506 m (SD = 342 m, range = 300–1,300 m; Spaul 2015). Eagles perched away from the nest were 12 times more likely to flush in response to recreationists than eagles perched on nests (Spaul and Heath in press). Based on the risk disturbance hypothesis, the lower rate of golden eagles flushing from nests than perches was likely a reflection of higher potential fitness costs of flushing from nests; for example, due to the risk of exposing eggs or nestlings to cooling or overheating.

Suter and Joness (1981) elicited expert opinions concerning the likely behavioral responses of nesting raptors, including golden eagles, to pedestrians, off-highway vehicles (OHVs), and construction activity. They asked experts to estimate distances at which 20% of golden eagles (i.e., relatively responsive or sensitive individuals within a population) would respond in particular ways during different phases of the nesting period (Table 1). Between 15 and 17 experts responded to each question. Median estimates of the distance at which relatively responsive golden eagles would flush from the nest when one or more pedestrians approached ranged from 100 to 333 m, depending on the phase of the nesting period (see Table 1). The median estimated distance at which eagles would flush from the nest when a noisy OHV (up to 100 a-weighted decibels [dBA]) approached was 183–350 m (Table 1).

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There was substantial variability among experts' estimates for both of these activities (15– 2,414 m; Table 1).

Whitfield et al. (2008) elicited opinions from experts concerning distances at which Scottish golden eagles would exhibit alertness (e.g., head raised in an alert posture) or flushing in response to a pedestrian during two phases of the nesting period (incubation and nestling). Between 14 and 25 experts responded to each of the four questions. Median responses for alert distances were 400 and 625 m during the incubation and nestling periods, respectively. Median responses for flushing were 225 and 400 m, respectively. Whitfield et al. (2008) did not report the full range of experts' estimates. Excluding the bottom 10% and top 10% of estimates, experts' responses ranged from 10 to 1,500 m, depending on the response metric and nesting phase.

The Service (Appendix 1) recently conducted an elicitation aimed at capturing contemporary opinions of biologists with expertise with golden eagles in the western U.S. Depending on the question, between 18 and 19 experts provided estimates of distances at which relatively sensitive breeding golden eagles (e.g., 20% of individuals) would flush from the nest in response to various human activities (see Table 2; Appendix 1). All estimates apply to the nesting phase during which the expert considered eagles to be most responsive to human disturbance. The median distances at which experts estimated that eagles would flush from the nest ranged from 366 to 549 m, depending on the human activity (see Table 2). As in previous expert elicitations, there was considerable variability among experts' estimates (range = 91–1,811 m; Table 2).

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Table 1: Distances (m) at which raptor experts (n = 15–17) estimated that relatively sensitive golden eagles would behaviorally respond to various human activities (Suter and Joness 1981).

Question Breeding Phase Median Range n 1. At what distance would an individual or small group of people a. laying 160 15–1073 16 approaching a nest cause 20% of sitting birds of each species listed to b. incubation 100 15–805 17 flush from the nest during the following periods? c. rearing young 333 15–1609 16

2. At what distance would extended a. nest construction 550 250–4023 16 activities involving several persons and approximately 90 dBA noise, e.g., b. laying 478 250–4023 16 drilling or earth moving, cause abandonment of the nest by 20% of c. incubation 402 150–1609 15 individuals of each species during the following periods? d. rearing young 383 100–1609 16

3. At what distance would a noisy off- road vehicle (up to 100 dBA) cause a. laying 183 30–2414 15 20% of sitting birds of each species listed to flush from a nest during the b. incubation 187 30–2414 16 following periods? c. rearing young 350 30–2414 15

4. At what distance would frequent (1 a. nest construction 457 91–5632 15 per hour) noisy off-road vehicles cause abandonment of the nest by 20% of the b. laying 457 91–2414 15 individuals of each species during the following periods? c. incubation 402 91–2414 15

d. rearing young 200 50–2414 15

5. Within what distance of an activity involving several people and large equipment would at least 80% of the members of each species hunt and kill prey? 400 30–3218 15

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Table 2: Distances (m) at which raptor experts (n = 18–19) estimated that relatively sensitive breeding golden eagles (e.g., 20% of individuals) would flush from the nest in response to various human disturbances (Appendix 1).

Rock Con- Military OHV Use Hiking Climbing struction Training Median 457 366 457 457 549 Mean 509 406 495 583 647 SD 402 312 345 412 455 Range 91–1554 91–1143 91–1143 101–1609 101–1811

Activity Patterns

Changes in activity patterns are also common metrics of human disturbance of wildlife (Frid and Dill 2002). For raptors, important activities that may be affected by human disturbance include foraging, parental care, self-maintenance, pair bond maintenance, vigilance against natural predators, and territory establishment or defense. For example, nesting bald eagles responded to nearby camping with decreased preening, sleeping, nest maintenance, food consumption, and provisioning of the young, increased brooding of nestlings, and greater time spent away from the nest (Steidl and Anthony 2000). When hikers were nearby, nesting female Mexican spotted owls (S. o. lucida) spent less time preening, allopreening, maintaining their nests, and handling prey, more frequently attended the nest, and more frequently emitted contact vocalizations (Swarthout and Steidl 2003). Nesting marsh harriers (Circus aeruginosus) spent less time in their territories, less time incubating eggs and protecting nestlings, and delivered less food to their young when exposed to nearby activity by humans, dogs, or livestock (Fernández and Azkona 1993). Female northern goshawks (Accipiter gentilis) spent less time on nests during exposure to sustained (ca. 1 hour) OHV activity than nesting females in control (no exposure) territories (Dunk et al. 2011).

Changes in activity patterns induced by human activities, such as reduced provisioning of the nest, could influence the fitness of raptors. For example, marsh harrier nestlings in territories with human disturbance had higher blood urea levels than those in undisturbed territories (Fernández and Azkona 1993). This result indicated poorer nutritional status of nestlings in territories with human disturbance and a potential negative effect of human activities on the fitness of marsh harrier pairs through reduced reproductive success.

Steidl et al. (1993) found notable but statistically non-significant tendencies for nesting golden eagles in Alaska to perform fewer feeding bouts and spend less time eating, maintaining the nest, and preening when humans camped closer to nests (400 m) than farther away (800 m). Eagles at nests with closer camping also tended to spend less time standing ("no particular behavior") at the nest, more time brooding or shading young, and more time away from the nest. The amount of food ("bites") consumed per day by both adults and nestlings showed a substantial, but statistically non-significant, negative trend at nests with closer camping (mean reduction: 67% for adults, 39% for nestlings, and 49% combined).

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In Idaho, Spaul and Heath (2016) found that nest attendance by egg-laying golden eagles was negatively associated with activity by human pedestrians (pedestrians/hour) (n = 10 and 11 occupied, egg-laying territories during the two field seasons). Nest attendance was a strong predictor of nest success (daily nest survival), so human disturbance apparently negatively affected reproduction by golden eagles (see Reproduction, Survival, and Population Responses, below).

The Service's (Appendix 1) expert elicitation appears to provide the only estimates of continuous distances (as opposed to two discrete distances in Steidl et al. 1993) at which breeding golden eagles' activity patterns may be impacted by human disturbance. The median distances at which experts (n = 18) estimated that relatively sensitive golden eagles (e.g., 20% of individuals) would noticeably reduce provisioning at the nest ranged from 457 to 869 m, depending on the human activity (see Table 3). There was considerable variability among experts' estimates (91–1,408 m; Table 3).

Table 3: Distances (m) at which raptor experts (n = 18) estimated that relatively sensitive breeding golden eagles (e.g., 20% of individuals) would noticeably reduce provisioning at the nest in response to various human disturbances (Appendix 1).

Rock Con- Military OHV Use Hiking Climbing struction Training Median 503 457 457 709 869 Mean 572 534 542 648 756 SD 384 368 365 370 416 Range 101–1372 91–1372 101–1372 101–1207 101–1408

Habitat Associations, Spatial Relationships, or Distribution

Human activities can also affect the habitat associations, ranging behavior, or distributions of wildlife (Hockin et al. 1992, Frid and Dill 2002). For example, researchers found fewer wintering bald eagles in areas with high levels of human activity and a negative association between recreational activity and the numbers of bald eagles at or near the river they studied and within the study area as a whole (Stalmaster and Newman 1978, Stalmaster and Kaiser 1998). Similarly, Bautista et al. (2004) found that the occurrence of Spanish imperial eagles (A. adalberti) near roads decreased during weekends (November–June), when road traffic was highest. Andersen et al. (1990) reported that several raptors evaluated together, including one golden eagle, three red-tailed hawks (Buteo jamaicensis), two ferruginous hawks (B. regalis), and a Swainson's hawk (B. swainsoni), appeared to respond to military training exercises during the breeding season (July–August) by shifting and enlarging their home ranges, using different areas within their home ranges, or leaving the area entirely. Dunk et al. (2011) found that fledgling northern goshawks used slightly less suitable habitat (based on relative habitat suitability modeling) during sustained (ca. 1 hour) exposure to OHV activity than before or after exposure.

A shift in habitat associations or spatial relationships could result in negative impacts on fitness; for example, if animals use lower quality or larger areas that reduce their foraging success or increase their energy expenditures (Frid and Dill 2002). However, the absence of an observable shift in habitat associations, spatial relationships, or distribution does not

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necessarily indicate the lack of an effect on fitness. Gill et al. (2001) noted that animals may remain in an area despite human disturbance if there are no suitable alternative areas nearby. Golden eagles are territorial so they could be further constrained from leaving an area if there are no vacant territories on the landscape (Kochert et al. 2002).

Some raptor species appear to alter their flight patterns, habitat associations, spatial relationships, or distribution in response to the presence of wind energy facilities (Walker et al. 2005, Pearce-Higgins et al. 2009, Garvin et al. 2011, Johnston et al. 2014, May 2015, Kolar and Bechard 2016). Changes in raptor behavior could occur in response to perception of wind turbines themselves as direct threats (potential sources of mortality) and/or to human activities associated with maintenance or operation of facilities (May 2015). Some raptors may be displaced from wind energy developments; although lower numbers of raptors observed in some studies could have been due to mortalities from collisions with wind turbines or reduced reproduction, rather than displacement (Pearce-Higgins et al. 2009, Garvin et al. 2011).

There is limited published information about effects of wind energy developments on the behavior of golden eagles. Johnston et al. (2014) found that migrating golden eagles appeared to avoid wind turbines in British Columbia, Canada by increasing their flight altitude. In Scotland, Walker et al. (2005) recorded only 3 golden eagle flights over a wind energy development constructed within a pair's home range. Both members of the pair were observed using the area prior to construction of the development but almost completely avoided it after construction. In California, Hunt et al. (1995) conducted road surveys for golden eagles in the Altamont Pass Wind Resource Area (WRA) during May–November of 1994. They sighted golden eagles in the WRA on 249 occasions. Eagle sightings were clustered near the boundary of the WRA and eagle densities were higher at an adjacent, ecologically similar reference site without wind energy development. However, it is unknown if lower densities in the WRA than in the reference site were due to avoidance of wind energy facilities, lower prey abundances due to ground squirrel control measures, or other factors.

Reproduction, Survival, and Population Responses

Early research on golden eagles suggested that human activities were responsible for the majority of golden eagle nest failures (D'Ostilio 1954, Camenzind 1969, Boeker and Ray 1971). The degree to which human disturbance contributed to nest failures in those study areas, as opposed to other human activities such as persecution or habitat modification, is unclear. As summarized below, the results of subsequent expert elicitations, empirical studies, and simulation modeling suggest that human disturbance does indeed negatively affect the fitness, occupancy, and population rates of golden eagles (Suter and Joness 1981, Watson and Dennis 1992, Kaisanlahti-Jokimäki et al. 2008, Martin et al. 2009, McIntyre and Schmidt 2012, Steenhof et al. 2014, Heath and Spaul 2016, Pauli et al. 2016; Appendix 1). However, expert elicitations provide the only estimates currently available for distances at which this occurs.

Watson and Dennis (1992) compared reproduction during a single year (1982) at 348 golden eagle nests in Great Britain and found that a significantly higher percentage (50.3%) of nests classified as "difficult" for humans to access fledged young than those classified as

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"easy" to access (30.9%); an intermediate percentage of sites classified as "moderate" accessibility fledged young (45.1%). Watson and Dennis (1992) suggested that other factors (e.g., egg collection by humans, greater accessibility to nest predators) may have contributed to the higher percentage of failures at more accessible nests but that unintentional human disturbance was likely the primary cause of the observed pattern.

Kaisanlahti-Jokimäki et al. (2008) compared golden eagle occupancy rates during the breeding season around 12 tourist destinations in Finland (n = 10–12 territories evaluated around each destination). They found that occupancy rates were significantly lower in territories near large tourist destinations than near medium-sized destinations. Modeling showed that occupancy was negatively associated with the size of the tourist destination and the length of snowmobile and ski routes surrounding the destination. The study did not determine whether golden eagle occupancy was impacted by tourist activity or some other factor, such as habitat changes associated with development of tourist destinations.

Martin et al. (2009) modeled occupancy dynamics of golden eagles in Denali National Park and Preserve, Alaska. Territory colonization by eagles (i.e., the probability of a historical territory being occupied given that it was unoccupied the previous year) was slightly higher in areas with lower levels of potential human disturbance (based on a qualitative assessment of accessibility to hikers). In the same study area, McIntyre and Schmidt (2012) did not find a relationship between golden eagle occupancy and reproduction and whether or not roads or hiking routes were located within 2 km of territory centroids. The authors suggested that the effects of human disturbance on golden eagles are likely low in Denali because of low levels of human activity during the early part of the breeding season, when eagles are most likely to abandon their nests in response to disturbance.

Steenhof et al. (2014) used more than 40 years of golden eagle occupancy and reproductive data from Idaho to compare 3 nesting territories with potentially high levels of OHV activity (located near motorized recreational trails, play areas, and parking areas) with territories that likely had less motorized recreation (based on trail density within territories). Significant declines in golden eagle occupancy and reproduction occurred in the 3 territories following a substantial increase in use of OHVs during the latter portion of the study period. Significant declines did not occur in territories with less or no OHV activity. The study did not reveal whether declines in occupancy and reproduction were caused by OHV use per se, or other activities associated with it such as hiking, camping, or shooting.

In a subsequent study in the same area in Idaho, Spaul and Heath (2016; Spaul 2015) found that the probability of territory occupancy by golden eagles (n = 23 territories) during the breeding season was lower in areas with higher seasonal-average OHV levels. The probability that eagles on territories would lay eggs was negatively associated with pedestrian activity (pedestrians/day/trail) near nests during the pre-laying portion of the nesting period. The survival of nests was negatively associated with acute exposure to OHV traffic (interval-specific OHVs/day/trail), suggesting that spikes in OHV traffic contributed to nest failures. Furthermore, nest attendance, a strong predictor of nest survival, appeared to be negatively affected by the presence of pedestrians, who generally arrived near eagle nests via OHVs and other motorized vehicles. Peak OHV levels in the study area coincided with hatching and early brood rearing (March–May), when offspring may be most vulnerable to exposure or starvation due to parents flushing from nests or reducing provisioning.

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Pauli et al. (2016) modeled the long-term population-level effects of human disturbance on golden eagles. Their model was based on known effects of recreation on golden eagle reproduction and occupancy in Idaho, as reported by Spaul and Heath (2016). They also modeled effects of both increased recreation levels and increased tolerance of golden eagles to recreation. Compared with a scenario with no recreation, levels of recreation observed in 2014 significantly and negatively affected population growth rate, population size, and final territory occupancy. Even moderate (<3%) annual increases in recreation levels substantially exacerbated these negative effects in simulations. A 3% annual increase in recreation resulted in population extinction within 100 years in 65% of simulations, and nearly 99% of simulations ended with less than 10 individuals remaining in the population (Pauli et al., unpubl. data). Simulated increases in eagles' tolerance to recreation mitigated negative effects of recreation on populations. However, when increases in both tolerance and recreation levels were included in simulations, the positive effects of increasing tolerance did not fully compensate for increasing recreation levels, and populations were negatively impacted.

Suter and Joness (1981) surveyed opinions of raptor experts (n = 15–16) regarding distances at which relatively sensitive golden eagles (20% of individuals) would abandon their nest in response to frequent use of noisy OHVs (up to 100 dBA) or other extended, noisy activities (ca. 90 dBA), such as construction with heavy equipment (Table 1). Median estimates ranged from 200 to 550 m, depending on the human activity and eagle nesting phase (see Table 1). Estimates were highly variable among experts (range = 50–5,632 m; Table 1).

The Service (Appendix 1) elicited expert estimates (n = 18) of distances at which relatively sensitive golden eagles (e.g., 20% of individuals) are likely to fail to breed or occupy a nest site in response to human activities. Median estimates ranged from 320 to 823 m, depending on the human activity (see Table 4). As in Suter and Joness' (1981) elicitation, estimates were variable among experts (range = 91–1,646 m; Table 4).

Table 4: Distances (m) at which raptor experts (n = 18) estimated that relatively sensitive breeding golden eagles (e.g., 20% of individuals) would fail to breed or occupy a nest site in response to various human disturbances (Appendix 1).

Rock Con- Military OHV Use Hiking Climbing struction Training Median 411 320 457 686 823 Mean 556 479 550 624 831 SD 328 314 336 376 480 Range 137–1097 101–1097 183–1143 91–1207 183–1646

Factors Influencing Responses to Human Disturbance

Multiple factors can affect the responses of raptors and other wildlife to human activities (Gutzwiller 1991, 1993, Hockin et al. 1992, Knight and Cole 1995a, b). It is important to recognize the potential influence of these factors in order to properly interpret research

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findings and determine appropriate actions for reducing or avoiding impacts from human disturbance.

Auditory vs. Visual Stimuli

In general, animals appear to be more responsive to louder sounds than to quieter ones (Bowles 1995). For example, Mexican spotted owls only flushed in response to helicopters and chainsaws when sound energy was above certain levels (chainsaws: 46 dBA, helicopters: 92 dBA; Delaney et al. 1999). Awbry and Bowles (1990:21 cited in USFWS 2006) stated that "what little published literature (on raptors) is available suggests that noise begins to disturb most birds at around 80–85 decibels (dB) sound levels and that the threshold for the flight response is around 95 dB." The Service (USFWS 2006) noted in its review of effects of human disturbance on northern spotted owls that raptors tend to be more sensitive to visual disturbances than to auditory ones. However, auditory and visual stimuli from human activities may often interact synergistically in their effects on wildlife (USFWS 2006). This synergistic effect could be responsible for findings that raptors are often more strongly affected by terrestrial activities than aerial activities (USFWS 2006; e.g., Fraser et al. 1985, Delaney et al. 1999, Grubb et al. 2010). The Service (USFWS 2006) recommended an injury threshold for northern spotted owls of 46 dBA for terrestrial activities due to the potential for stronger effects of ground-based activities than of aerial activities.

Mode of Human Presence

Whether an activity is motorized or non-motorized can influence whether or not animals are likely to encounter it and perceive it as threatening (Knight and Cole 1995a). Motorized vehicles may have a high potential for disturbing wildlife due to their ability to move rapidly through large areas and because some vehicles produce loud sounds (Ouren et al. 2007). Yet, non-motorized activities can also be widespread and are often more likely to disturb wildlife than motorized activities (Knight and Cole 1995a, Hill et al. 1997; e.g., Reed and Merenlender 2008, Spaul and Heath 2016, in press, Nordell et al. 2017). Breeding Spanish imperial eagles more frequently flushed in response to the presence of campers, ecotourists, and hunters than to humans engaged in motorized activities (Gonzalez et al. 2006). Gonzalez et al. (2006) attributed this result to campers, ecotourists, and hunters behaving in a provocative and unpredictable manner, such as remaining near eagle nests for relatively long periods of time, stopping at irregular intervals, walking in no particular direction, and looking up toward the sky or at the surrounding area. Stalmaster and Kaiser (1998) found that wintering bald eagles flushed more readily and flew farther away in response to pedestrians than to boating. However, boat traffic, particularly motorboats, disturbed a larger proportion of the eagle population than did pedestrians.

Rock climbing could be a severe form of disturbance for golden eagles and other cliff-nesting raptors as it often involves shouting and other noises and can bring humans into close proximity to nests (Richardson and Miller 1997). In addition, rock climbers can be active above golden eagle nests, and animals are generally more sensitive to terrestrial human activities occurring above them than below them (Knight and Cole 1995b). We found no research on the effects of rock climbing near golden eagle nets; however, Brambilla et al. (2004) found that Peregrine falcons (Falco peregrinus) nesting on cliffs used for rock

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climbing (cliffs with fixed protection and regularly frequented by climbers) had lower reproduction than those nesting on cliffs without rock climbing.

Little information exists concerning the relative sensitivity of golden eagles to different kinds of human activities. Holmes (1993) found that wintering golden eagles flushed at greater distances from direct approaches by pedestrians than by passenger vehicles. Spaul and Heath (2016, in press) found negative effects of both pedestrians and vehicles on breeding golden eagles. It was difficult to disentangle the effects of these two forms of disturbance since nearly all (96%) pedestrians in the study arrived near eagle nests by vehicle, rather than on foot. However, golden eagles were 60 times more likely to flush in response to motorized recreationists who stopped and became pedestrians, and 4.5 times more likely to flush in response to OHVs, than to road vehicles (Spaul and Heath in press). Spaul and Heath (2016) suggested that eagles perceived recreationists that disembarked from vehicles as greater threats than motorized recreationists because pedestrians were more likely to behave in an unpredictable way, go off trail, or be associated with eagles' past experiences with human persecution. They further noted that eagles in their study area may experience more exposure to vehicles than pedestrians, which could facilitate greater habituation to motorized recreation.

Overflights and even close passes by fixed-wing aircraft and helicopters rarely cause golden eagles on nests to flush or exhibit other strong startle reactions (Boeker 1970, DuBois 1984 cited in Kochert et al. 2002, Grubb et al. 2010). However, golden eagles on nests may flatten and freeze when approached by helicopters (Kochert et al. 2002). Use of helicopters to check nests in southwestern Idaho caused large numbers of adult golden eagles (121 of 227 adults [53%]) perched near nests to flush (DuBois 1984 cited in Kochert et al. 2002). Additionally, golden eagles occasionally collide with aircraft, either incidentally or when attacking them as territorial intruders (Bruderer 1978, Washburn et al. 2015, USFWS 2016b). Junda et al. (2015) used an unmanned aerial vehicle (drone) for surveying nests of bald eagles, ospreys (Pandion haliaetus), ferruginous hawks, and red-tailed hawks. The drone did not appear to disturb nesting raptors, although it did elicit an aggressive response from an osprey on one occasion.

Vegetation and Terrain

The degree to which a human activity is visually screened from an animal can strongly influence whether or not the animal detects and responds to it (Knight and Cole 1995b). For example, flight distances of wintering bald eagles were longer when humans approached on foot through open areas than through heavy riparian vegetation (Stalmaster and Newman 1978). Nesting bald eagles were significantly less responsive (alert posture, flushes, flight after flushing) to pedestrians when at nests with a high degree of visual screening than at nests with partial or low levels of screening (Watson 2004). Propagation of sound through the environment is likewise affected by vegetation and terrain, as well as distance and weather (Bowles 1995). Fyfe and Olendorff (1976) suggested that earlier detection of human activities by nesting raptors results in lower risk of the parent being startled and ejecting eggs or young when flushing.

Vegetation and terrain could also affect the behavior of humans and thus, their influence on raptors. For example, Spaul (2015) noted that the steep canyons, rocky outcrops, and cliffs

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used by nesting golden eagles in Idaho appeared to inspire motorized recreationists to leave trails and roads, disembark from their vehicles, and engage in unpredictable movements on foot. Golden eagles in that study flushed most frequently in response to motorized recreationists who left their vehicles to walk or hike (also see Spaul and Heath in press).

Proximity and Angle of Approach

The proximity of a human activity appears to be among the primary factors determining whether and how animals respond to it. Effects of proximity are usually evaluated through animals' alert or alarm responses and changes in activity patterns, which are discussed above. Grubb and King (1991) found an inverse relationship between bald eagles' distances from human activities and the severity of their responses to them (i.e., none, alert, flush, depart from the immediate area).

The angle at which humans approach an animal can also have a strong influence on the animal's response. Direct approaches often elicit stronger responses than tangential approaches (Frid and Dill 2002). Stopping and directly approaching an animal could respectively signal a predator’s detection of, and intent to capture, the animal (Frid and Dill 2002). However, some animals may be more responsive to tangential approaches than direct approaches (Fernández-Juricic et al. 2005). At tangential angles the rate of approach is slower than in direct approaches, potentially allowing animals to detect and respond to the activity sooner (Fernández-Juricic et al. 2005). Differences in the effects of direct and tangential approaches could have been partially responsible for the substantially different distances at which golden eagles responded to experimental (Holmes 1993) versus non- experimental (Spaul and Heath in press) human disturbance.

The proximity of a human disturbance and its angle of approach have a vertical dimension, as well as a horizontal one. The vertical dimension of an animal's location could affect how soon the animal detects and responds to a disturbance or its perception of risk from the disturbance (Fernández-Juricic et al. 2004). Bald eagles perched closer to the ground flushed more frequently and flew farther away in response to human disturbance than those perched higher (Knight and Knight 1984, McGarigal et al. 1991, Steidl and Anthony 1996, Stalmaster and Kaiser 1998, Watson 2004). Similarly, Holmes (1993) reported that wintering American kestrels (F. sparverius), prairie falcons (F. mexicanus), and ferruginous hawks perched closer to the ground flushed at greater distances than those perched higher.

Nutritional Status

Foraging animals may be less behaviorally responsive to disturbances when they are in worse physiological condition due to poor nutrition or when their environment appears to provide fewer alternative foraging locations (Ydenberg and Dill 1986, Beale and Monaghan 2004). Yet, fitness could be more negatively affected by human disturbance when animals are already physiologically stressed due to poor nutrition. White and Thurow (1985) reported that reproduction by ferruginous hawks was most affected by human disturbance during a poor prey year.

Nutritional status can also influence physiological attributes used by researchers to evaluate human disturbance. Female northern spotted owls had low stress hormone levels

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when their nutritional status was poor (Hayward et al. 2011). This result likely reflected 'allostatic overload', whereby normal physiological and behavioral coping mechanisms are overwhelmed due to stress and poor condition. Conversely, the higher nutritional status of northern spotted owls nesting near roads (presumably due to greater access to key prey species) appeared to physiologically offset the tendency to exhibit increased stress hormone levels in response to road traffic (Hayward et al. 2011).

Reproductive Status and Time of Year

Breeding raptors often appear to be less behaviorally responsive to human disturbance than nonbreeding ones. Delaney et al. (1999) found that female Mexican spotted owls only flushed in response to sound from helicopters or chainsaws after their young fledged. Similarly, breeding bald eagles were generally less behaviorally responsive to human activities than nonbreeding eagles (McGarigal et al. 1991, Steidl and Anthony 1996). Steidl and Anthony (1996) suggested that this was likely due to parents' fitness investment in offspring and thus, reluctance to leave them exposed; although territorial breeding eagles in the study may also have been more habituated to human activities than non-territorial individuals.

The earliest part of the breeding season (courtship through egg-laying) is a time when golden eagles are most likely to respond to human disturbance by abandoning their nesting attempt and possibly their territory (Fyfe and Olendorff 1976). Spaul and Heath (2016) found that recreational activity (hiking and OHV use) during this period reduced the probability that golden eagles on territories would lay eggs. In contrast, raptors often appear to be less behaviorally responsive to human disturbance during the incubation or early brood-rearing phase of the breeding season, when parents are invested in their nesting attempt and when offspring are most dependent on parental care for survival (Fyfe and Olendorff 1976, Richardson and Miller 1997). Disturbance during this phase, however, can have a strong negative effect on reproduction. Steenhof and Kochert (1982) reported that golden eagles that were disturbed by researchers during the incubation or early brood- rearing phases of nesting had fewer successful breeding attempts than those disturbed later in the nesting period or not at all (disturbance was defined as researchers eliciting a behavioral response or entering the nest). Spaul and Heath (2016) found that nest survival was negatively associated with short-term peaks in OHV use during the incubation and brood-rearing phases of nesting.

Previous Experience

Habituation is "a process that leads to decreased responsiveness to a stimulus with repeated presentation and is often adaptive in that it makes it less likely that individuals will respond to harmless stimuli (Blumstein 2016:255)." Animals often exhibit behavioral habituation to human activities that are spatially or temporally predictable and that consistently appear to pose little or no risk (Knight and Cole 1995b, Whittaker and Knight 1998). For instance, breeding Spanish imperial eagles were less likely to flush in response to human activity when their nests were located in areas with more frequent activity (Gonzalez et al. 2006). Similarly, ferruginous hawks nesting near roads with lower traffic volumes were more likely to flush in response to vehicle approaches than those nesting near roads with higher traffic volume (Nordell et al. 2017). Andersen et al. (1989) found that red-

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tailed hawks in an area with relatively frequent helicopter activity were more tolerant of helicopter overflights than those in an area with less helicopter activity. Reproduction by ospreys showed little or no sensitivity to research disturbance in a suburban setting (Poole 1981), whereas ospreys in a national park appeared to be strongly and negatively affected by human recreation (Swenson 1979).

Despite past widespread persecution by humans, golden eagles sometimes nest in areas with relatively high concentrations of humans or human activity. Whether the proximity of some golden eagle nests to humans or human activity is due to tolerance of human activity or limited availability of more suitable nest sites is unclear (see Gill et al. 2001).

It is possible that some eagle populations are becoming more tolerant of human activities across generations. This could occur through the process of 'natal habitat preference induction', whereby dispersing young prefer to settle in areas with stimuli similar to those in which they fledged (Davis and Stamps 2004). Dispersing eagles need not use human activity as a cue for selecting an area to settle in but could simply tolerate it as something that occurs in otherwise suitable areas. Through this mechanism, eagles could become increasingly tolerant of humans as successive generations are exposed to greater levels of human activity and declining or stable levels of persecution (Guinn 2013).

Pauli et al. (2016) included increased tolerance in their simulation modeling of recreation effects on golden eagle populations (see Reproduction, Survival, and Population Responses, above). Modeling of increased tolerance was theoretical, as it is currently unknown how quickly or through what mechanisms golden eagle populations become more tolerant of human activities. They found that the mitigating effects of tolerance on recreation impacts on simulated populations were greater through genetic inheritance or habituation than through natal habitat preference induction or random assignment. Their modeling suggested that rates of increased tolerance would be insufficient to compensate for the negative effects of even moderate increases in recreation levels (<3%/yr).

Repeated exposure to human activities sometimes results in sensitization of wildlife, rather than habituation. Sensitization can be defined as "increased responsiveness to a stimulus with repeated presentation (Blumstein 2016:255)." In the context of human disturbance, sensitization likely occurs when repeated activities regularly appear threatening (Knight and Cole 1995b) or have associated stimuli that are particularly aversive such as sudden loud noises (Dill 1974). Possibly due to persecution, wintering bald eagles spent more time being vigilant when foraging in areas with high levels of human activity than in areas with low levels of activity (Knight and Knight 1986). Fraser et al. (1985) found that breeding bald eagles flushed at increasing distances when exposed to greater numbers of experimental disturbance events by pedestrians. Ferruginous hawks have likewise exhibited increasing sensitization to human disturbance during the course of studies (White and Thurow 1985, Nordell et al. 2017). Even habituated raptors will respond to human disturbance above a threshold intensity or within some minimum proximity (USFWS 2006). For example, birds may be incapable of habituating to sound above approximately 92 dB (Awbry and Bowles 1990 cited in USFWS 2006).

Wildlife can appear to be tolerant of human activities and still be stressed by them. Strasser and Heath (2013) found that while American kestrels nested in a human- dominated landscape in Idaho, individuals nesting near large, busy roads and developed

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areas had higher stress hormone levels and were more likely to abandon their nests than kestrels nesting elsewhere. They suggested that favorable habitat located near areas with high human activity may be "ecological traps" for some individuals or populations (also see Gill et al. 2001).

Stressed animals can appear to be tolerant of human disturbance because their stress response no longer functions normally. Long-term or repeated activation of the physiological and behavioral stress response can cause animals to 'acclimate' to the stressor through stress hormone down-regulation (Romero 2004, Busch and Hayward 2009). Down- regulation of stress hormone levels can compromise an animal's ability to engage adaptive physiological and behavioral coping mechanisms in stressful situations. Alternatively, acclimated animals can experience 'facilitation', whereby they show little response to a previously experienced stressor but exhibit higher stress response levels with novel stressors (Romero 2004, Busch and Hayward 2009).

Protecting Breeding Golden Eagles from Human Disturbance

Biologists and land managers have identified human disturbance as a primary threat to raptor populations (LeFranc and Millsap 1984, Richardson and Miller 1997). Currently available information indicates that golden eagles vary in their sensitivity to human activities but that human disturbance can influence the species in ways that may result in reduced fitness and long-term population impacts (reviewed above). It is therefore important to consider options for avoiding or minimizing human disturbance of golden eagles.

Land management agencies often employ spatial and temporal restrictions (buffers) on human activities in order to avoid or minimize disturbance of raptors (Richardson and Miller 1997, Knight and Skagen 1998). Spatial buffers are defined zones around important locations, such as nests or key foraging areas, within which particular human activities are prohibited or limited. Temporal buffers are often used in conjunction with spatial buffers and are aimed at protecting raptors during periods when they are thought to be most sensitive to disturbance (Richardson and Miller 1997, Knight and Skagen 1998).

Both bald and golden eagles are protected from disturbance under the Eagle Act, but the Service currently only provides buffer recommendations for bald eagles (USFWS 2007). Appropriate buffer recommendations for golden eagles could differ from those for bald eagles, as golden eagles appear to be more sensitive to human disturbance (USFWS 2016b). Greater sensitivity of golden eagles than bald eagles could be due to differences in habitat associations (e.g., more exposure to visual or auditory disturbance when nesting on exposed cliffs and foraging in open areas), less habituation to human activities, or other factors. For both species, populations and individuals may vary in their sensitivity to human disturbance; for example, depending on their past experience with human activities or persecution. Regardless, species-specific buffer recommendations may be necessary for limiting human disturbance of golden eagles.

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Although the remainder of this synthesis is focused on spatial and temporal buffers for breeding golden eagles, other management actions may be useful for protecting the species from human disturbance. For example, Spaul and Heath (in press) suggested that "a combination of management strategies, such as trail closures, no-stopping zones, increased enforcement of existing trail regulations, limiting expansion of new trails, and management that considers the entire eagle territory and the full duration of eagle breeding seasons, would help reduce negative human-eagle interactions."

Temporal Buffers

Temporal buffer recommendations for golden eagles should include at least the first part of the breeding season, from courtship through the first few weeks of nestling development, when disturbance may be most likely to negatively affect reproduction (Suter and Joness 1981, Steenhof and Kochert 1982, Richardson and Miller 1997, Spaul and Heath 2016). However, potential vulnerability of older offspring to human disturbance (Fyfe and Olendorff 1976) suggests that it is prudent to protect golden eagles during the entire nesting period. It could also be important to protect the nest area from disturbance during the first few weeks after young fledge, when they are typically active in the vicinity of the nest (see Figure 2 in O'Toole et al. 1999). In the western U.S., the breeding season, including courtship through natal dispersal, is generally January–August (Kochert et al. 2002). The nesting chronology of golden eagles varies geographically so temporal buffers for breeding pairs should be tailored accordingly. For example, golden eagles in California began courtship and nest building as early as December (Hunt et al. 1998).

Although this document is focused on human disturbance of breeding golden eagles, human activities may also negatively impact eagles outside the breeding season (USFWS 2007). Survival of golden eagles could be negatively affected by human activities that decrease foraging efficiency or increase energy expenditures (Frid and Dill 2002); particularly during winter when many individuals may already be energetically stressed due to cold temperatures and reduced prey availability (Newton 1979). Reproduction of golden eagles could likewise be impacted by human disturbance outside the nesting season; for example, if individuals are unable to attain adequate breeding condition due to lost foraging opportunities or wasted energy (Newton 1979, Hirons 1985, Martin 1987). It might therefore be important to protect golden eagles from human activities outside the breeding season, as well as during it.

Spatial Buffers

Spatial buffers for raptors are often based on distances at which the species exhibits alertness or alarm, such as flushing from nests or perches (Knight and Skagen 1998, Richardson and Miller 1997, Tarlow and Blumstein 2007). Yet, caution is needed when interpreting flushing and other behavioral responses of golden eagles to disturbance. The fitness impacts of human disturbance may often be highest when behavioral responsiveness is lowest, and a single metric can provide a false picture of whether or not disturbance has occurred (Gill 2007, Tarlow and Blumstein 2007). Additionally, the distances at which golden eagles respond to human disturbance could vary tremendously, depending on an array of factors such as characteristics of the human activity, the time of year, the animal's physiological condition and previous experience with the human activity, and attributes of

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intervening terrain and vegetation (see Factors Influencing Responses to Human Disturbance, above). Failure to acknowledge the potential importance of these factors might result in protective buffers that target the wrong types of activities, that are the wrong size, or that are implemented in the wrong locations or during the wrong time of year. Such mistakes could lead to inadequate protection of golden eagles or unnecessary restrictions on human activities and wasted management resources.

Current state agency (Colorado Division of Wildlife 2008) and Service field office (USFWS 2002) recommendations for protecting breeding golden eagles from human disturbance call for 0.5-mile (0.8-km) buffers around used nests. These buffer recommendations are based on the opinions of a small number of experts and reviews of literature concerning effects of human activities on raptors. Additional sources of information about responses of breeding golden eagles to human disturbance have become available since formulation of existing recommendations, including both empirical research and elicitations of expert opinion. As reviewed below, those sources indicate that 0.5-mile buffers may indeed adequately protect many golden eagle nests from human disturbance. However, smaller or larger nest buffers may be appropriate depending on the phase of the nesting season and the level of risk that decision makers assume when promulgating regulations. Larger analysis or buffer areas may be needed to protect eagles when they are active away from the currently used nest (e.g., while foraging or engaged in territorial behavior) and when disturbance is likely to occur during more than one season or year (see Buffers Based on Spatial Use, below).

Buffers Around Used Nests

Spatial buffers for raptors and other wildlife are commonly based on distances at which the species becomes alert or flees in response to human activities (Knight and Skagen 1988, Richardson and Miller 1997, Tarlow and Blumstein 2007). Some raptor researchers have recommended basing nest buffer sizes on the distances within which 90 or 95% of alert or flight responses occurred during studies, rather than on mean or median distances (e.g., McGarigal et al. 1991, Holmes et al. 1993, Whitfield et al. 2008; see Fernández-Juricic et al. 2005 for methods used to recommend buffer sizes for other avian taxa). Buffer sizes based on 90 or 95% of the cumulative probability of observed alert or flight distances are intended to be conservative, in that they are aimed at preventing most or all disturbance at nests (Fernández-Juricic et al. 2005, Whitfield et al. 2008).

The only information currently available concerning alert distances of nesting golden eagles was provided by an elicitation of expert opinion (Whitfield et al. 2008). The median distances at which experts estimated that Scottish golden eagles would become alert to a pedestrian were 400 and 625 m during the incubation and nestling phases, respectively. Ninety percent of experts in that elicitation estimated that golden eagles would become alert to a pedestrian within 1.0–1.5 km of the nest, depending on the phase of the nesting season. Whitfield et al. (2008:2710) calculated this metric "...due to its potential equivalence to 90% of the cumulative probability of observed AD (alert distance) or FID (flight initiation distance)."

Spaul and Heath (in press; Spaul 2015) provided the only empirical data for distances at which breeding golden eagles flush in response to human disturbance. They found that golden eagles in southwestern Idaho flushed from nests and perches at mean distances of

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449 and 506 m, respectively. Restricting recreation within 910 and 1,000 m of eagles would have decreased flushing by 90 and 95%, respectively (R. Spaul, unpubl. data).

Expert opinion can supplement the limited empirical data available for determining nest buffers based on flushing distances. The median distances at which raptor experts estimated that Scottish golden eagles would flush from the nest in response to a human pedestrian were 225 and 400 m during the incubation and nestling phases, respectively (Whitfield et al. 2008). Ninety percent of experts in that elicitation estimated that golden eagles would flush from the nest in response to a pedestrian active within 1.0–1.5 km of the nest, depending on the nesting phase. Median estimates by U.S. experts surveyed by the Service (Appendix 1) ranged from 366 to 549 m, depending on the human activity (see Table 2). Ninety and 95 percent of U.S. experts surveyed estimated that golden eagles would flush in response to disturbance within 805–1,554 m, depending on the human activity (see Table 5).

Table 5: Distances (m) at or below which 90% and 95% of golden eagle experts (n = 18–19) estimated that relatively sensitive breeding golden eagles (e.g., 20% of individuals) would flush from the nest, noticeably reduce provisioning at the nest, or fail to breed or occupy a nest site in response to various human activities (Appendix 1).

Rock Con- Military OHV Use Hiking Climbing struction Training Flush from Nest 1097, 1207 805, 1097 914, 1097 914, 1554 1097, 1372 Reduce Provisioning 1097, 1097 914, 1143 914, 1097 1097, 1097 1280, 1372 Fail to Breed or Occupy Nest Site 914, 1006 914, 914 1097, 1097 1097, 1097 1372, 1408

The distances at which changes in parental behaviors occur could also be useful for determining nest buffer sizes for golden eagles, as they may represent distances at which negative effects on reproduction are likely. Steidl et al. (1993) provided the only empirical data currently available for distances at which human disturbance affects parental behaviors of golden eagles. They recorded substantial but statistically non-significant negative trends in provisioning and attendance at the nest when humans camped closer to nests than farther away (400 vs. 800 m). Steidl et al. (1993:13) stated that "based on our results thus far, we believe that human activity within 800 m of an occupied eagle nest has the potential to influence the survivorship of nestlings. Therefore, pending additional study, we recommend no human activity should be allowed within a 800 m radius of the nest to prevent disturbance to the nesting behaviors of golden eagles." Median distances at which experts (n = 18) surveyed by the Service (Appendix 1) estimated that relatively sensitive golden eagles (e.g., 20% of individuals) would noticeably reduce provisioning at the nest ranged from 457 to 869 m, depending on the human activity (see Table 3). The distances at or below which 90 and 95% of experts estimated that this would occur ranged from 914 to 1,372 m (see Table 5).

Nest buffers could also be based on the distances at which disturbance results in golden eagles failing to breed or occupy a nest site, or at which nest abandonment occurs. These distances may reflect those at which a negative effect on fitness is likely to occur. Only

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expert elicitation data currently exist for distances at which human disturbance might result in golden eagles failing to nest or occupy a nest site or abandoning their nesting attempt. Median distances at which experts surveyed by Suter and Joness (1981) estimated that relatively sensitive golden eagles would abandon their nests in response to frequent noisy (up to 100 dBA) OHV activity or extended noisy (ca. 90 dBA) construction ranged from 200 to 550 m, depending on the nesting season phase and human activity (see Table 1). Suter and Joness (1981) did not report the distances within which 90 or 95% of respondents estimated that golden eagles would abandon their nests in response to frequent OHV activity or extended noisy construction. These values may have been substantially greater than the median values reported above, as the maximum estimates for OHV activity and construction were 5.6 and 4.0 km, respectively. Median distances at which experts (n = 18) surveyed by the Service (Appendix 1) estimated that relatively sensitive golden eagles (e.g., 20% of individuals) would fail to breed or occupy a nest site in response to human disturbance ranged from 320 to 823 m, depending on the human activity (see Table 4). Ninety and 95 percent of respondents in that elicitation estimated that golden eagles would fail to breed or occupy a nest site in response to human activity within 914– 1,408 m, depending on the activity (see Table 5).

Buffers Based on Spatial Use

Solely buffering currently used nests could inadequately protect golden eagles from human disturbance. Activity by male golden eagles at used nests is generally limited to prey delivery or briefly relieving the female during incubation or brooding (Collopy 1984, Watson et al. 2014a). Male golden eagles often rest on perches in view of used nests but are also frequently active in other parts of their home ranges (Watson et al. 2014a). Because males provision females and offspring during the nesting season, chronic disturbance of them while foraging might negatively affect reproduction. Reproduction might also be affected if parents or offspring are disturbed after the young fledge and are active beyond the area immediately surrounding the nest. In southwestern Idaho, golden eagles perched away from nests were 12 times more likely to flush in response to recreationists than eagles at nests (Spaul and Heath in press). This suggests that frequent human activity away from used nests could result in chronic disturbance of foraging golden eagles and thus, reduced foraging success or provisioning rates.

Golden eagle territories typically contain multiple nests (Watson 2010; e.g., Kochert and Steenhof 2012, Watson et al. 2014a). Buffering all known nests could be important if long- term protection of breeding eagles is an objective (Kochert and Steenhof 2012, Watson et al. 2014a, Millsap et al. 2015). Kochert and Steenhof (2012) found an average of 6.9 nests per territory (SD = 3.7; range = 1–18) during their 41-year study in southwestern Idaho. The smaller numbers of nests per territory found in other studies were likely due to the shorter time spans of those studies, as well as possible ecological differences among study areas and populations (Kochert and Steenhof 2012). Over the course of their study, Kochert and Steenhof (2012) found that golden eagles used more than 1 nest in 92% of monitored territories, and between 5 and 8 nests in 45% of territories. Thirty four percent of nests were reused after more than 10 years of nonuse and some nests were reused after decades of nonuse.

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It could be important to protect alternative nests even if human disturbance is likely to occur during only a single breeding season. Watson et al. (2014a) reported that golden eagles in the Columbia Plateau of Oregon and Washington concentrated their activity near alternative nests when they were not located near the used nest. Golden eagles may frequently spend time near alternative nests due to their familiarity with the surrounding environment, for territorial reasons, or to strengthen pair bonds by decorating nests (Watson et al. 2014a, Millsap et al. 2015).

The core area is the disproportionately used portion of an individual or pair's home range (Bingham and Noon 1997, Powell 2000). Animals' core areas may often contain areas with the most dependable food resources (Bingham and Noon 1997, Powell 2000). Golden eagle breeding core areas may also generally contain both the used nest and most or all alternative nests (Watson et al. 2014a, Millsap et al. 2015). The risk of disturbing breeding golden eagles is likely greater within their core areas than outside of them due their concentrated use of those areas. Multiple studies have provided estimates of golden eagle core area sizes (Marzluff et al. 1997, Watson et al. 2014b, Braham et al. 2015, Crandall et al. 2015, USFWS unpubl. data). Mean breeding season core area estimates from these studies ranged from 1.94 to 25.95 km2 (Table 6). Variation in core area estimates within and among studies was likely due to both differences in estimation methods and ecological differences among home ranges and study areas (Bingham and Noon 1997, Powell 2000; see Table 6).

Small sample sizes in studies and variation in core area estimation methods could make it difficult to use published core area estimates for determining appropriate buffers for protecting golden eagles from human disturbance. To address this issue, the Service (unpubl. data) analyzed the spatial relationships of a large sample of satellite-telemetered golden eagles (n = 142) using data from 11 studies located across western North America. Based on average core area isopleth values for each individual (see Bingham and Noon 1997 and Vander Wal and Rodgers 2012 for methods; also see Table 6), the mean estimated breeding season core area was 6.9 km2 (SE = 0.9). Estimated breeding season core areas were smallest in middle latitudes (40–50o N; mean = 5.0 km2, SE = 0.4, n = 96), largest in northern latitudes (>50o N; mean = 15.2 km2, SE = 5.3, n = 14), and intermediate in southern latitudes (<40o N; mean = 8.0 km2, SE = 2.0, n = 32). Breeding season core area estimates were intended to represent spatial use during the incubation period or, if not nesting, a time when eagles were likely most active near their territory centers (May–June for northern latitudes, March–April for middle latitudes, and February–March for southern latitudes). This analysis is not yet completed and will include more eagles over time. We will update this synthesis to reflect revisions to these core area analyses as they become available.

Current estimates of breeding season core area sizes suggest that buffers of 0.5 mile (0.8 km) would often be inadequate for protecting golden eagles from human activities that occur away from the used nest. This is particularly true for activities that may result in disturbance outside the breeding season or over multiple years, as nonbreeding season, annual, and multi-annual core area estimates for golden eagles can be substantially larger than breeding season estimates (Marzluff et al. 1997, Watson et al. 2014b, Braham et al. 2015).

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Golden eagle experts (n = 19) surveyed by the Service (Appendix 1) were each asked to distribute 100 points among various types of spatial buffers in proportion to their relative efficacy at protecting breeding golden eagles from human disturbance (choices: fixed radius buffer around used nest; adaptive buffer around used nest based on environmental characteristics; buffer around used and known alternative nests; nesting core area/territory buffer; other [write-in]). Nearly 73% of the total points for all experts combined were allocated to buffers that include all known nests and/or the breeding core area or territory, whereas 27% were allocated to buffers around used nests alone. Seventeen (89%) respondents allocated 50 or more points to buffers around all known nests or based on nesting core areas or territories, whereas only 2 (11%) allocated 50 or more points to buffering around the used nest alone. These results suggest that experts in the western U.S. generally think that larger buffers based on the locations of all known nests or the sizes of core areas or territories would be more effective at protecting breeding golden eagles from human disturbance than buffers around used nests alone.

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Table 6: Estimated sizes (km2) of golden eagle core areas during the breeding season. See the footnotes for additional information about studies' core area estimation methods.

Study Location n Method* Mean (SD) Marzluff et al. 1997 Snake River, ID 9 Territories Concave polygon (90%) 1.94 (1.88) Watson et al. 2014b Columbia Plateau, OR and WA 10 Eagles Brownian bridge (50%) 4.9 (2.0) 25.95 adaptive Local (grand mean Braham et al. 2015 Mojave Desert, CA 8 Eagles Convex Hull (50%) Mar–Aug) 12 Eagles; Minimum Convex Crandall et al. 2015 South-Central MT 10 Territories Polygon (50%) 2.28 (1.83) Non-linear exponential regression (mean USFWS unpubl. data Western North America 142 Eagles isopleth = 61.9%) 6.9 *(1) Marzluff et al. (1997:676) used concave polygons "...because they minimized territory overlap, included all known locations of eagles, and did not rely upon statistical distributions of locations." They considered 90% concave polygons to represent core areas because "most territories showed little change in the rate of area increase for cluster polygons that included from 20 to 90% of the locations but typically increased sharply thereafter (Marzluff et al. 1997:676)." (2) Watson et al. (2014b) used the Brownian bridge movement model (Horne et al. 2007) to estimate utilization distributions (UDs). They chose this method because it allowed them to estimate UDs that included eagle flight paths, allowing "...evaluation of potential conflicts with wind turbine siting (Watson et al. 2014b:3)." (3) Braham et al. (2015) used adaptive Local Convex Hulls (Getz et al. 2007)—a nonparametric kernel method that they considered statistically appropriate given the short (15 minute) intervals at which data were collected. Getz et al. (2007:1) consider it a good estimation method "because of its ability to identify hard boundaries (e.g., rivers, cliff edges) and convergence to the true distribution as sample size increases." (4) Crandall et al. (2015) used 50% Minimum Convex Polygons to represent core areas. (5) The Service (USFWS unpubl. data) estimated core areas using a non-linear exponential regression analysis for each individual for each month or breeding season (see Bingham and Noon 1997 and Vander Wal and Rodgers 2012). Vander Wal and Rodgers (2012:48) described the method as follows: "Core areas were delineated using a time- maximizing function derived from kernel analyses. Essentially, we plotted utilization distribution area against volume and determined the point at which the slope of the line fitted to the data is equal to 1; this point represents a threshold where the proportional home range area begins to increase at a greater rate than the probability of use and the corresponding isopleth value defines the boundary of the core area; an animal’s time spent within this area is maximized relative to the periphery."

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Adaptation of Spatial Buffers

Spatial buffers for golden eagles need not be uniform in size or shape. If sufficient information exists for an eagle territory, a knowledgeable biologist could potentially adjust the size and shape of a recommended spatial buffer. For example, due to likely movement patterns of golden eagles and sound propagation from human activities, nests located in narrow canyons might be better protected from disturbance by longer, narrower buffers than by circular buffers. Conversely, golden eagles at nests with expansive views may detect, and possibly be disturbed by, human activities at large distances (Camp et al. 1997). Biologists could also adjust the size or shape of buffers to account for whether or not vegetation is likely to visually and aurally screen nest areas, foraging areas, or other important habitat features from human activities. The need for smaller or larger buffers might also be indicated by eagles' previous experiences with human activities. However, as reviewed in this synthesis, habituation and sensitization to disturbance are more complex phenomena than may be commonly thought. Past occupancy, turnover, or reproductive information for a territory could potentially be used to assess the likelihood that resident eagles have been negatively affected in the past by particular human activities. The Service is in the process of using telemetry data from a large number of golden eagles (see Buffers Based on Spatial Use, above) to create a computer program that could be used for estimating the size and shape of golden eagle nesting core areas. We will update this document with a link to that software when it becomes available.

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Appendix 1: Elicitation of Expert Opinion Concerning Human Disturbance of Breeding Golden Eagles

Introduction and Methods

The U.S. Fish and Wildlife Service (hereafter, Service) is currently evaluating appropriate buffer zones for protecting breeding golden eagles (Aquila chrysaetos) from human disturbance. Existing guidelines for protecting golden eagles from human disturbance are only available at the state level, in Utah and Colorado (USFWS 2002, Colorado Division of Wildlife 2008). Those guidelines were largely based on the recommendations of a small number of experts and did not involve a structured process for eliciting expert opinion. Subsequent to formulation of state guidelines, Spaul and Heath (in press) measured distances at which golden eagles in southwestern Idaho flushed from nests and perches in response to human recreation. That research provided crucial empirical data for evaluating buffer sizes for breeding golden eagles; but inferences from it may not apply to other geographic areas or other types of eagle responses or human activities. Two published expert opinion surveys are also available concerning distances at which breeding golden eagles may be disturbed by human activities (Suter and Joness 1981, Whitfield et al. 2008). However, one of the surveys was published 36 years ago and the other was specific to Scottish eagles. It is unclear whether these elicitations represent contemporary opinions of golden eagle experts in the U.S.

In order to supplement available information, we elicited estimates from experts in the U.S. for distances at which breeding golden eagles are likely to be disturbed by human activities. We also asked experts which parts of the home range should be buffered to most effectively protect breeding golden eagles from human disturbance. Our elicitation approach resembled the Delphi method (Delbecq et al. 1975), in that it was an iterative process, with more than one round of questionnaires, and intervening group discussions. The iterative nature of our method provided an opportunity to address possible sources of bias in expert judgments, such as poorly worded or incorrectly interpreted questions. It also provided respondents with feedback from other experts, potentially reminding or informing them of factors not considered during their previous responses to questions. However, social dynamics among experts can introduce other kinds of bias in elicitations, such as inordinate influence by individuals with dominant personalities, or a greater desire to achieve group consensus than to give carefully considered responses (Drescher et al. 2013). To address these issues, we provided a structured environment for group interactions and did not seek consensus judgments from the group. We also chose to not seek consensus because variation among experts could reflect differences in their experiences with human disturbance of golden eagles.

We contacted 40 biologists with substantial experience observing breeding golden eagles. We attempted to contact a large proportion of golden eagle experts in the western U.S., including male and female biologists from a variety of regions and with a variety of professional backgrounds. We identified candidates based on our knowledge of the

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community of golden eagle experts and on recommendations provided by experts contacted during the process. Twenty biologists agreed to participate in the elicitation. All 20 participants responded to the first questionnaire and 19 responded to the second questionnaire. Seventeen of the 19 participants in the full elicitation process responded to the questionnaires as individuals and 2 responded in consultation with colleagues with whom they regularly observed golden eagles.

We used two rounds of questionnaires to elicit experts' judgments concerning human disturbance of breeding golden eagles. We based the questions on established elicitation methods (Speirs-Bridge et al. 2010), a thorough review of research concerning human disturbance of golden eagles and other raptors (this synthesis), and input from golden eagle experts during the elicitation. We emailed the first questionnaire to participants in May 2015, and the second in May 2016. The first questionnaire was intended to stimulate thought about golden eagle responses to human activities, familiarize participants with the questions, and highlight ways in which the second questionnaire could be refined. Only the second questionnaire's questions and responses are described herein.

In March 2016, we facilitated two web-based phone discussions following completion of the first questionnaire and prior to distributing the second questionnaire. We conducted two discussions in order to accommodate the diverse schedules of respondents. Sixteen of 19 (84%) respondents to the second questionnaire participated in one of the discussions. While the discussions naturally differed, our approach to facilitating the discussions and the information we provided to participants were identical. In both cases, we presented discussion topics and summary materials in slide format and a biologist experienced with expert elicitation facilitated the discussion. Each discussion covered four main topics: (1) an overview of the elicitation's approach and potential applications; (2) clarification of the questions and disturbance scenarios; (3) a summary of the aggregated results of the first questionnaire; and (4) potential changes to the second questionnaire, based on respondents' feedback on the first questionnaire. The experts were aware of the identity of other participants in the discussion, and in the elicitation as a whole, but we maintained respondents' anonymity in regard to individual results and comments from the first questionnaire. After each discussion, we provided detailed notes from the discussion to all participants in the elicitation. All respondents were encouraged to review the notes and contact us with any additional questions or comments.

We asked the following questions in the second questionnaire:

Question 1a. Distribute 100 points among the following regions in proportion to their relative influence on your understanding of how breeding golden eagles respond to human disturbance (choices: Alaska/boreal; Interior Mountains [Rocky Mountains, Sierra Nevada, Cascades]; Wyoming Basin/Great Plains; Great Basin/Columbia Plateau; Southwest deserts/canyonlands; California Coast Ranges). We asked Question 1a to help us describe our sample of experts and to evaluate potential regional variation in expert opinions about human disturbance of golden eagles (Questions 2a–4e, below).

Question 1b. Distribute 100 points among the following nest substrates in proportion to the relative influence that golden eagles that use them have had on your understanding of the species' responses to human disturbance (choices: cliffs/rock outcrops; trees). Question 1b allowed us to further describe our sample of experts and to evaluate whether variation in

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estimates of distances at which golden eagles respond to human disturbance was related to respondents' experience with eagles nesting in cliffs/rock outcrops versus trees (Questions 2a–4e, below). It is possible that eagles using one type of nest are nearer to, or more visually or aurally exposed to, human disturbance than eagles using other types of nests.

Questions 2a–4e. Realistically, what do you think is the longest, shortest, and most likely distance at which a small but significant proportion of breeding golden eagles (e.g., upper 20% in terms of sensitivity) would (response metric) in response to (human activity)? Please rate your confidence (from 50-100%) that your interval, from shortest to longest, captures the most likely distance. Response Metrics: Questions 2a–e: Flush from the nest Questions 3a–e: Noticeably reduce their provisioning rate at the nest Questions 4a–e: Fail to breed or occupy a nest site Human Activities: Questions 2a, 3a, 4a: OHV activity Questions 2b, 3b, 4b: Hiking Questions 2c, 3c, 3d: Rock climbing Questions 2d, 3d, 4d: Construction activity Questions 2e, 3e, 4e: Military training We asked Questions 2a–4e to obtain experts' estimates of the distances at which breeding golden eagles would respond to human activities that are relatively common in the western U.S. and which are within the purview of public land management agencies and the Service’s permitting regulations. The list of human activities included in these questions was refined during discussions with our panel of experts. Herein, we only discuss experts' best estimates of the distances at which golden eagles would respond to human activities. Estimates of the longest and shortest distances at which eagles would respond to human activities, and respondents' confidence that this range captures the actual distance at which eagles would respond, will be discussed in a forthcoming publication.

We asked Questions 5a and 5b to obtain experts' opinions on how to prioritize the information obtained in this elicitation (Questions 2a–4e) and on various approaches to protecting breeding golden eagles from human disturbance:

Question 5a. Distribute 100 points among this elicitation's three response metrics in proportion to their relative appropriateness as bases for establishing buffers to protect breeding golden eagles from human disturbance (choices: flushing from the nest; noticeable reduction in provisioning; failure to occupy nest site or breed). Please consider both the ability of experts to reliably estimate distances at which golden eagles exhibit these responses and their potential to reflect take or reduced fitness of eagles.

Question 5b. Distribute 100 points among the following bases for establishing buffers in proportion to their relative efficacy at protecting breeding golden eagles from human disturbance (choices: fixed radius buffer around used nest; adaptive buffer around used nest based on environmental characteristics; buffer around used and known alternative nests; nesting core area/territory buffer). If you know of other appropriate bases for establishing buffers please write them in the blank boxes on the upper right side of the table and include them in your distribution of points.

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As discussed in the main body of this synthesis, golden eagle responses to human activities may vary among individuals and populations, and could depend on many factors other than the distance at which the activities occur. To narrow the range of conditions potentially influencing respondents' interpretation of Questions 2a–4e, we asked that they envision the human activities, golden eagles, and environment in the following way while answering the questionnaire: (1) The activity was occurring during the portion(s) of the nesting period during which the respondent considers golden eagles to be most responsive to it. (2) The activity was occurring in an open landscape (e.g., open rangeland) lacking terrain or vegetation capable of providing visual or auditory screening from the activity. (3) The eagles were not habituated to the activity in question or to human disturbance in general. The activity was occurring in a landscape with minimal ambient levels of disturbance. (4) Use of OHVs was to be envisioned as loud (e.g., unmuffled vehicles), involving multiple vehicles, and repetitive but not predictable in time or location. (5) Hiking or rock climbing included multiple recreationists, who were talking or shouting, stopping and looking around, and leaving flat areas or trails in order to travel cross-country or access terrain features. Hiking or rock climbing could potentially have occurred at or above the height of the nest. (6) Construction activities included multiple people and repeated, prolonged, and unpredictable use of heavy equipment or other loud machinery. (7) Military training included a combination of surface explosions, fast-moving heavy vehicles, and both large- and small-caliber gunfire (e.g., 5.7-50 mm, tank rounds). Training could have been focused, as in target range training, or dispersed, as in maneuvers. Training exercises may have been sustained and conducted over multiple days. (8) Questions about the distances at which human activities are likely to cause a particular behavioral response pertained to a "small but significant proportion of breeding golden eagles." A reasonable definition for "small but significant proportion" could be the most sensitive 20% of the population (Suter and Joness 1981).

Results and Discussion

Question 1a (regions in which experts obtained knowledge of, or experience with, human disturbance of golden eagles). All 19 participants responded to Question 1a. The mean number of points (out of 100) assigned by respondents to each region ranged from 8.4 in the California Coast Ranges to 30.3 in the Great Basin/Columbia Plateau (Figure 1). Seventeen (89%) respondents reported being influenced by their experience or knowledge from more than one region. Each region had at least slight influence (>5 points) on between 4 and 12 respondents (Figure 2). Although we did not formally stratify our sample of experts by region, our group of respondents included expertise from all major ecoregions occupied by breeding golden eagles in the western U.S.

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Figure 1: Mean points (0–100) assigned to regions in terms of their relative influence on experts' (n = 19) understanding of how breeding golden eagles respond to human disturbance.

Figure 2: Number of experts (out of 19) that assigned at least 5 points (out of 100) to a given region based on its relative influence on their understanding of how breeding golden eagles respond to human disturbance.

Question 1b (nest substrates used by eagles that influenced experts' knowledge of, or experience with, human disturbance of golden eagles). All 19 participants answered Question 1b. The mean number of points (out of 100) assigned by experts to cliffs/rock outcrops and trees were 75.7 (SD = 23.8) and 24.3 (23.8), respectively. Seventeen (89%) respondents have observed golden eagles using both nest substrates. However, only 3 (16%) respondents reported that golden eagles that nest in trees equally or more strongly (>50 points) influenced their understanding of the species' responses to human disturbance compared with those that nest in cliffs or rock outcrops (Figure 3).

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Figure 3: Number of experts (n = 19) that assigned at least 5, 25, and 50 points (out of 100) to golden eagles that nest in cliffs or rock outcrops versus trees in terms of their relative influence on the expert's understanding of golden eagle responses to human activities.

Questions 2a–4e (estimates of distances at which breeding golden eagles would respond to human activities). All 19 participants responded to Questions 2a–2d, and 18 responded to Questions 2e–4e. Minimum and maximum estimates of the most likely distances at which relatively sensitive breeding golden eagles would respond to human disturbance ranged from 91 to 1,811 meters (m), depending on the human activity and eagle response metric (Table 1; Figure 4). Median estimates of the most likely distance ranged from 320 to 869 m (Table 1; Figure 4). Quartiles for estimates of the likely distance are shown in Figure 4, portraying both central tendencies and variability among experts' responses.

Median responses by experts in this elicitation are relatively similar to those in previous elicitations of raptor experts (Suter and Joness 1981, Whitfield et al. 2008), and to mean distances at which golden eagles flushed from nests in response to human activities in a recent study in southwestern Idaho (Spaul and Heath in press) (Table 2). This congruence may suggest that these values provide a sound basis for formulating protective buffers for golden eagle nests. It is possible, however, that some respondents in our elicitation were influenced by the results of previous elicitations; particularly that of Suter and Joness (1981), which is well known in the raptor biology community.

Estimates of the most likely distances at which golden eagles respond to human activities were variable among experts (Table 1). The largest estimate per question was an average of 12.77 times larger than the smallest estimate (range = 6.25–17.93; Table 1). Some of this variability could be 'noise', in that it is associated with differences in experts' personalities or cognitive styles; but it is also possible that it reflects actual differences in eagle responses to human disturbance as observed by experts in the field.

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Table 1: Distances (m) at which experts (n = 18–19; see text) estimated that relatively sensitive breeding golden eagles are most likely to flush from the nest/noticeably reduce provisioning at the nest/or fail to breed or occupy a nest site in response to various human activities.

Military OHV Activity Hiking Rock Climbing Construction Training Min 91/101/137 91/91/101 91/101/183 101/101/91 101/101/183 Median 457/503/411 366/457/320 457/457/457 457/709/686 549/869/823 Mean 509/572/556 406/534/479 495/542/550 583/648/624 647/756/831 90% 1097/1097/914 805/914/914 914/914/1097 914/1097/1097 1097/1280/1372 95% 1207/1097/1006 1097/1143/914 1097/1097/1097 1554/1097/1097 1372/1372/1408 Max 1554/1372/1097 1143/1372/1097 1143/1372/1143 1609/1207/1207 1811/1408/1646

Table 2: Median distances (m) at which raptor experts in three elicitations estimated that breeding golden eagles would respond to human activities. Only human activities and eagle response metrics included in previous elicitations are included in the table. Median values reported for all elicitations are for nesting phases during which respondents thought eagles would be most responsive to disturbance. For additional comparison, the table also includes the mean distance (m) at which golden eagles in southwestern Idaho flushed from nests or perches in response to motorized and non-motorized recreation (combined).

Expert Elicitations Empirical Suter and Joness Whitfield et USFWS (this Activity Response 1981 al. 2008 elicitation) Spaul 2015 Hiking/walking Flush from nest 333 400 366 OHVs Flush from nest 350 457 Hiking + OHVs Flush from nest 449 OHVs Fail to breed/abandon nest 457 411 Construction Fail to breed/abandon nest 550 686

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A B C

Figure 4: Distances (m) at which experts (n = 18–19; see text) estimated that relatively sensitive breeding golden eagles are most likely to A) flush from the nest, B) noticeably reduce their provisioning rate at the nest, or C) fail to breed or occupy a nest site in response to human activities. The line inside each box indicates the median value, the bottom of the box is the 25th percentile, the top of the box is the 75th percentile, and the error bars indicate the range of estimates.

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We evaluated regional variation in experts' estimates of the distances at which breeding golden eagles respond to human activities. We assigned a respondent to a region if they allocated at least 20 of 100 points to that region in Question 1a. Estimates by 8 experts were included in 1 region, 9 were included in 2 regions, and 2 were included in 3 regions. Median estimates of the most likely distance at which sensitive breeding golden eagles would respond to human disturbance were variable within and among regions, disturbance metrics, and human activities (Table 3). However, there was a tendency for longer median (Table 3) and mean (Figure 5) distances from experts with substantial experience with eagles in the California Coast Ranges and shorter distances for those experienced with eagles in the Interior Mountains and Wyoming Basin/Great Plains. We caution against drawing inferences from this pattern or basing management actions such as protective buffers on it. This pattern could reflect regional variation in experts' views of the effects of human activities on golden eagles or could merely be an artifact of small sample sizes per region.

Table 3: Median distance (m) at which experts (sample sizes in parentheses) estimated that relatively sensitive golden eagles would likely flush from the nest/noticeably reduce provisioning at the nest/or fail to breed or occupy a nest site in response to human activities.

OHV Rock Activity Hiking Climbing Construction Military Training California Coast Ranges (3) 457/823/823 366/732/732 366/640/732 549/914/914 549/914/1097 Great Basin/ Columbia Plateau (9) 457/732/732 366/604/549 457/604/604 457/732/732 640/914/914 Alaska/ Boreal (4) 640/457/366 457/457/274 823/274/366 594/914/914 366/914/914 Southwest Deserts/ Canyonlands (5) 183/549/457 274/457/366 274/640/549 366/732/640 457/823/1097 Wyoming Basin/ Great Plains (6) 320/251/332 274/274/251 229/297/320 343/274/251 384/338/430 Interior Mountains (5) 183/183/283 137/187/160 183/251/283 366/251/283 251/274/526

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Figure 5: Grand means of distances (m) at which experts (sample sizes in parentheses) thought that breeding golden eagles were most likely to respond to human activities by flushing from the nest, noticeably reducing provisioning at the nest, or failing to breed or occupy a nest site (averaged across all activity types in the elicitation: OHV activity, hiking, rock climbing, construction activity, and military training).

Using linear regression, we evaluated variation in experts' responses to Questions 2a–4e in relation to their experience with golden eagles nesting in cliffs/rock outcrops versus trees (Question 1b). We ranked experts by their responses to questions 2a–4e, based on the longest, shortest, and most likely distances at which they thought golden eagles would respond to human activities. The coefficient of determination of the relationship of experts' mean ranks and points allocated to nest substrates was 0.0241 for cliffs/rock outcrops and 0.0240 for trees. In both cases, less than 2.5% of the variation in how experts were ranked was explained by their experience with golden eagles nesting in different substrates. Thus, there was apparently little or no relationship between experts' responses to Questions 2a– 4e and their experience with golden eagles nesting in cliffs/rock outcrops versus trees.

Question 5a (best response metric for determining buffer size). All 19 experts responded to Question 5a. The mean numbers of points (out of 100) allocated to flushing from the nest, noticeably reducing provisioning at the nest, and failing to breed or occupy a nest site were 33.9 (SD = 26.8), 27.3 (17.2), and 38.9 (27.7), respectively. The wide variability in experts' responses to this question may reflect their understanding of tradeoffs in the relative difficulty of detecting a response in the field versus its potential utility as a measure of negative impact. For example, some experts noted in their comments on the questionnaires or during the web-based discussions that flushing from the nest is relatively easy to observe but may not always reflect a negative impact on eagles, whereas a failure to breed or occupy a nest site is a clear negative impact but may be difficult to link to human activities.

Question 5b (most effective type of buffer). All 19 respondents answered Question 5b. Sixteen experts allocated all of their points to one or more of the provided choices and 3 also or instead wrote in a different basis for establishing buffers for breeding golden eagles. Of the provided choices, core area/territory buffers received the most points from all experts combined and fixed buffers around the used nest received the least (Table 4). Two

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respondents wrote in adaptive buffers around all known nests and 1 wrote in a combination of adaptive buffers around all known nests and the core area/territory (Table 4). These results show relatively wide variation among respondents in terms of the specific basis they think is most appropriate for determining buffers.

Watson et al. (2014) found that breeding golden eagles in eastern Washington and Oregon concentrated their activity around alternative nests when away from the used nest, and that most (87%) alternative nests were located within eagles' home range core areas. Based on this finding, we compared respondents' combined allocation of points to buffers based on core areas/territories or all known nests versus those for used nests alone. Nearly 73% of the total points for all experts combined were allocated to buffering large areas that include all known nests and/or the breeding core area or territory, whereas 27% were allocated to buffering around used nests alone (Table 4). Seventeen (89%) respondents allocated 50 or more points (out of 100) to buffers around all known nests or based on nesting core areas or territories, whereas only 2 (11%) allocated 50 or more points to buffering around the used nest alone. Thus, there was strong agreement among experts that buffers would be most effective at protecting breeding golden eagles from disturbance if they encompass more of the home range than just the area around the currently used nest.

Table 4: Combined points allocated by experts (n = 19) to different bases for establishing buffers, in proportion to their relative efficacy at protecting breeding golden eagles from human disturbance.

Basis Points (%) Core Area/Territory 620 (32.6) All Known Nests 525 (27.6) Adaptive Used 305 (16.1) Fixed Used 215 (11.3) Adaptive All Known (write-in) 135 (7.1) Adaptive All Known + Core/Territory (write-in) 100 (5.3) Total 1900 (100) All Known + Core/Territory (adaptive or fixed) 1380 (72.6) Used Nest (adaptive or fixed) 520 (27.4) Total 1900 (100)

Management Considerations

Median values in our results resemble those in previous elicitations, as well as mean values from a recent empirical study (Table 2). Together, this information suggests that 800 m (0.5 mile) buffers recommended in current state guidelines (USFWS 2002, Colorado Division of Wildlife 2008) will often protect golden eagles from human disturbance when they are at or near the used nest. However, experts in our elicitation strongly indicated that buffers based on home range core areas, territories, or the area including all known (used and alternative) nests would be more effective at protecting golden eagles from human disturbance than areas around used nests. We recommend that buffer guidelines for golden eagles be based on the full body of currently available information, as reviewed in the main body of this synthesis, rather than on these elicitation results alone.

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Acknowledgments

This elicitation was coordinated, analyzed, and authored by Dan L. Hansen, Brian Woodbridge, David Leal, Steve Morey, Jeffrey R. Dunk, James W. Watson, and James T. Driscoll. Emily Bjerre provided helpful feedback on the elicitation. The following individuals participated in the elicitation as respondents (alphabetical order): Jim Anderson, Sue Anderson, Peter Bloom, Michael Collopy, Erica Craig, Tim Craig, Ross Crandall, James Driscoll, Rick Gerhardt, Alan Harmata, Frank Isaacs, Kenneth Jacobsen, Michael Kochert, Colleen Lenihan, Stephen Lewis, Mike Lockhart, Carol McIntyre, Robert Oakleaf, Steven Slater, Jeff Smith, Robert Spaul, Dale Stahlecker, and James Watson.

References

Colorado Division of Wildlife. 2008. Recommended buffer zones and seasonal restrictions for Colorado raptors. Available online at: http://cpw.state.co.us/Documents/WildlifeSpecies/LivingWithWildlife/RaptorBufferG uidelines2008.pdf (last accessed 20 July 2015). Delbecq, A.L., A.H. Van de Ven, and D.H. Gustafson. 1975. Group techniques for program planning: A guide to nominal group and Delphi processes. Scott, Foresman and Company, Glenview, Illinois. Drescher, M., A.H. Perera, C.J. Johnson, L.J. Buse, C.A. Drew, and M.A. Burgman. 2013. Toward rigorous use of expert knowledge in ecological research. Ecosphere 4(7): Article 83. Spaul, R.J. 2015. Recreation disturbance to a shrub-steppe raptor: Biological consequences, behavioral mechanisms and management implications. M.S. thesis. Boise State University, Idaho. Speirs-Bridge, A., F. Fidler, M. McBride, L. Flander, G. Cumming, and M. Burgman. 2010. Reducing overconfidence in the interval judgments of experts. Risk Analysis 30(3):512–523. Suter, G.W., II, and J.L. Joness. 1981. Criteria for Golden eagle, ferruginous hawk, and prairie falcon nest site protection. Raptor Research 15(1):12–18. USFWS (U.S. Fish and Wildlife Service). 2002. Utah Field Office guidelines for raptor protection from human and land use disturbances. U.S. Fish and Wildlife Service, Utah Field Office, Salt Lake City. Whitfield, D.P., M. Ruddock, and R. Bullman. 2008. Expert opinion as a tool for quantifying bird tolerance to human disturbance. Biological Conservation 141:2708–2717.

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