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Compositional turnover in ecto- and endoparasite assemblages of an African bat, Miniopterus natalensis (Chiroptera, Miniopteridae): effects of hierarchical scale and host sex

Published online by Cambridge University Press:  01 September 2020

Boris R. Krasnov Open the ORCID record for Boris R. Krasnov [Opens in a new window] ,
Kerstin Junker Open the ORCID record for Kerstin Junker [Opens in a new window] ,
Simon Wood ,
Edward A. Ueckermann ,
Gert J. Venter ,
Luther van der Mescht ,
Heloise Heyne  and
David S. Jacobs Open the ORCID record for David S. Jacobs [Opens in a new window]
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, 8499000Midreshet Ben-Gurion, Israel
Kerstin Junker
Affiliation:
Epidemiology, Parasites and Vectors Programme, Agricultural Research Council-Onderstepoort Veterinary Institute, Private Bag X05, Onderstepoort0110, South Africa
Simon Wood
Affiliation:
Burian Drive 2551, Coquitlam V3K 5W8, British Columbia, Canada
Edward A. Ueckermann
Affiliation:
Unit for Environmental Sciences and Management, Potchefstroom Campus, North-West University, Private Bag X6001, Potchefstroom2520, South Africa
Gert J. Venter
Affiliation:
Epidemiology, Parasites and Vectors Programme, Agricultural Research Council-Onderstepoort Veterinary Institute, Private Bag X05, Onderstepoort0110, South Africa
Luther van der Mescht
Affiliation:
Department of Conservation and Entomology, Stellenbosch University, Private Bag X1, Matieland7602, South Africa
Heloise Heyne
Affiliation:
Epidemiology, Parasites and Vectors Programme, Agricultural Research Council-Onderstepoort Veterinary Institute, Private Bag X05, Onderstepoort0110, South Africa
David S. Jacobs
Affiliation:
Department of Biological Sciences, University of Cape Town, Private Bag X3, Rondebosch7701, South Africa
*
Author for correspondence: Boris R. Krasnov, E-mail: [email protected]
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Abstract

We studied the compositional turnover in infracommunities and component communities of ecto- and endoparasites infesting a bat, Miniopterus natalensis (Chiroptera, Miniopteridae), across seven sampling sites using the zeta diversity metric (measuring similarity between multiple communities) and calculating zeta decline and retention rate (both scales) and zeta decay (component communities). We asked whether the patterns of zeta diversity differ between (a) infracommunities and component communities; (b) ecto- and endoparasites and (c) subsets of communities infecting male and female bats. The pattern of compositional turnover differed between infracommunities and component communities in endoparasites only. The shape of zeta decline for infracommunities indicated that there were approximately equal probabilities of ecto- and endoparasitic species to occur on/in any bat individual within a site. The shape of zeta decline for component communities suggested the stochasticity of ectoparasite turnover, whereas the turnover of endoparasites was driven by niche-based processes. Compositional turnover in component communities of ectoparasites was more spatially dependent than that of endoparasites. Spatial independence of compositional turnover in endoparasites was due to subcommunities harboured by female bats. We conclude that the patterns of compositional turnover in infracommunities were similar in ecto- and endoparasites, whereas the patterns of turnover in component communities differed between these groups.

Keywords

EctoparasitesendoparasitesMiniopterus natalensiszeta decayzeta diversity
Type
Research Article
Information
Parasitology , Volume 147 , Issue 14 , December 2020 , pp. 1728 - 1742
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Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Anderson, RC (2000) Nematode Parasites of Vertebrates. Their Development and Transmission, 2nd Edn. Wallingford, UK: CABI.CrossRefGoogle Scholar
Anthony, ELP (1988) Age determination in bats. In Kunz, TH (ed.), Ecological and Behavioral Methods for the Study of Bats. Washington, DC, USA: Smithsonian Institution Press, pp. 47–58.Google Scholar
Bahram, M, Koljalg, U, Courty, P-E, Diedhiou, AG, Kjøller, R, Polme, S, Ryberg, M, Veldre, V and Tedersoo, L (2013) The distance decay of similarity in communities of ectomycorrhizal fungi in different ecosystems and scales. Journal of Ecology 101, 1335–1344.CrossRefGoogle Scholar
Baruš, V (1973) The finding of nematodes and acanthocephalans in Egyptian bats. Folia Parasitologica 20, 213–222.Google Scholar
Blankespoor, HD and Ulmer, MJ (1970) Helminths from six species of Iowa bats. Proceedings of the Iowa Academy of Science 77, 200–206.Google Scholar
Carola, G-R and Baselga, A (2018) Variation among European beetle taxa in patterns of distance decay of similarity suggests a major role of dispersal processes. Ecography 41, 1825–1834.Google Scholar
Christe, P, Arlettaz, R and Vogel, P (2000) Variation in intensity of a parasitic mite (Spinturnix Myoti) in relation to the reproductive cycle and immunocompetence of its bat host (Myotis myotis). Ecology Letters 3, 207–212.CrossRefGoogle Scholar
Christe, P, Giorgi, MS, Vogel, P and Arlettaz, R (2003) Differential species specific ectoparasitic mite intensities in two intimately coexisting sibling bat species: resource mediated host attractiveness or parasite specialization? Journal of Animal Ecology 72, 866–872.CrossRefGoogle Scholar
Christe, P, Glaizot, O, Evanno, G, Bruyndonckx, N, Devevey, G, Yannic, G, Patthey, P, Maeder, A, Vogel, P and Arlettaz, R (2007) Host sex and ectoparasites choice: preference for, and higher survival on female hosts. Journal of Animal Ecology 766, 703–710.CrossRefGoogle Scholar
Clark, NJ, Clegg, SM, Sam, K, Goulding, W, Koane, B and Wells, K (2018) Climate, host phylogeny and the connectivity of host communities govern regional parasite assembly. Diversity and Distributions 24, 13–23.CrossRefGoogle Scholar
Cottenie, K (2005) Integrating environmental and spatial processes in ecological community dynamics. Ecology Letters 8, 1175–1182.CrossRefGoogle ScholarPubMed
Dallas, TA, Laine, A-L and Ovaskainen, O (2019) Detecting parasite associations within multi-species host and parasite communities. Proceedings of the Royal Society of London B 286, 20191109.Google ScholarPubMed
Dick, CW and Gettinger, D (2005) A faunal survey of streblid flies (Diptera: Streblidae) associated with bats in Paraguay. Journal of Parasitology 91, 1015–1024.CrossRefGoogle ScholarPubMed
Dick, CW and Patterson, BD (2006) Bat flies. In Morand, S, Krasnov, BR and Poulin, R (eds), Micromammals and Macroparasites: From Evolutionary Ecology to Management. Tokyo, Japan: Springer-Verlag, pp. 179–194.CrossRefGoogle Scholar
Dowling, APG (2006) Mesostigmatid mites. In Morand, S, Krasnov, BR and Poulin, R (eds), Micromammals and Macroparasites: From Evolutionary Ecology to Management. Tokyo, Japan: Springer-Verlag, pp. 103–117.CrossRefGoogle Scholar
Dubois, G (1956) Contribution à l’étude des trématodes de chiroptères. Revue Suisse de Zoology 63, 683–695.CrossRefGoogle Scholar
Durden, LA (2006) Argasid and ixodid ticks. In Morand, S, Krasnov, BR and Poulin, R (eds), Micromammals and Macroparasites: From Evolutionary Ecology to Management. Tokyo, Japan: Springer-Verlag, pp. 91–102.CrossRefGoogle Scholar
Dybing, NA, Fleming, PA and Adams, J (2013) Environmental conditions predict helminth prevalence in red foxes in Western Australia. International Journal for Parasitology: Parasites and Wildlife 2, 165–172.Google ScholarPubMed
Esteban, JG, Amengual, B and Cobo, JS (2001) Composition and structure of helminth communities in two populations of Pipistrellus Pipistrellus (Chiroptera: Vespertilionidae) from Spain. Folia Parasitologica 48, 143–148.CrossRefGoogle ScholarPubMed
Georgiev, BB, Bray, RA, Timothy, D and Littlewood, J (2006) Cestodes of small mammals: taxonomy and life cycles. In Morand, S, Krasnov, BR and Poulin, R (eds), Micromammals and Macroparasites: From Evolutionary Ecology to Management. Tokyo, Japan: Springer-Verlag, pp. 29–62.CrossRefGoogle Scholar
Gómez, A and Nichols, E (2013) Neglected wild life: parasitic biodiversity as a conservation target. International Journal for Parasitology: Parasites and Wildlife 2, 222–227.Google ScholarPubMed
Gotelli, NJ and Rohde, K (2002) Co-occurrence of ectoparasites of marine fishes: a null model analysis. Ecology Letters 5, 86–94.CrossRefGoogle Scholar
Guerrero, R, Bain, O, Attout, T and Martin, C (2006) The infective larva of Litomosoides yutajensis Guerrero et al., 2003 (Nematoda: Onchocercidae), a Wolbachia-free filaria from bats. Parasite 13, 127–130.CrossRefGoogle Scholar
Holmes, JC and Price, PW (1986) Communities of parasites. In Kittawa, J and Anderson, DJ (eds), Community Ecology: Pattern and Process. Oxford, UK: Blackwell Publishing, pp. 187–213.Google Scholar
Hubbell, SP (2001) The Unified Neutral Theory of Biodiversity and Biogeography. Princeton, NJ: Princeton University Press.Google Scholar
Hui, C and McGeoch, MA (2014) Zeta diversity as a concept and metric that unifies incidence-based biodiversity patterns. American Naturalist 184, 684–694.CrossRefGoogle ScholarPubMed
Hulbert, IAR and Boag, B (2001) The potential role of habitat on intestinal helminths of mountain hares, Lepus timidus. Journal of Helminthology 75, 345–349.CrossRefGoogle ScholarPubMed
Jacobs, DS (1999) Intraspecific variation in wingspan and echolocation call flexibility might explain the use of different habitats by the insectivorous bat, Miniopterus Schreibersii (Vespertilionidae: Miniopterinae). Acta Chiropterologica 1, 93–103.Google Scholar
Jameson, DK (1959) A survey of the parasites of five species of bats. Southwestern Naturalist 4, 61–65.CrossRefGoogle Scholar
Jobling, B (1936) A revision of the subfamilies of the Streblidae and the genera of the subfamily Streblinae (Diptera Acalypterae) including a redescription of Metelasmus Pseudopterus Coquillett and a description of two new species from Africa. Parasitology 28, 355–380.CrossRefGoogle Scholar
Junker, K, Bain, O and Boomker, J (2008) Helminth parasites of natal long-fingered bats, Miniopterus natalensis (Chiroptera: Miniopteridae), in South Africa. Onderstepoort Journal of Veterinary Research 75, 261–265.CrossRefGoogle Scholar
Junker, K, Barbuto, M, Casiraghi, M, Martin, C, Uni, S, Boomker, J and Bain, O (2009) Litomosa chiropterorum Ortlepp, 1932 (Nematoda: Filarioidea) from a South African miniopterid: redescription, Wolbachia screening and phylogenetic relationships with Litomosoides. Parasite 16, 43–50.CrossRefGoogle ScholarPubMed
Krasnov, BR, Shenbrot, GI, Mouillot, D, Khokhlova, IS and Poulin, R (2005) Spatial variation in species diversity and composition of flea assemblages in small mammalian hosts: geographical distance or faunal similarity? Journal of Biogeography 32, 633–644.CrossRefGoogle Scholar
Krasnov, BR, Matthee, S, Lareschi, M, Korallo-Vinarskaya, NP and Vinarski, MV (2010) Co-occurrence of ectoparasites on rodent hosts: null model analyses of data from three continents. Oikos 116, 120–128.CrossRefGoogle Scholar
Krasnov, BR, Stanko, M, Matthee, S, Laudisoit, A, Leirs, H, Khokhlova, IS, Korallo-Vinarskaya, NP, Vinarski, MV and Morand, S (2011) Male hosts drive infracommunity structure of ectoparasites. Oecologia 166, 1099–1110.CrossRefGoogle ScholarPubMed
Krasnov, BR, Bordes, F, Khokhlova, IS and Morand, S (2012) Gender-biased parasitism in small mammals: patterns, mechanisms, consequences. Mammalia 76, 1–13.CrossRefGoogle Scholar
Krasnov, BR, Shenbrot, GI, Khokhlova, IS, Stanko, M, Morand, S and Mouillot, D (2015) Assembly rules of ectoparasite communities across scales: combining patterns of abiotic factors, host composition, geographic space, phylogeny and traits. Ecography 38, 184–197.CrossRefGoogle Scholar
Krasnov, BR, Vinarski, MV, Korallo-Vinarskaya, NP and Khokhlova, IS (2020) Patterns of zeta diversity in ectoparasite communities harboured by small mammals at three hierarchical scales: taxon-invariance and scale-dependence. Oecologia 192, 1057–1071.CrossRefGoogle ScholarPubMed
Kudlai, O, Stunžėnas, V and Tkach, V (2015) The taxonomic identity and phylogenetic relationshops of Cercaria pugnax and C. helvetica XII (Digenea: Lecithodendriidae) based on morphological and molecular data. Folia Parasitologica 62, 003.CrossRefGoogle Scholar
Lafferty, KD, Dobson, AP and Kuris, AM (2006) Parasites dominate food web links. Proceedings of the National Academy of Sciences of the USA 103, 11211–11216.CrossRefGoogle ScholarPubMed
Latombe, G, Hui, C and McGeoch, MA (2017) Multi-site generalised dissimilarity modelling: using zeta diversity to differentiate drivers of turnover in rare and widespread species. Methods in Ecology and Evolution 8, 431–442.CrossRefGoogle Scholar
Latombe, G, McGeoch, MA, Nipperess, D and Hui, C (2018a) Zetadiv: Functions to Compute Compositional Turnover Using Zeta Diversity. R package version 1.1.1. Available at https://CRAN.R-project.org/package=zetadiv.Google Scholar
Latombe, G, Richardson, DM, Pyšek, P, Kučera, T and Hui, C (2018b) Drivers of species turnover vary with species commonness for native and alien plants with different residence times. Ecology 99, 2763–2775.CrossRefGoogle Scholar
Leach, MC, Bowell, VA, Allan, TF and Morton, DB (2004) Measurement of aversion to determine humane methods of anaesthesia and euthanasia. Animal Welfare 13, 77–86.Google Scholar
Lehane, MJ (2005) The Biology of Blood-Sucking in Insects, 2nd Edn. New York, USA: Cambridge University Press.CrossRefGoogle Scholar
Maa, TC (1965) Ascodipterinae of Africa (Diptera: Streblidae). Journal of Medical Entomology 4, 311–326.CrossRefGoogle Scholar
Matějusová, I, Morand, S and Gelnar, M (2000) Nestedness in assemblages of gyrodactylids (Monogenea: Gyrodactylidea) parasitising two species of cyprinid – with reference to generalists and specialists. International Journal for Parasitology 30, 1153–1158.CrossRefGoogle ScholarPubMed
McGeoch, MA, Latombe, G, Andrew, NR, Nakagawa, S, Nipperess, DA, Roigé, M, Marzinelli, EM, Campbell, AH, Vergés, A, Thomas, T, Steinberg, PD, Selwood, KE, Henriksen, ME and Hui, C (2019) Measuring continuous compositional change using decline and decay in zeta diversity. Ecology 100, e02832.CrossRefGoogle ScholarPubMed
McLean, JA and Speakman, JR (1997) Non-nutritional maternal support in the brown long-eared bat. Animal Behaviour 54, 1193–1204.CrossRefGoogle ScholarPubMed
Mellado, A and Zamora, R (2017) Parasites structuring ecological communities: the mistletoe footprint in Mediterranean pine forests. Functional Ecology 31, 2167–2176.CrossRefGoogle Scholar
Miller-Butterworth, CM, Jacobs, DS and Harley, EH (2003) Strong population structure is correlated with morphology and ecology in a migratory bat. Nature 424, 187–191.CrossRefGoogle Scholar
Morand, S, Rohde, K and Hayward, C (2002) Order in ectoparasite communities of marine fish is explained by epidemiological processes. Parasitology 124, S57–S63.CrossRefGoogle ScholarPubMed
Moravec, F, Prokopič, J and Shlikas, AV (1987) The biology of nematodes of the family Capillariidae Neveu-Lemaire, 1936. Folia Parasitologica 34, 39–56.Google ScholarPubMed
Nekola, JC and White, PS (1999) The distance decay of similarity in biogeography and ecology. Journal of Biogeography 26, 867–878.CrossRefGoogle Scholar
Ortlepp, RJ (1932) Some helminths from South African Chiroptera. 18th Report of the Director of Veterinary Services and Animal Industry, Union of South Africa, 183–196.Google Scholar
Perdiguero-Alonso, D, Montero, FE, Raga, JA and Kostadinova, A (2008) Composition and structure of the parasite faunas of cod, Gadus Morhua L. (Teleostei: Gadidae), in the North East Atlantic. Parasites & Vectors 1, 23.CrossRefGoogle Scholar
Poulin, R (2007) Evolutionary Ecology of Parasites: From Individuals to Communities, 2nd Edn. Princeton, USA: Princeton University Press.CrossRefGoogle Scholar
Poulin, R and Luque, JL (2003) A general test of the interactive-isolationist continuum in gastrointestinal parasite communities of fish. International Journal for Parasitology 33, 1623–1630.CrossRefGoogle ScholarPubMed
Poulin, R and Morand, S (2004) Parasite Biodiversity. Washington, DC, USA: Smithsonian Institution Scholarly Press.Google Scholar
Poulin, R, Krasnov, BR and Mouillot, D (2011) Host specificity in phylogenetic and geographic space. Trends in Parasitology 27, 355–361.CrossRefGoogle ScholarPubMed
Quiroz-Martínez, B and Salgado-Maldonado, G (2013) Patterns of distribution of the helminth parasites of freshwater fishes of Mexico. PLoS One 8, e54787.CrossRefGoogle Scholar
Racey, PA (1969) Diagnosis of pregnancy and experimental extension of gestation in the pipistrelle bat, Pipistrellus pipistrellus. Journal of Reproduction and Fertility 19, 465–474.CrossRefGoogle ScholarPubMed
Radovsky, FJ (1994) The evolution of parasitism and the distribution of some dermanyssoid mites (Mesostigmata) on vertebrate hosts. In Houck, MA (ed.), Mites: Ecological & Evolutionary Analyses of Life-History Patterns. Dordrecht, The Netherlands: Springer Science + Business Media, pp. 186–217.CrossRefGoogle Scholar
R Core Team (2019) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. Available at http://www.R-project.org/.Google Scholar
Sándor, AD, Corduneanu, A, Péter, A, Mihalca, AD, Barti, L, Csősz, I, Szőke, K and Hornok, S (2019) Bats and ticks: host selection and seasonality of bat-specialist ticks in Eastern Europe. Parasites & Vectors 12, 605.CrossRefGoogle ScholarPubMed
Saoud, MFA and Ramadan, MM (1976) Studies on the helminth parasites of bats in Egypt and the factors influencing their occurence with particular reference to digenetic Trematodes. Zeitschrift für Parasitenkunde 51, 37–47.CrossRefGoogle Scholar
Schoeman, MC and Jacobs, DS (2011) The relative influence of competition and prey defences on the trophic structure of animalivorous bat ensembles. Oecologia 166, 493–506.CrossRefGoogle ScholarPubMed
Skinner, JD and Chimimba, CT (2005) The Mammals of the Southern African Subregion, 3rd Edn. Cape Town, South Africa: Cambridge University Press.CrossRefGoogle Scholar
Spickett, A, Junker, K, Krasnov, BR, Haukisalmi, V and Matthee, S (2017) Intra- and interspecific similarity in species composition of helminth communities in two closely-related rodents from South Africa. Parasitology 144, 1211–1220.CrossRefGoogle ScholarPubMed
Stoffberg, S, Jacobs, DS and Miller-Butterworth, CM (2004) Field identification of two morphologically similar bats, Miniopterus Schreibersii natalensis and Miniopterus Fraterculus (Chiroptera: Vespertilionidae). African Zoology 39, 47–53.CrossRefGoogle Scholar
Sukhdeo, MVK (2012) Where are the parasites in food webs? Parasites & Vectors 5, 239.CrossRefGoogle ScholarPubMed
van der Merwe, M (1973) Aspects of social behaviour of the Natal clinging bat Miniopterus Schreibersi natalensis (A. Smith, 1834). Mammalia 37, 379–389.CrossRefGoogle Scholar
van der Merwe, M (1975) Preliminary study on the annual movements of the Natal clinging bat. South African Journal of Science 71, 237–241.Google Scholar
van der Mescht, L, Krasnov, BR, Matthee, CA and Matthee, S (2016) Community structure of fleas within and among populations of three closely related rodent hosts: nestedness and beta-diversity. Parasitology 143, 1268–1278.CrossRefGoogle ScholarPubMed
Warburton, EM, Kohler, SL and Vonhof, MJ (2016) Patterns of parasite community dissimilarity: the significant role of land use and lack of distance decay in a bat–helminth system. Oikos 125, 374–385.CrossRefGoogle Scholar
Wilkinson, GS and South, JM (2002) Life history, ecology and longevity in bats. Aging Cell 1, 124–131.CrossRefGoogle ScholarPubMed
Wood, CL, Byers, JE, Cottingham, KL, Altman, I, Donahue, MJ and Blakeslee, AMH (2007) Parasites alter community structure. Proceedings of the National Academy of Sciences of the USA 104, 9335–9339.CrossRefGoogle ScholarPubMed
Zumpt, F (1950) Ectoparasites of bats from the Sterkfontein caves (Transvaal). Journal of the Entomological Society of South Africa 13, 87–98.Google Scholar
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