- Email: [email protected]
Does social status of males change their aggressive behavior repertoire in goitered gazelle (gazella subgutturosa guld., 1780)?
Behavioural Processes 108 (2014) 20–26
Contents lists available at ScienceDirect
Behavioural Processes journal homepage: www.elsevier.com/locate/behavproc
Does social status of males change their aggressive behavior repertoire in goitered gazelle (gazella subgutturosa guld., 1780)? D.A. Blank a,b , W. Yang a,∗ a Key Laboratory of Biogeography and Bioresource in Arid Land, Xinjiang Institute of Ecology and Geography, The Chinese Academy of Sciences, Urumqi, China b Institute of Zoology, Kazakh Academy of Sciences, Alma-Ata, Kazakhstan
a r t i c l e
i n f o
Article history: Received 6 July 2014 Received in revised form 23 August 2014 Accepted 11 September 2014 Available online 18 September 2014 Keywords: Aggressive behavior Goitered gazelle Social status Territorial male
a b s t r a c t Aggression in ungulates is a very common behavior which serves a great variety of social functions, the most important of which is territorial protection from intruders. Typically during the rut, territorial males in Antilopinae species have access to mating females, and territoriality leads to a drastic change in the males’ lifestyle as they spend most of their aggressive efforts on protecting their territories from other males. In contrast, non-territorial males generally behave in a constant manner all year round, with most of their aggression spent on hierarchical interactions within groups. In this paper, we discuss the differences in aggressive behaviors between territorial and non-territorial males of goitered gazelles (Gazella subgutturosa). We found that territorial males of this species demonstrated most of their aggressive displays, such as threat postures and space-claim patterns, to other territorial males-neighbors, but rarely chased after them at the end of a conflict. Inversely, territorial males frequently chased non-territorial and immature males while only occasionally demonstrating aggressive patterns. Non-territorial males mostly chased other males in their agonistic interactions, displaying threat postures less often than territorial males, but also showing aggressive patterns not found in territorial males. So we concluded that territorial and non-territorial males of goitered gazelles had different repertoires of aggressive behaviors, and when adult males switched their social status from territorial during the rut to non-territorial outside the rut, they obviously changed their preference in aggressive behaviors accordingly. © 2014 Elsevier B.V. All rights reserved.
1. Introduction In Antilopinae species aggressive interactions occur among all sexes, ages, and social classes (Walther et al., 1983). Aggression serves a great variety of social functions, and it is hard to find any part of the social life of bovids where aggression is not involved (Walther, 1984; Rajagopal et al., 2010). Also aggression has shown to be a powerful mechanism for intra-sexual and natural selection among males leading to sexual dimorphism in the size and shape of the horns and body proportions (Lundrigan, 1996; PerezBarberia et al., 2002; Bro-Jorgensen, 2007; Wronski et al., 2010). Furthermore, though there are several roles for aggressive behavior in bovid life, one of its most important functions for adult male gazelles, who compete for mates, is establishing and ratification of their individual territorial borders and preventing invasion from other males’ (Walther et al., 1983).
∗ Corresponding author. Fax: +86 991 7885320. E-mail addresses: [email protected] (D.A. Blank), [email protected] (W. Yang). http://dx.doi.org/10.1016/j.beproc.2014.09.017 0376-6357/© 2014 Elsevier B.V. All rights reserved.
Aggressive behavior has been investigated in detail for several gazelle species, including the Thomson gazelle (Eudorcas thomsoni—Walther, 1978), Grant’s gazelle (Nanger granti—Walther et al., 1983) and mountain gazelle (Gazella gazella—Grau and Walther, 1976), but never has it been a subject of special consideration for the goitered gazelle (Gazella subgutturosa). In goitered gazelle, the majority of adult males establish individual territories during the rut in November–December, and a few also show territoriality during a “false” rut in April–May, though the majority remains non-territorial at this time. Non-territorial males continue their daily movements during the rut as all males do outside of the rutting period (Blank et al., 2012). During the rest of the year, goitered gazelles do not show territoriality at all. In Antilopinae species, territorial males are the most likely to have access to mating females, and territoriality requires drastic changes in their behaviors during the rut, because they spend most of their aggressive efforts protecting their territorial borders from other males (Walther et al., 1983). In contrast, non-territorial males generally behave the same way all year round, with most of their aggressive efforts spent in hierarchical interactions within groups (Blank, 1992). In this paper, we discuss whether territorial and
D.A. Blank, W. Yang / Behavioural Processes 108 (2014) 20–26
21
non-territorial goitered gazelle males behave similarly or differently during their aggressive interactions and whether their aggressive repertoires consist of different behaviors. We theorized that aggressive behaviors seen in goitered gazelles would be similar on the whole to such behaviors in other gazelle species. Walther (1978) found that territorial Thomson’s gazelle bucks demonstrated reciprocal threat displays toward each other, while one-sided displays were directed toward non-territorial bachelors. Based on this study, we predicted our first hypothesis for goitered gazelles that territorial males also would demonstrate reciprocal displays to each other more frequently than non-territorial males, and they would do it without chasing one another during their aggressive interactions with their neighbors, while onesided displays with chasing would be typical for interactions between territorial males and non-territorial males. In addition, non-territorial males would have a consistent behavior and would show more displays to their peers and less to immature males. Furthermore, the goitered gazelles’ repertoire of agonistic displays would be similar to aggressive behaviors of other gazelle species. Walther (1984) noted that during pauses in agonistic encounters, some additional displays may be observed that are not clearly aggressive behaviors, such as threat postures, but are still related to agonistic behavior. These behaviors have been called space-claim displays, and include the grazing ritual, object-horning, and marking with urine/feces and preorbital glands. Walther found that territorial males of some gazelles use these displays mostly during their territorial conflicts, while this behavior is not typical for non-territorial males (Walther, 1984). So we predict our second hypothesis that mostly territorial males of goitered gazelles would perform space-claim displays and non-territorial males would not. Walther et al. (1983) also found for Thomson’s gazelle that territorial males displayed clash-fighting in their conflicts with neighbors, while non-territorial males prefer horn-pressing fighting instead. So we supposed that it would be true for goitered gazelles as well and predicted our third hypothesis that territorial males in the rut would show only clash-fighting in conflicts with peers, while non-territorial males would use horn-pressing fighting. Walther (1978) found that fighting territorial Thomson’s gazelle males never ran from each other after conflict but instead walked away, while they frequently chased when engaged in conflicts with non-territorial and immature males. So we predicted our fourth hypothesis that this behavior would apply to goitered gazelles as well, and a territorial male would mostly walk during agonistic interactions with his neighbors, while he would use a faster gait (trot and gallop) in interactions with non-territorial and immature males. Additionally, it was reasonable to assume that non-territorial males would also demonstrate similar behaviors and mostly walk when engaged with peers and use faster gaits in encounters with immature males.
of 50–100 m, with observation posts usually established on elevations, from where we could see usually 30–50 gazelles at the same time. During the rut, the goitered gazelle territory size was 50–80 ha (Blank, 1985), and we typically could observe 5–6 individual territories simultaneously from our elevated observation sites. Since, females were distributed unevenly among territories (Blank, 1998), we chose a male closest to the observation point that had at least one female in his territory. To avoid pseudoreplication, we changed our observation sites every several days and tried to observe gazelles in different parts of the study area (over ∼4600 km2 ). The total size of the study population in the Ili depression was estimated to range from 1.5 thousand in 1981 up to 5 thousand in 1986 (Blank, 1990). For focal observations we used binoculars (magnification 8×) and a telescope (magnification 30×–60×). We conducted 181 h of focal observations in April, 470 h in May, 374 h in June, 173 h in July, 59 h in August, 60 h in October, 224 h in November and 148 h in December over the 6-year period. We investigated the frequency changes in aggressive noncontact displays and actual fights (battles) according to the breeding cycle, and distinguished three biological seasons for the goitered gazelle: rutting season (November–December), “false” rut (April–May), and outside the rut (June–October); data were absent or too scarce for January, February, March, and September. For our analyses in this paper, we distinguished two kinds of agonistic behavior in goitered gazelles: aggressive displays in which we included all agonistic displays of one male to another with no physical contact; and fights (or battles) which included any form of physical agonistic contact (Walther et al., 1983). An ethogram of the main agonistic displays is listed in Table 1. We differentiated gazelles according to sex (horned males and hornless females) and age (adult and immature males, and adult and immature females), which was defined according to the descriptions provided by Zhevnerov (1984): adult males (older than 2 years old—horns 1.5 times longer than ears and absence of the black spot on the front of the muzzle), adult females (older than 2 years old—hornless and absence of black spot on the front of the muzzle), sub-adult males (1–2 years old—horns are equal or shorter than ears and presence of a black spot on the muzzle front), and sub-adult females (1–2 years old—hornless and black spot on the muzzle front). Young (up to 1 year old—body size is smaller in 2–3 times compared to adult gazelles and black sport on the muzzle front) were also noted, but we did not use our observations of either young or females for this paper. Our data had a nonparametric statistical distribution according to the Shapiro-Wilk and Kolmogorov-Smirnov tests. We used the Mann-Whitney U test to compare two types of fighting, as well as the Chi-squared goodness-of-fit test for comparing proportions of rare aggressive displays. The Log-Linear Model test was used for analyses of the frequencies of separate behavioral acts. All statistical analyses were conducted using SPSS 17.0 software package.
2. Materials and methods
3. Results
Our observations were conducted in the Ili depression (southeastern Kazakhstan) during a 6-year period from 1981 to 1986. We mostly did focal animal observations, concentrating on only one randomly selected group of gazelles (usually the closest) at a time, continuously observing the separate group members for up to 9 h and recording all aggressive displays and fights (battles) that accompanied territorial defense, breeding or social behavior. Gazelles were determined to be members of a group if they were less than 50 m from each other, moved in the same direction and stayed together for longer than half an hour. All of the behaviors were recorded in the order in which they occurred and each time they occurred. In most cases, gazelles were observed from distances
Territorial males performed mostly reciprocal displays to other territorial males (86%, N = 78) and considerably less often one-sided displays (Log-Linear Model test, Z = 2.483, P = 0.013). In contrast, during interactions with non-territorial bachelors or immature males, territorial males used mostly (for adult males) or only (for immature) one-sided displays (Fig. 1), while non-territorial bachelors or immature males usually did not answer to the aggressive displays of territorial males (Log-Linear Model test, Z = −5.112, P < 0.001). During aggressive interactions of two territorial males, rivals most often used frontal threat displays, slightly less often the behaviors of bush and ground horning, the grazing ritual, walking parallel to each other and/or looking at their opponents (95%,
22
D.A. Blank, W. Yang / Behavioural Processes 108 (2014) 20–26
Table 1 Description of the recorded aggressive displays (ethogram) in adult goitered gazelle males during observations based on Walther et al. (1983) and Blank (1998). Posture
Description
Clash-fighting of territorial males
After preliminary threat displays, rivals run toward each other and clash together, which can be heard at the distance of 700–800 m. When the horns are almost invariably interlocked, each rival tries to press the horns and head of the opponent to the ground and push him back. They then separate again, moving backward and repeat the same clashing actions. At the end of the fight, both rivals return to their own territories from opposite directions. During a long, intensive fight, the combatant’s heads and necks are twisted aside, and they fight with their necks, when the horns are interlocked; the rival tries to twist the neck of his opponent upward-sideward, when the neck is twisted back. Sometimes, the muzzle, neck or front parts of the breast are hooked by the rival’s horns, which hit these parts. Opponents open their mouths widely and roar constantly. Their tails are pressed to their hindquarters. Typically without preliminary threat displays, rivals approach each other with heads lowered to the ground and lean the front surfaces of their horns against each other. They fight while standing on all four legs with the forelegs widely spread, and hind legs in a normal position or relatively close together. Each tries to press the horns of the opponent to the ground and move him backward. Then every rival hits the opponent’s head with maximum power and presses his head to the ground and back, making jerks. The horns almost invariably interlock (horn of one between horns of another). This fight can transfer to fight-circling, when rivals with locked horns move in circles. In this case, they pivot with their hindquarters while keeping their heads in the center of the circle. During fighting, the ears are apart horizontally and directed sidewise at the top or sometimes backward and the tail is pressed to the rump. This fight is common for non-territorial males. Horns are directed toward opponent. Ears are directed forward-sideward; tail is in normal position. Rivals stand in lateral T-position, parallel or, most commonly, a reverse-parallel orientation. The posture is erect, with the neck vertically erected upwards “proudly”. The entire body is as high as possible due to all four legs stretched up. The muzzle top is pressed to a throat and the horns are directed forward with the head is turned in a more or less pronounced fashion away from the opponent. Tail is uplifted and making waving movements from one side to the other; ears are apart horizontally and directed sidewise at the tops, with the ear holes directed forward or downward. All walking movements are unusually slow. In the case of shrub or saxaul (Haloxylon aphyllum) horning, the male approaches the tree in a dominance posture (head level with the body, horns directed forward, ears apart), sniffs the bare trunk, positions the trunk between the horns and thrashes with the forehead, goring the trunk with the power of his whole body; he cleans small branches from bigger ones and breaks some shrub’s branches, with pauses to smell the scratched vegetation, which he touches with his muzzle top after every 2–3 thrashing acts before continuing to horn. The ears stay apart horizontally and slightly backward (45◦ ) at the tops and downward by the ear holes. Head movements are up-down along the branch and from side to side, sometimes round the head axis and he pushes the shrub with the entire body and trying to scratch as high as possible. A buck sniffs points of low grass and starts to horn, scratches and gores the plants and naked ground, making sharp horning movements from one side to another and setting his horns against the ground, as if trying to shift the ground like he does with his real rival. Two territorial males meet at the boundary of neighboring territories, threatening and fighting each other. After several clashes, they simultaneously begin to graze and step backwards. If they do not renew the fight, permanent grazing leads to enlargement of the distance. The longer the grazing ritual lasts, the greater the distance becomes. Sooner or later, they turn into a reverse (hindquarters to hindquarters) position and move farther and farther away from each other, each of them grazing back toward the center of their own territory. A lateral display of two males engaging in a slow, tense, regular walk in parallel same or opposite directions to each other; horns are held high, and often their hair is raised. One male looks attentively for any movements of the other male. One or both opponents freeze in an agonistic posture and hold it for several seconds, then continue their displays. Stepping forward and stretching the body, lowering the belly toward the ground, with the hind legs sloping backward; urination with a lifted tail. Abrupt bringing hind legs forward so that the hooves are placed lateral to the stationary forelegs, squatting closer to the ground and taking a crouched posture and defecating. One male follows the other, often roaring toward his opponent and demonstrating threat or dominant postures. This is a typical behavior of territorial males that expel intruders from their territories. Stretching the head and neck forward horizontally with the nose pointing horizontally forward. Ears are directed backward and usually pressed to the head in a position either parallel to the ground or slightly downward with the foramen inward. Rarely ears are laid back, pressed to each other, or held one apart of the other at a 45◦ angle. The tail is lifted to varying degrees, up to a vertical position. Head and neck are stretched forward and upward up to 45◦ above the horizontal, the top of the muzzle is lifted forward and upward, and the ears are pressed to the head. The ritualized act of marking with the male’s preorbital glands rarely begins with sniffing the plant stem or twig. Instead, the goitered gazelle male opens both preorbital glands, sometimes opening his mouth at the same time, and carefully lowers the preorbital region toward the plant stem, bringing the stem’s tip or twig into the widely opened gland. With quivering movements of the gland‘s margin, he deposits some secretions which soon hardened in the open air. The male sometimes marks the same plant stem a second time using either the same or his other preorbital gland. To position himself for scent marking, the male commonly stretches his head upward to get his preorbital gland as high as possible, although he never raises his body to stand on just his hind legs for this purpose. Roaring consists of gruff, wheezing or hissing sounds resembling gurgling or sneezing. In producing these sounds, the male open his mouth wide, lifts his tongue slightly and takes a deep breath, then closes his mouth and passes air through his nostrils or possibly through his partly closed mouth. Posture: Muzzle is raised to an angle of up to 45◦ from a horizontal position. Ears are directed backward and tightly pressed to the head with the ear holes inside. Abruptly, the male jerks his head and whole body forward and upward, and his protruding thyroid cartilage moves up and down. When running, roaring is intermittent. One male approaches another to a very close distance, breaking an individual distance and forcing the opponent to retreat or start battling. One male approaches another very closely and touches his opponent’s body (usually hindquarters) with his muzzle. In a mating bipedal posture, one male follows the hindquarters of another male keeping in a bipedal position for several seconds. One male approaches the other to a close distance, trying to sniff any body part (often hindquarters) of his opponent.
Horn-pressing fights of adult males
Frontal threat posture Dominance
Bush horning
Ground horning
Grazing ritual
Parallel walk Looking to opponent Display freezing Urination Defecation Chasing Low-stretch
High- stretch Preorbital marking
Roaring
Close approaching Muzzle touching Mating posture Sniffing opponent
D.A. Blank, W. Yang / Behavioural Processes 108 (2014) 20–26
23
Table 2 Frequency of various aggressive patterns in encounters of males with different age and social status. Behavioral patterns
Frontal threat Bush horning Grazing ritual Parallel walking Looking to opponent Ground horning Display freezing Urination-defecation Chasing Dominance Low-high-stretch Preorbital marking Chasing roaring Close approaching Muzzle touching Mating posture Sniffing opponent
Territorial vs.
Non-territorial vs.
Immature vs.
Territorial
Non-territorial
Immature
Non-territorial
Immature
Immature
123 90 95 49 41 43 35 36 21 0 3 5 28 0 0 0 0
89 40 3 5 50 2 1 19 254 27 25 7 111 0 0 0 0
19 2 0 0 7 1 0 1 87 2 32 0 30 0 0 0 0
60 11 12 19 10 9 8 3 116 37 1 1 83 30 2 9 6
24 3 1 0 1 0 1 0 89 17 19 0 24 20 12 11 4
13 4 1 0 0 0 2 0 21 6 0 0 14 9 0 0 2
N = 458; Table 2), rarely did they chase one another at the end of their demonstrations (5%) (Z = 8.788, P < 0.001). Conversely, territorial males often chased non-territorial and immature males (58%, N = 439 and 77%, N = 113, respectively) after aggressive displays (42% and 24%) or even without them (16% and 53%, respectively) (Log-Linear Model test, Z = −2.700 and −4.664, P = 0.007 and <0.001, respectively). In addition, territorial males addressed most of their roaring-chasing to non-territorial males and considerably less to peers and immature males (Log-Linear Model test, Z = 5.180 and 6.445, P < 0.001 for both). Furthermore, territorial males exhibited a poorer repertoire (less variability) of aggressive displays to non-territorial bachelors and even less to immature males compared to aggression displays with peers (Log-Linear Model test, Z = −4.496 and −8.635, P < 0.001, respectively), and chased after non-territorial bachelors most often, immature males less often and peers least often (Z = −5.465 and −7.866, P < 0.001, respectively; Table 2). Non-territorial males performed one-sided displays with their peers and immature males with the same frequency (Log-Linear Model test, Z = 0.353, P = 0.724), though reciprocal displays were slightly more typical for encounters of non-territorial adult males with their peers (Z = 1.959, P = 0.05). In contrast, immature males demonstrated mostly reciprocal displays with their peers (Fig. 1). Similar to territorial males, non-territorial males used mostly threat displays (Log-Linear Model test, Z = 2.018–2.553, P = 0.011–0.014), but at a lower rate compared to territorial bucks (Z = −5.682,
Fig. 1. Proportion of reciprocal (Reciproc) and one-side displays (one-side) in encounters of males with different social status: T–T—territorial male vs. territorial male; T–N—territorial male vs. non-territorial males; T–I—territorial male vs. immature; N–N—non-territorial male vs. non-territorial male; N–I—non-territorial male vs. immature; I–I—immature vs. immature.
P < 0.001), and they performed other agonistic displays more rarely as well (Z = −2.390, P = 0.017; Table 2). Only chasing and roaring-chasing were observed more frequently in non-territorial males than even threat displays (Log-Linear Model test, Z = 5.682, P < 0.001 for both). In contrast to territorial bucks, non-territorial males addressed most of their roaring-chasing to peers (Z = 5.007, P < 0.001). There were four agonistic displays that were not found in territorial males and only observed in non-territorial and immature males: close-approaching, sniffing, touching and mating posture (Table 2). Among space-claim displays of aggression, the grazing ritual was very typical for boundary encounters between territorial males (95%, N = 91), but rarely observed in displays addressed to bachelors (1.4%, N = 219) and never toward immature males (Z = 4.085, P < 0.001) (Table 2). Non-territorial males used the grazing ritual infrequently in their aggressive displays toward their peers (9.2%, N = 130) compared to contests between territorial males (Chi-squared goodness-of-fit test, Chi-squared = 60.840, df = 1, P < 0.001), and only accidently toward immature males (1 case); immature males used this ritual exceptionally rarely (only 1 observed case during the entire study period; Table 2). Among other space-claim displays, territorial males preferred object-horning (bush and ground horning) directed to their peers, especially in November–December (67–74%, N = 52 and 74); considerably less often space-claim demonstrations consisted of urine and feces marking during aggressive displays (22-29%; Log-Linear Model test, Z = −2.677, P = 0.007) and very rarely preorbital gland markings (4%; Z = −4.055, P < 0.001). Territorial bucks demonstrated similar behaviors to non-territorial males, preferring object-horning to other space-claim displays as urination-defecation and preorbital markings (Log-Linear Model test, Z = 2.959, P = 0.003), but the frequency of these displays was observed less often compared to the aggressive interactions of territorial peers to one another (LogLinear Model test, Z = −2.126, P = 0.034). Territorial bucks did not demonstrate space-claim displays to immature males at all, while non-territorial bucks and especially immature males used spaceclaim behaviors accidently. When territorial males fought, they mostly engaged in demonstrations of clash-fighting (80%, N = 15) and rarely used horn-pressing fights (Mann-Whitney U, Z = −3.720, P < 0.001), while when fighting with bachelors, territorial males preferred horn-pressing (80%, N = 5) (Chi-squared goodness-of-fit test, Chisquared = 36.000, df = 1, P < 0.001) (Fig. 2). Fighting between a territorial and an immature male was only observed once and the combatants used horn-pressing fight in this case. Unlike territorial males, non-territorial males fought mostly using horn-pressing
24
D.A. Blank, W. Yang / Behavioural Processes 108 (2014) 20–26
Fig. 2. Proportion of fighting type (fighting-clash vs. fighting-pressing) in encounters of males with different age and social status: T–T—territorial male vs. territorial male; T–N—territorial male vs. non-territorial males; T–I—territorial male vs. immature; N–N—non-territorial male vs. non-territorial male; N–I—non-territorial male vs. immature; I–I—immature vs. immature.
during the non-rutting period (Log-Linear Model test, Z = 2.888, P = 0.004), while during the rut no difference was found since fights among non-territorial males (bachelors) were observed very rarely. Non-territorial males fought with immature individuals and immature males fought among themselves using the horn-pressing display, while cases of clash-fighting were seen as being accidently performed (6%, N = 33 for immature male interactions only). Territorial males mostly walked during their aggressive interactions with territorial neighbors, with trotting and galloping seen considerably less often (Log-Linear Model test, Z = 3.771, P < 0.001). In addition, territorial males walked slightly more often (78-80%, N = 10) during the “false” rut in April-May compared to the real rut in November–December (60–76%, N = 59) (Log-Linear Model test, Z = −2.812, P = 0.005), when the proportions of galloping increased to 33% in December (N = 48). While expelling non-territorial adult males-intruders from their territories, territorial males walked (40–46%, N = 164 and 150) and galloped (24–39%) with almost the same frequency (Log-Linear Model test, Z = 0.087, P > 0.5), but trotted less often (Z = −3.157, P = 0.002). While chasing immature males, territorial males walked, trotted and galloped with the same proportions (Log-Linear Model test, Z = 0.873 and −1.569, P > 0.5, respectively). Non-territorial adult males also chased their peers and immature males most often at a walk (up to 85%, N = 40), and less frequently at a trot (7-23%) or gallop (4-21%), without a significant difference for peers (Log-Linear Model test, Z = 0.353, P > 0.5) but with a difference for immature males (Z = 2.101, P = 0.036). Immature males chased peers without a preference in gait (LogLinear Model test, Z = 1.165, P > 0.5). 4. Discussion Our data only partly supported our first hypothesis in that territorial bucks, interacting with each other, demonstrated agonistic patterns of behavior more frequently than non-territorial males; they used only reciprocal aggressive displays, such as threat, objecthorning, grazing ritual, parallel walking and others, but did not chase one another. In addition, territorial males showed mostly one-sided displays in encounters with non-territorial and immature males, because they did not receive aggressive displays in response from rivals of lower status. These aggressive interactions ended in a chase to expel the lower ranked individuals from the male’s territory. Territorial males protected their individual territories during the rut by expelling all other males outside of their borders, which was important for receiving exclusive rights to mating females (Blank et al., 2012). In Antilopinae species, territorial males typically have access to mating with females, even though non-territorial
males are also fertile (Skinner and Louw, 1996). Having a higher social status, territorial males showed a higher rate of aggressive displays compared to non-territorial males, because of higher hormonal (testosterone) levels (Li et al., 2004; Shargal et al., 2008) caused by the physiological function of the testicles reaching maximum activity during the rut (Tsapluk, 1972). Thus, territorial (dominant) goitered gazelle males having higher hormonal levels (Rajagopal et al., 2010) demonstrated more frequent aggressive displays during the rut compared to non-territorial males. Since all territorial males with their own individual territories were of an equal social status to their territorial neighbors, encounters performed between them were mostly reciprocal displays of aggressiveness and dominance. However, if one territorial male intruded into the territory of his neighbor while chasing females or bachelors, the trespassing male lost his dominant status and walked or ran back into his own territory if approached by the territory owner. As soon as the retreating male crossed across the border of his own territory, the situation changed again, and the retreating male turned back into a dominant territorial male that no longer retreated, and instead demonstrated aggressiveness and dominance toward any follower. This same pattern of behavior also was described for territorial blackbucks (Antelope cervicapra), when they frequently intruded into a neighbor’s territory (Walther et al., 1983), as well as Thomson’s gazelles (Walther, 1978). So territorial goitered gazelle males did not chase each other at the end of territorial conflicts, and only rarely retreated, with a walking gait, when they intruded into a neighboring territory and were followed by the threatening territorial owner in a pursuit march. In contrast, as the territorial male was always dominant inside his own territory, his aggressive interactions with non-territorial bachelors and immature males were almost exclusively one-sided displays, when only the territorial males demonstrated aggressiveness and dominance and the other males only retreated (Walther, 1984). Territorial bucks typically chased trespassing non-territorial bachelors without any preliminary confrontation, and simply rushed toward the intruding bachelor at a gallop while making loud roaring sounds; the bachelor turned and ran until he crossed the territorial boundary. This behavior is typical for all Antilopinae species (Walther et al., 1983). The frequent chases in agonistic interactions of dominant (territorial buck) vs. subdominant (nonterritorial male) have been explained by rump presentation of the retreating non-territorial male, which, it is thought, likely elicits a stop to the aggression (Guthrie, 1971). Non-territorial males did not show a preference between reciprocal or one-sided displays and in interactions with each other performed both types in almost equal proportions; immature males preferred reciprocal displays with peers. Of the most common reciprocal displays in territorial male goitered gazelles were (in descended frequency) the frontal threat posture, bush horning, grazing ritual, parallel walking, looking at the opponent, ground horning, and freezing in place. Other aggressive patterns were observed infrequently with the exception of chasing (with or without roaring) and the dominance posture, which were more typically seen in encounters between territorial males vs. non-territorial males and non-territorial males vs. their peers and immature males. Frontal threat displays indicate a readiness to fight and are “symbolic” actions in which an animal performs the same initial movements of fighting but without touching his opponent; in other words the threat display is a fighting posture that the male holds or “freezes” in place for at least several seconds (Walther, 1984). In Thomson’s gazelles, threat postures might be demonstrations of reciprocal displays made to rivals of similar status and power (age, body size), with 70.7% of such postures leading to fights; in cases when one opponent was clearly outmatched by the other, the weaker animal ran in 84% of cases (Walther, 1978). Among Antilopinae species, threat displays are the
D.A. Blank, W. Yang / Behavioural Processes 108 (2014) 20–26
most developed in Grant’s gazelles and least in springbok (Antidorcas marsupialis) (Estes, 1991), with goitered gazelles likely in between. Another typical aggressive display was parallel walking in either the same direction or opposite each other. In goitered gazelles, this behavior was usual for territorial bucks and infrequently observed in non-territorial males. Lateral displays are widely assumed to have an aggressive or threatening purpose and are frequently observed in the aggressive repertoires of many vertebrate species (Chiszar, 1978). This pattern of behavior also is observed in most Antilopinae, including gazelle species (Walther et al., 1983; Estes, 1991), and in cervids, such as red deer (Cervus elaphus) (CluttonBrock et al., 1979) and fallow deer (Dama dama) (Jennings et al., 2003). The act of parallel walking does not reduce the level of escalated or risky behavior while fighting, but it does permit an animal the opportunity to decide whether to continue fighting; and often this behavior is a final act before an interaction is terminated (Jennings et al., 2003). However, lateral threat displays and lateral fighting are evolutionally quite ancient behaviors and have been observed even in reptiles; among ungulates it is more typical for the more ancient cervid and bovid species, which are often hornless with canine tusks or have very short horns (Farlow and Dodson, 1975; Meng et al., 2012). In modern cervid and bovid species with well-developed sophisticated horns, lateral displays have been replaced with more frontal threat postures, because the frontal position allows combatants to be ready for parrying from an unexpected attack and avoid serious wounding from an opponent’s horns (Geist, 1966; Barrette, 1977). So since goitered gazelles have well-developed horns, displays of parallel walking were observed considerably less often than frontal threat postures. In addition to parallel walking, looking directly at an opponent and freezing in place were also part of a male’s threat displays. Typically at close range, rivals stopped their aggressive displays and froze for several seconds in a threat posture, while when the combatants were further apart they looked at their opponent and tracked his movements very attentively. Similar behavior has been found common for other gazelle species, as well (Walther et al., 1983). Our data supported our second hypothesis as, frequently in their interactions with peers, territorial males used space-claim behaviors closely related to aggressive patterns, such as bush and ground horning and the grazing ritual, while they demonstrated such agonistic behaviors considerably less often toward non-territorial adult males and what appeared to be accidently to immature males. Non-territorial males also used space-claim behaviors toward peers but only in limited cases, and again accidently toward immature males. In agonistic encounters of hoofed mammals, certain behavior patterns are not necessarily indentified as direct expressions of aggressive displays but rather as marking behaviors; however these activities always have undertones of aggression and occur in the immediate presence of an opponent. These indirect aggression activities are addressed not toward the opponent but toward the ground or vegetation and are called space-claim displays (Walther, 1984). Among space-claim displays in goitered gazelles, territorial males used mostly bush horning and the grazing ritual, and to a lesser extent ground horning. Ground and bush horning (object horning) are considered a mixture of both aggressive and marking behaviors, but our special investigations discovered that object-horning in goitered gazelles is rather more aggression than marking (Blank and Yang, 2014). Bush horning in our current investigations was found to be one of the most frequent behaviors after threat displays, and an important aggressive demonstration in conflicts between territorial males. Similar behavior was also found in Thomson’s gazelles (Walther, 1978). It was also observed that ground horning had enough agonistic importance to solve
25
territorial conflicts, and in gerenuk (Litocranius walleri), adult males were noted to use ground horning as a particularly strong threat toward young males (Estes, 1991). For goitered gazelles, neither bush horning nor ground horning displays were important aggressive demonstrations in agonistic behavior of non-territorial males. Urination-defecation and especially preorbital markings were used as space-claim displays as well, but their role was very limited in aggressive behavior of goitered gazelles, though both were observed frequently in connection with agonistic encounters in other ungulate species (Walther, 1984). Clearly, these acts were used more as marking behaviors in goitered gazelle rather than as aggressive displays. In addition, preorbital marking was used almost exclusively as a marking behavior for territorial goitered gazelle males, while non-territorial males demonstrated these kinds of space-claim behaviors very rarely. After bush horning, the grazing ritual was next in importance in goitered gazelles’ space-claim displays. The grazing ritual began as the two rivals held their heads close to the ground similar to a number of aggressive displays in many species. This ritual was observed, when both rivals stopped their aggressive displays toward each other and started what appeared to be grazing. But in fact, they were not really grazing, because the rivals continued to look at each other with their heads down, and then either restarted their contest or often just ended the conflict and left the area. The agonistic grazing of horned and antlered ungulates is possibly derived from an ancestral form of redirected aggression (Walther, 1984). In Thomson’s gazelle, the grazing ritual is also a primary behavior of territorial bucks, which they perform quite frequently; 36.7% of territorial boundary encounters were carried out exclusively by this ritual and most usually ended the territorial conflict. It is thought that this grazing ritual allows a territorial male to exit from conflicts without “losing face” (Walther et al., 1983). For goitered gazelles, the grazing ritual was observed rarely in aggressive interactions between territorial males vs. non-territorial bachelors and never between territorial males vs. immature males. Nonterritorial males used the grazing ritual infrequently and immature males very rarely. The point is that the grazing ritual was connected quite closely with territoriality, when a territorial male could not retreat from his territory, but just took a break in his aggressive displays; while non-territorial males were interested in establishing their hierarchical status within their group and the grazing ritual was a redundant behavior for that purpose. The grazing ritual is a typical behavior for most gazelle species (Walther et al., 1983; Habibi et al., 1993). In wildebeest (Connochaetus taurinus—Estes, 1969), bontebok (Damaliscus dorcas—David, 1973), kongoni (Alcelaphus buselaphus—Gosling, 1974) and topi, the grazing ritual is also restricted to territorial males (Walther, 1984). This situation is clearly different in species such as Grant’s gazelle and Oryx antelope (Oryx beiza), when actual grazing occurs relatively often in encounters between dominant and subordinate opponents, the latter of which respond by grazing (one-sided displays) when approached by a dominant (Walther, 1984). There were also aggressive behavioral elements that were observed only in non-territorial males and never in territorial bucks that were related to breaking individual distances between males and sniffing or touching one another. This behavior was observed when one opponent treated the other as an unequal rival with a lower social status. Territorial males did not display this behavior even toward immature males, who were already treated as the lowest status of individuals. Instead, the territorial males either just ran toward the young males to expel them from their territories, or else did not pay any attention to them at all (Blank, 1992). Our results also supported our third hypothesis, with the territorial males demonstrating mostly clash-fighting battles with peers and horn-pressing fights with non-territorial and immature males. In Thomson’s gazelle, clash-fighting is the most common type of
26
D.A. Blank, W. Yang / Behavioural Processes 108 (2014) 20–26
fighting between territorial neighbors, with the combatants jumping toward each other with all four legs (Walther et al., 1983). Territorial male goitered gazelles used mostly horn-pressing fights with non-territorial and immature males, and non-territorial bucks with peers and immature males. Horn-pressing fights are observed in all Antilopinae species, but with differences in frequency. In Grant’s gazelle, for instance, these fights are very common, whereas in Thomson’s gazelle, horn-pressing fighting usually occurs only in very long, intensive fights (Walther et al., 1983). Clash-fighting and horn-pressing fights both belong to high intensity fighting, when combatants move forward and backward according to their opponents’ maneuvers, but as a rule neither moves the other very far from his original position (Walther, 1984). Our data supported our fourth hypothesis in part. Indeed, territorial and non-territorial males mostly walked during interactions with their peers, because they were of equal status and it was not clear who was superior (Estes, 1991). However, territorial males used faster gaits more frequently in interactions with nonterritorial and immature males, because in these cases territorial males clearly overmatched the non-territorial and immature males in status and strength. There are cases in which chasing appeared to be a purely executive-type behavior and a “symbolic” action, when without any previous encounter, one (territorial) animal ran after the other (non-territorial and immature) male, preferring often faster gaits. Typically, this is most frequently used by animals of a high social status, such as territorial males, toward very inferior partners, especially immature males (Walther, 1984). In some antelope species, such as oribi (Ourebia ourebi), the horns are so dangerous that simply chasing a rival normally substitutes for fighting (Estes, 1991). However in contrast to our hypothesis, nonterritorial males did not demonstrate preference for faster gaits with immature males compared to peers, and used mostly walking in aggressive interactions with immature males like they did with peers in spite of their unequal status. Apparently, in contrast to the agonistic behaviors between territorial bucks and inferior males, chasing with fast gaits lacks of importance as a symbolic action in hierarchical interactions between non-territorial and immature males. In contrast, immature males had no gait preference in their aggressive interactions with their peers. Often while chasing, territorial males utter certain vocalizations, such as a roaring sound in impala (Aepyceros melampus) that in itself can cause an inferior male to flee as fast as he can (Schenkel, 1966). A similar behavior was observed in goitered gazelle, when territorial males addressed most of their vocalized chasing to non-territorial males, and less to immature males and peers. In contrast, nonterritorial males addressed most of their vocalized chasing to peers and considerably less to immature males. These observations also support the idea that territorial and non-territorial males behave differently during their agonistic interactions. So we concluded that territorial and non-territorial males had different repertoires of aggressive behaviors because of the differences in their social status and their motivations for agonistic displays.
Acknowledgments We thank the National Natural Science Foundation of China (U1303301), Chinese Academy of Sciences (CAS) for granting our work (Visiting Professorships for Senior International Scientists—2011T1Z42), West Light Foundation (CAS—Y336171) for creating all conditions for writing this paper. We are very grateful to the Institute of Zoology, former Academy of Sciences of Kazakhstan, which has given us the possibility for investigations of goitered gazelles in their natural environment during 10 years. We are grateful to Ms. Patricia Johnston for her useful
suggestions and remarks and constant help in English editing of this manuscript. References Barrette, C., 1977. Fighting behaviour of muntjac and the evolution of antlers. Evolution 31 (1), 169–176. Blank, D.A., 1985. Peculiarities of social and reproductive behaviour of Gazella subgutturosa in the Iliisky Valley. Zool. J. 64, 1059–1070 (in Russian, English abstract). Blank, D.A., 1990. Persian gazelle. In: Kovshar, A.F. (Ed.), Rare Animals of Desert Regions. Nauka Kazakh SSR Press, Alma-Ata, pp. 56–80 (in Russian). Blank, D.A., 1992. Social and reproductive behaviour of the Persian gazelle. In: PhD thesis. University of Tel Aviv. Blank, D.A., 1998. Mating behaviour of the Persian gazelle (Gazella subgutturosa Guldenstaedt, 1780). Mammalia 62 (4), 499–519. Blank, D.A., Ruckstuhl, K.E., Yang, W., 2012. Social organization in goitered gazelle (Gazella subgutturosa Guldenstaedt, 1780). Ethol. Ecol. Evol. 24, 306–321. Blank, D.A., Yang, W., 2014. Object-horning in goitered gazelle: agonistic or marking behaviour? Behav. Process. 103, 165–172. Bro-Jorgensen, J., 2007. The intensity of sexual selection predicts weapon size in male bovids. Evolution 61 (6), 1316–1326. Chiszar, D.A., 1978. Lateral displays in the lower vertebrates: forms, functions, and origins. In: Reese, E.S., Lighter, F.J. (Eds.), Adaptation in the Aquatic and Terrestrial Environments. J. Wiley, New York, pp. 105–135, Contrasts in Behaviour. Clutton-Brock, T.H., Albon, S.D., Gibson, R.M., Guinness, F.E., 1979. The logical stag: adaptive of fighting in red deer (Cervus elaphus L.). Anim. Behav. 27, 221–225. David, J.H.M., 1973. The behaviour of the bontebok, Damaliscus dorcas dorcas (Pallas 1766), with special reference to territorial behaviour. Z. Tierpsychol. 33, 38–107. Estes, R.D., 1969. Territorial behaviour of the wildebeest (Connochaetus taurinus Burchell, 1823). Z. Tierpsychol. 26, 284–370. Estes, R.D., 1991. The Behaviour Guide to African Mammals. University of California Press, Los Angeles. Farlow, J.O., Dodson, P., 1975. The behavioral significance of frill and horn morphology in Ceratopsian dinosaurs. Evolution 29 (2), 353–361. Geist, V., 1966. The evolution of horn-like organs. Behaviour 27, 175–214. Gosling, L.M., 1974. The social behaviour of Coke’s hartebeest Alcelaphus buselaphus cokei. In: Geist, V., Walther, F.R. (Eds.), The Behaviour of Ungulates and Its Relation to Management, IUCN Publ. No. 24. IUCN, Morges, pp. 488–511, Contrasts in Behaviour. Grau, G.A., Walther, F.R., 1976. Mountain gazelle agonistic behaviour. Anim. Behav. 24, 626–636. Guthrie, R.D., 1971. A new theory of mammalian rump patch evolution. Behaviour 38 (1/2), 132–145. Habibi, K., Thouless, C.R., Lindsay, N., 1993. Comparative behaviour of sand and mountain gazelles. J. Zool. (Lond.) 229, 41–53. Jennings, D.J., Gammell, M.P., Carlin, C.M., Hayden, T.J., 2003. Is the parallel walk between competing male fallow deer, Dama dama, a lateral display of individual quality? Anim. Behav. 65, 1005–1012. Li, C., Zhigang, J., Yan, Z., Coie, Y., 2004. Relationship between serum testosterone, dominance and mating success pere davids deer stags. Ethology 110, 681–691. Lundrigan, B., 1996. Morphology of horns and fighting behavior in the family Bovidae. J. Mammal. 77 (2), 462–475. Meng, X., Cody, N., Gong, B., Xiang, L., 2012. Stable fighting strategies to maintain social ranks in captive male Alpine musk deer (Moschus sifanicus). Anim. Sci. J. 83, 617–622. Perez-Barberia, F.J., Gordon, I.J., Pagel, M., 2002. The origin of sexual dimorphism in body size in ungulates. Evolution 56, 1276–1285. Rajagopal, T., Govindaraju, A., Geraldine, P., Balasundaram, C., 2010. Assessment of dominance hierarchy through urine scent marking and its chemical constituents in male blackbuck Antelope cervicapra, a critically endangered species. Behav. Process. 85, 58–67. Schenkel, R., 1966. On sociology and behaviour in impala (Aepyceros melamous suara Matschie). Z. Saugetierk. 31, 177–205. Shargal, D., Shore, L., Roteri, N., Terkel, A., Zorovsky, Y., Shemesh, M., Steinberger, Y., 2008. Fecal testosterone is elevated in high ranking female ibexes (Capra nubiana) and associated with increased aggression and a preponderance of male offspring. Theriogenology 69, 673–680. Skinner, J.D., Louw, G.N., 1996. The Springbok (Antidorcas marsupialis— Zimmermann, 1780). Transvaal Museum, Pretoria. Tsapluk, O.E., 1972. Age and seasonal dynamics of sexual activity in Gazella subgutturosa Gueld. Proceed. Acad. Scien. Kazakh SSR, Biol. Series 3, 39–46 (in Russian). Walther, F.R., 1978. Forms of aggression in Thomson’s gazelle: their situational motivation and their relative frequency in different sex, age, and social classes. Z. Tierpsychol. 47, 113–172. Walther, F.R., 1984. Communication and Expression in Hoofed Animals. Indiana University Press, Bloomington. Walther, F.R., Mungall, E.C., Grau, G.H., 1983. Gazelles and Their Relatives. Noyes Publications, Park Ridge, NJ. Wronski, T., Sandouka, M.A., Plath, M., Cunningham, P., 2010. Differences in sexual dimorphism among four gazelle taxa (gazelle spp.) in the Middle East. Anim. Biol. 60, 395–412. Zhevnerov, V.V., 1984. Goitered gazelle of the Barsa-Kelmes Island. Nauka Press of the Kazakh SSR, Alma-Ata (in Russian).
Contents lists available at ScienceDirect
Behavioural Processes journal homepage: www.elsevier.com/locate/behavproc
Does social status of males change their aggressive behavior repertoire in goitered gazelle (gazella subgutturosa guld., 1780)? D.A. Blank a,b , W. Yang a,∗ a Key Laboratory of Biogeography and Bioresource in Arid Land, Xinjiang Institute of Ecology and Geography, The Chinese Academy of Sciences, Urumqi, China b Institute of Zoology, Kazakh Academy of Sciences, Alma-Ata, Kazakhstan
a r t i c l e
i n f o
Article history: Received 6 July 2014 Received in revised form 23 August 2014 Accepted 11 September 2014 Available online 18 September 2014 Keywords: Aggressive behavior Goitered gazelle Social status Territorial male
a b s t r a c t Aggression in ungulates is a very common behavior which serves a great variety of social functions, the most important of which is territorial protection from intruders. Typically during the rut, territorial males in Antilopinae species have access to mating females, and territoriality leads to a drastic change in the males’ lifestyle as they spend most of their aggressive efforts on protecting their territories from other males. In contrast, non-territorial males generally behave in a constant manner all year round, with most of their aggression spent on hierarchical interactions within groups. In this paper, we discuss the differences in aggressive behaviors between territorial and non-territorial males of goitered gazelles (Gazella subgutturosa). We found that territorial males of this species demonstrated most of their aggressive displays, such as threat postures and space-claim patterns, to other territorial males-neighbors, but rarely chased after them at the end of a conflict. Inversely, territorial males frequently chased non-territorial and immature males while only occasionally demonstrating aggressive patterns. Non-territorial males mostly chased other males in their agonistic interactions, displaying threat postures less often than territorial males, but also showing aggressive patterns not found in territorial males. So we concluded that territorial and non-territorial males of goitered gazelles had different repertoires of aggressive behaviors, and when adult males switched their social status from territorial during the rut to non-territorial outside the rut, they obviously changed their preference in aggressive behaviors accordingly. © 2014 Elsevier B.V. All rights reserved.
1. Introduction In Antilopinae species aggressive interactions occur among all sexes, ages, and social classes (Walther et al., 1983). Aggression serves a great variety of social functions, and it is hard to find any part of the social life of bovids where aggression is not involved (Walther, 1984; Rajagopal et al., 2010). Also aggression has shown to be a powerful mechanism for intra-sexual and natural selection among males leading to sexual dimorphism in the size and shape of the horns and body proportions (Lundrigan, 1996; PerezBarberia et al., 2002; Bro-Jorgensen, 2007; Wronski et al., 2010). Furthermore, though there are several roles for aggressive behavior in bovid life, one of its most important functions for adult male gazelles, who compete for mates, is establishing and ratification of their individual territorial borders and preventing invasion from other males’ (Walther et al., 1983).
∗ Corresponding author. Fax: +86 991 7885320. E-mail addresses: [email protected] (D.A. Blank), [email protected] (W. Yang). http://dx.doi.org/10.1016/j.beproc.2014.09.017 0376-6357/© 2014 Elsevier B.V. All rights reserved.
Aggressive behavior has been investigated in detail for several gazelle species, including the Thomson gazelle (Eudorcas thomsoni—Walther, 1978), Grant’s gazelle (Nanger granti—Walther et al., 1983) and mountain gazelle (Gazella gazella—Grau and Walther, 1976), but never has it been a subject of special consideration for the goitered gazelle (Gazella subgutturosa). In goitered gazelle, the majority of adult males establish individual territories during the rut in November–December, and a few also show territoriality during a “false” rut in April–May, though the majority remains non-territorial at this time. Non-territorial males continue their daily movements during the rut as all males do outside of the rutting period (Blank et al., 2012). During the rest of the year, goitered gazelles do not show territoriality at all. In Antilopinae species, territorial males are the most likely to have access to mating females, and territoriality requires drastic changes in their behaviors during the rut, because they spend most of their aggressive efforts protecting their territorial borders from other males (Walther et al., 1983). In contrast, non-territorial males generally behave the same way all year round, with most of their aggressive efforts spent in hierarchical interactions within groups (Blank, 1992). In this paper, we discuss whether territorial and
D.A. Blank, W. Yang / Behavioural Processes 108 (2014) 20–26
21
non-territorial goitered gazelle males behave similarly or differently during their aggressive interactions and whether their aggressive repertoires consist of different behaviors. We theorized that aggressive behaviors seen in goitered gazelles would be similar on the whole to such behaviors in other gazelle species. Walther (1978) found that territorial Thomson’s gazelle bucks demonstrated reciprocal threat displays toward each other, while one-sided displays were directed toward non-territorial bachelors. Based on this study, we predicted our first hypothesis for goitered gazelles that territorial males also would demonstrate reciprocal displays to each other more frequently than non-territorial males, and they would do it without chasing one another during their aggressive interactions with their neighbors, while onesided displays with chasing would be typical for interactions between territorial males and non-territorial males. In addition, non-territorial males would have a consistent behavior and would show more displays to their peers and less to immature males. Furthermore, the goitered gazelles’ repertoire of agonistic displays would be similar to aggressive behaviors of other gazelle species. Walther (1984) noted that during pauses in agonistic encounters, some additional displays may be observed that are not clearly aggressive behaviors, such as threat postures, but are still related to agonistic behavior. These behaviors have been called space-claim displays, and include the grazing ritual, object-horning, and marking with urine/feces and preorbital glands. Walther found that territorial males of some gazelles use these displays mostly during their territorial conflicts, while this behavior is not typical for non-territorial males (Walther, 1984). So we predict our second hypothesis that mostly territorial males of goitered gazelles would perform space-claim displays and non-territorial males would not. Walther et al. (1983) also found for Thomson’s gazelle that territorial males displayed clash-fighting in their conflicts with neighbors, while non-territorial males prefer horn-pressing fighting instead. So we supposed that it would be true for goitered gazelles as well and predicted our third hypothesis that territorial males in the rut would show only clash-fighting in conflicts with peers, while non-territorial males would use horn-pressing fighting. Walther (1978) found that fighting territorial Thomson’s gazelle males never ran from each other after conflict but instead walked away, while they frequently chased when engaged in conflicts with non-territorial and immature males. So we predicted our fourth hypothesis that this behavior would apply to goitered gazelles as well, and a territorial male would mostly walk during agonistic interactions with his neighbors, while he would use a faster gait (trot and gallop) in interactions with non-territorial and immature males. Additionally, it was reasonable to assume that non-territorial males would also demonstrate similar behaviors and mostly walk when engaged with peers and use faster gaits in encounters with immature males.
of 50–100 m, with observation posts usually established on elevations, from where we could see usually 30–50 gazelles at the same time. During the rut, the goitered gazelle territory size was 50–80 ha (Blank, 1985), and we typically could observe 5–6 individual territories simultaneously from our elevated observation sites. Since, females were distributed unevenly among territories (Blank, 1998), we chose a male closest to the observation point that had at least one female in his territory. To avoid pseudoreplication, we changed our observation sites every several days and tried to observe gazelles in different parts of the study area (over ∼4600 km2 ). The total size of the study population in the Ili depression was estimated to range from 1.5 thousand in 1981 up to 5 thousand in 1986 (Blank, 1990). For focal observations we used binoculars (magnification 8×) and a telescope (magnification 30×–60×). We conducted 181 h of focal observations in April, 470 h in May, 374 h in June, 173 h in July, 59 h in August, 60 h in October, 224 h in November and 148 h in December over the 6-year period. We investigated the frequency changes in aggressive noncontact displays and actual fights (battles) according to the breeding cycle, and distinguished three biological seasons for the goitered gazelle: rutting season (November–December), “false” rut (April–May), and outside the rut (June–October); data were absent or too scarce for January, February, March, and September. For our analyses in this paper, we distinguished two kinds of agonistic behavior in goitered gazelles: aggressive displays in which we included all agonistic displays of one male to another with no physical contact; and fights (or battles) which included any form of physical agonistic contact (Walther et al., 1983). An ethogram of the main agonistic displays is listed in Table 1. We differentiated gazelles according to sex (horned males and hornless females) and age (adult and immature males, and adult and immature females), which was defined according to the descriptions provided by Zhevnerov (1984): adult males (older than 2 years old—horns 1.5 times longer than ears and absence of the black spot on the front of the muzzle), adult females (older than 2 years old—hornless and absence of black spot on the front of the muzzle), sub-adult males (1–2 years old—horns are equal or shorter than ears and presence of a black spot on the muzzle front), and sub-adult females (1–2 years old—hornless and black spot on the muzzle front). Young (up to 1 year old—body size is smaller in 2–3 times compared to adult gazelles and black sport on the muzzle front) were also noted, but we did not use our observations of either young or females for this paper. Our data had a nonparametric statistical distribution according to the Shapiro-Wilk and Kolmogorov-Smirnov tests. We used the Mann-Whitney U test to compare two types of fighting, as well as the Chi-squared goodness-of-fit test for comparing proportions of rare aggressive displays. The Log-Linear Model test was used for analyses of the frequencies of separate behavioral acts. All statistical analyses were conducted using SPSS 17.0 software package.
2. Materials and methods
3. Results
Our observations were conducted in the Ili depression (southeastern Kazakhstan) during a 6-year period from 1981 to 1986. We mostly did focal animal observations, concentrating on only one randomly selected group of gazelles (usually the closest) at a time, continuously observing the separate group members for up to 9 h and recording all aggressive displays and fights (battles) that accompanied territorial defense, breeding or social behavior. Gazelles were determined to be members of a group if they were less than 50 m from each other, moved in the same direction and stayed together for longer than half an hour. All of the behaviors were recorded in the order in which they occurred and each time they occurred. In most cases, gazelles were observed from distances
Territorial males performed mostly reciprocal displays to other territorial males (86%, N = 78) and considerably less often one-sided displays (Log-Linear Model test, Z = 2.483, P = 0.013). In contrast, during interactions with non-territorial bachelors or immature males, territorial males used mostly (for adult males) or only (for immature) one-sided displays (Fig. 1), while non-territorial bachelors or immature males usually did not answer to the aggressive displays of territorial males (Log-Linear Model test, Z = −5.112, P < 0.001). During aggressive interactions of two territorial males, rivals most often used frontal threat displays, slightly less often the behaviors of bush and ground horning, the grazing ritual, walking parallel to each other and/or looking at their opponents (95%,
22
D.A. Blank, W. Yang / Behavioural Processes 108 (2014) 20–26
Table 1 Description of the recorded aggressive displays (ethogram) in adult goitered gazelle males during observations based on Walther et al. (1983) and Blank (1998). Posture
Description
Clash-fighting of territorial males
After preliminary threat displays, rivals run toward each other and clash together, which can be heard at the distance of 700–800 m. When the horns are almost invariably interlocked, each rival tries to press the horns and head of the opponent to the ground and push him back. They then separate again, moving backward and repeat the same clashing actions. At the end of the fight, both rivals return to their own territories from opposite directions. During a long, intensive fight, the combatant’s heads and necks are twisted aside, and they fight with their necks, when the horns are interlocked; the rival tries to twist the neck of his opponent upward-sideward, when the neck is twisted back. Sometimes, the muzzle, neck or front parts of the breast are hooked by the rival’s horns, which hit these parts. Opponents open their mouths widely and roar constantly. Their tails are pressed to their hindquarters. Typically without preliminary threat displays, rivals approach each other with heads lowered to the ground and lean the front surfaces of their horns against each other. They fight while standing on all four legs with the forelegs widely spread, and hind legs in a normal position or relatively close together. Each tries to press the horns of the opponent to the ground and move him backward. Then every rival hits the opponent’s head with maximum power and presses his head to the ground and back, making jerks. The horns almost invariably interlock (horn of one between horns of another). This fight can transfer to fight-circling, when rivals with locked horns move in circles. In this case, they pivot with their hindquarters while keeping their heads in the center of the circle. During fighting, the ears are apart horizontally and directed sidewise at the top or sometimes backward and the tail is pressed to the rump. This fight is common for non-territorial males. Horns are directed toward opponent. Ears are directed forward-sideward; tail is in normal position. Rivals stand in lateral T-position, parallel or, most commonly, a reverse-parallel orientation. The posture is erect, with the neck vertically erected upwards “proudly”. The entire body is as high as possible due to all four legs stretched up. The muzzle top is pressed to a throat and the horns are directed forward with the head is turned in a more or less pronounced fashion away from the opponent. Tail is uplifted and making waving movements from one side to the other; ears are apart horizontally and directed sidewise at the tops, with the ear holes directed forward or downward. All walking movements are unusually slow. In the case of shrub or saxaul (Haloxylon aphyllum) horning, the male approaches the tree in a dominance posture (head level with the body, horns directed forward, ears apart), sniffs the bare trunk, positions the trunk between the horns and thrashes with the forehead, goring the trunk with the power of his whole body; he cleans small branches from bigger ones and breaks some shrub’s branches, with pauses to smell the scratched vegetation, which he touches with his muzzle top after every 2–3 thrashing acts before continuing to horn. The ears stay apart horizontally and slightly backward (45◦ ) at the tops and downward by the ear holes. Head movements are up-down along the branch and from side to side, sometimes round the head axis and he pushes the shrub with the entire body and trying to scratch as high as possible. A buck sniffs points of low grass and starts to horn, scratches and gores the plants and naked ground, making sharp horning movements from one side to another and setting his horns against the ground, as if trying to shift the ground like he does with his real rival. Two territorial males meet at the boundary of neighboring territories, threatening and fighting each other. After several clashes, they simultaneously begin to graze and step backwards. If they do not renew the fight, permanent grazing leads to enlargement of the distance. The longer the grazing ritual lasts, the greater the distance becomes. Sooner or later, they turn into a reverse (hindquarters to hindquarters) position and move farther and farther away from each other, each of them grazing back toward the center of their own territory. A lateral display of two males engaging in a slow, tense, regular walk in parallel same or opposite directions to each other; horns are held high, and often their hair is raised. One male looks attentively for any movements of the other male. One or both opponents freeze in an agonistic posture and hold it for several seconds, then continue their displays. Stepping forward and stretching the body, lowering the belly toward the ground, with the hind legs sloping backward; urination with a lifted tail. Abrupt bringing hind legs forward so that the hooves are placed lateral to the stationary forelegs, squatting closer to the ground and taking a crouched posture and defecating. One male follows the other, often roaring toward his opponent and demonstrating threat or dominant postures. This is a typical behavior of territorial males that expel intruders from their territories. Stretching the head and neck forward horizontally with the nose pointing horizontally forward. Ears are directed backward and usually pressed to the head in a position either parallel to the ground or slightly downward with the foramen inward. Rarely ears are laid back, pressed to each other, or held one apart of the other at a 45◦ angle. The tail is lifted to varying degrees, up to a vertical position. Head and neck are stretched forward and upward up to 45◦ above the horizontal, the top of the muzzle is lifted forward and upward, and the ears are pressed to the head. The ritualized act of marking with the male’s preorbital glands rarely begins with sniffing the plant stem or twig. Instead, the goitered gazelle male opens both preorbital glands, sometimes opening his mouth at the same time, and carefully lowers the preorbital region toward the plant stem, bringing the stem’s tip or twig into the widely opened gland. With quivering movements of the gland‘s margin, he deposits some secretions which soon hardened in the open air. The male sometimes marks the same plant stem a second time using either the same or his other preorbital gland. To position himself for scent marking, the male commonly stretches his head upward to get his preorbital gland as high as possible, although he never raises his body to stand on just his hind legs for this purpose. Roaring consists of gruff, wheezing or hissing sounds resembling gurgling or sneezing. In producing these sounds, the male open his mouth wide, lifts his tongue slightly and takes a deep breath, then closes his mouth and passes air through his nostrils or possibly through his partly closed mouth. Posture: Muzzle is raised to an angle of up to 45◦ from a horizontal position. Ears are directed backward and tightly pressed to the head with the ear holes inside. Abruptly, the male jerks his head and whole body forward and upward, and his protruding thyroid cartilage moves up and down. When running, roaring is intermittent. One male approaches another to a very close distance, breaking an individual distance and forcing the opponent to retreat or start battling. One male approaches another very closely and touches his opponent’s body (usually hindquarters) with his muzzle. In a mating bipedal posture, one male follows the hindquarters of another male keeping in a bipedal position for several seconds. One male approaches the other to a close distance, trying to sniff any body part (often hindquarters) of his opponent.
Horn-pressing fights of adult males
Frontal threat posture Dominance
Bush horning
Ground horning
Grazing ritual
Parallel walk Looking to opponent Display freezing Urination Defecation Chasing Low-stretch
High- stretch Preorbital marking
Roaring
Close approaching Muzzle touching Mating posture Sniffing opponent
D.A. Blank, W. Yang / Behavioural Processes 108 (2014) 20–26
23
Table 2 Frequency of various aggressive patterns in encounters of males with different age and social status. Behavioral patterns
Frontal threat Bush horning Grazing ritual Parallel walking Looking to opponent Ground horning Display freezing Urination-defecation Chasing Dominance Low-high-stretch Preorbital marking Chasing roaring Close approaching Muzzle touching Mating posture Sniffing opponent
Territorial vs.
Non-territorial vs.
Immature vs.
Territorial
Non-territorial
Immature
Non-territorial
Immature
Immature
123 90 95 49 41 43 35 36 21 0 3 5 28 0 0 0 0
89 40 3 5 50 2 1 19 254 27 25 7 111 0 0 0 0
19 2 0 0 7 1 0 1 87 2 32 0 30 0 0 0 0
60 11 12 19 10 9 8 3 116 37 1 1 83 30 2 9 6
24 3 1 0 1 0 1 0 89 17 19 0 24 20 12 11 4
13 4 1 0 0 0 2 0 21 6 0 0 14 9 0 0 2
N = 458; Table 2), rarely did they chase one another at the end of their demonstrations (5%) (Z = 8.788, P < 0.001). Conversely, territorial males often chased non-territorial and immature males (58%, N = 439 and 77%, N = 113, respectively) after aggressive displays (42% and 24%) or even without them (16% and 53%, respectively) (Log-Linear Model test, Z = −2.700 and −4.664, P = 0.007 and <0.001, respectively). In addition, territorial males addressed most of their roaring-chasing to non-territorial males and considerably less to peers and immature males (Log-Linear Model test, Z = 5.180 and 6.445, P < 0.001 for both). Furthermore, territorial males exhibited a poorer repertoire (less variability) of aggressive displays to non-territorial bachelors and even less to immature males compared to aggression displays with peers (Log-Linear Model test, Z = −4.496 and −8.635, P < 0.001, respectively), and chased after non-territorial bachelors most often, immature males less often and peers least often (Z = −5.465 and −7.866, P < 0.001, respectively; Table 2). Non-territorial males performed one-sided displays with their peers and immature males with the same frequency (Log-Linear Model test, Z = 0.353, P = 0.724), though reciprocal displays were slightly more typical for encounters of non-territorial adult males with their peers (Z = 1.959, P = 0.05). In contrast, immature males demonstrated mostly reciprocal displays with their peers (Fig. 1). Similar to territorial males, non-territorial males used mostly threat displays (Log-Linear Model test, Z = 2.018–2.553, P = 0.011–0.014), but at a lower rate compared to territorial bucks (Z = −5.682,
Fig. 1. Proportion of reciprocal (Reciproc) and one-side displays (one-side) in encounters of males with different social status: T–T—territorial male vs. territorial male; T–N—territorial male vs. non-territorial males; T–I—territorial male vs. immature; N–N—non-territorial male vs. non-territorial male; N–I—non-territorial male vs. immature; I–I—immature vs. immature.
P < 0.001), and they performed other agonistic displays more rarely as well (Z = −2.390, P = 0.017; Table 2). Only chasing and roaring-chasing were observed more frequently in non-territorial males than even threat displays (Log-Linear Model test, Z = 5.682, P < 0.001 for both). In contrast to territorial bucks, non-territorial males addressed most of their roaring-chasing to peers (Z = 5.007, P < 0.001). There were four agonistic displays that were not found in territorial males and only observed in non-territorial and immature males: close-approaching, sniffing, touching and mating posture (Table 2). Among space-claim displays of aggression, the grazing ritual was very typical for boundary encounters between territorial males (95%, N = 91), but rarely observed in displays addressed to bachelors (1.4%, N = 219) and never toward immature males (Z = 4.085, P < 0.001) (Table 2). Non-territorial males used the grazing ritual infrequently in their aggressive displays toward their peers (9.2%, N = 130) compared to contests between territorial males (Chi-squared goodness-of-fit test, Chi-squared = 60.840, df = 1, P < 0.001), and only accidently toward immature males (1 case); immature males used this ritual exceptionally rarely (only 1 observed case during the entire study period; Table 2). Among other space-claim displays, territorial males preferred object-horning (bush and ground horning) directed to their peers, especially in November–December (67–74%, N = 52 and 74); considerably less often space-claim demonstrations consisted of urine and feces marking during aggressive displays (22-29%; Log-Linear Model test, Z = −2.677, P = 0.007) and very rarely preorbital gland markings (4%; Z = −4.055, P < 0.001). Territorial bucks demonstrated similar behaviors to non-territorial males, preferring object-horning to other space-claim displays as urination-defecation and preorbital markings (Log-Linear Model test, Z = 2.959, P = 0.003), but the frequency of these displays was observed less often compared to the aggressive interactions of territorial peers to one another (LogLinear Model test, Z = −2.126, P = 0.034). Territorial bucks did not demonstrate space-claim displays to immature males at all, while non-territorial bucks and especially immature males used spaceclaim behaviors accidently. When territorial males fought, they mostly engaged in demonstrations of clash-fighting (80%, N = 15) and rarely used horn-pressing fights (Mann-Whitney U, Z = −3.720, P < 0.001), while when fighting with bachelors, territorial males preferred horn-pressing (80%, N = 5) (Chi-squared goodness-of-fit test, Chisquared = 36.000, df = 1, P < 0.001) (Fig. 2). Fighting between a territorial and an immature male was only observed once and the combatants used horn-pressing fight in this case. Unlike territorial males, non-territorial males fought mostly using horn-pressing
24
D.A. Blank, W. Yang / Behavioural Processes 108 (2014) 20–26
Fig. 2. Proportion of fighting type (fighting-clash vs. fighting-pressing) in encounters of males with different age and social status: T–T—territorial male vs. territorial male; T–N—territorial male vs. non-territorial males; T–I—territorial male vs. immature; N–N—non-territorial male vs. non-territorial male; N–I—non-territorial male vs. immature; I–I—immature vs. immature.
during the non-rutting period (Log-Linear Model test, Z = 2.888, P = 0.004), while during the rut no difference was found since fights among non-territorial males (bachelors) were observed very rarely. Non-territorial males fought with immature individuals and immature males fought among themselves using the horn-pressing display, while cases of clash-fighting were seen as being accidently performed (6%, N = 33 for immature male interactions only). Territorial males mostly walked during their aggressive interactions with territorial neighbors, with trotting and galloping seen considerably less often (Log-Linear Model test, Z = 3.771, P < 0.001). In addition, territorial males walked slightly more often (78-80%, N = 10) during the “false” rut in April-May compared to the real rut in November–December (60–76%, N = 59) (Log-Linear Model test, Z = −2.812, P = 0.005), when the proportions of galloping increased to 33% in December (N = 48). While expelling non-territorial adult males-intruders from their territories, territorial males walked (40–46%, N = 164 and 150) and galloped (24–39%) with almost the same frequency (Log-Linear Model test, Z = 0.087, P > 0.5), but trotted less often (Z = −3.157, P = 0.002). While chasing immature males, territorial males walked, trotted and galloped with the same proportions (Log-Linear Model test, Z = 0.873 and −1.569, P > 0.5, respectively). Non-territorial adult males also chased their peers and immature males most often at a walk (up to 85%, N = 40), and less frequently at a trot (7-23%) or gallop (4-21%), without a significant difference for peers (Log-Linear Model test, Z = 0.353, P > 0.5) but with a difference for immature males (Z = 2.101, P = 0.036). Immature males chased peers without a preference in gait (LogLinear Model test, Z = 1.165, P > 0.5). 4. Discussion Our data only partly supported our first hypothesis in that territorial bucks, interacting with each other, demonstrated agonistic patterns of behavior more frequently than non-territorial males; they used only reciprocal aggressive displays, such as threat, objecthorning, grazing ritual, parallel walking and others, but did not chase one another. In addition, territorial males showed mostly one-sided displays in encounters with non-territorial and immature males, because they did not receive aggressive displays in response from rivals of lower status. These aggressive interactions ended in a chase to expel the lower ranked individuals from the male’s territory. Territorial males protected their individual territories during the rut by expelling all other males outside of their borders, which was important for receiving exclusive rights to mating females (Blank et al., 2012). In Antilopinae species, territorial males typically have access to mating with females, even though non-territorial
males are also fertile (Skinner and Louw, 1996). Having a higher social status, territorial males showed a higher rate of aggressive displays compared to non-territorial males, because of higher hormonal (testosterone) levels (Li et al., 2004; Shargal et al., 2008) caused by the physiological function of the testicles reaching maximum activity during the rut (Tsapluk, 1972). Thus, territorial (dominant) goitered gazelle males having higher hormonal levels (Rajagopal et al., 2010) demonstrated more frequent aggressive displays during the rut compared to non-territorial males. Since all territorial males with their own individual territories were of an equal social status to their territorial neighbors, encounters performed between them were mostly reciprocal displays of aggressiveness and dominance. However, if one territorial male intruded into the territory of his neighbor while chasing females or bachelors, the trespassing male lost his dominant status and walked or ran back into his own territory if approached by the territory owner. As soon as the retreating male crossed across the border of his own territory, the situation changed again, and the retreating male turned back into a dominant territorial male that no longer retreated, and instead demonstrated aggressiveness and dominance toward any follower. This same pattern of behavior also was described for territorial blackbucks (Antelope cervicapra), when they frequently intruded into a neighbor’s territory (Walther et al., 1983), as well as Thomson’s gazelles (Walther, 1978). So territorial goitered gazelle males did not chase each other at the end of territorial conflicts, and only rarely retreated, with a walking gait, when they intruded into a neighboring territory and were followed by the threatening territorial owner in a pursuit march. In contrast, as the territorial male was always dominant inside his own territory, his aggressive interactions with non-territorial bachelors and immature males were almost exclusively one-sided displays, when only the territorial males demonstrated aggressiveness and dominance and the other males only retreated (Walther, 1984). Territorial bucks typically chased trespassing non-territorial bachelors without any preliminary confrontation, and simply rushed toward the intruding bachelor at a gallop while making loud roaring sounds; the bachelor turned and ran until he crossed the territorial boundary. This behavior is typical for all Antilopinae species (Walther et al., 1983). The frequent chases in agonistic interactions of dominant (territorial buck) vs. subdominant (nonterritorial male) have been explained by rump presentation of the retreating non-territorial male, which, it is thought, likely elicits a stop to the aggression (Guthrie, 1971). Non-territorial males did not show a preference between reciprocal or one-sided displays and in interactions with each other performed both types in almost equal proportions; immature males preferred reciprocal displays with peers. Of the most common reciprocal displays in territorial male goitered gazelles were (in descended frequency) the frontal threat posture, bush horning, grazing ritual, parallel walking, looking at the opponent, ground horning, and freezing in place. Other aggressive patterns were observed infrequently with the exception of chasing (with or without roaring) and the dominance posture, which were more typically seen in encounters between territorial males vs. non-territorial males and non-territorial males vs. their peers and immature males. Frontal threat displays indicate a readiness to fight and are “symbolic” actions in which an animal performs the same initial movements of fighting but without touching his opponent; in other words the threat display is a fighting posture that the male holds or “freezes” in place for at least several seconds (Walther, 1984). In Thomson’s gazelles, threat postures might be demonstrations of reciprocal displays made to rivals of similar status and power (age, body size), with 70.7% of such postures leading to fights; in cases when one opponent was clearly outmatched by the other, the weaker animal ran in 84% of cases (Walther, 1978). Among Antilopinae species, threat displays are the
D.A. Blank, W. Yang / Behavioural Processes 108 (2014) 20–26
most developed in Grant’s gazelles and least in springbok (Antidorcas marsupialis) (Estes, 1991), with goitered gazelles likely in between. Another typical aggressive display was parallel walking in either the same direction or opposite each other. In goitered gazelles, this behavior was usual for territorial bucks and infrequently observed in non-territorial males. Lateral displays are widely assumed to have an aggressive or threatening purpose and are frequently observed in the aggressive repertoires of many vertebrate species (Chiszar, 1978). This pattern of behavior also is observed in most Antilopinae, including gazelle species (Walther et al., 1983; Estes, 1991), and in cervids, such as red deer (Cervus elaphus) (CluttonBrock et al., 1979) and fallow deer (Dama dama) (Jennings et al., 2003). The act of parallel walking does not reduce the level of escalated or risky behavior while fighting, but it does permit an animal the opportunity to decide whether to continue fighting; and often this behavior is a final act before an interaction is terminated (Jennings et al., 2003). However, lateral threat displays and lateral fighting are evolutionally quite ancient behaviors and have been observed even in reptiles; among ungulates it is more typical for the more ancient cervid and bovid species, which are often hornless with canine tusks or have very short horns (Farlow and Dodson, 1975; Meng et al., 2012). In modern cervid and bovid species with well-developed sophisticated horns, lateral displays have been replaced with more frontal threat postures, because the frontal position allows combatants to be ready for parrying from an unexpected attack and avoid serious wounding from an opponent’s horns (Geist, 1966; Barrette, 1977). So since goitered gazelles have well-developed horns, displays of parallel walking were observed considerably less often than frontal threat postures. In addition to parallel walking, looking directly at an opponent and freezing in place were also part of a male’s threat displays. Typically at close range, rivals stopped their aggressive displays and froze for several seconds in a threat posture, while when the combatants were further apart they looked at their opponent and tracked his movements very attentively. Similar behavior has been found common for other gazelle species, as well (Walther et al., 1983). Our data supported our second hypothesis as, frequently in their interactions with peers, territorial males used space-claim behaviors closely related to aggressive patterns, such as bush and ground horning and the grazing ritual, while they demonstrated such agonistic behaviors considerably less often toward non-territorial adult males and what appeared to be accidently to immature males. Non-territorial males also used space-claim behaviors toward peers but only in limited cases, and again accidently toward immature males. In agonistic encounters of hoofed mammals, certain behavior patterns are not necessarily indentified as direct expressions of aggressive displays but rather as marking behaviors; however these activities always have undertones of aggression and occur in the immediate presence of an opponent. These indirect aggression activities are addressed not toward the opponent but toward the ground or vegetation and are called space-claim displays (Walther, 1984). Among space-claim displays in goitered gazelles, territorial males used mostly bush horning and the grazing ritual, and to a lesser extent ground horning. Ground and bush horning (object horning) are considered a mixture of both aggressive and marking behaviors, but our special investigations discovered that object-horning in goitered gazelles is rather more aggression than marking (Blank and Yang, 2014). Bush horning in our current investigations was found to be one of the most frequent behaviors after threat displays, and an important aggressive demonstration in conflicts between territorial males. Similar behavior was also found in Thomson’s gazelles (Walther, 1978). It was also observed that ground horning had enough agonistic importance to solve
25
territorial conflicts, and in gerenuk (Litocranius walleri), adult males were noted to use ground horning as a particularly strong threat toward young males (Estes, 1991). For goitered gazelles, neither bush horning nor ground horning displays were important aggressive demonstrations in agonistic behavior of non-territorial males. Urination-defecation and especially preorbital markings were used as space-claim displays as well, but their role was very limited in aggressive behavior of goitered gazelles, though both were observed frequently in connection with agonistic encounters in other ungulate species (Walther, 1984). Clearly, these acts were used more as marking behaviors in goitered gazelle rather than as aggressive displays. In addition, preorbital marking was used almost exclusively as a marking behavior for territorial goitered gazelle males, while non-territorial males demonstrated these kinds of space-claim behaviors very rarely. After bush horning, the grazing ritual was next in importance in goitered gazelles’ space-claim displays. The grazing ritual began as the two rivals held their heads close to the ground similar to a number of aggressive displays in many species. This ritual was observed, when both rivals stopped their aggressive displays toward each other and started what appeared to be grazing. But in fact, they were not really grazing, because the rivals continued to look at each other with their heads down, and then either restarted their contest or often just ended the conflict and left the area. The agonistic grazing of horned and antlered ungulates is possibly derived from an ancestral form of redirected aggression (Walther, 1984). In Thomson’s gazelle, the grazing ritual is also a primary behavior of territorial bucks, which they perform quite frequently; 36.7% of territorial boundary encounters were carried out exclusively by this ritual and most usually ended the territorial conflict. It is thought that this grazing ritual allows a territorial male to exit from conflicts without “losing face” (Walther et al., 1983). For goitered gazelles, the grazing ritual was observed rarely in aggressive interactions between territorial males vs. non-territorial bachelors and never between territorial males vs. immature males. Nonterritorial males used the grazing ritual infrequently and immature males very rarely. The point is that the grazing ritual was connected quite closely with territoriality, when a territorial male could not retreat from his territory, but just took a break in his aggressive displays; while non-territorial males were interested in establishing their hierarchical status within their group and the grazing ritual was a redundant behavior for that purpose. The grazing ritual is a typical behavior for most gazelle species (Walther et al., 1983; Habibi et al., 1993). In wildebeest (Connochaetus taurinus—Estes, 1969), bontebok (Damaliscus dorcas—David, 1973), kongoni (Alcelaphus buselaphus—Gosling, 1974) and topi, the grazing ritual is also restricted to territorial males (Walther, 1984). This situation is clearly different in species such as Grant’s gazelle and Oryx antelope (Oryx beiza), when actual grazing occurs relatively often in encounters between dominant and subordinate opponents, the latter of which respond by grazing (one-sided displays) when approached by a dominant (Walther, 1984). There were also aggressive behavioral elements that were observed only in non-territorial males and never in territorial bucks that were related to breaking individual distances between males and sniffing or touching one another. This behavior was observed when one opponent treated the other as an unequal rival with a lower social status. Territorial males did not display this behavior even toward immature males, who were already treated as the lowest status of individuals. Instead, the territorial males either just ran toward the young males to expel them from their territories, or else did not pay any attention to them at all (Blank, 1992). Our results also supported our third hypothesis, with the territorial males demonstrating mostly clash-fighting battles with peers and horn-pressing fights with non-territorial and immature males. In Thomson’s gazelle, clash-fighting is the most common type of
26
D.A. Blank, W. Yang / Behavioural Processes 108 (2014) 20–26
fighting between territorial neighbors, with the combatants jumping toward each other with all four legs (Walther et al., 1983). Territorial male goitered gazelles used mostly horn-pressing fights with non-territorial and immature males, and non-territorial bucks with peers and immature males. Horn-pressing fights are observed in all Antilopinae species, but with differences in frequency. In Grant’s gazelle, for instance, these fights are very common, whereas in Thomson’s gazelle, horn-pressing fighting usually occurs only in very long, intensive fights (Walther et al., 1983). Clash-fighting and horn-pressing fights both belong to high intensity fighting, when combatants move forward and backward according to their opponents’ maneuvers, but as a rule neither moves the other very far from his original position (Walther, 1984). Our data supported our fourth hypothesis in part. Indeed, territorial and non-territorial males mostly walked during interactions with their peers, because they were of equal status and it was not clear who was superior (Estes, 1991). However, territorial males used faster gaits more frequently in interactions with nonterritorial and immature males, because in these cases territorial males clearly overmatched the non-territorial and immature males in status and strength. There are cases in which chasing appeared to be a purely executive-type behavior and a “symbolic” action, when without any previous encounter, one (territorial) animal ran after the other (non-territorial and immature) male, preferring often faster gaits. Typically, this is most frequently used by animals of a high social status, such as territorial males, toward very inferior partners, especially immature males (Walther, 1984). In some antelope species, such as oribi (Ourebia ourebi), the horns are so dangerous that simply chasing a rival normally substitutes for fighting (Estes, 1991). However in contrast to our hypothesis, nonterritorial males did not demonstrate preference for faster gaits with immature males compared to peers, and used mostly walking in aggressive interactions with immature males like they did with peers in spite of their unequal status. Apparently, in contrast to the agonistic behaviors between territorial bucks and inferior males, chasing with fast gaits lacks of importance as a symbolic action in hierarchical interactions between non-territorial and immature males. In contrast, immature males had no gait preference in their aggressive interactions with their peers. Often while chasing, territorial males utter certain vocalizations, such as a roaring sound in impala (Aepyceros melampus) that in itself can cause an inferior male to flee as fast as he can (Schenkel, 1966). A similar behavior was observed in goitered gazelle, when territorial males addressed most of their vocalized chasing to non-territorial males, and less to immature males and peers. In contrast, nonterritorial males addressed most of their vocalized chasing to peers and considerably less to immature males. These observations also support the idea that territorial and non-territorial males behave differently during their agonistic interactions. So we concluded that territorial and non-territorial males had different repertoires of aggressive behaviors because of the differences in their social status and their motivations for agonistic displays.
Acknowledgments We thank the National Natural Science Foundation of China (U1303301), Chinese Academy of Sciences (CAS) for granting our work (Visiting Professorships for Senior International Scientists—2011T1Z42), West Light Foundation (CAS—Y336171) for creating all conditions for writing this paper. We are very grateful to the Institute of Zoology, former Academy of Sciences of Kazakhstan, which has given us the possibility for investigations of goitered gazelles in their natural environment during 10 years. We are grateful to Ms. Patricia Johnston for her useful
suggestions and remarks and constant help in English editing of this manuscript. References Barrette, C., 1977. Fighting behaviour of muntjac and the evolution of antlers. Evolution 31 (1), 169–176. Blank, D.A., 1985. Peculiarities of social and reproductive behaviour of Gazella subgutturosa in the Iliisky Valley. Zool. J. 64, 1059–1070 (in Russian, English abstract). Blank, D.A., 1990. Persian gazelle. In: Kovshar, A.F. (Ed.), Rare Animals of Desert Regions. Nauka Kazakh SSR Press, Alma-Ata, pp. 56–80 (in Russian). Blank, D.A., 1992. Social and reproductive behaviour of the Persian gazelle. In: PhD thesis. University of Tel Aviv. Blank, D.A., 1998. Mating behaviour of the Persian gazelle (Gazella subgutturosa Guldenstaedt, 1780). Mammalia 62 (4), 499–519. Blank, D.A., Ruckstuhl, K.E., Yang, W., 2012. Social organization in goitered gazelle (Gazella subgutturosa Guldenstaedt, 1780). Ethol. Ecol. Evol. 24, 306–321. Blank, D.A., Yang, W., 2014. Object-horning in goitered gazelle: agonistic or marking behaviour? Behav. Process. 103, 165–172. Bro-Jorgensen, J., 2007. The intensity of sexual selection predicts weapon size in male bovids. Evolution 61 (6), 1316–1326. Chiszar, D.A., 1978. Lateral displays in the lower vertebrates: forms, functions, and origins. In: Reese, E.S., Lighter, F.J. (Eds.), Adaptation in the Aquatic and Terrestrial Environments. J. Wiley, New York, pp. 105–135, Contrasts in Behaviour. Clutton-Brock, T.H., Albon, S.D., Gibson, R.M., Guinness, F.E., 1979. The logical stag: adaptive of fighting in red deer (Cervus elaphus L.). Anim. Behav. 27, 221–225. David, J.H.M., 1973. The behaviour of the bontebok, Damaliscus dorcas dorcas (Pallas 1766), with special reference to territorial behaviour. Z. Tierpsychol. 33, 38–107. Estes, R.D., 1969. Territorial behaviour of the wildebeest (Connochaetus taurinus Burchell, 1823). Z. Tierpsychol. 26, 284–370. Estes, R.D., 1991. The Behaviour Guide to African Mammals. University of California Press, Los Angeles. Farlow, J.O., Dodson, P., 1975. The behavioral significance of frill and horn morphology in Ceratopsian dinosaurs. Evolution 29 (2), 353–361. Geist, V., 1966. The evolution of horn-like organs. Behaviour 27, 175–214. Gosling, L.M., 1974. The social behaviour of Coke’s hartebeest Alcelaphus buselaphus cokei. In: Geist, V., Walther, F.R. (Eds.), The Behaviour of Ungulates and Its Relation to Management, IUCN Publ. No. 24. IUCN, Morges, pp. 488–511, Contrasts in Behaviour. Grau, G.A., Walther, F.R., 1976. Mountain gazelle agonistic behaviour. Anim. Behav. 24, 626–636. Guthrie, R.D., 1971. A new theory of mammalian rump patch evolution. Behaviour 38 (1/2), 132–145. Habibi, K., Thouless, C.R., Lindsay, N., 1993. Comparative behaviour of sand and mountain gazelles. J. Zool. (Lond.) 229, 41–53. Jennings, D.J., Gammell, M.P., Carlin, C.M., Hayden, T.J., 2003. Is the parallel walk between competing male fallow deer, Dama dama, a lateral display of individual quality? Anim. Behav. 65, 1005–1012. Li, C., Zhigang, J., Yan, Z., Coie, Y., 2004. Relationship between serum testosterone, dominance and mating success pere davids deer stags. Ethology 110, 681–691. Lundrigan, B., 1996. Morphology of horns and fighting behavior in the family Bovidae. J. Mammal. 77 (2), 462–475. Meng, X., Cody, N., Gong, B., Xiang, L., 2012. Stable fighting strategies to maintain social ranks in captive male Alpine musk deer (Moschus sifanicus). Anim. Sci. J. 83, 617–622. Perez-Barberia, F.J., Gordon, I.J., Pagel, M., 2002. The origin of sexual dimorphism in body size in ungulates. Evolution 56, 1276–1285. Rajagopal, T., Govindaraju, A., Geraldine, P., Balasundaram, C., 2010. Assessment of dominance hierarchy through urine scent marking and its chemical constituents in male blackbuck Antelope cervicapra, a critically endangered species. Behav. Process. 85, 58–67. Schenkel, R., 1966. On sociology and behaviour in impala (Aepyceros melamous suara Matschie). Z. Saugetierk. 31, 177–205. Shargal, D., Shore, L., Roteri, N., Terkel, A., Zorovsky, Y., Shemesh, M., Steinberger, Y., 2008. Fecal testosterone is elevated in high ranking female ibexes (Capra nubiana) and associated with increased aggression and a preponderance of male offspring. Theriogenology 69, 673–680. Skinner, J.D., Louw, G.N., 1996. The Springbok (Antidorcas marsupialis— Zimmermann, 1780). Transvaal Museum, Pretoria. Tsapluk, O.E., 1972. Age and seasonal dynamics of sexual activity in Gazella subgutturosa Gueld. Proceed. Acad. Scien. Kazakh SSR, Biol. Series 3, 39–46 (in Russian). Walther, F.R., 1978. Forms of aggression in Thomson’s gazelle: their situational motivation and their relative frequency in different sex, age, and social classes. Z. Tierpsychol. 47, 113–172. Walther, F.R., 1984. Communication and Expression in Hoofed Animals. Indiana University Press, Bloomington. Walther, F.R., Mungall, E.C., Grau, G.H., 1983. Gazelles and Their Relatives. Noyes Publications, Park Ridge, NJ. Wronski, T., Sandouka, M.A., Plath, M., Cunningham, P., 2010. Differences in sexual dimorphism among four gazelle taxa (gazelle spp.) in the Middle East. Anim. Biol. 60, 395–412. Zhevnerov, V.V., 1984. Goitered gazelle of the Barsa-Kelmes Island. Nauka Press of the Kazakh SSR, Alma-Ata (in Russian).