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Behavioural Processes 164 (2019) 186–192

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Behavioural Processes

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Female-female aggression in goitered : the desire for isolation T ⁎ D..A. Blanka,b,c, a Research Center for Ecology and Environment of Central Asia, Bishkek, b Key Laboratory of Biogeography and Bioresources in Arid Land, Institute of Ecology and Geography, the Chinese Academy of Sciences, Urumqi, c Al-Farabi Kazakh National University, Almaty,

ARTICLE INFO ABSTRACT

Keywords: In contrast to males, which compete with other males for access to mates, females compete with each other for Birthing grounds forage-rich sites, birthing grounds, comfortable resting places, and access to sources of water and salt licking Female-female aggression locations. This behavior has been observed in many species. However, many agonistic interactions between ’ fl females con ict females occur where resources are not immediately at stake, and the reasons for their rivalry are often unclear. Gazella subgutturosa Therefore in this paper, I want to analyze the main causes of female-female aggression in the yearly cycle of goitered gazelles. I found that adult females had conflicts moistly with sub-adult females and less with other adult females; and these behaviors were observed mainly in May, with less in June, and only a few cases dis- played during the rest of the year. The months of May-June had the most abundant and highest quality forage of the year, when competition for resources would seem to be least expected. Struggles for resting places occurred throughout the entire year, with only some bias for May that did not represent a primary level of aggression. In reality, the high rate of female-female aggressive interactions was related to the protection of birthing grounds, where mothers isolated themselves to give births, establish a strong selective mother-young bonds, keep their hiding fawns separated from alien offspring (having initial problems with distant visual recognition), and protect them against disturbance from all other females, which can undermine a fawn’s hidden status and make it more vulnerable to predation.

1. Introduction forage, and social rank) than for access to a potential mate (LeBas, 2006; Clutton-Brock, 2007). Aggression serves a great variety of social functions, including intra- The presence of female dominance hierarchies is known for social sexual and social selection among individuals leading to sexual di- organization of many artiodactyl ungulates, including , , morphism in size, shape of horns and body proportions (West-Eberhard, , , , , Rangifer, , , and 1983; Lundrigan, 1996; Perez-Barberia et al., 2002; Bro-Jørgensen, Gazella (refer in Roberts, 1996), with female ungulates demonstrating 2007). Hence, aggression is closely related to social hierarchy and non-random, near-linear or linear dominance hierarchies (Thouless and sexual selection (Clutton-Brock and Parker, 1995), in which the role of Guinness, 1986; Festa-Bianchet, 1991; Hass, 1991; Alados and Escós, the sexes typically differs in polygynous : males compete for 1992). High rank grants priority of access to feeding sites (Hall, 1983), females, which in turn lead females to make different choices among which can lead to enhanced fecundity, higher offspring survival (Alados competing males (Trivers, 1972). The key factor determining the role of and Escós, 1992), and a lower risk of predation for highly dominant sexes in breeding is their relative parental investment, and when one females (Byers, 1997). use individual characteristics in ago- sex invests more in rearing young (females in ungulates) than the other nistic encounters related to social rank including body mass, body size, (males), members of the latter (males in ungulates) will compete among or weapons such as horns or antlers (Espmark, 1964; Lott and Galland, themselves to mate with members of the former (females) (Trivers, 1987; Greenberg-Cohen et al., 1994; Wronski et al., 2010; Cunningham 1972). In polygynous ungulates, intrasexual aggression typically differs and Wronski, 2011). Social rank in females may also increase with age between the sexes. In contrast to males, which compete for mates, fe- in some ungulate species (bison – Bison bison: Rutberg, 1983; red – males have a greater level of energy invested in parental care, therefore Cervus elaphus; Thouless and Guinness, 1986; white-tailed deer – Odo- females compete with each other more commonly for access to re- coileus virginianus: Townsend and Bailey, 1981; bighorn – Ovis cana- sources necessary for successful reproduction (breeding sites, nutritious densis: Festa-Bianchet, 1991; chamois – Rupicapra rupicapra: Locati and

⁎ Corresponding author. E-mail address: [email protected]. https://doi.org/10.1016/j.beproc.2019.05.012 Received 22 December 2018; Received in revised form 10 May 2019; Accepted 11 May 2019 Available online 12 May 2019 0376-6357/ © 2019 Elsevier B.V. All rights reserved. D.A. Blank Behavioural Processes 164 (2019) 186–192

Lovari, 1991; Cuvier’s – Gazella cuvieri: Alados and Escós, 1992; et al., 2012). Females give births only once a year, in May (Blank et al., – Gazella subgutturosa: Marmazinskaya, 1999 and other 2015a), and most of them (up to 75% in years with favorable en- Gazella species: Wronski et al., 2010; sable – Hippotragus : vironmental conditions) produce twins, while younger and older fe- Thompson, 1993; mountain goats - Oreamnos americanus: Cȏte, 2000). males usually produce a single offspring (Kingswood and Blank, 1996). Individual traits, which help to achieve high rank, may be transmitted During their first weeks of life, goitered gazelle fawns stay alone through inheritance (Réale et al., 1999). The hierarchical relationships without their mothers for most of the day (Blank, 1985), with females established when animals are young depend on size and experience, returning to their offspring only to suckle. During these visits the young and their dominance is generally kept with age (Thouless and Guinness, receive a number of suckles before the mothers again leave for several 1986; Festa-Bianchet, 1991), in some species, however, females with more hours until the next bout of suckling. As their fawns grow, the offspring have a higher rank than barren females (mule deer - Koutnik, females stay with their offspring for longer periods of time until the 1981; - Ammotragus lervia: Cassinello, 1995), while there young reach the age of two months, when they start to follow their is no differences in others ( - Cȏte, 2000). mothers constantly (Blank, 1985). Young males leave their mothers A stable hierarchical environment tends to favor a reduction in the usually at the age of 6-7 months, while young females can stay with energy costs and risk of injury during fighting; therefore individuals try their mothers until the age of 2-3 years, forming the maternal family to avoid fighting with a dominant opponent when they have no chances group from individuals of different generations (Blank et al., 2012). to win (Clutton-Brock et al., 1979; Jackson, 1988). Consequently, in- I observed goitered gazelle behaviors in their natural of the itiators of conflicts win the majority of encounters (Rutberg, 1983; Altyn-Emel National Park (formerly the Kapchagai Preserve Bennett, 1986; Thomson, 1993). In many ungulate species, females are before the 1990s), which covered 4,600 km2 in the Hollow, south- organized in stable and highly linear hierarchies (mule deer – Odocoi- eastern Kazakhstan. My study spanned a 6-year period from 1981 to leus hemionus: Koutnik, 1981; bison – Rutberg, 1983; – Addax 1986, when the total population number fluctuated between 1500 and nasomaculatus: Reason and Laird, 1988; – Rangifer tarandus: 5000 gazelles. This study area was represented by a gravel desert, Hirotani, 1990; sable antelope – Hippotragus niger: Thompson, 1993; which was scarred with a thick net of dry river beds, karst craters and – Antilocapra Americana: Fairbanks, 1994; Nubian ibex – depressions, and intermingled with clusters of small hills and plateaus. nubiana: Greenberg-Cohen et al., 1994; mountain goat - Cȏte, Vegetation was scattered and represented mostly by desert dwarf 2000). shrubs, which were most abundant along the dry river beds. All animals In free-living goitered gazelles, a precise linear hierarchy is absent and especially goitered gazelles (Red Data Book from 1970s) in the because of their typically unstable groups and aggregations; in cap- Altyn-Emel National Park had been protected from human hunting for tivity, though, several females establish the highest status in hierarchy more than 15 years (Blank, 1990). and several females have the lowest status, while hierarchical positions When females compete directly with each other, the purpose for the of females of intermediate position change frequently (Marmazinskaya, conflict is often unclear (Clutton-Brock, 2007). Nevertheless, there are 1999). Of secondary sexual characteristics, a reciprocal definition of several expected causes of female-female aggression. The female com- social status occurs according to age, body size and degree of devel- petition hypothesis asserts that females aggressively compete for lim- opment, though individual features also have a significant importance. ited food resources or feeding sites with other conspecifics (Prins, 1989; Adult males are always dominant above females, but within intrasexual Alados and Escós, 1992; Roberts, 1996; Wronski et al., 2010). In tem- interactions, older individuals are dominant above younger animals. perate zones, forage amounts and quality decrease significantly during Between individuals of the same age and sub-adult gazelles of both cold seasons (autumn, winter), with shrinkage of pasture areas because sexes, domination and subordination often change. In goitered gazelles, of snow cover. This in turn leads to an increase in competition for an increase in aggressive interactions can be related to stress, starva- feeding sites and higher female-female aggression rates (Espmark, tion, breaking individual intervals and distances between groups, the 1964). According to this observation, I proposed that the same phe- presence of a large number of gazelles on pasture during migrations or nomenon would be observed in goitered gazelles in my study area in new individuals in a group, and even a female in estrous can be a cause the Kazakhstan deserts and suggested my first hypothesis that the of frequent aggressive contacts between females (Marmazinskaya, maximal frequency of female-female aggressive displays would be 1999). In other gazelle species (Cuvier’s gazelle – Gazella cuvieri and found during the season of low forage quantity and quality (October- gazelle – dama), the aggression of dominant females can March). suppress the reproduction of subdominants (Alados and Escós, 1992), Females of mountain goats (Cȏte, 2000) and red deer (Cervus ela- and in some antelope and deer species, receptive females use their phus – Clutton-Brock et al., 1982) interacted more often with animals of horns in conflict with other females for access to males (Bebié and similar rank. According to these studies I suggested that this also would McElligott, 2006; Bro-Jǿrgensen, 2011). In other ungulate species, fe- be true in my study and proposed my second hypothesis that adult fe- males interact with each other more aggressively in mixed-sex groups males of goitered gazelle would have more aggressive contacts with with more males (Weckerly et al., 2001). In many ungulates, females other adult females of similar social rank than with sub-adult females. displace each other, competing for forage-rich sites, comfortable resting Many studies have recorded female-female aggressive encounters, places, access to watering and salt lick locations (Alados and Escós, where passive displacements are one of the main causes of the female- 1992; Roberts, 1996; Clutton-Brock, 2009). Most investigations con- female aggressive interactions that occur frequently between females cluded that female-female conflicts are based on competition for a re- (Thouless, 1990; Alados and Escós, 1992; Lovari and Locati, 1993). source, but many agonistic interactions among social animals occur According to these observations, I proposed my third hypothesis that it where resources are not immediately at stake, and reciprocal aggression also would be common in goitered gazelle female-female aggressive is common (Clutton-Brock and Parker, 1995). In spite of the fact that behavior because of displacement of an opponent from her resting some information has been collected on female-female aggressive in- place. teractions, the specific causes of these conflicts are still poorly under- Females often compete fairly intensively for resources that are ne- stood (Clutton-Brock and Huchard, 2013). Therefore in this paper, I cessary for the successful rearing of young (Clutton-Brock, 2009). The want to analyze the main causes of female-female aggression in goi- female competition hypothesis suggests that female-female aggressive tered gazelles. contacts would be observed especially frequently during the time of The goitered gazelle is a medium-sized ungulate, which was ori- advanced gestation and rearing of young, and especially often im- ginally spread widely throughout Middle and Central Asia, , mediately after birth, because gestation and particularly lactation have , Turkey, and the Caucasus (Kingswood and Blank, 1996). very high energy costs (Hanwell and Peaker, 1977; Oftedal, 1985) that This species typically lives in small groups of 2-3 individuals (Blank can place a heavy burden on the female body condition and influence

187 D.A. Blank Behavioural Processes 164 (2019) 186–192 her ability to breed successfully in subsequent years (Clutton-Brock 3. Results et al., 1982, 1983) - or even to just survive (Putman and Langbein, 1992). The successful defense of feeding sites by lactating mothers in The most common aggressive display a dominant female had toward reindeer and caribou (Rangifer tarandus) leads these females to maintain a subdominant female was pursuit while in an almost neutral posture, their body weight (Kojola, 1989), which can reduce disease and the with only the tail raised (in 39%, N = 56 and 54%, N = 35 in May and mortality of their young (Reimers, 1993). Thus, regardless of the fact June, respectively). The aggressive female pursued the subdominant that the birthing period coincides with the most favorable seasons with most often while walking (68.9%, maximal access to high quality food (Thomson and Turner, 1982; N = 151; Fig. 1), less often by running (24.5%; Log-linear model Bowyer, 1991; Blank and Yang, 2015), females compete among them- test, Z = 2.512, P = 0.012, walk compared to run), and least often selves for access to birthing territories, or other resources necessary for through sudden jerking movements (6.6%, N = 151; Z = 3.620, conception and/or rearing offspring (Clutton-Brock, 2009). Based on P < 0.0001, jerk compared to run). In addition, the frequency of the these observations, I proposed my fourth hypothesis that in the Ka- female-female aggressive interactions fluctuated in similar ways for zakhstan population of goitered gazelles, the frequency of female-fe- different patterns (Log-linear Model test, P > 0.05), when aggressive male aggressive interactions would increase during advanced preg- behaviors were observed most often in May (57.0%, N = 151; Fig. 1), nancy (April) and the first weeks after birth (May), when the high less often in June (24.2%) and least frequently during other months energy costs of pregnancy and the intensive investment in early care (19%, N = 149) with significant differences between months (Log- immediately after birth requiring a maximal supply of milk (Blank and linear model test, Z = - 3.759-4.079, P < 0.0001, May compared to Yang, 2015), followed by a reduction of these displays in June. April, June-December). During these interactions, the dominant fe- males displayed a neutral posture (40.2% cases, N = 107) or threat posture (forehead directed forward – 49.8%) in almost equal proportion 2. Materials and methods (P > 0.05), while the dominance posture was demonstrated sig- nificantly less often compared to others (14%, N = 107; Log-linear For my research, I used the continuous focal observation Model test, Z = 2.885, P = 0.004 compared to threat posture). Threats method (Altmann, 1974). All behaviors for one focal individual were were sometimes accompanied by sounds similar to a male’s roaring, recorded by one observer during the entire observation period and were though in females the sounds were more gentle and soft (in 34.7% recorded in the order in which they occurred and each time they oc- cases, N = 49) and forehead threats occasionally escalated into fore- curred (all occurrence method). In most cases, gazelles were observed head-to-forehead butting (32.6%; Z = 3.478, P = 0.001 threat com- from distances of 50-100 m using binoculars (magnification 8x)ora pared to roaring and to butting), with almost the same frequency be- spotting scope (magnification 30x – 60x). Observation posts were tween roaring and butting (P > 0.05). In female-female interactions, usually established on elevations, from where I could typically see 30- females showed the threat posture more often (76.6%, N = 64) than the 50 gazelles at the same time; I chose to observe the female that was dominance posture (23.3% - Log-linear Model test, Z = 2.885, closest to the observation point. Similar to most studies of wild un- P = 0.004 compared to threat posture). gulates conducted without individual tagging (Stankowich and Coss, Dominant females sometimes approached too closely to a laying or 2006), and taking into account the heightened susceptibility to tran- standing subdominant female without any specific threatening displays, quilization and increased mortality during immobilization procedures but this was apparently accepted as aggression, since laying females got (Greth et al., 1993; Charles and Foster, 1999), my goitered gazelles up and walked away and standing females just retreated. This threat were not marked, and I was not able to identify most of them in- method was used most often in May (62.2% cases, N = 37; Fig. 1; Log- dividually. I was able to differentiate gazelles according to sex (horned linear Model test, Z = - 2.645, P = 0.008 compared to July), less in males and hornless females) and according to age (adult and sub-adult June (21.6%, Z = - 1.936, P = 0.053 compared to May) and rarely in females), and I was also able to recognize some females with distinctive other months (10.8% in April and 5.4% in July, N = 37; Z = - 2.645, features in coat coloration, especially for the period after giving birth P = 0.008 compared to May). In some cases, a dominant females tou- when they remained continuously in the vicinity of their hiding new- ched her opponent with her muzzle, but this was observed more rarely borns (Blank et al., 2015a). But, since most individuals were not (22.9% cases, N = 48) than when a female just came too close without identified, I established my observation posts in different parts of my touching (77.1%; Log-linear Model test, Z = 2.723, P = 0.006). Simi- study area (at a distance of at least 10 km apart) to reduce pseudo- larly cases of hindquarter sniffing were found significantly less often replication. Observations were done for as long as possible (up to (9.8% cases, N = 41) than just coming close (Log-linear Model test, 9 hours), recording all activities related to female aggressive behavior. Z = 3.267, P = 0.001 - sniffing compared to coming close). While observing these behaviors, I defined several behavioral patterns: Subdominant females walked away most often from a threatening neutral posture (walking to or away with a neutral position of head and female (61.3% cases, N = 80) and ran less often (38.7%), with a sig- tail), pursuing (walking or running after an opponent in a neutral or nificant difference between these cases (Log-linear Model test, threat posture), shark jerk (unexpected tossing one female to another in Z = 3.169, threat posture), threating (lowering head and directing forehead to- P = 0.002 walk vs run). Furthermore, these responses were ob- ward opponent), dominance display (directing forehead toward oppo- served mostly in May (Z = - 2.645, P = 0.008 compared to July), less in nent with head in upper position), butting (approaching each other June (Z = 2.553, P = 0.011 compared to July) and in April (Z = with lowered heads and leaning foreheads together), and roaring -2.387, P = 0.017 compared to May) and least in July. Sometimes the (producing soft wheezing sounds with widely opened mouth). The de- threatened female chose to stay in place and just turned to face her tail ethogram is presented in Table 1. opponent and/or threatened the aggressor in reply, putting her fore- Over the 6-year period of my study, I conducted 181 hours of focal head forward or displaying a dominant posture. Staying in place was observations in April, 470 hours in May, 374 hours in June, 173 hours observed less often in an attacking female than a retreating one (18.4% in July, 224 hours in November and 148 hours in December over the 6- vs 81.6% cases, respectively) with a significant difference (Log-linear year period. Model test, Z = 4.664, P < 0.0001 staying vs retreating). A female’s The Log-linear Model test was used for analyses of proportions of ears were directed backward and pressed to the head more often (75% separate behavioral acts. All statistical analyses were conducted using cases, N = 32) than directed aside when making a threat (Log-linear SPSS 22.0 software package. Model test, Z = 2.231, P = 0.026). Adult females made aggressive displays most often to sub-adult fe- males (57.6% cases), less often toward other adult females (42.4%,

188 D.A. Blank Behavioural Processes 164 (2019) 186–192

Table 1 Description of the recorded displays of aggression (ethogram) during female-female contacts in goitered gazelle within the study period according to Walther (1984), Blank (1998), Blank et al. (2015b).

Behavioral patterns Description

Threat posture Female approaches another female with her chin pressed to her neck and the sinciput (part of placement in males) directed toward her opponent or lowered toward the ground; ears are directed forward-sideward or backward and pressed to the neck; tail is in normal position or raised in an arc. Dominance posture A female is slowly walking, approaching to another in the dominance posture, with her chin pressed to her neck and forehead directed forward; ears are set apart with the foramen directed downward. Roaring Roaring consists of gruff, wheezing and hissing sounds. The female often raises her head, opens her mouth wide, takes a deep breath, then closes her mouth and passes air through her nostrils; roaring sometimes consists of a series of short sounds. Butting Rivals approach each other with heads lowered to the ground and lean their foreheads against each other. Each tries to move an opponent backward. During butting, the ears are apart horizontally and with the tops directed sideways or sometimes backward; tail is pressed to the rump. Low-stretch (neck-stretch) posture The head and neck are stretched forward horizontally; ears directed backward and pressed to the head in a position either parallel to the ground or slightly downward with the foramen inward; sometimes the ears are held with one apart from the other at a 45° angle; tail is raised to a horizontal position. Walk approach, neutral posture A female approaches closely to another by a slow walk in a neutral posture and drives her away; sometimes she makes a down-up movement with her muzzle as if this motion is a signal to compel her opponent to leave. Sharp jerk Unexpected fast running of one female after another female with her ears pressed back to her head. Playing run Female’s muzzle is lowered to the ground; she looks toward the adult female through the grass; waves her tail; presses the front body part to the ground as if a dog playing.

Fig. 1. Number of aggressive female-female interactions over months.

N = 139), with a significant difference between these cases (Log-linear 4. Discussion Model test, Z = 3.045, P = 0.002). Aggressive interactions were ob- served most often in May (57.6% cases, My first hypothesis stated that female-female aggressive interactions N = 139), less in June (24.5%) and April (13.7%), and least in July were related mostly to competition with conspecifics for limited food (4.3%, N = 139), with significant differences between months (Z = - resources or feeding sites. And since the worst forage condition and 4.342-4.886, P < 0.0001 April, June, July compared to May). Female- poorest quality content were found during the coldest period of the year female aggressive interactions were observed most often when an alien (October – March) (Blank, 1990), female-female aggressive interactions female came into the area established by a mother for her hiding fawns had to be more frequent during these months. However, my data and/or approached the mother’s fawn (61.7% cases, N = 120; Log- showed the opposite results when females demonstrated their max- linear Model test, Z = 5.202, P < 0.0001 compared to resting place imum aggressive interactions during the warm period, especially in competition), less often were cases of aggression seen when one female May and June, when forage conditions were good and high quality came too close to another (24.2% cases) and even more rarely during vegetation was in abundance (Blank, 1990). Thus, my data completely competition for a resting place (14.1%, N = 120), with no significant contradicted to my first hypothesis, and the frequency of aggressive difference (Z = 1.727, P = 0.084 close approaching compared to interactions was not associated with competition for limited forage resting place competition). Furthermore, these three cases had different resources. Still, for environments that typically do not have sufficient distributions of female-female aggression frequency over months, with amounts of food, it is likely that an acute lack of forage (and real the maximal bias toward May in the first case (expelling from area – starvation) could see an increase in the frequency of aggressive inter- 58.8%) and minimal bias in the third case (resting place competition – actions (Marmazinskaya, 1999). In the Arctic, with a permanent deficit 38.1%). of suitable feeding sites, for example, reindeer females (Rangifer tar- andus) demonstrated frequent agonistic behaviors during competition for places with better access to forage (Espmark, 1964). This, however,

189 D.A. Blank Behavioural Processes 164 (2019) 186–192 was not the case in my study area. parturition, pregnant females of many ungulate species isolate them- My second hypothesis predicted that females of the same social rank selves and their offspring from conspecifics for protection from pre- would interact more often than females of different social status dators, but also, and more importantly, to establish a strong, selective (Clutton-Brock et al., 1982; Cȏte, 2000). In other words, adult goitered mother-young bond (Lent, 1974; Ciuti et al., 2006). The isolation allows gazelle females would demonstrate their aggressive behavior mainly the mothers to identify their offspring by their individual olfactory, toward other adult females and would show them more frequent ag- visual and vocal characteristics. Bonding time periods, though, are gressive displays than toward sub-adult females. My data demonstrated different between hider and follower species (Keller et al., 2003; that indeed mothers had frequent aggressive interactions with other Poindron et al., 2007; Blank and Yang, 2017). Since contact between adult females, however, aggressive displays toward sub-adult females hiding young and their mothers is initially much more limited, mothers were observed significantly more often than toward adult females. So of hider species require a longer period of time than follower species to my data did not support my second hypothesis, either. study the individuals cues of their young and establish their mutual My third hypothesis proposed that one of the main causes of female- mother-young bonds. In contrast, the young of follower species stay female interactions was the displacement of an opponent from an at- with their mothers continuously, allowing for more immediate re- tractive resting place (Prins, 1989; Thouless, 1990; Alados and Escós, cognition and bonding (Blank and Yang, 2017). Nevertheless both un- 1992; Lovari and Locati, 1993) - for example, displacing each other gulate mothers individually recognize their neonates typically within from bedding sites located in shady areas during hot afternoons (Hass, hours or more rarely within 1-2 days after birth (Poindron et al., 2007). 1991). My data demonstrated that indeed goitered gazelle females did In my study, however, goitered gazelle mothers strived for isolation and have aggressive interactions related to competition for resting places. demonstrated their high levels of aggressiveness to other females ap- This behavior is common for many ungulate species when older and proaching their fawns’ hiding places during at least the first several more dominant females drive away younger females from resting places weeks postpartum. The point here is that, immediately after giving (argali – Ovis ammon: Fedosenko and Blank, 2005; Siberian ibex – Capra birth, goitered gazelle mothers can only distinguish their own young sibirica: Fedosenko, 2003). However, aggressive interactions for bed- when close to them using olfactory cues and are limited to recognizing ding sites between goitered gazelle females were observed least often just the location of their fawns’ hiding places – not their fawns directly - compared to other causes (expelling from area and close approach). from a distance. Only after several weeks are the mothers able to re- Furthermore, since competition for a resting place could happen at any cognize their fawns at greater distances using visible or vocal cues time of year, the frequencies of aggressive interactions between females (Blank and Yang, 2017). This is likely due to problems of distant re- would have to be distributed evenly over months, without a significant cognition (Blank and Yang, 2017) as each mother with her fawns oc- bias for any particular month. My data demonstrated that though the cupied a certain area within which her fawn stayed alone during the frequency of female-female interactions because of resting place com- first several weeks of life (Blank et al., 2015a), while the mother did not petition had a more even distribution over months than the two other allow any other females to bring their alien fawns into her territory. As causes, it also had some bias toward May. Thus, my data contradicted a result, females with fawns dispersed all over the suitable territories my third hypothesis almost completely and competition for a resting during their birthing period. Though these areas have no precise bor- place was not a main cause of the female-female aggressive interac- ders that are strongly protected against intruders (like in male rutting tions. territories), a mother prevents other females, especially sub-adults, The fourth hypothesis predicted that females would compete for from approaching the area with her hiding fawn by demonstrating birthing grounds with access to resources necessary for rearing off- aggressive patterns of behavior (Blank, 1994; Marmazinskaya, 1999). spring (Clutton-Brock, 2009) and show aggressive interactions most Sub-adult males leave their mothers at the age of 6 months during often during advanced gestation and during the first month after giving rutting season, when adult males drive them away from their mothers; birth, when a mother’s energy costs are the highest (Hanwell and sub-adult females, on the other hand, can stay with their mothers sig- Peaker, 1977; Oftedal, 1985). According to this hypothesis, the fre- nifi cantly longer (2-3 years), forming mother-daughter groups (Festa- quency of female-female aggressive interactions in goitered gazelle Bianchet, 1991; Marmazinskaya, 1999). Mothers allow their sub-adult would increase during advanced pregnancy in April and reach a max- daughters to follow them all year round, except during the birthing and imum immediately after giving birth in May, since lactation, which is early postpartum period, when they very aggressively chase them away especially intensive during the first weeks postpartum, requires the from the birthing area, in spite of the constant insistence of their highest energy investment from females (Blank and Yang, 2015). daughters to follow their mothers (Zhevnerov and Bekenov, 1983; Therefore, forage demands would be highest during May and mothers Blank, 1994). It seems obvious that this was the case in my study, when would demonstrate aggressive displays especially frequently (Oftedal, sub-adult females tried to follow their mothers after the new offspring 1985). In subsequent months (June-July), the milk supply for goitered were born. The older offspring were not tolerated in the vicinity of the gazelle offspring decreases, reducing the mother’s energy costs and mother’s hiding young; and since sub-adult females purposely ap- competition for forage, so the frequency of observed agonistic beha- proached their mothers, then the adult females were more often ob- viors would decline considerably, reaching a minimum after suckling served in aggressive conflicts with sub-adult females (daughters) com- was terminated (September-December). At first glance, my data sup- pared to aggressive interactions with other adult females (other ported this hypothesis. Indeed, goitered gazelle females demonstrated mothers), which also from time to time crossed into each other’s oc- maximal frequency of aggressive interactions in May, less in June, with cupied areas. Since there was a high interest in fawns by both sub-adult a gradual decline thereafter, though April, in contrast to this hypoth- and other adult females, they often approached hiding places and esis, also showed a low intensity of female-female aggressive interac- forced the young to stand and move around, depriving the fawns of the tions. According to the logic of this hypothesis, mothers would protect main advantage to hiding - to be undetectable by predators during the their birthing grounds particularly from other mothers with similar period when they were unaccompanied. And making the hiding posi- forage demands, and they would display aggressive behaviors to other tion of fawns known for predators was very likely a second cause why mothers most often, paying less attention to sub-adult females (Roberts, the mother tried to expel all other females from the area of her hiding 1996). However, my data demonstrated that goitered gazelle mothers fawn. displayed more aggressive patterns toward sub-adult females than other After several weeks (mid-June), the growing fawns started to spend adult females. This means, then, that the main cause of female-female longer periods of time with their mothers, which enhanced the mothers’ aggressive behavior in goitered gazelles was not forage protection on abilities to visually recognize their own fawns from a greater distance their birthing grounds, but some other reason. (Blank and Yang, 2017). Fawns began to leave their hiding places more I have another possible explanation for this phenomenon. Before and more to move around independently from their mothers; and as

190 D.A. Blank Behavioural Processes 164 (2019) 186–192 their running abilities considerably improved, their mothers monitored 149–155. their hiding fawns less and less (Blank, 2017). As a consequence, the Blank, D.A., Ruckstuhl, K., Yang, W., 2015a. Antipredator strategy of female goitered ’ gazellles (Gazella subgutturosa Guld., 1780) with hiding fawn. Behav. Proc. 119, mothers intolerance to other females gradually disappeared through 44–49. June, and the intolerance dropped drastically in July, when aggressive Blank, D., Ruckstuhl, K.E., Yang, W., 2015b. Seasonal dynamics of agonistic displays in displays between females became negligible. From July on, mothers did territorial and non-territorial males of Goitered gazelle. Zoology 118, 63–68. Blank, D.A., Yang, W., 2015. Strategy of goitered gazelle suckling behavior and its not oppose being followed by sub-adult females and formed into female adaptation to the environment. . Res. 60 (4), 393–401. groups with them (Blank et al., 2012). In July, the fawns’ hiding period Blank, D.A., Yang, W., 2017. Mother-young recognition in goitered gazelle during hiding ended (Blank and Yang, 2015) and mothers and fawns started to move period. Behav. Proc. 142, 21–28. more widely with a weak attachment to any specific locations. Without Bowyer, R.T., 1991. Timing of parturition and lactation in southern mule deer. J. Mammal. 72 (1), 138–145. individual birthing areas, aggressiveness between adult females de- Bro-Jørgensen, J., 2007. The intensity of sexual selection predicts weapon size in male clined to very low levels, with female-female aggressive interactions bovids. Evol.: Int. J. Org. Evol. 61 (6), 1316–1326. ǿ fl occurring over resting places, breaking individual distances and ap- Bro-J rgensen, J., 2011. Intra- and intersexual con icts and cooperation in the evolution of mating strategies: lessons learnt from ungulates. Evol. Biol. 38, 28–41. proaching an alien herd (Marmazinskaya, 1999). Similar aggressive Byers, J.A., 1997. American pronghorn: social adaptations and the ghost of predators behaviors of mothers toward conspecifics, especially toward sub-adult past. University of Chicago Press, Chicago. females that approached hiding fawns, were observed in Cassinello, J., 1995. Factors modifying female social ranks in Ammotragus. Appl. Anim. Behav. Sci. 45, 175–180. (Autenrieth and Fichter, 1975) and two roe deer species (Capreolus Charles, A., Foster, M.A., 1999. Immobilization of goitered gazelles (Gazella subgutturosa) capreolus, C. pygargus – Danilkin and Hewison, 1996). Aggression of and Arabian mountain gazelles (Gazella gazella) with xylazine-ketamine. J. Zoo and mothers toward other females during the first days after giving birth Wildl. Med. 30 (3), 448–450. Ciuti, S., Bongi, P., Vassale, S., Appollonio, M., 2006. Influence of fawning on the spatial also was found in argali (Ovis ammon), though this species has a very behaviour and habitat selection of female fallow deer (Dama dama) during late short (only a few days) hiding period (Fedosenko, 2000; Fedosenko and pregnancy and early lactation. J. Zool. Lond. 268, 97–107. Blank, 2005). In addition, isolating pregnant females from their herds Clutton-Brock, T., 2007. Sexual selection in males and females. Science 318, 1882–1885. Clutton-Brock, T., 2009. Sexual selection in females. Anim. Behav. 77, 3–11. prior to parturition and their solitary life during the initial few-weeks Clutton-Brock, T.H., Albon, S.D., Gibson, R.M., Guinness, F.E., 1979. The logical stag: after birth were observed for many cervids and bovids (reviewed by adaptive aspects of fighting in red deer (Cervus elaphus L.). Anim. Behav. 27, Lent, 1974). Unfortunately the mothers’ aggression toward other fe- 211–225. males was not specifically considered in most reports. Clutton-Brock, T., Albon, S.D., Guinness, F.E., 1982. Competition between female re- latives in a matrilocal mammal. Nature 300, 178–180. So I concluded that the female-female aggressive interactions that I Clutton-Brock, T., Guinness, F.E., Albon, S.D., 1983. Costs of reproduction to red deer observed in my wild population of goitered gazelles were related to hinds. J. Anim. Ecol. 52, 367–383. competition for birthing grounds, but that the reason for this behavior Clutton-Brock, T., Huchard, E., 2013. Social competition and its consequences in female mammals. J. Zool. 289, 151–171. was associated not with competition for forage but rather with the Clutton-Brock, T., Parker, G.A., 1995. Punishment in animal societies. Nature 373, mother’s desire to be isolated with her fawn from conspecifics to es- 209–216. ȏ tablish a mother-young bond and to keep her hiding fawn separated C te, S.D., 2000. Dominance hierarchies in female mountain goats: stability, aggres- siveness and determinants of rank. Behaviour 137 (11), 1541–1566. from alien fawns due to the slow development of distant visual and Cunningham, P.L., Wronski, T., 2011. Sex ratios of Gazella sub- auditory recognition. In addition, enforcing separation protected her gutturosa marica Thomas, 1897 in the Mahazat as-Sayd protected area, Saudi Arabia. fawn from being disturbed and revealed by alien females, which would Mammalia 75, 243–248. ff ’ Danilkin, A., Hewison, A.J.M., 1996. Behavioural Ecology of Siberian and European roe jeopardize the o spring s ability to remain undetected from predators. Deer. Chapman and Hall Publication, London-New York-Madras. Espmark, Y., 1964. Studies in dominance-subordination relationship in a group of semi- Acknowledgments domestic reindeer (Rangifer tarandus L.). Anim. Behav. 12, 420–426. Fairbanks, W.S., 1994. Dominance, age and aggression among female pronghorn, Antilocapra Americana (Family: ). Ethology 97, 278–293. I thank the Chinese Academy of Sciences (CAS) for The Main Service Fedosenko, A.K., 2000. Argali in Russia and adjacent countries: Status, ecology, behavior, Project of Characteristic Institute (TSS-2015-014-FW-1-2) for granting conservation and economic use. Publication of GU Centrokhotcontrol, Moscow (in our work and creating all conditions for writing this paper. I am very Russian). Fedosenko, A.K., 2003. Siberian ibex in Russia and adjacent countries: Status, ecology, grateful to the Institute of Zoology, former Academy of Sciences of behavior, conservation and economic use. Publication of GU Centrokhotcontrol, Kazakhstan, which has given us the possibility to study of goitered Moscow (in Russian). – gazelles in their natural environment for 10 years. I am grateful to Ms. Fedosenko, A.K., Blank, D.A., 2005. Ovis ammon. Mamm. Spe. 773, 1 15. Festa-Bianchet, M., 1991. 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