The critical role of dietary foliage in maintaining the gut microbiome and metabolome of folivorous sifakas

Abstract

The gut microbiome (GMB) of folivores metabolizes dietary fiber into nutrients, including short-chain fatty acids (SCFAs); however, experiments probing the consequences of foliage quality on host GMBs are lacking. We therefore examined GMB structure and function via amplicon sequencing and Nuclear Magnetic Resonance spectroscopy in 31 captive sifakas (Propithecus coquereli) during dietary manipulations associated with husbandry. Supplementing standard diets with diverse foliage blends, versus with a single plant species, promoted more diverse GMBs, enriched for taxa implicated in plant-fiber metabolism, but depleted in taxa implicated in starch metabolism and bile tolerance. The consumption of diverse blends was associated with greater concentrations of colonic SCFAs. Abundant foliage, via forest access, promoted compositionally distinct and more stable GMBs, but reduced concentrations of SCFAs, possibly reflecting selection of high-quality leaves. In 11 subjects denied forest access, we examined the temporal pace of microbial shifts when supplemental foliage was abruptly switched between diverse blends and single species. The sifaka GMB responded within days, with community diversity and composition closely tracking foliage diversity. By providing experimental evidence that the folivore GMB is sensitive to minor changes in dietary foliage, we reveal the fragility of specialist GMBs, with implications for managing the wellbeing of endangered wildlife.

The importance of scale in comparative microbiome research: New insights from the gut and glands of captive and wild lemurs

“…We collected a total of 289 fecal samples during animal follows or routine captures, conducted from 2013 to 2017, as previously described (Greene et al, , in review; Junge et al, ; Table ). We also collected 56 glandular secretion samples from a subset of 35 adult lemurs (Table ), obtained during routine captures of sifakas ( Propithecus diadema ) in September 2014 and of woolly lemurs ( Avahi Laniger ) in March 2015 (Junge et al, ), and during handling of awake, gently restrained ring‐tailed lemurs at the DLC in November 2016 (Scordato & Drea, ).…”

“…From a conservation perspective the notion of rewilding is exciting, as captive populations provide a genetic “safety net” for endangered wildlife and their natural microbiota (Trevelline et al, ). Microbial tools can thus contribute to the optimization of animal diets, nutrition, and health (Greene et al, ; Stumpf et al, ). Ultimately, a better understanding of how captivity perturbs GMBs relative to host traits could lead to improved management techniques with clear conservation implications.…”

“…Increasingly, researchers have adopted small‐scale comparative approaches, investigating GMB composition across host populations, species, and habitat types (Greene et al, in review; Perofsky, Lewis, & Meyers, ; Umanets et al, ). Opportunities for longitudinal sampling and experimental manipulation using captive populations have facilitated studies on the timing of microbiome acquisition across host ontogenetic development (McKenney, Rodrigo, & Yoder, ), patterns of recovery from enteric infection (McKenney, Greene, Drea, & Yoder, ), and response to changing dietary quality (Greene, McKenney, O'Connell, & Drea, ). While these studies have contributed important insights, the lemurs' unique potential for wide‐scale, comparative analyses across species and microbiota remains largely untapped.…”

“…Notably, the routine use of chows, domesticated produce, and carbohydrate‐based treat items generally result in fiber‐limited, but sugar‐rich (i.e., “westernized”) diets (Clayton, Al‐Ghalith, et al, ). For herbivores (animals that consume a broadly plant‐based diet) and folivores (animals that consume a specifically foliage‐based diet), increasing plant‐fiber consumption can mitigate the microbial consequences associated with captivity, as evidenced by improved GMB diversity, stability, membership, and nutrient production (Clayton, Al‐Ghalith, et al, ; Greene et al, ; Kohl et al, ). A second mechanism proposed to explain captivity‐induced dysbiosis centers around changes in environmental conditions.…”

“…Studies in captive monkeys have established linkages between GMBs and disease states (McKenna et al, ), breastfeeding (O'Sullivan et al, ), and westernized or fibrous diets (Albert, Rani, & Sela, ; Amato et al, ), and have informed methods development and provided validation for future field studies (Hale, Tan, Knight, & Amato, ). Capitalizing on the potential for longitudinal and experimental research at the DLC, members of our team have related GMB structure to (a) specific sites along the gastrointestinal tract (Greene & McKenney, ), (b) enteric infection with Cryptosporidium and subsequent antibiotic administration (McKenney, Greene et al, ), (c) host feeding strategy across infant ontogenetic development (McKenney et al, ) and in adulthood (McKenney, O'Connell, Rodrigo, & Yoder, ), (d) bamboo specialization (McKenney et al, ), and (e) shifts in dietary quality (Greene et al, ).…”