Skip to main content

Bamboo Specialists from Two Mammalian Orders (Primates, Carnivora) Share a High Number of Low-Abundance Gut Microbes


Bamboo specialization is one of the most extreme examples of convergent herbivory, yet it is unclear how this specific high-fiber diet might selectively shape the composition of the gut microbiome compared to host phylogeny. To address these questions, we used deep sequencing to investigate the nature and comparative impact of phylogenetic and dietary selection for specific gut microbial membership in three bamboo specialists—the bamboo lemur (Hapalemur griseus, Primates: Lemuridae), giant panda (Ailuropoda melanoleuca, Carnivora: Ursidae), and red panda (Ailurus fulgens, Carnivora: Musteloideadae), as well as two phylogenetic controls—the ringtail lemur (Lemur catta) and the Asian black bear (Ursus thibetanus). We detected significantly higher Shannon diversity in the bamboo lemur (10.029) compared to both the giant panda (8.256; p = 0.0001936) and the red panda (6.484; p = 0.0000029). We also detected significantly enriched bacterial taxa that distinguished each species. Our results complement previous work in finding that phylogeny predominantly governs high-level microbiome community structure. However, we also find that 48 low-abundance OTUs are shared among bamboo specialists, compared to only 8 OTUs shared by the bamboo lemur and its sister species, the ringtail lemur (Lemur catta, a generalist). Our results suggest that deep sequencing is necessary to detect low-abundance bacterial OTUs, which may be specifically adapted to a high-fiber diet. These findings provide a more comprehensive framework for understanding the evolution and ecology of the microbiome as well as the host.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6


  1. Hu Y, Wu Q, Ma S, Ma T, Shan L, Wang X, Nie Y, Ning Z, Yan L, Xiu Y (2017) Comparative genomics reveals convergent evolution between the bamboo-eating giant and red pandas. Proc Natl Acad Sci 114:1081–1086

    Article  PubMed  CAS  Google Scholar 

  2. dos Reis M, Inoue J, Hasegawa M, Asher RJ, Donoghue PC, Yang Z (2012) Phylogenomic datasets provide both precision and accuracy in estimating the timescale of placental mammal phylogeny. Proc Biol Sci 279:3491–3500.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Li Y, Guo W, Han S, Kong F, Wang C, Li D, Zhang H, Yang M, Xu H, Zeng B, Zhao J (2015) The evolution of the gut microbiota in the giant and the red pandas. Sci Rep 5:10185.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. Pozzi L, Nekaris KA-I, Perkin A, Bearder SK, Pimley ER, Schulze H, Streicher U, Nadler T, Kitchener A, Zischler H (2015) Remarkable ancient divergences amongst neglected lorisiform primates. Zool J Linnean Soc 175:661–674

    Article  Google Scholar 

  5. McKenney EA, Rodrigo A, Yoder AD (2015) Patterns of gut bacterial colonization in three primate species. PLoS One 10:e0124618

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Delsuc F, Metcalf JL, Wegener Parfrey L, Song SJ, Gonzalez A, Knight R (2014) Convergence of gut microbiomes in myrmecophagous mammals. Mol Ecol 23:1301–1317.

    Article  PubMed  CAS  Google Scholar 

  7. Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, Schlegel ML, Tucker TA, Schrenzel MD, Knight R (2008) Evolution of mammals and their gut microbes. Science 320:1647–1651

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Muegge BD, Kuczynski J, Knights D, Clemente JC, Gonzalez A, Fontana L, Henrissat B, Knight R, Gordon JI (2011) Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332:970–974.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, Biddinger SB, Dutton RJ, Turnbaugh PJ (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nature 505:559–563.

    Article  PubMed  CAS  Google Scholar 

  10. Stevens CE, Hume ID (1998) Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients. Physiol Rev 78:393–427

    Article  PubMed  CAS  Google Scholar 

  11. Simpson H, Campbell B (2015) Review article: dietary fibre–microbiota interactions. Aliment Pharmacol Ther 42:158–179

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Flynn JJ, Nedbal MA, Dragoo JW, Honeycutt RL (2000) Whence the red panda? Mol Phylogenet Evol 17:190–199

    Article  PubMed  CAS  Google Scholar 

  13. Beijing Zoo BU BAU, Beijing Second Medical College, Beijing Natural History Museum, Shaanxi Zoology Institute (1986) Systematic anatomy and organ-histology. In: Gao F (ed) Morphology of the giant panda1st edn. Science Press, Beijing, pp 189–195

    Google Scholar 

  14. Campbell JL, Eisemann JH, Williams CV, Glenn KM (2000) Description of the gastrointestinal tract of five lemur species: Propithecus tattersalli, Propithecus verreauxi coquereli, Varecia variegata, Hapalemur griseus, and Lemur catta. Am J Primatol 52:133–142

    Article  PubMed  CAS  Google Scholar 

  15. Bleijenberg MCK, Nijboer J (1989) Feeding herbivorous carnivores. In: Glatston AR (ed) Red Panda Biology. SPB Academic Pub., The Hague

  16. Dierenfeld E, Hintz H, Robertson J (1982) Utilization of bamboo by the giant panda. J Nutr 112:636–641

    Article  PubMed  CAS  Google Scholar 

  17. Fulton K, Crissey S, Oftedal O, Ullrey D (1987) Fiber utilization in the red panda. Proceedings of the 7th Dr Scholl Conference on the Nutrition of Captive Wild Animals

  18. Campbell J, Williams C, Eisemann J (2004) Characterizing gastrointestinal transit time in four lemur species using barium-impregnated polyethylene spheres (BIPS). Am J Primatol 64:309–321

    Article  PubMed  CAS  Google Scholar 

  19. Ganzhorn JU (1986) Feeding behavior ofLemur catta andLemur fulvus. Int J Primatol 7:17–30

    Article  Google Scholar 

  20. Zhu L, Wu Q, Dai J, Zhang S, & Wei F (2011) Evidence of cellulose metabolism by the giant panda gut microbiome. Proc Natl Acad Sci 108(43):17714-17719.

  21. Xue Z, Zhang W, Wang L, Hou R, Zhang M, Fei L, Zhang X, Huang H, Bridgewater LC, Jiang Y, Jiang C, Zhao L, Pang X, Zhang Z (2015) The bamboo-eating giant panda harbors a carnivore-like gut microbiota, with excessive seasonal variations. MBio 6:e00022-00015.

    CAS  Article  Google Scholar 

  22. Wei G, Lu H, Zhou Z, Xie H, Wang A, Nelson K, Zhao L (2007) The microbial community in the feces of the giant panda (Ailuropoda melanoleuca) as determined by PCR-TGGE profiling and clone library analysis. Microb Ecol 54:194–202.

    Article  PubMed  CAS  Google Scholar 

  23. Fang W, Fang Z, Zhou P, Chang F, Hong Y, Zhang X, Peng H, Xiao Y (2012) Evidence for lignin oxidation by the giant panda fecal microbiome. PLoS One 7:e50312.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM, Neal PR, Arrieta JM, Herndl GJ (2006) Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci 103:12115–12120.

    Article  PubMed  CAS  Google Scholar 

  25. Ochman H, Worobey M, Kuo C-H, Ndjango J-BN, Peeters M, Hahn BH, Hugenholtz P (2010) Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biol 8:e1000546

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    Article  PubMed  CAS  Google Scholar 

  27. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60

    Article  PubMed  PubMed Central  Google Scholar 

  28. Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10

    Article  Google Scholar 

  29. Yildirim S, Yeoman CJ, Sipos M, Torralba M, Wilson BA, Goldberg TL, Stumpf RM, Leigh SR, White BA, Nelson KE (2010) Characterization of the fecal microbiome from non-human wild primates reveals species specific microbial communities. PLoS One 5:e13963

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Lemos LN, Fulthorpe RR, Triplett EW, Roesch LF (2011) Rethinking microbial diversity analysis in the high throughput sequencing era. J Microbiol Methods 86:42–51.

    Article  PubMed  CAS  Google Scholar 

  31. Lynch MD, Neufeld JD (2015) Ecology and exploration of the rare biosphere. Nat Rev Microbiol 13:217–229.

    Article  PubMed  CAS  Google Scholar 

  32. Biagi E, Nylund L, Candela M, Ostan R, Bucci L, Pini E, Nikkïla J, Monti D, Satokari R, Franceschi C (2010) Through ageing, and beyond: gut microbiota and inflammatory status in seniors and centenarians. PLoS One 5:e10667

  33. Leek JT, Scharpf RB, Bravo HC, Simcha D, Langmead B, Johnson WE, Geman D, Baggerly K, Irizarry RA (2010) Tackling the widespread and critical impact of batch effects in high-throughput data. Nat Rev Genet 11:733–739.

    Article  PubMed  CAS  Google Scholar 

  34. Brooks AW, Kohl KD, Brucker RM, van Opstal EJ, Bordenstein SR (2016) Phylosymbiosis: relationships and functional effects of microbial communities across host evolutionary history. PLoS Biol 14:e2000225

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Hirayama K, Kawamura S, Mitsuoka T, & Tashiro K (1989) The faecal flora of the giant panda (Ailuropoda melanoleuca). J Appl Microbiol 67(4):411-415.

  36. Dill-McFarland KA, Weimer PJ, Pauli JN, Peery MZ, Suen G (2016) Diet specialization selects for an unusual and simplified gut microbiota in two- and three-toed sloths. Environ Microbiol 18:1391–1402

    Article  PubMed  CAS  Google Scholar 

  37. Nagy KA, Montgomery GG (1980) Field metabolic rate, water flux, and food consumption in three-toed sloths (Bradypus variegatus). J Mammal 61:465–472

    Article  Google Scholar 

  38. McNab BK (1988) Energy conservation in a tree-kangaroo (Dendrolagus matschiei) and the red panda (Ailurus fulgens). Physiol Zool 61:280–292

    Article  Google Scholar 

  39. Nie Y, Speakman JR, Wu Q, Zhang C, Hu Y, Xia M, Yan L, Hambly C, Wang L, Wei W (2015) Exceptionally low daily energy expenditure in the bamboo-eating giant panda. Science 349:171–174

    Article  PubMed  CAS  Google Scholar 

  40. Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO (2007) Development of the human infant intestinal microbiota. PLoS Biol 5:e177

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Mackie RI, Sghir A, Gaskins HR (1999) Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr 69:1035s–1045s

    Article  PubMed  CAS  Google Scholar 

  42. Campbell BJ, Yu L, Heidelberg JF, Kirchman DL (2011) Activity of abundant and rare bacteria in a coastal ocean. Proc Natl Acad Sci 108:12776–12781

    Article  PubMed  Google Scholar 

  43. Thauer RK, Kaster A-K, Seedorf H, Buckel W, Hedderich R (2008) Methanogenic archaea: ecologically relevant differences in energy conservation. Nat Rev Microbiol 6:579–591

    Article  PubMed  CAS  Google Scholar 

  44. Ransom-Jones E, Jones DL, McCarthy AJ, McDonald JE (2012) The Fibrobacteres: an important phylum of cellulose-degrading bacteria. Microb Ecol 63:267–281

    Article  PubMed  CAS  Google Scholar 

  45. Barker CJ, Gillett A, Polkinghorne A, Timms P (2013) Investigation of the koala (Phascolarctos cinereus) hindgut microbiome via 16S pyrosequencing. Vet Microbiol 167:554–564.

    Article  PubMed  CAS  Google Scholar 

  46. Köhler T, Stingl U, Meuser K, Brune A (2008) Novel lineages of Planctomycetes densely colonize the alkaline gut of soil-feeding termites (Cubitermes spp.). Environ Microbiol 10:1260–1270

    Article  PubMed  CAS  Google Scholar 

  47. Hongoh Y, Sato T, Dolan MF, Noda S, Ui S, Kudo T, Ohkuma M (2007) The motility symbiont of the termite gut flagellate Caduceia versatilis is a member of the “Synergistes” group. Appl Environ Microbiol 73:6270–6276

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references


The authors would like to thank the staff at the Duke Lemur Center, the National Zoological Park, and Ion Torrent for their help and support. We are also especially grateful to Dr. Robert Fleischer and Dr. Scott Langdon for providing lab space and equipment for DNA extraction and sequencing.


This research was funded in by the National Science Foundation (grant no. 1455848) and the Wainwright fund.

Author information

Authors and Affiliations



Conceived of and designed the experiments: EAM ADY

Collected samples: EAM MM

Analyzed and interpreted the data: EAM AR

Contributed reagents/materials/analysis tools: EAM AR ADY

Wrote the manuscript: EAM MM AR ADY

Corresponding author

Correspondence to Erin A. McKenney.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Research Involving Animals

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures were reviewed and approved by Duke University IACUC under protocol number A203-11-08.

Additional information

AR and ADY are joint senior authors. This study is a contribution from the Duke Lemur Center (DLC publication #1383).

Electronic supplementary material

Figure S1
figure 7

Rarefaction curves (GIF 116 kb)

Figure S4
figure 8

Deep sequencing coverage detects rare membership in complex communities and affects UPGMA clustering. Samples sequenced on the Roche 454 platform (denoted by asterisks) cluster separately from samples sequenced on the Ion Torrent and Illumina MiSeq platforms. This discrepancy is likely driven by different data sizes (see Table S2), as limited sampling fails to detect the presence of rare OTUs. However, within this larger clustering effect, the microbiome tree topology appears to recapitulate host phylogenetic relationships as previously demonstrated [25]. Both OTUs and samples have been ordered by UPGMA hierarchical clustering. (GIF 38 kb)

figure 9

(GIF 128 kb)

High resolution image (EPS 83 kb)

Figure S2

Discrepancies in sequencing sample size drive patterns in Principal Coordinate Analysis of jackknifed unweighted UniFrac distance. UniFrac distance integrates the phylogenetic differences between different OTUs based on presence/absence in each gut community. Ion Torrent data was compared with two published data sets. McKenney et al. [5] used the Illumina MiSeq platform to sequence the v4 region in feces collected from three ringtail lemurs (Lemur catta, diverged from the bamboo lemur 11.8 mya [4]). Li et al. [3] compared V1-V3 regions amplified from 6 captive red pandas, 5 giant pandas, and 6 Asian black bears and sequenced using the 454 GS FLX Titanium platform. Each library was subsampled at a depth of 1280 to match the number of sequences in the smallest library (see Table S2). Ellipsoids were calculated using the InterQuartile Range (IQR) method and plotted to visualize the confidence interval for each sample. (PDF 24 kb)

Figure S3

Boxplot comparison of unweighted UniFrac distance reveals discrepancies between sequencing platforms, as well as phylogenetic effect. UniFrac distance integrates the phylogenetic differences between different OTUs based on presence/absence in each gut community. (PDF 30 kb)

High resolution image (EPS 137 kb)

High resolution image (EPS 73 kb)

Table S1

(DOCX 78 kb)

Table S2

(DOCX 111 kb)

Table S3

(DOCX 167 kb)

Table S4

(DOCX 69 kb)

Additional File 1

(TXT 2 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

McKenney, E.A., Maslanka, M., Rodrigo, A. et al. Bamboo Specialists from Two Mammalian Orders (Primates, Carnivora) Share a High Number of Low-Abundance Gut Microbes. Microb Ecol 76, 272–284 (2018).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI:


  • Gut microbiome
  • Convergent evolution
  • Feeding strategy
  • Bamboo specialist
  • Host-microbiome relationship