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Variation in the helminth community structure in spiny mice (Acomys dimidiatus) from four montane wadis in the St Katherine region of the Sinai Peninsula in Egypt

Published online by Cambridge University Press:  23 August 2004

J. M. BEHNKE ,
P. D. HARRIS ,
A. BAJER ,
C. J. BARNARD ,
N. SHERIF ,
L. CLIFFE ,
J. HURST ,
M. LAMB ,
A. RHODES  and
M. JAMES
...Show all authors
J. M. BEHNKE
Affiliation:
School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK
P. D. HARRIS
Affiliation:
School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK
A. BAJER
Affiliation:
Department of Parasitology, Institute of Zoology, University of Warszawa, ul. Miecznikowa 1, 02-096 Warszawa, Poland
C. J. BARNARD
Affiliation:
School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK
N. SHERIF
Affiliation:
Department of Zoology, Suez Canal University, Ismailia, Egypt
L. CLIFFE
Affiliation:
School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK
J. HURST
Affiliation:
School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK
M. LAMB
Affiliation:
School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK
A. RHODES
Affiliation:
School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK
M. JAMES
Affiliation:
School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK
S. CLIFFORD
Affiliation:
School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK
F. S. GILBERT
Affiliation:
School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK
S. ZALAT
Affiliation:
Department of Zoology, Suez Canal University, Ismailia, Egypt
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Abstract

We compared helminth communities in spiny mice (Acomys dimidiatus) from 4 wadis in the arid montane region of the southern Sinai in Egypt, in a 4-week period in late summer. Total helminth species richness was 14 (8 nematodes, 5 cestodes and 1 acanthocephalan) with 94% of mice carrying at least 1 species and an overall mean species richness of 1·85. The most prevalent parasites were Protospirura muricola (47·8%) and Dentostomella kuntzi (46·3%). One larval cestode, Joyeuxiella rossicum, represents a new host record. The helminth community was dominated by intestinal nematodes (88·7%) of which 58·2% were arthropod-transmitted heteroxenic species. At the component community level, 70% of the worms were recovered from mice in just two wadis (Gharaba and Tlah) and 48·6% of intestinal nematodes were from Wadi Gharaba. Although only 7 species of helminths were recorded from Wadi Gharaba, this site gave the highest Berger-Parker dominance index because of P. muricola. P. muricola was also dominant in Wadi El Arbaein whilst Syphacia minuta was the dominant species in Wadis Gebal and Tlah. At the infracommunity level, mean species richness and Brillouin's index of diversity were highest in Wadi Tlah and lowest in Wadi Gebal, and the former was age dependent. Whilst mice from different wadis differed in the nematodes that were most common, those from Wadi Gharaba carried the highest mean number of worms/mouse. The abundance of P. muricola in particular varied markedly between sites: Wadi Gharaba was distinct as the site showing the highest mean worm burden whereas mice from Wadi Gebal were uninfected. None of the directly transmitted oxyuroid nematodes showed significant variation in abundance between wadis, or host sex or age classes. Overall, the single extrinsic factor in the study, site of capture, was more important than the intrinsic factors in explaining variation in helminth communities in the region. We conclude that in the high mountains of southern Sinai, each wadi is distinct in terms of its rodent parasites, and hence we expect spatially different coevolutionary pressures on their hosts, with resultant variation in life-histories.

Keywords

spiny mouseAcomys dimidiatushelminthsnematodescestodesacanthocephalanscomponent communityhelminth diversitysite-specific variation
Type
Research Article
Information
Parasitology , Volume 129 , Issue 3 , September 2004 , pp. 379 - 398
Copyright
© 2004 Cambridge University Press

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References

REFERENCES

ABU-MADI, M. A., BEHNKE, J. M., LEWIS, J. W. & GILBERT, F. S. ( 1998). Descriptive epidemiology of Heligmosomoides polygyrus in Apodemus sylvaticus from three contrasting habitats in south-east England. Journal of Helminthology 72, 93–100.CrossRefGoogle Scholar
ABU-MADI, M. A., BEHNKE, J. M., LEWIS, J. W. & GILBERT, F. S. ( 2000). Seasonal and site specific variation in the component community structure of intestinal helminths in Apodemus sylvaticus from three contrasting habitats in south-east England. Journal of Helminthology 74, 7–16.Google Scholar
ABU-MADI, M. A., LEWIS, J. W., MIKHAIL, M., EL-NAGGER, M. E. & BEHNKE, J. M. ( 2001). Monospecific helminth and arthropod infections in an urban population of brown rats from Doha, Qatar. Journal of Helminthology 75, 313–320.Google Scholar
BANGS, E. E. ( 1985). Occurrence of the nematode Protospirura muris in Alaskan Northern red-backed voles, Clethrionomys rutilus. Canadian Field Naturalist 99, 386–388.Google Scholar
BARNARD, C. J., BEHNKE, J. M., BAJER, A., BRAY, D., RACE, T., FRAKE, K., OSMOND, J., DINMORE, J. & SIŃSKI, E. ( 2002). Local variation in endoparasite intensities of bank voles (Clethrionomys glaroelus) from ecologically similar sites: morphometric and endocrine correlates. Journal of Helminthology 76, 103–112.CrossRefGoogle Scholar
BARNARD, C. J., KULIS, K., BEHNKE, J. M., BAJER, A., GROMADZKA-OSTROWSKA, J., STACHON, M. & SIŃSKI, E. ( 2003 a). Local variation in helminth burdens of bank voles (Clethrionomys glareolus) from ecologically similar sites: temporal stability and relationships with hormone concentrations and social behaviour. Journal of Helminthology 77, 185–195.Google Scholar
BARNARD, C. J., SAYED, E., BARNARD, L. E., BEHNKE, J. M., ABDEL NABI, I., SHERIF, N., SHUTT, A. & ZALAT, S. ( 2003 b). Local variation in helminth burdens of Egyptian spiny mice (Acomys cahirinus dimidiatus) from ecologically similar sites: relationships with hormone concentrations and social behaviour. Journal of Helminthology 77, 197–207.Google Scholar
BEHNKE, J. M., BARNARD, C. J., BAJER, A., BRAY, D., DINMORE, J., FRAKE, K., OSMOND, J., RACE, T. & SIŃSKI, E. ( 2001). Variation in the helminth community structure in bank voles (Clethrionomys glareolus) from three comparable localities in the Mazury Lake District region of Poland. Parasitology 123, 401–414.CrossRefGoogle Scholar
BEHNKE, J. M., BARNARD, C. J., MASON, N., HARRIS, P. D., SHERIF, N. E., ZALAT, S. & GILBERT, F. S. ( 2000). Intestinal helminths of spiny mice (Acomys cahirinus dimidiatus) from St Katherine's Protectorate in the Sinai, Egypt. Journal of Helminthology 74, 31–44.Google Scholar
BEHNKE, J. M., IRAQI, F., MENGE, D., BAKER, L., GIBSON, J. & WAKELIN, D. ( 2003). Chasing the genes that control resistance to gastrointestinal nematodes. Journal of Helminthology 77, 99–109.CrossRefGoogle Scholar
BEHNKE, J. M., LEWIS, J. W., MOHD ZAIN, S. N. & GILBERT, F. S. ( 1999). Helminth infections in Apodemus sylvaticus in southern England: interactive effects of host age, sex and year on the prevalence and abundance of infections. Journal of Helminthology 73, 31–44.Google Scholar
BROWN, J. S. ( 1989). Desert rodent community structure: a test of four mechanisms of coexistence. Ecological Monographs 59, 1–20.CrossRefGoogle Scholar
bujalska, g. & hansson, l. (Eds) ( 2000). Bank vole biology: recent advances in the population biology of a model species. Polish Journal of Ecology 48 (Suppl.), 1–235.Google Scholar
BUSH, A. O., LAFFERTY, K. D., LOTZ, J. M. & SHOSTAK, A. W. ( 1997). Parasitology meets ecology on its own terms: Margolis et al., revisited. Journal of Parasitology 83, 575–583.CrossRefGoogle Scholar
CAMPOS, M. Q. & VARGAS, M. V. ( 1977). Biologia de Protospirura muricola Gedoelst, 1916 y Mastophorus muris (Gmelin, 1790) (Nematoda: Spiruridae), en Costa Rica. I. Huespedes intermediarios. Revista de Biologia Tropical 25, 191–207.Google Scholar
CHABAUD, A. G. ( 1975). Keys to genera of the Order Spirurida. Part 2. Spiruroidea, Habronematoidea and Acuariodea. In CIH Keys to the Nematode Parasites of Vertebrates ( ed. Anderson, R. C., Chabaud, A. G. & Willmott, S.). Commonwealth Agricultural Bureaux, Slough, UK.
CRAWLEY, M. T. (1993). GLIM for Ecologists. Blackwell Scientific Press, Oxford.
DE BELLOCQ, J. G., MORAND, S. & FELIU, C. ( 2002). Patterns of parasite species richness of Western Palaearctic micro-mammals: island effects. Ecography 25, 173–183.CrossRefGoogle Scholar
DOBSON, A. P. ( 1989). Behavioural and life history adaptations of parasites for living in desert environments. Journal of Arid Environments 17, 185–192.Google Scholar
ELLIOTT, J. M. ( 1977). Some Methods for the Statistical Analysis of Samples of Benthic Invertebrates. Freshwater Biological Association, Cumbria, UK.
FICHET-CALVET, E., JUEFEI WANG, JOMAA, I., BEN ISMAIL, R. & ASHFORD, R. W. ( 2003). Patterns of the tapeworm Raillietina trapezoides infection in the fat sand rat Psammomys obesus in Tunisia: season, climatic conditions, host age and crowding effects. Parasitology 126, 481–492.CrossRefGoogle Scholar
flowerdew, j. r., gurnell, j. & gipps, j. h. w. (Eds) ( 1985). The Ecology of Woodland Rodents. Bank Voles and Wood Mice. The Zoological Society of London, Clarendon Press, Oxford.
GERLACH, G. & MUSOLF, K. ( 2000). Fragmentation of landscape as a cause for genetic subdivision in bank voles. Conservation Biology 14, 1066–1074.CrossRefGoogle Scholar
GILBERT, F., GONZALEZ, A. & EVANS-FREKE, I. (1998). Corridors maintain species richness in fragmented landscapes of natural microecosystems. Proceedings of the Royal Society of London, B 265, 577–582.CrossRefGoogle Scholar
GILBERT, F., WILLMER, P., SEMIDA, F., GHAZOUL, J. & ZALAT, S. ( 1996). Spatial variation in a plant–pollinator system in the wadis of Sinai, Egypt. Oecologia 108, 479–487.CrossRefGoogle Scholar
GILBERT, F., ZALAT, S. & SEMID, A. F. ( 1999). Insect–plant coevolution in the mountains of Sinai. Egyptian Journal of Biology 1, 142–151.Google Scholar
GIPPOLITI, S. & AMOR, G. ( 2001). Anthropochorous wild mammal taxa and conservation lists. Conservation Biology 16, 1162–1164.Google Scholar
GREENBERG, Z. ( 1969). Helminths of mammals and birds of Israel. I. Helminths of Acomys spp. (Rodentia, Murinae). Israel Journal of Zoology 18, 25–38.Google Scholar
HANSKI, I. A. ( 1997). Metapopulation dynamics: from concepts to predictive models. In Metapopulation Biology: Ecology, Genetics and Evolution ( ed. Hanski, I. A. & Gilpin, M. E.), pp. 69–91. Academic Press, San Diego.CrossRef
HARTVIGSEN, R. & KENNEDY, C. R. ( 1993). Patterns in the composition and richness of helminth communities in brown trout, Salmo trutta, in a group of reservoirs. Journal of Fish Biology 43, 603–615.CrossRefGoogle Scholar
HAUKISALMI, V. & HENTTONEN, H. ( 2000). Variability of helminth assemblages and populations in the bank vole Clethrionomys glareolus. Polish Journal of Ecology 48 (Suppl.), 219–231.Google Scholar
HOBBS, J. J. ( 1995). Mount Sinai. University of Texas Press, Austin, Texas.
HOLMES, J. C. ( 1973). Site selection by parasitic helminths; interspecific interactions, site segregation, and their importance to the development of helminth communities. Canadian Journal of Zoology 51, 333–347.CrossRefGoogle Scholar
HOOGSTRAAL, H. & TRAUB, R. ( 1965). The fleas (Siphonaptera) of Egypt. Host–parasite relationships of rodents of the families Spalacidae, Muridae, Gliridae, Dipodidae and Hystricidae. The Journal of The Egyptian Public Health Association 40, 343–379.Google Scholar
JANOVY, J. Jr., CLOPTON, R. E., CLOPTON, D. A., SNYDER, S. D., EFTING, A. & KREBS, L. ( 1995). Species density distributions as null models for ecologically significant interactions of parasite species in an assemblage. Ecological Modelling 77, 189–196.CrossRefGoogle Scholar
JONES, A. ( 1983). A revision of the cestode genus Joyeuxiella Fuhrmann, 1935 (Dipelididae: Dipylidiinae). Systematic Parasitology 5, 203–213.CrossRefGoogle Scholar
JONES, M. & DAYAN, T. ( 2000). Foraging behaviour and microhabitat use by spiny mice, Acomys cahirinus and A. russatus, in the presence of Blanford's fox (Vulpes cana) odor. Journal of Chemical Ecology 26, 455–469.Google Scholar
JONES, M., MANDELIK, Y. & DAYAN, T. ( 2001). Coexistence of temporally partitioned spiny mice: roles of habitat structure and foraging behavior. Ecology 82, 2164–2176.CrossRefGoogle Scholar
KENNEDY, C. R. & HARTVIGSEN, R. A. ( 2000). Richness and diversity of intestinal metazoan communities in brown trout Salmo trutta compared to those of eels Anguilla anguilla in their European heartlands. Parasitology 121, 55–64.CrossRefGoogle Scholar
KIMBERLY, H. D., DUSZYNSKI, D. W. & PATRICK, M. J. ( 2001). Biotic and abiotic effects on endoparasites infecting Dipodomys and Perognathus species. Journal of Parasitology 87, 300–307.Google Scholar
KINSELLA, J. M. ( 1974). Comparison of helminth parasites of the cotton rat Sigmodon hispidus, from several habitats in Florida. American Museum Novitates 2540, 1–12.Google Scholar
KISIELEWSKA, K. ( 1970). Ecological organization of intestinal helminth groupings in Clethrionomys glareolus (Schreb.) (Rodentia). III. Structure of the helminth groupings in C. glareolus populations of various forest biocoenoses in Poland. Acta Parasitologica Polonica 18, 163–176.Google Scholar
KOTLER, B. P. & BROWN, J. S. ( 1999). Mechanisms of coexistence of optimal foragers as determinants of the local abundances and distributions of desert granivores. Journal of Mammalogy 80, 361–374.CrossRefGoogle Scholar
KRASNOV, B., KHOKHLOVA, I., FIELDEN, R. & BURDELOVA, N. ( 2001). The effect of temperature and humidity on the survival of pre-imaginal stages of two flea species (Siphonaptera: Pulicidae). Journal of Medical Entomology 38, 629–637.CrossRefGoogle Scholar
MARGOLIS, L., ESCH, G. W., HOLMES, J. C., KURIS, A. M. & SCHAD, G. A. ( 1982). The use of ecological terms in parasitology (report of an ad hoc committee of The American Society of Parasitologists). Journal of Parasitology 68, 131–133.CrossRefGoogle Scholar
MARTIN, J. L. & HUFFMAN, D. G. ( 1980). An analysis of the community and population dynamics of the helminths of Sigmodon hispidus (Rodentia: Criceditae) from three central Texas vegetational regions. Proceedings of the Helminthological Society of Washington 47, 247–255.Google Scholar
MONTGOMERY, S. S. J. & MONTGOMERY, W. I. ( 1990). Structure, stability and species interactions in helminth communities of wood mice Apodemus sylvaticus. International Journal for Parasitology 20, 225–242.CrossRefGoogle Scholar
MOLYNEUX, D. & ASHFORD, R. W. ( 1983). The Biology of Trypanosoma and Leishmania, Parasites of Man and Domestic Animals. Taylor & Francis, London.
MORAND, S. & GUEGAN, J. F. ( 2000). Patterns of endemism in host–parasite associations: lessons from epidemiological models and comparative tests. Belgian Journal of Entomology 2, 135–147.Google Scholar
MORRIS, P. ( 1972). A review of mammalian age determination methods. Mammal Review 2, 69–104.CrossRefGoogle Scholar
POULIN, R. ( 1993). The disparity between observed and uniform distributions: a new look at parasite aggregation. International Journal for Parasitology 23, 937–944.CrossRefGoogle Scholar
PRICE, M. V. ( 1986). Structure of desert rodent communities: a critical review of questions and approaches. American Zoologist 26, 39–49.CrossRefGoogle Scholar
QUENTIN, J. C. ( 1969). Cycle biologique de Protospirura muricola Gedoelst 1916 (Nematoda; Spiruridae). Annales de Parasitologie (Paris) 44, 485–504.CrossRefGoogle Scholar
QUENTIN, J. C. ( 1970). Morphogenese larvarie du spiruride Mastophorus muris (Gmelin, 1790). Annales de Parasitologie (Paris) 45, 839–855.CrossRefGoogle Scholar
ROHDE, K. ( 1994). Niche restriction in parasites: proximate and ultimate causes. Parasitology 109, S69–S84.CrossRefGoogle Scholar
ROHLF, F. J. & SOKAL, R. R. ( 1995). Statistical Tables. W.H. Freeman and Company, San Francisco.
SCHARFF, A., TENORA, F., KAWALIKA, M., BARUS, V. & BURDA, H. ( 1996). Helminths from Zambian mole-rats (Cryptomys spp., Bathyergidae, Rodentia). Helminthologia 33, 105–110.Google Scholar
SCHARFF, A., BURDA, H., TENORA, F., KAWALIKA, M. & BARUS, V. ( 1997). Parasites in social subterranean Zambian mole-rats (Cryptomys spp., Bathyergidae, Rodentia). Journal of Zoology, London 241, 571–577.CrossRefGoogle Scholar
SEMIDA, F., ABDEL-DAYEM, M., ZALAT, S. & GILBERT, F. ( 2001). Habitat heterogeneity and altitudinal gradients in relation to beetle diversity in South Sinai, Egypt. Egyptian Journal of Biology 3, 137–146.Google Scholar
SHELDON, B. C. & VERHULST, S. ( 1996). Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology and Evolution 11, 317–321.CrossRefGoogle Scholar
STACY, J. E., REFSETH, U. H., THORESEN, M., IMS, R. A., STENSETH, N. C. & JAKOBSEN, K. S. ( 1994). Genetic variability among root voles (Microtus oeconomus) from different geographical regions: populations can be distinguished by DNA fingerprinting. Biological Journal of the Linnean Society 52, 273–286.CrossRefGoogle Scholar
TARASOVSKAYA, N. E. ( 1994). On the finding of cysticercoids of Joyeuxiella rossicum (Cestoda: Dipylidiidae) in rodents from Kirgistan. Izvestiya NAN Respubliki Kazakhstan. Serie Biologicheneskaya 6, 20–22. (In Russian.)Google Scholar
TENORA, F., HENTTONEN, H. & HAUKISALMI, V. ( 1983). On helminths of rodents in Finland. Annals Zoologica Fennici 20, 37–45.Google Scholar
THOMPSON, J. N. ( 1994). The Co-evolutionary Process. University of Chicago Press, Chicago.
WARD, H. L. & NELSON, D. R. ( 1967). Acanthocephala of the genus Moniliformis from rodents of Egypt with the description of a new species from Egyptian spiny mouse (Acomys cahirinus). Journal of Parasitology 53, 150–156.CrossRefGoogle Scholar
WASHINGTON, H. G. ( 1984). Diversity, biotic and similarity indices. A review with special relevance to aquatic ecosystems. Water Research 18, 653–694.CrossRefGoogle Scholar
WERTHEIM, G. ( 1962). A study of Mastophorus muris (Gmelin, 1790) (Nematoda: Spiruridae). Transactions of the American Microscopical Society 81, 274–279.CrossRefGoogle Scholar
WERTHEIM, G. & GREENBERG, Z. ( 1970). Notes on helminth parasites of myomorph rodents from Southern Sinai. Journal of Helminthology 44, 243–252.CrossRefGoogle Scholar
WERTHEIM, G., SCHMIDT, G. D. & GREENBERG, Z. ( 1986). Witenbergitaenia sinaica. N., sp.n. (Anoplocephalidae) and other cestodes from small mammals in Israel and in the Sinai Peninsula. Bulletin du Museum National d'Histoire Naturelle, Paris, 4e serie 8, 543–550.Google Scholar
WILLMER, P., GILBERT, F., GHAZOUL, J., ZALAT, S. & SEMIDA, F. ( 1994). A novel form of territoriality: daily paternal investment in an anthrophorid bee. Animal Behaviour 48, 535–549.CrossRefGoogle Scholar
WILSON, K. & GRENFELL, B. T. ( 1997) Generalized linear modelling for parasitologists. Parasitology Today 13, 33–38.CrossRefGoogle Scholar
WOLFF, K., EL-AKKAD, S. & ABBOTT, R. J. ( 1997). Population substructure in Alkanna orientalis L. Boiss. (Boraginaceae) in the Sinai desert, in relation to its pollinator behaviour. Molecular Ecology 6, 194–201.Google Scholar
ZALAT, S. & GILBERT, F. ( 1998). A walk in Sinai: St. Katherine to Al Galt Al Azraq (The Blue Pool). El Haramen Press, Cairo, Egypt.
ZALAT, S., SEMIDA, F., GILBERT, F., EL BANNA, S., SAYED, E., EL-ALQAMY, H. & BEHNKE, J. ( 2001). Spatial variation in the biodiversity of Bedouin gardens in the St Katherine Protecorate, South Sinai, Egypt. Egyptian Journal of Biology 3, 147–155.Google Scholar