Browsing by Author "Greene, LK"

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Open Access
Dietary and Nutritional Selections by Ecologically Diverse Lemurs in Nonnative Forests
(International Journal of Primatology, 2024-08-01) Greene, LK; Blanco, MB; Farmer, C; O’Malley, M; Gherardi, C; Irwin, MT
Open Access
Gut Microbial Diversity and Ecological Specialization in Four Sympatric Lemur Species Under Lean Conditions
(International Journal of Primatology, 2021-12-01) Greene, LK; Rambeloson, E; Rasoanaivo, HA; Foss, ED; Yoder, AD; Drea, CM; Blanco, MB
The gut microbiome is gaining recognition for its role in primate nutrition, but we stand to benefit from microbiome comparisons across diverse hosts and environmental conditions. We compared gut microbiome structure in four lemur species from four phylogenetic lineages, including 9 individual mouse lemurs (Microcebus danfossi), 6 brown lemurs (Eulemur fulvus), 20 sifakas (Propithecus coquereli), and a single sportive lemur (Lepilemur grewcockorum). In northwestern Madagascar, these species are sympatric, but use different feeding strategies to cope with environmental challenges, including relying on tree gums and insects (mouse lemurs), and some vs. significant leaf matter (brown lemurs vs. sifakas and sportive lemurs). From one fecal sample collected per lemur in the dry season in the Anjajavy Forest, we determined gut microbiome diversity, variability, and membership via 16S rRNA sequencing. The lemurs harbored strongly species-specific gut microbiomes. Brown lemurs showed more diverse and generalized consortia; mouse lemurs, sifakas, and the sportive lemur had less diverse consortia with more distinct memberships. Consistent with their fallback foods, mouse lemur microbiomes included taxa putatively associated with gum and insect digestion, whereas those of sifakas and the sportive lemur showed stronger and distinct signatures of leaf fiber and secondary compound metabolism. These results point to feeding strategy, intertwined with host phylogeny, as a driver of gut microbiome composition, but highlight real-time dietary specificity as a contributing driver of microbiome diversity. While illuminating how gut microbiomes facilitate host nutrition on challenging foods, these results help explain how ecologically diverse primates living in sympatry may differentially cope with seasonal or stochastic lean times.
Open Access
Love is in the air: Sociality and pair bondedness influence sifaka reproductive signalling
(Animal Behaviour, 2014-01-01) Greene, LK; Drea, CM
© 2013 The Association for the Study of Animal Behaviour.Social complexity, often estimated by group size, is seen as driving the complexity of vocal signals, but its relation to olfactory signals, which arguably arose to function in nonsocial realms, remains underappreciated. That olfactory signals also may mediate within-group interaction, vary with social complexity and promote social cohesion underscores a potentially crucial link with sociality. To examine that link, we integrated chemical and behavioural analyses to ask whether olfactory signals facilitate reproductive coordination in a strepsirrhine primate, the Coquerel's sifaka, Propithecus coquereli. Belonging to a clade comprising primarily solitary, nocturnal species, the diurnal, group-living sifaka represents an interesting test case. Convergent with diurnal, group-living lemurids, sifakas expressed chemically rich scent signals, consistent with the social complexity hypothesis for communication. These signals minimally encoded the sex of the signaller and varied with female reproductive state. Likewise, sex and female fertility were reflected in within-group scent investigation, scent marking and overmarking. We further asked whether, within breeding pairs, the stability or quality of the pair's bond influences the composition of glandular signals and patterns of investigatory or scent-marking behaviour. Indeed, reproductively successful pairs tended to show greater similarity in their scent signals than did reproductively unsuccessful pairs, potentially through chemical convergence. Moreover, scent marking was temporally coordinated within breeding pairs and was influenced by past reproductive success. That olfactory signalling reflects social bondedness or reproductive history lends support to recent suggestions that the quality of relationships may be a more valuable proxy than group size for estimating social complexity. We suggest that olfactory signalling in sifakas is more complex than previously recognized and, as in other socially integrated species, can be a crucial mechanism for promoting group cohesion and maintaining social bonds. Thus, the evolution of sociality may well be reflected in the complexity of olfactory signalling.
Open Access
Mix it and fix it: functions of composite olfactory signals in ring-tailed lemurs.
(R Soc Open Sci, 2016-04) Greene, LK; Grogan, KE; Smyth, KN; Adams, CA; Klager, SA; Drea, CM
Animals communicating via scent often deposit composite signals that incorporate odorants from multiple sources; however, the function of mixing chemical signals remains understudied. We tested both a 'multiple-messages' and a 'fixative' hypothesis of composite olfactory signalling, which, respectively, posit that mixing scents functions to increase information content or prolong signal longevity. Our subjects-adult, male ring-tailed lemurs (Lemur catta)-have a complex scent-marking repertoire, involving volatile antebrachial (A) secretions, deposited pure or after being mixed with a squalene-rich paste exuded from brachial (B) glands. Using behavioural bioassays, we examined recipient responses to odorants collected from conspecific strangers. We concurrently presented pure A, pure B and mixed A + B secretions, in fresh or decayed conditions. Lemurs preferentially responded to mixed over pure secretions, their interest increasing and shifting over time, from sniffing and countermarking fresh mixtures, to licking and countermarking decayed mixtures. Substituting synthetic squalene (S)-a well-known fixative-for B secretions did not replicate prior results: B secretions, which contain additional chemicals that probably encode salient information, were preferred over pure S. Whereas support for the 'multiple-messages' hypothesis underscores the unique contribution from each of an animal's various secretions, support for the 'fixative' hypothesis highlights the synergistic benefits of composite signals.
Open Access
Molecular Adaptation to Folivory and the Conservation Implications for Madagascar’s Lemurs
(Frontiers in Ecology and Evolution, 2021-10-06) Guevara, EE; Greene, LK; Blanco, MB; Farmer, C; Ranaivonasy, J; Ratsirarson, J; Mahefarisoa, KL; Rajaonarivelo, T; Rakotondrainibe, HH; Junge, RE; Williams, CV; Rambeloson, E; Rasoanaivo, HA; Rahalinarivo, V; Andrianandrianina, LH; Clayton, JB; Rothman, RS; Lawler, RR; Bradley, BJ; Yoder, AD
The lemurs of Madagascar include numerous species characterized by folivory across several families. Many extant lemuriform folivores exist in sympatry in Madagascar’s remaining forests. These species avoid feeding competition by adopting different dietary strategies within folivory, reflected in behavioral, morphological, and microbiota diversity across species. These conditions make lemurs an ideal study system for understanding adaptation to leaf-eating. Most folivorous lemurs are also highly endangered. The significance of folivory for conservation outlook is complex. Though generalist folivores may be relatively well equipped to survive habitat disturbance, specialist folivores occupying narrow dietary niches may be less resilient. Characterizing the genetic bases of adaptation to folivory across species and lineages can provide insights into their differential physiology and potential to resist habitat change. We recently reported accelerated genetic change in RNASE1, a gene encoding an enzyme (RNase 1) involved in molecular adaptation in mammalian folivores, including various monkeys and sifakas (genus Propithecus; family Indriidae). Here, we sought to assess whether other lemurs, including phylogenetically and ecologically diverse folivores, might show parallel adaptive change in RNASE1 that could underlie a capacity for efficient folivory. We characterized RNASE1 in 21 lemur species representing all five families and members of the three extant folivorous lineages: (1) bamboo lemurs (family Lemuridae), (2) sportive lemurs (family Lepilemuridae), and (3) indriids (family Indriidae). We found pervasive sequence change in RNASE1 across all indriids, a dN/dS value > 3 in this clade, and evidence for shared change in isoelectric point, indicating altered enzymatic function. Sportive and bamboo lemurs, in contrast, showed more modest sequence change. The greater change in indriids may reflect a shared strategy emphasizing complex gut morphology and microbiota to facilitate folivory. This case study illustrates how genetic analysis may reveal differences in functional traits that could influence species’ ecology and, in turn, their resilience to habitat change. Moreover, our results support the body of work demonstrating that not all primate folivores are built the same and reiterate the need to avoid generalizations about dietary guild in considering conservation outlook, particularly in lemurs where such diversity in folivory has probably led to extensive specialization via niche partitioning.
Open Access
Of fruits and fats: high-sugar diets restore fatty acid profiles in the white adipose tissue of captive dwarf lemurs.
(Proceedings. Biological sciences, 2022-06) Blanco, MB; Greene, LK; Ellsaesser, LN; Schopler, B; Davison, M; Ostrowski, C; Klopfer, PH; Fietz, J; Ehmke, EE
Fat-storing hibernators rely on fatty acids from white adipose tissue (WAT) as an energy source to sustain hibernation. Whereas arctic and temperate hibernators preferentially recruit dietary polyunsaturated fatty acids (PUFAs), tropical hibernators can rely on monounsaturated fatty acids that produce fewer lipid peroxides during oxidation. Nevertheless, compositional data on WAT from tropical hibernators are scant and questions remain regarding fat recruitment and metabolism under different environmental conditions. We analyse fatty acid profiles from the WAT of captive dwarf lemurs (Cheirogaleus medius) subjected to high-sugar or high-fat diets during fattening and cold or warm conditions during hibernation. Dwarf lemurs fed high-sugar (compared to high-fat) diets displayed WAT profiles more comparable to wild lemurs that fatten on fruits and better depleted their fat reserves during hibernation. One PUFA, linoleic acid, remained elevated before hibernation, potentially lingering from the diets provisioned prior to fattening. That dwarf lemurs preferentially recruit the PUFA linoleic acid from diets that are naturally low in availability could explain the discrepancy between captive and wild lemurs' WAT. While demonstrating that minor dietary changes can produce major changes in seasonal fat deposition and depletion, our results highlight the complex role for PUFA metabolism in the ecology of tropical hibernators.