Stable isotopes document resource partitioning and effects of forest disturbance on sympatric cheirogaleid lemurs

Deforestation continues to jeopardize Malagasy primates as viable habitats become smaller, more fragmented, and more disturbed. This deforestation can lead to changes in diet, microhabitat, and gene flow between populations of endangered species, and it remains unclear how these changes may affect gut microbiome (GM) characteristics. The black-and-white ruffed lemur (Varecia variegata), which is among Madagascar's most threatened lemur species, provides a critical model for understanding the relationships between historical and on-going deforestation (habitat disturbance), feeding ecology, and GM composition and diversity. We studied four populations inhabiting two rainforests (relatively pristine vs. highly disturbed) in southeastern Madagascar. We conducted full-day focal animal behavioral follows and collected fecal samples opportunistically across a three-month period. Our results indicate that lemurs inhabiting sites characterized by habitat disturbance and low dietary diversity exhibited reduced gut microbial alpha diversity. We also show that these same factors were associated with high community dissimilarity using weighted and unweighted UniFrac metrics. Finally, an indicator species analysis showed that the most pristine site was characterized by an abundance of methanogenic archaea.While it is impossible to disentangle the relative contributions of each confounding variable presented by our sampling design, these results provide crucial information about GM variability, thereby underscoring the importance of monitoring endangered species at the population-level.

Section: Introductionmentioning

confidence: 99%

Extensive variability in the gut microbiome of a highly‐specialized and critically endangered lemur species across sites

Donohue

Asangba

Ralainirina

et al. 2019

“…Across all TA, most sources ( n = 63) covered species threatened with extinction. Four DD species were also included in research (DD lemur species: furry‐eared dwarf lemur, Cheirogaleus crossleyi : Crowley, Blanco, Arrigo‐Nelson, & Irwin, 2013), and 62 species across the total sample (13.5%) were not listed by the IUCN. Two studies considered insects, each exploring how the ecosystem services the insects provided were impacted by fragmentation (pollination: Bodin, Tengö, Norman, Lundberg, & Elmqvist, 2006; seed dispersal: Dausmann, Glos, Linsenmair, & Ganzhorn, 2008).…”

Section: Resultsmentioning

confidence: 99%

“…For “Other” studies, Crowley et al (2013) used stable isotope analysis to examine resource partitioning in response to fragmentation between mouse and dwarf lemurs (Goodman's mouse lemur, Microcebus lehilahytsara ; furry‐eared dwarf lemur, C. crossleyi ; Sibree's dwarf lemur, C. sibreei ), finding these cheirogaleids to modify behavioral strategies to consume similar resources across sites, despite the impact of fragmentation on resource availability. Two other studies also examined nutrition and resource access.…”

Section: Resultsmentioning

confidence: 99%

Trends in forest fragment research in Madagascar: Documented responses by lemurs and other taxa

Kling

Yaeger

Wright

2020

The rise in research investigating fragmentation and its impact on primates and other taxa reflects the growing presence of fragmented landscapes themselves. Although numerous studies report the negative effects of fragmentation on biodiversity, it is difficult to generalize responses to fragmentation for specific taxonomic groups, such as non-human primates, when studies have not employed a definitive concept of fragmentation or fragments themselves. Madagascar's high degree of fragmentation, wealth of endemic taxa, and extensive history of ecological research provide the opportunity to compare fragmentation studies across similar contexts. We conducted a literature search of peer-reviewed articles on fragmentation in Madagascar to characterize its trends. A total of 70 articles, 46 of which concentrated on lemurs, tested the impacts of fragmentation on Malagasy taxa, while additional sources conducted research in one or more fragments without testing its effects (n = 112 total, 79 on lemurs). Studies on lemurs most frequently tested fragmentation's impacts on genetics and biodiversity metrics (n = 16 and 15 studies, respectively), although health, modeling, behavioral, and cross-disciplinary techniques were also reported. Responses to fragmentation were reported for 49 lemur species, with most studies concentrated in eastern Madagascar (87%). Although there was variation in the metrics reported in studies testing the effects of fragmentation on Malagasy species, the most common measures were fragment area, isolation, or comparison to a control site. Landscape-scale approaches and examination of fragmentation per se were rarely employed. Characterizing trends of fragmentation research in Madagascar emphasizes the challenges of documenting fragmentation's effects while highlighting the benefits of research within fragmented landscapes, particularly when combined with consideration for how the matrix within human-modified landscapes may impact primate populations. K E Y W O R D S forest fragments, fragmentation, lemurs, literature search, Madagascar

“…Loudon et al () found nitrogen enrichment in ring‐tailed lemurs ( Lemur catta ) in suboptimal health. Crowley et al () found slightly higher δ 15 N (∼0.5‰) in Cheirogaleus crossleyi in the fragmented forests of Tsinjoarivo, but were unable to ascertain if the increase in δ 15 N was due to increased insect consumption or nutritional stress. Ben‐David, McColl, Boonstra, and Karels (), however, found no effect between food restriction and isotope composition, although it was noted that physiological effects (i.e., stable nitrogen composition) may have been obscured by diet selection.…”

Section: Discussionmentioning

confidence: 97%

“…The establishment of the Institute for the Conservation of Tropical Environments by Wright led to collaborations and exchanges among scientists resulting in over 800 publications from 1987 to 2016. Of the nearly 100 publications that focus on the effects of logging or habitat modification in the rainforests of eastern Madagascar, the majority address compositional or functional change at the species or population level (e.g., Crowley et al, ; Crowley, Blanco, Arrigo‐Nelson, & Irwin, ; Gerber, Arrigo‐Nelson, Karpanty, Kotschwar, & Wright, ; Herrera, Wright, Lauterbur, Ratovonjanahary, & Taylor, ; Irwin et al, ; Pochron, Tucker, & Wright, ; Wright, ). Research on the effects of logging on composition or function at the community level comprises ∼20% of the total (e.g., Benstead, Douglas, & Pringle, ; Bixby, Benstead, Douglas, & Pringle, ; Brown & Gurevitch, ; Bublitz et al, ; Rainio & Niemelä, ; Razafindratsima, Jones, & Dunham, ; Wright et al, ), while research on the effects of logging on structural/compositional and functional attributes of the genetic component of biodiversity accounts for ∼10% of the total (e.g., Baden et al, ; Tomiuk et al, ; Yoder et al, ).…”

Section: Introductionmentioning

confidence: 99%

Of lemurs and louse flies: The biogeochemical and biotic effects of forest disturbance on Propithecus edwardsi and its obligate ectoparasite Allobosca crassipes in Ranomafana National Park, southeastern Madagascar

McGee

Vaughn

2017

From alleles to ecosystems and landscapes, anthropogenic activity continues to affect the environment, with particularly adverse effects on biodiversity hotspots such as Madagascar. Selective logging has been proposed as a "win-win" conservation strategy, yet its effects on different components of biodiversity are still not fully understood. Here we examine biotic factors (i.e., dietary differences) that may be driving differences in biogeochemical stocks between disturbed and undisturbed forests. We present the stable nitrogen (δ N) and carbon (δ C) isotope composition of hair from the lemur Propithecus edwardsi and of whole bodies of its obligate ectoparasite, the louse-fly Allobosca crassipes, from sites in Ranomafana National Park (RNP) that are comparable except for the history of logging and subsequent forest regeneration. P. edwardsi and A. crassipes from the disturbed (i.e., heavily selectively logged) site are lower in N and C relative to P. edwardsi and A. crassipes from sites that were minimally selectively logged or not commercially logged at all. There is a ∼3‰ decrease in N between disturbed and undisturbed sites that corresponds to a difference of nearly a full trophic level. Flowers from Bakerella clavata, a staple food source for P. edwardsi in disturbed habitats and a fallback food for P. edwardsi in primary forests, were also analyzed isotopically. B. clavata is δ N-depleted in both disturbed and undisturbed sites. Data from longitudinal behavioral surveys of P. edwardsi in RNP and other forests in eastern Madagascar point to significant differences in consumption patterns of B. clavata, with P. edwardsi in disturbed forests consuming almost twice as much of this plant. Depletion of N in animal tissues is a complex issue, but likely the result of the interaction of physiological and ecological factors. Anthropogenic disturbance in RNP from selective logging has had both biotic and biogeochemical effects that are observable trophically.