Black and gold howler monkeys (Alouatta caraya) as sentinels of ecosystem health: Patterns of zoonotic protozoa infection relative to degree of human-primate contact

American Journal of Primatology

Volumn 73, Issue 1, 2011, Pages 75-83

  Kowalewski, Martin M ^a   Salzer, Johanna S ^b   Deutsch, Joseph C ^c   Raño, Mariana ^a   Kuhlenschmidt, Mark S ^c   Gillespie, Thomas R ^b,d  

^a MUSEO ARGENTINO DE CIENCIAS NATURALES BERNARDINO RIVADAVIA   (Argentina)

^b EMORY UNIVERSITY   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^d EMORY UNIVERSITY   (United States)

Author keywords

Cryptosporidium; Disturbance ecology; Giardia; Neglected pathogens; Primate; Zoonoses

Indexed keywords

ANTIBODY; BIODIVERSITY; CONSERVATION MANAGEMENT; DISEASE PREVALENCE; ECOSYSTEM HEALTH; EPIDEMIC; EPIDEMIOLOGY; FUNCTIONAL MORPHOLOGY; HABITAT TYPE; HUMAN ACTIVITY; INFECTIOUS DISEASE; LAND USE; LIVESTOCK; PATHOGENICITY; PRIMATE; PROTOZOAN; RURAL AREA; WILD POPULATION;

ALOUATTA; ANIMAL; ARGENTINA; ARTICLE; CLASSIFICATION; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM; DISEASE CARRIER; DISEASE TRANSMISSION; ECOSYSTEM; ENVIRONMENTAL HEALTH; FECES; GIARDIA; GIARDIASIS; HUMAN; LIVESTOCK; PARASITOLOGY; PHYSIOLOGY; PREVALENCE; TREE; ZOONOSIS;

ALOUATTA; ANIMALS; ARGENTINA; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM; DISEASE RESERVOIRS; ECOSYSTEM; ENVIRONMENTAL HEALTH; FECES; GIARDIA; GIARDIASIS; HUMANS; LIVESTOCK; PREVALENCE; TREES; ZOONOSES;

ARGENTINA;

ALOUATTA; ALOUATTA CARAYA; ANIMALIA; CRYPTOSPORIDIUM; CRYPTOSPORIDIUM SP.; GIARDIA; GIARDIA SP.; PRIMATES; PROTOZOA;

EID: 78649506355     PISSN: 02752565     EISSN: 10982345     Source Type: Journal    
DOI: 10.1002/ajp.20803     Document Type: Article

References (76)

1. Acha PN, Szyfres B. 2003. Zoonoses and communicable diseases common to man and animal, 3rd ed., Vol. III. Parasitoses. Pan American Health Organization, WHO.
2. Agostini I, Holzmann I, Di Bitetti MS. 2008. Infant hybrids in a newly formed mixed species group of howler monkeys (Alouatta guariba clamitans and Alouatta caraya) in northeastern Argentina. Primates 49:304-307.
3. Alarcón-Cháires P. 2006. Riqueza ecológica versus pobreza social. Contradicciones y perspectivas del desarrollo indígena en Latinoamérica. Cimadamore AD, Eversole R, McNeish JA, editors. Pueblos indígenas y pobreza. Enfoques multidisciplinarios. CLACSO, Consejo Latinoamericano de Ciencias Sociales, Buenos Aires.
4. Altizer S, Dobson A, Hosseini P, Hudson P, Pascual M, Rohani P. 2006. Seasonality and the dynamics of infectious diseases. Ecology Letters 9:467-484.
5. Appelbee AJ, Thompson RCA, Olson ME. 2005. Giardia and Cryptosporidium in mammalian wildlife-current status and future needs. Trends in Parasitology 21:370-376.
6. Atías A. 1999. El hospedero. La relación hospedero-parasito (The host. Host-parasite relationship). Atias A, editor. Parasitología médica. Mediterraneo: Chile. p 49-53.
7. Ayalew D, Boelee E, Endeshaw T, Petros B. 2008. Cryptosporidium and Giardia infection and drinking water sources among children in Lege Dini, Ethiopia. Tropical Medicine & International Health 13:472-475.
8. Bicca-Marques JC. 2003. How do howler monkeys cope with habitat fragmentation? Marsh LK, editor. Primates in fragments: ecology and conservation. New York: Kluwer Academic/Plenum Publishers. p 283-303.
9. Borda CE, Rea MJ, Rosa JR, Maidana C. 1996. Intestinal parasitism in San Cayetano, Corrientes, Argentina. Bulletin of the Pan American Health Organization 30:227-233.
10. Bravo SP, Sallenave A. 2003. Foraging behavior and activity patterns of Alouatta caraya in the northeastern Argentinean flooded forest. International Journal of Primatology 24:825-846.
11. Cabral JNH, Rossato RS, de M Gomes MJT, Araújo FAP, Oliveira F, Praetzel K. 2005. Gastrointestinais de bugios-ruivos (Alouatta guariba clamitans Cabrera 1940) da região extremo-sul de Porto Alegre/RS, Brasil, diagnosticados através da coproscopia: implicações para a conservação da espécie e seus ha. Congresso Brasileiro de Parasitologia, Porto Alegre, RS, Brasil [Abstract].
12. Chapman CA, Wasserman MD, Gillespie TR, Speirs ML, Lawes MJ, Saj TL, Ziegler TE. 2006. Do nutrition, parasitism, and stress have synergistic effects on red colobus populations living in forest fragments? American Journal of Physical Anthropology 131:525-534.
13. Chester AC, MacMurray FG, Restifo MD, Mann O. 1985. Giardiasis as a chronic disease. Digestive Diseases and Sciences 30:215-218.
14. Clarke MR, Crockett CM, Zucker EL, Zaldivar M. 2002a. Mantled howler population of Hacienda La Pacifica, Costa Rica, between 1991 and 1998: effects of deforestation. American Journal of Primatology 56:155-163.
15. Clarke MR, Collins DA, Zucker EL. 2002b. Responses to deforestation in a group of mantled howlers (Alouatta palliata) in Costa Rica. International Journal of Primatology 23:365-381.
16. Cordon PG, Soldan OCP, Vasquez VF, Soto VJR, Bordes SL, Moreno SM, Rosales MJ. 2008. Prevalence of enteroparasites and genotyping of Giardia lamblia in Peruvian children. Parasitology Research 103:459-465.
17. Crockett CM. 1998. Conservation biology of the genus Alouatta. International Journal of Primatology 19:549-578.
18. Crockett CM, Eisenberg JF. 1987. Howlers: variations in group size and demography. Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT, editors. Primate Societies. Chicago: The University of Chicago Press. p 54-68.
19. Crompton DW. 2000. The public health importance of hookworm disease. Parasitology 121:39-50.
20. De la Cruz R. 2004. Visión de los Pueblos Indígenas en el contexto de las decisiones sobre ABS y 8 (j): Impacto de las decisiones de la CDB/COP sobre el mandato de la IGC de la OMPI. Notas Informales. Policy and Global Change Series. Trade and Biodiversity. COICA, ICTSD and IUCN.
21. Dib HH, Lu SQ, Wen SF. 2008. Prevalence of Giardia lamblia with or without diarrhea in South East, South East Asia and the Far East. Parasitology Research 103:239-251.
22. Eisenberg JF, Muckenhirn NA, Rudran R. 1972. The relation between ecology and social structure in primates. Science 176:863-874.
23. Estrada A, Saenz J, Harvey C, Naranjo E, Muñoz D, Rosales-Meda M. 2006. Primates in agroecosystems: conservation value of some agricultural practices in Mesoamerican landscapes. Estrada A, Garber PA, Pavelka MSM, Luecke L, editors. New perspectives in the study of Mesoamerican Primates: distribution, ecology, behavior, and conservation. New York: Springer. p 437-470.
24. Gamboa M, Basualdo J, Córdoba M, Pezzani B, Minvielle M, Lahitte H. 2003. Distribution of intestinal parasitoses in relation to environmental and sociocultural parameters in La Plata, Argentina. Journal of Helminthology 77:15-20.
25. Gillespie TR. 2006. Noninvasive assessment of gastrointestinal parasite infections in free-ranging primates. International Journal of Primatology 27:1129-1143.
26. Gillespie TR, Chapman CA. 2006. Forest fragment attributes predict parasite infection dynamics in primate metapopulations. Conservation Biology 20:441-448.
27. Gillespie TR, Chapman CA. 2008. Forest fragmentation, the decline of an endangered primate, and changes in host-parasite interactions relative to an unfragmented forest. American Journal of Primatology 70:222-230.
28. Gillespie TR, Chapman CA, Greiner EC. 2005. Effects of logging on gastrointestinal parasite infections and infection risk in African primates. The Journal of Applied Ecology 42:699-707.
29. Gillespie TR, Nunn CL, Leendertz FH. 2008. Integrative approaches to the study of primate infectious disease: implications for biodiversity conservation and global health. Yearbook of Physical Anthropology 51:53-69.
30. Glander KE. 1992. Dispersal patterns in Costa Rica mantled howling monkeys. American Journal of Primatology 13:415-436.
31. Graczyk TK, Marcogliese DJ, deLafontaine Y, DaSilva AJ, Mhangami-Ruwende, Pieniazek NJ. 2001a. Cryptosporidium parvum oocysts in zebra mussels (Dreissena polymorpha): evidence from the St. Lawrence River. Parasitology Research 87:231-234.
32. Graczyk TK, DaSilva AJ, Cranfield MR, Bosco Nizeyi J, Kalema GRNN, Pieniazek NJ. 2001b. Cryptosporidium parvum Genotype 2 infections in free-ranging mountain gorillas (Gorilla gorilla beringei) of the Bwindi Impenetrable National Park, Uganda. Parasitology Research 87:368-370.
33. Graczyk TK, Bosco-Nizeyi J, Ssebide B, Thompson RC, Read C, Cranfield MR. 2002. Anthropozoonotic Giardia duodenalis genotype (assemblage) a infections in habitats of free-ranging human-habituated gorillas, Uganda. Journal of Parasitology 88:905-909.
34. Hay SI, Cox J, Rogers DJ, Randolph SE, Stern DI, Shanks DG. 2002. Climate change and the resurgence of malaria in the East African highlands. Nature 415:905-909.
35. Hill DR. 2001. Giardia lamblia. Gillepie S, Pearson RD, editors. Principles and practice of clinical parasitology. John Wiley & Sons. p 219-241.
36. Hollm-Delgado MG, Gilman RH, Bern C, Cabrera L, Sterling CR, Black RE, Checkley W. 2008. Lack of an adverse effect of Giardia intestinalis infection on the health of Peruvian children. American Journal of Epidemiology 168:647-655.
37. Horwich RH, Lyon J. 1998. A Belizean rain forest-the community Baboon Sanctuary, 3rd ed. Orangutan, Gays Mills.
38. Istre GR, Dunlop TS, Gaspard GB, Hopkins RS. 1984. Waterborne giardiasis at a mountain resort: evidence for acquired immunity. American Journal of Public Health 74:602-604.
39. Johnston SP, Ballard MM, Beach MJ, Causer L, Wilkins PP. 2003. Evaluation of three commercial assays for detection of Giardia and Cryptosporidium organisms in fecal specimens. Journal of Clinical Microbiology 41:623-626.
40. Kowalewski MM. 2007. Patterns of affiliation and co-operation in howler monkeys: an alternative model to explain social organization in non-human primates. Dissertation. Department of Anthropology, University of Illinois. Urbana-Champaign. 362p. AAT 3290280.
41. Kowalewski MM, Gillespie TR. 2009. Ecological and anthropogenic influences on patterns of parasitism in free-ranging primates: a meta-analysis of the Genus Alouatta. Estrada A, Garber P, Strier K, Bicca-Marques J, Heymann E, editors. South American Primates: testing new theories in the study of primate behavior, ecology, and conservation. New York: Springer. p 433-461.
42. Kowalewski MM, Zunino GE. 2004. Birth seasonality in Alouatta caraya in Northern Argentina. International Journal of Primatology 25:383-400.
43. Kowalewski MM, Bravo SP, Zunino GE. 1995. Aggressions between males of Alouatta caraya in forest patches from northern Argentina. Neotropical Primates 3:179-181.
44. Ledesma A, Gorodner JO, Fernández GJ. 2006. Cryptosporidium sp. en infantes de barrios periféricos de Resistencia, Chaco. Comunicaciones Científicas y Tecnológicas/Universidad Nacional del Nordeste, CHACO: Argentina.
45. Levy D, Bens M, Craun G, Calderon R, Herwaldt B. 1998. Surveillance for Waterborne-Disease Outbreaks-United States, 1995-1996. Morbidity and Mortality Weekly Report CDC Surveillance Summaries 47:1-34.
46. Martínez Alier J. 2005. El ecologismo de los pobres. Barcelona: Icaria Editorial.
47. McGlade TR, Robertson ID, Elliot AD, Thompson RCA. 2003. High prevalence of Giardia detected in cats by PCR. Veterinary Parasitology 110:197-205.
48. Miner BG, Sultan SE, Morgan SG, Padilla DK, Relyea RA. 2005. Ecological consequences of phenotypic plasticity. Trends in Ecology & Evolution 20:685-692.
49. Minvielle M, Pezzani B, Cordoba M, De Luca M, Apezteguía M, Basualdo J. 2004. Epidemiological survey of Giardia spp and Blastocystis hominis in an Argentinian rural community. Korean Journal of Parasitology 42:61-66.
50. Muñoz D, Estrada A, Naranjo E, Ochoa S. 2006 Foraging ecology of howler monkeys in a cacao (Theobroma cacao) plantation in Comalcalco, Mexico. American Journal of Primatology 68:127-142.
51. Muller GCK, Krambeck A, Hirano ZNB, Silva Filho HH. 2000. Levantamento preliminar de endoparasitas em bugíos Alouatta clamitans. Neotropical Primates 8:107-108.
52. Nizeyi JB, Mwebe R, Nanteza A, Cranfield MR, Kalema GR, Graczyk TK. 1999. Cryptosporidium sp. and Giardia sp. infections in mountain gorillas (Gorilla gorilla berengei) of the Bwindi Impenetrable National Park, Uganda. The Journal of Parasitology 85:1084-1088.
53. Nunn CL, Altizer S. 2006. Infectious diseases in primates: behavior, ecology and evolution. New York: Oxford Series in Ecology and Evolution, Oxford University Press.
54. Oklander LI. 2007. Estructura social y relaciones de parentesco en poblaciones silvestres de monos aulladores (Alouatta caraya) del noreste argentino. Dissertation, Universidad de Buenos Aires, Argentina.
55. Oklander LI, Zunino GE, Di Fiore A, Corach D. 2007. Isolation, characterization and evaluation of 11 autosomal STRs suitable for population studies in black and gold howler monkeys Alouatta caraya. Molecular Ecology Notes 7:117-120.
56. Pezzani B, Minvielle M, Laplace R, Cotter G, Basualdo J. 2003. Presencia de elementos parasitarios en contenido intestinal de múridos de la ciudad de La Plata. Acta Bioquímica Clínica Latinoamericana 1:87.
57. Pozo-Montuy G, Serio-Silva JC. 2006. Movement and resource use by a group of Alouatta pigra in a forest fragment in Balancán, México. Primates 48:102-107.
58. Reinthaler FF, Feierl G, Stunzner D, Marth E. 1998. Diarrhea in returning Austrian tourists: epidemiology, etiology, and cost-analyses. Journal of Travel Medicine 5:65-72.
59. Rumiz DI, Zunino GE, Obregozo ML, Ruiz JC. 1986. Alouatta caraya: habitat and resource utilization in Northern Argentina. Taub DM, King FA, editors. Current Perspectives in Primate Social Dynamics. New York: Van Nostrand Rehinol. p 175-193.
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. Journal of Parasitology 93:439-440.
61. Santa Cruz ACM, Borda JT, Patiño EM, Gomez L, Zunino GE. 2000. Habitat fragmentation and parasitism in howler monkeys (Alouatta caraya). Neotropical Primates 8:146-148.
62. Savioli L, Smith H, Thompson A. 2006. Giardia and Cryptosporidium join the "Neglected Diseases Initiative." Trends in Parasitology 22:203-208.
63. Shlim DR, Hoge CW, Rajah R, Scott RM, Pandy P, Echeverria P. 1999. Persistent high risk of diarrhea among foreigners in Nepal during the first 2 years of residence. Clinical Infectious Diseases 29:613-616.
64. Smith H, Nichols RA. 2006. Zoonotic protozoa-food for thought. Parasitologia 48:101-104.
65. Teodorovic S, Braverman JM, Elmendorf HG. 2007. Unusually low levels of genetic variation among Giardia lamblia isolates. Eukaryotic Cell 6:1421-1430.
66. Thompson RC. 2000. Giardiasis as a re-emerging infectious disease and its zoonotic potential. International Journal of Parasitology 30:1259-1267.
67. Thompson RCA. 2004. Epidemiology and zoonotic potential of Giardia infections. Sterling CR, Adam RD, editors. World class parasites, Vol. 8: the pathogenic enteric protozoa: Giardia, Entamoeba, Cryptosporidium and Cyclospora. Boston, Massachusetts: Kluwer Academic Publishers. p 1-14.
68. Traub RJ, Robertson ID, Irwin P, Mencke N, Monis P, Thompson RC. 2003. Humans, dogs and parasitic zoonoses-unravelling the relationships in a remote endemic community in northeast India using molecular tools. Parasitology Research 90:156-157.
69. Vitazkova SK, Wade SE. 2006. Parasites of free-ranging black howler monkeys (Alouatta pigra) from Belize and Mexico. American Journal of Primatology 68:1089-1097.
70. Vitazkova SK, Wade SE. 2007 Effects of Ecology on the Gastrointestinal Parasites of Alouatta pigra. International Journal of Primatology 28:1327-1343.
71. Volotão ACC, Costa-Macedo LM, Haddad FS, Brandão A, Peralta JM, Fernandes O. 2007. Genotyping of Giardia duodenalis from human and animal samples from Brazil using beta-giardin gene: a phylogenetic analysis. Acta Tropica 102:10-19.
72. Volotão ACC, Souza Júnior JC, Grassinia C, Peralta JM, Fernandes O. 2008. Genotyping of Giardia duodenalis from Southern Brown Howler Monkeys (Alouatta clamitans) from Brazil. Veterinary Parasitology 158:133-137.
73. WHO/UNICEF. 2000. Global water supply and sanitation assessment 2000 report. WHO/UNICEF Joint Monitoring Programme for Water Supply and Sanitation. WHO, Geneva, Switzerland.
74. Young OP. 1981. Chasing behavior between males within a howler monkey troop. Primates 22:424-426.
75. Zunino GE, Kowalewski MM. 2008. Primate research and conservation in northern Argentina: the field station Corrientes (Estación Biológica de Usos Múltiples-EBCo). Tropical Conservation Science 1:140-150.
76. Zunino GE, Kowalewski MM, Oklander LI, Gonzalez V. 2007. Habitat fragmentation and population trends of the black and gold howler monkey (Alouatta caraya) in a semideciduous forest in northern Argentina. American Journal of Primatology 69:966-975.