Hostname: page-component-848d4c4894-p2v8j Total loading time: 0.001 Render date: 2024-06-05T10:09:03.828Z Has data issue: false hasContentIssue false

Spatial and temporal variation of compositional, functional, and phylogenetic diversity in ectoparasite infracommunities harboured by small mammals

Published online by Cambridge University Press:  15 February 2021

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
Maxim V. Vinarski
Affiliation:
Laboratory of Macroecology and Biogeography of Invertebrates, Saint-Petersburg State University, 7/9 University Emb., 199034Saint-Petersburg, Russian Federation Omsk State University, 11 Neftezavodskaya str., 644053Omsk, Russian Federation
Natalia P. Korallo-Vinarskaya
Affiliation:
Laboratory of Arthropod-Borne Viral Infections, Omsk Research Institute of Natural Foci Infections, Mira str. 7, 644080Omsk, Russian Federation Omsk State Pedagogical University, 14 Tukhachevskogo Emb., 644099 Omsk, Russian Federation
Georgy I. Shenbrot
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
Irina S. Khokhlova
Affiliation:
Wyler Department of Dryland Agriculture, French Associates Institute for Agriculture and Biotechnology of Drylands, Ben-Gurion University of the Negev, Sede Boqer Campus, 8499000Midreshet Ben-Gurion, Israel
*
Author for correspondence: Boris R. Krasnov, E-mail: krasnov@bgu.ac.il

Abstract

We studied patterns of compositional, functional, and phylogenetic α- and β-diversity in flea and gamasid mite infracommunities of small Siberian mammals, taking into account host-associated (species) and environmental (biome or sampling period) factors. We asked: (a) How do these factors and their interactions affect infracommunity diversity? (b) Does infracommunity composition, in terms of species, traits, and phylogenetic lineages, deviate from random? (c) Are species, traits, and phylogenetic lineages in infracommunities clustered or overdispersed?, and (d) Do patterns of diversity differ between the three diversity facets and/or the two ectoparasite taxa? We found that the α-diversity of infracommunities was strongly affected by host species, biome, and sampling period. The highest proportion of infracommunity diversity in both taxa was associated with the interaction between either host species and biome or host species and sampling period. Infracommunities of both taxa within, as well as between, host species, biomes, and sampling periods were characterized by the clustering of species, traits and lineages. The patterns of the effects of host species, biome, and sampling period on infracommunity diversity were congruent among the three diversity facets in both fleas and mites. We conclude that the assembly patterns in ectoparasite infracommunities mirror those characteristics of component and compound communities.

Type
Research Article
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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

Ackerly, DD and Cornwell, WK (2007) A trait-based approach to community assembly: partitioning of species trait values into within- and among-community components. Ecology Letters 10, 135145.CrossRefGoogle ScholarPubMed
Al-Azzazy, MM and Alhewairini, SS (2020) Effect of temperature and humidity on development, reproduction, and predation rate of Amblyseius swirskii (Phytoseiidae) fed on Phyllocoptruta oleivora (Eriophyidae) and Eutetranychus orientalis (Tetranychidae). International Journal of Acarology 46, 304312.CrossRefGoogle Scholar
Bordes, F, Blumstein, DT and Morand, S (2007) Rodent sociality and parasite diversity. Biology Letters 3, 692694.CrossRefGoogle ScholarPubMed
Bordes, F, Morand, S and Guerrero, R (2008) Bat fly species richness in Neotropical bats: correlations with host ecology and host brain. Oecologia 158, 109116.CrossRefGoogle ScholarPubMed
Bordes, F, Morand, S and Krasnov, BR (2011) Does investment into “expensive” tissue compromise anti-parasitic defence? Testes size, brain size and parasite diversity in rodent hosts. Oecologia 165, 716.CrossRefGoogle ScholarPubMed
Bozinovic, F, Muñoz, JLP and Cruz-Neto, AP (2007) Intraspecific variability in the basal metabolic rate: testing the food habits hypothesis. Physiological and Biochemical Zoology 80, 452460.CrossRefGoogle ScholarPubMed
Cavender-Bares, J, Kozak, KH, Fine, PVA and Kembel, SW (2009) The merging of community ecology and phylogenetic biology. Ecology Letters 12, 693715.CrossRefGoogle ScholarPubMed
Clarke, KR and Warwick, RM (1999) The taxonomic distinctness measure of biodiversity: weighting of step lengths between hierarchical levels. Marine Ecology Progress Series 184, 2129.CrossRefGoogle Scholar
Collyer, ML and Adams, DC (2018) RRPP: an r package for fitting linear models to high-dimensional data using residual randomization. Methods in Ecology and Evolution 9, 17721779.CrossRefGoogle Scholar
De Bello, F, Lavergne, S, Meynard, CN, Lepš, J and Thuiller, W (2010) The partitioning of diversity: showing Theseus a way out of the labyrinth. Journal of Vegetation Science 21, 9921000.CrossRefGoogle Scholar
Esser, HJ, Foley, JE, Bongers, F, Herre, EA, Miller, MJ, Prins, HHT and Jansen, PA (2016) Host body size and the diversity of tick assemblages on Neotropical vertebrates. International Journal for Parasitology: Parasites and Wildlife 5, 295304.Google ScholarPubMed
Gower, JC (1971) A general coefficient of similarity and some of its properties. Biometrics 27, 857871.CrossRefGoogle Scholar
Gregory, RD, Keymer, AE and Harvey, PH (1996) Helminth parasite richness among vertebrates. Biodiversity and Conservation 5, 985997.CrossRefGoogle Scholar
Hämäläinen, A, Raharivololona, B, Ravoniarimbinina, P and Kraus C, (2015) Host sex and age influence endoparasite burdens in the gray mouse lemur. Frontiers in Zoology 12, 25. doi: 10.1186/s12983-015-0118-9.CrossRefGoogle ScholarPubMed
Hoberg, EP and Brooks, DR (2015) Evolution in action: climate change, biodiversity dynamics and emerging infectious disease. Philosophical Transactions of the Royal Society of London B 370, 20130553.CrossRefGoogle ScholarPubMed
Holmes, JC and Price, PW (1986) Communities of parasites. In Kittawa, J and Anderson, DJ (eds), Community Ecology: Pattern and Process. Oxford, UK: Blackwell Scientific Publications, pp. 187213.Google Scholar
Jombart, T and Dray, S (2010) Adephylo: new tools for investigating the phylogenetic signal in biological traits. Bioinformatics (Oxford, England) 26, 19071909.CrossRefGoogle ScholarPubMed
Jost, L (2006) Entropy and diversity. Oikos 113, 363375.CrossRefGoogle Scholar
Korallo-Vinarskaya, NP, Vinarski, MV, Khokhlova, IS, Shenbrot, GI and Krasnov, BR (2015) Intraspecific variation of body size in a gamasid mite Laelaps Clethrionomydis: environment, geography and host dependence. Parasitology Research 114, 37673774.CrossRefGoogle Scholar
Korallo, NP, Vinarski, MV, Krasnov, BR, Shenbrot, GI, Mouillot, D and Poulin, R (2007) Are there general rules governing parasite diversity? Small mammalian hosts and gamasid mite assemblages. Diversity and Distributions 13, 353360.CrossRefGoogle Scholar
Kozlova, RG (1983) The effect of air moisture on development, survival and behaviour of the mite Haemogamasus nidi (Gamasoidea, Haemogamasidae). Parazitologiya 17, 293298 (in Russian).Google Scholar
Krasnov, BR (2008) Functional and Evolutionary Ecology of Fleas. A Model for Ecological Parasitology. Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
Krasnov, BR, Shenbrot, GI, Medvedev, SG, Vatschenok, VS and Khokhlova, IS (1997) Host-habitat relation as an important determinant of spatial distribution of flea assemblages (Siphonaptera) on rodents in the Negev Desert. Parasitology 114, 159173.CrossRefGoogle Scholar
Krasnov, BR, Shenbrot, GI, Khokhlova, IS and Degen, AA (2004) Flea species richness and parameters of host body, host geography and host ‘milieu’. Journal of Animal Ecology 73, 11211128.CrossRefGoogle Scholar
Krasnov, BR, Shenbrot, GI, Khokhlova, IS, Hawlena, H and Degen, A (2006a) Temporal variation in parasite infestation of a host individual: does a parasite-free host remain uninfested permanently? Parasitology Research 99, 541545.CrossRefGoogle Scholar
Krasnov, BR, Stanko, M and Morand, S (2006b) Are ectoparasite communities structured? Species co-occurrence, temporal variation and null models. Journal of Animal Ecology 75, 13301339.CrossRefGoogle Scholar
Krasnov, BR, Poulin, R and Mouillot, D (2011) Scale-dependence of phylogenetic signal in ecological traits of ectoparasites. Ecography 34, 114122.CrossRefGoogle Scholar
Krasnov, BR, Vinarski, MV, Korallo-Vinarskaya, NP and Khokhlova, IS (2013) Ecological correlates of body size in gamasid mites parasitic on small mammals: abundance and niche breadth. Ecography 36, 10421050.CrossRefGoogle Scholar
Krasnov, BR, Shenbrot, GI and Khokhlova, IS (2015a) Historical biogeography of fleas: the former Bering Land Bridge and phylogenetic dissimilarity between the Nearctic and Palearctic assemblages. Parasitology Research 114, 16771686.CrossRefGoogle Scholar
Krasnov, BR, Shenbrot, GI, Khokhlova, IS, Stanko, M, Morand, S and Mouillot, D (2015b) Assembly rules of ectoparasite communities across scales: combining patterns of abiotic factors, host composition, geographic space, phylogeny and traits. Ecography 38, 184197.CrossRefGoogle Scholar
Krasnov, BR, Shenbrot, GI, Korallo-Vinarskaya, NP, Vinarski, MV, Warburton, EM and Khokhlova, IS (2019a) The effects of environment, hosts and space on compositional, phylogenetic and functional beta-diversity in two taxa of arthropod ectoparasites. Parasitology Research 118, 21072120.CrossRefGoogle Scholar
Krasnov, BR, Shenbrot, GI, Korallo-Vinarskaya, NP, Vinarski, MV, van der Mescht, L, Warburton, EM and Khokhlova, IS (2019b) Do the pattern and strength of species associations in ectoparasite communities conform to biogeographic rules? Parasitology Research 118, 11131125.CrossRefGoogle Scholar
Llopis-Belenguer, C, Pavoine, S, Blasco-Costa, I and Balbuena, JA (2020) Assembly rules of helminth parasite communities in grey mullets: combining components of diversity. International Journal for Parasitology 50, 10891098. doi: 10.1016/j.ijpara.2020.06.006CrossRefGoogle ScholarPubMed
MacArthur, RH and Levins, R (1967) The limiting similarity, convergence, and divergence of coexisting species. American Naturalist 101, 377385.CrossRefGoogle Scholar
Martin, LB 2nd, Navara, KJ, Bailey, MT, Hutch, CR, Powell, ND, Sheridan, JF and Nelson, RJ (2008) Food restriction compromises immune memory in deer mice (Peromyscus maniculatus) by reducing spleen-derived antibody-producing B cell numbers. Physiological and Biochemical Zoology 81, 366372.CrossRefGoogle ScholarPubMed
Morand, S and Harvey, PH (2000) Mammalian metabolism, longevity and parasite species richness. Proceedings of the Royal Society of London B 267, 19992003.CrossRefGoogle ScholarPubMed
Morand, S and Poulin, R (1998) Density, body mass and parasite species richness of terrestrial mammals. Evolutionary Ecology 12, 717727.CrossRefGoogle Scholar
Morand, S, Rohde, K and Hayward, C (2002) Order in ectoparasite communities of marine fish is explained by epidemiological processes. Parasitology 124(Suppl.), S57S63.CrossRefGoogle ScholarPubMed
Mouillot, D, Simková, A, Morand, S and Poulin, R (2005) Parasite species coexistence and limiting similarity: a multiscale look at phylogenetic, functional and reproductive distances. Oecologia 146, 269278.CrossRefGoogle Scholar
Norton, J, Rollinson, D and Lewis, JW (2004) Patterns of infracommunity species richness in eels, Anguilla anguilla. Journal of Helminthology 78, 141146.CrossRefGoogle ScholarPubMed
Oksanen, J, Blanchet, G, Friendly, M, Kindt, P, Legendre, P, McGlinn, D, Minchin, PR, O'Hara, RB, Simpson, GL, Solymos, P, Stevens, MHH, Szoecs, E and Wagner, H (2019) vegan: Community Ecology Package. R package version 2.5-2. Available at https://CRAN.R-project.org/package=vegan.Google Scholar
Ostfeld, RS and Keesing, F (2000) Pulsed resources and community dynamics of consumers in terrestrial ecosystems. Trends in Ecology and Evolution 15, 232237.CrossRefGoogle ScholarPubMed
Park, Y-G and Lee, J-H (2020) Temperature-dependent development and oviposition models and life history characteristics of Amblyseius eharai (Amitai et Swirski) (Acari: Phytoseiidae) preying on Tetranychus urticae (Koch) (Acari: Tetranychidae). Journal of Asia-Pacific Entomology 23, 869878.CrossRefGoogle Scholar
Paseka, RE and Grunberg, RL (2019) Allometric and trait-based patterns in parasite stoichiometry. Oikos 128, 102112.CrossRefGoogle Scholar
Pavoine, S (2020) Adiv: an R package to analyse biodiversity in ecology. Methods in Ecology and Evolution 11, 11061112.CrossRefGoogle Scholar
Pavoine, S and Bonsall, MB (2011) Measuring biodiversity to explain community assembly: a unified approach. Biological Reviews 86, 792812.CrossRefGoogle ScholarPubMed
Pavoine, S and Dolédec, S (2005) The apportionment of quadratic entropy: a useful alternative for partitioning diversity in ecological data. Environmental and Ecological Statistics 12, 125138.CrossRefGoogle Scholar
Pavoine, S, Dufour, AB and Chessel, D (2004) From dissimilarities among species to dissimilarities among communities: a double principal coordinate analysis. Journal of Theoretical Biology 228, 523537.CrossRefGoogle ScholarPubMed
Pavoine, S, Baguette, M and Bonsall, MB (2010) Decomposition of trait diversity among the nodes of a phylogenetic tree. Ecological Monographs 80, 485507.CrossRefGoogle Scholar
Pavoine, S, Blondel, J, Dufour, AB, Gasc, A and Bonsall, MB (2013) A new technique for analysing interacting factors affecting biodiversity patterns: crossed-DPCoA. PLoS ONE 8, e54530.CrossRefGoogle ScholarPubMed
Pavoine, S, Marcon, E and Ricotta, C (2016) “Equivalent numbers” for species, phylogenetic or functional diversity in a nested hierarchy of multiple scales. Methods in Ecology and Evolution 7, 11521163.CrossRefGoogle Scholar
Poulin, R (1996) Richness, nestedness, and randomness in parasite infracommunity structure. Oecologia 105, 545551.CrossRefGoogle ScholarPubMed
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, 16231630.CrossRefGoogle ScholarPubMed
Radovsky, FJ (1985) Evolution of mammalian mesostigmatid mites. In Kim, KC (ed.), Coevolution of Parasitic Arthropods and Mammals. New York, USA: John Wiley & Sons, pp. 441504.Google Scholar
Rao, CR (1982) Diversity and dissimilarity coefficients: a unified approach. Theoretical Population Biology 21, 2443.CrossRefGoogle Scholar
R Core Team (2019) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. Available at https://www.R-project.org/.Google Scholar
Ricotta, C and Szeidl, L (2009) Diversity partitioning of Rao's quadratic entropy. Theoretical Population Biology 76, 299302.CrossRefGoogle ScholarPubMed
Rikhter, GD (ed.) (1963) Western Siberia. Moscow, USSR: Academy of Sciences of the USSR (in Russian).Google Scholar
Rocha, M, Bini, LM, Domisch, S, Tolonen, KT, Jyrkänkallio-Mikkola, J, Soininen, J, Hjort, J and Heino, J (2018) Local environment and space drive multiple facets of stream macroinvertebrate beta diversity. Journal of Biogeography 45, 27442754.CrossRefGoogle Scholar
Rosi, MI, Cona, MI, Videla, F, Puig, S and Roig, VG (2000) Architecture of Ctenomys mendocinus (Rodentia) burrows from two habitats differing in abundance and complexity of vegetation. Acta Theriologica 45, 493505.CrossRefGoogle Scholar
Salgado-Maldonado, G, Novelo-Turcotte, MT, Vazquez, G and Caspeta-Mandujano, JM (2014) The communities of helminth parasites of Heterandria bimaculata (Teleostei: Poeciliidae) from the upper Río La Antigua basin, east-central Mexico show a predictable structure. Parasitology 141, 970980.CrossRefGoogle Scholar
Sánchez, CA, Becker, DJ, Teitelbaum, CS, Barriga, P, Brown, LM, Majewska, AA, Hall, RJ and Altizer, S (2018) On the relationship between body condition and parasite infection in wildlife: a review and meta-analysis. Ecology Letters 21, 18691884.CrossRefGoogle ScholarPubMed
Shenbrot, GI, Krasnov, BR, Khokhlova, IS, Demidova, T and Fielden, LJ (2002) Habitat-dependent differences in architecture and microclimate of the Sundevall's jird (Meriones crassus) burrows in the Negev Desert, Israel. Journal of Arid Environments 51, 265279.CrossRefGoogle Scholar
Snyder-Mackler, N, Sanz, J, Kohn, JN, Brinkworth, JF, Morrow, S, Shaver, AO, Grenier, J-C, Pique-Regi, R, Johnson, ZP, Wilson, MT, Barreiro, LB and Tung, J (2016) Social status alters immune regulation and response to infection in macaques. Science (New York, N.Y.) 354, 10411045.CrossRefGoogle ScholarPubMed
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, 12111220.CrossRefGoogle ScholarPubMed
Surkova, EN, Korallo-Vinarskaya, NP, Vinarski, MV, Stanko, M, Warburton, EM, van der Mescht, L, Khokhlova, IS and Krasnov, BR (2018a) Sexual size dimorphism and sex ratio in arthropod ectoparasites: contrasting patterns at different hierarchical scales. International Journal for Parasitology 48, 969978.CrossRefGoogle Scholar
Surkova, EN, Korallo-Vinarskaya, NP, Vinarski, MV, van der Mescht, L, Warburton, EM, Khokhlova, IS and Krasnov, BR (2018b) Body size distribution in flea communities harboured by Siberian small mammals as affected by host species, host sex and scale: scale matters the most. Evolutionary Ecology 32, 643662.CrossRefGoogle Scholar
Thioulouse, J, Dray, S, Dufour, A-B, Siberchicot, A, Jombart, T and Pavoine, S (2018) Multivariate Analysis of Ecological Data with Ade4. New York, USA: Springer.CrossRefGoogle Scholar
Timi, JT and Lanfranchi, AL (2008) The importance of the compound community on the parasite infracommunity structure in a small benthic fish. Parasitology Research 104, 295302.CrossRefGoogle Scholar
van der Mescht, L, Warburton, EM, Khokhlova, IS, Stanko, M, Vinarski, MV, Korallo-Vinarskaya, NP and Krasnov, BR (2018) Biogeography of parasite abundance: latitudinal gradient and distance decay of similarity in the abundance of fleas and mites parasitic on small mammals in the Palearctic at three spatial scales. International Journal for Parasitology 48, 857866.CrossRefGoogle ScholarPubMed
Vinarski, MV and Korallo-Vinarskaya, NP (2016) An annotated catalogue of the gamasid mites associated with small mammals in Asiatic Russia. The family Laelapidae s. str. (Acari: Mesostigmata: Gamasina). Zootaxa 4111, 223245.CrossRefGoogle Scholar
Vinarski, MV, Korallo-Vinarskaya, NP, Shenbrot, GI, Warburton, EM, Surkova, EN, Khokhlova, IS and Krasnov, BR (2020) Species associations and trait dissimilarity in communities of ectoparasitic arthropods harboured by small mammals at three hierarchical scales. Ecological Entomology 45, 321332.CrossRefGoogle Scholar
Warburton, EM, van der Mescht, L, Stanko, M, Vinarski, MV, Korallo-Vinarskaya, NP, Khokhlova, IS and Krasnov, BR (2017) Beta-diversity of ectoparasites at two spatial scales: nested hierarchy, geography and habitat type. Oecologia 184, 507520.CrossRefGoogle ScholarPubMed
Webb, CO, Ackerly, DD, McPeek, MA and Donoghue, MJ (2002) Phylogenies and community ecology. Annual Review of Ecology and Systematics 33, 475505.CrossRefGoogle Scholar
Wilson, MW and Shmida, A (1984) Measuring beta diversity with presence–absence data. Journal of Ecology 72, 10551064.CrossRefGoogle Scholar
Zelmer, DA, Paredes-Calderón, L, León-Règagnon, V and García-Prieto, L (2004) Nestedness in colonization-dominated systems: helminth infracommunities of Rana vaillanti Brocchi (Anura: Ranidae) in Los Tuxtlas, Veracruz, Mexico. Journal of Parasitology 90. 705710.CrossRefGoogle ScholarPubMed
Zemskaya, AA (1969) Types of parasitism of gamasid mites. Medical Parasitology and Parasitic Diseases [Meditsinskaya Parazitologiya i Parazitarnye Bolezni] 38, 393405 (in Russian).Google Scholar
Zhu, Q, Hastriter, MW, Whiting, MF and Dittmar, K (2015) Fleas (Siphonaptera) are cretaceous, and evolved with Theria. Molecular Phylogenetic and Evolution 90, 129139.CrossRefGoogle ScholarPubMed
Supplementary material: File

Krasnov et al. supplementary material

Krasnov et al. supplementary material

Download Krasnov et al. supplementary material(File)
File 195.6 KB