Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-07T23:29:57.020Z Has data issue: false hasContentIssue false
  • English
  • Français

Host body microcosm and ectoparasite infracommunities: arthropod ectoparasites are not spatially segregated

Published online by Cambridge University Press:  05 September 2012

SHAI PILOSOF ,
MARCELA LARESCHI  and
BORIS R. KRASNOV
SHAI PILOSOF
Affiliation:
Mitrani Department of Desert Ecology, Swiss Institute for Dryland Environmental and Energy Research, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boqer Campus, 84990 Midreshet Ben-Gurion, Israel Albert Katz International School for Desert Studies, Ben-Gurion University of the Negev, Sede-Boqer Campus, 84990 Midreshet Ben-Gurion, Israel
MARCELA LARESCHI
Affiliation:
Albert Katz International School for Desert Studies, Ben-Gurion University of the Negev, Sede-Boqer Campus, 84990 Midreshet Ben-Gurion, Israel Center for Parasitological Studies and Vectors (CEPAVE, National Research and Technological Council, La Plata National University, Argentina), Calle 2 N 584, 1900 La Plata, Argentina
BORIS R. KRASNOV*
Affiliation:
Mitrani Department of Desert Ecology, Swiss Institute for Dryland Environmental and Energy Research, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boqer Campus, 84990 Midreshet Ben-Gurion, Israel
*
*Corresponding author: Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boqer Campus, 84990 Midreshet Ben-Gurion, Israel. Tel: + 972 8 6588764. Fax: +972 8 6586369. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

We studied the distribution of ectoparasite species (an ixodid tick, a chigger mite, 7 mesostigmate mites, 5 fleas and 3 lice) on bodies of 5 species of rodent hosts from the marshlands in Argentina to establish whether arthropod ectoparasites are segregated across body parts of the same host individual. We asked (a) whether an individual ectoparasite species prefers certain parts of the body of its host and, if yes, whether these preferences overlap among ectoparasite species; (b) whether ectoparasite species composition differs among different parts of a host's body; and (c) whether co-occurrences of ectoparasite species within pre-defined body parts of a host are non-random and, if yes, whether ectoparasites co-occur in the same body part of a host either less or more often than expected by chance. It was found that, in general, ectoparasite species were not segregated across body parts of a host. Although some ectoparasites preferred certain body parts, these preferences were similar among ectoparasites belonging to different species and/or higher taxa resulting in similarity among host body parts in ectoparasite species composition. In addition, ectoparasite species demonstrated a tendency to co-occur on the same body parts of a host and not to be segregated among them. It was concluded that the distribution of ectoparasites on the body of a small mammalian host is driven mainly by their interaction with the host rather than by distinct preferences or interactions among ectoparasite species.

Keywords

body partco-occurrenceectoparasitesgroomingrodentssimilarity
Type
Research Article
Information
Parasitology , Volume 139 , Issue 13 , November 2012 , pp. 1739 - 1748
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Beldoménico, P. M., Lareschi, M., Nava, S., Mangold, A. J. and Guglielmone, A. A. (2005). The parasitism of immature stages of Ixodes loricatus (Acari: Ixodidae) on wild rodents in Argentina. Experimental and Applicative Acarology 36, 139–148.CrossRefGoogle ScholarPubMed
Bush, A. O. and Holmes, J. C. (1986 a). Intestinal helminths of lesser scaup ducks: patterns of association. Canadian Journal of Zoology 64, 132–141.CrossRefGoogle Scholar
Bush, A. O. and Holmes, J. C. (1986 b). Intestinal helminths of lesser scaup ducks: an interactive community. Canadian Journal of Zoology 64, 132–141.CrossRefGoogle Scholar
Bush, A. O., Lafferty, K. D., Lotz, J. M. and Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.CrossRefGoogle Scholar
Bush, S. E. and Malenke, J. R. (2008). Host defence mediates interspecific competition in ectoparasites. Journal of Animal Ecology 77, 558–564.CrossRefGoogle ScholarPubMed
Chilton, N. B., Bull, C. M. and Andrews, R. H. (1992). Niche segregation in reptile ticks: attachment sites and reproductive success of females. Oecologia 90, 255–259.CrossRefGoogle ScholarPubMed
Choe, J. C. and Kim, K. C. (1989). Microhabitat selection and coexistence in feather mites (Acari, Analgoidea) in Alaskan seabirds. Oecologia 79, 10–14.CrossRefGoogle ScholarPubMed
Clarke, K. R. (1993). Non-parametric multivariate analysis of changes in community structure. Australian Journal of Ecology 18, 117–143.CrossRefGoogle Scholar
Clarke, K. R. and Gorley, R. N. (2006). Primer v6: User Manual/Tutorial. Primer-E Ltd, Plymouth Marine Laboratory, Plymouth, UK.Google Scholar
Combes, C. (2001). Parasitism. The Ecology and Evolution of Intimate Interactions. University of Chicago Press, Chicago, IL, USA.Google Scholar
Connel, J. H. (1980). Diversity and the coevolution of competitors, or the ghost of competition past. Oikos 35, 131–138.CrossRefGoogle Scholar
Denwood, M. J., Stear, M. J., Matthews, L., Reid, S. W. J., Toft, N. and Innocent, G. T. (2008). The distribution of the pathogenic nematode Nematodirus battus in lambs is zero-inflated. Parasitology 135, 1225–1235.CrossRefGoogle ScholarPubMed
Dubinina, V. B. and Dubinin, M. N. (1951). Parasite fauna of mammals of the Dauric Steppe. Fauna and Ecology of Rodents 4, 98–156 (in Russian).Google Scholar
Entsminger, G. L. (2012). EcoSim Professional: Null modeling software for ecologists, Version 1. Acquired Intelligence Inc., Kesey-Bear and Pinyon Publishing. Montrose, CO 81403, USA. http://www.garyentsminger.com/ecosim/index.htmGoogle Scholar
Friggens, M. M. and Brown, J. H. (2005). Niche partitioning in the cestode communities of two elasmobranchs. Oikos 108, 76–84.CrossRefGoogle Scholar
Furman, D. P. (1959). Feeding habits of symbiotic mesostigmatid mites of mammals in relation to pathogen-vector potentials. American Journal of Tropical Medicine and Hygiene 8, 5–12.CrossRefGoogle ScholarPubMed
Geets, A., Coene, H. and Ollevier, F. (1997). Ectoparasites of the whitespotted rabbitfish, Siganus sutor (Valenciennes, 1835) off the Kenyan Coast: Distribution within the host population and site selection on the gills. Parasitology 115, 69–79.CrossRefGoogle ScholarPubMed
Gotelli, N. J. (2000). Null model analysis of species co-occurrence patterns. Ecology 81, 2606–2621.CrossRefGoogle Scholar
Gotelli, N. J. and Graves, G. R. (1996) Null Models in Ecology. Smithsonian Institution Press, Washington, USA.Google Scholar
Gotelli, N. J. and McCabe, D. J. (2002). Species co-occurrence: A meta-analysis of J. M. Diamond's assembly rules model. Ecology 83, 2091–2096.CrossRefGoogle Scholar
Gotelli, N. J. and Rohde, K. (2002). Co-occurrence of ectoparasites of marine fishes: a null model analysis. Ecology Letters 5, 86–94.CrossRefGoogle Scholar
Haukisalmi, V. and Henttonen, H. (1990). The impact of climatic factors and host density on the long-term population dynamics of vole helminths. Oecologia 83, 309–315.CrossRefGoogle ScholarPubMed
Holmes, J. C. and Price, P. W. (1986). Communities of parasites. In Community Ecology: Patterns and Processes (ed. Kikkawa, J. and Anderson, D. J.), pp. 187–213. Blackwell Science, NY, USA.Google Scholar
Jackman, S. (2011). pscl: Classes and Methods for R Developed in the Political Science. Computational Laboratory and Department of Political Science, Stanford University, Stanford, CA, USA.Google Scholar
Kadulski, S. and Dobryńszuk, J. (1976). Observations of the ectoparasites of the European hare. In Ecology and Management of European Hare Populations. Proceedings of an International Symposium Held in Poznań on 23–24 December 1974 (ed. Pielowski, Z. and Pucek, Z.), pp. 177–183. Polish Hunting Association, Warsaw, Poland.Google Scholar
Kelly, D. W. and Thompson, C. E. (2000). Epidemiology and optimal foraging: modelling the ideal free distribution of insect vectors. Parasitology 120, 319–327.CrossRefGoogle ScholarPubMed
Krasnov, B. R. (2008). Functional and Evolutionary Ecology of Fleas. A Model for Ecological Parasitology. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Krasnov, B. R., Mouillot, D., Khokhlova, I. S., Shenbrot, G. I. and Poulin, R. (2005). Covariance in species diversity and facilitation among non-interactive parasite taxa: all against the host. Parasitology 131, 557–568.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Stanko, M. and Morand, S. (2006). Are ectoparasite communities structured? Species co-occurrence, temporal variation and null models. Journal of Animal Ecology 75, 1330–1339.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Hovhanyan, A., Khokhlova, I. S. and Degen, A. A. (2007). Density-dependence and feeding success in haematophagous ectoparasites. Parasitology 134, 1379–1386.CrossRefGoogle ScholarPubMed
Kuris, A. (1990). Guild structure of larval trematodes in molluscan hosts: prevalence, dominance and significance of competition. In Parasite Communities, Patterns and Processes (ed. Esch, G. W., Bush, A. O. and Aho, J. M.), pp. 69–100. Chapman & Hall, London, UK.CrossRefGoogle Scholar
Lareschi, M. and Krasnov, B. R. (2010). Determinants of ectoparasite assemblage structure on rodent hosts from South American marshlands: the effect of host species, locality and season. Medical and Veterinary Entomology 24, 284–292.Google ScholarPubMed
Lareschi, M. & Liljesthrom, G. (2000). Distribución espacial de los huevos de tres especies del género Hoplopleura Enderlein (Phthiraptera: Hoplopleuridae) ectoparásitas de roedores (Rodentia: Muridae: Sigmodontinae). Revista de la Sociedad Entomológica Argentina 59, 1–6.Google Scholar
Lareschi, M., Notarnicola, J., Nava, S. and Navone, G. (2007). Parasite community (arthropods and filarioids) associated with wild rodents from the marshes of La Plata River, Argentina. Comparative Parasitology 74, 141–147.CrossRefGoogle Scholar
Linsdale, J. M. and Davis, B. S. (1956). Taxonomic appraisal and occurrence of fleas at the Hastings Reservation in Central California. University of California Publications in Zoology 54, 293–370.Google Scholar
Ma, L.-M. (1983). Distribution of fleas in the hair coat of the host. Acta Entomologica Sinica 26, 409–412 (in Chinese).Google Scholar
Ma, L.-M. (1989). The distribution of fleas on the host body in relation to temperature and the number of fleas. Acta Entomologica Sinica 32, 68–73 (in Chinese).Google Scholar
Martin, T. G., Wintle, B. A., Rhodes, J. R., Kuhnert, P. M., Field, S. A., Low-Choy, S. J., Tyre, A. J. and Possingham, H. P. (2005). Zero tolerance ecology: improving ecological inference by modelling the source of zero observations. Ecology Letters 8, 1235–1246.CrossRefGoogle ScholarPubMed
Marshall, A. G. (1981). The Ecology of Ectoparasitic Insects. Academic Press, London, UK.Google Scholar
Mead-Briggs, A. R., Vaughan, J. A. and Rennison, B. D. (1975). Seasonal variation in numbers of the rabbit flea on the wild rabbit. Parasitology 70, 103–118.CrossRefGoogle ScholarPubMed
Mestre, A., Mesquita-Joanes, F., Proctor, H. and Monrós, J. S. (2011). Different scales of spatial segregation of two species of feather mites on the wings of a passerine bird. Journal of Parasitology 97, 237–244.CrossRefGoogle ScholarPubMed
Morand, S., Hafner, M. S., Page, R. D. M. and Reed, D. L. (2000). Comparative body size relationships in pocket gophers and their chewing lice. Biological Journal of the Linnean Society 70, 239–249.CrossRefGoogle Scholar
Morrone, J. J. (2001) Biogeografía de América Latina y el Caribe. Manuales y Tesis Sociedad Entomológica Aragonesa 3, 1–148.Google Scholar
Mullens, B. A. and Gerhardt, R. R. (1979). Feeding behaviour of some Tennessee Tabanidae. Environmental Entomology 8, 1047–1051.CrossRefGoogle Scholar
Munroe, S. E. M., Avery, T. S., Shutler, D. and Dadswell, M. J. (2011). Spatial attachment-site preferences of macroectoparasites on Atlantic sturgeons Acipenser oxyrinchus in Minas Basin, Bay of Fundy, Canada. Journal of Parasitology 97, 377–383.CrossRefGoogle Scholar
Murray, M. D. and Nicholls, D. G. (1965). Studies of the ectoparasites of seals and penguins. I. The ecology of the louse Lepidophthirus macrorhini Enderlein on the southern elephant seal, Mirounga leonina (L.). Australian Journal of Zoology 13, 437–454.CrossRefGoogle Scholar
Murray, M. D., Smith, M. S. R. and Soucek, Z. (1965). Studies of the ectoparasites of seals and penguins. II. The ecology of the louse Antarctophthirus ogmorhini Enderlein on the Weddel seal, Leptonychotes weddelli Lesson. Australian Journal of Zoology 13, 761–771.CrossRefGoogle Scholar
Nelson, B. C. and Murray, N. D. (1971). The distribution of Mallophaga on the domestic pigeon (Columba livia). International Journal for Parasitology 1, 21–29.CrossRefGoogle ScholarPubMed
Nikitina, N. A. and Nikolaeva, G. (1981). Ability of rodents to clean themselves of specific and non-specific fleas. Zoologicheskyi Zhurnal 60, 165–167 (in Russian).Google Scholar
Nilsson, A. (1981). Spatial differentiation of ectoparasites on small mammals. Holarctic Ecology 4, 184–190.Google Scholar
Patrick, M. J. (1991). Distribution of enteric helminthes in Glaucomys volans L. (Sciuridae): a test for competition. Ecology 72, 755–758.CrossRefGoogle Scholar
Poulin, R. (2007). Evolutionary Ecology of Parasites: From Individuals to Communities, 2nd Edn. Princeton University Press, Princeton, NJ, USA.CrossRefGoogle Scholar
Prasad, R. S. (1972). Different site selections by the rat fleas Xenopsyllsa cheopis and Xenopsyllsa astia (Siphonaptera, Pulicidae). Entomologist's Gazette 108, 63–64.Google Scholar
R Development Core Team. (2011). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org.Google Scholar
Radovsky, F. J. (1985). Evolution of mammalian mesostigmatid mites. In Coevolution of Parasitic Arthropods and Mammals (ed. Kim, K. C.), pp. 441–504. John Wiley and Sons, NY, USA.Google Scholar
Reiczigel, J. and Rozsa, L. (1998). Host-mediated site segregation of ectoparasites: an individual-based simulation study. Journal of Parasitology 98, 491–498.CrossRefGoogle Scholar
Reed, D. L., Hafner, M. S., Allen, S. K. and Smith, M. B. (2000). Spatial partitioning of host habitat by chewing lice of the genera Geomydoecus and Thomomydoecus (Phthiraptera: Trichodectidae). Journal of Parasitology 86, 951–955.CrossRefGoogle ScholarPubMed
Rohde, K. (1979). A critical evaluation of intrinsic and extrinsic factors responsible for niche restriction in parasites. American Naturalist 114, 648–671.CrossRefGoogle Scholar
Rohde, K. (1991). Intra- and interspecific interactions in low density populations in resource-rich habitats. Oikos 60, 91–104.CrossRefGoogle Scholar
Ross, A. (1961). Biological studies of bat ectoparasites of the genus Trichobius (Diptera: Streblidae) in North America, north of Mexico. Wasmann Journal of Biology 19, 229–246.Google Scholar
Rozsa, L. (1993). An experimental test of the site specificity of preening to control lice in feral pigeons. Journal of Parasitology 79, 968–970.CrossRefGoogle ScholarPubMed
Roubal, F. R. and Quartararo, N. (1992). Observations on the pigmentation in the monogeneans, Anoplodiscus spp. (family Anoplodiscidae) in different microhabitats on their sparid teleost hosts. International Journal for Parasitology 22, 459–464.CrossRefGoogle ScholarPubMed
Rust, R. W. (1974). The population dynamics and host utilization of Geomydoecus oregonus, a parasite of Thomomys bottae. Oecologia 15, 287–304.CrossRefGoogle ScholarPubMed
Shepherd, R. C. H. and Edmonds, J. W. (1979). The distribution of the stickfast fleas, Echidnophaga myrmecobii Rothschild and E. perilis Jordan, on the wild rabbit, Oryctolagus cuniculus (L.). Australian Journal of Zoology 27, 261–271.CrossRefGoogle Scholar
Šimkova, A., Verneau, O., Gelnar, M. and Morand, S. (2006). Specificity and specialization of congeneric monogeneans parasitizing Cyprinid fish. Evolution 60, 1023–1037.Google ScholarPubMed
Sokolov, V. E. (1982). Mammal Skin. University of California Press, Berkeley, CA, USA.CrossRefGoogle Scholar
Sørensen, T. (1948). A method of establishing groups of equal amplitude in plant sociology based on similarity of species content and its application to analyses of the vegetation on Danish commons. Videnski Selskab Biologiske Skrifter 5, 1–34.Google Scholar
Stock, T. M. and Holmes, J. C. (1988). Functional relationships and microhabitat distributions of enteric helminths of grebes (Podicepedidae): the evidence for interactive communities. Journal of Parasitology 74, 214–227.CrossRefGoogle ScholarPubMed
Stone, L. and Roberts, A. (1991). Conditions for a species to gain advantage from the presence of competitors. Ecology 72, 1964–1972.CrossRefGoogle Scholar
ter Hofstede, T. M., Fenton, M. B. and Whitaker, J. O. Jr (2004). Host and host-site specificity of bat flies (Diptera: Streblidae and Nycteribiidae) on Neotropical bats (Chiroptera). Canadian Journal of Zoology 82, 616–626.CrossRefGoogle Scholar
Tello, J. S., Stevens, R. D. and Dick, C. W. (2008). Patterns of species co-occurrence and density compensation: a test for interspecific competition in bat ectoparasite infracommunities. Oikos 117, 693–702.CrossRefGoogle Scholar
Traub, R. (1972). The relationship between the spines, combs and other skeletal features of fleas (Siphonaptera) and the vestiture, affinities and habits of their hosts. Journal of Medical Entomology 9, 601.Google Scholar
Vansulin, S. A. and Volkova, L. A. (1962). The coat of Rhombomys opimus Licht. and its action upon the numerousness of the fleas parasitizing these rodents during different seasons. Zoologicheskyi Zhurnal 41, 147–150 (in Russian).Google Scholar
Vashchenok, V. S. (1988). Fleas - Vectors of Pathogens Causing Diseases in Humans and Animals. Nauka, Leningrad, USSR (in Russian).Google Scholar
Wallach, A. D., Shanas, U., Mumcuoglu, K. Y. and Inbar, M. (2008). Ectoparasites on reintroduced roe deer Capreolus capreolus in Israel. Journal of Wildlife Diseases 44, 693–696.CrossRefGoogle ScholarPubMed
Wilson, K., Bjørnstad, O. N., Dobson, A. P., Merler, S., Poglaen, G., Randolph, S. E., Read, A. F. and Skorping, A. (2001). Heterogeneities in macroparasite infections: Patterns and processes. In The Ecology of Wildlife Diseases (ed. Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. and Dobson, A. P.), pp. 6–44. Oxford University Press, Oxford, UK.Google Scholar
Zeileis, A., Kleiber, K. and Jackman, S. (2008). Regression models for count data in R. Journal of Statistical Software 27, 1–25.CrossRefGoogle Scholar
Zuur, A. F., Ieno, E. N. and Smith, G. M. (2007). Analysing Ecological Data. Springer, Berlin, Germany.CrossRefGoogle Scholar
Zuur, A. F., Ieno, E. N., Walker, N., Saveliev, A. A. and Smith, G. M. (2009). Mixed Effects Models and Extensions in Ecology. R. Springer, NY, USA.CrossRefGoogle Scholar
Supplementary material: File

Pilosof Supplementary Material

Table 1

Download Pilosof Supplementary Material(File)
File 187.4 KB