The anthropogenic environment lessens the intensity and prevalence of gastrointestinal parasites in Balinese long-tailed macaques (Macaca fascicularis)

Primates

Volumn 52, Issue 2, 2011, Pages 117-128

  Lane, Kelly E ^a   Holley, Concerta ^a   Hollocher, Hope ^a   Fuentes, Agustin ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

Ecosystem; Gastrointestinal parasites; Intensity; Macaques; Parasite species diversity

Indexed keywords

ECOSYSTEM STRUCTURE; HABITAT TYPE; PARASITE; PRIMATE; SPECIES DIVERSITY;

ANIMAL; ANIMAL DISEASE; ARTICLE; ENVIRONMENT; GASTROINTESTINAL TRACT; HOST PARASITE INTERACTION; HUMAN; HUMAN ACTIVITIES; INDONESIA; INTESTINE INFECTION; MACACA FASCICULARIS; MONKEY DISEASE; PARASITE; PARASITOLOGY; PHYSIOLOGY; PREVALENCE; PRINCIPAL COMPONENT ANALYSIS;

ANIMALS; ENVIRONMENT; GASTROINTESTINAL TRACT; HOST-PARASITE INTERACTIONS; HUMAN ACTIVITIES; HUMANS; INDONESIA; INTESTINAL DISEASES, PARASITIC; MACACA FASCICULARIS; MONKEY DISEASES; PARASITES; PREVALENCE; PRINCIPAL COMPONENT ANALYSIS;

MACACA; MACACA FASCICULARIS;

EID: 79953233583     PISSN: 00328332     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10329-010-0230-6     Document Type: Article

References (80)

1. Anderson DR, Beaudoin RL (1966) Host habitat and age as factors in the prevalence of intestinal parasites of the muskrat. Bull Wildl Dis Assoc 2: 70-77.
2. Arneberg P, Skorping A, Grenfell B, Read AF (1998) Host densities as determinants of abundance in parasite communities: comparative analyses of directly transmitted nematodes of mammals. Ecography 25: 88-94.
3. Bagge AM, Poulin R, Valtonen ET (2004) Fish population size, and not density, as the determining factor of parasitic infection: a case study. Parasitology 128: 305-313.
4. Baird JK (2003) Host age as a determinant of naturally acquired immunity in Plasmodium falciparum. Parasitol Today 11: 105-111.
5. Baudoin M (1975) Host castration as a parasitic strategy. Evolution 29(2): 335-352.
6. Brown CR, Brown MB (1986) Ectoparasitism as a cost of coloniality in cliff swallows (Hirundo pyrrhonota). Ecology 67: 1206-1218.
7. Chapman CA, Gillespie TR, Goldberg TL (2005a) Primates and the ecology of their infectious diseases: how will anthropogenic change affect host-parasite interactions? Evol Anthropol 14: 134-144.
8. Chapman CA, Gillespie TR, Speirs ML (2005b) Parasite prevalence and richness in sympatric colobines: gastrointestinal parasites from forest edge and interior primate groups. Am J Primatol 68: 1-12.
9. Combes C (1996) Parasites, biodiversity and ecosystem stability. Biodivers Conserv 5: 953-962.
10. Combes C (2001) Parasitism: the ecology and evolution of intimate interactions. University of Chicago Press, Chicago.
11. Cote IM, Poulin R (1995) Parasitism and group size in social mammals: a meta-analysis. Behav Ecol 6: 159-165.
12. Daszak P, Cunningham AA, Hyatt AD (2001) Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Trop 78: 103-116.
13. Dobson AP (1988) The population biology of parasite-induced changes in host behavior. Q Rev Biol 63: 139-165.
14. Ekanayake DK, Arulkanthan A, Horadagoda NU, Sanjeevani GKM, Kieft R, Gunatilake S, Dittus WPJ (2006) Prevalence of Crypotosporidium and other enteric parasites among wild non-human primates in Polonnaruwa, Sri Lanka. Am J Trop Med 74: 322-329.
15. Ezenwa VO (2006) Host social behavior and parasitic infection: a multifactorial approach. Behav Ecol 15: 446-454.
16. Ferrari N, Cattadori IM, Nespereira J, Rizzoli A, Hudson PJ (2004) The role of host sex in parasite dynamics: experiments on the yellow-necked mouse Apodemus flavicollis. Ecol Lett 7: 88-94.
17. Foreyt WJ (2001) Veterinary parasitology: reference manual, 5th edn. Blackwell, Oxford.
18. Freeland WJ (1979) Primate social groups as biological islands. Ecology 61: 1297-1303.
19. Fuentes A (2007) Social organization: social systems and the complexities in understanding the evolution of primate behavior. In: Campbell CJ, Fuentes A, MacKinnon KC, Panger M, Bearder SK (eds) Primates in perspective. Oxford University Press, Oxford, pp 609-621.
20. Fuentes A (2009) A new synthesis: resituating approaches to the evolution of human behavior. Anthropol Today 25: 12-17.
21. Fuentes A, Southern M, Suaryana KG (2005) Monkey forests and human landscapes: is extensive sympatry sustainable for Homo sapiens and Macaca fascicularis in Bali? In: Patterson J (ed) Commensalism and conflict: the primate-human interface. American Society of Primatology Publications, Norman.
22. Garcia LS (1999) Practical guide to diagnostic parasitology. American Society of Microbiology Press, Washington DC.
23. Gasser RB, de Gruijter JM, Polderman AM (2009) The utility of molecular methods for elucidating primate-pathogen relationships--the Oesophagostomum bifurcum example. In: Huffman MA, Chapman CA (eds) Primate parasite ecology: the dynamics and study of host-parasite relationships. Cambridge University Press, Cambridge, pp 47-63.
24. Greiner EC, McIntosh A (2009) Collection methods and diagnostic procedures for primate parasitology. In: Huffman MA, Chapman CA (eds) Primate parasite ecology: the dynamics and study of host-parasite relationships. Cambridge University Press, Cambridge, pp 3-28.
25. Grutter AS (1998) Habitat-related differences in the abundance of parasites from a coral reef fish: an indication of the movement patterns of Hemigymnus melapterus. J Fish Biol 53: 49-57.
26. Gurarie D, Seto EYW (2008) Connectivity sustains disease transmission in environments with low potential for endemicity. J R Soc Interface 6(35): 495-508.
27. Hartwig W (2007) Primate evolution. In: Campbell CJ, Fuentes A, MacKinnon KC, Panger M, Bearder SK (eds) Primates in perspective. Oxford University Press, Oxford, pp 11-22.
28. Haufstater G, Meade BJ (1982) Alteration of sleeping groves by yellow baboons (Papio cynocephalus) as a strategy for parasite avoidance. Primates 23: 287-297.
29. Hurd H (2001) Host fecundity reduction: a strategy for damage limitation? Trends Parasitol 17: 363-368.
30. Jaffee B, Phillips R, Muldoon A, Mangel M (1992) Density-dependent host-pathogen dynamics in soil microcosms. Ecology 73: 495-506.
31. Jones-Engel L, Engel GA, Schillaci MA, Kyes K, Froelich J, Paputungan U, Kyes RC (2004) Prevalence of enteric parasites in pet macaques in Sulawesi, Indonesia. Am J Primatol 62: 71-82.
32. Keesing F, Holt RD, Ostfeld RS (2006) Effects of species diversity on disease risk. Ecol Lett 9: 485-498.
33. Kripalani RH, Kulkarni A (1998) Rainfall variability over South-east Asia--connections with Indian monsoon and ENSO extremes: new perspectives. Int J Climatol 17: 1155-1168.
34. Kumagai M, Koayashi S, Okita T, Ohtoma H (2001) Modifications of Kohn's chlorazol black E staining and Wheatley's trichrome staining for temporary wet mount and permanent preparation of Entamoeba histolytica. J Parasitol 87: 701-704.
35. Lane KE, Lute M, Rompis A, Wandia IN, Arta Putra IG, Hollocher H, Fuentes A (2010) Pests, pestilence, and people: the long-tailed macaque and its role in the cultural complexities of Bali. In: Gursky-Doyen S, Supriatna J (eds) Indonesian primates, developments in primatology: progress and prospects. Springer, Berlin, pp 235-248.
36. Lane KE, Putra IGA, Wandia IN, Rompis A, Hollocher H, Fuentes A (2011) Balinese perceptions of pathogen exposure in human communities surrounding long-tailed macaque populations. Ecol Environ Anthropol (in press).
37. Lee P (1999) Comparative primate socioecology. Cambridge University Press, Cambridge.
38. Legesse M, Erko B (2004) Zoonotic intestinal parasites in Papio anubis (baboon) and Cercopithecus aethiops (vervet) from four localities in Ethiopia. Acta Tropica 90: 231-236.
39. Loudon J, Howell M, Fuentes A (2006) The importance of integrative anthropology: a preliminary investigation employing primatological and cultural anthropological data-collection methods in assessing human-monkey co-existence in Bali, Indonesia. Ecol Environ Anthropol 2(1): 2-13.
40. Margolis L, Esch GW, Holmes JC, Kuris AM, Schad GA (1982) The use of ecological terms in parasitology (report of an ad hoc committee of the American Society of Parasitologists) J Parasitol 68: 131-133.
41. McKenna P (1981) The diagnostic value and interpretation of fecal egg counts in sheep. N Z Vet J 29: 129-132.
42. Mohl K, Grosse K, Hamedy A, Wuste T, Kabelitz P, Lucker E (2009) Biology of Alaria spp. and human exposition risk to Alaria mesocercariae-a review. Parasitol Res 105: 1-15.
43. Moller AP (1993) A fungus infecting domestic flies manipulates sexual behavior of its host. Behav Ecol Sociobiol 33: 403-407.
44. Morand S (2000) Wormy world: comparative tests of theoretical hypotheses on parasite species richness. In: Poulin R, Morand S, Skorping A (eds) Evolutionary biology of host-parasite relationships: theory meets reality. Elsevier, Amsterdam.
45. Mouritsen KN, Poulin R (2003) The mud flat anemone-cockle association: mutualism in the intertidal zone? Oecologia 135: 131-137.
46. Niezen JH, Charleston WAG, Hodgson J, Miller CM, Waghorn TS, Robertson HA (2001) Effect of plant species on the larvae of gastrointestinal nematodes which parasitize sheep. Int J Parasitol 28: 791-803.
47. Nunn CL, Altizer S (2006) Infectious diseases in primates. Oxford University Press, Oxford.
48. Nunn CL, Altizer S, Jones KE, Sechrest W (2003) Comparative tests of parasite species richness in primates. Am Nat 162: 597-614.
49. Ostfeld RS, Glass GE, Keesing F (2005) Spatial epidemiology: an emerging (or reemerging) discipline. Trends Ecol Evol 20: 328-336.
50. Paterson S, Lello J (2003) Mixed models: getting the best use of parasitological data. Trends Ecol Evol 19: 370-375.
51. Patz JA, Graczyk TK, Geller N, Vittor AY (2000) Effects of environmental change of emerging parasitic diseases. Int J Parasitol 30: 1395-1405.
52. Pederson AB, Fenton A (2006) Emphasizing the ecology in parasite community ecology. Trends Ecol Evol 22: 133-139.
53. Poulin R (1997) Species richness of parasite assemblages: evolution and patterns. Annu Rev Ecol Syst 28: 341-358.
54. Poulin R, Morand S (2004) Parasite biodiversity. Smithsonian Institute Press, Washington, DC.
55. R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org.
56. Rendtorff RC, Holt CJ (1954) The experimental transmission of human intestinal protozoan parasites. 4. Attempts to transmit Entamoeba coli and Giardia lamblia cysts by water. Am J Hyg 60: 327-338.
57. Roberts MG, Dobson AP, Arneberg P, de Leo GA, Krecek RC, Manfredi MT, Lanfranchi P, Zaffaroni E (2002) Parasite community ecology and biodiversity. In: Hudson PJ, Rizzoli A, Grenfell BT, Hesterbeek H, Dobson AP (eds) The ecology of wildlife diseases. Oxford University Press, Oxford, pp 63-82.
58. Roepstorff A, Murrell KD (1997) Transmission dynamics of helminth parasites of pigs on continuous pasture: Ascaris suum and Trichuris suis. Int J Parasitol 27: 563-572.
59. Rozsa L, Reiczigel J, Majoros G (2000) Quantifying parasites in samples of hosts. J Parasitol 86: 228-232.
60. Salzer JS, Rwego IB, Goldberg TL, Kuhlenschmidt MS, Gillespie TR (2007) Giardia sp. and Cryptosporidium sp. infections in primates in fragmented and undisturbed forest in western Uganda. J Parasitol 93: 439-440.
61. Schrag SJ, Weiner P (1995) Emerging infectious disease: what are the relative roles of ecology and evolution? Trends Ecol Evol 10: 319-324.
62. Singh S, Shrivastav AB, Sharma RK (2009) The epidemiology of gastrointestinal parasitism and body condition in free-ranging herbivores. Journal Threatened Taxa 1: 535-537.
63. Sleeman JM, Meader LL, Mudakikwa AB, Foster JW, Patton S (2000) Gastrointestinal parasites of mountain gorillas (Gorilla gorilla beringei) in the Parc National des Volcans, Rwanda. J Zoo Wildl Med 31: 322-328.
64. Slifko TR, Smith HV, Rose JB (2000) Emerging parasite zoonoses associated with water and food. Int J Parasitol 30: 1379-1393.
65. Snaith TV, Chapman CA, Rothman JM, Wasserman MD (2008) Bigger groups have fewer parasites and similar cortisol levels: a multi-group analysis in red colobus monkeys. Am J Primatol 70: 1-9.
66. Sogandaresbernal F (1955) Some helminth parasites of fresh and brackish water fishes from Louisiana and Panama. J Parasitol 41: 582-587.
67. Southern MW (2002) An assessment of potential habitat corridors and landscape ecology for long-tailed macaques (Macaca fascicularis) on Bali, Indonesia [dissertation]. Central Washington University, Ellensberg.
68. Spellerberg IF, Fedor PJ (2003) A tribute to Claude Shannon (1916-2001) and a plea for more rigorous use of species richness, species diversity, and the 'Shannon-Wiener' Index. Glob Ecol Biogeogr 12: 177-179.
69. Stirnadel HA, Ebert D (1997) Prevalence, host specificity and impact on host fecundity of microparasites and epibionts in three sympatric Daphnia species. J Anim Ecol 66: 212-222.
70. Stuart MD, Strier KB, Peirberg SM (1993) A coprological survey of parasites of wild muriquis, Brachyteles arachnoids, and brown howling monkeys, Alouatta fusca. J Helminthol Soc WA 60: 111-115.
71. Stuart M, Pendergast V, Rumfelt S, Pierberg S, Greenspan L, Glander K, Clarke M (1998) Parasites of wild howlers (Alouatta spp.). Int J Primatol 19: 493-512.
72. Thieltges DW, Jensen KT, Poulin R (2008) The role of biotic factors in the transmission of free-living endohelminth stages. Parasitology 135: 407-426.
73. Thierry B (2007) The macaques: a double-layered social organization. In: Campbell CJ, Fuentes A, MacKinnon KC, Panger M, Bearder SK (eds) Primates in perspective. Oxford University Press, Oxford, pp 224-240.
74. Trejo-Macias G, Estrada A, Cabrera MAM (2007) Survey of helminth parasites in populations of Aloutta palliata mexicana and A. pigra in continuous and in fragmented habitat in southern Mexico. Int J Primatol 28: 931-945.
75. van Schaik CP (1996) Social evolution in primates: the role of ecological factors and male behaviour. Proc Br Acad 88: 9-31.
76. Varadharajan A, Pythal C (1999) Parasites of wildlife-I: a preliminary investigation on the parasites of wild animals at the Zoological Garden, Thiruvanathapuram, Kerala. Zoos' Print Journal 14: 159-164.
77. Wang WLL, Dunlop SG (1954) Animal parasites in sewage and irrigation water. Sew Ind Wastes 26: 1020-1032.
78. Wolfe ND, Switzer WM (2009) Primate exposure and the emergence of novel retroviruses. In: Huffman MA, Chapman CA (eds) Primate parasite ecology: the dynamics and study of host-parasite relationships. Cambridge University Press, Cambridge, pp 353-370.
79. Wolfe ND, Escalante AA, Karesh WB, Kilbourn A, Spielman A, Lal AA (1998) Wild primate populations in emerging infectious disease research: the missing link? EID 4: 149-158.
80. Zajac AM, Conboy GA (2006) Veterinary clinical parasitology, 7th edn. Blackwell-Wiley, Oxford.