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Habitat Degradation Impacts Black Howler Monkey (Alouatta Pigra) Gastrointestinal Microbiomes

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Habitat Degradation Impacts Black Howler Monkey (Alouatta Pigra) Gastrointestinal Microbiomes The ISME Journal (2013) 7, 1344–1353 & 2013 International Society for Microbial Ecology All rights reserved 1751-7362/13 www.nature.com/ismej ORIGINAL ARTICLE Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes Katherine R Amato1,2, Carl J Yeoman3,4, Angela Kent5, Nicoletta Righini2, Franck Carbonero6, Alejandro Estrada7, H Rex Gaskins4,6, Rebecca M Stumpf2,4, Suleyman Yildirim4, Manolito Torralba8, Marcus Gillis8, Brenda A Wilson4,9, Karen E Nelson8, Bryan A White4,6 and Steven R Leigh2,4,10 1Program in Ecology, Evolution and Conservation Biology, University of Illinois, Urbana, IL, USA; 2Department of Anthropology, University of Illinois, Urbana, IL, USA; 3Department of Animal and Range Sciences, Montana State University, Bozeman, MT, USA; 4Institute for Genomic Biology, University of Illinois, Urbana, IL, USA; 5Department of Natural Resources and Environmental Sciences, University of Illinois, Urbana, IL, USA; 6Department of Animal Sciences, University of Illinois, Urbana, IL, USA; 7Estacion de Biologia Tropical Los Tuxtlas, Instituto de Biologia, Universidad Nacional Autonoma de Mexico, San Andre´s Tuxtla, Mexico; 8The J. Craig Venter Institute, Rockville, MD, USA and 9Department of Microbiology, University of Illinois, Urbana, IL, USA The gastrointestinal (GI) microbiome contributes significantly to host nutrition and health. However, relationships involving GI microbes, their hosts and host macrohabitats remain to be established. Here, we define clear patterns of variation in the GI microbiomes of six groups of Mexican black howler monkeys (Alouatta pigra) occupying a gradation of habitats including a continuous evergreen rainforest, an evergreen rainforest fragment, a continuous semi-deciduous forest and captivity. High throughput microbial 16S ribosomal RNA gene sequencing indicated that diversity, richness and composition of howler GI microbiomes varied with host habitat in relation to diet. Howlers occupying suboptimal habitats consumed less diverse diets and correspondingly had less diverse gut microbiomes. Quantitative real-time PCR also revealed a reduction in the number of genes related to butyrate production and hydrogen metabolism in the microbiomes of howlers occupying suboptimal habitats, which may impact host health. The ISME Journal (2013) 7, 1344–1353; doi:10.1038/ismej.2013.16; published online 14 March 2013 Subject Category: Microbe-microbe and microbe-host interactions Keywords: Alouatta; gut microbiome; habitat; primate Introduction seasons and habitats. However, while experimental studies imply that shifts in host diet in The mammalian gastrointestinal (GI) microbiome wild, mammalian populations should impact GI contributes significantly to host digestive efficiency microbiome composition, the relationship between (Bauchop, 1971; Lambert, 1998; Flint and Bayer, host habitat, diet and GI microbiome composition 2008), while diet strongly influences the micro- remains to be examined. biome’s composition (Ley et al., 2006, 2008; Understanding the interaction between host habi- Turnbaugh et al., 2009; Yildirim et al., 2010; tat and microbiome composition may also be useful Wu et al., 2011). Across species, host diet and GI for conservation efforts because changes in the GI microbiome composition are correlated (Ley et al., microbiome have been shown to affect host nutrition 2008), while within species, dietary shifts alter GI and health (Dethlefsen et al., 2007; Sekirov et al., microbiome composition (Ley et al., 2006; 2010; Flint et al., 2011; Hooper et al., 2012). Turnbaugh et al., 2009). For most wild, mammalian Dysbioses may manifest themselves in a number of populations, dietary shifts are common across different ways, but within the GI-tract they are most often seen as losses of microbial species diversity. Correspondence: SR Leigh, Department of Anthropology, Reductions in GI microbiome diversity may reduce University of Illinois at Urbana-Champaign, 1206 West Gregory microbial functional groups, making the micro- Drive, Urbana, IL 61801, USA. biome less efficient, less resistant to disturbance E-mail: [email protected] and more susceptible to pathogenic invasion 10Present address: Department of Anthropology, University of Colorado, Boulder, CO, USA. (Rosenfeld, 2002; Costello et al., 2012). Hosts with Received 3 July 2012; revised 16 November 2012; accepted 6 low GI microbiome diversity also exhibit increased January 2013; published online 14 March 2013 stress responses (higher glucocorticoid levels) and Habitat influences primate gut microbiomes KR Amato et al 1345 reduced immune function (fewer cells that important perspectives from non-human primate secrete local, strain-specific immunoglobulin A) ecology, biological anthropology, community ecol- (Macpherson et al., 2008; Neish, 2009; Messaoudi ogy and microbial ecology (Benezra et al., 2012; et al., 2010; Hooper et al., 2012). Costello et al., 2012), and illustrate a ‘co-degrada- Here, we explore cross-habitat patterns in the GI tion’ of howler habitat, diet and GI microbiomes that microbiome richness, diversity and composition of presents new concerns for conservation biology. an endangered Mesoamerican primate, the black howler monkey (A. pigra; IUCN, 2012) using 16S ribosomal RNA gene sequencing to survey coloniz- Materials and methods ing bacteria. The howler monkey (Alouatta sp.) provides an exceptional model for understanding Fecal sample collection how variation in host habitat and diet impacts Samples were collected across an 8-week period GI microbiome structure, and ultimately, host nutri- (May–June 2009) from two neighboring groups of tion and health. Howlers can consume a leaf-heavy black howlers inhabiting a CR in Palenque National diet (Milton, 1980; Lambert, 1998; Estrada and Park, Mexico (Balam Group, n ¼ 6 and Motiepa Coates-Estrada, 2005; Di Fiore and Campbell, Group, n ¼ 8). Additional samples were obtained 2007), permitting them to occupy areas with limited from two groups of howlers in a continuous, but SD resource availability and to persist longer in forest B200 km from the national park (Tormento degraded habitats than more frugivorous primate Group 1, n ¼ 3, and Tormento Group 2, n ¼ 4), taxa (Estrada and Coates-Estrada, 1996; Zunino a FR located 7 km outside of the national park near et al., 2007). As many leaves contain high levels of human dwellings (Cuartel Group, n ¼ 4), and a resistant fiber and toxins, GI microbiome contribu- rehabilitation center located 5 km outside of the tions to daily energy flows through metabolism of national park, which housed locally rescued mon- xenobiotics are critical to howler nutrition (Milton, keys on an atypical diet (AcaJungla, n ¼ 7; 1979; Lambert, 1998; Lambert and Fellner, 2012). Supplementary Figure S1; additional information Fibrolytic processes of the GI microbiome contribute about the collection sites is provided in Supple- up to 31% of a howler’s required daily energy via the mentary Information). No continuous forest exists formation of short-chain fatty acids (93.7% acetate, between the sample sites, and they are separated by 5.9% propionate, 0.4% butyrate in A. palliata; Milton distances far exceeding the territories occupied and McBee, 1983). Therefore, if shifts in howler diet by A. pigra groups, precluding migration of groups change GI microbiome composition or reduce micro- among habitats. biome richness and diversity, there may be conse- Fecal samples were collected immediately upon quences for howler nutrition and health. defecation, and then stored in 96% ethanol at 4 1C In this study, we test the hypothesis that howlers until transport to the University of Illinois occupying habitats of different qualities develop at Champaign-Urbana where they were stored at different GI microbiomes. Animals in disturbed À 20 1C until processing. A total of 128 samples habitats generally consume different types of food were collected. Individuals in the CR were sampled resources than their counterparts in undisturbed weekly when possible for the duration of the study. habitats (Kamler et al., 2007; Flaherty et al., 2010; Abbas et al., 2011; Chaves et al., 2012). As a result, their diets typically deviate from the host species Behavioral data collection archetypical dietary regime and are likely to be Feeding data for the CR and SD groups were obtained associated with shifts in GI microbiome composi- from B225 h of focal individual sampling with tion. Specifically, because habitat degradation binoculars. Twenty-minute focal samples of behavior leads to differences in available plant species and were collected between 0600 and 1600 hours each reductions in plant diversity (Benitez-Malvido and day, with activity recorded instantaneously every Martinez-Ramos, 2003; Vellend, 2003; Lindborg and 2 min. During a feeding bout (active consumption of Eriksson, 2004), we predict that howlers inhabiting food resources), the food type (e.g. young leaves, disturbed habitats will exhibit signs of dysbiosis, mature fruit, flowers) and plant species were such as lower microbial richness and diversity. If recorded. Qualitative dietary data were collected for this is the case, then host nutrition and health may rainforest fragments during fieldwork. General diet be negatively affected. data for the captive group were obtained from To explore the relationship between host habitat, veterinary records at the rehabilitation center. diet and GI microbiome composition, we analyzed As quantitative dietary data were expressed in fecal samples from six
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