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Social interactions in striped hyena inferred from camera trap data: is it more social than previously thought?

Abstract Understanding the drivers promoting sociality over solitariness in animal species is imperative for predicting future population trends and informing conservation and management. In this study we investigate the social structure of a desert dwelling population of striped hyena Hyaena hyaena. This species is historically regarded as strictly solitary albeit being the least studied of the extant Hyaenids. Accumulating evidence regarding the frequency of social interactions suggests a revision of striped hyena social structure is required. We hypothesized that striped hyena has a social structure that is more complex than expected for a strictly solitary species. For that end, we deployed an array of camera-traps in a remote desert region in Israel, and compared observed frequencies of striped hyena co-occurrence against null models to test whether hyena co-occurred more than expected by chance. Seven adults were (re)captured by our camera-traps in 49 different instances over 83 tracking days. Of these, 6 exhibited shared space-use around a scarce, isolated perennial water source. Five of them, co-occurred with other hyena (in 3 instances) significantly more frequent than expected by chance (and that timing suggests reproduction is unlikely to be the driving factor). Our findings substantiate evidence of complex social structure in striped hyena, highlight the importance of a scarce resource in space-use and sociality, and provide a baseline for future research of striped hyena social structure. We suggest that similar methods be employed to evaluate social structure in other “solitary species” to better understand their social dynamics.

(that are not related to reproduction or territorial disputes) between solitary carnivore conspecifics. These are kinship (Hamilton 1964) and resource dispersion (Macdonald 1983;Wrangham and Rubenstein 1986).
Among solitary species, 'encounters' (co-occurrence; 2 individuals observed at the same time and place) and 'shared space-use' (2 individuals observed in the same location but not at the same time) can emerge, even without social preference (i.e., conspecific attraction), simply because individuals are independently attracted to resources. Therefore, for differentiating between 'random' encounters (sensu unintentional, asynchronized, independent of intraspecific attraction) and intended ones (i.e., synchronized or a result of intraspecific attraction), one could contrast between observed intraspecific co-occurrences and a null model that assumes a complete lack of synchronization/attraction among individuals.
Among the Carnivora, the Hyaenidae family, that includes 4 extant species (Holekamp and Kolowski 2009) is considered to be of particular interest as it contains the full range of social organization from strictly solitary to highly gregarious (Wagner 2006;Watts and Holekamp 2009). Hyaenids exhibit a gradient of gregariousness (Table 1) likely linked to dietary differences and variations in resource availability and distribution (Wagner 2006). The least studied Hyaenid is the striped hyena Hyaena hyaena (Mills and Hofer 1998;Watts and Holekamp 2007;Holekamp and Kolowski 2009;Wagner 2013), which is commonly considered to be solitary (Mills and Hofer 1998;Watts and Holekamp 2007;Wagner 2013) and even strictly solitary (e.g., "Striped hyaenas lead a solitary existence and they are only rarely seen together", Kruuk 1976, p. 105). Due to its cryptic nature, there is a general lack of knowledge on the species' natural history and behavior. Specifically, data on its social organization and social structure that could inform population estimates and contribute to future conservation efforts are lacking (Abi Said and Dloniak 2015).
In this study, we evaluate the social structure of a population of striped hyena in Israel, and in line with accumulating evidence (e.g., Macdonald 1978;Rieger 1979;Heptner and Sludskij 1980;Bothma and Walker 1999;Wagner 2006;Wagner et al. 2008, see 'discussion' for further details), hypothesize that striped hyena will exhibit a more complex social structure and social interactions evidenced via higher levels of intraspecific encounters than expected by chance. We deem this behavior to be linked (at least partially) to resource dispersion/availability (in particular water, a scarce resource in our studied system). Moreover, we predict that individuals will exhibit greater space sharing at proximity to water sources. To test these predictions, we deployed an array of camera traps in the Negev Highlands (a remote desert region in Israel) and compared the observed co-occurrence data with a null model based on randomized data generated using settings based on those occurring in the study area. This study is the first to evaluate the spatiotemporal distribution of a striped hyena population in the Negev Highlands and assess its social structure.

Study area
The study area spans circa 400 km 2 and covers a section of the Negev Highlands at the south of Israel ( Figure 1A). This region is a hyper-arid (annual precipitation <80 mm) rocky mountainous desert that spans over 2,000 km 2 (Evenari et al. 1982). It is characterized by high plateaus that descend in steep slopes and cliffs (Hillel and Tadmor 1962). In the summer months (June-September), the driest and hottest time of the year temperatures can rise up to 44.8 C (mean annual temperature is $19 C, Nativ et al. 1997). Most water sources in the region are ephemeral (following flash floods in the rainy season) while perennial springs are scarce and dispersed making them a rare resource in a very warm and arid environment.  (2007), Mills (1982Mills ( , 1983, and Owens and Owens (1979) (2007), Kotze et al. (2012), Marneweck et al. (2015), and Richardson and Coetzee (1988). Cameras were spaced to maximize the chances that each (hypothetical, partially overlapping) HR-zone will be covered by at least 2 cameras.

Study species
The striped hyena is listed in the IUCN Red List as 'near threatened' with a global population of <10,000 individuals, highly patchy distribution, and under continual decline (Abi Said and Dloniak 2015). An adult striped hyena measures total length (head to end of tail) 130-166 cm, height at shoulder 60-95 cm, and weight 25-55 kg (Rieger 1981), making it the largest and heaviest carnivore species in the Negev Highlands. The species lacks obvious sexual dimorphism, thus challenging the ability to determine sex remotely. It is an omnivorous scavenger feeding on small vertebrates (sometimes hunting them), invertebrates, larger carcasses, and anthropogenic-related resources including vegetables, fruits, and organic wastes (Wagner 2006). Across its distribution, parturition is reported to occur throughout the year (Rieger 1979); however, in Israel, the peak of parturition is reported to occur in the spring, i.e., March-April (Mills and Hofer 1998). The striped hyena is commonly considered to be a solitary carnivore (Kruuk 1976;Mills and Hofer 1998;Wagner 2013).

Camera traps
During the study, we used 15 Bushnell camera-traps (models 119678c, 119676c, 119477, 119537, 119437, and 119447) with passive infrared motion sensor (triggered by warmer-than-ambient objects that cross their detection range up to $17 m away). We encased each camera in a camouflaged, protective box that was secured to rock faces. The cameras were used in 1 of 2 settings, either "camera only"-which takes 3 pictures per event after a trigger-time of 0.2 s, or 'hybrid'-which we set to take 2-3 pictures per event followed by a 10-15 s of video after $2 s. In both settings, the camera had a 15 s 'rest' interval following a trigger event, before it could have been triggered again in a subsequent event.

Field methods and data collection
To maximize the cover by our array, the study area (circa 400 km 2 ) was divided into 8 overlapping circular zones ( Figure 1B) each representing approximately 60 km 2 which is equivalent to the smallest reported home-ranges (HR) of striped hyena in Israel-60 km 2 (Van Aarde et al. 1988) and 110 km 2 (The Society for the Protection of Nature in Israel [SPNI] n.d.) both for VHF-collared females in the Negev desert. The 15 cameras were spaced so that at least 2 cameras were placed in each hypothetical HR-zone to provide a full coverage of the study area. The locations of the HR-zones ( Figure 1B) were designed to form an array that covered the entire study area (average distance between cameras ¼ 2.53 km). The position of each camera within the HR zones was determined in situ following field surveys with local trackers and the cameras were often placed where signs of hyena and other wildlife (e.g., paw prints, scats) were abundant. Notably, 3 of the 15 camera traps (C13, C14, and C17) were placed on 2 perennial water sources. Camera C13 and C14 represent one spatial location (as they were placed approximately 200 m from each other on a perennial water source) and camera C17 was situated on another location also on a perennial water source. Cameras were deployed from the 22 July until the 12 October 2015 (83 consecutive days) summing to a total trapping effort of 1,245 trapping days. This data collection period corresponded with the Israeli summer (June-September).

Determining spatiotemporal distribution
We used the data from the camera trap array to test the hypothesis that striped hyena exhibit more frequent encounters than expected by chance. We take the capture of an individual hyena by a camera trap to indicate its use of that area. Where more than 1 hyena was captured (non-simultaneously) by a camera trap, we take that to indicate overlap in space-use (i.e., 'shared space-use' or cluster in space). If these captures were within 24 h from each other we consider it as 'proximate shared space-use'. Instances of more than 1 individual captured in the same place at the same time are 'co-occurrence'. Furthermore, for hyena that were captured by more than 1 camera, the minimal area to be covered in between those cameras was taken as the minimal area of overlap between their HRs (i.e., the area that they share in common).

Contrasting observation with null model randomizations
To determine if observed frequencies of shared space-use and cooccurrences are more than expected by chance, we compared our observations with expectation derived from a null model assuming fully independent space-use among individuals (see Spiegel et al. [2016Spiegel et al. [ , 2018 for a more thorough discussion of this approach). Briefly, by using data permutations, we generated a distribution of expected frequencies under this null model. Constraining the permutations to the structure of the data allows us to account for differential use of the cameras (i.e., explicitly accounting for the fact that some cameras are located near resources that attract individuals independently of each other). We created 10,000 realizations of the null model, each including the same number of total hyena observations (N ¼ 49), and the same camera specific frequencies (e.g., 42 instances of observations in camera C17) and sampling nights. For determining the timing of these permuted observations in each realization we first calculate the number of instances that 2 or more individuals will be captured by the same camera during a 24 h period-allowing us to test 'intention' in proximate shared spaceuse. Then, we draw observation times from the empirical distribution to determine for each dyad if they also co-occurred. Significance level of the camera-trap data (i.e., how likely was this data to happen by chance) is determined as the number of iterations in the simulated null model with encounter frequencies similar or higher than the observed (i.e., how many iterations it took to produce output equivalent to the observed data).

Joint observations and HR overlap
All co-occurrences that were documented throughout the study are summarized in Table 3. Camera C16 (positioned on a col about 1 km south-east of camera C17-see Figure 2, and operational for only 37 days) captured 1 occasion in which 2 individuals were cooccurring (H3 with H4, see Figure 3A). Camera C17 (situated on a perennial water source) captured 2 occasions in which 2 individuals co-occurred (H3 with H5, and H1 with H7, see Figure 3B, C, respectively). Over the duration of the study, 7 adult hyena (H1-H7) and 1 juvenile (H8) were captured by camera C17. Six of these adults were captured on more than 1 occasion while individual H6 was only captured once (thus, this location is not necessarily a part of its permanent HR). Therefore, the location of camera C17 is considered a point of overlap between the HRs of 6 adult hyena (after excluding H6 and H8). Accordingly, these hyena are considered to share, at the minimum level, that point in common within their HRs. H4 was also captured in the location of camera C16. H1 and H3 were captured at all 3 camera locations that captured hyena, i.e., also by camera C13 and C14 (both located on a perennial water source approximately 10 km west of camera C17, and about 200 m from each other) and with one of these hyena involved at each of the 3 co-occurrences ( Figure 3). In accordance, we inferred a minimum overlap between the HRs of these hyena (H1, H3, and H4) that exceed the location of camera C17 (Figure 2).

Shared space-use and social interactions
Our results demonstrate that shared space-use occurred at specific locations (hyena encounters occurred at 4 out of 15 camera traps). Mostly, these locations were in the proximity of resources (i.e., perennial water sources). In 7 instances, different individuals were observed at the same camera within a 24 h period. These instances include both co-occurrences and 'proximate shared space-use' (Table 3). This frequency of proximate shared space-use is not significantly different (P ¼ 0.72) to null expectations accounting for the sampling effort (camera specific activity duration), and camera differential capture success ( Figure 4A). Nevertheless, the observed frequency of co-occurrence (N ¼ 3) is significantly higher than null expectation (P ¼ 0.0023), in which only 23 instances out of 10,000 modeled yielded 3 or more instances of co-occurrence. This result demonstrates that hyenas show conspecific attraction beyond shared space-use, are clustering in space and time, and suggests that they exhibit a more complex social structure than the term 'strictly solitary' implies.

Discussion
In this study, we tested the hypothesis that striped hyena, despite historically being considered strictly solitary, exhibit social interactions and spatiotemporal overlap suggesting a more complex social structure. With our camera-traps, we documented 7 adult hyena, 6 of which exhibited a shared space-use of varying degrees (from sharing 1 spatial location by all of them, to sharing 3 distant locations by 2). In addition, we documented 3 co-occurrences of adult hyena (2 of  H1) and, if observed in more than 1 location, also by a distinct color. The dashed ovals represent the (schematic) minimal home-range that is expected to be covered by the hyena that were (re)captured in more than 1 camera location (i.e., H1, H3, and H4). The color/pattern of the dashed line corresponds to the color/pattern of the associated hyena (i.e., H1-black, H3-gray, H4-double-line). All hyena were captured at the location of camera C17 (the one that is encircled by all hyena) and it is thus considered to be a point of overlap where all home-ranges meet. H6 and H8 are not included in this consideration of overlap as H6 appeared only once and H8 is a juvenile.
which were located on a perennial water source and the third on a nearby col). We found that co-occurrences in our study took place more frequently than expected by chance (3 out of 49 that we encountered vs. 23 out of 10,000 in the null model simulation that accounted for structures and dependencies in the data). Our results demonstrate that the social interactions by the hyena were 'intentional' (i.e., meeting more than expected by chance if their use was independent of others) thus exhibiting conspecific attraction.
Alternately, there could have been an external (perhaps environmental) cue, that we did not detect, that drives individual hyena to use the same area at the same time, and thus created an apparent conspecific attraction. Solitary species are expected to have very little contact with conspecifics and to exhibit asynchrony in general activity (especially in movement throughout the habitat with conspecifics). The striped hyena in our population deviated from this definition. Their shared space-use indicated overlap in HR on scarce water sources and their co-occurrences suggest intentional social interactions, evidencing a more complex social structure than expected from a 'strictly solitary'. This study presents the first documentation of such behavior in striped hyena that is tested against a null hypothesis of random encounters. In all hyena co-occurrences, due to a lack of data on sex and relatedness, the relationship of association within dyads (e.g., breeding pair, siblings) could not be determined (excepting H2 and H8, inferred to be a mother and her offspring). However, due to their timing, these co-occurrences are unlikely to be motivated by reproduction. While striped hyena produce litters throughout the year in the wild (Rieger 1979), the peak of parturition in Israel is reported to be in the spring-i.e., March-May (Mills and Hofer 1998). With a gestation period of 90-92 days (Rieger 1979;Mills and Hofer 1998), mating in Israel is likely to occur December-February. All records of hyena co-occurrence in this study took place during July and August, thus outwith the likely mating period. Likewise, the shared space-use of the 6 adult hyena at the perennial water source of camera C17 also took place during July-September.

Supporting evidence of sociality in striped hyena
Despite historically being considered as a strictly solitary species (Kruuk 1976;Mills and Hofer 1998;Wagner 2013), accumulating evidence suggests that the striped hyena social structure is more complex. Heptner and Sludskij (1980) describe the occurrence of monogamous pairs and groups of up to 5-6 in Central Asia. Holekamp and Kolowski (2009) report on groups of up to 7 occurring in North Africa (i.e., Libya). In Kenya, striped hyena were frequently observed resting in pairs and on occasion in groups of up to 4 individuals (Wagner 2006;Wagner et al. 2008). These groups consisted mostly of unrelated or distantly related hyena (on occasion containing full siblings: brother-brother or brother-sister) and were always mixed sex with 1 female and up to 3 males (Wagner 2006;Wagner et al. 2008). Wagner (2006) reported 2 sub-adult female siblings in Kenya that were observed regularly at the den of their mother assisting with rearing new born cubs. Striped hyena cubs have also been reported to be attended by adult males (the father and sometimes more than 1 male) until independence in the African  savannah (Bothma and Walker 1999). For Israel's striped hyena, Macdonald (1978) reported !2 striped hyena moving and eating together in more than half of his observations ( Lastly, a pair of subadult striped hyena was reported as arriving together to an INPA feeding site in the Negev Highlands, Israel (Skinner and Ilani 1979). Altogether, the data presented in this study contribute further to accumulating evidence of a more complex social structure than 'strictly solitary' in striped hyena. Moreover, it presents the first account of hyena co-occurrences in Israel on a resource that is not food, thus underscoring the importance that scarce perennial water sources might have in driving social interactions and clustering in space in arid environments. Furthermore, contrary to the aforementioned examples, we were also able to show that even after accounting for the attraction to key resources the observed frequencies exceed those expected by independent space-use. These aspects contribute to our understanding of social structures and their driving forces in species that are otherwise considered to be strictly solitary.

Drivers and conditions explaining striped hyena space clustering
Striped hyena are reported to remain in the vicinity (up to 10 km) of water sources (Rieger 1979(Rieger , 1981, especially during the warmer period of the year (Heptner and Sludskij 1980) which in Israel is June until September. Such behavior indicates dependence on water sources. Considering this, the formation of a cluster of adult hyena exhibiting shared space-use around the location of camera C17 is likely linked to its proximity to a scarce and isolated perennial water source. Macdonald et al. (1999) describe a population of red fox dwelling in a Saudi Arabian desert that exhibit a loose-sense of territoriality unlike red fox populations elsewhere. Their proposed explanation is that existing harsh environment and dispersed scarce resources (in this case, food-rich dumps and shadow) require forming large territories that are difficult to defend thus favoring the formation of a shared space-use cluster. The cluster of striped hyena that we describe persists in similar conditions where a scarce resource (water) could have led to increased tolerance and consequently a lack of strict territoriality. Possibly, such spatial overlap intensifies during the dry summer months when all ephemeral water sources are completely dry, but this is impossible to test with our dataset. The formation of such a shared space-use in terms of the scarcity and dispersion of water as a resource is consistent with the resource dispersion rationale (sensu Macdonald and Johnson 2015). Resource dispersion provides an explanation for a driving (or at least a facilitating) mechanism by which the formation of such clustering in space could be favored.
The hyena in our study could potentially socialize during the day at resting points similar to a population described from Kenya (Wagner 2006;Wagner et al. 2008). The hyena female (H2) may have had assistance at the den in rearing the juvenile (H8) from the father (as for Heptner and Sludskij 1980;Bothma and Walker 1999), other males from the cluster (Bothma and Walker 1999), and/or subadult siblings (Wagner 2006). Lastly, the described space-sharing cluster could be a philopatry-based family group (as described in Heptner and Sludskij 1980;Bothma and Walker 1999), contain monogamous pairs (as reported by Heptner and Sludskij 1980), or be polyandrous (Wagner et al. 2008) or polygynous in mating system.
We suggest that future research on striped hyena should focus on several parallel areas. Firstly, direct behavioral observations are required, e.g., using more camera traps over longer periods (while taking video footage) to evaluate the nature of the social interactions Results from a permutation test contrasting observed frequency (vertical dashed lines) of (A) proximate shared space-use (individuals captured at the same camera during a 24 h period) and (B) co-occurrence (individuals captured in the same camera at the same time) with expectations from null model assuming space use is independent among individuals and accounting for camera specific sampling effort and capture frequencies. These results (dashed lines) demonstrate that while hyena in the studied population readily share space, this rate is not different from expectations based on resource distribution. Nevertheless, this analysis reveals that hyena co-occurred significantly more than expected from shared space-use alone.
(upon co-occurrence) and thereby to understand the extent of the complexity of their social structure. Such data would enable social network analyses to be conducted. Secondly, future research should aim at higher resolution spatiotemporal data (e.g., from GPS collars) and data on age-sex and genetics (DNA, e.g., from feces/blood).

Conservation implications
Defining a species as solitary can ultimately bear consequences for its protection. For example, abundance estimates of the IUCN Red List often assume a linear relationship between species' abundance and area of occupancy (Akc¸akaya et al. 2006). Accordingly, a region that was previously assumed to host a particular number of solitary individuals will accommodate more if the species exhibits clustering behavior and shared space-use. Moreover, establishing the complexity of the social structure of striped hyena, as well as its clustering in space, has important implications for conservation efforts of this elusive and under-studied species. On the one hand, current abundance estimates in the IUCN Red List species account are based on the assumption that the striped hyena is a strictly solitary species that lives at low densities (Mills and Hofer 1998;Abi Said and Dloniak 2015). Consequently, our findings that the striped hyena in our study exhibited social interactions and shared space-use suggests that current estimates of abundance/density of striped hyena may be underestimated. On the other hand, should cooperative care (if occurring) promote the species' reproductive success, as for spotted and brown hyena (Table 1), decreasing population density and increasing fragmentation of populations may have serious implications for the future sustainability of wild striped hyena populations, e.g., via an 'Allee effect' (Allee et al. 1949;Courchamp et al. 1999).
In light of accumulating evidence, it is time to change the default assumption that the striped hyena is a strictly solitary species (Mills and Hofer 1998). The evidence from across its range and in this study suggests that under some conditions, and in accordance with resource dispersion rationale, striped hyena sometimes cluster in space (i.e., shared space-use) and exhibit social interactions that suggest a more complex social structure. The striped hyena, the least studied of the Hyaenids, receives a much undeserved bad reputation and is persecuted across its range (Holekamp and Kolowski 2009;Wagner 2013). In part, this undeserved reputation is the result of past accounts of hyena that raided human graves (Leakey et al. 1999;Wagner 2013), caused damage to agriculture and livestock (Wagner 2013), and legends of them enchanting people and dragging them to a den where they eat them (e.g., in the Middle East, Qarqaz et al. 2004). Combined with a declining availability of food, the striped hyena has been extirpated in many areas and populations continue to decline (where known) across their range (Abi Said and Dloniak 2015). With a better understanding of striped hyena ecology and social structure we can address some of the threats that imperil its future and enhance the conservation of this fascinating species.