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Vocal acoustics in the endangered proboscis monkey (Nasalis larvatus)

Röper KM, Scheumann M, Wiechert AB, Nathan S, Goossens B, Owren MJ, et al.

Am J Primatol, 2014 Feb;76(2):192-201.
PMID: 24123122 DOI: 10.1002/ajp.22221

The endangered proboscis monkey (Nasalis larvatus) is a sexually highly dimorphic Old World primate endemic to the island of Borneo. Previous studies focused mainly on its ecology and behavior, but knowledge of its vocalizations is limited. The present study provides quantified information on vocal rate and on the vocal acoustics of the prominent calls of this species. We audio-recorded vocal behavior of 10 groups over two 4-month periods at the Lower Kinabatangan Wildlife Sanctuary in Sabah, Borneo. We observed monkeys and recorded calls in evening and morning sessions at sleeping trees along riverbanks. We found no differences in the vocal rate between evening and morning observation sessions. Based on multiparametric analysis, we identified acoustic features of the four common call-types "shrieks," "honks," "roars," and "brays." "Chorus" events were also noted in which multiple callers produced a mix of vocalizations. The four call-types were distinguishable based on a combination of fundamental frequency variation, call duration, and degree of voicing. Three of the call-types can be considered as "loud calls" and are therefore deemed promising candidates for non-invasive, vocalization-based monitoring of proboscis monkeys for conservation purposes.
Fulltext Fecal parasite risk in the endangered proboscis monkey is higher in an anthropogenically managed forest environment compared to a riparian rain forest in Sabah, Borneo

Klaus A, Strube C, Röper KM, Radespiel U, Schaarschmidt F, Nathan S, et al.

PLoS One, 2018;13(4):e0195584.
PMID: 29630671 DOI: 10.1371/journal.pone.0195584

Understanding determinants shaping infection risk of endangered wildlife is a major topic in conservation medicine. The proboscis monkey, Nasalis larvatus, an endemic primate flagship species for conservation in Borneo, is endangered through habitat loss, but can still be found in riparian lowland and mangrove forests, and in some protected areas. To assess socioecological and anthropogenic influence on intestinal helminth infections in N. larvatus, 724 fecal samples of harem and bachelor groups, varying in size and the number of juveniles, were collected between June and October 2012 from two study sites in Malaysian Borneo: 634 samples were obtained from groups inhabiting the Lower Kinabatangan Wildlife Sanctuary (LKWS), 90 samples were collected from groups of the Labuk Bay Proboscis Monkey Sanctuary (LBPMS), where monkeys are fed on stationary feeding platforms. Parasite risk was quantified by intestinal helminth prevalence, host parasite species richness (PSR), and eggs per gram feces (epg). Generalized linear mixed effect models were applied to explore whether study site, group type, group size, the number of juveniles per group, and sampling month predict parasite risk. At the LBPMS, prevalence and epg of Trichuris spp., strongylids, and Strongyloides spp. but not Ascaris spp., as well as host PSR were significantly elevated. Only for Strongyloides spp., prevalence showed significant changes between months; at both sites, the beginning rainy season with increased precipitation was linked to higher prevalence, suggesting the external life cycle of Strongyloides spp. to benefit from humidity. Higher prevalence, epgs, and PSR within the LBPMS suggest that anthropogenic factors shape host infection risk more than socioecological factors, most likely via higher re-infection rates and chronic stress. Noninvasive measurement of fecal parasite stages is an important tool for assessing transmission dynamics and infection risks for endangered tropical wildlife. Findings will contribute to healthcare management in nature and in anthropogenically managed environments.
Fulltext Dispersal and genetic structure in a tropical small mammal, the Bornean tree shrew (Tupaia longipes), in a fragmented landscape along the Kinabatangan River, Sabah, Malaysia

Brunke J, Russo IM, Orozco-terWengel P, Zimmermann E, Bruford MW, Goossens B, et al.

BMC Genet, 2020 04 17;21(1):43.
PMID: 32303177 DOI: 10.1186/s12863-020-00849-z

BACKGROUND: Constraints in migratory capabilities, such as the disruption of gene flow and genetic connectivity caused by habitat fragmentation, are known to affect genetic diversity and the long-term persistence of populations. Although negative population trends due to ongoing forest loss are widespread, the consequence of habitat fragmentation on genetic diversity, gene flow and genetic structure has rarely been investigated in Bornean small mammals. To fill this gap in knowledge, we used nuclear and mitochondrial DNA markers to assess genetic diversity, gene flow and the genetic structure in the Bornean tree shrew, Tupaia longipes, that inhabits forest fragments of the Lower Kinabatangan Wildlife Sanctuary, Sabah. Furthermore, we used these markers to assess dispersal regimes in male and female T. longipes.
RESULTS: In addition to the Kinabatangan River, a known barrier for dispersal in tree shrews, the heterogeneous landscape along the riverbanks affected the genetic structure in this species. Specifically, while in larger connected forest fragments along the northern riverbank genetic connectivity was relatively undisturbed, patterns of genetic differentiation and the distribution of mitochondrial haplotypes in a local scale indicated reduced migration on the strongly fragmented southern riverside. Especially, oil palm plantations seem to negatively affect dispersal in T. longipes. Clear sex-biased dispersal was not detected based on relatedness, assignment tests, and haplotype diversity.
CONCLUSION: This study revealed the importance of landscape connectivity to maintain migration and gene flow between fragmented populations, and to ensure the long-term persistence of species in anthropogenically disturbed landscapes.
Fulltext Co-infection patterns of intestinal parasites in arboreal primates (proboscis monkeys, Nasalis larvatus) in Borneo

Klaus A, Zimmermann E, Röper KM, Radespiel U, Nathan S, Goossens B, et al.

Int J Parasitol Parasites Wildl, 2017 Dec;6(3):320-329.
PMID: 29988805 DOI: 10.1016/j.ijppaw.2017.09.005

Non-human primates of South-East Asia remain under-studied concerning parasite epidemiology and co-infection patterns. Simultaneously, efforts in conservation demand knowledge of parasite abundance and biodiversity in threatened species. The Endangered proboscis monkey, Nasalis larvatus, a primate flagship species for conservation in Borneo, was investigated in the present study. Habitat loss and fragmentation are among the greatest threats to bachelor and harem groups of this folivorous colobine. Designed as a follow-up study, prevalence and co-infection status of intestinal parasites from N. larvatus in a protected area in Malaysian Borneo were analyzed from fecal samples using a flotation method. For the first time, the intestinal parasite co-infection patterns were examined using quantitative analyses. Overall, 92.3% of fecal samples (N = 652) were positive for helminth eggs. Five helminth groups were detected: (1) trichurids (82.7% prevalence) including Trichuris spp. (82.1%) and Anatrichosoma spp. (1.4%), (2) strongyles (58.9%) including Trichostrongylus spp. (48.5%) and Oesophagostomum/Ternidens spp. (22.8%), (3) Strongyloides fuelleborni (32.7%), (4) Ascaris lumbricoides (8.6%), and (5) Enterobius spp. (5.5%). On average, an individual was co-infected with two different groups. Significant positive associations were found for co-infections of trichurids with strongyles and S. fuelleborni as well as S. fuelleborni with A. lumbricoides and strongyles. This study shows a high prevalence of various gastrointestinal helminths with potential transmission pathways primarily related to soil and with zoonotic relevance in wild proboscis monkeys in their remaining natural habitats. Observed positive associations of trichurids with strongyles and Strongyloides spp. may result from the high prevalence of trichurids. Similarly, positive associations between Strongyloides and Ascaris were found, both of which typically occur predominantly in juvenile hosts. These findings should be considered when proposing conservation actions in altered habitats nearby human settlements and when managing captive populations.