Altitude and human disturbance are associated with helminth diversity in an endangered primate, Procolobus gordonorum

Autoři: Claudia Barelli aff001;  Viviana Gonzalez-Astudillo aff003;  Roger Mundry aff005;  Francesco Rovero aff002;  Heidi C. Hauffe aff001;  Thomas R. Gillespie aff003
Působiště autorů: Department of Biodiversity and Molecular Ecology, Research and Innovation Centre, Fondazione E. Mach, San Michele all’Adige, Trento, Italy aff001;  MUSE–Science Museum, Tropical Biodiversity Section, Trento, Italy aff002;  Department of Environmental Sciences and Program in Population Biology, Ecology and Evolutionary Biology, Emory University, Atlanta, GA, United States of America aff003;  Pathology Resident, California Animal Health & Food Safety Laboratory, University of California, Davis, CA, United States of America aff004;  Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany aff005;  Department of Biology, University of Florence, Florence, Italy aff006;  Department of Environmental Health, Rollins School of Public Health, Emory University, Atlanta, GA, United States of America aff007
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
prolekare.web.journal.doi_sk: 10.1371/journal.pone.0225142


Gastrointestinal parasites colonizing the mammalian gut influence the host immune system and health. Parasite infections, mainly helminths, have been studied intensively in both humans and non-human animals, but relatively rarely within a conservation framework. The Udzungwa red colobus monkey (Procolobus gordonorum) is an endangered endemic primate species living in the Udzungwa Mountains of Tanzania, a global biodiversity hotspot. Since this endemic primate species is highly sensitive to human disturbance, here we investigate whether habitat type (driven by natural and human-induced factors) is associated with helminth diversity. Using standard flotation and sedimentation techniques, we analyzed 251 fecal samples belonging to 25 social groups from four different forest blocks within the Udzungwa Mountains. Five parasitic helminth taxa were recovered from Udzungwa red colobus, including Trichuris sp., Strongyloides fulleborni, S. stercoralis, a strongylid nematode and Colobenterobius sp. We used Generalized Linear Mixed Models to explore the contribution of habitat type, altitude and fecal glucocorticoid levels (as biomarkers of stress) in predicting gut parasite variation. Although some parasites (e.g., Trichuris sp.) infected more than 50% of individuals, compared to others (e.g., Colobenterobius sp.) that infected less than 3%, both parasite richness and prevalence did not differ significantly across forests, even when controlling for seasonality. Stress hormone levels also did not predict variation in parasite richness, while altitude could explain it resulting in lower richness at lower altitudes. Because human activities causing disturbance are concentrated mainly at lower altitudes, we suggest that protection of primate forest habitat preserves natural diversity at both macro- and microscales, and that the importance of the latter should not be underestimated.

Klíčová slova:

Colobus – Forests – Helminths – Monkeys – Nematode infections – Parasitic diseases – Primates – Trichuris


1. Maizels RM, Balic A, Gomez-Escobar N, Nair M, Taylor MD, Allen JE. Helminth parasites–masters of regulation. Immunol Rev. 2004; 201: 89–116. doi: 10.1111/j.0105-2896.2004.00191.x 15361235

2. Elias D, Britton S, Kassu A, Akuffo H. Chronic helminth infections may negatively influence immunity against tuberculosis and other diseases of public health importance. Expert Rev Anti Infect Ther. 2007; 5: 475–484. doi: 10.1586/14787210.5.3.475 17547511

3. WHO. Soil-transmitted helminth infections. Fact sheet No 366. (accessed 2019); 2019.

4. Hotez PJ, Brindley PJ, Bethony JM, King CH, Pearce EJ, Jacobson J. Helminth infections: the great neglected tropical diseases. J Clin Invest. 2008; 118: 1311–1321. doi: 10.1172/JCI34261 18382743

5. Bilbo SD, Wray GA, Perkins SE, Parker W. Reconstitution of the human biome as the most reasonable solution for epidemics of allergic and autoimmune diseases. Med Hypotheses. 2011; 77: 494–504. doi: 10.1016/j.mehy.2011.06.019 21741180

6. Loke P, Lim YAL. Helminths and the microbiota: parts of the hygiene hypothesis. Parasite Immunol. 2015; 37: 314–323. doi: 10.1111/pim.12193 25869420

7. Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, et al. Biodiversity loss and its impact on humanity. Nature. 2012; 486: 59–67. doi: 10.1038/nature11148 22678280

8. Rogovin K, Randall JA, Kolosova I, Moshkin M. Social correlates of stress in adult males of the great gerbil, Rhombomys opimus, in years of high and low population densities. Horm Behav. 2003; 43: 132–139. doi: 10.1016/s0018-506x(02)00028-4 12614643

9. Chapman CA, Saj TL, Snaith TV. Temporal dynamics of nutrition, parasitism, and stress in colobus monkeys: implications for population regulation and conservation. Am J Phys Anthropol. 2007; 134: 240–250. doi: 10.1002/ajpa.20664 17596853

10. Trejo-Macías G, Estrada A, Cabrera MÁM. Survey of helminth parasites in populations of Alouatta palliata mexicana and A. pigra in continuous and in fragmented habitat in southern Mexico. Int J Primatol. 2007; 28: 931–945.

11. Mbora DNM, McPeek MA. Host density and human activities mediate increased parasite prevalence and richness in primates threatened by habitat loss and fragmentation. J Anim Ecol. 2009; 78: 210–218. doi: 10.1111/j.1365-2656.2008.01481.x 19120603

12. Marcogliese DJ, Pietrock M. Combined effects of parasites and contaminants on animal health: parasites do matter. Trends Parasitol. 2011; 27: 123–130. doi: 10.1016/ 21144800

13. Gillespie TR, Chapman CA, Greiner EC. Effects of logging on gastrointestinal parasite infections and infection risk in African primate populations. J Appl Ecol. 2005; 42: 699–707.

14. Gillespie TR, Chapman CA. Prediction of parasite infection dynamics in primate metapopulations based on attributes of forest fragmentation. Conserv Biol. 2006; 20: 441–448. doi: 10.1111/j.1523-1739.2006.00290.x 16903105

15. Gillespie TR, Chapman CA. Forest fragmentation, the decline of an endangered primate, and changes in host-parasite interactions relative to an unfragmented forest. Am J Primatol. 2008; 70: 222–230. doi: 10.1002/ajp.20475 17879941

16. Hussain S, Ram MS, Kumar A, Shivaji S, Umapathy G. Human presence increases parasitic load in endangered lion-tailed macaques (Macaca silenus) in its fragmented rainforest habitats in southern India. PLoS ONE. 2013; 8: e63685. doi: 10.1371/journal.pone.0063685 23717465

17. Salzer JS, Carroll D, Williams-Newkirk A, Lang S, Kerbis-Peterhans J, Rwego I, et al. Effects of anthropogenic and demographic factors on patterns of parasitism in African small mammal communities. Parasitology. 2015; 142: 512–522. doi: 10.1017/S0031182014001450 25262668

18. Jrijer J, Bordes F, Morand S, Neifar L. Gastro-intestinal helminth parasites of the common North African gerbil Meriones shawi (Duvernoy) in Tunisia: Parasites diversity and habitat anthropization effect. Trop Biomed. 2016; 33: 702–710.

19. Martínez-Mota R, Pozo-Montuy G, Bonilla Sánchez YM, Gillespie TR. Effects of anthropogenic stress on the presence of parasites in a threatened population of black howler monkeys (Alouatta pigra). Therya. 2018; 9: 161–169.

20. Rakotoniaina JH, Kappeler PM, Ravoniarimbinina P, Pechouskova E, Hämäläinen AM, Grass J, et al. Does habitat disturbance affect stress, body condition and parasitism in two sympatric lemurs? Conserv Physiol. 2016; 4: cow034. doi: 10.1093/conphys/cow034 27656285

21. Estrada A, Garber PA, Rylands AB, Roos C, Fernandez-Duque E, Di Fiore A, K. et al. Impending extinction crisis of the world´s primates: why primates matter. Sci Adv. 2017; 3: e1600946. doi: 10.1126/sciadv.1600946 28116351

22. Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GA, Kent J. Biodiversity hotspots for conservation priorities. Nature. 2000; 403: 853–858. doi: 10.1038/35002501 10706275

23. Mittermeier RA, Robles Gil P, Hoffmann M, Pilgrim J, Brooks T, Mittermeier CG, et al. Hotspots Revisited: Earth’s Biologically Richest and Most Endangered Ecoregions. Mexico City, Mexico: CEMEX; 2004.

24. Rovero F, Menegon M, Fjeldså J, Collett L, Doggart N, Leonard C, et al. Targeted vertebrate surveys enhance the faunal importance and improve explanatory models within the Eastern Arc Mountains of Kenya and Tanzania. Divers Distrib. 2014; 20: 1438–1449.

25. Laurance WF, Useche DC, Rendeiro J, Kalka M, Bradshaw CJ, Sloan SP, et al. Averting biodiversity collapse in tropical forest protected areas. Nature. 2012; 489: 290–294. doi: 10.1038/nature11318 22832582

26. Rovero F, Mtui AS, Kitegile AS, Nielsen MR. Hunting or habitat degradation? Decline of primate populations in Udzungwa Mountains, Tanzania: An analysis of threats. Biol Conserv. 2012; 146: 89–96.

27. Rovero F, Mtui A, Kitegile A, Jacob P, Araldi A, Tenan S. Primates decline rapidly in unprotected forests: Evidence from a monitoring program with data constraints. PLoS ONE. 2015; 10: e0118330. doi: 10.1371/journal.pone.0118330 25714404

28. Cristóbal-Azkarate J, Hervier B, Vegas-Carrillo S, Osorio-Sarabia D, Rodríguez-Luna E, Vea JJ. Parasitic infections of three Mexican howler monkey groups (Alouatta palliata mexicana) living in forest fragments in Mexico. Primates. 2010; 51: 231–239. doi: 10.1007/s10329-010-0193-7 20224913

29. Trejo-Macías G, Estrada A. Risk factors connected to gastrointestinal parasites in mantled Alouatta palliata mexicana and black howler monkeys Alouatta pigra living in continuous and in fragmented rainforests in Mexico. Curr Zool. 2012; 58: 375–383.

30. Gillespie TR, Barelli C, Heistermann M. Effects of social status and stress on patterns of gastrointestinal parasitism in wild white‐handed gibbons (Hylobates lar). Am J Phys Anthropol. 2013; 150: 602–608. doi: 10.1002/ajpa.22232 23440877

31. Gaetano TJ, Danzy J, Mtshali MS, Theron N, Schmitt CA, Grobler JP, et al. Mapping correlates of parasitism in wild South African vervet monkeys (Chlorocebus aethiops). S Afr J Wildl Res. 2014; 44: 56–70.

32. Martínez-Mota R, Garber PA, Palme R, Gillespie TR. The relative effects of reproductive condition, stress, and seasonality on patterns of parasitism in wild female black howler monkeys (Alouatta pigra). Am J Primatol. 2017; 79: e22669.

33. Marshall AR, Jørgensbye HIO, Rovero F, Platts PJ, White PCL, Lovett JC. The species-area relationship and confounding variables in a threatened monkey community. Am J Primatol. 2010; 72: 325–36. doi: 10.1002/ajp.20787 20039329

34. Barelli C, Mundry R, Araldi A, Hodges K, Rocchini D, Rovero F. Modeling primate abundance in complex landscapes: A case study from the Udzungwa Mountains of Tanzania. Int J Primatol. 2015; 36: 209–226.

35. Ruiz-Lopez MJ, Barelli C, Rovero F, Hodges K, Roos C, Peterman WE, Ting N. A landscape genetics approach demonstrates the effects of human disturbance on a primate indicator species in an East African biodiversity hotspot. Heredity. 2016; 116: 167–176. doi: 10.1038/hdy.2015.82 26374237

36. Cavada N, Tenan S, Barelli C, Rovero F. Effects of anthropogenic disturbance on primate density at the landscape scale. Conserv Biol. 2018; doi: 10.1111/cobi.13269 30561170

37. Araldi A, Barelli C, Hodges K, Rovero F. Density estimation of the endangered Udzungwa red colobus (Procolobus gordonorum) and other arboreal primates in the Udzungwa Mountains using systematic distance sampling. Int J Primatol. 2014; 35: 941–956.

38. Barelli C, Rovero F, Hodges K, Araldi A, Heistermann M. Physiological stress levels in the endemic and endangered Udzungwa red colobus vary with elevation. Afr Zool. 2015; 50: 23–30.

39. Barelli C, Albanese D, Donati C, Pindo M, Dallago C, Rovero F, et al. Habitat fragmentation is associated to gut microbiota diversity of an endangered primate: implications for conservation. Sci Rep. 2015; 5: 14862. doi: 10.1038/srep14862 26445280

40. Gillespie TR. Noninvasive assessment of gastrointestinal parasite infections in free-ranging primates. Int J Primatol. 2006; 27: 1129–1143.

41. Gillespie TR, Lonsdorf EV, Canfield EP, Meyer DJ, Nadler Y, Raphael J, et al. Demographic and ecological effects on patterns of parasitism in eastern chimpanzees (Pan troglodytes schweinfurthii) in Gombe National Park, Tanzania. Am J Phys Anthropol. 2010; 143: 534–544. doi: 10.1002/ajpa.21348 20623606

42. Ziegler TE, Wittwer DJ. Fecal steroid research in the field and laboratory: Improved methods for storage, transport, processing, and analysis. Am J Primatol. 2005; 67: 159–174. doi: 10.1002/ajp.20175 16163716

43. Shutt K, Setchell JM, Heistermann M. Non-invasive monitoring of physiological stress in the Western lowland gorilla (Gorilla gorilla gorilla): validation of a fecal glucocorticoid assay and methods for practical application in the field. Gen Comp Endocrinol. 2012; 179: 167–177. doi: 10.1016/j.ygcen.2012.08.008 22926327

44. Khan MZ, Altmann J, Isani SS, Yu J. A matter of time: evaluating the storage of fecal samples for steroid analysis. Gen Comp Endocrinol. 2002; 128: 57–64. doi: 10.1016/s0016-6480(02)00063-1 12270788

45. Rimbach R, Heymann EW, Link A, Heistermann M. Validation of an enzyme immunoassay for assessing adrenocortical activity and evaluation of factors that affect levels of fecal glucocorticoid metabolites in two New World primates. Gen Comp Endocrinol. 2013; 191: 13–23. doi: 10.1016/j.ygcen.2013.05.010 23707497

46. Wheeler BC, Tiddi B, Kalbitzer U, Visalberghi E, Heistermann M. Methodological considerations in the analysis of fecal glucocorticoid metabolites in tufted capuchins (Cebus apella). Int J Primatol. 2013; 34: 879–898. doi: 10.1007/s10764-013-9703-y 24098064

47. Kalbitzer M, Heistermann M. Long-term storage effects in steroid metabolite extracts from baboon (Papio sp.) faeces–a comparison of three commonly applied storage methods. Meth Ecol Evol. 2013; 4: 593–600.

48. Bush AO, Lafferty KD, Lotz JM, Shostak AW. Parasitology meets ecology on its own terms: Margolis et al. Revisited. J Parasitol. 1997; 83: 575–583. 9267395

49. Greiner EC, McIntosh A. Collection methods and diagnostic procedures for primate parasitology. In: Huffman MA, Chapman CA, editors. Primate Parasite Ecology: the Dynamics and Study of Host-parasite Relationships. Cambridge: Cambridge University Press; 2009. pp. 3–27.

50. Baayen RH. Analyzing Linguistic Data. Cambridge: Cambridge University Press; 2008.

51. McCullagh P & Nelder JA. Generalized linear models. Chapman and Hall. London; 1989.

52. Hilbe JM. Negative Binomial Regression. Cambridge University Press, Cambridge, New Jersey; 2011.

53. Stolwijk AM, Straatman H, Zielhuis GA. Studying seasonality by using sine and cosine functions in regression analysis. J Epidemiol Community Health. 1999; 53: 235–238. doi: 10.1136/jech.53.4.235 10396550

54. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White J-SS. Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol. 2009; 24: 127–135. doi: 10.1016/j.tree.2008.10.008 19185386

55. Forstmeier W, Schielzeth H. Cryptic multiple hypotheses testing in linear models: overestimated effect sizes and the winner’s curse. Behav Ecol Sociobiol. 2011; 65: 47–55. doi: 10.1007/s00265-010-1038-5 21297852

56. Quinn GP, Keough MJ. Experimental Designs and Data Analysis for Biologists. Cambridge: Cambridge University Press; 2002.

57. Field A. Discovering Statistics using SPSS. London: Sage Publications; 2005.

58. Fox J, Monette G. Generalized Collinearity Diagnostics. J Am Stat Assoc. 1992; 87: 178–183.

59. R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna, Austria; 2019.

60. Bates D, Mächler M, Bolker B, Walker S. Fitting Linear Mixed-Effects Models Using lme4; 2015.

61. Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Maechler M, Bolker BM. glmmTMB Balances Speed and Flexibility Among Packages for Zero-inflated Generalized Linear Mixed Modeling; 2017.

62. Fox J, Weisberg S. An R Companion to Applied Regression. 2nd ed. Thousand Oaks CA: Sage; 2011.

63. Dobson AJ. An Introduction to Generalized Linear Models. Chapman & Hall/CRC, Boca Raton; 2002.

64. Barr DJ, Levy R, Scheepers C, Tily HJ. Random effects structure for confirmatory hypothesis testing: Keep it maximal. J Memory Lang. 2013; 68: 255–278.

65. Clough D, Heistermann M, Kappeler PM. Host intrinsic determinants and potential consequences of parasite infection in free‐ranging red‐fronted lemurs (Eulemur fulvus rufus). Am J Phys Anthropol. 2010; 142: 441–452. doi: 10.1002/ajpa.21243 20091843

66. Young H, Griffin RH, Wood CL, Nunn CL. Does habitat disturbance increase infectious disease risk for primates?. Ecol Lett. 2013; 16: 656–663. doi: 10.1111/ele.12094 23448139

67. Vitazkova SK, Wade SE. Parasites of free‐ranging black howler monkeys (Alouatta pigra) from Belize and Mexico. Am J Primatol. 2006; 68:1089–1097. doi: 10.1002/ajp.20309 17044010

68. Kowalewski MM, Gillespie TR. Ecological and anthropogenic influences on patterns of parasitism in free-ranging primates: a meta-analysis of the genus Alouatta. In: Garber PA, Estrada A, Bicca-Marques JC, Heymann EW, Strier KB, editors. South American Primates. New York, NY: Springer; 2009. pp. 433–461.

69. DeFries R, Rovero F, Wright P, Ahumada J, Andelman S, Brandon K, Dempewolf J, Hansen A, Hewson J, Liu J. From plot to landscape scale: linking tropical biodiversity measurements across spatial scales. Front Ecol Environ. 2010; 8: 153–160.

70. Navarro-Gonzalez N, Verheyden H, Hoste H, Cargnelutti B, Lourtet B, Merlet J et al Diet quality and immunocompetence influence parasite load of roe deer in a fragmented landscape. Eur J Wildl Res. 2011; 57: 639–645.

71. Appleton CC, Henzi SP. Environmental correlates of gastrointestinal parasitism in montane and lowland baboons in Natal, South Africa. Int J Primatol. 1993; 4: 623–635.

72. Resasco J, Bitters ME, Cunningham SA, Jones HI, McKenzie VJ, Davies KF. Experimental habitat fragmentation disrupts nematode infections in Australian skinks. Ecology. 2019; 100: e02547. doi: 10.1002/ecy.2547 30488947

73. Cardoso TS, Simões RO, Luque JLF, Maldonado A, Gentile R. The influence of habitat fragmentation on helminth communities in rodent populations from a Brazilian Mountain Atlantic Forest. J Helminthol. 2016; 90: 460–468. doi: 10.1017/S0022149X15000589 26206199

74. Hudson PJ, Dobson AP, Lafferty KD. Is a healthy ecosystem one that is rich in parasites?. Trends Ecol Evol. 2006; 21: 381–385. doi: 10.1016/j.tree.2006.04.007 16713014

75. Gillespie TR, Greiner EC, Chapman CA. Gastrointestinal parasites of the colobus monkeys of 608 Uganda. J Parasitol. 2005; 91: 569–573. doi: 10.1645/GE-434R 16108549

76. Altizer S, Nunn CL, Lindenfors P. Do threatened hosts have fewer parasites? A comparative study in primates. J Anim Ecol. 2007; 76: 304–314. doi: 10.1111/j.1365-2656.2007.01214.x 17302838

77. Teichroeb JA, Kutz SJ, Parkar U, Thompson RA, Sicotte P. Ecology of the gastrointestinal parasites of Colobus vellerosus at Boabeng‐Fiema, Ghana: Possible anthropozoonotic transmission. Am J Phys Anthropol. 2009; 140: 498–507. doi: 10.1002/ajpa.21098 19434756

78. Hodder SA, Chapman CA. Do nematode infections of red colobus (Procolobus rufomitratus) and black-and-white colobus (Colobus guereza) on humanized forest edges differ from those on nonhumanized forest edges? Int J Primatol. 2012; 33: 845–859.

79. Modrý D, Pafćo B, Petrželková KJ, Hasegawa H. Parasites of Apes: An Atlas of Coproscopic Diagnostics. Frankfurt: Chimaira; 2018.

80. Raminelli JLF, de Sousa MBC, Cunha MS, Barbosa MFV. Morning and afternoon patterns of fecal cortisol excretion among reproductive and non reproductive male and female common marmosets, Callithrix jacchus. Biolo Rhythm Res. 2001; 32: 159–167.

81. Pedersen AB, Greives TJ. The interaction of parasites and resources cause crashes in a wild mouse population. J Anim Ecol. 2008; 77: 370–377. doi: 10.1111/j.1365-2656.2007.01321.x 18028357

82. Monello R, Millspaugh J, Woods R, Gompper M. The influence of parasites on faecal glucocorticoid metabolite levels in raccoons: an experimental assessment in a natural setting. J Zool. 2010; 282: 100–108.

83. Cizauskas CA, Turner WC, Pitts N, Getz WM. Seasonal patterns of hormones, macroparasites, and microparasites in wild African ungulates: the interplay among stress, reproduction, and disease. PLoS ONE. 2015; 10: e0120800. doi: 10.1371/journal.pone.0120800 25875647

84. Mas-Coma S, Valero MA, Bargues MD. Effects of climate change on animal and zoonotic helminthiases. Rev Sci Tech. 2008; 27: 443–457. 18819671

85. Cavada N, Havmøller RW, Scharff N, Rovero F. A landscape-scale assessment of tropical mammals reveals the effects of habitat and anthropogenic disturbance on community occupancy. PLoS ONE. 2019; 14: e0215682. doi: 10.1371/journal.pone.0215682 31002707

86. Matlack GR. Microenvironment variation within and among forest edge sites in the eastern United States. Biol Conserv. 1993; 66: 185–194.

87. Marshall AR. Ecological report on Magombera forest. 2008.

88. Kreisinger J, Bastien G, Hauffe HC, Marchesi J, Perkins SE. Interactions between multiple helminths and the gut microbiota in wild rodents. Philos Trans Royal Soc B. 2015; 370: 20140295.

89. Rapin A, Harris NL. Helminth–Bacterial interactions: cause and consequence. Trends Immunol. 2018; 9: 724–733.

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