Seasonal variations in gastrointestinal parasites excreted by the gray mouse lemur Microcebus murinus in Madagascar

Endangered Species Research

Volumn 11, Issue 2, 2010, Pages 113-122

  Raharivololona, Brigitte M ^a,b   Ganzhorn, Jörg U ^b  

^a UNIVERSITY OF ANTANANARIVO   (Madagascar)

^b UNIVERSITY OF HAMBURG   (Germany)

Author keywords

Cestoda; Madagascar; Nematoda; Parasite infection; Primates; Seasonal variation; Torpor

Indexed keywords

ENVIRONMENTAL FACTOR; EVERGREEN FOREST; FECES; HOST-PARASITE INTERACTION; LITTORAL ENVIRONMENT; NEMATODE; PARASITE INFESTATION; PRIMATE; RODENT; SEASONAL VARIATION;

MADAGASCAR;

CESTODA; MICROCEBUS; MICROCEBUS MURINUS; NEMATODA; PRIMATES; STREPSIRHINI;

EID: 77952296839     PISSN: 18635407     EISSN: 16134796     Source Type: Journal    
DOI: 10.3354/esr00255     Document Type: Article

References (75)

1. Boesch C (2008) Why do chimpanzees die in the forest? The challenges of understanding and controlling for wild ape health. Am J Primatol 70:722-726.
2. Cassinello J, Gomendio M, Roldan ERS. (2001) Relationship between coefficient of inbreeding and parasite burden in endangered gazelles. Conserv Biol Pract 15:1171-1174.
3. Chabaud AG, Brygoo ER. (1956) Description de Rictularia lemuri n. sp. (Nematoda: Thelaziidae). Mem Inst Sci Madag Ser A 11:43-49.
4. Chabaud AG, Choquet MT. (1955) Deux nématodes parasites de lémurien. Ann Parasitol 30:329-338.
5. Chabaud AG, Larivière M. (1955) Cycle évolutif d'un ascaride: Subulura jacchi. (Marcel, 1857) parasite de primates, chez la blatte Blabera fusca. C R Soc Biol 149:1416-1419.
6. Chabaud AG, Petter AJ. (1958) Les nematodes parasites de lémuriens malgaches. I. Mem Inst Sci Madag Ser A 12: 139-158.
7. Chabaud AG, Petter AJ. (1959) Les nematodes parasites de lémuriens malgaches. II. Un nouvel oxyure: Lemuricola contagiosus. Mem Inst Sci Madag Ser A 13:127-132.
8. Chabaud AG, Brygoo ER, Petter AJ. (1961a) Les nématodes parasites de lémuriens malgaches. IV. Description de deux nouveaux genres et observations sur Protofilaria furcata Chandler. Bull Mus Natl Hist Nat 2e Ser 33:532-544.
9. Chabaud AG, Petter AJ, Golvan Y. (1961b) Les nématodes parasites de lémuriens malgaches. III. Collection récoltée par M. et Mme. Francis Petter. Ann Parasitol 36:113-126.
10. Chabaud AG, Brygoo ER, Petter AJ. (1964) Les nématodes parasites de lémuriens malgaches. V. Nématodes de Daubentonia madagascariensis. Vie Milieu. (Suppl 17): 205-212.
11. Chabaud AG, Brygoo ER, Petter AJ. (1965) Les nématodes parasites de lémuriens malgaches. VI. Description de six espèces nouvelles et conclusions générales. Ann Parasitol 40:181-214.
12. Chapman C, Huffman MA. (2009) Primates and their parasites. Cambridge University Press, Cambridge.
13. Chapman CA, Gillespie TR, Speirs ML. (2005) Parasite prevalence and richness in sympatric colobines: effects of host density. Am J Primatol 67:259-266.
14. Coltman DW, Pilkington JG, Smith JA, Pemberton JM. (1999) Parasite-mediated selection against inbred Soay sheep in a free-living, island population. Evolution 53: 1259-1267.
15. Daszak P, Cunningham AA, Hyatt AD. (2000) Emerging infectious diseases of wildlife-threats to biodiversity and human health. Science 287:443-449.
16. Dausmann K. (in press) An (opposable) thumbs-up for hibernation- hypometabolism in primates. In: Masters J, Gamba M, Génin F (eds) Leaping ahead: advances in prosimian biology. Springer, New York.
17. Dobson AP. (1988) The population biology of parasite-induced changes in host behavior. Q Rev Biol 63:139-165.
18. Dutton CJ, Junge RE, Louis EE Jr. (2003) Biochemical evaluation of free-ranging ring-tailed lemurs. (Lemur catta) in Tsimanampetsotsa Strict Nature Reserve, Madagascar. J Zoo Wildl Med 34:16-24.
19. Dutton CJ, Junge RE, Louis EE Jr. (2008) Biomedical evaluation of free-ranging red ruffed lemurs. (Varecia variegata) within the Masoala National Park, Madagascar. J Zoo Wildl Med 39:76-85.
20. Euzéby J. (1981) Diagnostic expérimental des Helminthoses animales. Ministère de l'Agriculture, Paris.
21. Ganzhorn JU Hapke A, Raharivololona BM, Ramanamanjato JB, Schmid J, Sommer S. (in press) Population genetics, parasitism and long-term population dynamics of Microcebus murinus in littoral forest fragments of south-eastern Madagascar. In: Masters J, Gamba M, Génin F. (eds) Leaping ahead: advances in prosimian biology. Springer, New York.
22. Gillespie TR, Greiner EC, Chapman CA. (2004) Gastrointestinal parasites of the guenons of western Uganda. J Parasitol 90:1356-1360.
23. Gillespie TR, Greiner EC, Chapman CA. (2005) Gastrointestinal parasites of the colobus monkeys of Uganda. J Parasitol 91:569-573.
24. Graczyk TK, DaSilva AJ, Cranfield MR, Nizeyi JB, Kalema G, Pieniazek NJ. (2001) Cryptosporidium parvum genotype 2 infections in free-ranging mountain gorillas. (Gorilla gorilla beringei) of the Bwindi Impenetrable National Park, Uganda. Parasitol Res 87:368-370.
25. Gulland FMD, Albon SD, Pemberton JM, Moorcroft PR, Clutton-Brock TH. (1993) Parasite associated polymorphism in a cyclic ungulate population. Proc R Soc Lond B 254:7-13.
26. Huffman MA, Gotoh S, Turner LA, Hamai M, Yoshida K. (1997) Seasonal trends in intestinal nematode infection and medical plant use among chimpanzees in the Mahale Mountains, Tanzania. Primates 38:111-125.
27. Hugot JP. (1998) Phylogeny of neotropical monkeys: the interplay of morphological molecular, and parasitological data. Mol Phylogenet Evol 9:408-413.
28. Hugot JP, Baylac M. (2007) Shape patterns of genital papillae in pinworms. (Enterobiinae, Oxyurida, Nematoda) parasite of primates: a landmark analysis. Infect Genet Evol 7: 168-179.
29. Hugot JP, Morand S, Gardner SL. (1995) Morphology and morphometrics of three oxyurids parasitic in primates with a description of Lemuricola microcebi n. sp. Int J Parasitol 25:1065-1075.
30. Hugot JP, Gardner SL, Morand S. (1996) The Enterobiinae subfam. nov. (Nematoda, Oxyurida) pinworm parasites of primates and rodents. Int J Parasitol 26:147-159.
31. Irwin MT, Raharison JL. (in press) A review of the endoparasites of the lemurs of Madagascar. Malagasy Nature.
32. Junge RE, Louis EE. (2002) Medical evaluation of free-ranging primates in Betampona Reserve, Madagascar. Lemur News 7:23-25.
33. Junge RE, Louis EE. (2005) Preliminary biomedical evaluation of wild ruffed lemurs. (Varecia variegata and V. rubra). Am J Primatol 66:85-94.
34. Junge RE, Louis EE Jr. (2007) Biomedical evaluation of black lemurs. (Eulemur macaco macaco) in Lokobe Reserve, Madagascar. J Zoo Wildl Med 38:67-76.
35. Junge RE, Sauther ML. (2006) Overview on the health and disease ecology of wild lemurs: conservation implications. In: Gould L, Sauther ML. (eds) Lemurs: ecology and adaptation. Springer, New York, p 423-440.
36. Junge RE, Dutton CJ, Knightly F, Williams CV, Rasambainarivo FT, Louis EE. (2008) Comparison of biomedical evaluation for white-fronted brown lemurs. (Eulemur fulvus albifrons) from four sites in Madagascar. J Zoo Wildl Med 39:567-575.
37. Kobbe S, Dausmann KH. (2009) Hibernation in Malagasy mouse lemurs as a strategy to counter environmental challenge. Naturwissenschaften 96:1221-1227.
38. Lahann P. (2007) Feeding ecology and seed dispersal of sympatric cheirogaleid lemurs. (Microcebus murinus, Cheirogaleus medius, Cheirogaleus major) in the littoral rainforest of south-east Madagascar. J Zool 271:88-98.
39. Larsen MN, Roepstorff A. (1999) Seasonal variation in development and survival of Ascaris suum and Trichuris suis eggs on pastures. Parasitology 119:209-220.
40. Martens P. (1999) How will climate change affect human health? Am Sci 87:534-541.
41. Martin RD. (1972) Behaviour and ecology of nocturnal Prosimians. Z Tierpsychol (Beiheft 9):43-89.
42. May B, Moody DB, Stebbins WC. (1988) The significant features of Japanese macaque coo sounds: a psychophysical study. Anim Behav 36:1432-1444.
43. Meyer-Lucht Y. (2003) Einfluss von Verstädterung auf Populationsstruktur, genetische Variabilität und Parasitenbefall bei der Gelbhalsmaus (Apodemus flavicollis). Diploma thesis, Universität Hamburg.
44. Meyer-Lucht Y, Sommer S. (2005) MHC diversity and the association to nematode parasitism in the yellow-necked mouse. (Apodemus flavicollis). Mol Ecol 14:2233-2243.
45. Mittermeier RA, Gil P, Hoffmann M, Pilgrim J and others. (2004) Hotspots revisited. CEMEX, Mexico City.
46. Mittermeier RA, Konstant WR, Hawkins F, Louis EE and others. (2006) Lemurs of Madagascar, 2nd edn. Conservation International, Washington, DC.
47. Nizeyi JB, Mwebe R, Nanteza A, Cranfield MR, Kalema GR, Graczyk TK. (1999) Cryptosporidium sp. and Giardia sp. infections in mountain gorillas. (Gorilla gorilla beringei) of the Bwindi Impenetrable National Park, Uganda. J Parasitol 85:1084-1088.
48. Nizeyi JB, Cranfield MR, Graczyk TK. (2002a) Cattle near the Bwindi Impenetrable National Park, Uganda, as a reservoir of Cryptosporidium parvum and Giardia duodenalis for local community and free-ranging gorillas. Parasitol Res 88:380-385.
49. Nizeyi JB, Sebunya D, da Silva AJ, Cranfield MR, Pieniazek NJ, Graczyk TK. (2002b) Cryptosporidiosis in people sharing habitats with free-ranging mountain gorillas. (Gorilla gorilla beringei), Uganda. Am J Trop Med Hyg 66:442-444.
50. Ortmann S, Schmid J, Ganzhorn JU, Heldmaier G. (1996) Body temperature and torpor in a Malagasy small primate, the mouse lemur. In: Geiser F, Hulbert AJ, Nicol SC. (eds) Adaptations to the cold: the 10th International Hibernation Symposium. University of New England Press, Armidale, NSW, p 55-61.
51. Pascual M, Ahumada JA, Chaves LF, Rodó X, Bouma M. (2006) Malaria resurgence in the East African highlands: temperature trends revisited. Proc Natl Acad Sci USA 103:5829-5834.
52. Paterson S, Wilson K, Pemberton JM. (1998) Major histocompatibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population. (Ovis aries L.). Evolution 95:3714-3719.
53. Petter AJ, Chabaud AG, Delavenay R, Brygoo ER. (1972) Une nouvelle espèce de nématode du genre Lemuricola, parasite de Daubentonia madagascariensis Gmelin, et considérations sur le genre Lemuricola. Ann Parasitol Hum Comp 47:391-398.
54. Petter JJ, Albignac R, Rumpler Y. (1977) Mammifères: lémuriens. (primates prosimiens) In: ORSTOM-CNRS. (eds) Faune de Madagascar 44. ORSTOM-CNRS, Paris.
55. Petter-Rousseaux A. (1980) Seasonal activity rhythms, reproduction, and body weight variations in five sympatric nocturnal prosimians, in simulated light and climatic conditions. In: Charles-Dominique P, Cooper HM, Hladik A, Hladik CM and others. (eds) Nocturnal Malagasy primates: ecology, physiology, and behavior. Academic Press, New York, p 137-152.
56. Raharivololona BM. (2006) Gastrointestinal parasites of Cheirogaleus spp. and Microcebus murinus in the littoral forest of Mandena, Madagascar. Lemur News 11:31-35.
57. Raharivololona BM. (2009) L'infestation parasitaire de Microcebus murinus de la forêt littorale de Mandena, Madagascar. Madag Conserv Dev 4:52-62.
58. Raharivololona BM, Ganzhorn JU. (2009) Gastrointestinal parasite infection of the gray mouse lemur. (Microcebus murinus) in the littoral forest of Mandena, Madagascar: effects of forest fragmentation and degradation. Madag Conserv Dev 4:103-112.
59. Raharivololona BM, Rakotondravao, Ganzhorn JU. (2007) Gastrointestinal parasites of small mammals in the littoral forest of Mandena. In: Ganzhorn JU, Goodman SM, Vincelette M. (eds) Biodiversity, ecology, and conservation of littoral ecosystems in southeastern Madagascar, Tolagnaro. (Fort Dauphin). Smithsonian Institution, Washington, DC, p 247-258.
60. Ramanamanjato JB, Ganzhorn JU. (2001) Effects of forest fragmentation, introduced Rattus rattus and the role of exotic tree plantations and secondary vegetation for the conservation of an endemic rodent and a small lemur in littoral forests of southeastern Madagascar. Anim Conserv 4:175-183.
61. Randriamiadamanana M. (1998) Contribution au diagnostic coprologique du parasite Spirocerca lupi chez les lémuriens du Parc Botanique et Zoologique de Tsimbazaza. Mémoire d'ingéniorat, Ecole Supérieure des Sciences Agronomiques, Université d'Antananarivo.
62. Rasambainarivo F. (2008) Contribution à l'étude des parasites des lémuriens en captivité: comparaison entre deux parcs zoologiques. PhD thesis, Université d'Antananarivo.
63. Rogers WP, Sommerville RI. (1963) The infective stage of nematode parasites and its significance in parasitism. Adv Parasitol 1:109-177.
64. Schad J, Sommer S, Ganzhorn JU. (2004) MHC variability of a small lemur in the littoral forest fragments of southeastern Madagascar. Conserv Genet 5:299-309.
65. Schad J, Ganzhorn JU, Sommer S. (2005) Parasite burden and constitution of major histocompatibility complex in the Malagasy mouse lemur, Microcebus murinus. Evolution 59:439-450.
66. Schmid J, Ganzhorn JU. (2009) Optional strategies for reduced metabolism in gray mouse lemurs. Naturwissenschaften 96:737-741.
67. Schwensow N, Fietz J, Dausmann KH, Sommer S. (2007) Neutral versus adaptive genetic variation in parasite resistance: importance of major histocompatibility complex supertypes in a free-ranging primate. Heredity 99: 265-277.
68. Sloss MW, Kemp RL, Zajak A. (1994) Veterinary clinical parasitology. Iowa State University Press, Ames, IA.
69. Stear MJ, Bishop SC, Doligalska M, Duncan JL and others. (1995) Regulation of egg production, worm burden, worm length and worm fecundity by host responses in sheep infected with Ostertagia circumcincta. Parasite Immunol 17:643-652.
70. Stuart MD, Strier KB. (1995) Primates and parasites: a case for a multidisciplinary approach. Int J Primatol 15:577-593.
71. Taraschewski H. (2006) Parasiten und Wirte als Bestandteile von Ökosystemen. In: Hiepe T, Lucius R, Gottstein B. (eds) Allgemeine Parasitologie mit den Grundzügen der Immunologie, Diagnostik und Bekämpfung. Parey, Stuttgart, p 276-322.
72. Thorne ET, William ES, Spraker TR, Helms W, Segerstrom T. (1988) Bluetongue in free-ranging pronghorn antelope. (Antilocapra americana) in Wyoming: 1976 and 1984. J Wildl Dis 24:113-119.
73. Vincelette M, Dumouchel J, Giroux J, Heriarivo R. (2007a) The Tolagnaro. (Fort Dauphin) region: a brief overview of the geology, hydrology, and climatology. In: Ganzhorn JU, Goodman SM, Vincelette M. (eds) Biodiversity, ecology and conservation of littoral ecosystems in southeastern Madagascar, Tolagnaro (Fort Dauphin). Smithsonian Institution, Washington, DC, p 9-17.
74. Wolfe ND, Escalante AA, Karesh WB, Kilbourn A, Spielman A, Lal AA. (1998) Wild primate populations in emerging infectious disease research: the missing link. Emerg Infect Dis 4:149-158.
75. Wright PC and others. (2009) Habitat disturbance and seasonal fluctuations of lemur parasites in the rain forest of Ranomafana National Park, Madagascar. In: Chapman C, Huffman MA. (eds) Primates and their parasites. Cambridge University Press, Cambridge, p 311-330.