Fecal androgens of bison bulls during the rut

The influence of sex hormones is a key proximate factor underlying male reproductive behavior in mammals. Effective conservation policies for the remaining purebred plains bison (Bison bison bison) herds require knowledge of the physiology underlying bison reproductive biology. We used fecal steroid analysis to characterize androgen levels in adult bison bulls before, during, and after the rut, and to examine androgen levels of bulls differing in reproductive status, age, and mating success. Fieldwork was carried out at the Fort Niobrara National Wildlife Refuge in north-central Nebraska. All adult bison in the herd were individually known by unique brands. Fecal samples were collected during 2003 from bulls during pre-rut (June), rut (July-August), and post-rut (September), and behavioral observations focused on reproductive status and mating success during the rut. Matched sample data indicated that androgen levels (ng/g feces) of bulls peaked during the rut, doubling from pre-rut to rut and then declining by 75% during post-rut. Dominant bulls that tended (guarded) cows maintained higher androgen levels than bulls that were not tending. There was a positive correlation between bull age (associated with mating success) and androgens, with higher androgen levels in prime-aged bulls compared with younger bulls. Nonetheless, there was no correlation between mating success (measured by number of copulations observed) and androgen level. This suggests that while androgens may provide the proximate motivation to compete for matings, other factors determine the mating success of bison bulls.     

不同年龄雄性北山羊发情期时间分配特征

前人研究表明,可多次繁殖的反刍物种其雄性个体在发情期采食时间显著减少。目前有两个假说解释这一现象,即能量摄入最大化假说和能量保存假说。为验证雄性北山羊在不同发情阶段所采取的能量保存策略,作者于2014年10-12月在新疆天山中部采用焦点动物取样法采集数据,采用Kruskal-Wallis检验和Spearman秩相关性检验分析数据。研究发现雄性北山羊成体和亚成体发情期采食时间均显著低于发情前期和发情后期,但二者在不同发情阶段卧息时间无显著变化,发情期采食和卧息时间比亦显著降低。发情期发情行为时间显著高于发情前期和发情后期,非发情时间主要用于采食。发情期采食时间和卧息时间都与发情行为时间呈显著的负相关关系。雌性北山羊发情期采食时间亦显著低于发情前期和发情后期,发情期和发情后期卧息时间显著高于发情前期。本研究结果表明,发情期不同年龄阶段雄羊都主要采取能量摄入最大化策略,但同时也具有部分能量保存策略的特征。     

雄性麋鹿的交配机会、社会等级和皮质醇水平

我们在北京麋鹿苑研究了发情期雄性麋鹿的社会行为、社会等级和血清皮质醇水平,并分析了三者间的相互关系。按照雄性麋鹿的行为,将雄性麋鹿分为优势群和从属群。优势群包括群主和挑战者,从属群包括单身汉和被淘汰群主。使用SJ—Ⅰ型事件记录器进行常规行为取样,用放射免疫分析法测定血清皮质醇含量。发现：(1)优势雄鹿的发情行为频次明显高于从属雄鹿;(2)攻击行为的发生频次在两组间无显著差异;(3)血清皮质醇含量在两组间也无显著差异。由此我们认为,发情期雄性麋鹿的社会等级序位影响许多行为的表达,优势雄鹿成功交配的机会比从属雄鹿多。而攻击行为和肾上腺皮质醇的分泌与社群等级无明显相关,可能是麋鹿在圈养状态下的一种适应策略,这将有利于缓解发情期雄鹿的紧张,从而允许更多的能量投放在发情交配上。     

不同发情阶段雄性鹅喉羚的时间分配特征

以往研究表明受发情交配行为制约,一些雄性反刍动物在发情期食物摄入量明显降低。已有两个相关假说解释该现象:能量摄入最大化假说和能量保存假说。作者于2009 ～ 2010 年在卡拉麦里山有蹄类自然保护区研究了雄性鹅喉羚不同发情阶段的时间分配。结果表明雄羚发情期采食时间比例明显下降(37. 9% ),低于发情前期(63. 6% )和发情后期(65. 8% );发情期卧息时间比例(6. 0% )与发情后期相近(5. 4% ),明显低于发情前期(23.2% );发情前期至发情后期采食卧息时间比(分别为2. 7、6. 3、12. 1)显著增加;发情期雄羚站立和移动时间比例明显升高,采食行为时间占非发情行为时间主要部分(86. 4% ),且采食行为与发情行为显著相关。相比之下,雌羚不同发情阶段采食行为时间分配比例相似。总之,除必需投入的发情行为外,发情期雄羚最大化其能量摄入;发情行为的投入是导致发情期雄羚食物摄入量下降的主导因子,雄性能量摄入最大化假说更好地解释了发情期鹅喉羚所采取的能量策略。     

Season effect on genitalia and epididymal sperm from Iberian red deer, roe deer and Cantabrian chamois

Seasonality deeply affects the physiology and behavior of many species, and must be taken into account when biological resource banks (BRBs) are established. We have studied the effect of seasonality on many reproductive parameters of free-ranging Iberian red deer, roe deer and Cantabrian chamois, living in Spain. Testicles from hunted animals were collected and sent to our laboratory at different times during the year. We recorded the weight and volume of testis, the weight of the epididymis and its separate parts (caput, corpus, and cauda), the weight of the sperm sample collected from the cauda epididymis, and several sperm parameters (sperm concentration, spermatozoa recovered, motility, HOS test reactivity, acrosomal status, and viability). We studied the data according to several periods, defined accordingly to each species. For red deer, we defined rut (mid-September to mid-October), post-rut (mid-October to mid-December), and non-breeding season (February). For roe deer, they were pre-rut (June), rut (July), post-rut (first fortnight of August), and non-breeding season (September). For chamois: non-breeding season (June to mid-September) and breeding season (October-November). The rut/breeding season yielded significantly higher numbers for almost all parameters. However, in the case of red deer, sperm quality was higher in the post-rut. For roe deer, testicular weight was similar in the pre-rut and in the rut, and sperm quality did not differ significantly between these two periods, although we noticed higher values in the rut. In the case of chamois, sperm quality did not differ significantly from the breeding season, but data distribution suggested that in the non-breeding season there are less males with sperm of good quality. On the whole, we find these results of interest for BRB planning. The best season to collect sperm in this species would be the breeding season. However, post-rut in red deer, pre-rut in roe deer, and non-breeding season in chamois could be used too, because of the acceptable sperm quality, despite the lower quantity salvaged. More in-depth research needs to be carried out on the quality of sperm salvaged at different times of the year in order to confirm these findings.     

Sperm competition roles and ejaculate investment in a promiscuous mammal

Theoretical models of sperm competition predict how males should allocate sperm and seminal fluid components to ejaculates according to their mating role (dominant vs. subordinate). Here, we present a detailed analysis of ejaculate expenditure according to male roles in the bank vole (Myodes glareolus). Sperm competition occurs regularly in this species, and dominant males typically achieve higher fertilization success than subordinates. Contrary to theoretical predictions, we found that dominant male bank voles invest more sperm per ejaculate than subordinates, both absolutely and relative to body and testes mass. The testes of dominant males were also absolutely (although not relatively) larger than those of subordinates. However, we found no evidence that subordinate males compensate for lower sperm numbers per ejaculate by increasing ejaculation frequency or sperm velocity. Similarly, we found no evidence for differential investment in copulatory plug size according to male roles in sperm competition, although dominant males had significantly larger seminal vesicles (both absolutely and relative to body mass) compared with subordinates. We conclude that sperm competition roles can have significant but unexpected influences on ejaculate investment in mammals with clearly defined differences in male social status.     

Social dominance, aggression and faecal glucocorticoid levels in a wild population of wolves, Canis lupus

Adrenal glucocorticoid (GC) secretion is an important component of the response to stress in vertebrates. A short-term increase in circulating GCs serves to redirect energy from processes that can be briefly curtailed without harm, allowing energy to be directed towards eliminating or avoiding the stressor. In contrast, prolonged elevation of GCs can cause a broad range of pathologies, including reproductive suppression. We examined whether social subordination in wolves leads to chronically elevated GC levels, and whether this ‘social stress’ causes reproductive suppression of subordinates in cooperatively breeding species. Behavioural and endocrine data collected over 2 years from three packs of free-living wolves in Yellowstone National Park did not support this hypothesis. GC levels were significantly higher in dominant wolves than in subordinates, for both sexes, in all packs, in both years of study. Unlike other cooperatively breeding carnivores (e.g. dwarf mongooses, Helogale parvula, and African wild dogs, Lycaon pictus), high GCs in dominant wolves were not associated with high rates of aggression or agonistic interaction. Aggression increased for wolves of all ranks during mating periods, accompanied by a significant rise in GC levels. If chronic elevation of GCs carries fitness costs, then social stress in wolves (and many other social species) is a cost of dominance, not a consequence of subordination. The specific behavioural correlates of dominance that affect GC levels appear to vary among species, even those with similar social systems.     

Reproductive effort of bison bulls (<Emphasis Type="Italic">Bison bison</Emphasis>) in semi-natural conditions

Reproductive effort (RE) is defined as the investment in any current reproductive act. In male ungulates, variation in RE can be explained by differences in age, dominance, phase in the breeding season and number of oestrus females simultaneously present. We investigated the relation between these factors and RE in American bison males in semi-natural conditions. We looked for differences between males in RE, measured by tending behaviour, and maintenance activities (feeding/resting) during the rut. We found no effect of age on RE. During early rut there was no difference in RE between males of different rank. Dominant males had a higher RE during peak rut, and in late rut both the first and second ranking males showed more RE than lower ranking bulls. For all males, there was a clear increase in RE towards peak rut and when more females were attractive. Maintenance behaviours decreased when more females were synchronously in oestrus. The most dominant bulls spent less time grazing than lower ranking males, and all males decreased feeding during peak rut. Resting decreased with age. We conclude that dominance, phase of rut and the number of females synchronously in oestrus are the factors that best explain variation in RE.     

Elevated glucocorticoid concentrations during gestation predict reduced reproductive success in subordinate female banded mongooses

Dominant females in social species have been hypothesized to reduce the reproductive success of their subordinates by inducing elevated circulating glucocorticoid (GC) concentrations. However, this ‘stress-related suppression'' hypothesis has received little support in cooperatively breeding species, despite evident reproductive skews among females. We tested this hypothesis in the banded mongoose (Mungos mungo), a cooperative mammal in which multiple females conceive and carry to term in each communal breeding attempt. As predicted, lower ranked females had lower reproductive success, even among females that carried to term. While there were no rank-related differences in faecal glucocorticoid (fGC) concentrations prior to gestation or in the first trimester, lower ranked females had significantly higher fGC concentrations than higher ranked females in the second and third trimesters. Finally, females with higher fGC concentrations during the third trimester lost a greater proportion of their gestated young prior to their emergence from the burrow. Together, our results are consistent with a role for rank-related maternal stress in generating reproductive skew among females in this cooperative breeder. While studies of reproductive skew frequently consider the possibility that rank-related stress reduces the conception rates of subordinates, our findings highlight the possibility of detrimental effects on reproductive outcomes even after pregnancies have become established.     

The relationship between dominance, corticosterone, memory, and food caching in mountain chickadees (Poecile gambeli)

It has been hypothesized that in avian social groups subordinate individuals should maintain more energy reserves than dominants, as an insurance against increased perceived risk of starvation. Subordinates might also have elevated baseline corticosterone levels because corticosterone is known to facilitate fattening in birds. Recent experiments showed that moderately elevated corticosterone levels resulting from unpredictable food supply are correlated with enhanced cache retrieval efficiency and more accurate performance on a spatial memory task. Given the correlation between corticosterone and memory, a further prediction is that subordinates might be more efficient at cache retrieval and show more accurate performance on spatial memory tasks. We tested these predictions in dominant-subordinate pairs of mountain chickadees (Poecile gambeli). Each pair was housed in the same cage but caching behavior was tested individually in an adjacent aviary to avoid the confounding effects of small spaces in which birds could unnaturally and directly influence each other's behavior. In sharp contrast to our hypothesis, we found that subordinate chickadees cached less food, showed less efficient cache retrieval, and performed significantly worse on the spatial memory task than dominants. Although the behavioral differences could have resulted from social stress of subordination, and dominant birds reached significantly higher levels of corticosterone during their response to acute stress compared to subordinates, there were no significant differences between dominants and subordinates in baseline levels or in the pattern of adrenocortical stress response. We find no evidence, therefore, to support the hypothesis that subordinate mountain chickadees maintain elevated baseline corticosterone levels whereas lower caching rates and inferior cache retrieval efficiency might contribute to reduced survival of subordinates commonly found in food-caching parids.     

Effects of social status, age, and season on androgen and cortisol levels in wild male golden lion tamarins (Leontopithecus rosalia)

This study examines factors affecting androgen and cortisol levels in wild, male golden lion tamarins (Leontopithecus rosalia). Golden lion tamarins are a cooperatively breeding species in which groups often contain two potentially breeding males. Brothers frequently emigrate together and develop a clear dominance hierarchy, but interactions between them are primarily affiliative. Duos in which the males are not related are less stable. In addition, reproductive skew theory predicts that dominant males will be less likely to share reproduction with related subordinates. As such, we predicted that both androgens and cortisol would be higher in subordinate males unrelated to the dominant male. We also predicted that androgens in breeding males would be higher during the mating season than the birth/infant care season, as per Wingfield's "challenge hypothesis" (1990). Fecal samples were collected from 24 males in 14 social groups and assayed by enzyme immunoassay. Androgen levels were higher in breeding males during the mating season, thus supporting the challenge hypothesis. However, while subordinate males unrelated to the dominant male had significantly lower androgens than any other group, cortisol levels were not correspondingly higher. These results suggest that unrelated subordinate males show measurable reproductive suppression and may use strategies such as infantilization to avert aggression from dominant males.     

Cortisol and corticosterone in the songbird immune and nervous systems: local vs. systemic levels during development

Glucocorticoids (GCs) have profound effects on the immune and nervous systems during development. However, circulating GC levels are low neonatally and show little response to stressors. This paradox could be resolved if immune and neural tissues locally synthesize GCs. Here, we measured baseline corticosterone and cortisol levels in plasma, immune organs, and brain regions of developing zebra finches. Steroids were extracted using solid phase-extraction and quantified using specific immunoassays. As expected, corticosterone was the predominant GC in plasma and increased with age. In contrast, cortisol was the predominant GC in immune tissues (bursa of Fabricius, thymus, spleen) and decreased with age. Cortisol levels in immune tissues were higher than cortisol levels in plasma. In the brain, corticosterone and cortisol levels were similarly low, providing little evidence for local synthesis of GCs in the brain. This is the first study to measure 1) cortisol in the plasma of songbirds, 2) corticosterone or cortisol in the brain of songbirds, and 3) corticosterone or cortisol in the immune system of any species. Despite the prevailing dogma that corticosterone is the primary GC in birds, these results indicate that cortisol is the predominant GC in the immune system of developing zebra finches. These results raise the hypothesis that cortisol is synthesized de novo from cholesterol in the immune system as an "immunosteroid," analogous to neurosteroids synthesized in the brain. Local production of GCs in immune tissues may allow GCs to regulate lymphocyte selection while avoiding the costs of high systemic GCs during development.     

Fecal testosterone is elevated in high ranking female ibexes (Capra nubiana) and associated with increased aggression and a preponderance of male offspring

We monitored fecal testosterone and progesterone levels in 26 adult ibexes (17 males, 9 females) in a captive herd Nubian ibex held on 250 ha tract to test if testosterone is associated with dominance. The ibexes were observed over a 20-month period, and including two mating seasons, during which time we collected fecal samples twice during early gestation and postpartum intervals and once during lactation and pre-rut season intervals. The social hierarchy was linear with age in adult males and nearly linear in adult females. High ranking males were in solitude, but females were aggregated with the kids in the presence of a dominant female. The testosterone concentration in the males in the pre-rut (211+/-12 ng/g; N=13; dominant male 296 ng/g) was significant higher than other seasons (P<0.05). High testosterone in dominant male at pre-rut was associated with a decrease in confrontations. The individuals with the highest average testosterone concentrations were the dominant male and female (166+/-82 ng/g; 130+/-32 ng/g, N=6, respectively). In females, testosterone was highest in during the post-partum interval and was associated with an increase in aggression. The three highest fertile ranking females had higher testosterone (119+/-14 ng/g vs. 92+/-18 ng/g, P<0.05) than the four subordinate females. The sex ratio of the offspring was 8M/3F for the three older females and 5M/7F for the younger females. In early gestation period, females with only male fetuses had higher testosterone than other gravidities (119+/-14 ng/g, N=6 vs. 91+/-18 ng/g, N=7, P<0.01). Progesterone was significantly higher in the eight multiparous pregnancies than in those with the five singletons (210+/-19 ng/g vs. 186+/-12 ng/g, P<0.02). We conclude that high testosterone in females is associated with an increase in aggressive confrontations in early- and mid-lactation. In contrast, increased testosterone during pre-rut in males is associated with fewer confrontations. In addition, the data support the hypothesis that higher ranking, older dimorphic female ungulates have higher testosterone concentrations and have more male births than subordinate females.     

Gender Differences in the Costs that Subordinate Group Members Impose on Dominant Males in a Cooperative Breeder

In group-living species, a dominant male's ability to monopolize reproduction, and the cost of doing so, are expected to vary with a group's gender composition. We used spawning observations of a group-living cichlid, Neolamprologus pulcher , to test this expectation. We constructed groups that contained a dominant breeding pair and either two male subordinates, one male and one female subordinate or two female subordinates. Parasitic spawning by male subordinates was more common in groups with two male subordinates than in groups with one male and one female subordinate. Female subordinates were never observed laying eggs in dominant females' clutches, but three female subordinates laid independent clutches. During spawning, frequencies of dominant male aggression towards male and female subordinates were similar. Dominant males were less aggressive during non-reproductive periods. The declines were greater for female subordinates, such that, during non-reproductive periods, dominant males were more aggressive towards male subordinates. Aggression towards each subordinate was also affected by the second subordinate's gender; the direction of that effect differed for large and small subordinates. Male subordinates approached breeding shelters less often than female subordinates, and both male and female subordinates approached shelters more frequently when the second subordinate was male. Collectively, these patterns suggest: (1) that male subordinates impose higher costs on dominant males than female subordinates do and (2) that the presence of a second male subordinate imposes additional costs beyond those of the first male subordinate. We discuss the implications of these effects for dominant and subordinate group members.     

Small Subordinate Male Advantage in the Zebrafish

Dominance is an important determinant of reproductive success in many species, and size is usually an indicator of dominance status, with larger, dominant individuals physically and physiologically preventing smaller subordinates from mating. However, small size may be advantageous in some mating contexts because enhanced manoeuvrability enables males to get closer to females during mating. Here, we determined the paternity success and testes size of dominant and subordinate male zebrafish (Danio rerio), in pairs that controlled for social status. There was no statistical difference in both body size and testes size between dominant and subordinate males. Dominant males sired significantly more offspring than subordinates, but when subordinates were small, they had a greater share of the paternity than larger subordinates. Small male advantage may be one mechanism by which variation in body size is maintained in this species.     

Male dominance status,female choice and mating success in the brown lemming, Lemmus trimucronatus

The objective of this study was to determine whether female brown lemmings would selectively mate with dominant conspecific males. In dyadic encounters, oestrous females paired with dominant males engaged in more frequent lordosis and contact social behaviours than those paired with subordinate males. However, the mount and thrust scores of dominant and subordinate males did not differ significantly. When females had simultaneous access to tethered dominant and subordinate males, they spent more time in close proximity to dominant males and avoided contact with subordinate males. Copulation scores were higher with dominant males. In triadic encounters with free-moving dominant and subordinate males, oestrous females spent more time near, and engaged in more sexual behaviour with, dominant males. Intermale agonistic interactions resulted in ‘privileged access’ to females by dominant males. Sexual behaviour scores were lower and there was a 10-fold increase in intermale aggression in triadic encounters between females and unfamiliar dominant and subordinate males. Both intermale agonistic interactions and female ‘choice’ behaviour accounted for the differential copulatory success of dominant males.     

Sociality and oxytocin and vasopressin in the brain of male and female dominant and subordinate mandarin voles

The dominant–subordinate hierarchy in animals often needs to be established via agonistic encounters and consequently affects reproduction and survival. Differences in brain neuropeptides and sociality among dominant and subordinate males and females remain poorly understood. Here we explore neuropeptide levels and sociality during agonistic encounter tests in mandarin voles. We found that dominant mandarin voles engaged in higher levels of approaching, investigating, self-grooming and exploring behavior than subordinates. Dominant males habituated better to a stimulus vole than dominant females. Dominant males displayed significantly less oxytocin-immunoreactive neurons in the paraventricular nuclei and more vasopressin-immunoreactive neurons in the paraventricular nuclei, supraoptic nuclei, and the lateral and anterior hypothalamus than subordinates. Dominant females displayed significantly more vasopressin-immunoreactive neurons in the lateral hypothalamus and anterior hypothalamus than subordinates. Sex differences were found in the level of oxytocin and vasopressin. These results indicate that distinct parameters related to central nervous oxytocin and vasopressin are associated with behaviors during agonistic encounters in a sex-specific manner in mandarin voles.     

Infanticide by subordinates influences reproductive sharing in cooperatively breeding meerkats

In cooperative animal societies, dominant females typically show higher breeding success than subordinates, and are commonly believed to control the extent of reproductive sharing. However, studies of social insect societies reveal that subordinates too can interfere with the breeding attempts of others, with important implications for the distribution of fitness within colonies. Here, we show that subordinate females in a high-skew vertebrate (the meerkat, Suricata suricatta), also exert a substantial influence over the reproductive attempts of others. In meerkat societies, pregnant dominants are known to kill subordinate litters, but we show that pregnant subordinates also kill pups; not only those of other subordinates but the dominant's as well. Litters born to females of any rank were half as likely to survive their first 4 days if a subordinate was pregnant. However, dominant females were more likely than subordinates to give birth when no other females were pregnant, and so lost fewer litters to infanticide than subordinates. This is probably due in part to dominants employing counter-tactics to reduce the incidence of subordinate pregnancy. We discuss the broad implications of subordinates having a degree of control over reproductive sharing for future attempts to understand the distribution of reproduction in animal societies.     

Reproductive success of bison bulls (Bison bison bison) in semi-natural conditions

Sexual size dimorphism has been related to a high variance in male reproductive success. Research on American bison (Bison bison bison), a species that shows moderate sexual dimorphism, has put forward the assumption that under wild conditions the largest part of the female herd is bred by a limited number of males. Thus far, this hypothesis has never been supported by genetic data. The aim of this study is therefore to test the hypothesis of extreme male reproductive variance among bison through the determination of the reproductive success of the bulls in private herds. We analysed genetic paternity in four private herds (n=19, 33, 39 and 54) kept under semi-natural conditions. By analysing blood, hair and tissue samples, using 8-10 polymorphic microsatellites, the reproductive success of the bulls was quantified. Additional genetic data were gathered through a survey distributed among bison breeders with private herds over the world. Results show a highly differential reproductive success for bison males in private herds kept under semi-natural conditions. In each study group, a single male sires at least 70% of the calves. In the survey groups, a single male sires 81-100% of the calves. Only one survey group displayed a deviating pattern showing a more evenly distribution of paternity (28.57, 33.33 and 38.10%) among three same aged subadult males.     

Fighting Tactics of Fallow Bucks (Dama dama,Cervidae): Reducing the Risks of Serious Conflict

Competition between male fallow deer (Dama dama), during the breeding season was studied to determine if conflict strategies were consistent with the reduction of risk. Agonistic interactions between males were analysed in relation to age, dominance rank and availability of mating opportunities. The breeding season was divided into two main periods: the pre-rut began when all males had cleaned the velvet from their antlers and ended on the last day before matings were first observed, while the rut refers to the period between the first and last matings. Overall, socially mature males (≥4yr old) were involved in more interactions than immature (≤3yr old) males. Males established dominance rank largely by non-contact agonistic interactions during the pre-rut and there was substantial carry-over of rank to the rut, when it was correlated with mating success. The mating success of males was skewed; mature males achieved 99.4% of the matings and immature males accounted for 0.6%. A mature male was 13 times more likely to fight than an immature male; the mature males that fought most often did so between 0.4 and 0.5 times per hour. During the rut, the number of fights was positively correlated across days with the number of matings. The majority of agonistic interactions (79%) comprising dyads of immature males, involved antler contact. In contrast, mature males engaged antlers in only 42% of their interactions. Fights between mature males lasted more than twice as long as those between immature males and were more likely to occur between opponents with similar dominance ranks. However, towards the end of the rut formerly mismatched opponents were more likely to fight. Thus males operated conditional competitive strategies to decide when to interact and fight. The persistence of rank order from the pre-rut period to the rut and the tendency for mature males to resolve disputes without antler contact, served to reduce the frequency of fights and therefore the risk of serious injury.