Effects of seasonality and previous logging on faecal helminth-microbiota associations in wild lemurs
1.
Pfeiffer, J. K. & Virgin, H. W. Transkingdom control of viral infection and immunity in the mammalian intestine. Science 351, 5872 (2016).
Article CAS Google Scholar
2.
Ramanan, D. et al. Helminth infection promotes colonization resistance via type 2 immunity. Science 352, 608–612 (2016).
ADS CAS PubMed PubMed Central Article Google Scholar
3.
Leclaire, S. & Faulkner, C. T. Gastrointestinal parasites in relation to host traits and group factors in wild meerkats Suricata suricatta. Parasitology 141, 925–933 (2014).
PubMed Article Google Scholar
4.
Kabat, A. M., Srinivasan, N. & Maloy, K. J. Modulation of immune development and function by intestinal microbiota. Trends Immunol. 35, 507–517 (2014).
CAS PubMed PubMed Central Article Google Scholar
5.
McHardy, I. L. X. T. M. et al. HIV Infection is associated with compositional and functional shifts in the rectal mucosal microbiota. Microbiome 1, 1 (2013).
Article Google Scholar
6.
Sekirov, I., Russell, S. & Antunes, L. Gut microbiota in health and disease. Physiol. Rev. 90, 859–904 (2010).
CAS PubMed Article Google Scholar
7.
de Vos, W. M. & de Vos, E. A. Role of the intestinal microbiome in health and disease: from correlation to causation. Nutr. Rev. 70, 45–56 (2012).
Article Google Scholar
8.
Patterson, E. et al. Gut microbiota, the pharmabiotics they produce and host health. Proc. Nutr. Soc. 73, 477–489 (2014).
CAS PubMed Article Google Scholar
9.
Bennett, G. et al. Host age, social group, and habitat type influence the gut microbiota of wild ring-tailed lemurs (Lemur catta). Am. J. Primatol. 1, 1–10 (2016).
Google Scholar
10.
Belongia, E. A. Epidemiology and impact of coinfections acquired from Ixodes ticks. Vector-Borne Zoonotic Dis. 2, 265–273 (2002).
PubMed Article Google Scholar
11.
Eckburg, P. B. et al. Diversity of the human intestinal microbial flora. Science 308, 1635–1638 (2015).
ADS Article Google Scholar
12.
Tompkins, D. M., Dunn, A. M., Smith, M. J. & Telfer, S. Wildlife diseases: from individuals to ecosystems. J. Anim. Ecol. 80, 19–38 (2011).
PubMed Article Google Scholar
13.
Hansen, J., Gulati, A. & Sartor, R. B. The role of mucosal immunity and host genetics in defining intestinal commensal bacteria. Curr. Opin. Gastroenterol. 26, 564–571 (2010).
CAS PubMed PubMed Central Article Google Scholar
14.
Barelli, C. et al. Habitat fragmentation is associated to gut microbiota diversity of an endangered primate: implications for conservation. Sci. Rep. 5, 14862 (2015).
ADS CAS PubMed PubMed Central Article Google Scholar
15.
McKenney, E. A., Rodrigo, A. & Yoder, A. D. Patterns of gut bacterial colonization in three primate species. PLoS ONE 10, 1–18 (2015).
Article CAS Google Scholar
16.
Lozupone, C. A., Stombaugh, J. I., Gordon, J. I., Jansson, J. K. & Knight, R. Diversity, stability and resilience of the human gut microbiota. Nature 489, 220–230 (2012).
ADS CAS PubMed PubMed Central Article Google Scholar
17.
De Filippo, C. et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl. Acad. Sci. 107, 14691–14696 (2010).
ADS PubMed Article Google Scholar
18.
Muegge, B. D. et al. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Proc. Natl. Acad. Sci. 332, 970–974 (2012).
Google Scholar
19.
Wu, G. D. et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 334, 105–108 (2011).
ADS CAS PubMed PubMed Central Article Google Scholar
20.
Boutin, S., Bernatchez, L., Audet, C. & Derom̂e, N. Network analysis highlights complex interactions between pathogen, host and commensal microbiota. PLoS ONE 8, 1–16 (2013).
Google Scholar
21.
Maurice, C. F. et al. Marked seasonal variation in the wild mouse gut microbiota. ISME J. 9, 2423–2434 (2015).
CAS PubMed PubMed Central Article Google Scholar
22.
Amato, K. R. et al. Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. ISME J. 716, 1344–1353 (2013).
Article CAS Google Scholar
23.
Dishaw, L. J. et al. The gut of geographically disparate Ciona intestinalis harbors a core microbiota. PLoS ONE 9, e93386 (2014).
ADS PubMed PubMed Central Article CAS Google Scholar
24.
Amato, K. R. et al. The gut microbiota appears to compensate for seasonal diet variation in the wild black howler monkey (Alouatta pigra). Microb. Ecol. 69, 434–443 (2015).
CAS PubMed Article Google Scholar
25.
Moore, S. L. & Wilson, K. Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297, 2015–2018 (2002).
ADS CAS PubMed Article Google Scholar
26.
Nunn, C. L., Thrall, P. H., Leendertz, F. H. & Boesch, C. The spread of fecally transmitted parasites in socially-structured populations. PLoS ONE 6, e21677 (2011).
ADS CAS PubMed PubMed Central Article Google Scholar
27.
Huffman, M. A., Gotoh, S. & Turner, L. A. Seasonal trends in intestinal nematode infection and medicinal plant use among chimpanzees in the mahale mountains. Tanzania. 38, 111–125 (1997).
Google Scholar
28.
Benavides, J. A. et al. From parasite encounter to infection: multiple-scale drivers of parasite richness in a wild social primate population. Am. J. Phys. Anthropol. 147, 52–63 (2012).
PubMed Article Google Scholar
29.
Barrett, M. A., Brown, J. L., Junge, R. E. & Yoder, A. D. Climate change, predictive modeling and lemur health: assessing impacts of changing climate on health and conservation in Madagascar. Biol. Conserv. 157, 409–422 (2013).
Article Google Scholar
30.
Aivelo, T., Laakkonen, J. & Jernvall, J. Population and individual level dynamics of intestinal microbiota of a small primate. Appl. Environ. Microbiol. 82, 00559–16 (2016).
Article CAS Google Scholar
31.
Nunn, C. C. & Altizer, S. S. Infectious Diseases in Primates: Behavior, Ecology and Evolution (Oxford University, Press, 2006).
Google Scholar
32.
Raharivololona, B. & Ganzhorn, J. Seasonal variations in gastrointestinal parasites excreted by the gray mouse lemur Microcebus murinus in Madagascar. Endanger. Species Res. 11, 113–122 (2010).
Article Google Scholar
33.
Huffman, M. & Chapman, C. Primate Parasite Ecology: the Dynamics and Study of Host–Parasite Relationships (Cambridge University, Press, 2009).
Google Scholar
34.
Setchell, J. M. et al. Parasite prevalence, abundance, and diversity in a semi-free-ranging colony of Mandrillus sphinx. Int. J. Primatol. 28, 1345–1362 (2007).
Article Google Scholar
35.
Maldonado-López, S., Maldonado-López, Y., Gómez-Tagle, C. A., Cuevas-Reyes, P. & Stoner, K. E. Patterns of infection by intestinal parasites in sympatric howler monkey (Alouatta palliata) and spider monkey (Ateles geoffroyi) populations in a tropical dry forest in Costa Rica. Primates 55, 383–392 (2014).
PubMed Article Google Scholar
36.
Caldwell, J. P. Pinworms (enterobius vermicularis). Can. Fam. Physician 28, 306–309 (1986).
Google Scholar
37.
Hanson, C. A., Fuhrman, J. A., Horner-Devine, M. C. & Martiny, J. B. H. Beyond biogeographic patterns: processes shaping the microbial landscape. Nat. Rev. Microbiol. 10, 1–10 (2012).
Article CAS Google Scholar
38.
Keele, B. et al. Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science 313, 523–526 (2006).
ADS CAS PubMed PubMed Central Article Google Scholar
39.
Gillespie, T. R., Chapman, C. A. & Greiner, E. C. Effects of logging on gastrointestinal parasite infections and infection risk in African primates. J. Appl. Ecol. 42, 699–707 (2005).
Article Google Scholar
40.
Chapman, C. A., Gillespie, T. R. & Goldberg, T. L. Primates and the ecology of their infectious diseases: how will anthropogenic change affect host-parasite interactions?. Evol. Anthropol. 14, 134–144 (2005).
Article Google Scholar
41.
McCord, A. I. et al. Fecal microbiomes of non-human primates in Western Uganda reveal species-specific communities largely resistant to habitat perturbation. Am. J. Primatol. 76, 347–354 (2014).
PubMed Article Google Scholar
42.
Chapman, C., Speirs, M. & Gillespie, T. Life on the edge: gastrointestinal parasites from the forest edge and interior primate groups. Am. J. Primatol. 409, 397–409 (2006).
Article Google Scholar
43.
Kowalewski, M. M. et al. Black and gold howler monkeys (Alouatta caraya) as sentinels of ecosystem health: patterns of zoonotic protozoa infection relative to degree of human-primate contact. Am. J. Primatol. 73, 75–83 (2011).
PubMed Article Google Scholar
44.
Chapman, C. A. et al. do food availability, parasitism, and stress have synergistic effects on red colobus populations living in forest fragments?. Am. J. Phys. Anthropol. 131, 525–534 (2006).
PubMed Article Google Scholar
45.
Hughes, S. & Kelly, P. Interactions of malnutrition and immune impairment, with specific reference to immunity against parasites. Parasite Immunol. 28, 577–588 (2006).
CAS PubMed PubMed Central Google Scholar
46.
Angelstam, P. et al. Habitat modelling as a tool for landscape-scale conservation : a review of parameters for focal forest birds source. Ecol. Bull. 51, 427–453 (2004).
Google Scholar
47.
Kreisinger, J., Bastien, G., Hauffe, H. C., Marchesi, J. & Perkins, S. E. (2015) Interactions between multiple helminths and the gut microbiota in wild rodents. Philos. Trans. R. Soc. B Biol. Sci.370, 20140295.
48.
Mutapi, F. The gut microbiome in the helminth infected host. Trends Parasitol. 31, 405–406 (2015).
PubMed Article Google Scholar
49.
Kay, G. L. et al. Differences in the faecal microbiome in schistosoma haematobium infected children vs. uninfected children. PLoS Negl. Trop. Dis. 9, e0003861 (2015).
PubMed PubMed Central Article CAS Google Scholar
50.
Lee, S. C. et al. Helminth colonization is associated with increased diversity of the gut microbiota. PLoS Negl. Trop. Dis. 8, 1–10 (2014).
ADS Google Scholar
51.
Morton, E. R. et al. Variation in rural African gut microbiomes is strongly shaped by parasitism and diet. bioRxiv (2015).
52.
Cooper, P. et al. Patent human infections with the whipworm, Trichuris trichiura, are not associated with alterations in the faecal microbiota. PLoS ONE 8, 1–10 (2013).
Google Scholar
53.
Cantacessi, C. et al. Impact of experimental hookworm infection on the human gut microbiota. J. Infect. Dis. 210, 1–4 (2014).
Article CAS Google Scholar
54.
Houlden, A. et al. Chronic Trichuris muris infection in C57BL/6 mice causes significant changes in host microbiota and metabolome: effects reversed by pathogen clearance. PLoS ONE 10, e0125945 (2015).
PubMed PubMed Central Article CAS Google Scholar
55.
McKenney, E. A., Greene, L. K., Drea, C. M. & Yoder, A. D. Down for the count: cryptosporidium infection depletes the gut microbiome in Coquerel’s sifakas. Microb. Ecol. Health Dis. 28, 1335165 (2017).
PubMed PubMed Central Google Scholar
56.
Fogel, A. T. The gut microbiome of wild lemurs: a comparison of sympatric lemur catta and propithecus verreauxi. Folia Primatol. 86, 85–95 (2015).
PubMed Article Google Scholar
57.
Springer, A. et al. Patterns of seasonality and group membership characterize the gut microbiota in a longitudinal study of wild Verreaux’s sifakas (Propithecus verreauxi). Ecol. Evol. 7, 5732–5745 (2017).
PubMed PubMed Central Article Google Scholar
58.
Walk, S. T., Blum, A. M., Ewing, S. A. S., Weinstock, J. V. & Young, V. B. Alteration of the murine gut microbiota during infection with the parasitic helminth Heligmosomoides polygyrus. Inflamm. Bowel Dis. 16, 1841–1849 (2010).
PubMed PubMed Central Article Google Scholar
59.
Li, R. W. et al. Alterations in the porcine colon microbiota induced by the gastrointestinal nematode Trichuris suis. Infect. Immun. 80, 2150–2157 (2012).
CAS PubMed PubMed Central Article Google Scholar
60.
Rausch, S. et al. Small intestinal nematode infection of mice is associated with increased enterobacterial loads alongside the intestinal tract. PLoS ONE 8, 1–13 (2013).
Article CAS Google Scholar
61.
Irwin, M. T., Johnson, S. E. & Wright, P. C. The state of lemur conservation in south-eastern Madagascar: population and habitat assessments for diurnal and cathemeral lemurs using surveys, satellite imagery and GIS. Oryx 39, 204–218 (2005).
Article Google Scholar
62.
Markolf, M. et al. True lemurs…true species: species delimitation using multiple data sources in the brown lemur complex. BMC Evol. Biol. 13, 233 (2013).
PubMed PubMed Central Article Google Scholar
63.
Wright, P. et al. Long-term lemur research at Centre Valbio, Ranomafana National Park, Madagascar. in Long-term field studies of primates (eds. Kappeler, P. M. & Watts, D. P.) 67–100 (Springer, Berlin Heidelberg, 2012). https://doi.org/10.1007/978-3-642-22514-7
64.
de Winter, I. et al. Occupancy strongly influences faecal microbial composition of wild lemurs. Microbiol. Ecol. 94, 1–13 (2018).
Google Scholar
65.
IUCN. The IUCN Red List of Threatened Species. Version 2016–1. (2016).
66.
Chabaud, A. G. & Petter, A. J. Les nématodes parasites de Lémuriens malgaches, II Un nouvel oxyure: Lemuricola contagiosus. Mém. Inst. Sci. MadagascarA, 127–158 (1959).
67.
Chabaud, A. G., Brygoo, E.-R. & Petter, A.-J. Les Nématodes parasites de Lémuriens malgaches VI. Description de six espèces nouvelles et conclusions générales. Ann. Parasitol. Hum. Comparée 181–214 (1965).
68.
Irwin, M. T. & Raharison, J. A review of the endoparasites of the lemurs of Madagascar. 66–93 (2009).
69.
Schwitzer, N. et al. Parasite prevalence in blue-eyed black lemurs Eulemur flavifrons in differently degraded forest fragments. Endanger. Species Res. 12, 215–225 (2010).
Article Google Scholar
70.
Junge, R. E. & Louis, E. E. Biomedical evaluation of black lemurs (Eulemur macaco macaco) in Lokobe Reserve, Madagascar. J. Zoo Wildl. Med. 38, 67–76 (2007).
PubMed Article Google Scholar
71.
Nègre, A., Tarnaud, L., Roblot, J. F., Gantier, J. C. & Guillot, J. Plants consumed by Eulemur fulvus in Comoros Islands (Mayotte) and potential effects on intestinal parasites. Int. J. Primatol. 27, 1495–1517 (2006).
Article Google Scholar
72.
Junge, R. E. et al. Comparison of biomedical evaluation for white-fronted brown lemurs (Eulemur fulvus albifrons) from four sites in Madagascar. J. Zoo Wildl. Med. 39, 567–575 (2008).
PubMed Article Google Scholar
73.
Rajilić-Stojanović, M., Heilig, H. G. H. J., Tims, S., Zoetendal, E. G. & De Vos, W. M. Long-term monitoring of the human intestinal microbiota composition. Environ. Microbiol. 15, 1146–1159 (2013).
Article CAS Google Scholar
74.
Crowley, B. E., McGoogan, K. C. & Lehman, S. M. Edge effects on foliar stable isotope values in a Madagascan tropical dry forest. PLoS ONE 7, e44538 (2012).
ADS CAS PubMed PubMed Central Article Google Scholar
75.
Sato, H., Ichino, S. & Hanya, G. Dietary modification by common brown lemurs (Eulemur fulvus) during seasonal drought conditions in western Madagascar. Primates 55, 219–230 (2014).
PubMed Article Google Scholar
76.
Styger, E., Rakotoarimanana, J. E. M., Rabevohitra, R. & Fernandes, E. C. M. Indigenous fruit trees of Madagascar: potential components of agroforestry systems to improve human nutrition and restore biological diversity. Agrofor. Syst. 46, 289–310 (1999).
Article Google Scholar
77.
Sato, H. Habitat shifting by the common brown lemur (Eulemur fulvus fulvus): a response to food scarcity. Primates 54, 229–235 (2013).
PubMed Article Google Scholar
78.
Guernier, V., Hochberg, M. E. & Guégan, J. F. Ecology drives the worldwide distribution of human diseases. PLoS Biol. 2, e141 (2004).
PubMed PubMed Central Article CAS Google Scholar
79.
Froeschke, G., Harf, R., Sommer, S. & Matthee, S. Effects of precipitation on parasite burden along a natural climatic gradient in southern Africa: implications for possible shifts in infestation patterns due to global changes. Oikos 119, 1029–1039 (2010).
Article Google Scholar
80.
Brooker, S., Clements, A. C. A. & Bundy, D. A. P. Global epidemiology, ecology and control of soil-transmitted helminth infections. Adv. Parasitol. 62, 221–261 (2006).
CAS PubMed PubMed Central Article Google Scholar
81.
Luong, L. T., Grear, D. A. & Hudson, P. J. Manipulation of host-resource dynamics impacts transmission of trophic parasites. Int. J. Parasitol. 44, 737–742 (2014).
PubMed Article Google Scholar
82.
Wright, P. C., Vololontiana, R. & Pochron, S. T. The key to Madagascar frugivores. in Tropical fruits and frugivores 121–138 (Springer, Dordrecht, 2005).
83.
Tecot, S. R. Seasonality and predictability: The hormonal and behavioral responses of the redbellied lemur (Eulemur rubriventer) in Ranomafana National Park, southeastern Madagascar (University of Texas, Austin, 2008).
Google Scholar
84.
Clough, D. Gastro-intestinal parasites of red-fronted lemurs in Kirindy Forest, western Madagascar. J. Parasitol. 96, 245–251 (2010).
PubMed Article Google Scholar
85.
Overdorff, D. J. & Johnson, S. E. Eulemur, true lemurs. in The Natural History of Madagascar (eds. Goodman, S. M. & Benstead, J.) 1320–1324 (University of Chicago Press, Chiago, 2003).
86.
Ostner, J., Kappeler, P. M. & Heistermann, M. Androgen and glucocorticoid levels reflect seasonally occurring social challenges in male redfronted lemurs (Eulemur fulvus rufus). Behav. Ecol. Sociobiol. 62, 627–638 (2008).
PubMed Article Google Scholar
87.
Johns, A. D. & Skorupa, J. P. Responses of rain-forest primates to habitat disturbance: a review. Int. J. Primatol. 8, 157–191 (1987).
Article Google Scholar
88.
Wright, P. & Andriamihaja, B. Making a rain forest national park work in Madagascar: Ranomafana National Park and its long-term research commitment. in Making parks work: Strategies for preserving tropical nature 112–136 (2002).
89.
de Winter, I. I. et al. Past disturbance effects on forest structure and lemur abundances (Biol, Conserv, 2018).
Google Scholar
90.
Di Rienzi, S. C. et al. The human gut and groundwater harbor non-photosynthetic bacteria belonging to a new candidate phylum sibling to cyanobacteria. Elife 2, 1 (2013).
Article CAS Google Scholar
91.
Vitazkova, S. & Wade, S. Effects of ecology on the gastrointestinal parasites of Alouatta pigra. Int. J. Primatol. 28(28), 1327–1343 (2007).
Article Google Scholar
92.
Martinez-Mota, R. The effects of habitat disturbance, host traits, and host physiology on patterns of gastrointestinal parasite infection in black howler monkeys (Alouatta pigra). PhD dissertation, Department ofAnthropology, University of Illinois (2015).
93.
Arneberg, P. Host population density and body mass as determinants of species richness in parasite communities: comparative analyses of directly transmitted nematodes of mammals. Ecography 25, 88–94 (2002).
Article Google Scholar
94.
Reynolds, L. A. et al. Commensal-pathogen interactions in the intestinal tract: lactobacilli promote infection with, and are promoted by, helminth parasites. Gut Microbes 5, 522–532 (2014).
PubMed PubMed Central Article Google Scholar
95.
Zhernakova, A. et al. Population-based metagenomics analysis reveals markers for gut microbiome composition and diversity. Science 352, 565–569 (2016).
ADS CAS PubMed PubMed Central Article Google Scholar
96.
Hayes, K. S. et al. Exploitation of the intestinal microflora by the parasitic nematode Trichuris muris. Science 328, 1391–1394 (2010).
ADS CAS PubMed PubMed Central Article Google Scholar
97.
Reynolds, L. A., Finlay, B. B. & Maizels, R. M. Cohabitation in the intestine: interactions among helminth parasites, bacterial microbiota, and host immunity. J. Immunol. 195, 4059–4066 (2015).
CAS PubMed PubMed Central Article Google Scholar
98.
Pedersen, A. B., Altizer, S., Poss, M., Cunningham, A. & Nunn, C. L. Patterns of host specificity and transmission among parasites of wild primates. Int. J. Parasitol. 35, 647–657 (2005).
PubMed Article Google Scholar
99.
Goodman, S. M. et al. The distribution and conservation of bats in the dry regions of Madagascar. Anim. Conserv. 8, 153–165 (2005).
Article Google Scholar
100.
Irwin, M. T. et al. Patterns of species change in anthropogenically disturbed forests of Madagascar. Biol. Conserv. 143, 2351–2362 (2010).
Article Google Scholar
101.
Balko, E. A. & Underwood, H. B. Effects of forest structure and composition on food availability for Varecia variegata at Ranomafana National Park, Madagascar. Am. J. Primatol. 66, 45–70 (2005).
PubMed Article Google Scholar
102.
Köhler, J., Glaw, F. & Vences, M. First record of Mabuya comorensis (Reptilia: Scincidae) for Madagascar, with notes on the herpetofauna of Nosy Tanikely. Boll. Mus. Reg. Sci. Nat. Torino 15, 75–82 (1998).
Google Scholar
103.
Erhart, E. M. & Overdorff, D. J. Population demography and social structure changes in Eulemur fulvus rufus from 1988 to 2003. Am. J. Phys. Anthropol. 136, 183–193 (2008).
PubMed Article Google Scholar
104.
Johnson, S. E., Gordon, A. D., Stumpf, R. M., Overdorff, D. J. & Wright, P. C. Morphological variation in populations of Eulemur albocollaris and E. fulvus rufus. Int. J. Primatol. 26, 1399–1416 (2005).
Article Google Scholar
105.
Pyritz, L. W., Kappeler, P. M. & Fichtel, C. Coordination of group movements in wild red-fronted lemurs (Eulemur rufifrons): processes and influence of ecological and reproductive seasonality. Int. J. Primatol. 32, 1325–1347 (2011).
PubMed PubMed Central Article Google Scholar
106.
Tecot, S. R. It’s all in the timing: birth seasonality and infant survival in Eulemur rubriventer. Int. J. Primatol. 31, 715–735 (2010).
Article Google Scholar
107.
Mittermeier, R. A. et al. Lemur diversity in Madagascar. Int. J. Primatol. 29, 1607–1656 (2008).
Article Google Scholar
108.
Overdorff, D. Similarities, differences, and seasonal patterns in the diets of Eulemur rubriventer and Eulemur rufifrons in the Ranomafana National Park, Madagascar. Int. J. Primatol. 14, 721–753 (1993).
Article Google Scholar
109.
Berg, W., Jolly, A., Rambeloarivony, H., Andrianome, V. & Rasamimanana, H. A scoring system for coat and tail condition in ringtailed lemurs, Lemur catta. Am. J. Primatol. 71, 183–190 (2009).
PubMed Article Google Scholar
110.
Van Gool, T., Weijts, R., Lommerse, E. & Mank, T. G. Triple faeces test: an effective tool for detection of intestinal parasites in routine clinical practice. Eur. J. Clin. Microbiol. Infect. Dis. 22, 284–290 (2003).
PubMed Article Google Scholar
111.
Yu, Z. & Morrison, M. Improved extraction of PCR-quality community DNA from digesta and fecal samples. Biotechniques 36, 808–812 (2004).
CAS PubMed Article Google Scholar
112.
Salonen, A. et al. Comparative analysis of fecal DNA extraction methods with phylogenetic microarray: effective recovery of bacterial and archaeal DNA using mechanical cell lysis. J. Microbiol. Methods 81, 127–134 (2010).
CAS PubMed Article Google Scholar
113.
Tian, L. et al. Effects of pectin supplementation on the fermentation patterns of different structural carbohydrates in rats. Mol. Nutr. Food Res. 1–11 (2016).
114.
van den Bogert, B., de Vos, W. M., Zoetendal, E. G. & Kleerebezem, M. Microarray analysis and barcoded pyrosequencing provide consistent microbial profiles depending on the source of human intestinal samples. Appl. Environ. Microbiol. 77, 2071–2080 (2011).
PubMed PubMed Central Article CAS Google Scholar
115.
Daims, H., Brühl, A., Amann, R., Schleifer, K. H. & Wagner, M. The domain-specific probe EUB338 is insufficient for the detection of all Bacteria: development and evaluation of a more comprehensive probe set. Syst. Appl. Microbiol. 22, 434–444 (1999).
CAS PubMed Article Google Scholar
116.
Ramiro-Garcia, J. et al. NG-Tax, a highly accurate and validated pipeline for analysis of 16S rRNA amplicons from complex biomes. NF1000 Res. 5, 5 (2016).
Google Scholar
117.
Dryden, M. W., Payne, P. A., Ridley, R. & Smith, V. Comparison of common fecal flotation techniques for the recovery of parasite eggs and oocysts. Vet. Ther. 6, 15–28 (2005).
CAS PubMed Google Scholar
118.
Gillespie, T. R. Noninvasive assessment of gastrointestinal parasite infections in free-ranging primates. Int. J. Primatol. 27, 1129–1143 (2006).
Article Google Scholar
119.
Gillespie, T. R. & Chapman, C. A. Prediction of parasite infection dynamics in primate metapopulations based on attributes of forest fragmentation. Conserv. Biol. 20, 441–448 (2006).
PubMed Article Google Scholar
120.
Zeger, S. L., Liang, K.-Y. & Albert, P. S. Models for longitudinal data: a generalized estimating equation approach. Biometrics 44, 1049–1060 (1988).
MathSciNet CAS PubMed MATH Article Google Scholar
121.
Scrucca, L. Dispmod: Dispersion Models. R package version 1.1. (2012). https://cran.r-project.org/package=dispmod.
122.
Nakagawa, S. & Schielzeth, H. A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol. Evol. 4, 133–142 (2013).
Article Google Scholar
123.
R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria (2018). https://www.r-project.org/.
124.
Bates, D., Maechler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).
Article Google Scholar
125.
Lenth, R. V. Least-squares means: the R package lsmeans. J. Stat. Softw.69, (2016).
126.
Fox, J., Friendly, M. & Weisberg, S. Hypothesis tests for multivariate linear models using the car package. R J. 5, 39–52 (2013).
Article Google Scholar
127.
Hartig, F. DHARMa: Residual Diagnostics for Hierarchical (multi-level/mixed) Regression Models. R package version 0.1. 5. (2017).
128.
Barton, K. MuMIn: Multi-model Inference, R package version 0.12. 0. (2009). More