• Genome-wide SNP loci reveal novel insights into koala (Phascolarctos cinereus) population variability across its range

      Kjeldsen, Shannon R.; Zenger, Kyall R.; Leigh, Kellie; Ellis, William A.; Tobey, Jennifer R.; Phalen, David; Melzer, Alistair; FitzGibbon, Sean; Raadsma, Herman W. (2016)
      The koala (Phascolarctos cinereus) is an iconic Australian species that is currently undergoing a number of threatening processes, including disease and habitat loss. A thorough understanding of population genetic structuring and genomic variability of this species is essential to effectively manage populations across the species range. Using a reduced representation genome sequencing method known as double digest restriction-associated sequencing, this study has provided the first genome-wide SNP marker panel in the koala. In this study, 33,019 loci were identified in the koala and a filtered panel of 3060 high-utility SNP markers, including 95 sex-linked markers, were used to provide key insights into population variability and genomic variation in 171 koalas from eight populations across their geographic range. Broad-scale genetic differentiation between geographically separated populations (including sub-species) was assessed and revealed significant differentiation between all populations (FST range = 0.01–0.28), with the largest divergence observed between the three geographically distant subgroups (QLD, NSW and VIC) along the east coast of Australia (average FST range = 0.17–0.23). Sub-group divergence appears to be a reflection of an isolation by distance effect and sampling strategy rather than true evidence of sub-speciation. This is further supported by low proportions of AMOVA variation between sub-species groups (11.19 %). Fine-scale analysis using genome-wide SNP loci and the NETVIEW pipeline revealed cryptic genetic sub-structuring within localised geographic regions, which corresponded to the hierarchical mating system of the species. High levels of genome-wide SNP heterozygosity were observed amongst all populations (He = 0.25–0.35), and when evaluating across the species to other vertebrate taxa were amongst the highest values observed. This illustrates that the species as a whole still retains high levels of diversity which is comparable to other outbred vertebrate taxa for genome-wide SNPs. Insights into the potential for adaptive variation in the koala were also gained using outlier analysis of genome-wide SNPs. A total of 10 putative outlier SNPs were identified indicating the high likelihood of local adaptations within populations and regions. This is the first use of genome-wide markers to assess population differentiation at a broad-scale in the koala and the first time that sex-linked SNPs have been identified in this species. The application of this novel genomic resource to populations across the species range will provide in-depth information allowing informed conservation priorities and management plans for in situ koalas across Australia and ex situ around the world.
    • Genomic analysis of snub-nosed monkeys (Rhinopithecus) identifies genes and processes related to high-altitude adaptation

      Yu, Li; Wang, Guo-Dong; Ruan, Jue; Chen, Yong-Bin; Yang, Cui-Ping; Cao, Xue; Wu, Hong; Liu, Yan-Hu; Du, Zheng-Lin; Wang, Xiao-Ping; et al. (2016)
      The snub-nosed monkey genus Rhinopithecus includes five closely related species distributed across altitudinal gradients from 800 to 4,500 m. Rhinopithecus bieti, Rhinopithecus roxellana, and Rhinopithecus strykeri inhabit high-altitude habitats, whereas Rhinopithecus brelichi and Rhinopithecus avunculus inhabit lowland regions. We report the de novo whole-genome sequence of R. bieti and genomic sequences for the four other species. Eight shared substitutions were found in six genes related to lung function, DNA repair, and angiogenesis in the high-altitude snub-nosed monkeys. Functional assays showed that the high-altitude variant of CDT1 (Ala537Val) renders cells more resistant to UV irradiation, and the high-altitude variants of RNASE4 (Asn89Lys and Thr128Ile) confer enhanced ability to induce endothelial tube formation in vitro. Genomic scans in the R. bieti and R. roxellana populations identified signatures of selection between and within populations at genes involved in functions relevant to high-altitude adaptation. These results provide valuable insights into the adaptation to high altitude in the snub-nosed monkeys.
    • Genomic comparisons reveal biogeographic and anthropogenic impacts in the koala ( Phascolarctos cinereus ): a dietary-specialist species distributed across heterogeneous environments

      Kjeldsen, Shannon R.; Raadsma, Herman W.; Leigh, Kellie A.; Tobey, Jennifer R.; Phalen, David; Krockenberger, Andrew; Ellis, William A.; Hynes, Emily; Higgins, Damien P.; Zenger, Kyall R. (2018)
      The Australian koala is an iconic marsupial with highly specific dietary requirements distributed across heterogeneous environments, over a large geographic range. The distribution and genetic structure of koala populations has been heavily influenced by human actions, specifically habitat modification, hunting and translocation of koalas. There is currently limited information on population diversity and gene flow at a species-wide scale, or with consideration to the potential impacts of local adaptation. Using species-wide sampling across heterogeneous environments, and high-density genome-wide markers (SNPs and PAVs), we show that most koala populations display levels of diversity comparable to other outbred species, except for those populations impacted by population reductions. Genetic clustering analysis and phylogenetic reconstruction reveals a lack of support for current taxonomic classification of three koala subspecies, with only a single evolutionary significant unit supported. Furthermore, ~70% of genetic variance is accounted for at the individual level. The Sydney Basin region is highlighted as a unique reservoir of genetic diversity, having higher diversity levels (i.e., Blue Mountains region; AvHecorr=0.20, PL%?=?68.6). Broad-scale population differentiation is primarily driven by an isolation by distance genetic structure model (49% of genetic variance), with clinal local adaptation corresponding to habitat bioregions. Signatures of selection were detected between bioregions, with no single region returning evidence of strong selection. The results of this study show that although the koala is widely considered to be a dietary-specialist species, this apparent specialisation has not limited the koala’s ability to maintain gene flow and adapt across divergent environments as long as the required food source is available.
    • Geographic comparison of plant genera used in frugivory among the pitheciids Cacajao, Callicebus, Chiropotes, and Pithecia

      Boyle, Sarah A.; Thompson, Cynthia L.; Deluycker, Anneke; Alvarez, Silvia J.; Alvim, Thiago H.G.; Aquino, Rolando; Bezerra, Bruna M.; Boubli, Jean P.; Bowler, Mark; Caselli, Christini Barbosa; et al. (2016)
      Pitheciids are known for their frugivorous diets, but there has been no broad-scale comparison of fruit genera used by these primates that range across five geographic regions in South America. We compiled 31 fruit lists from data collected from 18 species (three Cacajao, six Callicebus, five Chiropotes, and four Pithecia) at 26 study sites in six countries. Together, these lists contained 455 plant genera from 96 families. We predicted that 1) closely related Chiropotes and Cacajao would demonstrate the greatest similarity in fruit lists; 2) pitheciids living in closer geographic proximity would have greater similarities in fruit lists; and 3) fruit genus richness would be lower in lists from forest fragments than continuous forests. Fruit genus richness was greatest for the composite Chiropotes list, even though Pithecia had the greatest overall sampling effort. We also found that the Callicebus composite fruit list had lower similarity scores in comparison with the composite food lists of the other three genera (both within and between geographic areas). Chiropotes and Pithecia showed strongest similarities in fruit lists, followed by sister taxa Chiropotes and Cacajao. Overall, pitheciids in closer proximity had more similarities in their fruit list, and this pattern was evident in the fruit lists for both Callicebus and Chiropotes. There was no difference in the number of fruit genera used by pitheciids in habitat fragments and continuous forest. Our findings demonstrate that pitheciids use a variety of fruit genera, but phylogenetic and geographic patterns in fruit use are not consistent across all pitheciid genera. This study represents the most extensive examination of pitheciid fruit consumption to date, but future research is needed to investigate the extent to which the trends in fruit genus richness noted here are attributable to habitat differences among study sites, differences in feeding ecology, or a combination of both. Am. J. Primatol. 78:493–506, 2016. © 2015 Wiley Periodicals, Inc.
    • Giant otters: using knowledge of life history for conservation

      Groenendijk, Jessica; Hajek, Frank; Johnson, Paul; Macdonald, David W.; Macdonald, David W.; Newman, Chris; Harrington, Lauren A. (Oxford University PressOxford, UK, 2017)
    • Giant panda distributional and habitat-use shifts in a changing landscape

      Wei, Wei; Swaisgood, Ronald R.; Dai, Qiang; Yang, Zhisong; Yuan, Shibin; Owen, Megan A.; Pilfold, Nicholas W.; Yang, Xuyu; Gu, Xiaodong; Zhou, Hong; et al. (2018)
      Long‐term data on populations, threats, and habitat‐use changes are fundamentally important for conservation policy and management decisions affecting species, but these data are often in short supply. Here, we analyze survey data from 57,087 plots collected in approximately three‐fourths of the giant panda's (Ailuropoda melanoleuca) distributional range during China's national surveys conducted in 1999–2003 and 2011–2014. Pandas associated preferentially with several ecological factors and avoided areas impacted by human activities, such as roads, livestock, mining, and tourism. Promise is shown by dramatic declines in logging rates, but is counterbalanced with recently emerging threats. Pandas have increasingly utilized secondary forest as these forests recovered under protective measures. Pandas have undergone a distributional shift to higher elevations, despite the elevational stability of their bamboo food source, perhaps in response to a similar upward shift in the distribution of livestock. Our findings showcase robust on‐the‐ground data from one of the largest‐scale survey efforts worldwide for an endangered species and highlight how science and policy have contributed to this remarkable success story, and help frame future management strategies.
    • Giant pandas a beacon for hope at World Conservation Congress

      Garshelis, Dave; Swaisgood, Ronald R.; Dajun Wang; Steinmetz, Rob (2016)
    • Giant pandas use odor cues to discriminate kin from nonkin

      Gilad, Oranit; Swaisgood, Ronald R.; Owen, Megan A.; Zhou, Xiaoping (2016)
      Sociality is an important factor in both the mechanism and function of kin recognition, yet it is little explored in solitary species. While there may be future opportunities for nepotistic functions of kin discrimination among solitary species, the ability to discriminate kin from nonkin may still have important roles in social regulation. The solitary giant panda Ailuropoda melanoleuca offers a good model system to explore kin discrimination in a solitary mammal. As kin discrimination in many other mammals is olfactorily mediated, we investigated whether giant pandas are able to discriminate odor cues from daughters even after months and years of separation. Our results indicate that giant pandas are capable of discriminating between kin and nonkin using odor cues available in urine and body odor. Daughters preferentially investigated the odors of unrelated adult female pandas over the odors of their mothers, and mothers spent more time investigating the odors of unrelated age-matched female pandas over those from their daughters. Because these studies were conducted months or years after the mother–daughter period of dependency ended, it is still unclear what mechanism is used for recognition. Long-term olfactory memories and phenotype matching should both be considered, and further studies are required for such determination.
    • Glucocorticoid measurement in plasma, urates, and feathers from California condors (Gymnogyps californianus) in response to a human-induced stressor

      Glucs, Zeka E.; Smith, Donald R.; Tubbs, Christopher W.; Scherbinski, Jennie Jones; Welch, Alacia; Burnett, Joseph; Clark, Michael; Eng, Curtis; Finkelstein, Myra E. (2018)
      Vertebrates respond to stressful stimuli with the secretion of glucocorticoid (GC) hormones, such as corticosterone (CORT), and measurements of these hormones in wild species can provide insight into physiological responses to environmental and human-induced stressors. California condors (Gymnogyps californianus) are a critically endangered and intensively managed avian species for which information on GC response to stress is lacking. Here we evaluated a commercially available I125 double antibody radioimmunoassay (RIA) and an enzyme-linked immunosorbent assay (ELISA) kit for measurement of CORT and GC metabolites (GCM) in California condor plasma, urate, and feather samples. The precision and accuracy of the RIA assay outperformed the ELISA for CORT and GCM measurements, and CORT and GCM values were not comparable between the two assays for any sample type. RIA measurements of total CORT in condor plasma collected from 41 condors within 15 minutes of a handling stressor were highly variable (median = 70 ng/mL, range = 1–189 ng/mL) and significantly different between wild and captive condors (p = 0.02, two-tailed t-test, n = 10 wild and 11 captive). Urate GCM levels (median = 620 ng/g dry wt., range = 0.74–7200 ng/g dry wt., n = 216) significantly increased within 2 hr of the acute handling stressor (p = 0.032, n = 11 condors, one-tailed paired t-test), while feather section CORT concentrations (median = 18 pg/mm, range = 6.3–68 ng/g, n = 37) also varied widely within and between feathers. Comparison of multiple regression linear models shows condor age as a significant predictors of plasma CORT levels, while age, sex, and plasma CORT levels predicted GCM levels in urates collected within 30 min of the start of handling. Our findings highlight the need for validation when selecting an immunoassay for use with a new species, and suggest that non-invasively collected urates and feathers hold promise for assessing condor responses to acute or chronic environmental and human-induced stressors.
    • Grand Cayman Blue Iguana (Cyclura lewisi) AZA Animal Program Population Viability Analysis Report.

      Mechak, L.; Grant, Tandora D.; Krebs, J. (Associaton of Zoos and Aquariums, 2015)
    • Great ape genetic diversity and population history

      Prado-Martinez, Javier; Sudmant, Peter H.; Kidd, Jeffrey M.; Li, Heng; Kelley, Joanna L.; Lorente-Galdos, Belen; Veeramah, Krishna R.; Woerner, August E.; O’Connor, Timothy D.; Santpere, Gabriel; et al. (2013)
      Most great ape genetic variation remains uncharacterized; however, its study is critical for understanding population history, recombination, selection and susceptibility to disease. Here we sequence to high coverage a total of 79 wild- and captive-born individuals representing all six great ape species and seven subspecies and report 88.8 million single nucleotide polymorphisms. Our analysis provides support for genetically distinct populations within each species, signals of gene flow, and the split of common chimpanzees into two distinct groups: Nigeria–Cameroon/western and central/eastern populations. We find extensive inbreeding in almost all wild populations, with eastern gorillas being the most extreme. Inferred effective population sizes have varied radically over time in different lineages and this appears to have a profound effect on the genetic diversity at, or close to, genes in almost all species. We discover and assign 1,982 loss-of-function variants throughout the human and great ape lineages, determining that the rate of gene loss has not been different in the human branch compared to other internal branches in the great ape phylogeny. This comprehensive catalogue of great ape genome diversity provides a framework for understanding evolution and a resource for more effective management of wild and captive great ape populations.
    • Groundwork for effective conservation education: an example of in situ and ex situ collaboration in South East Asia

      Crudge, B.; O'Connor, David; Hunt, M.; Davis, Elizabeth Oneita; Browne-Nuñez, Christine (2016)
      ...Here, we present the collaborative efforts of San Diego Zoo Global, USA, and Free the Bears to design innovative surveys aimed at improving our understanding of public knowledge, attitudes and behaviours towards bears and bear-part consumption in South East Asia. Over 1500 surveys were completed in Cambodia and Lao PDR.....
    • Growth, coloration, and demography of an introduced population of the Acklins Rock Iguana (Cyclura rileyi nuchalis) in the Exuma Islands, The Bahamas

      Iverson, John B.; Smith, G.R.; Pasachnik, Stesha A.; Hines, K.N.; Pieper, L.; Iverson, John B.; Grant, Tandora D.; Knapp, Charles R.; Pasachnik, Stesha A. (2016)
      In 1973, five Acklins Rock Iguanas (Cyclura rileyi nuchalis) from Fish Cay in the Acklins Islands, The Bahamas, were translocated to Bush Hill Cay in the northern Exuma Islands. That population has flourished, despite the presence of invasive rats, and numbered > 300 individuals by the mid-1990s....
    • Growth, reproduction and diet of Roatan Spiny-tailed Iguanas, Ctenosaura oedirhina, with notes on the status of the species

      Pasachnik, Stesha A. (2013)
      Roatan Spiny-tailed Iguanas, Ctenosaura oedirhina, are listed as Endangered by the IUCN Redlist Assessment and under Appendix II of Convention on International Trade of Endangered Species of Wild Fauna and Flora (CITES). These iguanas occur primarily on Roatan and Barbaretta, off the Caribbean coast of Honduras. Habitat destruction associated with development, small-scale agriculture, and exploitation for food and the pet trade are contributing to the decline of these iguanas. This species was described in 1987 (de Queiroz) when it was split from the sister taxon C. bakeri, found on the island of Utila, Honduras. Since its description little has been done to understand its biology or protect this narrow-range endemic. Herein, I examined the morphology and body condition of this species across its range and report on its reproductive biology and diet. Similar to many members of the Iguaninae, males are larger on average and have relatively longer tails than females. Likewise, reproductive and dietary data are consistent with those for closely related species. The body condition of both males and females was lower in more pristine study sites, indicating that supplemental feeding in developed areas may be having an effect. A female-biased sex ratio was found in sites protected by grassroots efforts, where the populations were large enough to be studied. Conservation measures should focus on alleviating the threats of harvesting and habitat destruction through increased law enforcement, outreach, and education.
    • Habitat differentiation among three Nigeria–Cameroon chimpanzee (Pan troglodytes ellioti) populations

      Abwe, Ekwoge E.; Morgan, Bethan J.; Tchiengue, Barthelemy; Kentatchime, Fabrice; Doudja, Roger; Ketchen, Marcel E.; Teguia, Eric; Ambahe, Ruffin; Venditti, Dana M.; Mitchell, Matthew W.; et al. (2019)
      Ecological niche models (ENMs) are often used to predict species distribution patterns from datasets that describe abiotic and biotic factors at coarse spatial scales. Ground-truthing ENMs provide important information about how these factors relate to species-specific requirements at a scale that is biologically relevant for the species. Chimpanzees are territorial and have a predominantly frugivorous diet. The spatial and temporal variation in fruit availability for different chimpanzee populations is thus crucial, but rarely depicted in ENMs. The genetic and geographic distinction within Nigeria–Cameroon chimpanzee (Pan troglodytes ellioti) populations represents a unique opportunity to understand fine scale species-relevant ecological variation in relation to ENMs. In Cameroon, P. t. ellioti is composed of two genetically distinct populations that occupy different niches: rainforests in western Cameroon and forest–woodland–savanna mosaic (ecotone) in central Cameroon. We investigated habitat variation at three representative sites using chimpanzee-relevant environmental variables, including fruit availability, to assess how these variables distinguish these niches from one another. Contrary to the assumption of most ENM studies that intact forest is essential for the survival of chimpanzees, we hypothesized that the ecotone and human-modified habitats in Cameroon have sufficient resources to sustain large chimpanzee populations. Rainfall, and the diversity, density, and size of trees were higher at the rainforest. The ecotone had a higher density of terrestrial herbs and lianas. Fruit availability was higher at Ganga (ecotone) than at Bekob and Njuma. Seasonal variation in fruit availability was highest at Ganga, and periods of fruit scarcity were longer than at the rainforest sites. Introduced and secondary forest species linked with anthropogenic modification were common at Bekob, which reduced seasonality in fruit availability. Our findings highlight the value of incorporating fine scale species-relevant ecological data to create more realistic models, which have implications for local conservation planning efforts.
    • Habitat drives dispersal and survival of translocated juvenile desert tortoises

      Nafus, Melia G.; Esque, Todd C.; Averill-Murray, Roy C.; Nussear, Kenneth E.; Swaisgood, Ronald R. (2017)
      In spite of growing reliance on translocations in wildlife conservation, translocation efficacy remains inconsistent. One factor that can contribute to failed translocations is releasing animals into poor-quality or otherwise inadequate habitat. Here, we used a targeted approach to test the relationship of habitat features to post-translocation dispersal and survival of juvenile Mojave desert tortoises Gopherus agassizii. We selected three habitat characteristics – rodent burrows, substrate texture (prevalence and size of rocks) and washes (ephemeral river beds) – that are tied to desert tortoise ecology. At the point of release, we documented rodent burrow abundance, substrate texture and wash presence and analysed their relationship to the maximum dispersal. We also documented the relative use by each individual for each habitat characteristic and analysed their relationships with survival and fatal encounters with a predator in the first year after release. In general, the presence of refugia or other areas that enabled animals to avoid detection, such as burrows and substrate, decreased the overall mortality as well as predator-mediated mortality. The presence of washes and substrate that enhanced the tortoises’ ability to avoid detection also associated with the reduced dispersal away from the release site. These results indicate an important role for all three measured habitat characteristics in driving dispersal, survival or fatal encounters with a predator in the first year after translocation. Synthesis and applications. Resource managers using translocations as a conservation tool should prioritize acquiring data linking habitat to fitness. In particular, for species that depend on avoiding detection, refuges such as burrows and habitat that improved concealment had notable ability to improve the survival and dispersal. Our study on juvenile Mojave desert tortoises showed that refuge availability or the distributions of habitat appropriate for concealment are important considerations for identifying translocation sites for species highly dependent on crypsis, camouflage or other forms of habitat matching.
    • Habitat utilization of Roatán Spiny-tailed Iguanas (Ctenosaura oedirhina) and its implications for conservation

      Goode, A.B.C.; Pasachnik, Stesha A.; Maple, T.L.; Iverson, John B.; Grant, Tandora D.; Knapp, Charles R.; Pasachnik, Stesha A. (2016)
      ...With data gathered from use/availability surveys, resource selection functions can identify habitats and environmental variables associated with the presence of a species. Herein, we used these techniques to better understand the distribution of the Roatán Spiny-tailed Iguanas (Ctenosaura oedirhina), a narrow-range endemic on the island of Roatán, Honduras....
    • Hapalemur meridionalis. The IUCN Red List of Threatened Species 2020

      Donati, G; Balestri, M; Campera, M; Eppley, Timothy M. (2020)
      There is a suspected population reduction of greater than or equal to30% in this species over a three generation period. Causes of this reduction (which have not ceased) include continuing decline in area, extent and quality of habitat, and exploitation through hunting. Between 1999-2005 habitat loss in the Tsitongambarika Protected Area has been 1.74% per year (Andriamasimanana 2008). A population reduction of greater than or equal to 30% is also suspected to be met in the next 27 years (over a three generation time period) due to the same causes. These causes have not ceased, and will to a large extent not be easily reversible. Of note, it has been estimated that there will be a 21% reduction in the species' range from 2000 to 2080 due to climate change alone (Brown and Yoder 2015). Based on these premises, the species is listed as Vulnerable.
    • Harpy eagles (Harpia harpyja) nesting at Refugio Amazonas, Tambopata, Peru feed on abundant disturbance-tolerant species

      Bowler, Mark; Couceiro, Daniel; Martinez, Rocio; Orihuela, Gabriela; Shoobridge, Juan Diego; Nycander, Eduardo; de Miranda, Everton B. P.; Tobler, Mathias W. (2020)
      The harpy eagle (Harpia harpyja) is one of the main predators of arboreal mammals in the neotropics, affecting the ecology and behaviour these species. Knowledge of harpy eagle diets across their geographical range is patchy, the ability of harpy eagles to adapt to changing habitats is still open to question….