Abstract
We applied a step-down factor analysis (SDFA) and multi-site generalised dissimilarity modelling (MS-GDM) to local flea communities harboured by small mammals (i.e., collected at small sampling sites over a short time period) in two South American regions (Patagonia and the Northwestern Argentina) with the aim of understanding whether these communities were assembled via niche-based or dispersal-based processes. The SDFA allows us to determine whether clusters of flea assemblages across different types of climates, vegetation and soils can be distinguished (suggesting niche-based assembly). MS-GDM allows us to determine whether a substantial proportion of the variation in flea species turnover is explained by specific climate-associated, vegetation-associated and soil-associated variables (indicating niche-based assembly) or host turnover (indicating dispersal-based assembly). Mapping of assemblages on climate, vegetation and soil maps, according to their loadings on axis 1 or axis 2 of the SDFA, did not provide clear-cut results. Clusters of similar loadings could be recognized within some, but not other, climate, vegetation and soil types. However, MS-GDM demonstrated that the effect of environmental variables (especially air temperature) on flea compositional turnover was much stronger than that of host turnover, indicating the predominance of niche-based processes in local community assembly. A comparison of our results with those on the mechanisms that drive species assembly in regional communities allows us to conclude that local and regional communities result from the joint action of niche-based and dispersal-based processes, with the former more important at a smaller spatial scale and the latter at a larger spatial scale.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data supporting this paper can be obtained from corresponding author upon reasonable request.
References
Ackerly DD, Cornwell WK (2007) A trait-based approach to community assembly: partitioning of species trait values into within- and among-community components. Ecol Lett 10:135–145. https://doi.org/10.1111/j.1461-0248.2006.01006.x
Alroy J (2019) Discovering biogeographic and ecological clusters with a graph theoretic spin on factor analysis. Ecography 42:1504–1513. https://doi.org/10.1111/ecog.04464
Baker RJ, Williams SL (1972) A live trap for pocket gophers. J Wildl Manag 36:1320–1322. https://doi.org/10.2307/3799275
Bar-Massada A, Kent R, Carmel Y (2014) Environmental heterogeneity affects the location of modelled communities along the niche–neutrality continuum. Proc Roy Soc Lond B 281:20133249. https://doi.org/10.1098/rspb.2013.3249
Baselga A (2010) Partitioning the turnover and nestedness components of beta diversity. Global Ecol Biogeogr 19:134–143. https://doi.org/10.1111/j.1466-8238.2009.00490.x
Beck HE, Zimmermann NE, McVicar TR, Vergopolan N, Berg A, Wood EF (2018) Present and future Köppen-Geiger climate classification maps at 1-km resolution. Sci Data 5:180214. https://doi.org/10.1038/sdata.2018.214
Bell G, Lechowicz MJ, Waterway MJ (2006) The comparative evidence relating to functional and neutral interpretations of biological communities. Ecology 87:1378–1386. https://doi.org/10.1890/0012-9658(2006)87[1378:tcertf]2.0.co;2
Bivand RS, Pebesma EJ, Gomez-Rubio V (2013) Applied spatial data analysis with R, 2nd edn. Springer, NY
Blonder B, Nogués-Bravo D, Borregaard MK, Donoghue JC 2nd, Jørgensen PM, Kraft NJ, Lessard JP, Morueta-Holme N, Sandel B, Svenning JC, Violle C, Rahbek C, Enquist BJ (2015) Linking environmental filtering and disequilibrium to biogeography with a community climate framework. Ecology 96:972–985. https://doi.org/10.1890/14-0589.1
Braak CJF (1985) Correspondence analysis of incidence and abundance data: properties in terms of a unimodal response model. Biometrics 41:859–873. https://doi.org/10.2307/2530959
Brun P, Zimmermann NE, Hari C, Pellissier L, Karger DN (2022) Global climate-related predictors at kilometre resolution for the past and future. Earth Syst Sci Data Discuss (reprint). https://doi.org/10.5194/essd-2022-212
Cavender-Bares J, Ackerly DD, Baum DA, Bazzaz FA (2004) Phylogenetic overdispersion in Floridian oak communities. Am Nat 163(6):823–843. https://doi.org/10.1086/386375
Chase JM, Myers JA (2011) Disentangling the importance of ecological niches from stochastic processes across scales. Phil Trans Roy Soc Lond B 366:2351–2363. https://doi.org/10.1098/rstb.2011.0063
Eriksson A, Doherty J-F, Fischer E, Graciolli G, Poulin R (2020) Hosts and environment overshadow spatial distance as drivers of bat fly species composition in the Neotropics. J Biogeogr 47:736–747. https://doi.org/10.1111/jbi.13757
Ferrier S, Manion G, Elith J, Richardson K (2007) Using generalized dissimilarity modelling to analyse and predict patterns of beta diversity in regional biodiversity assessment. Divers Distrib 13:252–264. https://doi.org/10.1111/j.1472-4642.2007.00341.x
Gibert C, Escarguel G (2019) PER-SIMPER—a new tool for inferring community assembly processes from taxon occurrences. Global Ecol Biogeogr 28:374–385. https://doi.org/10.1111/geb.12859
Gibert C, Shenbrot GI, Stanko M, Khokhlova IS, Krasnov BR (2021) Dispersal-based versus niche-based processes as drivers of flea species composition on small mammalian hosts: inferences from species occurrences at large and small scales. Oecologia 197:471–484. https://doi.org/10.1007/s00442-021-05027-1
Gorsuch RL (2014) Factor analysis: classic edition, 2nd edn. Routledge, Oxfordshire
Gravel D, Canham CD, Beaudet M, Messier C (2006) Reconciling niche and neutrality: the continuum hypothesis. Ecol Lett 9:399–409. https://doi.org/10.1111/j.1461-0248.2006.00884.x
Gutiérrez PA, Martorelli SR (1999) Niche preferences and spatial distribution of Monogenea on the gills of Pimelodus maculatus in Río de la Plata (Argentina). Parasitology 119:183–188. https://doi.org/10.1017/s003118209900459x
Hasenack H, da Silva JS, Weber EJ, Hofmann GS (2017) A digital version of Hueck’s vegetation map of South America: 50 years after the release of his book on the sub-continent’s forests. Geografía y Sistemas De Información Geografíca 9:11–14
Hill MO (1973) Reciprocal averaging: an eigenvector method of ordination. J Ecol 61:237–249. https://doi.org/10.2307/2258931
Hopkins GW, Thacker JI, Dixon AFG, Waring P, Telfer MG (2002) Identifying rarity in insects: the importance of host plant range. Biol Cons 105:293–307. https://doi.org/10.1016/S0006-3207(01)00203-8
Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton Univ Press, Princeton
Hubbell SP (2006) Neutral theory and the evolution of ecological equivalence. Ecology 87:1387–1398. https://doi.org/10.1890/0012-9658
Hueck K, Seibert P (1972) Vegetationskarte von Südamerika: Erläuterung zur Karte 1:8.000.000. Gustav Fischer, Stuttgart, Germany
Hui C, McGeoch MA (2014) Zeta diversity as a concept and metric that unifies incidence-based biodiversity patterns. Amer Nat 184:684–694. https://doi.org/10.1086/678125
Hutchinson GE (1957) Concluding remarks. Cold Spring Harbor Symp Quant Biol 22:415–427. https://doi.org/10.1101/SQB.1957.022.01.039
Karger DN, Conrad O, Böhner J, Kawohl T, Kreft H, Soria-Auza RW, Zimmermann NE, Linder HP, Kessler M (2017) Climatologies at high resolution for the Earth’s land surface areas. Sci Data 4:170122. https://doi.org/10.1038/sdata.2017.122
Köppen W (1936) Handbuch der Klimatologie, vol I. Das geographische System der Klimate, Gebrüder Borntraeger, Berlin, Germany
Kraft NJB, Ackerly DD (2014) Assembly of plant communities. In: Monson RK (ed) Ecology and the environment The Plant Sciences, vol 8. Springer, NY, pp 68–88
Krasnov BR (2008) Functional and evolutionary ecology of fleas. Cambridge Univ Press, Cambridge, A model for ecological parasitology
Krasnov BR, Khokhlova IS (2001) The effect of behavioural interactions on the transfer of fleas (Siphonaptera) between two rodent species. J Vector Ecol 26:181–190
Krasnov BR, Shenbrot GI (2002) Coevolutionary events in history of association of jerboas (Rodentia: Dipodidae) and their flea parasites. Israel J Zool 48:331–350
Krasnov BR, Shenbrot GI, Medvedev SG, Vatschenok VS, Khokhlova IS (1997) Host-habitat relations as an important determinant of spatial distribution of flea assemblages (Siphonaptera) on rodents in the Negev Desert. Parasitol 114:159–173. https://doi.org/10.1017/s0031182096008347
Krasnov BR, Khokhlova IS, Fielden LJ, Burdelova NV (2001) Effect of air temperature and humidity on the survival of pre-imaginal stages of two flea species (Siphonaptera: Pulicidae). J Med Entomol 38:629–637. https://doi.org/10.1603/0022-2585-38.5.629
Krasnov BR, Khokhlova IS, Fielden LJ, Burdelova NV (2002) Time of survival under starvation in two flea species (Siphonaptera: Pulicidae) at different air temperatures and relative humidities. J Vector Ecol 27:70–81
Krasnov BR, Shenbrot GI, Mouillot D, Khokhlova IS, Poulin R (2005) Spatial variation in species diversity and composition of flea assemblages in small mammalian hosts: geographic distance or faunal similarity? J Biogeogr 32:633–644. https://doi.org/10.1111/j.1365-2699.2004.01206.x
Krasnov BR, Shenbrot GI, Khokhlova IS, Mouillot D, Poulin R (2008) Latitudinal gradients in niche breadth: empirical evidence from haematophagous ectoparasites. J Biogeogr 35:592–601. https://doi.org/10.1111/j.1365-2699.2007.01800.x
Krasnov BR, Shenbrot GI, Khokhlova IS, Stanko M, Morand S, Mouillot D (2015a) Assembly rules of ectoparasite communities across scales: combining patterns of abiotic factors, host composition, geographic space, phylogeny and traits. Ecography 38:184–197. https://doi.org/10.1111/ecog.00915
Krasnov BR, Shenbrot GI, Khokhlova IS (2015b) Historical biogeography of fleas: the former Bering Land Bridge and phylogenetic dissimilarity between the Nearctic and Palearctic assemblages. Paras Res 114:1677–1686. https://doi.org/10.1007/s00436-015-4349-7
Krasnov BR, Shenbrot GI, Vinarski MV, Korallo-Vinarskaya NP, Khokhlova IS (2020) Multi-site generalized dissimilarity modelling reveals drivers of species turnover in ectoparasite assemblages of small mammals across the northern and central Palaearctic. Global Ecol Biogeogr 29:1579–1594. https://doi.org/10.1111/geb.13143
Krasnov BR, Shenbrot GI, Khokhlova IS (2022) Regional flea and host assemblages form biogeographic, but not ecological, clusters: evidence for a dispersal-based mechanism as a driver of species composition. Parasitol 149:1450–1459. https://doi.org/10.1017/S0031182022000907
Latombe G, Hui C, McGeoch MA (2017) Multi-site generalised dissimilarity modelling: using zeta diversity to differentiate drivers of turnover in rare and widespread species. Methods Ecol Evol 8:431–442. https://doi.org/10.1111/2041-210X.12756
Latombe G, Richardson DM, Pyšek P, Kučera T, Hui C (2018) Drivers of species turnover vary with species commonness for native and alien plants with different residence times. Ecology 99:2763–2775. https://doi.org/10.1002/ecy.2528
Latombe G, McGeoch MA, Nipperess D, Hui C (2022) Zetadiv: functions to compute compositional turnover using zeta diversity. R package version 1.2.1. https://CRAN.R-project.org/package=zetadiv
Lehane MJ (2005) The biology of blood-sucking in insects, 2nd edn. Cambridge Univ Press, Cambridge
Li W, Cheng J-M, Yu K-L, Epstein HE, Du G-Z (2015) Niche and neutral processes together determine diversity loss in response to fertilization in an alpine meadow community. PLoS ONE 10:e0134560. https://doi.org/10.1371/journal.pone.0134560
López Berrizbeitia MF (2018). Sifonápteros de micromamíferos (Didelphimorphia, Chiroptera y Rodentia) del Noroeste Argentino: sistemática y distribución. Doctoral Thesis. San Miguel de Tucum an: Facultad de Ciencias Naturales e IML, Universidad Nacional de Tucumán. Tucumán, Argentina
López Berrizbeitia MF, Díaz MM (2019) Siphonaptera associated with small mammals (Didelphimorphia, Chiroptera, and Rodentia) from northwestern Argentina. Therya 10:279-308. https://doi.org/10.12933/therya-19-885
Lawrence AL, Webb CE, Clark NJ, Halajian A, Mihalca AD, Miret J, D’Amico G, Brown G, Kumsa B, Modrý D, Šlapeta J (2019) Out-of-Africa, human-mediated dispersal of the common cat flea, Ctenocephalides felis: the hitchhiker’s guide to world domination. Int J Parasitol 49:321–336. https://doi.org/10.1016/j.ijpara.2019.01.001
MacArthur RH, Levins R (1967) The limiting similarity, convergence, and divergence of coexisting species. Amer Nat 101:377–385. https://doi.org/10.1086/282505
Maestri R, Shenbrot GI, Krasnov BR (2017) Parasite beta diversity, host beta diversity and environment: application of two approaches to reveal patterns of flea species turnover in Mongolia. J Biogeogr 44:1880–1890. https://doi.org/10.1111/jbi.13025
Marshall AG (1981) The ecology of ectoparasitic insects. Academic Press, London
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 MV, Hui C (2019) Measuring continuous compositional change using decline and decay in zeta diversity. Ecology 100:e02832. https://doi.org/10.1002/ecy.2832
Medvedev SG (1996) Geographical distribution of families of fleas (Siphonaptera). Entomol Rev 76:978–992
Medvedev SG (1998) Classification of fleas (order Siphonaptera) and its theoretical foundations. Entomol Rev 78:511–521
Mouillot D, George-Nascimento M, Poulin R (2003) How parasites divide resources: a test of the niche apportionment hypothesis. J Anim Ecol 72:757–764. https://doi.org/10.1046/j.1365-2656.2003.00749.x
Nakaoka M, Ito N, Yamamoto T, Okuda T, Noda T (2006) Similarity of rocky intertidal assemblages along the Pacific coast of Japan: effects of spatial scales and geographic distance. Ecol Res 21:425–435. https://doi.org/10.1007/s11284-005-0138-6
Nekola JC, White PS (1999) The distance decay of similarity in biogeography and ecology. J Biogeogr 26:867–878. https://doi.org/10.1046/j.1365-2699.1999.00305.x
Palmer MW (2005) Distance decay in an old-growth neotropical forest. J Veget Sci 16:161–166. https://doi.org/10.1111/j.1654-1103.2005.tb02351.x
Pavoine S, Vela E, Gachet S, de Bélair G, Bonsall MB (2011) Linking patterns in phylogeny, traits, abiotic variables and space: a novel approach to linking environmental filtering and plant community assembly. J Ecol 99:165–175. https://doi.org/10.1111/j.1365-2745.2010.01743.x
Pearson RG, Dawson TP (2003) Predicting the impacts of climate change on the distribution of species: are bioclimate envelope models useful? Global Ecol Biogeogr 12:361–371. https://doi.org/10.1046/j.1466-822X.2003.00042.x
Pearson DE, Ortega YK, Eren Ö, Hierro JL (2018) Community assembly theory as a framework for biological invasions. Trends Ecol Evol 33:313–325. https://doi.org/10.1016/j.tree.2018.03.002
Pebesma EJ (2018) Simple features for R: standardized support for spatial vector data. The R J 10:439-446. https://doi.org/10.32614/RJ-2018-009
Pebesma EJ, Bivand RS (2005) Classes and methods for spatial data in R: the “sp” package. R News 5:9–13
Peel MC, Finlayson BL, McMahon TA (2007) Updated world map of the Köppen-Geiger climate classification. Hydrol Earth Syst Sci 11:1633–1644. https://doi.org/10.5194/hess-11-1633-2007
Poulin R (2003) The decay of similarity with geographical distance in parasite communities of vertebrate hosts. J Biogeogr 30:1609–1615. https://doi.org/10.1046/j.1365-2699.2003.00949.x
R Core Team (2021) R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org/
Revelle W (2022) psych: procedures for personality and psychological research, Northwestern University, Evanston, Illinois, USA. R package version 2.2.9. https://CRAN.R-project.org/package=psych
Rohde K (1994) Niche restriction in parasites: proximate and ultimate causes. Parasitol 109:S69–S84. https://doi.org/10.1017/s0031182000085097
Sanchez JP (2013) Sifonápteros parásitos de los roedores sigmodontinos de la Patagonia Norte de la Argentina: estudios sistemáticos y ecológicos. Tesis Doctoral, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, La Plata, Argentina
Sanchez JP, Lareschi M (2013) The fleas (Insecta: Siphonaptera) parasites of sigmodontine rodents (Cricetidae) from Northern Patagonia, Argentina. Comp Parasitol 80:110–117. https://doi.org/10.1654/4576.1
Sanchez JP, Lareschi M (2019) Diversity, distribution and parasitism rates of fleas (Insecta: Siphonaptera) on sigmodontine rodents (Cricetidae) from Argentinian Patagonia. Bull Entomol Res 109:72–83. https://doi.org/10.1017/S0007485318000196
Shenbrot GI, Sokolov VE, Geptner VG, Kovalskaya YM (1995) Dipodoidea. The mammals of Russia and adjacent regions, Nauka, Moscow, Russia (in Russian)
Shenbrot G, Krasnov B, Lu L (2007) Geographical range size and host specificity in ectoparasites: a case study with Amphipsylla fleas and rodent hosts. J Biogeogr 34:1679–1690. https://doi.org/10.1111/j.1365-2699.2007.01736.x
Sikes RS (2016) 2016 guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. J Mammal 97:663–688. https://doi.org/10.1093/jmammal/gyw078
Simková A, Desdevises Y, Gelnar M, Morand S (2000) Co-existence of nine gill ectoparasites (Dactylogyrus: Monogenea) parasitising the roach (Rutilus rutilus L.): history and present ecology. Int J Parasitol 30:1077–1088. https://doi.org/10.1016/s0020-7519(00)00098-9
Soberón J (2007) Grinnellian and Eltonian niches and geographic distributions of species. Ecol Lett 10:1115–1123. https://doi.org/10.1111/j.1461-0248.2007.01107
South A (2017) rnaturalearth: world map data from Natural Earth. R package version 0.1.0. https://CRAN.R-project.org/package=rnaturalearthter
Thompson R, Townsend C (2006) A truce with neutral theory: local deterministic factors, species traits and dispersal limitation together determine patterns of diversity in stream invertebrates. J Anim Ecol 75:476–484. https://doi.org/10.1111/j.1365-2656.2006.01068.x
Traub R (1980) The zoogeography and evolution of some fleas, lice and mammals. In: Traub R and Starcke H (eds) Fleas. Proceedings of the International Conference on fleas, Ashton Wold, England, June, 1977. A. A. Balkema, Rotterdam 93–172
van der Mescht L, le Roux PC, Matthee CA, Raath MJ, Matthee S (2016) The influence of life history characteristics on flea (Siphonaptera) species distribution models. Parasites Vectors 9:178. https://doi.org/10.1186/s13071-016-1466-9
Vilmi A, Gibert C, Escarguel G, Happonen H, Heino A, Jamoneau A, Passy SP, Picazo F, Soininen J, Tison-Rosebery J, Wang J (2021) Dispersal–niche continuum index: a new quantitative metric for assessing the relative importance of dispersal versus niche processes in community assembly. Ecography 44:370–379. https://doi.org/10.1111/ecog.05356
Vinarski MV, Korallo NP, Krasnov BR, Shenbrot GI, Poulin R (2007) Decay of similarity of gamasid mite assemblages parasitic on Palaearctic small mammals: geographic distance, host-species composition or environment. J Biogeogr 34:1691–1700. https://doi.org/10.1111/j.1365-2699.2007.01735.x
Wessels W (1998) Gerbillidae from the Miocene and Priocene of Europe. Mitt Bayer Staat Paläont Hist Geol 38:187–207
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer, NY
Whiting MF, Whiting AS, Hastriter MW, Dittmar K (2008) A molecular phylogeny of fleas (Insecta: Siphonaptera): origins and host associations. Cladistics 24:677–707. https://doi.org/10.1111/j.1096-0031.2008.00211.x
Acknowledgements
We thank Ulyses F.J. Pardiñas and Daniel Udrizar Sauthier (Centro Nacional Patagónico CENPAT, Puerto Madryn, Argentina) for their help with mammal identification in Patagonia and members of the Instituto de Investigaciones de Biodiversidad Argentina (PDBA) for their help with the field and laboratory work in the Northwestern Argentina.
Funding
Sampling in Patagonia was supported by the Agencia Nacional de Promoción de la Investigación, el Desarrollo Tecnológico y la Innovación (PICT2010-338), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) (PIP 0146) and the Universidad Nacional de La Plata (UNLP N752). Field sampling in the Northwestern Argentina was supported by the National Science Foundation (BSR-8906665) and CONICET (PIP N 4963 and 1587).
Author information
Authors and Affiliations
Contributions
M. Fernanda López Berrizbeitia, Juliana P. Sanchez, M. Mónica Díaz and Marcela Lareschi collected data. Boris R. Krasnov, Irina S. Khokhlova and Vasily I. Grabovsky analysed data. Boris R. Krasnov wrote the first version of the manuscript. All authors finalized the manuscript.
Corresponding author
Ethics declarations
Ethics approval
Sampling and procedures in Patagonia were carried out under permits from the Dirección de Fauna y Flora Silvestre de la Provincia del Chubut, Nos. 34/06, 38/08 and 71/2011. Sampling and procedures in the Northwestern Argentina were carried out under permits from the Secretaria de Biodiversidad de Jujuy (No. 025/2019-S.B), Secretaria de Ambiente y Desarrollo sustentable de Salta (No. 000163), Dirección de Flora, Fauna Silvestre y Suelos de la Provincia de Catamarca and Tucumán (No. 213–13 and No. 84–19) and Dirección General de Bosques y Fauna de la Provincia de Santiago del Estero (No. 1351/2017). All animals were handled in accordance with the animal care and use guidelines of the American Society of Mammalogists (Sikes 2016).
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Conflict of interest
BRK is a Section Editor of Parasitology Research. Other authors declare that they have no competing interests.
Additional information
Handling Editor: Una Ryan
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Krasnov, B.R., Berrizbeitia, M.F.L., Sanchez, J.P. et al. The species composition of local flea assemblages at a small scale in two South American regions is predominantly driven by niche-based mechanisms. Parasitol Res 122, 571–583 (2023). https://doi.org/10.1007/s00436-022-07759-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-022-07759-2