Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-23T04:06:38.901Z Has data issue: false hasContentIssue false
  • English
  • Français

Long-term spatiotemporal stability and dynamic changes in helminth infracommunities of spiny mice (Acomys dimidiatus) in St. Katherine's Protectorate, Sinai, Egypt

Published online by Cambridge University Press:  20 June 2018

Jerzy M. Behnke Open the ORCID record for Jerzy M. Behnke [Opens in a new window] ,
Anna Bajer ,
Jolanta Behnke-Borowczyk ,
Natalie Clisham ,
Francis Gilbert ,
Aimee Glover ,
Laura Jeffery ,
Jonathan Kirk ,
Ewa J. Mierzejewska  and
Simon C. Mills
...Show all authors
Jerzy M. Behnke
Affiliation:
School of Life Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK
Anna Bajer
Affiliation:
Department of Parasitology, Institute of Zoology, Faculty of Biology, University of Warsaw, 1 Miecznikowa Street, 02-096 Warsaw, Poland
Jolanta Behnke-Borowczyk
Affiliation:
Department of Forest Pathology, Faculty of Forestry, Poznań University of Life Sciences, 71C Wojska Polskiego Street, 60-625 Poznan, Poland
Natalie Clisham
Affiliation:
School of Life Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK
Francis Gilbert
Affiliation:
School of Life Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK
Aimee Glover
Affiliation:
School of Life Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK
Laura Jeffery
Affiliation:
School of Life Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK
Jonathan Kirk
Affiliation:
School of Life Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK
Ewa J. Mierzejewska
Affiliation:
Department of Parasitology, Institute of Zoology, Faculty of Biology, University of Warsaw, 1 Miecznikowa Street, 02-096 Warsaw, Poland
Simon C. Mills
Affiliation:
School of Life Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK
Eman M. E. Mohallal
Affiliation:
Desert Research Centre, 1 Mataf El Matareya St, El Matareya, Cairo, Egypt
Oliver Padget
Affiliation:
School of Life Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK
Ralph Wainer
Affiliation:
School of Life Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK
Samy Zalat
Affiliation:
Department of Zoology, Suez Canal University, Ismailia, Egypt
Get access Rights & Permissions [Opens in a new window]

Abstract

The importance of parasites as a selective force in host evolution is a topic of current interest. However, short-term ecological studies of host–parasite systems, on which such studies are usually based, provide only snap-shots of what may be dynamic systems. We report here on four surveys, carried out over a period of 12 years, of helminths of spiny mice (Acomys dimidiatus), the numerically dominant rodents inhabiting dry montane wadis in the Sinai Peninsula. With host age (age-dependent effects on prevalence and abundance were prominent) and sex (female bias in abundance in helminth diversity and in several taxa including Cestoda) taken into consideration, we focus on the relative importance of temporal and spatial effects on helminth infracommunities. We show that site of capture is the major determinant of prevalence and abundance of species (and higher taxa) contributing to helminth community structure, the only exceptions being Streptopharaus spp. and Dentostomella kuntzi. We provide evidence that most (notably the Spiruroidea, Protospirura muricola, Mastophorus muris and Gongylonema aegypti, but with exceptions among the Oxyuroidae, e.g. Syphacia minuta), show elements of temporal-site stability, with a rank order of measures among sites remaining similar over successive surveys. Hence, there are some elements of predictability in these systems.

Keywords

Acomys dimidiatuscestodeshelminthshelminth infracommunitiesnematodessite-specific parasite variationspiny mice
Type
Research Article
Information
Parasitology , Volume 146 , Issue 1 , January 2019 , pp. 50 - 73
Copyright
Copyright © Cambridge University Press 2018 

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.)

Footnotes

*

Current address: Department of Zoology, University of Oxford, Radcliffe Observatory Quarter, Woodstock Road, Oxford OX2 6GG, UK.

References

Abu-Madi, MA et al. (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
Alfudhala, SMS (2015) Molecular Ecology and Evolution of a Desert Rodent: Testing Predictions in Wild Nonmodel Species. PhD thesis. University of Sheffield.Google Scholar
Alsarraf, M et al. (2016) Long-term spatiotemporal stability and dynamic changes in the haemoparasite community of spiny mice (Acomys dimidiatus) in four montane wadis in the St. Katherine Protectorate, Sinai, Egypt. Parasites and Vectors 9, 195.Google Scholar
Anderson, RM and Gordon, DM (1982) Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortalities. Parasitology 85, 373–398.Google Scholar
Anya, AO (1966) Studies on the biology of some oxyurid nematodes. I. Factors in the development of eggs of Aspiculuris tetraptera Schulz. Journal of Helminthology 40, 253–260.Google Scholar
Arai, H (1980) Biology of the Tapeworm Hymenolepis Diminuta. New York & London: Academic Press.Google Scholar
Ashour, AA and Lewis, JW (1982) The morphology of Dentostomella kuntzi (Nematoda: Oxyuroidea) from Egyptian rodents. Journal of Helminthology 56, 159–168.Google Scholar
Babayan, SA et al. (2018) The immune and non-immune pathways that drive chronic gastrointestinal helminth burdens in the wild. Frontiers in Immunology 9, 56.Google Scholar
Bajer, A et al. (2005) Medium-term temporal stability of the helminth component community structure in bank voles (Clethrionomys glareolus) from the Mazury Lake District region of Poland. Parasitology 130, 213–228.Google Scholar
Barnard, CJ et al. (2002) Local variation in endoparasite intensities of bank voles (Clethrionomys glareolus) from ecologically similar sites: morphometric and endocrine correlates. Journal of Helminthology 76, 103–112.Google Scholar
Barnard, CJ et al. (2003) 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, JM (1975) Immune expulsion of the nematode Aspiculuris tetraptera from mice given primary and challenge infections. International Journal for Parasitology 5, 511–515.Google Scholar
Behnke, JM (1976) Aspiculuris tetraptera in wild Mus musculus. Age resistance and acquired immunity. Journal of Helminthology 50, 197–202.Google Scholar
Behnke, JM (2001) Hymenolepis diminuta (Cestoda). In Halton, DW, Behnke, JM and Marshall, I (eds), British Society for Parasitology. Practical Exercises in Parasitology. Cambridge: Cambridge University Press, pp. 115–121.Google Scholar
Behnke, JM, Bland, PW and Wakelin, D (1977) Effect of the expulsion phase of Trichinella spiralis on Hymenolepis diminuta infection in mice. Parasitology 75, 79–88.Google Scholar
Behnke, JM et al. (1999) Helminth infections in Apodemus sylvaticus in southern England: interactive effects of host-age, sex and year on prevalence and abundance of infections. Journal of Helminthology 73, 31–44.Google Scholar
Behnke, JM et al. (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, JM et al. (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.Google Scholar
Behnke, JM et al. (2004) 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. Parasitology 129, 379–398.Google Scholar
Behnke, JM et al. (2008) Temporal and between-site variation in helminth communities of bank voles (Myodes glareolus) from NE Poland. 2. The infracommunity level. Parasitology 135, 999–1018.Google Scholar
Booth, M (2006) The role of residential location in apparent helminth and malaria associations. Trends in Parasitology 22, 359–362.Google Scholar
Bordes, F et al. (2012) Is there sex-biased resistance and tolerance in Mediterranean wood mouse (Apodemus sylvaticus) populations facing multiple helminth infections? Oecologia 170, 123–135.Google Scholar
Bradley, CA and Altizer, S (2006) Urbanization and the ecology of wildlife diseases. Trends in Ecology and Evolution 22, 95–102.Google Scholar
Brooks, DR and Hoberg, EP (2007) How will global climate change affect parasite-host assemblages? Trends in Parasitology 23, 571–574.Google Scholar
Brouat, C et al. (2007) Host ecology and variation in helminth community structure in Mastomys rodents from Senegal. Parasitology 134, 437–450.Google Scholar
Bugmyrin, SV et al. (2005) Patterns of host-parasite interactions between the nematode Heligmosomum mixtum (Schulz, 1952) and the bank vole (Clethrionomys glareolus Schreber, 1780). Parasitologia 39, 414–422.Google Scholar
Bush, AO and Lotz, JM (2000) The ecology of “crowding”. Journal of Parasitology 86, 212–213.Google Scholar
Calabrese, JM, Brunner, JL and Ostfeld, RS (2011) Partitioning the aggregation of parasites on hosts into intrinsic and extrinsic components via an extended Poisson-Gamma mixture model. PLoS ONE 6, e29215.Google Scholar
Calvete, C et al. (2004) Spatial variation in helminth community structure in the red-legged partridge (Alectoris rufa L.): effects of definitive host density. Parasitology 129, 101–113.Google Scholar
Campos, MQ and Vargas, MV (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
Cassola, F (2016 a) Acomys dimidiatus. (errata version published in 2017) The IUCN Red List of Threatened Species 2016: e.T136471A115208221. Available at http://dx.doi.org/10.2305/IUCN.UK.2016-3.RLTS.T136471A22453198.en. Downloaded on 26 November 2017.Google Scholar
Cassola, F (2016 b) Acomys cahirinus. (errata version published in 2017) The IUCN Red List of Threatened Species 2016: e.T263A115048396. Available at http://dx.doi.org/10.2305/IUCN.UK.2016-3.RLTS.T263A22453346.en. Downloaded on 26 November 2017.Google Scholar
Chabaud, AG (1975) NO. 3. Keys to genera of the Order Spirurida. Part 2. Spiruroidea, Habronematoidea and Acuarioidea. In Anderson, RC, Chabaud, AG and Willmott, S (eds), CIH Keys to the Nematode Parasites of Vertebrates. Slough, UK: Commonwealth Agricultural Bureaux, pp. 29–58.Google Scholar
Decker, KH, Duszynski, DW and Patrick, MJ (2001) Biotic and abiotic effects on endoparasites infecting Dipodomys and Perognathus species. Journal of Parasitology 87, 300–307.Google Scholar
Dwużnik, D et al. (2017) Comparison of the helminth communities of Apodemus agrarius and Apodemus flavicollis from urban and suburban populations of mice. Parasitology Research 116, 2995–3006.Google Scholar
Eira, C et al. (2006) Ecological aspects influencing the helminth community of the wood mouse Apodemus sylvaticus in Dunas de Mira, Portugal. Acta Parsitologica 51, 300–308.Google Scholar
Eisen, RJ and Wright, NM (2001) Landscape features associated with infection by a malaria parasite (Plasmodium mexicanum) and the importance of multiple scale studies. Parasitology 122, 507–513.Google Scholar
Elliott, JM (1977) Some Methods for the Statistical Analysis of Samples of Benthic Invertebrates. Cumbria, UK: Freshwater Biological Association.Google Scholar
Elton, C, Ford, EB, Baker, JR and Gardiner, AD (1931) The health and parasites of a wild mouse population. Proceedings of the Zoological Society of London 1931, 657–721.Google Scholar
Elton, CS (1924) Periodic fluctuations in the numbers of animals: their causes and effects. Journal of Experimental Biology 2, 119–163.Google Scholar
Ferrari, N et al. (2004) The role of host sex in parasite dynamics: field experiments on the yellow-necked mouse Apodemus flavicollis. Ecology Letters 7, 88–94.Google Scholar
Ferrari, N et al. (2007) The role of sex in parasite dynamics: model simulations on transmission of Heligmosomoides polygyrus in populations of yellow-necked mice, Apodemus flavicollis. International Journal for Parasitology 37, 341–349.Google Scholar
Froeschke, G et al. (2010) Effects of precipitation on parasite burden along a natural climatic gradient in Southern Africa – implications for possible shifts in infestation patterns due to global changes. Oikos 119, 1029–1039.Google Scholar
Gilbert, F et al. (1996) Spatial variation in a plant-pollinator system in the wadis of Sinai, Egypt. Oecologia 108, 479–487.Google Scholar
Gouveia, A et al. (2015) Long-term pattern of population dynamics in the field vole from central Europe: cyclic pattern with amplitude dampening. Population Ecology 57, 581–589.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
Gregory, RD (1992) On the interpretation of host-parasite ecology: Heligmosomoides polygyrus (Nematoda) in wild wood mouse (Apodemus sylvaticus) populations. Journal of Zoology, London 226, 109–121.Google Scholar
Gregory, RD, Montgomery, SSJ and Montgomery, WI (1992) Population biology of Heligmosomoides polygyrus (Nematoda) in the wood mouse. Journal of Animal Ecology 61, 749–757.Google Scholar
Grzybek, M et al. (2015 a) Long-term spatiotemporal stability and dynamic changes in helminth infracommunities of bank voles (Myodes glareolus) in NE Poland. Parasitology 142, 1722–1743.Google Scholar
Grzybek, M et al. (2015 b) Female host sex-biased parasitism with the rodent stomach nematode Mastophorus muris in wild bank voles (Myodes glareolus). Parasitology Research 114, 523–533.Google Scholar
Haukisalmi, V, Henttonen, H and Tenora, F (1988) Population dynamics of common and rare helminths in cyclic vole populations. Journal of Animal Ecology 57, 807–825.Google Scholar
Hobbs, JJ (1995) Mount Sinai. Austin, Texas: University of Texas Press.Google Scholar
Holland, C (1987) Interspecific effects between Moniliformis (Acanthocephala), H. diminuta (Cestoda) and N. brasiliensis (Nematoda) in the laboratory rat. Parasitology 94, 567–581.Google Scholar
Holmes, JC (1961) Effects of concurrent infections on Hymenolepis diminuta (cestoda) and Moniliformis dubius (acanthocephala). 1. General effects and comparison with crowding. Journal of Parasitology 47, 209–216.Google Scholar
Houghton, J (2009) Global Warming: The Complete Briefing. 4th Edn. Cambridge: Cambridge University Press.Google Scholar
Hudson, PJ et al. (2006) Climate disruption and parasite-host dynamics: patterns and processes associated with warming and the frequency of extreme climatic events. Journal of Helminthology 80, 175–182.Google Scholar
Huntley, JW et al. (2014) A complete Holocene record of trematode-bivalve infection and implications for the response of parasitism to climate change. Proceedings of the National Academy of Sciences of the United States of America 111, 18150–18155.Google Scholar
Jackson, JA et al. (2014) An immunological marker of tolerance to infection in wild rodents. PLoS Biology 12, e1001901.Google Scholar
Janova, E et al. (2010) Determinants of the prevalence of Heligmosomum costellatum (Heligmosomidae: Trichostrongyloidea) in a common vole population in southern Moravia, Czech Republic. Journal of Helminthology 84, 410–414.Google Scholar
Joyeux, C (1927) Recherches sur la faune helminthologique algerienne (cestodes et trematodes). Archives De l'Institut Pasteur d'Algeri 5, 509–528.Google Scholar
Kinsella, JM (1974) Comparison of helminth parasites of the cotton rat, Sigmodon hispidus, from several habitats in Florida. American Museum Novitates 2540, 1–11.Google Scholar
Kisielewska, K (1970) Ecological organization of intestinal helminth groupings in Clethrionomys glareolus (Schreb.) (Rodentia). 1. Structure and seasonal dynamics of helminth groupings in a host population in the Bialowieża National Park. Acta Parasitologica Polonica 18, 121–147.Google Scholar
Kisielewska, K (1971) Intestinal helminths as indicators of the age structure of Microtus arvalis Pallas, 1778 population. Bulletin de L'Academie Polonaise des Sciences. Serie des Sciences Biologiques Cl.II 19, 275–282.Google Scholar
Knowles, SCL et al. (2013) Stability of within-host-parasite communities in a wild mammal system. Proceedings of the Royal Society B: Biological Sciences 280, 20130598.Google Scholar
Lambin, X, Petty, SJ and Mackinnon, JL (2000) Cyclic dynamics in field vole populations and generalist predation. Journal of Animal Ecology 69, 106–118.Google Scholar
Lewis, JW (1968) Studies on the helminth parasites of the long-tailed field mouse, Apodemus sylvaticus sylvaticus from Wales. Journal of Zoology, London 154, 287–312.Google Scholar
Lewis, JW and Ashour, AA (1983) The morphology of Streptopharagus kuntzi and S. numidicus (Nematoda: Spiruroidea) from Egyptian rodents. Systematic Parasitology 5, 223–233.Google Scholar
Lochmiller, PL and Deerenberg, C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88, 87–98.Google Scholar
Lowrie, FM, Behnke, JM and Barnard, CJ (2004) Density-dependent effects on the survival and growth of the rodent stomach worm Protospirura muricola in laboratory mice. Journal of Helminthology 78, 121–128.Google Scholar
Loxton, KC et al. (2017) Parasite dynamics in an invaded ecosystem: helminth communities of native wood mice are impacted by the invasive bank vole. Parasitology 144, 1476–1489.Google Scholar
Luong, LT, Grear, DA and Hudson, PJ (2009) Male hosts are responsible for the transmission of a trophically transmitted parasite, Pterygodermatites peromysci, to the intermediate host in the absence of sex-biased infection. International Journal for Parasitology 39, 1263–1268.Google Scholar
Marohasy, J (Ed.) (2017) Climate Change: The Facts 2017. Victoria, Australia: Institute of Public Affairs.Google Scholar
Mollhagan, T (1978) Habitat influence on helminth parasitism of the cotton rat in western Texas, with remarks on some of the parasites. The Southwestern Naturalist 23, 401–407.Google Scholar
Montgomery, SSJ and Montgomery, WI (1988) Cyclic and non-cyclic dynamics in populations of the helminth parasites of wood mice Apodemus sylvaticus. Journal of Helminthology 62, 78–90.Google Scholar
Montgomery, SSJ and Montgomery, WI (1989) Spatial and temporal variation in the infracommunity structure of helminths of Apodemus sylvaticus (Rodentia: Muridae). Parasitology 98, 145–150.Google Scholar
Montgomery, SSJ and Montgomery, WI (1990) Structure, stability and species interactions in helminth communities of wood mice Apodemus sylvaticus. International Journal for Parasitology 20, 225–242.Google Scholar
Montoliu, I et al. (2013) On the biology of Spiruroidea parasites of murine rodents on El Hierro (Canary Islands, Spain) with molecular characterization of Streptopharagus greenbergi Wertheim, 1993. Comptes Rendus Biologies 336, 440–448.Google Scholar
Moore, SL and Wilson, K (2002) Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297, 2015–2018.Google Scholar
Morgan, ER and Wall, R (2009) Climate change and parasitic disease: farmer mitigation. Trends in Parasitology 25, 308–312.Google Scholar
Myers, BJ (1954) Helminth parasites of reptiles, birds and mammals of Egypt. I. Streptopharagus kuntzi sp. nov., from rodents with a review of the genus. Canadian Journal of Zoology 32, 366–374.Google Scholar
Myers, BJ (1961) Helminth parasites of reptiles, birds and mammals of Egypt. VI. Dentostomella kuntzi n. sp. A new oxyurid nematode from Acomys spp. Canadian Journal of Zoology 39, 55–57.Google Scholar
Ostfeld, RS, Glass, G and Keesing, F (2005) Spatial epidemiology: an emerging (or re-emerging) discipline. Trends in Ecology and Evolution 20, 328–333.Google Scholar
Pacala, SW and Dobson, AP (1988) The relation between the number of parasites/host and host age: population dynamic causes and maximum likelihood estimation. Parasitology 96, 197–210.Google Scholar
Poulin, R (1993) The disparity between observed and uniform distributions: a new look at parasite aggregation. International Journal for Parasitology 23, 937–944.Google Scholar
Poulin, R (1996) Sexual inequalities in helminth infections: a cost of being a male? The American Naturalist 147, 287–295.Google Scholar
Quentin, JC (1966) Oxyures des muridae africains. Annales de Parasitologie Humaine et Comparee 41, 443–452.Google Scholar
Quentin, JC (1969) Cycle biologique de Protospirura muricola Gedoelst 1916 (Nematoda; Spiruridae). Annales de Parasitologie (Paris) 44, 485–504.Google Scholar
Quentin, JC and Wertheim, G (1975) Helminthes d'oiseaux et de mammiferes d'Israel. V. Spirurides nouveaux ou peu connus. Annales de Parasitologie Humaine et Comparée 50, 63–85.Google Scholar
Read, CP (1951) The ‘crowding’ effect in tapeworm infections. Journal of Parasitology 37, 174–178.Google Scholar
Rohlf, FJ and Sokal, RR (1995) Statistical Tables. San Francisco: Freeman W.H. and Company.Google Scholar
Schalk, G and Forbes, MR (1997) Male biases in parasitism of mammals: effects of study type, host age and parasite taxa. Oikos 78, 67–74.Google Scholar
Schutgens, M et al. (2015) Behavioural changes in the flour beetle Tribolium confusum infected with the spirurid nematode Protospirura muricola. Journal of Helminthology 89, 68–79.Google Scholar
Semida, FM et al. (2001) Habitat heterogeneity, altitudinal gradients in relation to beetle diversity in South Sinai, Egypt. Egyptian Journal of Biology 3, 137–146.Google Scholar
Spickett, A et al. (2017) Helminth parasitism in two closely related South African rodents: abundance, prevalence, species richness and impinging factors. Parasitology Research 116, 1395–1409.Google Scholar
Tenora, F and Stanĕk, M (1995) Changes of the helminthofauna in several muridae and Arvicolidae at Lednice in Moravia. II. Ecology. Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis 43, 57–65.Google Scholar
Tenora, F, Wiger, R and Barus, V (1979) Seasonal and annual variations in the prevalence of helminths in a cyclic population of Clethrionomys glareolus. Holarctic Ecology 2, 176–181.Google Scholar
Ward, HL and Nelson, DR (1967) Acanthocephala of the genus Moniliformis from rodents of Egypt with the description of a new species from the Egyptian spiny mouse (Acomys cahirinus). Journal of Parasitology 53, 150–156.Google Scholar
Wertheim, G (1993) Cuticular markings in species differentiation of Streptopharagus (Nematoda-Spiruroideas) parasitic in rodents. Annales de Parasitologie Humaine et Comparee 68, 49–60.Google Scholar
Wertheim, G and Greenberg, Z (1970) Notes on helminth parasites of myomorph rodents from Southern Sinai. Journal of Helminthology 44, 243–252.Google Scholar
Wertheim, G, Schmidt, GD and 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 d'Histoire Naturelle, Section A Zoologie Biologie et Ecologie Animales, Paris 8(3), 543–550.Google Scholar
Xu, R (2003) Measuring explained variation in linear mixed effects models. Statistics in Medicine 22, 3527–3541.Google Scholar
Young, RE and MacColl, ADC (2017) Spatial and temporal variation in macroparasite communities of three-spined stickleback. Parasitology 144, 436–449.Google Scholar
Zalat, S and Gilbert, F (1998) A Walk in Sinai: St. Katherine to Al Galt Al Azraq (The Blue Pool). Cairo, Egypt: El Haramen Press.Google Scholar
Zalat, S et al. (2001) Spatial variation in the biodiversity of Bedouin gardens in the St. Katherine Protectorate, South Sinai, Egypt. Egyptian Journal of Biology 3, 147–155.Google Scholar
Zalat, S et al. (2008) Biological explorations of Sinai: flora and fauna of Wadi Isla and Hebran, St. Katherine Protectorate, Egypt. Egyptian Journal of Natural History 5, 6–15.Google Scholar
Zell, R (2004) Global climate change and the emergence/re-emergence of infectious diseases. International Journal of Medical Microbiology 293(Suppl. 37), 16–26.Google Scholar
Supplementary material: File

Behnke et al. supplementary material

Behnke et al. supplementary material 1

Download Behnke et al. supplementary material(File)
File 26.9 KB