Male rock hyraxes that maintain an isochronous song rhythm achieve higher reproductive success.

Rhythmic stability (nonrandom temporal structure) is required for many neural and physiological functions, whereas rhythmic irregularities can indicate genetic or developmental deficiencies. Therefore, rhythmic courtship or contest signals are widespread in nature as honest advertisement displays. Examination of bird songs revealed the pervasiveness of categorical rhythmic patterns that can be described as small integer ratios between sequential inter-call intervals. As similar rhythmic profiles are prevalent in human music, it was suggested that a shared functionality could drive both animal songs and human musical rhythms, facilitating synchrony between signallers and enabling easy identification of performance errors. Here we examined whether the rhythmic structure and the rhythmic stability of vocal displays are related to reproductive success in male rock hyraxes (Procavia capensis), which presents an unusual case of a terrestrial singing mammal. We combined long-term parentage analysis of 13 male hyraxes (22 male/years) with an analysis of an audio library of 105 hyrax songs. Male annual reproductive success was determined by the number of offspring that survived to the age of 1 year. The frequency of singing events was used to determine the seasonal singing effort for each male. Songs were analysed for rhythmic structure, focusing on the presence of categorical rhythms and the contribution of rhythmic stability to annual reproductive success. We found that male hyraxes that sing more frequently tend to have more surviving offspring and that the rhythmic profile of hyrax songs is predominantly isochronous with sequential vocal element pairs nearly equally spaced. The ratio of isochronous vocal element transitions (on-integer) to element transitions that deviate from an isochronous pattern (off-integer) in hyrax songs is positively correlated with male reproductive success. Our findings support the notion that isochronous rhythmic stability can serve as an indication of quality in sexually selected signals and is not necessarily driven by the need for multiple caller synchronization. The relative scarcity of nonisochronous rhythmic categories in individually performed hyrax songs raises the question of whether such rhythmic categories could be a product of collective, coordinated signalling, while being selected against in individual performance.

Social context mediates testosterone's effect on snort acoustics in male hyrax songs.

Testosterone affects physical and motivational states, both of which may strongly influence vocalization structure and acoustics. The loud complex calls (i.e., songs) of male rock hyraxes (Procavia capensis) are used as honest signals for advertising physical and social states. The snort, a low frequency, noisy element of the song, encodes information on the singer's age and social rank via harshness, as measured by jitter (i.e., acoustic frequency stability) and duration; suggesting that the snort concomitantly advertises both vocal stability and aggression. Our past findings revealed that testosterone levels are related to both vocal elements and social status of male hyraxes, suggesting that hormonal mechanisms mediate the motivation for aggressive and courtship behaviors. Here we examined whether long-term androgen levels are related to snort acoustics and song structure by comparing levels of testosterone in hair with acoustic and structural parameters. We found that songs performed by individuals with higher testosterone levels include more singing bouts and longer, smoother snorts, but only in those songs induced by external triggers. It is possible that hyraxes with higher levels of testosterone possess the ability to perform higher-quality singing, but only invest in situations of high social arousal and potential benefit. Surprisingly, in spontaneous songs, hyraxes with high testosterone were found to snort more harshly than low-testosterone males. The context dependent effects of high testosterone on snort acoustics suggest that the aggressive emotional arousal associated with testosterone is naturally reflected in the jittery hyrax snort, but that it can be masked by high-quality performance.

The progression pattern of male hyrax songs and the role of climactic ending.

The study of animal vocal signals can either focus on the properties of distinct vocal elements or address the signal as a whole. Although some attention has been given to the continuous progression patterns of bird songs, such patterns in mammalian vocalisations have been largely overlooked. We examined temporal changes in structural and acoustic parameters in male rock hyrax songs. We found a gradual increase in call frequency and amplitude towards the song ending, as well as an abrupt increase in bout syntactic complexity, peaking in the last quintile of a song. In musical terms, such a pattern can be described as a crescendo (amplitude increase) with a terminal climax. In Western music, crescendos are used to maintain attention and direct the listeners towards a memorable highpoint of the musical piece. This structure may have an analogous function in animal communication, recruiting audience attention towards the climactic and potentially most informative part of the signal. Our playback experiments revealed that hyrax males tend to reply more to songs with a climactic ending, indicating that this progression pattern is important for hyrax communication. We suggest that animal vocal communication research can benefit from adding musical concepts to the analysis toolbox.

Experimental elevation of wildlife testosterone using silastic tube implants.

Testosterone (T) is a key androgen that mediates vertebrate molecular, cellular, and behavioral processes. Its manipulation is therefore of interest to a vast number of researchers studying animal behavior and reproduction, among others. Here, the usage of silastic implants across wildlife species is reviewed, and a method to manipulate rock hyrax (Procavia capensis) testosterone levels using silastic implants is presented. Using a series of in-vitro and in-vivo experiments, the secretion patterns of silastic tubes and silastic glue were tested and were surprisingly found to be similar. In addition, we studied endogenous T levels in wild-captured rock hyraxes (Procavia capensis), and using T implants succeeded in elevating T to the maximal physiological concentrations recorded during the mating period. The number of implants that were inserted was the only predictor of T levels, and seven 20mm implants were found to be the optimal dose. Implants induced sexual behaviors in the non-reproductive period. The duration of time that the implants were in the hyrax was the only significant factor that influenced the amount of T left over in the implant once it was removed. All together we affirm that T implants may offer a versatile tool for wildlife behavioral research by elevating T levels in the non-breeding period to maximal breeding levels.

Estimating vocal repertoire size is like collecting coupons: a theoretical framework with heterogeneity in signal abundance.

Vocal repertoire size is an important behavioural measure in songbirds and mammals with complex vocal communication systems, and has traditionally been used as an indicator of individual fitness, cognitive ability, and social structure. Estimates of asymptotic repertoire size have typically been made using curve fitting techniques. However, the exponential model usually applied in these techniques has never been provided with a theoretical justification based on probability theory, and the model has led to inaccurate estimates. We derived the precise expression for the expected number of distinct signal types observed for a fixed sampling effort: a variation of what is known in the statistical literature as the "Coupon Collector׳s problem". We used empirical data from three species (northern mockingbird, Carolina chickadee, and rock hyrax) to assess the performance of the Coupon Collector model compared to commonly used techniques, such as exponential fitting and repertoire enumeration, and also tested the different models against simulated artificial data sets with the statistical properties of the empirical data. We found that when signal probabilities are dissimilar, the Coupon Collector model provides far more accurate estimates of repertoire size than traditional techniques. Enumeration and exponential curve fitting greatly underestimated repertoire size, despite appearing to have reached saturation. Application of the Coupon Collector model can generate more accurate estimates of repertoire size than the commonly used exponential model of repertoire discovery, and could go a long way towards re-establishing repertoire size as a useful indicator in animal communication research.

The influence of androgenic steroid hormones on female aggression in 'atypical' mammals.

Dimorphism on dominance and agonistic behaviour in mammals tends to be strongly biased toward males. In this review, we focus on a select few species of mammals in which females are as or more aggressive than males, and/or are dominant to males, and explore the role of androgenic hormones in mediating this important difference. While the data are not as clear-cut as those published on traditional laboratory mammals, our review highlights important endocrine substrates for both organizational and activational influences of steroids on female aggressive behaviour. We highlight areas in which further observations and experiments are crucial, especially the potential facilitative effects of androgens on female aggression. Finally, new and innovative techniques, including molecular genetics and receptor pharmacology, portend important insights into the ways in which androgenic hormones regulate aggressive behaviour in 'atypical' female mammals.

Syntactic structure and geographical dialects in the songs of male rock hyraxes.

Few mammalian species produce vocalizations that are as richly structured as bird songs, and this greatly restricts the capacity for information transfer. Syntactically complex mammalian vocalizations have been previously studied only in primates, cetaceans and bats. We provide evidence of complex syntactic vocalizations in a small social mammal: the rock hyrax (Procavia capensis: Hyracoidea). We adopted three algorithms, commonly used in genetic sequence analysis and information theory, to examine the order of syllables in hyrax calls. Syntactic dialects exist, and the syntax of hyrax calls is significantly different between different regions in Israel. Call syntax difference is positively correlated to geographical distance over short distances. No correlation is found over long distances, which may reflect limited dispersal movement. These findings indicate that rich syntactic structure is more common in the vocalizations of mammalian taxa than previously thought and suggest the possibility of vocal production learning in the hyrax.

Sleep in the rock hyrax, Procavia capensis.

We investigated sleep in therock hyrax, Procavia capensis, a social mammal that typically lives in colonies on rocky outcrops throughout most parts of Southern Africa. The sleep of 5 wild-captured, adult rock hyraxes was recorded continuously for 72 h using telemetric relay of signals and allowing unimpeded movement. In addition to waking, slow wave sleep (SWS) and an unambiguous rapid eye movement (REM) state, a sleep state termed somnus innominatus (SI), characterized by low-voltage, high-frequency electroencephalogram, an electromyogram that stayed at the same amplitude as the preceding SWS episode and a mostly regular heart rate, were identified. If SI can be considered a form of low-voltage non-REM, the implication would be that the rock hyrax exhibits the lowest amount of REM recorded for any terrestrial mammal studied to date. Conversely, if SI is a form of REM sleep, it would lead to the classification of a novel subdivision of this state; however, further investigation would be required. The hyraxes spent on average 15.89 h (66.2%) of the time awake, 6.02 h (25.1%) in SWS, 43 min (3%) in SI and 6 min (0.4%) in REM. The unambiguous REM sleep amounts were on average less than 6 min/day. The most common state transition pathway in these animals was found to be wake → SWS → wake. No significant differences were noted with regard to total sleep time, number of episodes and episode duration for all states between the light and dark periods.Thus, prior classification of the rock hyrax as strongly diurnal does not appear to hold under controlled laboratory conditions.

Do singing rock hyraxes exploit conspecific calls to gain attention?

Signal detection theory predicts that signals directed at distant or busy receivers in noisy backgrounds will begin with an alert component, in order to draw attention. Instead of an alert component, however, animals could get the same effect by using an external stimulus. Here we combined observations of free-living rock hyraxes (Procavia capensis) with playback experiments to elucidate the circumstances under which males begin singing. We show that males sing following hyrax pup screams, which elicit a strong response from hyraxes within hearing distance, which are potential receivers. We hypothesize that singers enhance their singing display by exploiting the rarely emitted pup screams. To our knowledge, our findings are the first indication that animals may enhance signal reception by exploiting conspecifics' signals and the differential attention to these signals. We suggest that the utilization of external stimuli by signalers may be widespread, as an adaptive strategy for communication in complex environments.

Variance in centrality within rock hyrax social networks predicts adult longevity.

BACKGROUND: In communal mammals the levels of social interaction among group members vary considerably. In recent years, biologists have realized that within-group interactions may affect survival of the group members. Several recent studies have demonstrated that the social integration of adult females is positively associated with infant survival, and female longevity is affected by the strength and stability of the individual social bonds. Our aim was to determine the social factors that influence adult longevity in social mammals. METHODOLOGY/PRINCIPAL FINDINGS: As a model system, we studied the social rock hyrax (Procavia capensis), a plural breeder with low reproductive skew, whose groups are mainly composed of females. We applied network theory using 11 years of behavioral data to quantify the centrality of individuals within groups, and found adult longevity to be inversely correlated to the variance in centrality. In other words, animals in groups with more equal associations lived longer. Individual centrality was not correlated with longevity, implying that social tension may affect all group members and not only the weakest or less connected ones. CONCLUSIONS/SIGNIFICANCE: Our novel findings support previous studies emphasizing the adaptive value of social associations and the consequences of inequality among adults within social groups. However, contrary to previous studies, we suggest that it is not the number or strength of associations that an adult individual has (i.e. centrality) that is important, but the overall configuration of social relationships within the group (i.e. centrality SD) that is a key factor in influencing longevity.

Social status and cortisol levels in singing rock hyraxes.

Many mammals use acoustic signals to communicate with conspecifics. Rock hyraxes (Procavia capensis) are social mammals whose vocal communication is usually restricted to quiet sounds used between nearby individuals. Loud repetitive warning trills are an exception. In our study site, a third of the adult male hyraxes also produces a rich, complex and loud vocalization we term 'singing'. In this study, we examine whether singers, which are more conspicuous by the act of singing, have higher cortisol (i.e. basal stress; C) levels than non-singers, and whether there is an association between social status and stress hormones in male hyraxes. We show that 'singing' males are different from the general adult male population in that their C levels are higher than those of silent males. Only in singers, C levels are associated with social rank, with dominants showing the highest levels. Singers are also on average older and more dominant than most other sexually mature non-singing males. Further, they copulate more than non-singers, suggesting that singing males may have higher reproductive success. Our results support the 'stress of domination' hypothesis and indicate that in the rock hyrax singing may reflect high competitive ability, designating singers as a distinct class of males, unique in their personal attributes and behavior.

Hematology and serum biochemistry values of trapped, healthy, free-ranging rock hyraxes (Procavia capensis) and their association with age, sex, and gestational status.

BACKGROUND: The rock hyrax (Procavia capensis) is an herbivore prevalent from South Africa to Turkey, and a most common zoo animal. Although many studies of hyrax diseases and physiology are available, clinicopathologic data are limited. OBJECTIVES: The purpose of this study was to establish comprehensive hematologic and biochemical reference intervals for trapped, apparently healthy, free-ranging rock hyraxes using modern laboratory methods and to assess differences related to sex, gestation, and age. METHODS: Blood samples were obtained from 27 healthy, free-ranging hyraxes under anesthesia. Gender, body weight, and gestational status were recorded. Hematologic (n = 25) and serum biochemical (n = 22) analyses were performed using standard automated methodology. Data for male vs female, adult vs juvenile, and pregnant vs nonpregnant female hyraxes were compared using the Mann-Whitney U-test. Associations between variables were assessed using Pearson's or Spearman rank correlation tests. RESULTS: Significant age- and sex-related, but not gestation-related differences were observed in several variables. Serum alkaline phosphatase activity and phosphorus concentration were significantly higher in juveniles compared with adults. A unique type of monocyte comprised 1-3% of leukocytes in 4 hyraxes. Markedly high serum creatine kinase (CK) activity was observed in most hyraxes. CONCLUSIONS: The large number of animals and the availability of sex, age, and gestational data in this study will be useful to zoo and wildlife veterinarians working with rock hyraxes. High serum concentrations of betahydroxybutyric acid in the rock hyrax, compared with dogs, cats, and ruminants, may be related to its unique digestive system. High CK activity may have been the result of a capture myopathy-like syndrome. The unique monocytes in hyraxes resemble those of elephants and are a novel finding in this species.

Elevated testosterone levels and social ranks in female rock hyrax.

In mammals, males maintain significantly higher testosterone (T, 'the male hormone') levels than females throughout the year and are typically dominant over females. Our study of the cooperatively breeding rock hyrax (Procavia capensis) demonstrated a distinct exception. In most hyrax social groups that we studied, adult females were at the highest social rank within the group and showed higher than or equal T levels to males. To our knowledge, this is the first reported instance of adult female mammals demonstrating higher T levels than adult males. However, although T levels significantly correlated with rank in males, in females such correlations were not detected, suggesting a more complex interplay between behavior and endocrine factors in this species.

Seasonal patterns in body temperature of free-living rock hyrax (Procavia capensis).

Rock hyrax (Procavia capensis) are faced with large daily fluctuations in ambient temperature during summer and winter. In this study, peritoneal body temperature of free-living rock hyrax was investigated. During winter, when low ambient temperatures and food supply prevail, rock hyrax maintained a lower core body temperature relative to summer. In winter body temperatures during the day were more variable than at night. This daytime variability is likely a result of body temperatures being raised from basking in the sun. Body temperatures recorded during winter never fell to low levels recorded in previous laboratory studies. During summer ambient temperatures exceeded the thermoneutral zone of the rock hyrax throughout most of the day, while crevice temperatures remained within the thermoneutral zone of rock hyrax. However, in summer variation in core body temperature was small. Minimum and maximum body temperatures did not coincide with minimum and maximum ambient temperatures. Constant body temperatures were also recorded when ambient temperatures reached lethal limits. During summer it is likely that rock hyrax select cooler refugia to escape lethal temperatures and to prevent excessive water loss. Body temperature of rock hyrax recorded in this study reflects the adaptability of this animal to the wide range of ambient temperatures experienced in its natural environment.

Effects of food processing on masticatory strain and craniofacial growth in a retrognathic face.

Changes in the technology of food preparation over the last few thousand years (especially cooking, softening, and grinding) are hypothesized to have contributed to smaller facial size in humans because of less growth in response to strains generated by chewing softer, more processed food. While there is considerable comparative evidence to support this idea, most experimental tests of this hypothesis have been on non-human primates or other very prognathic mammals (rodents, swine) raised on hard versus very soft (nearly liquid) diets. Here, we examine facial growth and in vivo strains generated in response to raw/dried foods versus cooked foods in a retrognathic mammal, the rock hyrax (Procavia capensis). The results indicate that the hyrax cranium resembles the non-human primate cranium in having a steep gradient of strains from the occlusal to orbital regions, but differs from most non-anthropoids in being primarily twisted; the hyrax mandible is bent both vertically and laterally. In general, higher strains, as much as two-fold at some sites, are generated by masticating raw versus cooked food. Hyraxes raised on cooked food had significantly less growth (approximately 10%) in the ventral (inferior) and posterior portions of the face, where strains are highest, resembling many of the differences evident between humans raised on highly processed versus less processed diets. The results support the hypothesis that food processing techniques have led to decreased facial growth in the mandibular and maxillary arches in recent human populations.

Islands on the plains: metapopulation dynamics and female biased dispersal in hyraxes (Hyracoidea) in the Serengeti National Park.

Two species of hyrax, Heterohyrax brucei and Procavia johnstoni, inhabit rock outcrops, or kopjes, in the Serengeti National Park, Tanzania. Such distinct 'island' habitats provide an excellent model to investigate natural metapopulation dynamics with distinct small populations with extinction and colonization events, as well as migration between populations. Allele frequencies, genetic variability and genetic distances between populations were calculated based on DNA microsatellite markers. The genetic diversity in both species of hyrax, especially P. johnstoni, was surprisingly low: allelic diversity ranged from 2 to 7 alleles per locus. This may have been induced by colonization by a small number of individuals from single source populations. F-statistics, assignment tests and calculations of pairwise relatedness all indicated female-biased dispersal in H. brucei but not P. johnstoni. Values of FIS in P. johnstoni showed an excess of homozygotes indicative of high rates of inbreeding; evidence for inbreeding could not be detected in H. brucei. Although female dispersal patterns in H. brucei seem to prevent inbreeding and consequently reduce risk of local extinction, this seems not to be the case in P. johnstoni.

Steroidogenic correlates of pregnancy in the rock hyrax (Procavia capensis).

In pregnant rock hyraxes isolated leucocytes metabolise both [3H]pregnenolone and [3H]progesterone while whole blood, erythrocytes and an erythrocyte/leucocyte mixture only metabolised [3H]progesterone. Plasma displayed no tendency to metabolically convert any one of these two steroids. In whole blood [3H]progesterone appears to be converted to 5alpha-pregnane-3,20-dione and a compound with chromatographic properties similar to that of 5alpha-pregnan-3alpha-ol-20-one. 5Alpha-pregnane-3,20-dione exhibited a high relative binding affinity for the uterine progesterone eceptor (94%), but 5alpha-pregnan-3alpha-ol-20-one displayed very little affinity for the same receptor (0.4%). 5Alpha-pregnane-3,20-dione may therefore aid in the maintenance of pregnancy. Corpora lutea metabolised progesterone to 17alpha-hydroxyprogesterone, a compound exhibiting no progestational function because of its low relative binding affinity for the uterine progesterone receptor (2%). Progesterone appears to be the main product of the corpus luteum. However, 5alpha-pregnane-3,20-dione circulated at concentrations approximately 8.5 times higher than progesterone, probably due to the metabolic conversion of progesterone to 5alpha-pregnane-3,20-dione by the blood. We conclude that in the hyrax progesterone, produced by the corpora lutea, enters the circulation, where it is reduced to 5alpha-pregnanes. 5Alpha-pregane-3,20-dione may then be transported to the uterus where it binds to the progesterone receptor to assist in the maintenance of pregnancy. This mechanism appears to be analogous to that of the African elephant which is phylogenetically related to the hyrax, except that in the elephant the 5alpha-reduced metabolites are produced by luteal tissue and not the blood.

The gastrointestinal tract of the rock hyrax (Procavia habessinica). 1. Morphology and motility patterns of the tract.

The stomach of the rock hyrax (Procavia habessinica) is divided into a non glandular part with very slow movements, and a glandular part which rapidly mix the digesta. The large intestine has two fermentation chambers, the caecum, which rapidly mixes the digesta, and the colonic sac, which efficiently, but slowly, mixes digesta. Between these chambers runs the connecting colon. No retrograde transport is observed in any part of the large intestine.

Timing in the movement of jaws, tongue, and hyoid during feeding in the hyrax, Procavia syriacus.

The anatomical structures used during mammalian feeding are morphologically linked by their connecting musculature, suggesting a predictable timing relationship among their movements. Cine-x-ray (100 frames per second) was used to record feeding behavior in four adult hyraxes (Procavia syriacus), herbivores. Movement of jaws, tongue, and hyoid bone was cyclic, and prior to the first swallow cycle, cycle duration was constant through time for all structures. Minimum gape, beginning of forward movement of the tongue and hyoid, and beginning of intrinsic tongue expansion occurred simultaneously over a large number of cycles. However, maximum gape, maximum protrusion of hyoid, and maximum forward position of the tongue happened at statistically different points in time. After the first swallow, cycle duration increased. Most of the variation in cycle duration can be explained by variation in the opening or forward phase of movement; the closing and return phases are constant in duration. These results are a quantitative description of the coordination that exists during different feeding behaviors (ingestion, intraoral transport, mastication, and swallowing) in normal, freely functioning hyraxes. The patterns of phase duration differ from some results obtained by using anesthetized animals.