Hostname: page-component-848d4c4894-x5gtn Total loading time: 0 Render date: 2024-05-05T23:32:37.864Z Has data issue: false hasContentIssue false

Host phylogeny and ecology, but not host physiology, are the main drivers of (dis)similarity between the host spectra of fleas: application of a novel ordination approach to regional assemblages from four continents

Published online by Cambridge University Press:  20 September 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, 8499000 Midreshet Ben-Gurion, Israel
Luther van der Mescht
Affiliation:
Department of Conservation Ecology and Entomology, Stellenbosch University, Private Bag X1, Matieland 7602, South Africa
Sonja Matthee
Affiliation:
Department of Conservation Ecology and Entomology, Stellenbosch University, Private Bag X1, Matieland 7602, South Africa
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, 8499000 Midreshet Ben-Gurion, Israel
*
Author for correspondence: Boris R. Krasnov, E-mail: krasnov@bgu.ac.il

Abstract

We investigated the patterns of phylogenetic and functional (dis)similarity in the species composition of host spectra between co-habitating generalist flea species in regional assemblages from four continents (Europe, Asia, North America and Africa) using a recently developed ordination approach (Double Similarity Principal Component Analysis). From the functional perspective, we considered physiological [body mass and basal metabolic rate (BMR)] and ecological (shelter depth and complexity) host traits. We asked (a) whether host phylogeny, physiology or ecology is the main driver of (dis)similarities between flea host spectra and (b) whether the patterns of phylogenetic and functional (dis)similarity in host spectra vary between flea assemblages from different continents. Phylogenetic similarity between the host spectra was highest in Africa, lowest in North America and moderate in Europe and Asia. In each assemblage, phylogenetic clusters of hosts dominating in the host spectra could be distinguished. The functional similarity between the host spectra of co-occurring fleas was low for shelter structure in all assemblages and much higher for body mass and BMR in three of the four assemblages (except North America). We conclude that host phylogeny and shelter structure are the main drivers of (dis)similarity between the host spectra of co-habitating fleas. However, the effects of these factors on the patterns of (dis)similarity varied across continents.

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.)

Footnotes

*

Present affiliation and address: Clinvet International, Uitzich Road, Bainsvlei, 9338 Bloemfontein, Free State, South Africa.

References

Araujo, SBL, Braga, MP, Brooks, DR, Agosta, SJ, Hoberg, EP, von Hartenthal, FW and Boeger, WA (2015) Understanding host-switching by ecological fitting. PLoS ONE 10, e0139225.CrossRefGoogle ScholarPubMed
Barendregt, RW and Irving, E (1998) Changes in the extent of North American ice sheets during the late Cenozoic. Canadian Journal of Earth Sciences 35, 504509.CrossRefGoogle Scholar
Bordes, F, Blumstein, DT and Morand, S (2007) Rodent sociality and parasite diversity. Biology Letters 3, 692694.CrossRefGoogle ScholarPubMed
Brickner-Braun, I, Zucker-Milwerger, D, Braun, A, Turner, JS, Pinshow, B and Berliner, P (2014) Ventilation of multi-entranced rodent burrows by boundary layer eddies. Journal of Experimental Biology 217, 41414148.10.1242/jeb.114231CrossRefGoogle ScholarPubMed
Capellini, I, Venditti, C and Barton, RA (2010) Phylogeny and metabolic scaling in mammals. Ecology 91, 27832793.CrossRefGoogle ScholarPubMed
Combes, C (2001) Parasitism. The Ecology and Evolution of Intimate Interactions. Chicago: University of Chicago Press.Google Scholar
Darskaya, NF, Bragina, ZS and Petrov, VG (1970) On fleas of the common vole and shrews in dependence on sharp density fluctuations of these mammals. In Tiflov, VE (ed.), Vectors of Particularly Dangerous Diseases and Their Control. Stavropol, USSR: Scientific Anti-Plague Institute of Caucasus Trans-Caucasus, pp. 132152 (in Russian).Google Scholar
de Meilon, B, Davis, DHS and Hardy, F (1961) Plague in Southern Africa. Vol. I. The Siphonaptera (Excluding Ischnopsyllidae). Pretoria, South Africa: Government Printer.Google Scholar
Downs, CJ, Pinshow, B, Khokhlova, IS and Krasnov, BR (2015) Flea fitness is reduced by high fractional concentrations of CO2 that simulate levels found in their hosts’ burrows. Journal of Experimental Biology 218, 35963603.CrossRefGoogle ScholarPubMed
Ganem, G, Dufour, CMS, Avenant, NL, Caminade, P, Eiseb, SJ, Tougard, C and Pillay, N (2020) An update on the distribution and diversification of Rhabdomys sp. (Muridae, Rodentia). Journal of Vertebrate Biology 69, 20013.CrossRefGoogle Scholar
García-Navas, V (2019) Phylogenetic and functional diversity of African muroid rodents at different spatial scales. Organisms Diversity & Evolution 19, 637650.CrossRefGoogle Scholar
Genoud, M, Isler, K and Martin, RD (2018) Comparative analyses of basal rate of metabolism in mammals: data selection does matter. Biological Reviews 93, 404438.CrossRefGoogle ScholarPubMed
Goldberg, AR, Conway, CJ and Biggins, DE (2020) Flea sharing among sympatric rodent hosts: implications for potential plague effects on a threatened sciurid. Ecosphere (Washington, DC) 11, e03033.Google Scholar
Gupta, P, Vishnudas, CK, Robin, VV and Dharmarajan, G (2020) Host phylogeny matters: examining sources of variation in infection risk by blood parasites across a tropical montane bird community in India. Parasites & Vectors 13, 536.CrossRefGoogle ScholarPubMed
Hadfield, JD, Krasnov, BR, Poulin, R and Nakagawa, S (2014) Tale of two phylogenies: comparative analyses of ecological interactions. The American Naturalist 183, 174187.CrossRefGoogle ScholarPubMed
Hafner, MS and Nadler, SA (1988) Phylogenetic trees support the coevolution of parasites and their hosts. Nature 332, 258259.CrossRefGoogle ScholarPubMed
Jones, KE, Bielby, J, Cardillo, M, Fritz, SA, O'Dell, J, Orme, CDL, Safi, K, Sechrest, W, Boakes, EH, Carbone, C, Connolly, C, Cutts, MJ, Foster, JK, Grenyer, R, Habib, M, Plaster, CA, Price, SA, Rigby, EA, Rist, J, Teacher, A, Bininda-Emonds, ORP, Gittleman, JL, Mace, GM and Purvis, A (2009) PanTHERIA: a species-level database of life history, ecology, and geography of extant and recently extinct mammals. Ecology 90, 2648.CrossRefGoogle Scholar
Kalabukhov, NI (1969) Periodical (Seasonal and Annual) Changes in Organism of Rodents. Moscow, USSR: Nauka (in Russian).Google Scholar
Kiffner, C, Stanko, M, Morand, S, Khokhlova, IS, Shenbrot, GI, Laudisoit, A, Leirs, H, Hawlena, H and Krasnov, BR (2013) Sex-biased parasitism is not universal: evidence from rodent–flea associations from three biomes. Oecologia 173, 10091022.CrossRefGoogle Scholar
Krasnov, BR (2008) Functional and Evolutionary Ecology of Fleas. A Model for Ecological Parasitology. Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
Krasnov, BR, Khokhlova, IS, Fielden, LJ and Burdelova, NV (2001) The effect of air temperature and humidity on the survival of pre-imaginal stages of two flea species (Siphonaptera: Pulicidae). Journal of Medical Entomology 38, 629637.CrossRefGoogle ScholarPubMed
Krasnov, BR, Khokhlova, IS, Fielden, LJ and Burdelova, NV (2002) Time to survival under starvation in two flea species (Siphonaptera: Pulicidae) at different air temperatures and relative humidities. Journal of Vector Ecology 27, 7081.Google ScholarPubMed
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, Mouillot, D, Khokhlova, IS and Poulin, R (2005 a) Spatial variation in species diversity and composition of flea assemblages in small mammalian hosts: geographic distance or faunal similarity? Journal of Biogeography 32, 633644.CrossRefGoogle Scholar
Krasnov, BR, Mouillot, D, Shenbrot, GI, Khokhlova, IS and Poulin, R (2005 b) Abundance patterns and coexistence processes in communities of fleas parasitic on small mammals. Ecography 28, 453464.CrossRefGoogle Scholar
Krasnov, BR, Morand, S, Mouillot, D, Shenbrot, GI, Khokhlova, IS and Poulin, R (2006) Resource predictability and host specificity in fleas: the effect of host body mass. Parasitology 133, 8188.CrossRefGoogle ScholarPubMed
Krasnov, BR, Pilosof, S, Shenbrot, GI, Khokhlova, IS and Degen, AA (2014) Phylogenetic structure of host spectra in Palaearctic fleas: stability versus spatial variation in widespread, generalist species. Parasitology 141, 181191.CrossRefGoogle ScholarPubMed
Krasnov, BR, Shenbrot, GI, Khokhlova, IS and Degen, AA (2016) Trait-based and phylogenetic associations between parasites and their hosts: a case study with small mammals and fleas in the Palearctic. Oikos 125, 2938.CrossRefGoogle Scholar
Krasnov, BR, Shenbrot, GI, van der Mescht, L, Warburton, EM and Khokhlova, IS (2019) Phylogenetic and compositional diversity are governed by different rules: a study of fleas parasitic on small mammals in four biogeographic realms. Ecography 42, 10001011.CrossRefGoogle Scholar
Labunets, NF (1967) Zoogeographic characteristics of fleas of Western Khangai. Proceedings of Irkutsk State Scientific Anti-Plague Institute of Siberia and Far East 27, 231240, (in Russian).Google Scholar
Linsdale, JM and Davis, BS (1956) Taxonomic appraisal and occurrence of fleas at the Hastings Reservation in Central California. University of California Publications in Zoology 54, 293370.Google Scholar
Maddison, WP and Maddison, DR (2018) Mesquite: a modular system for evolutionary analysis, Version 3.51. Available at http://mesquiteproject.org.Google Scholar
Medvedev, SG (2005) An attempted system analysis of the evolution of the order of fleas (Siphonaptera). Lectures in Memoriam N. A. Kholodkovsky, No. 57. Saint Petersburg, Russia: Russian Entomological Society and Zoological Institute of Russian Academy of Sciences (in Russian).Google Scholar
Medvedev, SG (2014) The Palaearctic centers of taxonomic diversity of fleas (Siphonaptera). Entomological Review 94, 345358.CrossRefGoogle Scholar
Mittermeier, RA and Wilson, DE (eds) (2018). Handbook of the Mammals of the World. Volume 8. Insectivores, Sloths and Colugos. Barcelona, Spain: Lynx Edicions.Google Scholar
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
Nikitina, NA and Nikolaeva, G (1979) Study of the ability of some rodents to get rid of fleas. Zoologicheskyi Zhurnal 58, 931933, (in Russian).Google Scholar
Pärtel, M, Szava-Kovats, R and Zobel, M (2011) Dark diversity: shedding light on absent species. Trends in Ecology and Evolution 26, 124128.CrossRefGoogle ScholarPubMed
Pavoine, S (2019) An ordination approach to explore similarities among communities. Journal of Theoretical Biology 462, 8596.CrossRefGoogle ScholarPubMed
Pavoine, S (2020) adiv: An R package to analyse biodiversity in ecology. Methods in Ecology and Evolution 11, 11061112.CrossRefGoogle Scholar
Pavoine, S and Ricotta, C (2014) Functional and phylogenetic similarity among communities. Methods in Ecology and Evolution 5, 666675.CrossRefGoogle Scholar
Peters, RH (1983) The Ecological Implications of Body Size. Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
Poulin, R, Krasnov, BR, Shenbrot, GI, Mouillot, D and Khokhlova, IS (2006) Evolution of host specificity in fleas: is it directional and irreversible? International Journal of Parasitology 36, 185191.CrossRefGoogle ScholarPubMed
Poulin, R, Krasnov, BR, Mouillot, D and Thieltges, DW (2011) The comparative ecology and biogeography of parasites. Philosophical Transactions of the Royal Society of London B 366, 23792390.CrossRefGoogle ScholarPubMed
R Core Team (2020) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available at https://www.R-project.org/.Google Scholar
Revell, LJ (2012) phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution 3, 217223.CrossRefGoogle Scholar
Roll, U, Dayan, T and Kronfeld-Schor, N (2006) On the role of phylogeny in determining activity patterns of rodents. Evolutionary Ecology 20, 479490.CrossRefGoogle Scholar
Shenbrot, G, Krasnov, B, Khokhlova, I, Demidova, T and Fielden, L (2002) Habitat-dependent differences in architecture and microclimate of the burrows of Sundevall's jird (Meriones crassus) (Rodentia: Gerbillinae) in the Negev Desert, Israel. Journal of Arid Environments 51, 265279.CrossRefGoogle Scholar
Silva, M and Downing, JA (1995) CRC Handbook of Mammalian Body Masses. Boca Raton, Florida: CRC Press.Google Scholar
Sokolov, VE (1982) Mammal Skin. Berkley: University of California Press.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
Traub, R (1985) Coevolution of fleas and mammals. In Kim, KC (ed.), Coevolution of Parasitic Arthropods and Mammals. New York: John Wiley, pp. 295437.Google Scholar
Upham, NS, Esselstyn, JA and Jetz, W (2019) Inferring the mammal tree: species-level sets of phylogenies for questions in ecology, evolution, and conservation. PLoS Biology 17, e3000494.CrossRefGoogle ScholarPubMed
van der Mescht, L and Matthee, S (2017) Host range and distribution of small mammal fleas in South Africa, with a focus on species of medical and veterinary importance. Medical and Veterinary Entomology 31, 402413.CrossRefGoogle ScholarPubMed
van der Mescht, L, le Roux, PC, Matthee, CA, Raath, MJ and Matthee, S (2016) The influence of life history characteristics on flea (Siphonaptera) species distribution models. Parasites & Vectors 9, 178.CrossRefGoogle ScholarPubMed
White, CR and Seymour, RS (2005) Allometric scaling of mammalian metabolism. Journal of Experimental Biology 208, 16111619.CrossRefGoogle ScholarPubMed
Whiting, MF, Whiting, AS, Hastriter, MW and Dittmar, K (2008) A molecular phylogeny of fleas (Insecta: Siphonaptera): origins and host associations. Cladistics 24, 677707.CrossRefGoogle Scholar
Wilson, DE, Lacher, TE Jr and Mittermeier, RA (eds) (2016) Handbook of the Mammals of the World. Volume 6. Lagomorphs and Rodents I. Barcelona, Spain: Lynx Edicions.Google Scholar
Wilson, DE, Mittermeier, RA and Lacher, TE Jr (eds) (2017) Handbook of the Mammals of the World. Volume 7. Rodents II. Barcelona, Spain: Lynx Edicions.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 18.9 KB