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Parasite species coexistence and limiting similarity: a multiscale look at phylogenetic, functional and reproductive distances

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Abstract

The factors that control biodiversity have been the focus of numerous recent investigations; these include species interactions, speciation, environmental gradients and heterogeneity, all of these operating differently at each observation scale. We used a null model to examine the influence of two forces shaping the community structure of Dactylogyrus species parasitic on roach (Rutilus rutilus) gills: interspecific competition that might prevent the coexistence of the most similar species and environmental filters that might result in the most similar species coexisting together. The study was carried out on two sets of fish from two different localities in the Morava river basin (Czech Republic) to evaluate the consistency of the results across host populations, and at three different scales of observation to test for the scale dependence of assembly rules. In decreasing order, from largest to smallest, the three spatial scales investigated were: the individual fish, the individual gill arch and individual sections of each gill arch. The similarity between pairs of parasite species was measured using three different criteria: (1) phylogeny, (2) quantitative functional traits consisting of parasite size and morphometric measurements of the attachment organ’s sclerotized parts and (3) qualitative attributes of reproductive organs. First, our study reveals a strong conservatism of ecological characters for the nine Dactylogyrus parasite species, in particular regarding the attributes of their copulatory organs. Second, our study did not find any limitation of similarity among coexisting Dactylogyrus species due to interspecific competition, irrespective of the scale and the similarity measures considered. Conversely, our results support the niche filtering hypothesis, preventing the co-occurrence of species too dissimilar from one another. This process is particularly apparent at the scale of the individual fish and for functional traits associated with the hard parts of the parasites’ attachment organs. In both localities, the Dactylogyrus species that occur on the same fish individuals tend to have similar values for the haptor dimensions. Our study supports previous studies on monogenean parasite communities indicating a weak influence of competition as a structuring force, but it goes a step further by identifying environmental filtering as a key process shaping these communities.

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References

  • Bohning-Gaese K, Schuda MD, Helbig AJ (2003) Weak phylogenetic effects on ecological niches of Sylvia warblers. J Evol Biol 16:956–965

    Article  PubMed  CAS  Google Scholar 

  • Caswell H (1976) Community structure—neutral model analysis. Ecol Monogr 46:327–354

    Article  Google Scholar 

  • Chase JM, Leibold MA (2002) Spatial scale dictates the productivity–biodiversity relationship. Nature 416:427–430

    Article  PubMed  CAS  Google Scholar 

  • Chazdon RL, Careaga S, Webb C, Vargas O (2003) Community and phylogenetic structure of reproductive traits of woody species in wet tropical forests. Ecol Monogr 73:331–348

    Article  Google Scholar 

  • Chesson P (2000) Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst 31:343–366

    Article  Google Scholar 

  • Chesson P, Gebauer RLE, Schwinning S, Huntly N, Wiegand K, Ernest MSK, Sher A, Novoplansky A, Weltzin JF (2004) Resource pulses, species interactions, and diversity maintenance in arid and semi-arid environments. Oecologia 141:236–253

    Article  PubMed  Google Scholar 

  • Connor EF, Simberloff D (1979) The assembly of species communities: chance or competition? Ecology 60:1132–1140

    Article  Google Scholar 

  • Day T, Young KA (2004) Competitive and facilitative evolutionary diversification. Bioscience 54:101–109

    Article  Google Scholar 

  • Diaz S, Cabido M (2001) Vive la difference: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16:646–655

    Article  Google Scholar 

  • Dumay O, Tari PS, Tomasini JA, Mouillot D (2004) Functional groups of lagoon fish species in Languedoc Roussillon, southern France. J Fish Biol 64:970–983

    Article  Google Scholar 

  • von Euler F, Svensson S (2001) Taxonomic distinctness and species richness as measures of functional structure in bird assemblages. Oecologia 129:304–311

    Article  Google Scholar 

  • Franzen D (2004) Plant species coexistence and dispersion of seed traits in a grassland. Ecography 27:218–224

    Article  Google Scholar 

  • Gelnar M, Svobodova Z, Vykusova B (1990) Eudiplozoon nipponicum (Goto, 1991)—acclimatisation of parasite in Czech ponds. Czech Fish Bull 1:11–18

    Google Scholar 

  • Gotelli NJ (2000) Null model analysis of species co-occurrence patterns. Ecology 81:2606–2621

    Article  Google Scholar 

  • Gotelli NJ, Ellison AM (2002) Assembly rules for new England ant assemblages. Oikos 99:591–599

    Article  Google Scholar 

  • Gotelli NJ, Entsminger GL (2001) Swap and fill algorithms in null model analysis: rethinking the knight’s tour. Oecologia 129:281–291

    Article  Google Scholar 

  • Gotelli NJ, Rohde K (2002) Co-occurrence of ectoparasites of marine fishes: a null model analysis. Ecol Lett 5:86–94

    Article  Google Scholar 

  • Grime JP (1973) Competitive exclusion in herbaceous vegetation. Nature 242:344–347

    Article  Google Scholar 

  • Guégan JF, Hugueny B (1994) A nested parasite species subset pattern in tropical fish: host as major determinant of parasite infracommunity structure. Oecologia 100:184–189

    Article  Google Scholar 

  • Gusev AV (1985) Identification key to parasites of freshwater fish, Part I. In: Bauer ON (ed) Metazoa parasites. Publishing House Nauka, Leningrad

    Google Scholar 

  • Hardin G (1960) Competitive exclusion principle. Science 131:1292–1297

    Article  PubMed  CAS  Google Scholar 

  • Holmes JC, Price P (1986) Communities of parasites. In: Anderson DJ, Kikkawa J (eds) Community ecology, pattern and process. Blackwell Scientific, London, pp 187–213

    Google Scholar 

  • Hubbell SP (2001) The unified theory of biodiversity and biogegraphy. Princeton University Press, Princeton

    Google Scholar 

  • Jarkovsky J, Morand S, Šimková A, Gelnar M (2004) Reproductive barriers between congeneric monogenean parasites (Dactylogyrus: Monogenea): attachment apparatus morphology or copulatory organ incompatibility? Parasitol Res 92:95–105

    Article  PubMed  Google Scholar 

  • Kelly CK, Bowler MG (2002) Coexistence and relative abundance in forest trees. Nature 417:437–440

    Article  CAS  Google Scholar 

  • Kingston T, Jones G, Zubaid A, Kunz TH (2000) Resource partitioning in rhinolophoid bats revisited. Oecologia 124:332–342

    Article  Google Scholar 

  • Kohler SL (1992) Competition and the structure of a benthic stream community. Ecol Monogr 62:165–188

    Article  Google Scholar 

  • Krasnov BR, Mouillot D, Shenbrot GI, Khokhlova IS, Poulin R (2005) Abundance patterns and coexistence processes in communities of fleas parasitic on small mammals. Ecography 28:453–464

    Article  Google Scholar 

  • Lawton JH (1999) Are there general laws in ecology? Oikos 84:177–192

    Article  Google Scholar 

  • Litchman E, Klausmeier CA, Bossard P (2004) Phytoplankton nutrient competition under dynamic light regimes. Limnol Oceanogr 49:1457–1462

    Google Scholar 

  • Losos JB et al (2003) Niche lability in the evolution of a Caribbean lizard community. Nature 424:542–545

    Article  PubMed  CAS  Google Scholar 

  • MacArthur R, Levins R (1967) Limiting similarity convergence and divergence of coexisting species. Am Nat 101:377–387

    Article  Google Scholar 

  • Manly BFJ (1998) Randomization, bootstrap and Monte Carlo methods in biology, 2nd edn. Chapman & Hall, London

    Google Scholar 

  • Morand S, Poulin R, Rohde K, Hayward CJ (1999) Aggregation and species coexistence of ectoparasites of marine fishes. Int J Parasitol 29:663–672

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Mouillot D, George-Nascimento M, Poulin R (2005) Richness, structure and functioning in metazoan parasite communities. Oikos 109:447–460

    Article  Google Scholar 

  • Naeem S, Hawkins BA (1994) Minimal community structure: how parasitoids divide resources. Ecology 75:79–85

    Article  Google Scholar 

  • Peres-Neto PR (2004) Patterns in the co-occurrence of fish species in streams: the role of site suitability, morphology and phylogeny versus species interactions. Oecologia 140:352–360

    PubMed  Google Scholar 

  • Peterson AT, Soberon J, Sanchez-Cordero V (1999) Conservatism of ecological niches in evolutionary time. Science 285:1265–1267

    Article  PubMed  CAS  Google Scholar 

  • Poulin R (1996) Richness, nestedness, and randomness in parasite infracommunity structure. Oecologia 105:545–551

    Article  Google Scholar 

  • Poulin R (2004) Parasites and the neutral theory of biodiversity. Ecography 27:119–123

    Article  Google Scholar 

  • Poulin R, Valtonen ET (2001) Nested assemblages resulting from host-size variation: the case of endoparasite communities in fish hosts. Int J Parasitol 31:1194–1204

    Article  PubMed  CAS  Google Scholar 

  • Poulin R, Mouillot D, George-Nascimento M (2003) The relationship between species richness and productivity in metazoan parasite communities. Oecologia 137:277–285

    Article  PubMed  Google Scholar 

  • Rastetter EB, Agren GI (2002) Changes in individual allometry can lead to species coexistence without niche separation. Ecosystems 5:789–801

    Article  Google Scholar 

  • Rohde K (1991) Intra- and interspecific interactions in low density populations in resource-rich habitats. Oikos 60:91–104

    Article  Google Scholar 

  • Rohde K (2001) Spatial scaling laws may not apply to most animal species. Oikos 93:499–504

    Article  Google Scholar 

  • Rohde K, Hayward C, Heap M, Gosper D (1994) A tropical assemblage of ectoparasites-gill and head parasites of Lethrinus miniatus (Teleostei, Lethrinidae). Int J Parasitol 24:1031–1053

    Article  PubMed  CAS  Google Scholar 

  • Rosenfeld JS (2002) Functional redundancy in ecology and conservation. Oikos 98:156–162

    Article  Google Scholar 

  • Schluter D (1994) Experimental-evidence that competition promotes divergence in adaptive radiation. Science 266:798–801

    Article  PubMed  CAS  Google Scholar 

  • Schluter D (2000) Ecological character displacement in adaptive radiation. Am Nat 156:S4–S16

    Article  Google Scholar 

  • Simberloff D (2004) Community ecology: is it time to move on? Am Nat 163:787–799

    Article  PubMed  Google Scholar 

  • Šimková 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

    Article  PubMed  Google Scholar 

  • Šimková A, Ondracková M, Gelnar M, Morand S (2002) Morphology and coexistence of congeneric ectoparasite species: reinforcement of reproductive isolation?. Biol J Linn Soc 76:125–135

    Google Scholar 

  • Šimková A, Morand S, Jobet E, Gelnar M, Verneau O (2004) Molecular phylogeny of congeneric monogenean parasites (Dactylogyrus): a case of intrahost speciation. Evolution 58:1001–1018

    PubMed  Google Scholar 

  • Snyder RE, Chesson P (2004) How the spatial scales of dispersal, competition, and environmental heterogeneity interact to affect coexistence. Am Nat 164:633–650

    Article  PubMed  Google Scholar 

  • Statzner B, Doledec S, Hugueny B (2004) Biological trait composition of European stream invertebrate communities: assessing the effects of various trait filter types. Ecography 27:470–488

    Article  Google Scholar 

  • Stubbs WJ, Wilson JB (2004) Evidence for limiting similarity in a sand dune community. J Ecol 92:557–567

    Article  Google Scholar 

  • Tofts R, Silvertown J (2000) A phylogenetic approach to community assembly from a local species pool. Proc R Soc Lond Series B Biol Sci 267:363–369

    Article  CAS  Google Scholar 

  • Tokeshi M (1999) Species coexistence: ecological and evolutionary perspectives. Blackwell Science, London

    Google Scholar 

  • Watkins AJ, Wilson JB (2003) Local texture convergence: a new approach to seeking assembly rules. Oikos 102:525–532

    Article  Google Scholar 

  • Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505

    Article  Google Scholar 

  • Weither E, Clarke GDP, Keddy PA (1998) Community assembly rules, morphological dispersion, and the coexistence of plant species. Oikos 81:309–322

    Article  Google Scholar 

  • Worthen WB, Rohde K (1996) Nested subset analyses of colonization-dominated communities: metazoan ectoparasites of marine fishes. Oikos 75:471–478

    Article  Google Scholar 

Download references

Acknowledgements

Two anonymous referees have contributed many relevant comments to improve this article. This study was supported by Research Project of the Masaryk University, Brno, project number: MSM0021622416. AŠ was founded by the Grant Agency of the Czech Republic, project number: 524/03/P108.

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Authors and Affiliations

  1. UMR CNRS-UMII 5119 Ecosystêmes Lagunaires, Université Montpellier II, CC 093, 34095, Montpellier cedex 5, France

    David Mouillot

  2. Department of Zoology and Ecology, Faculty of Science, Masaryk University, Kotlářská 2, 611 37, Brno, Czech Republic

    Andrea Šimková

  3. Centre de Biologie et de Gestion des Populations (CBGP), UMR Agro.M-CIRAD-IRD-INRA, Campus International de Baillarguet, CS 30 016, 34988, Montferrier-sur-Lez Cédex, France

    Serge Morand

  4. Department of Zoology, University of Otago, P.O. Box 56, Dunedin, New Zealand

    Robert Poulin

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  1. David Mouillot
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Correspondence to David Mouillot.

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Communicated by Sven Bacher

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Mouillot, D., Šimková, A., Morand, S. et al. Parasite species coexistence and limiting similarity: a multiscale look at phylogenetic, functional and reproductive distances. Oecologia 146, 269–278 (2005). https://doi.org/10.1007/s00442-005-0194-1

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