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Journal of Mammalogy, 100(6):1941–1953, 2019 DOI:10.1093/jmammal/gyz135 Published online September 18, 2019

Pastoralist activities affect the movement patterns of a large African carnivore, the spotted hyena (Crocuta crocuta)

David S. Green* and Kay E. Holekamp Department of Integrative Biology, Michigan State University, East Lansing, MI 48823 (DSG, KEH) Program in Ecology, Evolutionary Biology, and Behavior, Michigan State University, East Lansing, MI 48823 (DSG, KEH) Downloaded from https://academic.oup.com/jmammal/article/100/6/1941/5571540 by guest on 25 September 2021 Present address of DSG: Institute for Natural Resources, Oregon State University, Corvallis, OR 97331 * Correspondent: [email protected]

Populations of large carnivores are declining in many parts of the world due to anthropogenic activity. Some species of large carnivores, however, are able to coexist with people by altering their behavior. Altered behaviors may be challenging to identify in large carnivores because these animals are typically cryptic, nocturnal, live at low densities, and because changes in their behavior may be subtle or emerge slowly over many years. We studied the effects of livestock presence on the movements of one large carnivore, the spotted hyena (Crocuta crocuta). We fit 22 adult female spotted hyenas with GPS collars to quantify their movements in areas with and without livestock or herders present, in and around a protected area in southwestern Kenya. We investigated anthropogenic, social, and ecological effects on the speed of movement, distances traveled, long-distance movements, and extraterritorial excursions by spotted hyenas. Hyenas living primarily within the protected area, but in the presence of livestock and herders, moved faster, traveled over longer distances, and were more likely to be within their territories than did conspecifics living in areas without livestock and herders. Hyenas of low social rank were more likely than hyenas of high social rank to engage in long-distance travel events, and these were more likely to occur when prey were scarce. The movement patterns of this large African carnivore indicate a flexibility that may allow them to persist in landscapes that are becoming increasingly defined by people.

Key words: anthropogenic disturbance, Crocuta crocuta, East Africa, GPS collars, Mara-Serengeti ecosystem, pastoralism, protected areas

Large carnivores often occupy apex trophic positions in their for real or perceived threats to livestock in North America and natural habitats, and they may limit populations of both sym- Europe (e.g., wolves Canis lupus—Liberg et al. 2012), and patric prey and other predators. However, populations of large hunted for sport in Africa (e.g., lions Panthera leo—Packer carnivores have been declining worldwide (Ripple et al. 2014). et al. 2009, 2010). This persecution has extirpated large carni- The reduction or complete extirpation of large carnivores can vore species from many ecosystems (Ripple et al. 2014). Other have ecosystem-wide consequences due to the removal of the effects of people on large carnivore populations may be indi- top-down control they exert over species at lower trophic levels rect, and these can include habitat loss and reduced prey avail- (Miller et al. 2001; Schmitz et al. 2010; Ripple et al. 2014). ability due to overharvesting (Ripple et al. 2014). The indirect Declining numbers of large carnivores can effect changes in bi- effects of humans on large carnivores have been harder to elu- odiversity (Estes et al. 2011) and disease prevalence (Levi et al. cidate than direct effects because they may elicit only subtle 2012), and often have negative economic consequences at both changes in the carnivores themselves, and because they may local and national levels (Taylor et al. 2016). take years to manifest. The negative effects of people on large carnivores are a factor Protected areas can help prevent conflicts between humans contributing to their declining numbers. For example, large car- and carnivores (Packer et al. 2013; Bauer et al. 2015), and most nivores are poached for their body parts in Asia (e.g., tigers populations of large carnivores currently reside within or ad- Panthera tigris—Dinerstein et al. 2007), killed in retaliation jacent to protected areas. However, edge effects associated

1941 1942 JOURNAL OF MAMMALOGY with nearby human populations, and human pressures inside of livestock elicits changes in the movement patterns of spotted the protected areas, have cast considerable doubt on the effi- hyenas in areas where they are being disturbed by people and cacy of protected areas as sanctuaries for carnivore conserva- livestock, 2) variation in hyena movements due to livestock is tion (Woodroffe and Ginsberg 1998; Wittemyer et al. 2008; also affected by social rank, and 3) certain ecological condi- Loveridge et al. 2017). For example, anthropogenic disturbance tions (e.g., rainfall, temperature, moonlight, prey availability) within protected areas can affect carnivore community struc- affect the movements of spotted hyenas, regardless of their so- ture (Baker and Leberg 2018; Farr et al. 2019) and influence cial rank or the presence of livestock. We also inquired whether their use of space (Olson et al. 2018; Ladle et al. 2019). In some the presence of livestock within the territorial boundaries of a areas of the world, conflict between carnivores and livestock spotted hyena clan increases the probability that hyenas spend or the people protecting them is a major cause of the decline time outside those same boundaries. Downloaded from https://academic.oup.com/jmammal/article/100/6/1941/5571540 by guest on 25 September 2021 in carnivore numbers (Woodroffe and Ginsberg 1998; Ripple et al. 2014), even within protected areas (Green et al. 2018). Aside from retaliatory killings, the mere presence of livestock Materials and Methods within protected areas can affect carnivore ecology and be- Study site.—From April 2012 through November 2014, we havior (Soofi et al. 2018; Broekhuis et al. 2019). Thus, under- studied the movement patterns of spotted hyenas within and standing how the activity of pastoralists may be influencing the around the Masai Mara National Reserve (henceforth, “the behaviors of large carnivores represents an important area of Reserve”) in southwestern Kenya (Fig. 1). The Reserve is cov- research due to increasing numbers of both humans and live- ered primarily with open grassland interspersed with riparian stock, particularly in developing nations. habitat along seasonal watercourses. The Reserve has histori- Behavior is the first line of defense for many species to cope cally supported many resident herbivore and carnivore species with changing environments (Sih 2013; Wong and Candolin year-round, and it is also visited seasonally by migrating herbi- 2015; Sih et al. 2016), and large carnivores often modify their vores from the Serengeti National Park to the south (Bell 1971; behaviors to mitigate the negative effects of people. It has been Sinclair and Norton-Griffiths 1979), and the Loita Plains to the hypothesized that the slow life histories, large body sizes, and northeast (Stelfox et al. 1986). The only permanent river in the complex habitat requirements of large carnivores might pre- Reserve, the Mara River, also serves as the boundary between vent them from finding ways to coexist with humans (Cardillo two different management agencies operating on its eastern 2005). In contrast to predictions of this hypothesis, empirical and western sides, respectively (Fig. 1). The eastern side of the work has shown that some large carnivores living in human- Reserve is managed by the Narok County Government. Within dominated landscapes can alter their behaviors in subtle ways the eastern side of the Reserve, the Talek region, in particular, to coexist with people. Some species shift their activity pat- is an area near the border that in recent decades has been sub- terns to become more nocturnal (Gaynor et al. 2018), increase jected to an exponential increase in the number of livestock their vigilance (Pangle and Holekamp 2010), modify how they present inside the Reserve (Boydston et al. 2003a; Kolowski navigate landscapes occupied by humans (Oriol-Cotterill et al. and Holekamp 2009; Green et al. 2018, 2019b). Formation of 2015), and change their space use to avoid areas of human ac- several private conservancies north of the Reserve (Fig. 1) has tivity altogether (Van Dyke et al. 1986; Schuette et al. 2013). created an island of land, called Talek town and environs, occu- Here, we used GPS collar technology to examine the ways in pied by several thousand Masai pastoralists and their livestock. which the movements of wild spotted hyenas (Crocuta crocuta) Herders from Talek communities accompanying their livestock were affected by livestock presence, while also accounting for inside the Reserve are armed with weapons (e.g., clubs, spears), other socio-ecological factors that might affect hyena move- and conflicts between herders and hyenas stemming from live- ments. Spotted hyenas are gregarious large carnivores that ex- stock depredation now represent the greatest source of mor- hibit remarkable plasticity in many aspects of their behavior tality for hyenas on the eastern side of the Reserve (Pangle and (Holekamp and Dloniak 2010). Spotted hyenas can cope with Holekamp 2010). In contrast to the eastern side, the western increasing human populations by shifting their activity patterns portion of the Reserve is managed by the Mara Conservancy, to become more nocturnal (Kolowski et al. 2007), and by using where no humans on foot or livestock are allowed (Green dense vegetation to provide cover from people (Boydston et al. et al. 2018). By comparing movements of spotted hyenas be- 2003a; Kolowski and Holekamp 2009). These behavioral adap- tween sides of the Reserve, we were able to exploit this nat- tations allow hyenas to persist in areas where other large carni- urally occurring variation in livestock presence to understand vores decline due to people (Green et al. 2018). Furthermore, its effects along with other variables likely to affect hyena spotted hyenas live in large social groups called “clans,” each of movements. which is structured by a strict, linear dominance hierarchy; it is Study subjects.—Spotted hyena clans are fission–fusion possible that differential priority of access to resources within a societies; clan members advertise and defend a communal clan may cause individual hyenas to respond to anthropogenic territory by scent marking, latrines and agonistic encounters disturbances in different ways. Thus, spotted hyenas may be with neighboring clans (Kruuk 1972; Mills 1990; Henschel and particularly useful in illuminating how pastoralism is effecting Skinner 1991; Boydston et al. 2001). To investigate the effects changes in the behaviors of large carnivores. The hypotheses we of livestock presence on hyena movements, we studied indi- investigated in the current research suggest that 1) the presence vidual members of three hyena clans (Fig. 1; Table 1) as part GREEN AND HOLEKAMP—PASTORALISTS AFFECT SPOTTED HYENA BEHAVIORS 1943

of a longitudinal study of the behavioral ecology of this species that began in 1979 (Frank 1986; Holekamp et al. 2012). Two study clans were located in the relatively pristine western side of the Reserve (“Serena North” and “Serena South” clans), and one clan was located in the Talek region on the eastern side of the Reserve (the “Talek West” clan; Fig. 1; see below for calculation of territory boundaries). Serena North and Serena South clans experienced no livestock whatsoever within their territories, whereas Talek hyenas were exposed to livestock and herders in their territory on a daily basis throughout the study Downloaded from https://academic.oup.com/jmammal/article/100/6/1941/5571540 by guest on 25 September 2021 period (Green et al. 2018, 2019b). Animals in each clan were individually identified by their spot patterns, ear damage, and other unique features. Each hyena clan is organized by a linear dominance hierarchy in which the highest-ranked individual is the alpha female, and social rank influences the space use patterns of individual clan members (Boydston et al. 2003b; Höner et al. 2005). Standardized ranks were calculated here for all clan members in each of our three study clans, ranging from 1 to −1, based on the outcomes of dyadic aggressive interactions (Holekamp and Smale 1993); a value of 1 was assigned to the highest-ranking female in the clan and a value of −1 was assigned to the lowest. Monitoring the movements of spotted hyenas.—Our subjects were 22 parous female spotted hyenas of either low or high social ranks (Table 1; Supplementary Data SD1). That is, females ranked −1 to −0.33 were considered to be low-ranking, and those ranked 0.33 to 1 in the dominance hierarchy of each clan were considered to be high-ranking; mid-ranking hyenas were not considered here. We anesthetized these females with Telazol (6.5 mg/kg) administered in a plastic dart fired from

a CO2-powered rifle (Telinject Inc., Saugus, California), and fitted them with GPS collars (Vectronic Aerospace, Berlin, Germany) following ASM guidelines (Sikes et al. 2016); this work was approved by the Michigan State University Institutional Animal Care and Use Committee most recently in Approval # 05/14/087-00. We set the collars to record GPS locations of each hyena at hourly intervals from 1600 to 1000 h, and once again at 1300 h. We only used locations obtained ≥ 24 h after immobilization to ensure that hyenas were fully re- covered from anesthesia. We focused on four metrics of the movements of spotted hyenas to determine how livestock presence influences these large carnivores: 1) speed of movement, 2) distance traveled, 3) the probability that individuals would engage in long-distance travel events, and 4) the probability that individuals would engage in extraterritorial movements. Speeds (in m/h) were

Reserve and the Serengeti National Park to the south in Tanzania. The gray-shaded region within the protected area indicates the “Mara Triangle,” the region of the Reserve experiencing comparatively little disturbance and no livestock incursions. The private wildlife conser- Fig. 1.—Locations of the territories of the three study clans, and loca- vancies north and east of the Reserve are bordered in white lines. (A) tions of adult female hyenas (Crocuta crocuta) fitted with GPS collars, The territory boundaries of our three study clans of spotted hyenas. collected in and around the Masai Mara National Reserve, Kenya. The The locations of our two weather stations are indicated with green GPS locations and territories are color-coded by clan; Serena North is stars. Talek town is indicated by a blue circle. (B) All GPS locations colored in yellow, Serena South in orange, and Talek West in red. The of high-ranking spotted hyenas. (C) All GPS locations of low-ranking solid line indicates the boundary between the Masai Mara National spotted hyenas. 1944 JOURNAL OF MAMMALOGY

Table 1.—Salient characteristics of the Serena North, Serena South, and Talek West clans of spotted hyenas (Crocuta crocuta) monitored in the current study based on data collected in 2013. Standard errors are presented in parentheses.

Parameter Serena North Serena South Talek West Mean monthly clan sizea 51.42 (0.87) 39.25 (1.34) 113.00 (1.80) Mean monthly density of hyenasb 1.13 (0.02)/km2 1.44 (0.05)/km2 1.47 (0.02)/km2 Hyenas collaredc 5H, 3L 4H, 2L 4H, 4L Mean distances traveledd 10.83 (1.47) km 9.99 (1.27) km 13.04 (1.85) km Mean distances traveled by high-ranking hyenasd 10.97 (0.18) km 9.65 (0.17) km 12.93 (0.14) km Mean distances traveled by low-ranking hyenasd 10.6 (0.24) km 10.38 (0.19) km 13.17 (0.21) km Territory sizee 45.64 km2 27.28 km2 76.8 km2 Livestockf 0 0 2,218.85 (240.35) Downloaded from https://academic.oup.com/jmammal/article/100/6/1941/5571540 by guest on 25 September 2021 a The mean number of hyenas, including cubs. b The mean number of hyenas per km2 of territory. c The number of hyenas collared during this study. “H” and “L” indicate the number of animals collared of high and low social rank, respectively. d The mean distance traveled by hyenas for which we had all 19 possible locations in a day. e The area of a 95% isopleth of a kernel utilization distribution. f The mean number of livestock (i.e., cattle, sheep, goats) counted per livestock census each month within territory boundaries. calculated between successive hourly locations in the move- The conservancies vary in their management, and several of ment paths of the hyenas with the package “adehabitatLT” in them appeared to have considerable numbers of livestock R (Calenge 2006; R Core Team 2017). We calculated distance grazing in them regularly, although we had no access to data traveled as the total distance traveled (in km) by a single hyena documenting livestock numbers there. Although territories of when its collar recorded all 19 possible locations from 1600 to the Serena North and Serena South clans were located entirely 1000 h. When we recorded all 19 possible locations, we also within the Reserve (area of Serena North = 45.64 km2; area of determined whether this was a long-distance travel event to Serena South = 27.28 km2), 23% (18 km2) of the Talek West see if hyenas occasionally took long-distance trips outside of clan territory extended beyond Reserve boundaries to the north their territories. We defined a long-distance travel event as any (Fig. 1; total area of Talek West = 76.8 km2). time during which the total distance traveled was greater than Environmental data.—The only hyenas exposed to livestock or equal to 2 SDs from the mean total distance traveled by all at any time in their territory during our study were members collared hyenas. of the Talek West clan. In the only full calendar year of study We determined territory boundaries for each of our three (2013), 2,218.85 ± 240.35 (monthly mean ± SE) livestock were study clans by calculating the 95% isopleth of a kernel utiliza- herded into the Reserve each evening in the Talek region to tion distribution calculated using the “ad hoc” method from all graze there throughout the night (estimated by recording all GPS collar locations collected in 2013 with the “adehabitatHR” livestock seen while systematically driving throughout the package in R (Calenge 2006). We used locations from 2013 to territory twice per month between 1600 and 2000 h—Green calculate territory boundaries because it was the only full year et al. 2018, 2019b). Therefore, we inquired how movements of that we collected locations from hyenas in all clans, including Talek West hyenas were affected by livestock presence within females of both low and high social rank. Although the number their territory by comparing them to Serena North and Serena of hyenas collared in each clan varied along with their duration South hyenas, which we used as controls because movements of deployment (Table 1; Supplementary Data SD1), we used of hyenas in those two clans could not be affected by livestock data from all individuals to calculate territory sizes because this or herders in their territories. To disentangle the effects of live- represents the most complete picture of the defended communal stock presence from other abiotic or biotic effects, we meas- territory. However, because the Talek West clan contained pro- ured temperature, rainfall, moonlight, and prey availability portionally more collared low-ranking hyenas than other clans, throughout the study. We recorded temperature in two ways: we also calculated territory sizes based on data from only two we set the GPS collars to record ambient temperature hourly (± high-ranking and two low-ranking females from each clan (see 1°C) at each hyena’s location, and we also recorded the daily Supplementary Data SD2), but found that these territory sizes maximum temperature in °C at two weather stations in the did not differ appreciably from those calculated using all col- Reserve (Fig. 1A). We used the hourly temperature from the lared individuals per clan. collars and the daily maximum temperatures from our weather For all GPS locations, we determined whether hyenas were stations to determine their influences on behaviors that were located within their clan’s territory. Hyenas rarely traveled out- measured hourly (e.g., speed) or throughout the day (e.g., dis- side of the Reserve and into the Serengeti National Park to the tance traveled), respectively. We also recorded the amount of south in Tanzania (n = 12; < 0.01% of all locations); we con- daily rainfall (in mm) at our weather stations. Both maximum sidered these locations to be inside the Reserve for all analyses daily temperature and daily rainfall values were assigned to because conditions in the northern Serengeti resemble condi- members of the hyena clans that lived closest to our weather tions inside the Masai Mara National Reserve. By contrast, we stations. The percentage of moon that illuminated each night considered any locations north or west of the Reserve to be was obtained from the United States Naval Observatory (http:// outside the Reserve, even if they fell in private conservancies. aa.usno.navy.mil/data/docs/MoonFraction.php). All locations GREEN AND HOLEKAMP—PASTORALISTS AFFECT SPOTTED HYENA BEHAVIORS 1945 that were obtained when the moon added extra illumination to distances that hyenas traveled (in km) and whether or not hy- otherwise dark times (i.e., between sunset and sunrise and be- enas engaged in a long-distance travel event as a function of tween moonrise and moonset) were assigned a value between 1) livestock, 2) social rank, 3) rainfall, 4) maximum daily tem- 0 and 1 corresponding to the proportion of the moon that was perature, 5) prey availability, and interactions between 6) social illuminated on that night (i.e., full moon = 1, new moon = 0). rank and prey availability and 7) social rank and livestock. We We assigned a moon value of 0 to dark hours before moonrise included these two interactions to inquire whether animals of and after moonset. low social rank traveled greater distances than animals of high Hyenas in the Reserve consume a wide diversity of prey social rank during periods of low prey availability, and whether (Cooper et al. 1999), but prey availability varies consider- the presence of livestock would disproportionately affect the ably throughout the year. The annual migration of wildebeest distances traveled by low-ranking animals. We also calculated Downloaded from https://academic.oup.com/jmammal/article/100/6/1941/5571540 by guest on 25 September 2021 (Connochaetes taurinus) and zebra (Equus quagga) represents a rectangular convex hull encompassing each territory using the a temporary, seasonal increase in available prey for hyenas on Minimum Bounding Geometry tool in ArcGIS (ESRI 2018), both sides of the Reserve. We assessed the effects of prey avail- and included its length as an eighth term in these analyses to ability on the movement patterns of spotted hyenas by com- account for any variation in distances traveled as a function of paring movements recorded during the annual high prey period territory size. In regard to distances traveled, we performed this (June–October) with those recorded during the annual period analysis using log-transformed data and we nested calendar of relatively low prey abundance (November–May—Holekamp date within hyena identity and coded this as a random effect et al. 1996; Cooper et al. 1999; Green et al. 2019b). on the intercept to account for any variation in the distances Effects on movement speed of hyenas.—To understand how traveled not explained by our predictor variables. Data were livestock presence affects the movements of spotted hyenas, limited for the long-distance travel events (n = 143 during this we first modeled the speed at which hyenas travelled (in m/h) study), so we only coded hyena identity as a random effect on between successive points as a function of 1) clan member- the intercept in this analysis. We used a Gaussian distribution ship, 2) social rank (i.e., low or high), 3) whether or not the for the distances traveled and a binomial distribution for the second location in the series was inside the formal bound- probability of engaging in a long-distance travel event. aries of the Reserve, both 4) hour and 5) hour2 fit as time- Effects on extraterritorial movements by hyenas.—To de- series variables to investigate the effect of time of day, 6) prey termine how livestock incursions into the Reserve affected the availability (i.e., low or high), 7) rainfall, 8) hourly ambient probability that hyenas would move outside their territorial temperature, 9) moonlight, as well as interactions between boundaries, we modeled whether or not individuals from all 10) prey availability and social rank, 11) livestock and social clans were located inside the boundaries of their territories as rank, 12) livestock and hour, and 13) livestock and moonlight. a function of 1) the presence of livestock, 2) social rank (i.e., We included the hour and the hour2 terms to account for the low or high), both 3) hour and 4) hour2 fit as time-series vari- crepuscular and nocturnal nature of spotted hyena activity ables to assess effects of time of day, 5) prey availability (i.e., (Kruuk 1972; Kolowski et al. 2007), and to assess variation low or high), 6) rainfall, 7) ambient temperature, 8) moonlight, in activity throughout the day. We included the four interac- and interactions between 9) prey availability and social rank, tion terms to test hypotheses suggesting, respectively, that 10) livestock and prey availability, and between 11) livestock prey availability and livestock might disproportionately affect and social rank. We included these interactions to investi- movements by animals of low social rank, that the presence of gate whether animals of low social rank, or those living with livestock might interact with the circadian rhythms in move- livestock, were more likely to be found inside their territo- ments of spotted hyenas, and that more ambient light from rial boundaries during periods of high prey availability, and the moon might affect how hyenas interact with livestock and whether animals of low social rank would be disproportion- herders. We nested calendar date within hyena identity and ately affected by the presence of livestock. We coded hyena coded this as a random effect on the intercept to account for identity as a random effect on the intercept to account for any any variation in the movement patterns of spotted hyenas not differences in territory use not explained by our covariates, and explained by our predictor variables; we performed this anal- we used a binomial distribution. ysis using log-transformed data and a Gaussian distribution. Model parameterization and performance.—We coded There was no significant difference between the two study the four models outlined above as generalized linear mixed- clans that had no livestock present within their territories (i.e., effects models and fit them in the “glmmPQL” package from Serena North and Serena South) in our models (P > 0.10), the “MASS” library in R v. 3.4.2 (Venables and Ripley 2002; so we combined data from these two clans here and in all R Core Team 2017). We standardized the covariates of rainfall subsequent analyses; we created the binary variable “live- and temperature in all analyses to have a mean of 0 and a SD stock,” indicating simply whether or not hyenas were exposed of 1. Prior to analysis, all covariates were tested for colline- to livestock within their territory (Serena North and Serena arity using Pearson’s correlation coefficients, but no covariates South = 0, Talek West = 1). were significantly correlated (Pearson’s correlation coefficient Effects on distances traveled by hyenas.—We performed < |0.6|). We used an α of 0.05 to determine whether specific two analyses to investigate how the presence of livestock af- parameters had significant effects on movement patterns. We fected the distances traveled by hyenas. We modeled the total present model fit as the conditional and marginal Pseudo-R2, 1946 JOURNAL OF MAMMALOGY calculated from the “MuMIn” package in R (Barton 2017). all significantly affected the speed of hyena movements. The Descriptive statistics are presented as mean estimates ± 1 SD, effects of time of day and moonlight on movement speed dif- and all results are presented as the mean parameter estimate fered between areas with and without livestock. The speed of and standard error (SE) on the scale for which the analysis was hyenas exposed to livestock remained elevated throughout the performed. night, whereas the speed of hyenas not exposed to livestock gradually decreased throughout the night (Fig. 2A). Moonlight increased the speed of hyenas exposed to livestock, but did not Results affect the speed of hyenas not exposed to livestock as greatly We collected a total of 138,403 hourly locations from 22 adult (Fig. 2B). High-ranking hyenas traveled at faster speeds than female hyenas (mean number of locations ± SD per hyena: low-ranking hyenas in the presence of livestock, but not where Downloaded from https://academic.oup.com/jmammal/article/100/6/1941/5571540 by guest on 25 September 2021 6,291.1 ± 2,909.4) on 952 different days (mean number of livestock were absent (Fig. 2C). Hyenas also traveled more days ± SD per hyena: 497.4 ± 180.7) between April 2012 and quickly outside Reserve boundaries than inside the Reserve (es- November 2014. We collected data from a total of 4,558 collar timate ± SE on the log scale = 0.4 ± 0.03, P < 0.01; Table 2); days when collars recorded all 19 possible locations (mean when hyenas were outside the Reserve they traveled on average number of days with all 19 locations ± SD per hyena: 207.2 ± at 914.2 ± 891.8 m/h, whereas they traveled at 655.7 ± 859 m/h 141). Females from all three monitored clans travelled out- inside the Reserve. The speed at which hyenas traveled was side their territory boundaries and outside Reserve boundaries also predicted by time of day (hour estimate ± SE on the log during our study (Figs. 1B and 1C), and this accounted for 33% scale = 0.33 ± 0.01, P < 0.01; hour2 estimate on the log scale ± and 7% of all locations, respectively. Because only 7% of all SE = −0.02 ± 4.35E-04, P < 0.01); movement speed of hyenas locations fell outside both territory and Reserve boundaries, was lowest in the early evening and late morning, and highest the fraction of that 7% falling within the conservancies was during the middle of the night (Fig. 2A). Hyenas traveled more clearly very small. We observed a total of 143 long-distance slowly when temperatures were higher than average (estimate ± travel events by collared female hyenas (mean distance trav- SE on the log scale = −0.32 ± 0.01, P < 0.01), but they moved eled during a long-distance travel event ± SD: 25.2 ± 3.1 km), more quickly when prey were abundant than when they were including one instance when one hyena traveled > 24 km from scarce (estimate ± SE on the log scale = 0.34 ± 0.03, P < 0.01; the Reserve to the north (Fig. 1C). Hyenas in our study also oc- Fig. 2D). Hyenas also moved more quickly during periods of casionally crossed the Mara River. heavy rainfall (estimate ± SE on the log scale = 0.02 ± 0.01, Hyenas living in regions with daily livestock presence trav- P = 0.02) and brighter moonlight (estimate ± SE on the log eled significantly faster than those in regions without live- scale = 0.1 ± 0.03, P < 0.01). Speed of travel was also influenced stock (estimate ± SE on the log scale = 0.44 ± 0.12, P < 0.01; by the interaction between social rank and prey availability (es- Table 2); hyenas living in regions with daily livestock in their timate ± SE on the log scale = −0.2 ± 0.04, P < 0.01; Fig. 2D); territory traveled on average 761.6 ± 914 m/h, whereas those high-ranking hyenas traveled at faster speeds than low-ranking without livestock in their territory traveled at 609.5 ± 820.2 hyenas during periods of high prey availability, but not when m/h. Interactions between presence of livestock and time of day prey were scarce (Fig. 2D). Nevertheless, there was consider- (estimate ± SE on the log scale = 0.02 ± 2.68E-03, P < 0.01; able variation in movement speeds unexplained by our predictor 2 2 Fig. 2A), between livestock presence and moonlight (estimate variables (R marginal = 0.13, R conditional = 0.22). ± SE on the log scale = 0.15 ± 0.04, P < 0.01; Table 2; Fig. Hyenas living in areas with livestock traveled significantly 2B), and between presence of livestock and social rank (esti- farther than hyenas living in regions without livestock (estimate mate ± SE on the log scale = −0.51 ± 0.18, P = 0.01; Fig. 2C) ± SE on the normal scale = 0.38 ± 0.11, P < 0.01); on average,

Table 2.—Results from the generalized linear mixed-effects model predicting speed (m/h) of movement by spotted hyenas (Crocuta crocuta) inside and near the Masai Mara National Reserve, Kenya. Parameter estimates, standard errors (SEs), 95% confidence intervals (CIs), degrees of freedom (df), T-, and P-values are displayed. Parameter estimates, SEs, and CIs are presented on the log scale. Parameter estimates, excluding the intercept, are indicated in bold font if the P-value was < 0.05. Here, “E” refers to scientific notation (e.g., multiply by 10 to the power of).

Parameter Value (SE) CI df T P-value Intercept 3.87 (0.08) 3.72, 4.02 126127 51.23 < 0.01 Livestock (Yes) 0.44 (0.12) 0.18, 0.7 18 3.59 < 0.01 Rank (Low) 0.22 (0.11) −0.02, 0.45 18 1.92 0.07 Outside Reserve 0.4 (0.03) 0.33, 0.46 126127 12.05 < 0.01 Hour 0.33 (0.01) 0.31, 0.35 126127 38.81 < 0.01 Hour2 −0.02 (4.35E-04) −0.03, −0.02 126127 −56.48 < 0.01 Prey (High) 0.34 (0.03) 0.29, 0.39 10794 12.7 < 0.01 Rain 0.02 (0.01) 0, 0.04 10794 2.4 0.02 Temperature −0.32 (0.01) −0.34, −0.3 126127 −33.37 < 0.01 Moonlight 0.1 (0.03) 0.04, 0.15 126127 3.57 < 0.01 Rank (Low) × Prey (High) −0.2 (0.04) −0.28, −0.12 10794 −4.85 < 0.01 Livestock (Yes) × Rank (Low) −0.51 (0.18) −0.88, −0.13 18 −2.83 0.01 Livestock (Yes) × Hour 0.02 (2.68E-03) 0.02, 0.03 126127 8.86 < 0.01 Livestock (Yes) × Moonlight 0.15 (0.04) 0.08, 0.23 126127 3.87 < 0.01 GREEN AND HOLEKAMP—PASTORALISTS AFFECT SPOTTED HYENA BEHAVIORS 1947 Downloaded from https://academic.oup.com/jmammal/article/100/6/1941/5571540 by guest on 25 September 2021

Fig. 2.—The significant interaction effects on speed of hyena (Crocuta crocuta) movement between (A) exposure to livestock and time of day, (B) exposure to livestock and moonlight, (C), exposure to livestock and social rank, and (D) prey availability and social rank. Means ± SE are presented in all figures, and the hours of darkness are shaded in gray in (A). hyenas living with livestock traveled 13 ± 5.1 km per day, and most of the variation was explained by hyena identity and 2 2 whereas those living without livestock traveled 10.4 ± 5.1 km. calendar date (R marginal = 0.06, R conditional = 0.89). Females also traveled greater distances during periods of high Hyenas of low social rank were more likely than high-ranking prey availability (estimate ± SE on the normal scale = 0.14 ± hyenas to engage in long-distance travel events (estimate ± SE 0.02, P < 0.01), and showed a trend toward traveling greater on the logit scale = 1.12 ± 0.345, P < 0.01). High prey avail- distances during periods of heavy rainfall (estimate ± SE on ability also increased the probability of engaging in long- the normal scale = 0.02 ± 0.01, P = 0.05), or if they were of distance travel (estimate ± SE on the logit scale = 0.75 ± 0.3, low social rank (estimate ± SE on the normal scale = 0.16 ± P < 0.01), but this interacted with social rank. During periods 0.08, P = 0.05). The interaction between prey availability and of low prey availability compared to when prey were abundant, social rank was also significant (estimate ± SE on the normal low- and high-ranking hyenas were more likely and less likely scale = −0.12 ± 0.04, P < 0.01; Fig. 3); low-ranking hyenas trav- to engage in long-distance travel, respectively (social rank × eled shorter distances than high-ranking hyenas during periods prey availability estimate ± SE on the logit scale = −0.86 ± of low prey availability, but the opposite pattern occurred during 0.37, P = 0.02; Fig. 4). Hyenas with larger territories were more periods of high prey availability (Fig. 3). The distances hyenas likely to engage in long-distance travel (estimate ± SE on the traveled were not predicted by any other variables (Table 3), logit scale = 0.43 ± 0.1, P < 0.01), but no other factors tested 1948 JOURNAL OF MAMMALOGY affected the probability of hyenas engaging in a long-distance territories at night than during daylight hours (hour estimate ± travel event, and the random effects explained very little varia- SE on the logit scale = −0.12 ± 0.02, P < 0.01; hour2 estimate 2 2 tion (Table 3; R marginal = 0.21, R conditional = 0.21). ± SE on the logit scale = 7.72E-03 ± 8.51E-04, P < 0.01). High- Female hyenas exposed to livestock were more likely to be lo- ranking females were more likely than low-ranking females to be cated inside their territorial boundaries than were hyenas living in located inside their territorial boundaries (estimate ± SE on the the absence of livestock (estimate ± SE on the logit scale = 1.54 ± logit scale = −0.77 ± 0.3, P = 0.02). Warmer than average tem- 0.33, P < 0.01; Table 4). Hyenas were less likely to be inside their peratures also increased the probability that hyenas would be located inside their territories (temperature estimate ± SE on the logit scale = 0.15 ± 0.02, P < 0.01; Table 4). Hyenas were more likely to be found outside their territories when prey availability in the Downloaded from https://academic.oup.com/jmammal/article/100/6/1941/5571540 by guest on 25 September 2021 Reserve was high (estimate ± SE on the logit scale = −0.36 ± 0.05, P < 0.01; Table 4). Interactions between the presence of livestock and social rank and between social rank and prey availability also affected the probability that hyenas would be located inside their territories (livestock present × low social rank estimate ± SE on the logit scale = −2.01 ± 0.49, P < 0.01; low social rank × high prey estimate on the logit scale ± SE = 0.26 ± 0.06, P < 0.01; Table 4; Fig. 5). Hyenas of low social rank were more likely to be inside of their territory in areas without livestock (Fig. 5A). Hyenas of low social rank were more likely to be inside of their territory when prey were scarce than when they were abundant (Fig. 5B). Neither moonlight, rainfall, nor the interaction between livestock presence and prey had a significant effect on extraterritorial movements by hyenas (P > 0.1; Table 4). Despite finding so many significant effects of monitored variables, a great deal of unexplained variation 2 2 remained in our data set (R marginal = 0.22, R conditional = 0.28).

Fig. 3.—The significant interaction effect P( < 0.05) between prey Discussion availability and social rank on distances hyenas (Crocuta crocuta) traveled. The means ± SE distances are presented, separated by Our results indicate that the presence of livestock appears to af- periods of low and high prey availability and for hyenas of low and fect the movement patterns of female spotted hyenas. Females high social rank. moved faster and traveled farther in areas where livestock were

Table 3.—Results from the generalized linear mixed-effects models that predicted distances traveled by spotted hyenas (Crocuta crocuta) and the probability they had a long-distance travel event. Parameter estimates, standard errors (SEs), 95% confidence intervals (CIs), degrees of freedom (df), T-, and P-values are displayed. We present parameter estimates, SEs, and CIs on the normal scale for distance, and on the logit scale for the probability of long-distance travel events. Parameter estimates, not including the intercept, are indicated in bold font if the P-value was < 0.05.

Parameter Value (SE) CI df T P-value Distance Intercept 8.94 (0.22) 8.5, 9.38 4450 39.92 < 0.01 Livestock (Yes) 0.38 (0.11) 0.15, 0.6 17 3.49 < 0.01 Rank (Low) 0.16 (0.08) 0, 0.32 17 2.07 0.05 Rain 0.02 (0.01) 0, 0.04 4450 1.99 0.05 Temperature 0.02 (0.01) −0.01, 0.04 4450 1.33 0.18 Prey (High) 0.14 (0.02) 0.09, 0.18 4450 5.43 < 0.01 Territory size 0 (0.02) −0.04, 0.05 17 0.15 0.88 Rank (Low) × Prey (High) −0.12 (0.04) −0.2, −0.05 4450 −3.21 < 0.01 Rank (Low) × Livestock (Yes) −0.23 (0.12) −0.48, 0.02 17 −1.94 0.07 Long-distance travel events Intercept −9.46 (1.19) −11.8, −7.12 4450 −7.93 < 0.01 Livestock (Yes) −0.76 (0.39) −1.59, 0.06 17 −1.95 0.07 Rank (Low) 1.12 (0.35) 0.39, 1.86 17 3.23 < 0.01 Rain 0.05 (0.08) −0.11, 0.21 4450 0.56 0.58 Temperature 0.13 (0.11) −0.08, 0.33 4450 1.21 0.23 Prey (High) 0.75 (0.3) 0.17, 1.34 4450 2.51 0.01 Territory size 0.43 (0.1) 0.22, 0.63 17 4.36 < 0.01 Rank (Low) × Prey (High) −0.86 (0.37) −1.58, −0.14 4450 −2.35 0.02 Rank (Low) × Livestock (Yes) 0.61 (0.36) −0.15, 1.37 17 1.7 0.11 GREEN AND HOLEKAMP—PASTORALISTS AFFECT SPOTTED HYENA BEHAVIORS 1949 grazed than in areas without livestock. The Talek West hyena exponentially in the vicinity of Talek town over the last two clan, which is exposed to livestock daily inside the Reserve, decades (Bedelian and Ogutu 2017). The very presence of the must also cope with an expanding population of Masai pas- northern conservancies, and their better enforcement of grazing toralists inhabiting the area sandwiched between the Reserve regulations than in the Reserve itself, may be driving livestock and the private conservancies to the north (Lamprey and Reid into the Reserve that would otherwise be grazing north of the 2004; Green et al. 2019b); numbers of livestock have increased Reserve. Now that livestock are also being herded daily into the Reserve for access to grazing year-round (Boydston et al. 2003a; Butt 2014; Green et al. 2018, 2019b), the potential for contact between large carnivores and people over livestock depredation is high both inside and outside Reserve boundaries. Downloaded from https://academic.oup.com/jmammal/article/100/6/1941/5571540 by guest on 25 September 2021 Although we do not know why hyenas moved at faster speeds or travelled over longer distances in areas with livestock, it is likely that these altered behaviors stem from direct and indirect exposure to people. No previous research has used GPS collars to document the effects of proximity to humans or livestock on the movement patterns of spotted hyenas, but research on African lions has indicated that, like our hyena subjects, lions move faster in areas where they are more likely to come into contact with people (Oriol-Cotterill et al. 2015). As with lions, we hypothesize that spotted hyenas in the current study moved at faster speeds and travelled farther in areas with high potential for direct conflicts with people because they are either being actively persecuted, or they are using speed and distance to avoid contact with humans. In any case, these longer and faster movements are likely to incur considerable extra energetic costs for the hyenas exposed to livestock and other forms of human activity (Houston et al. 2012). However, it is difficult to understand precisely how the indirect effects of people in this environment are influencing movement patterns of spotted hyenas. Previous research has indicated that there are fewer lions in the Reserve where livestock are present (Green et al. 2018; Farr et al. 2019), most likely stemming from direct conflicts with people. Thus, hyenas in this area Fig. 4.—The significant interaction effect P( < 0.05) of social rank appear to be undergoing a competitive release, and this may also and prey availability on the probability of hyenas (Crocuta crocuta) influence their movements. Future research should investigate engaging in a long-distance travel event. We present the proportion of all times hyenas traveled long distances, partitioned into periods how movement patterns of hyenas are influenced by competition of high and low prey availability, and shown for hyenas of high and with lions and other sympatric carnivores. low social rank. Periods of high prey availability (i.e., migratory herds Female spotted hyenas of all social ranks were recorded present; June–October) are indicated with white bars and gray bars traveling outside their territories. Adult female hyenas of low indicate periods of low prey availability (i.e., migratory herds absent; social rank, however, tended to range more widely than higher- November–May). ranking females, most likely to avoid intraspecific competition

Table 4.—Results from the generalized linear mixed-effects model predicting the probability that hyenas (Crocuta crocuta) would be located inside their territory. Parameter estimates, standard errors (SEs), 95% confidence intervals (CIs), degrees of freedom (df), T-, and P-values are displayed. We present the parameter estimates, SEs, and CIs on the logit scale. Parameter estimates, not including the intercept, are indicated in bold font if the P-value was < 0.05. Here, “E” refers to scientific notation (e.g., multiply by 10 to the power of).

Parameter Value (SE) CI df T P-value Intercept 3.89 (0.19) 3.51, 4.27 136923 20.15 < 0.01 Livestock (Yes) 1.54 (0.33) 0.84, 2.24 18 4.62 < 0.01 Rank (Low) −0.76 (0.3) −1.4, −0.12 18 −2.5 0.02 Hour −0.12 (0.02) −0.15, −0.09 136923 −7.33 < 0.01 Hour2 7.72E-03 (8.51E-04) 6.05E-03, 9.39E-03 136923 9.07 < 0.01 Prey (High) −0.36 (0.05) −0.46, −0.27 136923 −7.56 < 0.01 Rain 0.01 (0.01) −0.01, 0.04 136923 0.86 0.39 Temperature 0.15 (0.02) 0.11, 0.19 136923 7.79 < 0.01 Moonlight −0.05 (0.04) −0.12, 0.02 136923 −1.4 0.16 Rank (Low) × Prey (High) 0.26 (0.06) 0.15, 0.38 136923 4.41 < 0.01 Livestock (Yes) × Prey (High) −0.05 (0.06) −0.16, 0.07 136923 −0.79 0.43 Livestock (Yes) × Rank (Low) −2.01 (0.49) −3.04, −0.98 18 −4.09 < 0.01 1950 JOURNAL OF MAMMALOGY Downloaded from https://academic.oup.com/jmammal/article/100/6/1941/5571540 by guest on 25 September 2021

Fig. 5.—The significant interaction effects on the probability that a hyena (Crocuta crocuta) would be located inside its territory between (A) livestock presence and social rank and (B) social rank and prey availability. We present the proportion of all locations for hyenas that were inside their territories. Both of these interactions were statistically significant (P < 0.05). while foraging, when their ranging behavior is not limited by documented here, and the commuting behavior of Serengeti den-dwelling cubs (Boydston et al. 2003b). As in previous re- females (Hofer and East 1993a, 1993b, 1993c), represent search, we found that high-ranking hyenas were more likely adaptations by spotted hyenas to strong seasonal variation in than their low-ranking group-mates to be located inside of prey availability. In another area of sub-Saharan Africa, Cozzi their territories, and that this was more likely to occur when et al. (2015) reported on a female hyena that traveled 37 km in prey availability was low than when it was high. We also found a single day to feed on an elephant carcass. Because we found that, during periods of high prey availability, high-ranking hy- that long-distance travel events are affected by social rank, ex- enas traveled further and moved faster than their low-ranking traterritorial movements by spotted hyenas appear to be ne- conspecifics, and that this trend was reversed during periods cessitated by competition with conspecifics, and this need is of low prey availability. We hypothesize that hyenas of high exacerbated during periods of low prey availability. We hy- social rank travel farther and faster when prey are abundant pothesize that, like commuting trips by Serengeti hyenas, the because they are better able to usurp food from lower-ranking long-distance trips we documented here function to improve hyenas by covering more ground within their territories, and access to prey when prey are locally scarce. that hyenas of low social rank are traveling greater distances We present results showing that the fine-scale movements of and moving faster when prey are scarce to avoid having their spotted hyenas, like their broader use of space (Kruuk 1972; kills usurped by others. Mills 1990; Boydston et al. 2003a, 2003b; Kolowski et al. 2007; Although hyenas in other areas of sub-Saharan Africa are Kolowski and Holekamp 2009; Stratford and Stratford 2011), known to commute to regions of high prey availability when are affected by both social and naturally occurring ecological local prey are scarce (Hofer and East 1993a, 1993b, 1993c), conditions in addition to the presence of livestock. Our finding this has yet to be documented in any other places. We observed that spotted hyenas traveled faster on nights with more moon- hyenas repeatedly taking trips outside their territory bound- light contrasted with the result obtained by Cozzi et al. (2012), aries, but do not know precisely what ecological conditions who found no effects of lunar phase on hyena movements in were being sought on these trips. In contrast to Serengeti hy- Botswana’s Okavango Delta. Our result also differs from those enas (Hofer and East 1993a, 1993b, 1993c), our collared fe- obtained in previous research on lions. Oriol-Cotterill et al. males did not appear to be engaging in regular commuting (2015) found that lions moved more slowly in areas of high trips to feed at dense aggregations of migratory ungulates. The anthropogenic activity on moonlit nights. We hypothesize that hyenas we studied, however, were more likely to engage in moonlight might make hyenas more vulnerable to sources long-distance travel when prey were abundant compared to of mortality inside and outside the Reserve (e.g., lions and when they were scarce. Hyenas of both low and high social people), and that hyenas travelled faster to prevent or avoid po- rank went on long-distance trips, but low-ranking hyenas were tential conflicts. Regardless of the presence of livestock, hyenas more likely than high-ranking animals to make these trips moved more slowly when there was no moonlight. We hypothe- during periods of low prey availability within their territories. size that the absence of moonlight might simply make it harder It is likely that both the long-distance travel events we have for hyenas to navigate. GREEN AND HOLEKAMP—PASTORALISTS AFFECT SPOTTED HYENA BEHAVIORS 1951

We found that hyenas traveled more slowly and were more Supplementary Data likely to be inside their territory when temperatures were Supplementary data are available at Journal of Mammalogy above average. Increases in daily temperature, like those that online. have occurred over the last two decades, and are predicted Supplementary Data SD1.—The length of time each GPS to continue to occur, in this ecosystem (Ritchie 2008; Green collar was deployed on adult female hyenas (Crocuta crocuta) et al. 2019b), may effect additional changes in the move- in three clans with territories within the Masai Mara National ment patterns of spotted hyenas. For example, hyenas may Reserve, Kenya. limit their active period each night to cope with any poten- Supplementary Data SD2.—Analysis of the difference in tial effects of heat exhaustion. Higher than average rainfall hyena (Crocuta crocuta) territory size in 2013 calculated with also led to faster movements of our hyena subjects. Previous GPS locations from all collared females in each clan, or by Downloaded from https://academic.oup.com/jmammal/article/100/6/1941/5571540 by guest on 25 September 2021 work has documented slower movement rates by spotted hy- selecting two adult females each of low and high social rank enas during wet than dry seasons in other parts of Africa in each clan. The territories calculated using all of the loca- (Stratford and Stratford 2011), but none have documented tions for Talek West (“TW”), Serena North (“SN”), and Serena the effects of rainfall on the movements of spotted hyenas as South (“SS”) are shaded in red, yellow, and orange, respec- we have here. Livestock depredation by hyenas in or near the tively. The territories that were calculated using only two fe- Reserve increases during periods of heavy rain (Kolowski males each of low and high social rank per clan are displayed and Holekamp 2006), as herbivores are likely to disperse in solid blue lines. Sizes of territories between the two analyses more widely when water is more widely available. Thus, we varied only marginally (sizes of territories for SS, SN, and TW hypothesize that the effects of rainfall on the movement pat- calculated using GPS locations from all hyenas and four hy- terns we documented here might be an indirect effect of al- enas = 27.28 and 27.49 km2, 45.64 and 48.47 km2, and 76.80 tered prey distributions. and 73.29 km2, respectively), and the territorial boundaries Spotted hyenas are one of the few large carnivore species in calculated with locations from four hyenas greatly overlapped which population sizes may increase in areas of intensive an- the territories calculated using locations from all collared hy- thropogenic disturbance (Yirga et al. 2017; Green et al. 2018). enas (percent overlap between the two territories SS = 98.05%, Their movement patterns and space use, like those documented SN = 94.13%, TW = 99.23%). here and in previous studies (Boydston et al. 2003a; Kolowski et al. 2007; Kolowski and Holekamp 2009; Green et al. 2018), suggest some of the ways spotted hyenas are able to coexist Literature Cited with people and to cope with the disturbances humans cause in Baker, A. D., and P. L. Leberg. 2018. Impacts of human recreation their natural habitat. Spotted hyenas, however, appear to have on carnivores in protected areas. PLoS One 13:e0195436. the most flexible behavior among the large carnivore guild in Barton, K. 2017. MuMIn: multi-model inference. R package version sub-Saharan Africa (Holekamp and Dloniak 2010). This be- 1.40.0. https://CRAN.R-project.org/package=MuMIn. Accessed havioral plasticity allows hyenas to persist in disturbed areas 28 December 2017. where other large carnivore populations decline (e.g., Green Bauer, H., et al. 2015. Lion (Panthera leo) populations are et al 2018). In any case, when one of the most adaptive and declining rapidly across Africa, except in intensively man- plastic species in this ecosystem shows altered behavior in the aged areas. Proceedings of the National Academy of Sciences face of intensive anthropogenic activity, we can expect sym- 112:14894–14899. patric wildlife species to be faring considerably worse if they Bedelian, C., and J. O. Ogutu. 2017. Trade-offs for climate- resilient pastoral livelihoods in wildlife conservancies in the are more limited in their abilities to adapt to changing environ- Mara ecosystem, Kenya. Pastoralism: Research, Policy and ments (Green et al. 2019a). Practice 7:10. Bell, R. H. V. 1971. A grazing ecosystem in the Serengeti. Scientific Acknowledgments American 225:86–93. Boydston, E., K. Kapheim, M. Szykman, and K. E. Holekamp. We thank the National Commission for Science, Technology 2003b. Individual variation in space use by female spotted hyenas. and Innovation, the Narok County Government, the Mara Journal of Mammalogy 84:1006–1018. Conservancy, and the Kenya Wildlife Service for the per- Boydston, E., K. Kapheim, H. E. Watts, M. Szykman, and mission to conduct this work. This research was supported K. E. Holekamp. 2003a. Altered behaviour in spotted hyenas by National Science Foundation grants DEB 1353110, OISE associated with increased human activity. Animal Conservation 1556407, OISE 1853934, and IOS 1755089 to KEH and by 6:207–219. Boydston, E., T. L. Morelli, and K. E. Holekamp. 2001. Sex a NSF Graduate Research Fellowship to DSG. This research differences in territorial behavior exhibited by the spotted hyena was also supported by funding from the Lakeside Foundation (Hyaenidae, Crocuta crocuta). Ethology 107:369–385. and the Kenya Wildlife Trust. We also thank E. Thomas, Broekhuis, F., E. K. Madsen, and B. Klaassen. 2019. Predators L. Johnson-Ulrich, Z. M. Laubach, J. R. Greenberg, B. Pion, and pastoralists: how anthropogenic pressures inside wildlife areas E. D. Strauss, T. M. Montgomery, and J. W. Turner for their influence carnivore space use and movement behaviour. Animal assistance in the field. Conservation 22:404–416. 1952 JOURNAL OF MAMMALOGY

Butt, B. 2014. The political ecology of “incursions”: livestock, pro- Holekamp, K. E., and S. M. Dloniak. 2010. Intraspecific variation tected areas and socio-ecological dynamics in the Mara region of in the behavioral ecology of a tropical carnivore, the spotted hyena. Kenya. Africa 84:614–637. Advances in the Study of Behavior 42:189–229. Calenge, C. 2006. The package “adehabitat” for the R software: a Holekamp, K. E., and L. Smale. 1993. Ontogeny of dominance in tool for the analysis of space and habitat use by animals. Ecological free-living spotted hyaenas: juvenile rank relations with other im- Modelling 197:516–519. mature individuals. Animal Behaviour 46:451–466. Cardillo, M. 2005. Multiple causes of high extinction risk in large Holekamp, K. E., L. Smale, and M. Szykman. 1996. Rank and re- mammal species. Science 309:1239–1241. production in the female spotted hyaena. Journal of Reproduction Cooper, S. M., K. E. Holekamp, and L. Smale. 1999. A sea- and Fertility 108:229–237. sonal feast: long-term analysis of feeding behaviour in the Holekamp, K. E., J. E. Smith, C. C. Strelioff, R. C. Van Horn, spotted hyaena (Crocuta crocuta). African Journal of Ecology and H. E. Watts. 2012. Society, demography and genetic struc- Downloaded from https://academic.oup.com/jmammal/article/100/6/1941/5571540 by guest on 25 September 2021 37:149–160. ture in the spotted hyena. Molecular Ecology 21:613–632. Cozzi, G., et al. 2015. Effects of trophy hunting leftovers on the Höner, O. P., B. Wachter, M. L. East, V. A. Runyoro, and ranging behaviour of large carnivores: a case study on spotted hy- H. Hofer. 2005. The effect of prey abundance and foraging tactics enas. PLoS One 10:e0121471. on the population dynamics of a social, territorial carnivore, the Cozzi, G., F. Broekhuis, J. W. McNutt, L. A. Turnbull, spotted hyena. Oikos 108:544–554. D. W. Macdonald, and B. Schmid. 2012. Fear of the dark or Houston, A. I., E. Prosser, and E. Sans. 2012. The cost of distur- dinner by moonlight? Reduced temporal partitioning among bance: a waste of time and energy? Oikos 121:597–604. Africa’s large carnivores. Ecology 93:2590–2599. Kolowski, J. M., and K. E. Holekamp. 2006. Spatial, temporal, Dinerstein, E., et al. 2007. The fate of wild tigers. BioScience and physical characteristics of livestock depredations by large car- 57:508–514. nivores along a Kenyan reserve border. Biological Conservation ESRI. 2018. ArcGIS desktop: release 10.6.1. Environmental Systems 128:529–541. Research Institute, Redlands, California. Kolowski, J. M., and K. E. Holekamp. 2009. Ecological and an- Estes, J. A., et al. 2011. Trophic downgrading of planet Earth. thropogenic influences on space use by spotted hyaenas. Journal of Science 333:301–306. Zoology 277:23–36. Farr, M. T., D. S. Green, K. E. Holekamp, G. J. Roloff, and Kolowski, J. M., D. Katan, K. R. Theis, and K. E. Holekamp. E. F. Zipkin. 2019. Multispecies hierarchical modeling reveals var- 2007. Daily patterns of activity in the spotted hyena. Journal of iable responses of African carnivores to management alternatives. Mammalogy 88:1017–1028. Ecological Applications 29:e01845. Kruuk, H. 1972. The spotted hyena: a study of predation and social Frank, L. G. 1986. Social organization of the spotted hyaena (Crocuta behavior. University of Chicago Press, Chicago, Illinois. crocuta). I. Demography. Animal Behaviour 34:1500–1509. Ladle, A., T. Avgar, M. Wheatley, G. B. Stenhouse, Gaynor, K. M., C. E. Hojnowski, N. H. Carter, and S. E. Nielsen, and M. S. Boyce. 2019. Grizzly bear response to J. S. Brashares. 2018. The influence of human disturbance on spatio‐temporal variability in human recreational activity. Journal wildlife nocturnality. Science 360:1232–1235. of Applied Ecology 56:375–386. Green, D. S., M. T. Farr, K. E. Holekamp, E. D. Strauss, and Lamprey, R. H., and R. S. Reid. 2004. Expansion of human set- E. F. Zipkin. 2019a. Can hyena behaviour provide informa- tlement in Kenya’s Maasai Mara: what future for pastoralism and tion on population trends of sympatric carnivores? Philosophical wildlife? Journal of Biogeography 31:997–1032. Transactions of the Royal Society of London, B. Biological Levi, T., A. M. Kilpatrick, M. Mangel, and C. C. Wilmers. 2012. Sciences 374:20180052. Deer, predators, and the emergence of Lyme disease. Proceedings Green, D. S., L. Johnson-Ulrich, H. E. Couraud, and of the National Academy of Sciences 109:10942–10947. K. E. Holekamp. 2018. Anthropogenic disturbance induces op- Liberg, O., G. Chapron, P. Wabakken, H. C. Pedersen, N. T. Hobbs, posing population trends in spotted hyenas and African lions. and H. Sand. 2012. Shoot, shovel and shut up: cryptic poaching Biodiversity and Conservation 27:871–889. slows restoration of a large carnivore in Europe. Proceedings of Green, D. S., E. F. Zipkin, D. C. Incorvaia, and K. E. Holekamp. the Royal Society of London, B. Biological Sciences 279:910–915. 2019b. Long-term ecological changes influence herbivore diversity Loveridge, A. J., M. Valeix, N. B. Elliot, and D. W. Macdonald. and abundance inside a protected area in the Mara-Serengeti eco- 2017. The landscape of anthropogenic mortality: how African lions system. Global Ecology and Conservation 20:e00697. respond to spatial variation in risk. Journal of Applied Ecology Henschel, J. R., and J. D. Skinner. 1991. Territorial behaviour by 54:815–825. a clan of spotted hyaenas Crocuta crocuta. Ethology 88:223–235. Miller, B., et al. 2001. The importance of large carnivores to Hofer, H., and M. L. East. 1993a. The commuting system of healthy ecosystems. Endangered Species Update 18:202–210. Serengeti spotted hyaenas: how a predator copes with migratory Mills, M. G. L. 1990. Kalahari hyenas: comparative behavioral prey. I. Social organization. Animal Behaviour 46:547–557. ecology of two species. Unwin Hyman Academic, London, United Hofer, H., and M. L. East. 1993b. The commuting system of Kingdom. Serengeti spotted hyaenas: how a predator copes with migratory Olson, L. E., J. R. Squires, E. K. Roberts, J. S. Ivan, and prey. II. Intrusion pressure and commuters’ space use. Animal M. Hebblewhite. 2018. Sharing the same slope: behavioral re- Behaviour 46:559–574. sponses of a threatened mesocarnivore to motorized and nonmotorized Hofer, H., and M. L. East. 1993c. The commuting system of winter recreation. Ecology and Evolution 8:8555–8572. Serengeti spotted hyaenas: how a predator copes with migra- Oriol-Cotterill, A., D. W. Macdonald, M. Valeix, S. Ekwanga, tory prey. III. Attendance and maternal care. Animal Behaviour and L. G. Frank. 2015. Spatiotemporal patterns of lion space use 46:575–589. in a human-dominated landscape. Animal Behaviour 101:27–39. GREEN AND HOLEKAMP—PASTORALISTS AFFECT SPOTTED HYENA BEHAVIORS 1953

Packer, C., et al. 2009. Sport hunting, predator control and conser- Sinclair, A. R. E., and M. Norton-Griffiths. 1979. Serengeti: dy- vation of large carnivores. PLoS One 4:e5941. namics of an ecosystem. University of Chicago Press, Chicago, Illinois. Packer, C., et al. 2013. Conserving large carnivores: dollars and Soofi, M., et al. 2018. Livestock grazing in protected areas and its fence. Ecology Letters 16:635–641. effects on large mammals in the Hyrcanian forest, Iran. Biological Packer, C., H. Brink, B. M. Kissui, H. Maliti, H. Kushnir, and Conservation 217:377–382. T. Caro. 2010. Effects of trophy hunting on lion and leopard popu- Stelfox, J. G., et al. 1986. Herbivore dynamics in southern Narok, lations in Tanzania. Conservation Biology 25:142–153. Kenya. The Journal of Wildlife Management 50:339–347. Pangle, W. M., and K. E. Holekamp. 2010. Lethal and nonlethal an- Stratford, K. J., and S. M. C. Stratford. 2011. Fine-scale move- thropogenic effects on spotted hyenas in the Masai Mara National ments and use of space by spotted hyaena (Crocuta crocuta) on Reserve. Journal of Mammalogy 91:154–164. Ongava Game Reserve, Namibia. African Journal of Ecology R Core Team. 2017. R: a language and environment for statistical 49:343–352. Downloaded from https://academic.oup.com/jmammal/article/100/6/1941/5571540 by guest on 25 September 2021 computing. R Foundation for Statistical Computing, Vienna, Taylor, R. A., S. J. Ryan, J. S. Brashares, and L. R. Johnson. Austria. http://www.R-project.org/. Accessed 28 December 2017. 2016. Hunting, food subsidies, and mesopredator release: the dy- Ripple, W. J., et al. 2014. Status and ecological effects of the namics of crop-raiding baboons in a managed landscape. Ecology world’s largest carnivores. Science 343:1241484. 97:951–960. Ritchie, M. E. 2008. Global environmental changes and their impact Van Dyke, F. G., R. H. Brocke, H. G. Shaw, B. B. Ackerman, on the Serengeti. Pp. 183–208 in Serengeti III: human impacts on T. P. Hemker, and F. G. Lindzey. 1986. Reactions of moun- ecosystem dynamics (A. R. E. Sinclair, C. Packer, S. A. R. Mduma, tain lions to logging and human activity. The Journal of Wildlife and J. M. Fryxell, eds.). University of Chicago Press, Chicago, Management 50:95–102. Illinois and London. Venables, W. N., and B. D. Ripley. 2002. Modern applied statistics Schmitz, O. J., D. Hawlena, and G. C. Trussell. 2010. Predator con- with S. 4th ed. Springer, New York. trol of ecosystem nutrient dynamics. Ecology Letters 13:1199–1209. Wittemyer, G., P. Elsen, W. T. Bean, A. C. Burton, and Schuette, P., S. Creel, and D. Christianson. 2013. Coexistence J. S. Brashares. 2008. Accelerated human population growth at of African lions, livestock, and people in a landscape with vari- protected area edges. Science 321:123–126. able land use and seasonal movements. Biological Conservation Wong, B. B. M., and U. Candolin. 2015. Behavioral responses to 157:148–154. changing environments. Behavioral Ecology 26:665–673. Sih, A. 2013. Understanding variation in behavioural responses to Woodroffe, R., and J. R. Ginsberg. 1998. Edge effects and human-induced rapid environmental change: a conceptual over- the extinction of populations inside protected areas. Science view. Animal Behaviour 85:1077–1088. 280:2126–2128. Sih, A., P. C. Trimmer, and S. M. Ehlman. 2016. A conceptual Yirga, G., et al. 2017. Densities of spotted hyaena (Crocuta crocuta) framework for understanding behavioral responses to HIREC. and African golden wolf (Canis anthus) increase with increasing Current Opinion in Behavioral Sciences 12:109–114. anthropogenic influence. Mammalian Biology 85:60–69. Sikes, R. S., and The Animal Care and Use Committee of the American Society of Mammalogists. 2016. 2016 Guidelines of Submitted 14 February 2019. Accepted 15 August 2019. the American Society of Mammalogists for the use of wild mammals in research and education. Journal of Mammalogy 97:663–688. Associate Editor was Jacob Goheen.