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Roaring function in male goitered gazelles
Accepted Manuscript Title: ROARING FUNCTION IN MALE GOITERED GAZELLES Author: D.A. Blank K. Ruckstuhl W. Yang PII: DOI: Reference:
S0376-6357(14)00130-2 http://dx.doi.org/doi:10.1016/j.beproc.2014.05.009 BEPROC 2839
To appear in:
Behavioural Processes
Received date: Revised date: Accepted date:
4-1-2014 13-4-2014 31-5-2014
Please cite this article as: Blank, D.A., Ruckstuhl, K., Yang, W.,ROARING FUNCTION IN MALE GOITERED GAZELLES., Behavioural Processes (2014), http://dx.doi.org/10.1016/j.beproc.2014.05.009 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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ROARING FUNCTION IN MALE GOITERED GAZELLES. D.A. Blank a,b*, K. Ruckstuhl c, 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;
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Institute of Zoology, Kazakh Academy of Sciences, Alma-Ata, Kazakhstan. Department of Biological Sciences, University Calgary, Canada.
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*Corresponding author: David Blank – [email protected], Fax +86-991-7885320
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Abstract.
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very close distance. The goitered gazelle is a rare exception to this rule, and during the rutting
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period territorial males of this species are among the noisiest antelopes. Rutting vocalization is
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such an essential part the rutting behaviour in goitered gazelle that adult males have a hypertrophic
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larynx, the muscle tissues of which increase considerably in size during the rut. We were
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interested in the frequency and variance with which male goitered gazelles emit their calls
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depending on an animal’s age, reproductive status and time of the year in order to understand the
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main function of the rutting vocalizations. We found that roaring was mostly related to courting
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displays, while vocalizations during aggressive displays were less frequent in male-male
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interactions. Acoustic signals likely enhance courtship displays and also may aid in accelerating
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female ovulation, promoting synchronization of breeding cycles during the mating and birthing
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periods, which last only several days for most of the females in our population. We discuss the
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Most of the vocalizations of Antilopinae males are soft and usually only heard from a
potential benefits of such behaviours and compare it to other species living in similarly extreme
environments.
Key words: Aggressive displays, courting behaviour, goitered gazelle, male vocalization, rutting roaring.
INTRODUCTION
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and acoustic signals are particularly widespread in communication and used by individuals of all
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ages and sexes in different social contexts (Vannoni et al., 2005). Bovids represent an interesting
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group, which show a wide variations of vocal signals and examples of convergent evolution with
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cervids and humans (Fitch and Reby, 2001; Frey et al., 2007, 2008 a,b). Adult males of many
In ungulates, as in other mammals, communication plays a crucial role in social interactions,
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ungulate species are known to give distinct loud calls just during the rutting season (Minami and
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Kawamichi, 1992). Most of these vocalizations even during the rut uttered by Antilopinae males,
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for example, are rather soft and usually can be heard only from a very close distance from animals
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in captivity (Walther et al., 1983). These species vocalize mainly through the nose, and only
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optionally also through the mouth (Walther, 1984). Only a few Antilopinae species, such as the
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Mongolian gazelle (Procapra gutturosa – Frey et al., 2008b), and goitered gazelle (Gazella
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subgutturosa – Blank, 1998), are exceptions from this rule in that territorial males of these species
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are the noisiest of all Antilopinae species. Rutting adult males of Mongolian and goitered gazelles
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vocalize through widely opened mouths, while the females of these species produce both oral and
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nasal calls (Frey et al., 2008 a,b).
It is well known that gazelles use their vocalizations both for courting and aggressive
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displays (Walther et al., 1983), but there are variations in use among species. For example, Grant’s
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gazelle males (Nanger granti) rarely roar, but when they do, it is always connected to courting
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females, while in Thomson’s gazelles (Eudorcas thomsonii) rutting calls are most commonly heard
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during aggressive displays and more rarely while courting females (Walther et al., 1983). Roaring
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during the rut is a very typical phenomenon in goitered gazelles and vocalizations are an integral
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part of courtship and aggressive displays by territorial males (Blank, 1998). Goitered gazelle
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males are also distinctive in that they have an anatomical adaptation for uttering these relatively
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“real” rut in November-December and a “false” rut in April-May, do many adult males establish
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individual territories and increase the frequency of their courting and aggressive displays by many
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times. Goitered gazelles mate only during the “real” rut, and females give birth only once a year,
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in May (Blank and Fedosenko, 1983; Blank, 1998). The second “false” rut in goitered gazelles has
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been hypothesized to be an ancestral trait from warmer geological periods, when this species had
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the environmental conditions and ability to breed twice a year (Sludskiy 1956; Tsapluk 1972),
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loud rutting calls, namely, an enlarged and descended larynx, the muscle tissues of which considerably increase in size during the rut (Blank, 1998; Frey et al., 2011). The goitered gazelle is a medium-sized ungulate, which originally was spread widely all over
of Middle and Central Asia, Iran, Afghanistan, Turkey, and the Caucasus (Kingswood and Blank, 1996). This species typically lives in small groups of 2-3 individuals (Blank et al., 2012b). In male goitered gazelles, courting and aggressive displays are seen all year round, but only during the
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though this so called ancestral behaviour certainly needs further investigations. In spite of the fact that the morphology of the vocal apparatus and acoustical features of
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goitered gazelle vocalizations have been described well in recent reports (Efremova et al., 2011
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a,b; Frey et al., 2011; Volodin et al., 2011), the behavioural aspects of their vocalizations are still
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poorly understood. This paper describes the behavioural components the rutting vocalizations and
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quantifies the characteristics of goitered gazelle roaring depending on season, social status, and the
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age of displaying males. We suggest several hypotheses for the occurrence of rut roaring in
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goitered gazelles.
In polygynous cervids and bovids, vocal features were found to be linked to the physical
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quality of rutting males and to play a decisive role in the reproductive success of the caller (Reby
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and McComb, 2003; Reby et al., 2005; Charlton et al., 2007, 2008). Since in many Antilopinae
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species adult males use their vocalizations most often while courting females or expelling rivals
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from their territories (Walther et al., 1983), we expected to find significant seasonal fluctuations in
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male roaring rates, with adult males vocalizing most often during the rutting period in
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November-December, less often during the “false” rut in April-May, and least often during the rest
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of the year. In addition, due to a considerable increase in the size of the larynx muscle tissues
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during the rut (Frey et al., 2011), we expected that vocalizations would be louder and better heard
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during the rut than outside the rut.
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In other words, the frequency of vocalizations would increase with an increase in the number of
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potential individuals to whom the adult male would display either courting or aggressive
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behaviours.
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It also was found that the rutting vocalizations of adult male goitered gazelle have low
amplitude and consequently a poor propagation rate through the environment; therefore adult males must approach a recipient to perform their courting or aggressive displays at close range (Frey et al., 2011). So, we predicted that adult males would produce calls more often in the presence of other males or females than when they were alone, and that vocalization frequency would grow with the size of the female or male groups that intruded into the adult male’s territory.
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Territorial males are the most active individuals during the rutting period (Walther et al.,
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1983), so we predicted that territorial males would vocalize more often than sub-adult males and
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non-territorial males in groups, especially during the rut in November-December.
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The goitered gazelles’ retractable larynx and vocal tract have evolved in such a way that
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during the rut, adult males, as compared to other ruminant species, can emit rutting calls even
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while running at a full gallop (Frey et al., 2011). We therefore predicted that adult males would run
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mainly at a high (galloping) speed during their vocalized courting or aggressive displays, because
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of their intensified arousal and rutting displays, while outside the rut they would vocalize at
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usually lower speeds.
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MATERIAL AND METHODS
The term “roaring” is commonly used for vocalizations of large animals, such as lions
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(Panthera leo), leopards (P. pardus), elephant seals (Mirounga angustirostris), red deer and musk
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oxen (Ovibos moschatus), but we have used this term for the goitered gazelle’s vocalizations based
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on the more general definition of Weissengruber et al. (2002), who suggested that a roar is
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specified as a call type with a low fundamental frequency and lowered formant frequencies.
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Observations for our study were conducted in the Ili depression (southeastern Kazakhstan) during a 6-year period from 1981 to 1986. We mostly made focal animal observations,
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concentrating on only one randomly selected group of gazelles at a time (usually the closest), and
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continuously sampled separate group members for up to 9 hours while recording the courting and
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aggressive displays both accompanied by calls and without calls. With aggressive displays, every
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occurred. In most cases, gazelles were observed from distances of 50-100 m, with observation
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posts usually established on elevations from where we could see 30-50 gazelles at the same time.
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During the rut, the size of a male’s territory was 50-80 ha (Blank, 1985), and we typically could
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observe 5-6 individual territories simultaneously from our elevated observation point. And since
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females were distributed unevenly among territories (Blank, 1998), we chose a male closest to our
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observation point that had at least one female in his territory. To avoid pseudo-replication, we
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agonistic interaction between two rivals was calculated as a single incident, and the same for each vocalized aggressive display. Only one rival (territorial male) used his roaring against the male-intruder, which retreated usually without vocalization, each of such interaction also was calculated as a single case. Vocalizations were rarely observed during conflicts between territorial
males.
All behaviours were recorded in the order in which they occurred and each time they
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changed our observation point every day and tried to observe in different parts of the study area
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(over ～4600 km2), establishing 20 different observation sites. The total size of the study
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population in the Ili depression was estimated to range from 1.5 thousand in 1981 up to 5 thousand
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in 1986 (Blank, 1990). For focal observations we used binoculars (magnification 8x) and a
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telescope (magnification 30x- 60x). We conducted 181 hours of focal observations in April, 470
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hours in May, 374 hours in June, 173 hours in July, 224 hours in November and 148 hours in
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December over the 6-year period.
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Goitered gazelles vocalized while courting females and chasing other males when performing aggressive displays, so we made a distinction between courting and aggressive vocalizations.
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Courting territorial males demonstrated their roaring mostly while demonstrating the low-stretch
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and high-stretch postures; the description (ethogram) of these displays is presented in Table 1.
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Among aggressive displays, adult males vocalized mostly while in dominance and threat postures,
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and rarely during battles (horn-pressing) (Table 1). Frey et al. (2011), using auditory and video
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recording techniques, found that rutting calls of adult male goitered gazelles consist of three types
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of sounds: roars, growls and grunts. Since we were using only our ears and eyes, we did not
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distinguish these types of calls, and in this paper called rutting vocalization “roaring”, keeping in
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mind that these vocalizations consisted in fact of the three types of calls mentioned above. In
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addition, Frey et al. (2011) pointed out that male goitered gazelles produced their rutting
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January, February, March, and September. For our investigations into differences in goitered
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gazelle vocalized and non-vocalized courting and aggressive displays based on sex, age, season,
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and territorial status, we used two main indices: the absolute frequency of vocalization during
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courting or aggressive displays (number of behavioural acts per hour of observation) and relative
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frequency (proportion of observations with vocalizations out of the total number of all
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observations). The first index just stated whether the frequency of vocalized displays increased or
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vocalizations only through widely opened mouths, while our observations showed that during slow gaits (walking, trotting), the male’s nostrils also may participate in the producing rutting sounds (Table 1).
We investigated the frequency changes of vocalizations according to the breeding cycle and
distinguished three biological seasons for the goitered gazelle: rutting season (mid-November to mid-December), “false” rut (April-May) and outside of the rut (June-August); data were absent for
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decreased over months, while the second index gave an idea of whether the proportion of
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vocalized versus non-vocalized displays increased. It was possible to individually identify separate territorial males, since they stayed in the
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same area for several weeks. Most other individuals, though, were not individually recognizable,
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although we were able to differentiate gazelles according to sex (horned males and hornless
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females) and age (adult and sub-adult males and adult and sub-adult females). The age of all
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goitered gazelles observed was differentiated based on the descriptions of Zhevnerov (1984): adult
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males (older than 2 years old – horns 1.5 times longer than ears and absence of the black spot on
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the front of the muzzle), adult females (older than 2 years old – hornless and absence of black spot
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on the front of the muzzle), sub-adult males (1-2 years old – horns are equal or shorter than ears
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and presence of a black spot on the muzzle front), sub-adult females (1-2 years old – hornless and
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black spot on the muzzle front), young (up to 1 year old, body size 2-3 times smaller than in adult
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gazelles and a black spot on the muzzle front).
We used One-Way ANOVA followed by LSD Post-Hoc test and a General Linear Model
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(GLM, Type 3 Sum of Squares) to test for the effect of month and age on absolute and relative
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frequencies of vocalization acts. These data were normally distributed according to Shapiro-Wilk
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and Kolmogorov-Smirnov tests. We used Log-linear models to compare proportions of separate
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behavioural acts and Spearman’s Correlation for a possible correlation between frequency of
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increasing in occurrence 6.1 times in April, 36.4 times in November and 37.5 times in December
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compared to July (Post-Hoc LSD test, P < 0.05, 0.002 and 0.001, respectively) (Fig. 1). The
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frequency of aggressive patterns also increased during these months, but overall changes were
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insignificant (One-Way ANOVA, F = 1.974, df1 = 7, df2 = 83, P = 0.068). Furthermore, the roaring
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was soft and difficult to detect in most months at distances more than 50 m and only during the
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rutting period in November and December were these sounds relatively loud and clearly heard
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vocalized displays and group size. All statistical analyses were conducted using SPSS 17.0 software package.
RESULTS
We found that adult male goitered gazelles’ vocalized courting patterns were varied and
fluctuated significantly over months (One-Way ANOVA, F = 12.242, df1 = 7, df2 = 141, P < 0.001),
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from distances up to 300-400 m. The relative frequency of courting displays also fluctuated
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significantly over months (One-Way ANOVA, F = 3.514, df1 = 7, df2 = 132, P = 0.002), but in fact
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only in November was this value significantly larger compared to other months (Post-Hoc LSD
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test, P < 0.01), and insignificant at all other times (P > 0.05). The relative frequency of aggressive
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displays fluctuated insignificantly (One-Way ANOVA, F = 0.133, df1 = 6, df2 = 74, P > 0.05).
In adult males, the yearly average frequency of vocalized courting displays exceeded 2.4
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times the aggressive patterns with vocalizations (GLM test, F = 8.869, df = 1, P = 0.003), and only
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in July, were aggressive displays with calls observed more often than courting patterns (1.8 times)
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(GLM test, F = 9.039, df = 7, P < 0.001). The relative frequency showed the same trend, with
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courting displays’ exceeding 1.2 times the aggressive patterns (GLM test, F = 5.248, df = 1, P =
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0.023). In addition, our analysis showed that maximal frequency of vocalization by an adult male
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was demonstrated when he stayed together with one female (26%, n = 903), while he was roaring
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slightly less often with two or three females (21-22%) (Log-linear model test, Z = -2.111-2.574,
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P = 0.035 and 0.01), and much less when he had a larger female group or when alone (1-7%)
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(Z = -3.631-5.577, P < 0.001). However, the frequency of vocalizing of males in female groups of
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different sizes was closely correlated with the proportion of available groups (Spearman’s
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Correlation = 0.982, N = 203, P < 0.001). Furthermore, territorial single males vocalized
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significantly more often while courting females, than did non-territorial males in groups
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from the rut (Z = -4.337-5.002, P < 0.001), and adult males vocalized more often in male groups
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(up to 11 individuals) than when they had only one rival. However, frequency of vocalizing males
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in groups of different size was also closely correlated with the proportion of available groups
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(Spearman’s Correlation = 0.999, N = 185, P < 0.001).
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(Log-linear model test, Z = 4.494, P < 0.001), with the maximum difference in November and December (Z = 7.812 and 4.219, P < 0.001), a smaller difference in April (Z = 3.055, P = 0.002), and no difference between single and group males in other months (P > 0.05). During the aggressive displays in the rut (November-December), adult males vocalized most often when they had one rival, and considerably less often when they chased male groups of 2 or more rivals (Z = -4.293, P < 0.001). Outside the rut, the distribution of vocalization frequency was different
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Sub-adult males started to show vocalized courting displays in April, with some increase in
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frequency during May-July (One-Way ANOVA, F = 7.382, df1 = 3, df2 = 19, P = 0.002); in other
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months such behaviour was not observed. The relative frequency fluctuated insignificantly during
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April-July (One-Way ANOVA, F = 1.093, df1 = 3, df2 = 15, P > 0.05). The average frequency of
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calls during aggressive displays in sub-adult males was insignificantly higher than their calls
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during courting displays (GLM test, F = 1.328, df =1, P > 0.05). In April, vocalized courting
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displays in sub-adult males were observed much more rarely (3.4%, n = 58) compared to adult
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males. Further, this proportion increased from 15.3% (n = 98) in May and up to 40.9% (n = 44) in
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June and again decreased by as much as 12.5% (n = 8) in July. The proportion of vocalized
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aggressive displays in sub-adult males was even lower than in adult males and fluctuated between
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3-4% (n = 59) in April-May and 10% (n = 10) in June.
In any month, adult males produced calls usually when courting females, and especially
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frequently in November-December (98% cases, n = 911) and April-May (94%). They rarely
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vocalized before starting a chase (Log-linear model test, Z = 9.325, P < 0.001), though in July they
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called before chasing more frequently (up to 30% cases). Adult males commonly vocalized in the
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low-stretch or high-stretch postures, especially often in November-December (99.6%, n = 913),
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and even outside the rut this proportion only decreased to 88%; rarely did adult males vocalize in a
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neutral posture (Z = - 6.250, P < 0.001). Vocalizations were performed most often with an elevated
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tail (in a horizontal position), especially in November-December (89-96%, n = 859) and
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April-May (95-98%) (Log-linear model test, Z = 6.194, P < 0.001). More rarely they vocalized
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(Z = -7.023, P < 0.001) (Fig. 2). And November did not differ from December (Z = 1.556,
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P > 0.05). In contrast, outside the rut adult males produced calls mostly while moving at a slow
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pace (walking or trotting – 30-55%), and in July-August even in a standing position (11-38%)
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(Log-linear model test, Z = -5.807-7.922, P < 0.001). With aggressive behaviour, territorial males
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typically vocalized while driving intruders-bachelors (non-territorial males) out of their territories,
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and rarely used their calls during conflicts with other territorial males (Log-linear model test, Z =
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with the tail in a vertical or down position, but increasing the proportion of the last pattern by up to 20% outside the rut (August). While calling, the auricles were usually pressed backward toward the neck (70-99%, n = 753) and more rarely in a neutral position (Z = 9.242-11.781, P < 0.001). In November-December, roaring adult males chased females most often while galloping
(33-41%, n = 697) (Log-linear model test, Z = 2.458, P = 0.014), less frequently when walking (31-39%) or trotting (24-27%), and least often while standing (1-1.5%) and/or jerking (1-2.6%)
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2.638, P = 0.008). All year round, roaring adult males mostly walked (up to 75%) when chasing of
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other males, while trotting and galloping were observed considerably less often (15-30% and
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6-28%, respectively) than walking (Z = -3.307-4.315, P < 0.002). However during the rut, the
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territorial males chased their rivals more often using faster gaits (trot or gallop), resulting in a
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decrease in the portion of walking pursuits (45-50%, n = 601); conversely, walking pursuits
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increased outside the rut (53-75%, n = 330) (Z = -3.307-7.490, P < 0.001). Calls made by adult
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males while standing and/or jerking occurred least often (1-10%).
When courting females, territorial males produced calls periodically, while constant roaring
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during the entire chase sequence was rarely observed. During the most intensive courting period
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in November, however, the portion of constant roaring increased by up to 28% (Chi squire of fit
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test, Chi squire = 106.681, df = 1, P < 0.001). Most often during aggressive chases in the rut,
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territorial bucks used single, infrequent, and relatively long-term (2-3s) calls while expelling
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non-territorial males from their territories (46-54%, n = 74), as well as when following passing
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bachelor males (45-51%, n = 72) (Log-linear model test, Z = - 0.439, P > 0.05); outside the rut
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adult males followed each other mostly with bouts of short (less than 1s) and frequently repeated
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calls (Z = - 4.536, P < 0.001). There was no difference in the proportion of these calls between
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November and December (Z = -1.628, P > 0.05), but these two months differed significantly from
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other months (Z = -4.055-4.581, P < 0.001).
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and relative frequencies of vocalization during courtship significantly increased during the real rut.
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Hence, adult males roared more frequently per hour of observation not only because of an increase
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in the total number of courting displays during the rut, but also because of an increase in the
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proportion of vocalized versus non-vocalized displays. In contrast, during aggressive displays,
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adult males showed insignificant increases in vocalized displays compared to the non-rutting
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period. In addition, goitered gazelles vocalized considerably more often during courting displays
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DISCUSSION
Adult males showed considerable seasonal fluctuations in their vocalization; roaring during
their courtship and aggressive displays were observed all year round, with some increasing frequency during the “false” rut in April-May and maximum frequency during the real rutting period in November and December, compared to other months of the year. And both the absolute
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than aggressive demonstrations, and only in July, when testicle physiological activity was minimal
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and most adult males gathered in large groups (Tsapluk, 1972; Blank et al., 2012a), did the
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vocalized aggressive interactions exceed the courting displays. Thus, roaring in goitered gazelles
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is more related to courting displays than to aggressive patterns, with males accompanying up to
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half of their courting displays by roaring (Blank, 1998).
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The same phenomenon was found in red deer (Cervus elaphus), where the stag’s roar is
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speeding up ovulation, which improves mating success with frequent calling (Fedosenko, 1980;
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McComb, 1987, 1991; Charlton et al., 2007). Similarly in fallow bucks (Dama dama) time
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invested in vocal display is linked to mating success (McElligott et al., 1999). Among Antilopinae
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species, Grant’s gazelles only rarely emit relatively loud roars, except when courting females
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(Walther et al., 1983). It is possible that territorial male rutting roars in goitered gazelles serve the
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same function as in deer, namely to promote ovulation.
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Goitered gazelle rutting roars were loud enough to be clearly heard from a distance of several
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hundred meters, while outside the rut adult males’ calls were difficult to hear from a distance of
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more than 50 m. Furthermore, during the rut males produced long-term, usually single or
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infrequent calls, while outside of the rut adult males followed each other mostly with bouts of
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short and frequently repeated calls, especially during aggressive displays.
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male goitered gazelle is much larger and rests lower in the neck (Frey et al., 2011; Volodin et al.,
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2011). An increase in larynx size and the vocal tract elongation leads to the acoustic effect of
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producing calls with lower frequency and resonance, which are unexpected low for an animal the
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size of the goitered gazelles (Frey et al., 2011). The same phenomenon is found in three
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mammalian taxa: among bovids, which apart from goitered gazelles, is also present in Mongolian
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gazelle; among cervids, such as fallow deer and red deer; and in humans (Bigalke, 1972; Walther,
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allow increasing reproductive success through mate competition or mate choice (Espmark et al., 2000). It is likely that vocalizations in goitered gazelle are a result of the same processes, and rutting calls in adult males are such an important and essential component (Blank, 1998), that males have a large and very prominent larynx or “Adam’s apple” (Kingswood and Blank, 1996) with muscle tissue that noticeably increases in size (up to 50%) during the rut (Frey et al., 2011). Compared to domestic bovids of similar size, and even females of conspecifics, the larynx of the
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1981; Fitch and Reby, 2001; McElligott et al., 2006; Frey et al., 2008 a,b). As predicted, adult goitered gazelle males showed their vocalization most often when they
310
had females inside their territories or with rivals for aggressive displays, while they vocalized
311
rarely when they were alone. The significantly enlarged larynx of goitered gazelle males is
312
adapted for producing low-amplitude close-range calls (Frey et al., 2011). Therefore having
313
relatively large-sized individual territories, goitered gazelle usually started to call after
314
approaching females or rivals and rarely vocalized over long distances in response to activities of
315
other males in neighboring territories (Blank 1998). The same behaviour also was observed in
316
Mongolian gazelles (Frey et al., 2011).
Contrary to our predictions, the calling rate didn’t increase with group size, and vocalizations
318
of adult males were noted frequently when courting of small female groups (2-4 individuals),
319
while cases of vocalized courting displays for larger groups were observed significantly less often.
320
A similar behaviour was observed for aggressive displays during the rut, when adult males
321
produced calls most often for one rival (single bachelors), and considerably less often, when
322
chasing male groups of any size. In contrast, outside the rut, males addressed their vocalized
323
aggressive displays more often to male groups than to a single male. Our analyses showed,
324
however, that this was not a result of males’ preference to call for groups of a certain size, but was
325
a consequence of the goitered gazelles’ social structure, where small female groups and single
326
331 332
adult males or bachelors, which may gather into groups, sometimes also court females in mixed
333
groups, or when a bachelor group occasionally meets a herd of females. In this case, several males
334
will run after the same female, which then usually results in fighting. A territorial male is regularly
335
chasing male groups, attempting to separate the non-territorial males away from his females
336
(Walther et al., 1983). Since territorial males are constantly defending their territory from rivals,
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they have a high rate of aggressive displays, while bachelors without territories only occasionally
327 328 329 330
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males were more common during the rut than outside of it (Blank et al., 2012b). Territorial males vocalized during courting and aggressive displays significantly more often
than bachelor bucks in groups and sub-adult males. Territorial males, and territoriality as a whole, have the greatest impact on reproductive success, since in many Antilopinae species, including goitered gazelles, reproduction is almost exclusively done by territorial males (Walther et al., 1983). When females arrive in their territories, territorial males are busy courting. Non-territorial
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have conflicts within their groups. We found the frequency of vocalized courting and aggressive
339
displays to be closely correlated with the total frequency of all displays, including non-vocalized
340
ones; therefore territorial males vocalized significantly more often than bachelors in groups.
341
During the “false” rut (April-May), only some adult males became territorial, while the majority
342
stayed in groups (Blank, 1998); therefore the behavioural difference between single (territorial)
343
males and bachelors in groups was less pronounced. During the non-rut period, territoriality in
344
males was absent and the proportion of single males was at a minimum (Blank et al., 2012a), so
345
differences in the frequency of vocalization between single males and group males were
346
negligible.
The vocalizations of young males started to differentiate from females’ as early as the second
348
week of life (Efremova et al., 2011a). Young males become interested in females by the age of 6
349
months, but just follow the females and sniff their hindquarters, demonstrating only a neutral
350
posture (Blank, 1998). Vocalized courting and aggressive displays of sub-adult males started in
351
April at the age of one year. Later (May-July), the frequency of vocalized display increased, while
352
during the real rut in November-December, sub-adult males did not perform vocalized courting or
353
aggressive displays at all. Adult males had a sharp decrease in activity in June-July, starting at the
354
end of the “false” rut in May, while proportion of vocalized displays of sub-adults increased
355
during the same period compared to adult males. This behavior of sub-adult males corresponds to
356
361 362
while adult males vocalized courting displays significantly more often than aggressive displays.
357 358 359 360
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the cyclical physiology of their testicle development, which begins to function for the first time in April, when the “false” rut starts in adult males; sub-adult testicular activity continues through May-July then demonstrates a distinctive waning in November. In contrast, the activity of adult male testicles is at its maximum during the rut in November-December, less during the “false” rut in April-May and fades during non-rutting periods (Tsapluk, 1972). It is interesting to note that sub-adult males used calls with the same frequency during both courting and aggressive displays,
363
As observed in the non-rutting period, adult males following females preferred to make calls
364
while moving at a slow gaits (walking and trotting). During the rut, however, roaring territorial
365
males chased females most often when galloping – a phenomenon made possible by the
366
anatomical construction of the goitered gazelle’s vocal apparatus (Frey et al., 2011). The point is
367
that during the rutting period females don’t remain continually within an individual male’s
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territory, but instead just crosses through it on their way to their daytime resting sites (Blank,
369
1998). The territorial male, then, tries to keep the female group within his territory as long as
370
possible, herding and courting, usually at a gallop, one female after the other in an attempt to drive
371
them into the center of his territory (Walther et al. 1983). While engaged in this chasing, males
372
utter their roars very often (Blank, 1998). In contrast, territorial males used their vocalized
373
aggressive displays almost exclusively against bachelors-intruders while expelling them from their
374
territories, while they did not use their roaring for solving territorial conflicts with their neighbors.
375
They used their calls without physical conflict, because the male-intruders retreated without
376
resistance and without returning the calls - it was always a one-sided display. Roaring territorial
377
males used their calls to demonstrate their territorial status to bachelors (Walther, 1981), but they
378
did not vocalize when addressing their aggressive displays to their neighbors, possibly because all
379
neighbors were familiar with each other individually. During the rut territorial males mostly
380
expelled intruders-bachelors from their territories while walking, because the males-trespassers
381
(bachelors) usually retreated by walking or more rarely trotting. Outside the rut, adult males also
382
chased each other using a rather slow gaits (mostly walking) as opposed to a faster ones
383
(galloping), because aggressive interactions between members within the same male group always
384
had playful characteristics and serious conflicts were rarely observed (Blank 1992).
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Adult males produced their roaring calls while posed in erected postures (low-stretch and
391
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392
So why are goitered gazelles a rare example of mouth-produced rutting vocalizations, which are
393
louder than in most other Antilopinae species? Walther (1981) emphasized the exclusive
394
importance of rutting vocalizations for males of all territorial antelope species as an advertisement
395
of their territorial social status, both when courting females and when chasing away bachelors.
396
However, only a few have relatively loud rutting calls (Walther et al., 1983). Our explanation is
397
that most tropical antelope species have extended or perennial breeding periods, thus maintaining
386 387 388 389 390
high-stretch), when they vocalized with an extended throat region. An elevated head tends to decrease formant frequencies by a slight elongation of the length of the vocal tract and is, therefore, producing sounds of a lower tone (timbre). These stretched postures are also typical for roaring of red deer stags and Mongolian gazelles (Frey and Gebler, 2010). Many antelope species make rutting vocalizations when chasing females, though their
nasally-produced sounds are usually soft and difficult to detect at a distance (Walther et al. 1983).
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continual territoriality (Estes, 1991). In contrast, goitered gazelles have a very short, exacting
399
overall autumn rutting period (mid-November-mid-December), with most matings occurring
400
within a 4-6 day period (Blank, 1998). As a result, most females give birth within a short period
401
(just several days) at the end of May that coincides with the most favorable time of year, which is
402
very limited in the Central Asiatic deserts (Blank et al., 2012a). To achieve such a high
403
synchronization in birthing, goitered gazelles have to perform very short, vigorous rutting period
404
(one month) with intensive rutting vocalizations with low-formant calls, which are particularly
405
attractive for females, and are likely accelerating their ovulation and synchronization their
406
ovulatory cycles. Mongolian gazelles, which live in conditions comparable to those in Middle Asia
407
(Western Central Asia) with cold snowy winters and hot dry summers, have similar anatomical
408
and behavioural adaptations (Leimgruber et al., 2001; Frey et al., 2011).
Saiga antelope (Saiga tatarica) has another anatomical adaptation (trunk-like nose) for
410
producing low-formant rutting calls (nasal roaring), which are also attractive for females (Frey et
411
al., 2007); but similar to goitered and Mongolian gazelles, saiga almost constantly express their
412
vocalizations during their short and vigorous rutting period (Volodin et al., 2009) to also achieve a
413
very high synchronization in birthing (5-8 days – Bekenov et al., 1998). Other ungulates, such as
414
chiru (Pantholops hodsonii) and Tibetan gazelle (Procapra picticaudata), living in the
415
high-elevated cold deserts of the Tibetan Plateau, also use relatively loud, deep-throated roars
416
421 422
vocalizations (Pohle, 1974).
417 418 419 420
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(chiru) and grunting roars (Tibetan gazelle) frequently during their vigorous and brief rutting season to likely achieve a high synchronization in births, which last approximately a week (Schaller, 1998). The anatomical adaptations of these species still have not been investigated,
though it is known that chiru males have distinctive walnut-sized bulges of their nostrils that enlarge their nasal passages and that they use both nasal and mouth-produced calls for rutting vocalizations (Schaller, 1998). Tibetan gazelle has proboscis-like noses, which are inflated during
423
Finally, the springbok, a gazelle-like antelope, lives in a completely different environment in
424
southern Africa. It has been called both a seasonal and a non-seasonal breeder (Bigalke, 1972;
425
Smithers, 1983), but male springboks, which make relatively loud vibration rutting calls through
426
their widely opened nostrils, are also the nosiest among Antilopinae (Walther, 1981). This seems
427
contradict our supposition that relatively loud rutting vocalizations are important for
Page 14 of 24
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synchronizing mating and birthing cycles in females. In fact, springboks also demonstrate
429
synchronization of oestrous and the subsequent clumping of births (Skinner et al., 1992), though
430
this species gives birth in an opportunistic, pulse-like manner (in different months) because birth
431
peaks occur at the beginning of the rainy season, the timing and duration of which is unpredictable
432
in the arid environment of southern Africa (Skinner and Louw, 1996). In addition, the spring
433
birthing season of springboks in Cape Province and Namibia varies from year to year by up to two
434
months, and a second autumn birth peak occurs only during favorable years (Estes, 1991).
All these species have different anatomical adaptations for producing rutting vocalizations,
436
but each uses its relatively loud rutting roars to intensify courting and synchronize breeding cycles.
437
This point is attributable to the fact that most females give birth during the most favorable time of
438
year for rearing young, which is an especially narrow time window in the northern Asiatic deserts,
439
including the cold deserts of the Tibetan Plateau. Furthermore, the function of rutting vocalizations
440
as an advertisement of territorial status (Walther 1981) is not inconsistent in fact to our
441
explanations. Rutting vocalizations, as a cue to territorial (high social) status, make a territorial
442
male particularly attractive to females, so the main function of rutting vocalizations in adult male
443
goitered gazelles seems to be in courting females to promote synchronization of the mating and
444
birthing cycles. Females mate exclusively with territorial males, even though non-territorial males
445
are also fertile (Skinner and Louw, 1996). This, then, defines vocalizations as an extremely
446 447 448 449 450 451
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valuable part of a male’s breeding success, while vocalized aggressive displays are less often observed and likely play a minor role in male-male interactions.
Acknowledgments
We thank the National Natural Science Foundation of China (U1303301), Chinese Academy
452
of Sciences (CAS) for granting our work (Visiting Professorships for Senior International
453
Scientists – 2011T1Z42), West Light Foundation (CAS – Y336171) for creating all conditions for
454
writing this paper. We are very grateful to the Institute of Zoology, former Academy of Sciences of
455
Kazakhstan, which has given us the possibility for investigations of goitered gazelles in their
456
natural environment during 10 years. We thank Mrs. Patricia Johnston, who did the constant help
457
in editing this manuscript.
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466 467 468 469 470 471
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Bigalke, R.C., 1972. Observations on the behavior and feeding habits of the springbok, Antidorcas marsupialis. Zoologica Africana 7, 333-359.
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the Saiga antelope in Kazakhstan. Mammal Review 28(1): 1-52.
Blank, D.A., 1985. Peculiarities of social and reproductive behaviour of Gazella subgutturosa in the Ili Hollow. Zool. Zhurnal 64, 1059-1070 (in Russian with English abstract).
us
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Bekenov, A.B., Grachev, IU.A., and Milner-Gulland, E.J. 1998. The ecology and management of
Blank, D.A., 1990. Persian gazelle, in: Kovshar, A.F. (Ed.), Rare animals of desert regions. Nauka Kazakh SSR, Alma-Ata, pp. 56-80. (in Russian).
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Figure Legends:
Fig. 1. Frequency (act/h) fluctuations of vocalized courting (Court) and aggressive (Agress) displays of adult males over months. Totally, it was observed 204 cases of vocalized aggressive and 955 cases of vocalized courting behaviours during 1690 hours of focal observations. Fig. 2. Relative proportions of vocalized courting (A) and aggressive displays (B) in adult males at different paces over months.
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Jul Aug Months
Aggres
Court
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May
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A.
Mar
May
Jun
Standing
592 B.
Jul Aug Months
Walking
Trotting
Oct
Nov
Dec
Galloping
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Apr
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100% 90% 80% 70% 60% 50% 40% 30% 20% 10% 0%
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Proportion
590 591
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70% 60% 50% 40% 30%
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Proportion
100% 90% 80%
20% 10% 0%
Mar
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Apr
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Standing
Jun
Jul Aug Months
Walking
Trotting
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Galloping
Dec
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Table 1. Description of the recorded courting displays and roaring (ethogram) in adult males goitered gazelle during the rut according to Walther et al. (1983) and Blank (1998). Courting postures
Description Stretching the head and neck forward horizontally with the nose pointing horizontally forward. Auricles are directed backward and usually pressed to the head in a position either parallel to the ground or slightly downward with the aperture inward. Rarely auricles lay back, pressed to each other, or held one apart of the other at a 45° angle. Tail is lifted in different degrees, up to vertical position.
High‐stretch or nose‐lift or head‐up
Head and neck are stretched forward and upward up to 45° above the horizontal level, the top of the muzzle lifted forward and upward, and auricles pressed to the head.
Roaring
Roaring consists of gruff, wheezing or hissing sounds resembling gurgling or sneezing. In producing these sounds, the male opens his mouth widely, lifts his tongue slightly and takes a deep breath, then passes air through his partly closed mouth and possibly as well as his nostrils. During a long and fast gallop, the male’s mouth is open and his tongue out. Posture: Muzzle is raised to an angle of up to 45° from a horizontal position. Auricles are directed backward and tightly pressed, more or less, to the head by apertures inside. Abruptly, the male jerks his head and whole body forward and upward, and his protruding thyroid cartilage moves down and up. During the run, the roaring is intermittent.
Aggressive postures Dominance
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Low‐stretch or neck‐stretch
Description
Rivals stand in lateral T‐position, parallel or, most commonly, reserve‐parallel orientation. The erected posture, when the neck is vertically erected upwards “proudly”. The entire body stays as high as possible due to stretching all four legs upwards. The nose is pressed to a neck and horns are directed forward and the head is turned in a more or less pronounced fashion away from opponent. Tail is uplifted and in waving movements from one side to another; ears are apart horizontally and directed sidewise by tops, and their holes are directed forward or downward. All walking movements are unusually slow.
Ac ce p
597 598 599
Threat
Horns are directed forward. Ears are directed forward‐sideward; tail is normal position.
Horn‐pressing
The rivals approach each other with lowered heads to the ground without preliminary displays of threat and lean the frontal surfaces of their horns against each other. They fight while standing on all four legs with the forelegs widely spread, and hindlegs in normal position or relatively close together. Each of them tries to press the horns of the opponent to the ground and move him back. Then everyone hits the revival’s head with maximum power and presses the head to the ground and back again,
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marking jerks. The horns almost invariably interlock (horn of one between horns of another). This fight can transfer to fight‐circling, when rivals do circles with locked horns. In this situation, they pivot with their hindquarters while keeping their heads in the circle center. During fighting, the ears are directed sidewise by top horizontally or backward sometimes and tail is pressed. This fight is common for non‐territorial males.
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Highlights The quantitative characteristics of vocalized male displays in goitered gazelle have never been considered before now. Male vocalizations were mostly related to courting females and less often observed during aggressive displays. Aggressive calls of territorial male were used primarily for expelling male‐intruders. Rutting male vocalizations likely promote synchronization of breeding cycles for most females in the population.
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S0376-6357(14)00130-2 http://dx.doi.org/doi:10.1016/j.beproc.2014.05.009 BEPROC 2839
To appear in:
Behavioural Processes
Received date: Revised date: Accepted date:
4-1-2014 13-4-2014 31-5-2014
Please cite this article as: Blank, D.A., Ruckstuhl, K., Yang, W.,ROARING FUNCTION IN MALE GOITERED GAZELLES., Behavioural Processes (2014), http://dx.doi.org/10.1016/j.beproc.2014.05.009 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
1
ROARING FUNCTION IN MALE GOITERED GAZELLES. D.A. Blank a,b*, K. Ruckstuhl c, 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;
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Institute of Zoology, Kazakh Academy of Sciences, Alma-Ata, Kazakhstan. Department of Biological Sciences, University Calgary, Canada.
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*Corresponding author: David Blank – [email protected], Fax +86-991-7885320
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Abstract.
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very close distance. The goitered gazelle is a rare exception to this rule, and during the rutting
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period territorial males of this species are among the noisiest antelopes. Rutting vocalization is
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such an essential part the rutting behaviour in goitered gazelle that adult males have a hypertrophic
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larynx, the muscle tissues of which increase considerably in size during the rut. We were
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interested in the frequency and variance with which male goitered gazelles emit their calls
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depending on an animal’s age, reproductive status and time of the year in order to understand the
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main function of the rutting vocalizations. We found that roaring was mostly related to courting
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displays, while vocalizations during aggressive displays were less frequent in male-male
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interactions. Acoustic signals likely enhance courtship displays and also may aid in accelerating
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female ovulation, promoting synchronization of breeding cycles during the mating and birthing
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periods, which last only several days for most of the females in our population. We discuss the
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Most of the vocalizations of Antilopinae males are soft and usually only heard from a
potential benefits of such behaviours and compare it to other species living in similarly extreme
environments.
Key words: Aggressive displays, courting behaviour, goitered gazelle, male vocalization, rutting roaring.
INTRODUCTION
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and acoustic signals are particularly widespread in communication and used by individuals of all
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ages and sexes in different social contexts (Vannoni et al., 2005). Bovids represent an interesting
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group, which show a wide variations of vocal signals and examples of convergent evolution with
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cervids and humans (Fitch and Reby, 2001; Frey et al., 2007, 2008 a,b). Adult males of many
In ungulates, as in other mammals, communication plays a crucial role in social interactions,
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ungulate species are known to give distinct loud calls just during the rutting season (Minami and
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Kawamichi, 1992). Most of these vocalizations even during the rut uttered by Antilopinae males,
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for example, are rather soft and usually can be heard only from a very close distance from animals
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in captivity (Walther et al., 1983). These species vocalize mainly through the nose, and only
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optionally also through the mouth (Walther, 1984). Only a few Antilopinae species, such as the
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Mongolian gazelle (Procapra gutturosa – Frey et al., 2008b), and goitered gazelle (Gazella
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subgutturosa – Blank, 1998), are exceptions from this rule in that territorial males of these species
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are the noisiest of all Antilopinae species. Rutting adult males of Mongolian and goitered gazelles
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vocalize through widely opened mouths, while the females of these species produce both oral and
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nasal calls (Frey et al., 2008 a,b).
It is well known that gazelles use their vocalizations both for courting and aggressive
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displays (Walther et al., 1983), but there are variations in use among species. For example, Grant’s
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gazelle males (Nanger granti) rarely roar, but when they do, it is always connected to courting
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females, while in Thomson’s gazelles (Eudorcas thomsonii) rutting calls are most commonly heard
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during aggressive displays and more rarely while courting females (Walther et al., 1983). Roaring
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during the rut is a very typical phenomenon in goitered gazelles and vocalizations are an integral
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part of courtship and aggressive displays by territorial males (Blank, 1998). Goitered gazelle
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males are also distinctive in that they have an anatomical adaptation for uttering these relatively
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“real” rut in November-December and a “false” rut in April-May, do many adult males establish
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individual territories and increase the frequency of their courting and aggressive displays by many
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times. Goitered gazelles mate only during the “real” rut, and females give birth only once a year,
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in May (Blank and Fedosenko, 1983; Blank, 1998). The second “false” rut in goitered gazelles has
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been hypothesized to be an ancestral trait from warmer geological periods, when this species had
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the environmental conditions and ability to breed twice a year (Sludskiy 1956; Tsapluk 1972),
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loud rutting calls, namely, an enlarged and descended larynx, the muscle tissues of which considerably increase in size during the rut (Blank, 1998; Frey et al., 2011). The goitered gazelle is a medium-sized ungulate, which originally was spread widely all over
of Middle and Central Asia, Iran, Afghanistan, Turkey, and the Caucasus (Kingswood and Blank, 1996). This species typically lives in small groups of 2-3 individuals (Blank et al., 2012b). In male goitered gazelles, courting and aggressive displays are seen all year round, but only during the
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though this so called ancestral behaviour certainly needs further investigations. In spite of the fact that the morphology of the vocal apparatus and acoustical features of
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goitered gazelle vocalizations have been described well in recent reports (Efremova et al., 2011
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a,b; Frey et al., 2011; Volodin et al., 2011), the behavioural aspects of their vocalizations are still
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poorly understood. This paper describes the behavioural components the rutting vocalizations and
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quantifies the characteristics of goitered gazelle roaring depending on season, social status, and the
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age of displaying males. We suggest several hypotheses for the occurrence of rut roaring in
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goitered gazelles.
In polygynous cervids and bovids, vocal features were found to be linked to the physical
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quality of rutting males and to play a decisive role in the reproductive success of the caller (Reby
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and McComb, 2003; Reby et al., 2005; Charlton et al., 2007, 2008). Since in many Antilopinae
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species adult males use their vocalizations most often while courting females or expelling rivals
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from their territories (Walther et al., 1983), we expected to find significant seasonal fluctuations in
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male roaring rates, with adult males vocalizing most often during the rutting period in
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November-December, less often during the “false” rut in April-May, and least often during the rest
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of the year. In addition, due to a considerable increase in the size of the larynx muscle tissues
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during the rut (Frey et al., 2011), we expected that vocalizations would be louder and better heard
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during the rut than outside the rut.
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In other words, the frequency of vocalizations would increase with an increase in the number of
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potential individuals to whom the adult male would display either courting or aggressive
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behaviours.
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It also was found that the rutting vocalizations of adult male goitered gazelle have low
amplitude and consequently a poor propagation rate through the environment; therefore adult males must approach a recipient to perform their courting or aggressive displays at close range (Frey et al., 2011). So, we predicted that adult males would produce calls more often in the presence of other males or females than when they were alone, and that vocalization frequency would grow with the size of the female or male groups that intruded into the adult male’s territory.
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Territorial males are the most active individuals during the rutting period (Walther et al.,
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1983), so we predicted that territorial males would vocalize more often than sub-adult males and
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non-territorial males in groups, especially during the rut in November-December.
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The goitered gazelles’ retractable larynx and vocal tract have evolved in such a way that
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during the rut, adult males, as compared to other ruminant species, can emit rutting calls even
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while running at a full gallop (Frey et al., 2011). We therefore predicted that adult males would run
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mainly at a high (galloping) speed during their vocalized courting or aggressive displays, because
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of their intensified arousal and rutting displays, while outside the rut they would vocalize at
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usually lower speeds.
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MATERIAL AND METHODS
The term “roaring” is commonly used for vocalizations of large animals, such as lions
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(Panthera leo), leopards (P. pardus), elephant seals (Mirounga angustirostris), red deer and musk
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oxen (Ovibos moschatus), but we have used this term for the goitered gazelle’s vocalizations based
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on the more general definition of Weissengruber et al. (2002), who suggested that a roar is
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specified as a call type with a low fundamental frequency and lowered formant frequencies.
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Observations for our study were conducted in the Ili depression (southeastern Kazakhstan) during a 6-year period from 1981 to 1986. We mostly made focal animal observations,
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concentrating on only one randomly selected group of gazelles at a time (usually the closest), and
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continuously sampled separate group members for up to 9 hours while recording the courting and
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aggressive displays both accompanied by calls and without calls. With aggressive displays, every
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occurred. In most cases, gazelles were observed from distances of 50-100 m, with observation
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posts usually established on elevations from where we could see 30-50 gazelles at the same time.
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During the rut, the size of a male’s territory was 50-80 ha (Blank, 1985), and we typically could
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observe 5-6 individual territories simultaneously from our elevated observation point. And since
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females were distributed unevenly among territories (Blank, 1998), we chose a male closest to our
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observation point that had at least one female in his territory. To avoid pseudo-replication, we
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agonistic interaction between two rivals was calculated as a single incident, and the same for each vocalized aggressive display. Only one rival (territorial male) used his roaring against the male-intruder, which retreated usually without vocalization, each of such interaction also was calculated as a single case. Vocalizations were rarely observed during conflicts between territorial
males.
All behaviours were recorded in the order in which they occurred and each time they
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changed our observation point every day and tried to observe in different parts of the study area
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(over ～4600 km2), establishing 20 different observation sites. The total size of the study
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population in the Ili depression was estimated to range from 1.5 thousand in 1981 up to 5 thousand
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in 1986 (Blank, 1990). For focal observations we used binoculars (magnification 8x) and a
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telescope (magnification 30x- 60x). We conducted 181 hours of focal observations in April, 470
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hours in May, 374 hours in June, 173 hours in July, 224 hours in November and 148 hours in
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December over the 6-year period.
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Goitered gazelles vocalized while courting females and chasing other males when performing aggressive displays, so we made a distinction between courting and aggressive vocalizations.
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Courting territorial males demonstrated their roaring mostly while demonstrating the low-stretch
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and high-stretch postures; the description (ethogram) of these displays is presented in Table 1.
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Among aggressive displays, adult males vocalized mostly while in dominance and threat postures,
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and rarely during battles (horn-pressing) (Table 1). Frey et al. (2011), using auditory and video
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recording techniques, found that rutting calls of adult male goitered gazelles consist of three types
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of sounds: roars, growls and grunts. Since we were using only our ears and eyes, we did not
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distinguish these types of calls, and in this paper called rutting vocalization “roaring”, keeping in
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mind that these vocalizations consisted in fact of the three types of calls mentioned above. In
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addition, Frey et al. (2011) pointed out that male goitered gazelles produced their rutting
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January, February, March, and September. For our investigations into differences in goitered
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gazelle vocalized and non-vocalized courting and aggressive displays based on sex, age, season,
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and territorial status, we used two main indices: the absolute frequency of vocalization during
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courting or aggressive displays (number of behavioural acts per hour of observation) and relative
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frequency (proportion of observations with vocalizations out of the total number of all
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observations). The first index just stated whether the frequency of vocalized displays increased or
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vocalizations only through widely opened mouths, while our observations showed that during slow gaits (walking, trotting), the male’s nostrils also may participate in the producing rutting sounds (Table 1).
We investigated the frequency changes of vocalizations according to the breeding cycle and
distinguished three biological seasons for the goitered gazelle: rutting season (mid-November to mid-December), “false” rut (April-May) and outside of the rut (June-August); data were absent for
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decreased over months, while the second index gave an idea of whether the proportion of
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vocalized versus non-vocalized displays increased. It was possible to individually identify separate territorial males, since they stayed in the
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same area for several weeks. Most other individuals, though, were not individually recognizable,
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although we were able to differentiate gazelles according to sex (horned males and hornless
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females) and age (adult and sub-adult males and adult and sub-adult females). The age of all
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goitered gazelles observed was differentiated based on the descriptions of Zhevnerov (1984): adult
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males (older than 2 years old – horns 1.5 times longer than ears and absence of the black spot on
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the front of the muzzle), adult females (older than 2 years old – hornless and absence of black spot
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on the front of the muzzle), sub-adult males (1-2 years old – horns are equal or shorter than ears
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and presence of a black spot on the muzzle front), sub-adult females (1-2 years old – hornless and
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black spot on the muzzle front), young (up to 1 year old, body size 2-3 times smaller than in adult
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gazelles and a black spot on the muzzle front).
We used One-Way ANOVA followed by LSD Post-Hoc test and a General Linear Model
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(GLM, Type 3 Sum of Squares) to test for the effect of month and age on absolute and relative
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frequencies of vocalization acts. These data were normally distributed according to Shapiro-Wilk
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and Kolmogorov-Smirnov tests. We used Log-linear models to compare proportions of separate
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behavioural acts and Spearman’s Correlation for a possible correlation between frequency of
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increasing in occurrence 6.1 times in April, 36.4 times in November and 37.5 times in December
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compared to July (Post-Hoc LSD test, P < 0.05, 0.002 and 0.001, respectively) (Fig. 1). The
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frequency of aggressive patterns also increased during these months, but overall changes were
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insignificant (One-Way ANOVA, F = 1.974, df1 = 7, df2 = 83, P = 0.068). Furthermore, the roaring
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was soft and difficult to detect in most months at distances more than 50 m and only during the
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rutting period in November and December were these sounds relatively loud and clearly heard
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vocalized displays and group size. All statistical analyses were conducted using SPSS 17.0 software package.
RESULTS
We found that adult male goitered gazelles’ vocalized courting patterns were varied and
fluctuated significantly over months (One-Way ANOVA, F = 12.242, df1 = 7, df2 = 141, P < 0.001),
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from distances up to 300-400 m. The relative frequency of courting displays also fluctuated
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significantly over months (One-Way ANOVA, F = 3.514, df1 = 7, df2 = 132, P = 0.002), but in fact
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only in November was this value significantly larger compared to other months (Post-Hoc LSD
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test, P < 0.01), and insignificant at all other times (P > 0.05). The relative frequency of aggressive
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displays fluctuated insignificantly (One-Way ANOVA, F = 0.133, df1 = 6, df2 = 74, P > 0.05).
In adult males, the yearly average frequency of vocalized courting displays exceeded 2.4
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times the aggressive patterns with vocalizations (GLM test, F = 8.869, df = 1, P = 0.003), and only
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in July, were aggressive displays with calls observed more often than courting patterns (1.8 times)
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(GLM test, F = 9.039, df = 7, P < 0.001). The relative frequency showed the same trend, with
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courting displays’ exceeding 1.2 times the aggressive patterns (GLM test, F = 5.248, df = 1, P =
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0.023). In addition, our analysis showed that maximal frequency of vocalization by an adult male
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was demonstrated when he stayed together with one female (26%, n = 903), while he was roaring
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slightly less often with two or three females (21-22%) (Log-linear model test, Z = -2.111-2.574,
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P = 0.035 and 0.01), and much less when he had a larger female group or when alone (1-7%)
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(Z = -3.631-5.577, P < 0.001). However, the frequency of vocalizing of males in female groups of
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different sizes was closely correlated with the proportion of available groups (Spearman’s
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Correlation = 0.982, N = 203, P < 0.001). Furthermore, territorial single males vocalized
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significantly more often while courting females, than did non-territorial males in groups
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from the rut (Z = -4.337-5.002, P < 0.001), and adult males vocalized more often in male groups
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(up to 11 individuals) than when they had only one rival. However, frequency of vocalizing males
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in groups of different size was also closely correlated with the proportion of available groups
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(Spearman’s Correlation = 0.999, N = 185, P < 0.001).
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(Log-linear model test, Z = 4.494, P < 0.001), with the maximum difference in November and December (Z = 7.812 and 4.219, P < 0.001), a smaller difference in April (Z = 3.055, P = 0.002), and no difference between single and group males in other months (P > 0.05). During the aggressive displays in the rut (November-December), adult males vocalized most often when they had one rival, and considerably less often when they chased male groups of 2 or more rivals (Z = -4.293, P < 0.001). Outside the rut, the distribution of vocalization frequency was different
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Sub-adult males started to show vocalized courting displays in April, with some increase in
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frequency during May-July (One-Way ANOVA, F = 7.382, df1 = 3, df2 = 19, P = 0.002); in other
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months such behaviour was not observed. The relative frequency fluctuated insignificantly during
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April-July (One-Way ANOVA, F = 1.093, df1 = 3, df2 = 15, P > 0.05). The average frequency of
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calls during aggressive displays in sub-adult males was insignificantly higher than their calls
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during courting displays (GLM test, F = 1.328, df =1, P > 0.05). In April, vocalized courting
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displays in sub-adult males were observed much more rarely (3.4%, n = 58) compared to adult
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males. Further, this proportion increased from 15.3% (n = 98) in May and up to 40.9% (n = 44) in
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June and again decreased by as much as 12.5% (n = 8) in July. The proportion of vocalized
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aggressive displays in sub-adult males was even lower than in adult males and fluctuated between
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3-4% (n = 59) in April-May and 10% (n = 10) in June.
In any month, adult males produced calls usually when courting females, and especially
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frequently in November-December (98% cases, n = 911) and April-May (94%). They rarely
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vocalized before starting a chase (Log-linear model test, Z = 9.325, P < 0.001), though in July they
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called before chasing more frequently (up to 30% cases). Adult males commonly vocalized in the
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low-stretch or high-stretch postures, especially often in November-December (99.6%, n = 913),
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and even outside the rut this proportion only decreased to 88%; rarely did adult males vocalize in a
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neutral posture (Z = - 6.250, P < 0.001). Vocalizations were performed most often with an elevated
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tail (in a horizontal position), especially in November-December (89-96%, n = 859) and
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April-May (95-98%) (Log-linear model test, Z = 6.194, P < 0.001). More rarely they vocalized
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(Z = -7.023, P < 0.001) (Fig. 2). And November did not differ from December (Z = 1.556,
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P > 0.05). In contrast, outside the rut adult males produced calls mostly while moving at a slow
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pace (walking or trotting – 30-55%), and in July-August even in a standing position (11-38%)
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(Log-linear model test, Z = -5.807-7.922, P < 0.001). With aggressive behaviour, territorial males
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typically vocalized while driving intruders-bachelors (non-territorial males) out of their territories,
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and rarely used their calls during conflicts with other territorial males (Log-linear model test, Z =
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with the tail in a vertical or down position, but increasing the proportion of the last pattern by up to 20% outside the rut (August). While calling, the auricles were usually pressed backward toward the neck (70-99%, n = 753) and more rarely in a neutral position (Z = 9.242-11.781, P < 0.001). In November-December, roaring adult males chased females most often while galloping
(33-41%, n = 697) (Log-linear model test, Z = 2.458, P = 0.014), less frequently when walking (31-39%) or trotting (24-27%), and least often while standing (1-1.5%) and/or jerking (1-2.6%)
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2.638, P = 0.008). All year round, roaring adult males mostly walked (up to 75%) when chasing of
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other males, while trotting and galloping were observed considerably less often (15-30% and
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6-28%, respectively) than walking (Z = -3.307-4.315, P < 0.002). However during the rut, the
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territorial males chased their rivals more often using faster gaits (trot or gallop), resulting in a
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decrease in the portion of walking pursuits (45-50%, n = 601); conversely, walking pursuits
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increased outside the rut (53-75%, n = 330) (Z = -3.307-7.490, P < 0.001). Calls made by adult
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males while standing and/or jerking occurred least often (1-10%).
When courting females, territorial males produced calls periodically, while constant roaring
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during the entire chase sequence was rarely observed. During the most intensive courting period
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in November, however, the portion of constant roaring increased by up to 28% (Chi squire of fit
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test, Chi squire = 106.681, df = 1, P < 0.001). Most often during aggressive chases in the rut,
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territorial bucks used single, infrequent, and relatively long-term (2-3s) calls while expelling
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non-territorial males from their territories (46-54%, n = 74), as well as when following passing
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bachelor males (45-51%, n = 72) (Log-linear model test, Z = - 0.439, P > 0.05); outside the rut
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adult males followed each other mostly with bouts of short (less than 1s) and frequently repeated
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calls (Z = - 4.536, P < 0.001). There was no difference in the proportion of these calls between
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November and December (Z = -1.628, P > 0.05), but these two months differed significantly from
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other months (Z = -4.055-4.581, P < 0.001).
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and relative frequencies of vocalization during courtship significantly increased during the real rut.
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Hence, adult males roared more frequently per hour of observation not only because of an increase
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in the total number of courting displays during the rut, but also because of an increase in the
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proportion of vocalized versus non-vocalized displays. In contrast, during aggressive displays,
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adult males showed insignificant increases in vocalized displays compared to the non-rutting
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period. In addition, goitered gazelles vocalized considerably more often during courting displays
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DISCUSSION
Adult males showed considerable seasonal fluctuations in their vocalization; roaring during
their courtship and aggressive displays were observed all year round, with some increasing frequency during the “false” rut in April-May and maximum frequency during the real rutting period in November and December, compared to other months of the year. And both the absolute
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than aggressive demonstrations, and only in July, when testicle physiological activity was minimal
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and most adult males gathered in large groups (Tsapluk, 1972; Blank et al., 2012a), did the
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vocalized aggressive interactions exceed the courting displays. Thus, roaring in goitered gazelles
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is more related to courting displays than to aggressive patterns, with males accompanying up to
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half of their courting displays by roaring (Blank, 1998).
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The same phenomenon was found in red deer (Cervus elaphus), where the stag’s roar is
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speeding up ovulation, which improves mating success with frequent calling (Fedosenko, 1980;
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McComb, 1987, 1991; Charlton et al., 2007). Similarly in fallow bucks (Dama dama) time
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invested in vocal display is linked to mating success (McElligott et al., 1999). Among Antilopinae
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species, Grant’s gazelles only rarely emit relatively loud roars, except when courting females
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(Walther et al., 1983). It is possible that territorial male rutting roars in goitered gazelles serve the
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same function as in deer, namely to promote ovulation.
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Goitered gazelle rutting roars were loud enough to be clearly heard from a distance of several
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hundred meters, while outside the rut adult males’ calls were difficult to hear from a distance of
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more than 50 m. Furthermore, during the rut males produced long-term, usually single or
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infrequent calls, while outside of the rut adult males followed each other mostly with bouts of
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short and frequently repeated calls, especially during aggressive displays.
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male goitered gazelle is much larger and rests lower in the neck (Frey et al., 2011; Volodin et al.,
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2011). An increase in larynx size and the vocal tract elongation leads to the acoustic effect of
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producing calls with lower frequency and resonance, which are unexpected low for an animal the
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size of the goitered gazelles (Frey et al., 2011). The same phenomenon is found in three
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mammalian taxa: among bovids, which apart from goitered gazelles, is also present in Mongolian
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gazelle; among cervids, such as fallow deer and red deer; and in humans (Bigalke, 1972; Walther,
296 297 298 299 300
allow increasing reproductive success through mate competition or mate choice (Espmark et al., 2000). It is likely that vocalizations in goitered gazelle are a result of the same processes, and rutting calls in adult males are such an important and essential component (Blank, 1998), that males have a large and very prominent larynx or “Adam’s apple” (Kingswood and Blank, 1996) with muscle tissue that noticeably increases in size (up to 50%) during the rut (Frey et al., 2011). Compared to domestic bovids of similar size, and even females of conspecifics, the larynx of the
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1981; Fitch and Reby, 2001; McElligott et al., 2006; Frey et al., 2008 a,b). As predicted, adult goitered gazelle males showed their vocalization most often when they
310
had females inside their territories or with rivals for aggressive displays, while they vocalized
311
rarely when they were alone. The significantly enlarged larynx of goitered gazelle males is
312
adapted for producing low-amplitude close-range calls (Frey et al., 2011). Therefore having
313
relatively large-sized individual territories, goitered gazelle usually started to call after
314
approaching females or rivals and rarely vocalized over long distances in response to activities of
315
other males in neighboring territories (Blank 1998). The same behaviour also was observed in
316
Mongolian gazelles (Frey et al., 2011).
Contrary to our predictions, the calling rate didn’t increase with group size, and vocalizations
318
of adult males were noted frequently when courting of small female groups (2-4 individuals),
319
while cases of vocalized courting displays for larger groups were observed significantly less often.
320
A similar behaviour was observed for aggressive displays during the rut, when adult males
321
produced calls most often for one rival (single bachelors), and considerably less often, when
322
chasing male groups of any size. In contrast, outside the rut, males addressed their vocalized
323
aggressive displays more often to male groups than to a single male. Our analyses showed,
324
however, that this was not a result of males’ preference to call for groups of a certain size, but was
325
a consequence of the goitered gazelles’ social structure, where small female groups and single
326
331 332
adult males or bachelors, which may gather into groups, sometimes also court females in mixed
333
groups, or when a bachelor group occasionally meets a herd of females. In this case, several males
334
will run after the same female, which then usually results in fighting. A territorial male is regularly
335
chasing male groups, attempting to separate the non-territorial males away from his females
336
(Walther et al., 1983). Since territorial males are constantly defending their territory from rivals,
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they have a high rate of aggressive displays, while bachelors without territories only occasionally
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males were more common during the rut than outside of it (Blank et al., 2012b). Territorial males vocalized during courting and aggressive displays significantly more often
than bachelor bucks in groups and sub-adult males. Territorial males, and territoriality as a whole, have the greatest impact on reproductive success, since in many Antilopinae species, including goitered gazelles, reproduction is almost exclusively done by territorial males (Walther et al., 1983). When females arrive in their territories, territorial males are busy courting. Non-territorial
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have conflicts within their groups. We found the frequency of vocalized courting and aggressive
339
displays to be closely correlated with the total frequency of all displays, including non-vocalized
340
ones; therefore territorial males vocalized significantly more often than bachelors in groups.
341
During the “false” rut (April-May), only some adult males became territorial, while the majority
342
stayed in groups (Blank, 1998); therefore the behavioural difference between single (territorial)
343
males and bachelors in groups was less pronounced. During the non-rut period, territoriality in
344
males was absent and the proportion of single males was at a minimum (Blank et al., 2012a), so
345
differences in the frequency of vocalization between single males and group males were
346
negligible.
The vocalizations of young males started to differentiate from females’ as early as the second
348
week of life (Efremova et al., 2011a). Young males become interested in females by the age of 6
349
months, but just follow the females and sniff their hindquarters, demonstrating only a neutral
350
posture (Blank, 1998). Vocalized courting and aggressive displays of sub-adult males started in
351
April at the age of one year. Later (May-July), the frequency of vocalized display increased, while
352
during the real rut in November-December, sub-adult males did not perform vocalized courting or
353
aggressive displays at all. Adult males had a sharp decrease in activity in June-July, starting at the
354
end of the “false” rut in May, while proportion of vocalized displays of sub-adults increased
355
during the same period compared to adult males. This behavior of sub-adult males corresponds to
356
361 362
while adult males vocalized courting displays significantly more often than aggressive displays.
357 358 359 360
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the cyclical physiology of their testicle development, which begins to function for the first time in April, when the “false” rut starts in adult males; sub-adult testicular activity continues through May-July then demonstrates a distinctive waning in November. In contrast, the activity of adult male testicles is at its maximum during the rut in November-December, less during the “false” rut in April-May and fades during non-rutting periods (Tsapluk, 1972). It is interesting to note that sub-adult males used calls with the same frequency during both courting and aggressive displays,
363
As observed in the non-rutting period, adult males following females preferred to make calls
364
while moving at a slow gaits (walking and trotting). During the rut, however, roaring territorial
365
males chased females most often when galloping – a phenomenon made possible by the
366
anatomical construction of the goitered gazelle’s vocal apparatus (Frey et al., 2011). The point is
367
that during the rutting period females don’t remain continually within an individual male’s
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territory, but instead just crosses through it on their way to their daytime resting sites (Blank,
369
1998). The territorial male, then, tries to keep the female group within his territory as long as
370
possible, herding and courting, usually at a gallop, one female after the other in an attempt to drive
371
them into the center of his territory (Walther et al. 1983). While engaged in this chasing, males
372
utter their roars very often (Blank, 1998). In contrast, territorial males used their vocalized
373
aggressive displays almost exclusively against bachelors-intruders while expelling them from their
374
territories, while they did not use their roaring for solving territorial conflicts with their neighbors.
375
They used their calls without physical conflict, because the male-intruders retreated without
376
resistance and without returning the calls - it was always a one-sided display. Roaring territorial
377
males used their calls to demonstrate their territorial status to bachelors (Walther, 1981), but they
378
did not vocalize when addressing their aggressive displays to their neighbors, possibly because all
379
neighbors were familiar with each other individually. During the rut territorial males mostly
380
expelled intruders-bachelors from their territories while walking, because the males-trespassers
381
(bachelors) usually retreated by walking or more rarely trotting. Outside the rut, adult males also
382
chased each other using a rather slow gaits (mostly walking) as opposed to a faster ones
383
(galloping), because aggressive interactions between members within the same male group always
384
had playful characteristics and serious conflicts were rarely observed (Blank 1992).
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Adult males produced their roaring calls while posed in erected postures (low-stretch and
391
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392
So why are goitered gazelles a rare example of mouth-produced rutting vocalizations, which are
393
louder than in most other Antilopinae species? Walther (1981) emphasized the exclusive
394
importance of rutting vocalizations for males of all territorial antelope species as an advertisement
395
of their territorial social status, both when courting females and when chasing away bachelors.
396
However, only a few have relatively loud rutting calls (Walther et al., 1983). Our explanation is
397
that most tropical antelope species have extended or perennial breeding periods, thus maintaining
386 387 388 389 390
high-stretch), when they vocalized with an extended throat region. An elevated head tends to decrease formant frequencies by a slight elongation of the length of the vocal tract and is, therefore, producing sounds of a lower tone (timbre). These stretched postures are also typical for roaring of red deer stags and Mongolian gazelles (Frey and Gebler, 2010). Many antelope species make rutting vocalizations when chasing females, though their
nasally-produced sounds are usually soft and difficult to detect at a distance (Walther et al. 1983).
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continual territoriality (Estes, 1991). In contrast, goitered gazelles have a very short, exacting
399
overall autumn rutting period (mid-November-mid-December), with most matings occurring
400
within a 4-6 day period (Blank, 1998). As a result, most females give birth within a short period
401
(just several days) at the end of May that coincides with the most favorable time of year, which is
402
very limited in the Central Asiatic deserts (Blank et al., 2012a). To achieve such a high
403
synchronization in birthing, goitered gazelles have to perform very short, vigorous rutting period
404
(one month) with intensive rutting vocalizations with low-formant calls, which are particularly
405
attractive for females, and are likely accelerating their ovulation and synchronization their
406
ovulatory cycles. Mongolian gazelles, which live in conditions comparable to those in Middle Asia
407
(Western Central Asia) with cold snowy winters and hot dry summers, have similar anatomical
408
and behavioural adaptations (Leimgruber et al., 2001; Frey et al., 2011).
Saiga antelope (Saiga tatarica) has another anatomical adaptation (trunk-like nose) for
410
producing low-formant rutting calls (nasal roaring), which are also attractive for females (Frey et
411
al., 2007); but similar to goitered and Mongolian gazelles, saiga almost constantly express their
412
vocalizations during their short and vigorous rutting period (Volodin et al., 2009) to also achieve a
413
very high synchronization in birthing (5-8 days – Bekenov et al., 1998). Other ungulates, such as
414
chiru (Pantholops hodsonii) and Tibetan gazelle (Procapra picticaudata), living in the
415
high-elevated cold deserts of the Tibetan Plateau, also use relatively loud, deep-throated roars
416
421 422
vocalizations (Pohle, 1974).
417 418 419 420
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(chiru) and grunting roars (Tibetan gazelle) frequently during their vigorous and brief rutting season to likely achieve a high synchronization in births, which last approximately a week (Schaller, 1998). The anatomical adaptations of these species still have not been investigated,
though it is known that chiru males have distinctive walnut-sized bulges of their nostrils that enlarge their nasal passages and that they use both nasal and mouth-produced calls for rutting vocalizations (Schaller, 1998). Tibetan gazelle has proboscis-like noses, which are inflated during
423
Finally, the springbok, a gazelle-like antelope, lives in a completely different environment in
424
southern Africa. It has been called both a seasonal and a non-seasonal breeder (Bigalke, 1972;
425
Smithers, 1983), but male springboks, which make relatively loud vibration rutting calls through
426
their widely opened nostrils, are also the nosiest among Antilopinae (Walther, 1981). This seems
427
contradict our supposition that relatively loud rutting vocalizations are important for
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synchronizing mating and birthing cycles in females. In fact, springboks also demonstrate
429
synchronization of oestrous and the subsequent clumping of births (Skinner et al., 1992), though
430
this species gives birth in an opportunistic, pulse-like manner (in different months) because birth
431
peaks occur at the beginning of the rainy season, the timing and duration of which is unpredictable
432
in the arid environment of southern Africa (Skinner and Louw, 1996). In addition, the spring
433
birthing season of springboks in Cape Province and Namibia varies from year to year by up to two
434
months, and a second autumn birth peak occurs only during favorable years (Estes, 1991).
All these species have different anatomical adaptations for producing rutting vocalizations,
436
but each uses its relatively loud rutting roars to intensify courting and synchronize breeding cycles.
437
This point is attributable to the fact that most females give birth during the most favorable time of
438
year for rearing young, which is an especially narrow time window in the northern Asiatic deserts,
439
including the cold deserts of the Tibetan Plateau. Furthermore, the function of rutting vocalizations
440
as an advertisement of territorial status (Walther 1981) is not inconsistent in fact to our
441
explanations. Rutting vocalizations, as a cue to territorial (high social) status, make a territorial
442
male particularly attractive to females, so the main function of rutting vocalizations in adult male
443
goitered gazelles seems to be in courting females to promote synchronization of the mating and
444
birthing cycles. Females mate exclusively with territorial males, even though non-territorial males
445
are also fertile (Skinner and Louw, 1996). This, then, defines vocalizations as an extremely
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valuable part of a male’s breeding success, while vocalized aggressive displays are less often observed and likely play a minor role in male-male interactions.
Acknowledgments
We thank the National Natural Science Foundation of China (U1303301), Chinese Academy
452
of Sciences (CAS) for granting our work (Visiting Professorships for Senior International
453
Scientists – 2011T1Z42), West Light Foundation (CAS – Y336171) for creating all conditions for
454
writing this paper. We are very grateful to the Institute of Zoology, former Academy of Sciences of
455
Kazakhstan, which has given us the possibility for investigations of goitered gazelles in their
456
natural environment during 10 years. We thank Mrs. Patricia Johnston, who did the constant help
457
in editing this manuscript.
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Bigalke, R.C., 1972. Observations on the behavior and feeding habits of the springbok, Antidorcas marsupialis. Zoologica Africana 7, 333-359.
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the Saiga antelope in Kazakhstan. Mammal Review 28(1): 1-52.
Blank, D.A., 1985. Peculiarities of social and reproductive behaviour of Gazella subgutturosa in the Ili Hollow. Zool. Zhurnal 64, 1059-1070 (in Russian with English abstract).
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Bekenov, A.B., Grachev, IU.A., and Milner-Gulland, E.J. 1998. The ecology and management of
Blank, D.A., 1990. Persian gazelle, in: Kovshar, A.F. (Ed.), Rare animals of desert regions. Nauka Kazakh SSR, Alma-Ata, pp. 56-80. (in Russian).
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Figure Legends:
Fig. 1. Frequency (act/h) fluctuations of vocalized courting (Court) and aggressive (Agress) displays of adult males over months. Totally, it was observed 204 cases of vocalized aggressive and 955 cases of vocalized courting behaviours during 1690 hours of focal observations. Fig. 2. Relative proportions of vocalized courting (A) and aggressive displays (B) in adult males at different paces over months.
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A.
Mar
May
Jun
Standing
592 B.
Jul Aug Months
Walking
Trotting
Oct
Nov
Dec
Galloping
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Proportion
590 591
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Proportion
100% 90% 80%
20% 10% 0%
Mar
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Apr
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Galloping
Dec
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Table 1. Description of the recorded courting displays and roaring (ethogram) in adult males goitered gazelle during the rut according to Walther et al. (1983) and Blank (1998). Courting postures
Description Stretching the head and neck forward horizontally with the nose pointing horizontally forward. Auricles are directed backward and usually pressed to the head in a position either parallel to the ground or slightly downward with the aperture inward. Rarely auricles lay back, pressed to each other, or held one apart of the other at a 45° angle. Tail is lifted in different degrees, up to vertical position.
High‐stretch or nose‐lift or head‐up
Head and neck are stretched forward and upward up to 45° above the horizontal level, the top of the muzzle lifted forward and upward, and auricles pressed to the head.
Roaring
Roaring consists of gruff, wheezing or hissing sounds resembling gurgling or sneezing. In producing these sounds, the male opens his mouth widely, lifts his tongue slightly and takes a deep breath, then passes air through his partly closed mouth and possibly as well as his nostrils. During a long and fast gallop, the male’s mouth is open and his tongue out. Posture: Muzzle is raised to an angle of up to 45° from a horizontal position. Auricles are directed backward and tightly pressed, more or less, to the head by apertures inside. Abruptly, the male jerks his head and whole body forward and upward, and his protruding thyroid cartilage moves down and up. During the run, the roaring is intermittent.
Aggressive postures Dominance
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Low‐stretch or neck‐stretch
Description
Rivals stand in lateral T‐position, parallel or, most commonly, reserve‐parallel orientation. The erected posture, when the neck is vertically erected upwards “proudly”. The entire body stays as high as possible due to stretching all four legs upwards. The nose is pressed to a neck and horns are directed forward and the head is turned in a more or less pronounced fashion away from opponent. Tail is uplifted and in waving movements from one side to another; ears are apart horizontally and directed sidewise by tops, and their holes are directed forward or downward. All walking movements are unusually slow.
Ac ce p
597 598 599
Threat
Horns are directed forward. Ears are directed forward‐sideward; tail is normal position.
Horn‐pressing
The rivals approach each other with lowered heads to the ground without preliminary displays of threat and lean the frontal surfaces of their horns against each other. They fight while standing on all four legs with the forelegs widely spread, and hindlegs in normal position or relatively close together. Each of them tries to press the horns of the opponent to the ground and move him back. Then everyone hits the revival’s head with maximum power and presses the head to the ground and back again,
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marking jerks. The horns almost invariably interlock (horn of one between horns of another). This fight can transfer to fight‐circling, when rivals do circles with locked horns. In this situation, they pivot with their hindquarters while keeping their heads in the circle center. During fighting, the ears are directed sidewise by top horizontally or backward sometimes and tail is pressed. This fight is common for non‐territorial males.
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Ac ce p
600 601
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Highlights The quantitative characteristics of vocalized male displays in goitered gazelle have never been considered before now. Male vocalizations were mostly related to courting females and less often observed during aggressive displays. Aggressive calls of territorial male were used primarily for expelling male‐intruders. Rutting male vocalizations likely promote synchronization of breeding cycles for most females in the population.
Ac ce p
601 602 603 604 605 606 607 608 609
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