Sanje Mangabey Research Articles

Calibrating occupancy to density estimations to assess abundance and vulnerability of a threatened primate in Tanzania

AbstractThe current decline of mammals worldwide makes quantitative population assessments crucial, especially for range‐restricted and threatened species. However, robust abundance estimations are challenging for elusive or otherwise difficult to detect species. Alternative metrics requiring only presence/absence data, that is, occupancy, are possible but calibration with independent density estimates should be foreseen, although rarely performed. Here, we calibrated density estimates from acoustic surveys to occupancy estimates from camera‐trapping detections to derive the abundance of the endangered Sanje mangabey (Cercocebus sanjei) across its entire range in the Udzungwa Mountains of Tanzania. We found marked occupancy–density relationships for the two forest blocks where this primate occurs and used them to derive spatially explicit density estimates. Occupancy increased in montane forest zones at mid‐elevation but decreased slightly with proximity to forest borders. We predicted an average density (±SE) of 0.26 ± 0.05 groups/km2in the national park and 0.24 ± 0.06 in the nature reserve. Accordingly, and given the much larger area of the reserve, the average predicted individual abundance was 1555 ± 325 and 2471 ± 571 in the national park and nature reserve, respectively. We found higher density and abundance in the nature reserve compared with previous studies. Given the past disturbance and poorer protection in the nature reserve relative to the national park, our results instill optimism for the status of the species, although occupancy analysis highlighted the potential vulnerability of this primate to human disturbance. Our approach appears valuable for spatially explicit density estimations of elusive species, and provides robust assessments of vulnerability and identification of priority areas for conservation of threatened populations.

Estimating the population size of the Sanje mangabey (Cercocebus sanjei) using acoustic distance sampling.

The Sanje mangabey (Cercocebus sanjei) is endemic to the Udzungwa Mountains, Tanzania, and is classified as Endangered due to its putatively declining population size, habitat degradation and fragmentation. Previous population size estimates have ranged from 1,350 to 3,500 individuals, with the last direct survey being conducted 15 years before the present study. Previous estimates are now thought to have underestimated the population due to a limited knowledge of group and habitat size, nonsystematic approaches and the use of visual methods that are not suitable for surveying the Sanje mangabey with its semi-terrestrial and elusive behaviors. We used an acoustic survey method with observers recording the distinctive "whoop-gobble" vocalization produced by mangabeys and point transect distance sampling to model a detection function and estimate abundance. Twenty-eight surveys were conducted throughout the two forests where Sanje mangabeys are found: Mwanihana forest in the Udzungwa Mountains National Park (n = 13), and the Uzungwa Scarp Nature Reserve (n = 15). Group density was found to be significantly lower in the relatively unprotected Uzungwa Scarp forest (0.15 groups/km2 ; 95% CI: 0.08-0.27) compared to the well-protected Mwanihana forest (0.29 groups/km2 ; 95% CI: 0.19-0.43; p = .03). We estimate that there are 1,712 (95% CI: 1,141-2,567) individuals in Mwanihana and 1,455 (95% CI: 783-2,702) in the Uzungwa Scarp, resulting in a total population size of 3,167 (95% CI: 2,181-4,596) individuals. The difference in group density between sites is likely a result of the differing protection status and levels of enforcement between the forests, suggesting that protection of the Uzungwa Scarp should be increased to encourage recovery of the population, and reduce the threat of degradation and hunting. Our results contribute to the reassessment of the species' IUCN Red List status and informing management and conservation action planning.

Exaggerated Sexual Swellings and the Probability of Conception in Wild Sanje Mangabeys (Cercocebus sanjei)

Females of several catarrhine primate species exhibit exaggerated sexual swellings that change in size and coloration during the menstrual cycle and, in some species, gestation. Although their function remains under debate, studies indicate that swellings may contain information males could use to discern ovulation and the probability that a cycle will be conceptive. Here we combine visual ratings of swellings with hormonal data for a group of Sanje mangabeys (18 adult, 3 adolescent females) to determine if their swellings provide reliable information on female fertility. In all cases where ovulation was detected (N = 7), it occurred during maximum tumescence, and in 83.3% during the first two days of the “shiny phase,” a period during maximum tumescence when the swelling was brightest. There were no significant differences in maximum tumescence and shiny phase duration among cycles of different probability of conception, although there was a trend toward conceptive cycles exhibiting shorter shiny phases than nonconceptive ones. Only 25% (N = 4) of postconceptive swellings developed the shiny phase, and adolescents displayed the longest maximum tumescence and shiny phases. The conspicuous nature of the shiny phase and the frequent overlap between its onset and ovulation suggest that its presence serves as a general signal of ovulation and that the cycle has a high probability of being conceptive. It also suggests that swellings in some Sanje mangabeys are more accurate signals of fertility than in other primates.

Consequences of a male takeover on mating skew in wild Sanje mangabeys.

Among primate species living in multimale-multifemale groups, the number of receptive females may determine the rank of the lowest male that copulates (priority of access model, or PoA [Altmann SA. 1962. A field study of the sociobiology of rhesus monkeys, Macaca mulatta. Annals of the New York Academy of Sciences 102:338-435]). Factors, such as temporary instability in the hierarchy and female behavior can, however, affect high-ranking males' ability to monopolize females, reducing mating skew and causing the hierarchy to depart from predictions of PoA. Here, I use behavioral data collected over a 22-month period on a wild group of Sanje mangabeys (Cercocebus sanjei) to examine the effect of a takeover by two immigrating males who became α and β in the hierarchy, and of female behavior on male mating skew. Data on male agonistic interactions were collected on nine males using ad libitum observations, while information on male mating success (i.e., daily proportion of ejaculatory copulations with the focal female) was collected through focal follows of 12 sexually receptive females. Before the takeover, the hierarchy was stable and highly skewed, with the α-male monopolizing up to 75% of copulations. At this time, however, mating skew did not follow the predictions of PoA. During the takeover, from the time one of the newly immigrant males replaced the α until the second immigrant male became the new β, the stability of the hierarchy dropped significantly and mating was no longer skewed. Accordingly, the top two ranking males at that time (i.e., the new α and former β) accounted for only 33% of copulations. After the takeover, rank stability increased, and mating skew followed the PoA. Female mating solicitations also had a significant positive effect on male mating success, and may have contributed to the deviation from the PoA. This study demonstrates that temporary rank instability decreases high-ranking males' ability to monopolize copulations, causing a departure from the predictions of the PoA. Am. J. Primatol. 79:e22532, 2017. © 2016 Wiley Periodicals, Inc.

Estimating species richness and modelling habitat preferences of tropical forest mammals from camera trap data.

Medium-to-large mammals within tropical forests represent a rich and functionally diversified component of this biome; however, they continue to be threatened by hunting and habitat loss. Assessing these communities implies studying species’ richness and composition, and determining a state variable of species abundance in order to infer changes in species distribution and habitat associations. The Tropical Ecology, Assessment and Monitoring (TEAM) network fills a chronic gap in standardized data collection by implementing a systematic monitoring framework of biodiversity, including mammal communities, across several sites. In this study, we used TEAM camera trap data collected in the Udzungwa Mountains of Tanzania, an area of exceptional importance for mammal diversity, to propose an example of a baseline assessment of species’ occupancy. We used 60 camera trap locations and cumulated 1,818 camera days in 2009. Sampling yielded 10,647 images of 26 species of mammals. We estimated that a minimum of 32 species are in fact present, matching available knowledge from other sources. Estimated species richness at camera sites did not vary with a suite of habitat covariates derived from remote sensing, however the detection probability varied with functional guilds, with herbivores being more detectable than other guilds. Species-specific occupancy modelling revealed novel ecological knowledge for the 11 most detected species, highlighting patterns such as ‘montane forest dwellers’, e.g. the endemic Sanje mangabey (Cercocebus sanjei), and ‘lowland forest dwellers’, e.g. suni antelope (Neotragus moschatus). Our results show that the analysis of camera trap data with account for imperfect detection can provide a solid ecological assessment of mammal communities that can be systematically replicated across sites.

Reproductive characteristics of wild Sanje mangabeys (Cercocebus sanjei).

An accurate description of reproductive characteristics and ovarian endocrinology is necessary to address questions about the reproductive strategies and life history of a species and for meaningful, cross species analyses. Here we used analysis of fecal estradiol (fE) and behavioral observations to determine for the first time the reproductive characteristics and endocrinology of a wild group (N = 18 adult and 3 adolescent females) of Sanje mangabeys (Cercocebus sanjei). The study was conducted in the Udzungwa Mountains National Park, Tanzania, from October 2008 through September 2010. Average cycle length (±SD) was 29.3 ± 3.2 days in adults and 51.4 ± 5.5 days in adolescents. Menses appeared within 5.1 ± 2.1 days in adults and 4.8 ± 0.3 days in adolescents after the end of maximum tumescence, and lasted 6.7 ± 3.1 and 10.3 ± 5.0 days, respectively. Infant death tended to reduce the number of cycles to conception (4.3 ± 1.5 cycles after a surviving infant vs. 2.6 ± 1.0 cycles after infant death). Adolescents cycled for at least 16 months without conceiving. Implantation bleeding began 17.5 ± 0.7 days from the onset of detumescence, and lasted 10.0 ± 1.4 days. Gestation length averaged 171.8 ± 3.4 days. Postpartum amenorrhea lasted 6.7 ± 2.3 months while females whose infants had died resumed cycling within 14.3 ± 5.9 days. The interbirth interval after a surviving infant averaged 20.0 ± 4.3 months. These reproductive characteristics of the Sanje mangabey resembled those of other mangabeys and related cercopithecines, with the exception of an earlier onset and longer duration of menstruation and implantation bleeding. Further information on the physiology of the Sanje mangabey is needed to clarify what factors may cause the unusual characteristics of both, their menses and implantation bleeding.

Ecology of reproduction in Sanje mangabeys (Cercocebus sanjei): Dietary strategies and energetic condition during a high fruit period

The ability to increase energy storage when food is abundant for later use during late gestation and early lactation is often considered the primary benefit of the capital breeding strategy (clustering conceptions during high food periods, HFP) that promotes reproductive success among females living in unpredictable environments. Capital breeding, however, may also enable preconceptive females to increase hormone production for ovulation, which has been linked to energetic condition in capital breeders, and/or allow females entering the subsequent HFP to increase their energetic condition in order to continue nursing unweaned infants. Here, we investigate whether capital breeding provides these additional benefits in 16 female Sanje mangabeys (Cercocebus sanjei) and determine the dietary strategies used to increase energetic condition (measured by urinary C-peptide: UCP) during the HFP. Fecal estradiol (fE2 ) and UCP were negatively correlated with number of cycles before conception (r = -0.591, r = -0.646, P < 0.01) and were highest in conceptive cycles. Both peri-conceptive (preconception and early gestation) and non-peri-conceptive (lactation) females increased energetic condition over the HFP (r = 0.612, r = 0.583, P < 0.001) by increasing dietary fat (r = 0.619, r = 0.703, P < 0.001) and, for non-peri-conceptive females, protein (r = 0.437, P < 0.001). Feeding intake rate (FIR) and time spent foraging and feeding did not change over the HFP; however, non-peri-conceptive females exhibited a faster FIR compared to peri-conceptive females (t = -2.324, P < 0.05), consuming almost twice as much food per unit time. The results of this study confirm that Sanje mangabeys benefit in multiple phases of the reproductive cycle by using capital breeding, which may explain how this strategy promotes female reproductive success.

Reproductive seasonality in wild Sanje mangabeys (Cercocebus sanjei), Tanzania: Relationship between the capital breeding strategy and infant survival

The reproductive seasonality model states that it is adaptive for species in seasonally variable environments to temporally cluster reproductive events around periods of resource availability. Many studies have examined links between seasonal reproduction and phenological events, though few studies have fully tested the adaptive hypothesis by examining the effects of reproductive timing on outcomes. Our study tests the predictions of the model in an African cercopithecine, the Sanje mangabey, by examining the impact of food availability on the timing of conception, birth and weaning, and the relationship of reproductive timing and female energy balance (urinary C-peptide) to infant survival. From September 2008 through 2010, 28 infants were born. Distribution of conceptions was non-uniform, with a peak between January and March. There was a significant positive correlation between mean monthly fruit availability and number of conceptions per month. An increased food supply supports a positive energy balance, maximizing the potential for conception; a pattern found among many cercopithecines. Mothers that conceived within the peak period also exhibited higher levels of urinary C-peptide during preconception and early gestation, compared to conceptions outside the peak period. This strategy increased the probability of survival to year one, as it was significantly higher for infants conceived during the peak conceptive season. These results support the reproductive seasonality model and demonstrate that the timing of conception is critical for mangabey reproductive success.

The biological importance of the Eastern Arc Mountains of Tanzania and Kenya

The Eastern Arc Mountains are renown in Africa for high concentrations of endemic species of animals and plants. Thirteen separate mountain blocks comprise the Eastern Arc, supporting around 3300 km 2 of sub-montane, montane and upper montane forest, less than 30% of the estimated original forested area. At least 96 vertebrate species are endemic, split as follows: 10 mammal, 19 bird, 29 reptile and 38 amphibian species. This includes four endemic or nearly endemic species of primate – the Sanje Mangabey, the Iringa Red Colobus, the Mountain Galago and the new Kipunji monkey that forms its own monotypic genus. A further 71 vertebrate species are near-endemic. At least 800 vascular plant species are endemic, almost 10% of these being trees. These endemics include the majority of the species of African violet – Saintpaulia, a well-known flowering plant in Western households. An additional 32 species of bryophytes are also endemic. Many hundreds of invertebrates are also likely to be endemic, with data for butterflies, millipedes and dragonflies indicating potential trends in importance. Seventy-one of the endemic or near-endemic vertebrates are threatened by extinction (8 critical, 27 endangered, 36 vulnerable), with an additional seven wide ranging threatened species. Hundreds of plant species are also threatened. Most Eastern Arc endemics are closed-forest specialists and comprise taxa with an ancient history and those of more recent origin, including some possessing ancient affinities with taxa from West Africa, Madagascar, and even South America and Southeast Asia. Mountain block prioritisation for biodiversity conservation shows that Udzungwas, East Usambaras and Ulugurus are the most important blocks, with other important blocks being the Ngurus and West Usambaras. Rankings are correlated closely with the area of remaining forest. Most of the remaining forest is found within nearly 150 Government Forest Reserves, with 106 of these managed nationally for water catchment, biodiversity and soil conservation and where forest exploitation is not allowed. Outside these areas most forest has been cleared, except in small village burial/sacred sites, a few Village Forest Reserves, and inaccessible areas. In most Eastern Arc Mountains the local populations have not encroached beyond the reserve boundaries to develop farms, but forest resources within the boundaries are used for fuel and building materials and some forests are heavily degraded. Fire is also a problem as it enters and destroys forests during the dry seasons. The future of the biodiversity on the Eastern Arc Mountains is closely tied to management policies and capacity of the Tanzania Forestry and Beekeeping Division, Tanzania National Parks Authority, and Kenya Forest Department. Supporting these agencies in their mandated job is an essential conservation investment over the longer term.

Sanje Mangabey Cercocebus sanjei Kills an African Crowned Eagle Stephanoaetus coronatus

We present the first ever reported observations of a hunting African crowned eagle Stephanoaetus coronatus being killed by a primate, in the Udzungwa Mountains of south-central Tanzania. An adult female eagle launched an attack on a young Sanje mangabey Cercocebus sanjei who was feeding in a tree, but was intercepted and bitten by an adult mangabey who was feeding nearby. The adult mangabey and the eagle then fell together 25 m to the forest floor below. The eagle subsequently died from her injuries, while the mangabey escaped and is thought to have survived. This rare event is briefly discussed in the context of previous accounts of primate-crowned eagle interactions.

Protective Status, Ecology and Strategies for Improving Conservation of Cercocebus sanjei in the Udzungwa Mountains, Tanzania

Sanje mangabeys (Cercocebus sanjei), first described in 1981, are among the most endangered primates in the world. They are endemic to the Udzungwa Mountains of Tanzania, in a biogeographic region designated one of the world’s biodiversity hotspots. Conservation research since 1997 has documented the presence of the mangabey in only 3 of the relict montane forest blocks of the Udzungwas. The total population, possibly < 1,500 animals, is fragmented and not adequately protected. A substantial proportion (perhaps 40%) live in forest reserves outside the protective confines of the Udzungwa Mountains National Park, and they are affected by habitat loss and hunting. Efforts to improve their conservation status include assessment of distribution, relative abundance, and habitat quality, and initiation of observational research with habituated individuals to acquire critically important data on their habitat requirements, diet, movement patterns, socioecology, and community ecology. These interrelated research activities should contribute to effective management for conservation, provide baseline information to support current efforts to expand the boundaries of the national park, and guide potential future establishment of corridors between the major forests known to support mangabey groups.