Free‐Ranging Red Deer Hinds Show Greater Attentiveness to Roars with Formant Frequencies Typical of Young Males

Acoustic cues present in the reproductive calls of many animal species potentially encode important information about the caller. Here, we test the response of a free‐ranging population of peri‐oestrus red deer hinds to variation in a specific acoustic cue to body size in the male roar, the formant frequencies. Our results revealed: (1) that hinds showed greater overall attention (judged by longer looking responses and lower response latencies) to roars simulating males of sub‐adult body size than to those simulating a large adult male and (2) that hinds without dependent offspring had greater looking responses to male roars and lower response latencies than hinds with dependent offspring to roars simulating sub‐adult males. These findings indicate that free‐ranging red deer hinds may use formants as acoustic cues to gauge the body size and maturity of males in their natural environment, possibly to facilitate earlier detection and avoidance of young stags that are known to harass them.     

Female red deer prefer the roars of larger males

Surprisingly little is known about the role of acoustic cues in mammal female mate choice. Here, we examine the response of female red deer (Cervus elaphus) to male roars in which an acoustic cue to body size, the formants, has been re-scaled to simulate different size callers. Our results show that oestrous red deer hinds prefer roars simulating larger callers and constitute the first evidence that female mammals use an acoustic cue to body size in a mate choice context. We go on to suggest that sexual selection through female mating preferences may have provided an additional selection pressure along with male-male competition for broadcasting size-related information in red deer and other mammals.     

The induction of male sexual behavior in red deer (Cervus elaphus) by the administration of testosterone to hinds and estradiol-17β to stags

One-gram implants of testosterone were placed subcutaneously in two adult intact and one castrated red deer hinds, and 100-mg implants of estradiol-17β were given to three castrated and two intact red deer stags. Their sexual behavior was then observed in the wild and in captivity for up to 3 years. Testosterone initially produced prolonged and intense estrous behavior in the hinds; this gradually gave way to behavior normally shown only by rutting stags, such as flehmen, herding threats, and roaring. Testosterone-implanted hinds rose in the dominance hierarchy as measured by competition for food. Pregnancy, or the administration of progestagens, suppressed most of this testosterone-induced behavior. Testosterone also induced development of male secondary sexual characteristics such as formation of small antler pedicles (but not antlers), hypertrophy of the clitoris and neck musculature, and development of a neck mane and male rutting odor. Estradiol-17β mimicked the behavioral effects of testosterone when given to castrated stags, stimulating all components of rutting behavior. In intact stags, the only effects were to abolish antler casting and stimulate roaring; normal rutting behavior continued unchanged. In contrast to the effects of testosterone, estradiol-17β did not influence the social status of either intact or castrated stags. The distinctions between the behavioral effects of androgens and estrogens are ill defined and are determined more by the prior sexual differentiation of the brain and the duration of steroid treatment, than by the nature of the steroid.     

Oestrous red deer hinds prefer male roars with higher fundamental frequencies

Across vertebrates, the observation that lower-pitched vocalizations are typically associated with larger and/or higher quality males has lead to the widespread belief that inter- and intra-sexual selection will produce male calls with low fundamental frequencies (F0). Here we investigated the response of oestrous red deer hinds to playback of re-synthesized male roars characterized by either higher than average or lower than average F0. We found that hinds prefer higher rather than lower ‘pitched’ roars, providing, to our knowledge, the first evidence of such a bias in nonhuman mammals. Our findings can be interpreted in relation to previous observations that the minimum F0 of roars is positively correlated with male reproductive success in free-ranging red deer stags, and that across Cervids the F0 of male mating calls shows extreme variability. Females showing preferences for higher-pitched roars might derive genetic benefits through more competitive male offspring. Our results emphasize the need for further investigations of female preferences in mammals in order to better understand the extreme variation of F0 values observed in male sexual calls.     

Do Red Deer Stags (Cervus elaphus) Use Roar Fundamental Frequency (F0) to Assess Rivals?

It is well established that in humans, male voices are disproportionately lower pitched than female voices, and recent studies suggest that this dimorphism in fundamental frequency (F0) results from both intrasexual (male competition) and intersexual (female mate choice) selection for lower pitched voices in men. However, comparative investigations indicate that sexual dimorphism in F0 is not universal in terrestrial mammals. In the highly polygynous and sexually dimorphic Scottish red deer Cervus elaphus scoticus, more successful males give sexually-selected calls (roars) with higher minimum F0s, suggesting that high, rather than low F0s advertise quality in this subspecies. While playback experiments demonstrated that oestrous females prefer higher pitched roars, the potential role of roar F0 in male competition remains untested. Here we examined the response of rutting red deer stags to playbacks of re-synthesized male roars with different median F0s. Our results show that stags’ responses (latencies and durations of attention, vocal and approach responses) were not affected by the F0 of the roar. This suggests that intrasexual selection is unlikely to strongly influence the evolution of roar F0 in Scottish red deer stags, and illustrates how the F0 of terrestrial mammal vocal sexual signals may be subject to different selection pressures across species. Further investigations on species characterized by different F0 profiles are needed to provide a comparative background for evolutionary interpretations of sex differences in mammalian vocalizations.     

Social dominance in farmed red deer stags

The dominance hierarchy was observed and recorded in a group of five farmed rising 5-year-old red deer stags, kept apart from hinds, from February 1982 until September 1982. The stags were observed at approximately fortnightly intervals during this period. The frequency of roaring and of serious fighting was also recorded. The identity of the dominant stag altered during the study on five occasions; a triangular dominance relationship was observed in only one observation period, and otherwise the hierarchy was linear. The roaring rate was high during the period when sexual activity would have taken place if hinds had been available, and the frequency of serious fighting was highest when one particular stag was dominant. Dominant stags showed no tendency to selectively harass subordinates in particular hierarchial positions. Although body weight was not related to rank at the beginning or end of the study, it was after 8 weeks had elapsed. Deer farmers who must keep adult stags together during the winter should maximise spacing to reduce aggression, and if necessary cull out trouble-makers.     

Great expectations: dominance,breeding success and offspring sex ratios in red deer

Differences in dominance rank among red deer (Cervus elaphus) females (hinds) on Rhum were related to their breeding success as well as to the comparative success of male and female offspring. Males (stags) born to mothers above median rank were more successful than hinds, while hinds born to subordinate mothers were more successful than stags. The ratio of male to female calves produced by dominant mothers was significantly higher than that produced by subordinates. Since dominance rank among hinds is related to their body weight as adults and to their birth weight, these results suggest that the birth sex ratio may be affected by environmental factors operating during a female's early development.     

Social Organization in an Enclosed Group of Red Deer (Cervus elaphus L.) on Rhum. I. The Dominance Hierarchy of Females and their Offspring

Studies of the dominance hierarchy in red deer have mainly concentrated on the hierarchy among stags. This study aimed to investigate in detail the dominance hierarchy of a group of hinds and their offspring and to compare it between two feeding situations, one when the deer were browsing normally in a large area, and the other when they were competing for artificially provided food in a small area.     

Behavioural factors affecting male reproductive success in red deer (Cervus elaphus)

Variation in reproductive success among adult red deer stags was related to harem size, and the duration and timing of breeding access. All three factors were affected by dominance (fighting success) during the rut. The number of hinds using a stag's rutting area and the duration of individual rutting activity also affected breeding access. Dominance rank in bachelor herds, which may affect access to hinds conceiving after the rut, was correlated with rank in the preceding but not the following rut.     

Induction of early breeding in red deer (Cervus elaphus) by melatonin

Lactating (N = 12) and non-lactating (N = 6) red deer hinds and one stag at pasture were given concentrates (500 g/head) containing melatonin (5 mg/head) daily at 16:00 h from 18 June to 16 October. The stag shed the antler velvet and started rutting 5 weeks ahead of untreated stags, and hinds had their first oestrus and ovulation of the breeding season in mid-September, 5 weeks in advance of control lactating (N = 9) and non-lactating (N = 5) hinds. Treated hinds were allowed to mate with the treated stag and control hinds ran in an adjacent paddock with an untreated stag. All hinds became pregnant during the study with all but 2 melatonin-fed hinds (1 lactating, 1 non-lactating) and 1 control hind (lactating) conceiving at the first oestrus. Melatonin-treated hinds lost slightly more live weight than did controls from June to November, but their suckled calves grew throughout at a rate similar to those of control hinds.     

Roaring Behavior of Two Syntopic Howler Species (Alouatta caraya and A. guariba clamitans): Evidence Supports the Mate Defense Hypothesis

Long-distance calls are loud vocalizations involved in within and between group communication in animals. These calls may maintain cohesion with group members or communicate the ownership of valuable resources such as territory, food, or mates to individuals from other groups. In howlers (Alouatta spp.), three nonmutually exclusive hypotheses suggest that the ultimate function of roaring (howling) behavior is to protect resources from neighboring groups. The space/food defense hypothesis maintains that roars are used to gain exclusive access to food; the mate defense hypothesis holds that roars ensure exclusive access to mates; and the infanticide avoidance hypothesis states that the roaring behavior serves to avoid male takeovers and infanticide. To test these three hypotheses, we conducted a study on black-and-gold howlers (Alouatta caraya) and brown howlers (A. guariba clamitans) living in syntopy at El Pi?alito provincial park in northeast Argentina. We recorded 12 mo of data on the roaring behavior of two groups of each species, along with data on food availability and diet. Although all four groups overlapped extensively in their use of food resources during the study period, roars occurred much more frequently during interactions between groups of the same species than between groups of different species. Roaring frequency was not higher during the lean season, when high-quality food was less abundant. Howlers did not roar more frequently at home range boundaries, nor were roaring bouts spatially associated with valuable feeding resources. Males participated in all of the roaring bouts, whereas females participated in only 29% of them. Adults did not roar more frequently when there were unweaned infants in the group, as expected if roaring behavior decreases infanticide risk. These results provide no support for the food defense or infanticide avoidance hypotheses, but support predictions derived from the mate defense hypothesis.     

Movement pattern of red deer during drive hunts in Sweden

We investigated the movement pattern of GPS-collared red deer (Cervus elaphus) during drive hunts with loose dogs. In 46 flights of hinds (N?=?9), the median flight distance was 2.5 km (range 0.4–15.0). In 28 % of the flights, the hind left its home range. Average time before returning to home range was 23 h (range 2–88). Hinds in a less forested site left their home ranges more often, fled longer distances, moved at higher speed, and returned later than hinds in a homogenous forest. Speed of movement increased with number of hunts in the less forested site. In eight flights of stags (N?=?4), the median flight distance was 5.1 km (range 2.2–13.3). The start of hunting season seemed to trigger stags’ departure to their wintering areas. Knowledge of reactions to disturbance can aid game management to choose hunting methods and dogs that cause less disturbance but may also be used to deter deer from areas where they damage crops and forest plantations.     

Predator and non-predator long-distance calls in Guereza colobus monkeys

East African Guereza colobus monkey males are known for their conspicuous roaring behaviour; a spectacle that can dominate the predawn hours of African forests. Recent research has shown that these monkeys also produce roars during daytime hours in response to predators. While roars to leopards and eagles differ in how roaring phrases are assembled into sequences, there are no obvious structural differences between predawn roars and roars to eagles. Although recipients could use daytime information to disambiguate between the two contexts, this may be a risky strategy because eagles can be active before dawn. We carried out acoustic analyses, which showed that the duration of the first roaring phrase was significantly longer in predawn roars compared to eagle roars. Furthermore, the initial call repetition rate was faster in response to eagle roars compared to predawn roars. Apart from these two differences, all other acoustic characteristics were identical between the two contexts. Although these monkeys exhibit some of the most basic vocal behaviour found in non-human primates, callers are able to provide reliable contextual information by varying the duration and assemblage of individual vocal units. Playback experiments are needed to confirm whether recipients relate these acoustic differences to different contexts.     

Selectivity of wolf predation on red deer in the Bieszczady Mountains, Poland

A pattern of wolfCanis lupus Linnaeus, 1758 predation on red deerCervus elaphus Linnaeus, 1758 was studied in Bieszczady Mountains in 1991–2002. In total 324 remains of red deer > 4 months old, killed by wolves throughout the year, were found. The sex, age and bone marrow fat content of wolf kills were compared with the same characteristics within the free living red deer population. The overall contribution of calves killed by wolves (24%) in October-May was higher than in the population (17%), and decreased from autumn to spring. Adult males were more vulnerable to wolf predation than adult females: stags constituted 62% and hinds 38% of adult red deer killed by wolves, whereas in the population, the percentages were 37 and 63%, respectively. Stags killed by wolves were younger ([`(x)] = 4.1\bar x = 4.1 years old) than hinds ([`(x)] = 8.9\bar x = 8.9 years old). Wolves killed more > 8 years old hinds and < 5 years old stags than available in the population. In wolf kills, the average fat content in femur marrow was higher among hinds (84.9%) than stags (69.3%) and calves (66.1%). Only 8% of hinds had < 70% femur marrow fat content, whereas 40% of calves and 38% of stags had marrow fat values below that level. Marrow fat content showed seasonal variation and was the lowest in March among all sex-age classes. The monthly share of stags in all kills, and hinds in hind-calf part of the sample was negatively correlated with their monthly average bone marrow fat content, and monthly share of calves was positively correlated with monthly average bone marrow fat content of adults. The segregation of social units (hind-calf and stag groups), except during the rutting season, and the low fat reserves of males from midwinter until spring contribute to the high overall incidence of calves and adult males and the relatively low incidence of adult females among wolf kills.     

Variability of Female Responses to Conspecific vs. Heterospecific Male Mating Calls in Polygynous Deer: An Open Door to Hybridization?

Males of all polygynous deer species (Cervinae) give conspicuous calls during the reproductive season. The extreme interspecific diversity that characterizes these vocalizations suggests that they play a strong role in species discrimination. However, interbreeding between several species of Cervinae indicates permeable interspecific reproductive barriers. This study examines the contribution of vocal behavior to female species discrimination and mating preferences in two closely related polygynous deer species known to hybridize in the wild after introductions. Specifically, we investigate the reaction of estrous female red deer (Cervus elaphus) to playbacks of red deer vs. sika deer (Cervus nippon) male mating calls, with the prediction that females will prefer conspecific calls. While on average female red deer preferred male red deer roars, two out of twenty females spent more time in close proximity to the speaker broadcasting male sika deer moans. We suggest that this absence of strict vocal preference for species-specific mating calls may contribute to the permeability of pre-zygotic reproductive barriers observed between these species. Our results also highlight the importance of examining inter-individual variation when studying the role of female preferences in species discrimination and intraspecific mate selection.     

Artificial insemination following observational versus electronic methods of estrus detection in red deer hinds (Cervus elephus)

The objectives were to determine the efficacy of the HeatWatch (HW) electronic estrus detection system for monitoring behavioral estrus (including duration and intensity) in red deer hinds and to evaluate pregnancy rate to AI after detected estrus. Red deer hinds (Cervus elephus; n = 50) were allocated into two treatment groups: AI following synchronization (CIDR/PMSG) and observed estrus (induced estrus group: IE; n = 25) or AI following the detection of natural estrus (NE; n = 25) without hormonal treatment. Hinds were fitted with two HeatWatch (HW) electronic estrus detection transmitters, one above the tail (bottom) and one between the tuber coxae of the pelvic girdle (top), and visual observations for mounting activity began with the aid of young sterile red deer stags (18 months old) fitted with marking harnesses. Hinds in both groups were inseminated (10-12h after observed estrus) with frozen-thawed red deer semen using a transvaginal/cervical AI approach. Following a 26-day period of AI, hinds were placed with a mature fertile stag for an additional 30-day natural breeding period. Pregnancy diagnosis was performed 57 and 86 days after the start of AI. While the hinds were housed with the young stags, 82% were detected in estrus by visual appraisal of stag crayon marks, but only 32% of these were detected by HW. In contrast, in the hinds housed with the mature stag, 93% detected in estrus by crayon marks were also detected by HW. The top HW transmitter consistently recorded more mounts (P < 0.05) than the bottom transmitter. The pregnancy rate was numerically better in IE versus NE hinds (42% versus 29%, P > 0.10). In summary, there were no differences (P > 0.10) in the intensity (number) or duration of mounts (detected by HW) during estrus in IE versus NE hinds, and HW was most effective in detecting estrus in the presence of a heavier, mature stag versus a younger stag. When used in combination with transvaginal AI, an overall first-service pregnancy rate of 36.6% was achieved with AI of frozen-thawed semen in red deer hinds following detected estrus.     

"占群"还是"挑战"?不同时间限制条件下麋鹿个体的交配计策

在麋鹿的发情交配季节 ,雄性麋鹿可区分为 3种类型 :“群主”、“挑战者”和“单身汉”。“群主”是一头圈占并控制雌鹿活动的优势雄性。“挑战者”不占有雌性繁殖群 ,但在发情场附近地点展示炫耀。当雌性繁殖群的雌鹿外出采食靠近“挑战者”的展示炫耀地点时 ,“挑战者”会积极地寻求机会与之交配。“单身汉”在繁殖季节不表现发情行为。他们像非繁殖季节一样采食 ,采食后蹲在水塘中休息。我们对何种因素决定麋鹿个体的发情交配计策感兴趣。 1996至 1998年夏天 ,我们在北京麋鹿苑观察麋鹿发情交配行为以分析导致这些行为差异的原因。结果发现 ,“群主”、“挑战者”和“单身汉”用于维持生命的时间预算与用于发情的时间预算成反比 ,并且 ,“群主”、“挑战者”和“单身汉”用于维持生命的时间预算与用于发情的时间预算差异显著。“群主”的绝大部分时间用于发情占群 ,而用于采食、饮水的时间很少 ,所以 ,“群主”在发情期间基本上处于禁食状态 ,靠消耗体内脂肪维持生命。“单身汉”则相反 ,绝大部分时间用于采食、休息和反刍 ,基本上没有发情行为。“挑战者”在发情行为与维持生命行为之间的时间则居于“群主”与“单身汉”之间。交配次数是偏态分布的 ,与雄性发情时间呈正比。“群主”的交配概率最高     

Red deer stags use formants as assessment cues during intrasexual agonistic interactions

While vocal tract resonances or formants are key acoustic parameters that define differences between phonemes in human speech, little is known about their function in animal communication. Here, we used playback experiments to present red deer stags with re-synthesized vocalizations in which formant frequencies were systematically altered to simulate callers of different body sizes. In response to stimuli where lower formants indicated callers with longer vocal tracts, stags were more attentive, replied with more roars and extended their vocal tracts further in these replies. Our results indicate that mammals other than humans use formants in vital vocal exchanges and can adjust their own formant frequencies in relation to those that they hear.     

Female-biased dispersal under conditions of low male mating competition in a polygynous mammal

Sex-biased dispersal is a common phenomenon in birds and mammals. Competition for mates has been argued to be an important selective pressure favouring dispersal. Sexual differences in the level of intrasexual competition may produce asymmetries in the costs-benefits balance of dispersal and philopatry for males and females, which may favour male-biased dispersal in polygynous species such as most mammals. This being the case, condition-dependent dispersal predicts that male-bias should decrease if mating competition relaxes. We test this expectation for red deer, where male-biased dispersal is the norm. In southwestern Spain, red deer populations located in nonfenced hunting estates presented altered structures with sex ratio strongly biased to females and high proportion of young males. As a consequence, mate competition in these populations was lower than in other, most typical red deer populations. We found that, under such conditions of altered population structure, dispersal was female-biased rather than male-biased. Additionally, mate competition positively related to male dispersal but negatively to female dispersal. Other factors such as resource competition, age of individuals and sex ratio were not related to male or female dispersal. Males may not disperse if intrasexual competition is low and then females may disperse as a response to male philopatry. We propose hypotheses related to female mate choice to explain female dispersal under male philopatry. The shift of the sex-biased dispersal pattern along the gradient of mate competition highlights its condition-dependence as well as the interaction between male and female dispersal in the evolution of sex-biased dispersal.     

Marrow fat content, sex and age of red deer killed by wolves in winter in the Carpathian Mountains

Age, sex and legbone marrow fat content of 90 red deer Cervus elaphus killed by wolves Canis lupus in winter in southeastern Poland were examined 1984–1988. The majority of kills were calves (44%) and hinds (40%); stags formed only 16%. The average age of hinds was 7.2 yr compared to 5.3 yr in stags. Animals older than 10 yr comprised only 13% of prey. Adults showed high femoral fat content (> 80%) throughout the winter (76% in early winter and 52% in late winter). Among calves femur marrow fat varied through the winter. In early winter 70% of calves had a high fat content (> 80%), though by late winter only 20% had such a high fat content, whilst 43% had low fat content (< 20%).