Locomotor ecology of Lepilemur edwardsi and Avahi occidentalis

A well-known principle holds that where food supply is limited, two sympatric species with the same diet, morphology, and behavior will compete, leading to exclusion of one species or differentiation of their ecological niches. Avahi occidentalis and Lepilemur edwardsi are two saltatory, nocturnal folivorous lemurs of similar body size which live sympatrically over much of their range and may often be seen feeding in the same trees. We report a study of their locomotor behavior, carried out in order to determine to what extent locomotion might contribute to niche separation. Avahi lives at a higher level in the forest and is the more committed leaper, with a much larger home range and nightly travel distance, while Lepilemur climbs more and has a very small nightly travel distance. Avahi uses small, low-angled supports more often, while Lepilemur makes more use of large, high-angled supports (however, neither species uses vertical supports at a frequency greater than the availability of such supports in the forest stratum in which they live). Both species tend to land on larger-diameter supports on longer leaps, but Avahi also takes off from larger-diameter supports in longer leaps, reducing loss of energy to the substrate during takeoff. We suggest that the differences in locomotion and ranging behavior between them are consistent with niche differentiation on the basis of food quality, Avahi investing more energy in harvesting better quality but more patchy food, Lepilemur minimizing expenditure in harvesting a less selective, quantitatively poorer diet. Am J Phys Anthropol 104:471–486, 1997. © 1997 Wiley-Liss, Inc.     

The role of scent marking in Lemur catta agonistic behavior

Certain forms of marking behavior in Lemur catta have been considered to be aggressive in nature but had not been analyzed specifically in this respect. This study examines the relationship between the occurrence of all forms of marking behavior displayed by a captive group of lemurs and their physical and nonphysical aggressive interactions. All forms of marking behavior, especially males' tail mark and tail wave displays, were found to correlate with aggressive behavior including female-instigated agonism. In comparison, allogrooming, a behavior thought not to have an agonistic component, was not significantly correlated with any marking nor agonistic category. The data suggest that in intersexual interactions male marking behavior is an aggressive but nonphysical substitute for physical aggression toward females who have generally been regarded as dominant to males in this species.     

圈养马麝刻板行为表达与粪样类固醇激素的关系

2017年7月1日-8月31日及2018年6月1日-7月31日,在甘肃兴隆山保护区马麝繁育中心,采用焦点取样法和连续记录法进行了圈养马麝的刻板行为取样,采集同期粪样,并用放射免疫分析法（RIA）检测粪样中肾上腺皮质醇、睾酮及雌二醇激素的水平,分析了圈养马麝刻板行为表达与上述3种激素水平的关系。结果显示,展现刻板行为的圈养马麝的皮质醇水平（111.099 ± 16.231）ng/g略高于无刻板行为表达的马麝（95.640± 9.738） ng/g,差异未达显著（P> 0.05）;展现刻板行为雄麝的睾酮水平（135.900± 21.582）ng/g略高于无刻板行为的雄麝（108.182 ± 9.689） ng/g,差异也不显著（P> 0.05）;展现刻板行为雌麝的雌二醇水平（0.445 ± 0.116）ng/g显著低于无刻板行为雌麝（10.843 ± 1.142）ng/g（P< 0.05）。研究结果表明,圈养雄性马麝的刻板行为表达与其类固醇激素水平不相关;而雌麝的刻板行为表达与雌二醇分泌显著负相关,这与其繁殖及健康状况有关。在麝类驯养实践中,可将粪样类固醇激素水平（尤其是雌二醇）作为其受胁迫水平及行为健康的监测指标。     

Evidence for social enhancement of reproduction in two Eulemur species

Across the past 20 years, captive reproduction has declined steeply in mongoose lemurs (Eulemur mongoz) and has been only moderately successful in black lemurs (E. macaco). At the same time, reproduction has been so successful in brown lemurs (E. fulvus) that contraception has been used since 1987 to limit captive numbers. No obvious cause for the differential reproductive success has been identified. Our experience with a pair of unrelated mongoose lemurs at the Philadelphia Zoological Garden suggested that they reproduced in only those years when they were caged in close proximity to another nonreproductive, full-sibling pair of mongoose lemurs. Examination of the worldwide pattern of captive reproduction by Eulemur species during the past two decades revealed that female black and mongoose lemurs housed in institutions with either additional conspecific males or additional conspecific pairs had a higher rate of reproduction than those maintained as an isolated pair. Black lemurs also had higher rates of reproduction when additional conspecific females were present. No similar pattern was found for brown lemurs or for two comparable mammals, the pudu (Pudu pudu) and the okapi (Okapia johnstoni). The evidence presented for the black and mongoose lemurs supports the existence of the Allee effect in these two species, namely, that reproduction is enhanced by the presence of conspecifics. © 1996 Wiley-Liss, Inc.     

Evidence for individual vocal differences in Woodland Kingfishers Halcyon senegalensis cyanoleuca

Theoretical criteria have been advanced to describe conditions under which avian species are able to recognise the voices of neighbours, thereby reducing physical conflict. Namely, that the signal should be sufficiently stereotyped to allow species specific recognition but sufficiently varied to allow individual recognition. Although this has been quantitatively demonstrated in many species and genera, one exception is the kingfishers (family Alcedinidae). Here, temporal and frequency measurements from recordings of the territorial calls of nine Woodland Kingfishers Halcyon senegalensis cyanoleuca were analysed to calculate the between-individual and within-individual coefficients of variance. Our results indicate that temporal parameters tend towards individual specificity, with frequency parameters more stereotyped across the species. Multivariate statistics discriminated the nine individuals and identified two components, which accounted for 72.1% of the total variance between individuals. We conclude that a suite of vocal characters in the temporal domain is used to discriminate between individuals in Woodland Kingfishers.     

Functional ecology of feeding in elasmobranchs

Feeding behavior in the species of captive chondrichthyans is studied to clarify the functional mechanisms responsible for feeding ecology. Kinematics and pressure in the buccal, hyoid and pharyngeal regions were quantified in Squalus acanthias, Chiloscyllium plagiosum and Leucoraja erinacea using sonomicrometry and pressure transducers. Means and coefficients of variation were analyzed by species and by behavior to test for stereotypy and flexibility in the feeding mechanism. Several instances of mechanical stereotypy as well as flexibility were found in the feeding kinematics and pressure of the three chondrichthyan species. In general, Squalus acanthias shows more stereotyped feeding behavior than C. plagiosum and L. erinacea. Different aspects of feeding behavior stand out among the three species. Chiloscyllium plagiosum generates lowest pressures, S. acanthias achieves the greatest area changes, and L. erinacea has longer durations for manipulating prey. Capture events are functionally and behaviorally stereotyped while processing events are functionally and behaviorally flexible with the ability to use suction or compression to process the same food item. Squalus acanthias is a functional specialist and C. plagiosum is functionally a generalist, with both species exhibiting behavioral flexibility. Leucoraja erinacea is a functional and behavioral generalist. Using functional morphology to explain mechanical stereotypy and flexibility in the feeding behavior of three suction feeding chondrichthyan species has allowed a better understanding of specialist and generalist trophic behaviors.     

兴隆山自然保护区麝场圈养马麝刻板行为的比较

于2001年3月—2002年1月,采用焦点取样法对甘肃兴隆山自然保护区麝场圈养马麝的刻板行为进行了研究。结果表明:该麝场的圈养马麝有刻板行为的发育,雌麝的刻板行为持续时间少于雄麝,但二者间的差异不显著。野捕马麝幼年期的人工哺乳经历使其刻板行为表达强度相对小于麝场圈养下繁殖马麝。年龄对雌雄麝的刻板行为表达强度的效应相似,亚成体马麝的刻板行为表达较多,成体马麝体的刻板行为表达相对较少,老年马麝刻板行为持续时间最长,2.5和4.5岁是圈养马麝刻板行为发育的关键时期。此外,能顺利繁殖的个体,其刻板行为表达的持续时间少于繁殖失败的个体。     

Introducing a semi-naturalistic exhibit as structural enrichment for two brown bears (Ursus arctos). Does this ensure their captive well-being?

In this study we used the daily activity pattern and use of space as indicators of change in the program of structural enrichment, implemented with 2 subjects of the species Ursus arctos in the Barcelona Zoo. We collected 930 sampling points in each study phase for each of the individuals: The samples were taken in a balanced way at different times of day. We observed a wider range of behavior in the male than the female. With respect to the indicators, we observed statistically significant differences in behavior in both individuals in the 2 study phases. Both individuals showed an increase in vigilance, maintenance, and inactivity when their enclosure was changed. In terms of the subjects' well-being, we considered the percentage of stereotyped behavior within acceptable limits. The percentage of activity observed in the male was very similar to that of individuals of this species in the wild. In terms of the use of space, we observed homogeneity only in the male during the enrichment program. The 2 individuals responded in different ways to the structural enrichment.     

Evolution of Multiple Additive Loci Caused Divergence between Drosophila yakuba and D. santomea in Wing Rowing during Male Courtship

In Drosophila, male flies perform innate, stereotyped courtship behavior. This innate behavior evolves rapidly between fly species, and is likely to have contributed to reproductive isolation and species divergence. We currently understand little about the neurobiological and genetic mechanisms that contributed to the evolution of courtship behavior. Here we describe a novel behavioral difference between the two closely related species D. yakuba and D. santomea: the frequency of wing rowing during courtship. During courtship, D. santomea males repeatedly rotate their wing blades to face forward and then back (rowing), while D. yakuba males rarely row their wings. We found little intraspecific variation in the frequency of wing rowing for both species. We exploited multiplexed shotgun genotyping (MSG) to genotype two backcross populations with a single lane of Illumina sequencing. We performed quantitative trait locus (QTL) mapping using the ancestry information estimated by MSG and found that the species difference in wing rowing mapped to four or five genetically separable regions. We found no evidence that these loci display epistasis. The identified loci all act in the same direction and can account for most of the species difference.     

Effect of feeding boxes on the behavior of stereotyping amur tigers (Panthera tigris altaica) in the Zurich Zoo,Zurich, Switzerland

The stereotyped pacing shown by the two Amur tigers in the Zurich Zoo was hypothesized as being caused by permanently frustrated appetitive foraging behavior. Several electrically controlled feeding boxes were installed and access to each box was possible only twice a day for 15 min at semi‐random times. The boxes had to be opened actively by the tigers. Two trials were carried out: one with solitary confinement, and one with paired confinement. During box feeding, the female's stereotyped pacing was significantly reduced from 16% (solitary confinement, conventional feeding) and 7% (paired confinement, conventional feeding) to 1% (solitary confinement) and less than 0.01% (paired confinement) of the daily observed time. The female's sleeping increased significantly in both solitary and paired confinement. The male only showed a significant reduction in stereotyped pacing behavior when kept with the female (conventional feeding: 10%; box feeding: <0.01% of the daily observed time). On days with a box‐feeding regime in paired confinement, the male spent 25% (83 min) of the observed time with active behavior at the feeding boxes. The results support the hypothesis that permanently frustrated appetitive foraging behavior causes stereotyped pacing in adult tigers. Zoo Biol 21:573–584, 2002. © 2002 Wiley‐Liss, Inc.     

A comparison of auditory brainstem responses and behavioral estimates of hearing sensitivity in Lemur catta and Nycticebus coucang

Primates depend on acoustic signals and cues to avoid predators, locate food, and share information. Accordingly, the structure and function of acoustic stimuli have long been emphasized in studies of primate behavioral and cognitive ecology. Yet, few studies have addressed how well primates hear such stimuli; indeed, the auditory thresholds of most primate species are unknown. This empirical void is due in part to the logistic and economic challenges attendant on traditional behavioral testing methods. Technological advances have produced a safe and cost‐effective alternative—the auditory brainstem response (ABR) method, which can be utilized in field conditions, on virtually any animal species, and without subject training. Here we used the ABR and four methods of threshold determination to construct audiograms for two strepsirrhine primates: the ring‐tailed lemur (Lemur catta) and slow loris (Nycticebus coucang). Next, to verify the general efficacy of the ABR method, we compared our results to published behaviorally‐derived audiograms. We found that the four ABR threshold detection methods produced similar results, including relatively elevated thresholds but similarly shaped audiograms compared to those derived behaviorally. The ABR and behavioral absolute thresholds were significantly correlated, and the frequencies of best sensitivity and high‐frequency limits were comparable. However, at frequencies ≤2 kHz, ABR thresholds were especially elevated, resulting in decreased agreement with behavioral thresholds and, in Lemur, the ABR 10‐dB range starting points were more than 2 octaves higher than the behavioral points. Finally, a comparison of ABR‐ and behaviorally‐derived audiograms from various animal taxa demonstrates the widespread efficacy of the ABR for estimating frequency of best sensitivity, but otherwise suggests caution; factors such as stimulus properties and threshold definition affect results. We conclude that the ABR method is a promising technique for estimating primate hearing sensitivity, but that additional data are required to explore its efficacy for estimating low‐frequency thresholds. Am. J. Primatol. 72:217–233, 2010. © 2009 Wiley‐Liss, Inc.     

The effect of housing and environmental enrichment on stereotyped behavior of adult vervet monkeys (Chlorocebus aethiops)

Little information is available on the response of vervet monkeys to different housing conditions or on the suitability of enrichment devices or methods for vervet monkeys. In this study, the authors evaluated the occurrence of stereotyped behavior in adult vervet monkeys under various conditions of housing and enrichment. The variables included cage size, cage level (upper or lower), enrichment with a foraging log, enrichment with an exercise cage and presence of a mate. The authors first determined the incidence of stereotyped behavior in captive-bred, singly housed adult female and male vervet monkeys. They then exposed monkeys to different housing and enrichment situations and compared the incidence of stereotyped behavior among the monkeys. The authors found that more females than males engaged in stereotyped behavior and that females, on average, engaged in such behavior for longer periods of time than males. Stereotyped behavior was most often associated with a small, single cage. The average amount of observed stereotyped activity in monkeys housed in a small cage was significantly lower when the monkeys had access to either a foraging log or an exercise cage. Stereotyped behavior was also lower in female monkeys that were housed (either with a male or without a male) in a larger cage. The least amount of abnormal behavior was associated with the largest, most complex and enriched housing situation. Males and females housed in cages on the lower level of two-level housing engaged in more stereotyped behavior than did monkeys housed in the upper level, regardless of the presence or type of enrichment provided.     

Visitors excite primates in zoos

Fifteen species of primate were observed to assess the effects of zoo visitors on their social behavior. When visitors were present primates were less affiliative, more active, but more aggressive. These changes were particularly marked in arboreal monkeys, especially in smaller species, and were reduced by 50% by lowering the height of spectators. Detailed observations of a group of mandrills indicated that with increasing numbers of visitors the monkeys showed a linear increase in attention to visitors, in activity, and in stereotyped behavior. All of these effects are consistent with an interpretation that visitors are a source of stressful excitement rather than of enrichment.     

Signature whistles in wild bottlenose dolphins: long-term stability and emission rates

Whistles are key elements in the acoustic repertoire of bottlenose dolphins. In this species, the frequency contours of whistles are used as individual signatures. Assessing the long-lasting stability of such stereotyped signals, and the abundant production of non-stereotyped whistles in the wild, is relevant to a more complete understanding of their biological function. Additionally, studying the effects of group size and activity patterns on whistle emission rate may provide insights into the use of these calls. In this study, we document the decades-long occurrence of whistles with stereotyped frequency contours in a population of wild bottlenose dolphins, resident in the region of the Sado estuary, Portugal. Confirmed stereotypy throughout more than 20 years, and positive identification using the signature identification (SIGID) criteria, suggests that the identified stereotyped whistles are in fact signature whistles. The potential roles of non-stereotyped whistles, which represent 68 % of all whistles recorded, are still unclear and should be further investigated. Emission rates were significantly higher during food-related events. Finally, our data show a comparatively high overall whistle production for this population, and no positive correlation between group size and emission rates, suggesting social or environmental restriction mechanisms in vocal production.     

The role of nocturnal omnivorous lemurs as seed dispersers in Malagasy rain forests

Fruit-eating animals play important roles as seed dispersal agents in terrestrial systems. Yet, the extent to which seed dispersal by nocturnal omnivores may facilitate germination and the recruitment of plant communities has rarely been investigated. Characterizing their roles in seed dispersal is necessary to provide a more complete picture of how seed dispersal processes affect ecosystem functioning. We investigated the roles and impacts of two species of nocturnal omnivorous lemur species, Microcebus jollyae and M. rufus, on seed dispersal in Madagascar's rain forests, through analysis of fecal samples and germination experiments. Data show that these lemur species, which are among the world's smallest primates, dispersed 22 plant species from various forest strata and that the defecated seeds germinated faster and at higher rates than control seeds for the eight plant species we tested. Even though mouse lemurs dispersed both native and non-native plant species, non-native plant species represented a relatively small proportion (17%). These results demonstrate that overlooked nocturnal omnivores can act as important seed dispersers, which may have critical implications for forest regeneration and the maintenance of plant diversity in fragmented/degraded forests. Finally, we provide critical insights into the previously unobserved behavior and diet of endangered nocturnal lemurs for their effective conservation.     

Lateral bias to the leading limb in an olfactory social signal by male ring-tailed lemurs

Because ring-tailed lemurs (Lemur catta) show handedness during feeding, I investigated whether they also show lateral preference in the limbs used by males during scent marking. During a bout of marking, a male alternates a variable number of shoulder rubs and arm marks. It is a complex social signal that has both olfactory and visual components and is frequently part of intrasexual agonistic interactions. I used all-occurrences behavior sampling, manually recorded all totally visible bouts, and required a minimum of 50 bouts per animal. The subjects included six wild and four group-living captive male lemurs. I considered limb usage to be lateralized for each individual lemur if the frequency of use of one side was significantly above chance as determined by binomial z-scores at P<.05. I measured consistency of lateral preference by calculating handedness index (HI) scores for each individual. Overall, I recorded 1,583 bouts of scent marking, and 66% of the bouts began with shoulder rubbing. Eight of the 10 males showed a significant, moderately strong lateral preference for the lead limb in the first shoulder rub performed in a bout, and for six of these eight the preferred lead limb for shoulder rubbing was the left one. Six of the 10 males showed a significant but weak lateral preference in the first arm mark, and five of these preferred the opposite limb to that used for the first shoulder rub. Although the preferences were not at the population level, eight of the 10 lemurs showed a lateral bias in the lead limb used for a component of this complex social signal.     

Effects of food,proximity, and kinship on social behavior in ringtailed lemurs

Efforts to understand the variation in primate social systems and their underlying interaction patterns have focused on both intrinsic and extrinsic factors. In the socioecological model, food distribution and abundance have been argued to be the primary influences on the social behavior of primate species. We examined the relationship of food resources and two intrinsic factors—kinship and proximity—with patterns of affiliative and agonistic relationships in two semi‐free ranging ringtailed lemur, Lemur catta, social groups (N=14) at The Duke Lemur Center in Durham, NC. In analyzing these three factors concurrently within the same system, we attempt to establish their relative power in explaining the characteristics of social relationships. Patterns of affiliation and high‐intensity agonism were best explained by kinship. Proximity also explained affiliation but did not explain agonism, which varied considerably between groups. The influence of food on social interactions was highly variable between the two groups and, therefore, did not convincingly account for the social behavior patterns we observed. Finally, different intensities of agonism have different patterns and should be analyzed individually. The variation between social groups makes it difficult for us to conclude that any one factor is primarily and universally responsible for patterns of social behavior in this species. Am. J. Primatol. 72:981–991, 2010. © 2010 Wiley‐Liss, Inc.     

Food mechanical properties in three sympatric species of Hapalemur in Ranomafana National Park,Madagascar

We investigated mechanical dietary properties of sympatric bamboo lemurs, Hapalemur g. griseus, H. aureus, and H. (Prolemur) simus, in Ranomafana National Park, Madagascar. Each lemur species relies on bamboo, though previous behavioral observations found that they specialize on different parts of a common resource (Tan: Int J Primatol 20 1999 547–566; Tan: PhD dissertation 2000 State University of New York, Stony Brook). On the basis of these earlier behavioral ecology studies, we hypothesized that specialization on bamboo is related to differences in mechanical properties of specific parts. We quantified mechanical properties of individual plant parts from the diets of the bamboo lemur species using a portable tester. The diets of the Hapalemur spp. exhibited high levels of mechanical heterogeneity. The lemurs, however, could be segregated based on the most challenging (i.e., mechanically demanding) foods. Giant bamboo culm pith was the toughest and stiffest food eaten, and its sole lemur consumer, H. simus, had the most challenging diet. However, the mechanical dietary properties of H. simus and H. aureus overlapped considerably. In the cases where lemur species converged on the same bamboo part, the size of the part eaten increased with body size. Plant parts that were harvested orally but not necessarily masticated were the most demanding, indicating that food preparation may place significant loads on the masticatory apparatus. Finally, we describe how mechanical properties can influence feeding behavior. The elaborate procurement processes of H. simus feeding on culm pith and H. griseus and H. aureus feeding on young leaf bases are related to the toughnesses of protective coverings and the lemurs' exploitation of mechanical vulnerabilities in these plants. Am J Phys Anthropol, 2009. © 2008 Wiley‐Liss, Inc.     

Hormonal acceleration of song development illuminates motor control mechanism in canaries

In songbirds, the ontogeny of singing behavior shows strong parallels with human speech learning. As in humans, development of learned vocal behavior requires exposure to an acoustic model of species‐typical vocalizations, and, subsequently, a sensorimotor practice period after which the vocalization is produced in a stereotyped manner. This requires mastering motor instructions driving the vocal organ and the respiratory system. Recently, it was shown that, in the case of canaries (Serinus canaria), the diverse syllables, constituting the song, are generated with air sac pressure patterns with characteristic shapes, remarkably, those belonging to a very specific mathematical family. Here, we treated juvenile canaries with testosterone at the onset of the sensorimotor practice period. This hormone exposure accelerated the development of song into stereotyped adultlike song. After 20 days of testosterone treatment, subsyringeal air sac pressure patterns of song resembled those produced by adults, while those of untreated control birds of the same age did not. Detailed temporal structure and modulation patterns emerged rapidly with testosterone treatment, and all previously identified categories of adult song were observed. This research shows that the known effect of testosterone on the neural circuits gives rise to the stereotyped categories of respiratory motor gestures. Extensive practice of these motor patterns during the sensorimotor phase is not required for their expression. © 2010 Wiley Periodicals, Inc. Develop Neurobiol 70: 943–960, 2010