Relative contributions of disparate animal vectors to the development of freshwater ciliate communities

Abstract

Here, we evaluate the role of two disparate animal groups, amphibians and odonates, in the dispersal of ciliates. We performed a 33-day outdoor experiment from July to August 2018 with four treatments: (i) a control, with only wind action; (ii) a treatment with the addition from propagules of odonates; (iii) a treatment with propagules from amphibians; and (iv) a treatment with the addition of propagules from both animals. We recorded 54 species of ciliates from 11 groups, with Peritrichia the most representative. Species richness and abundance increased markedly after the 12th day. The species composition of the ciliate species showed differences between treatments within each time period, as well as between the different treatments throughout the experiment. As expected, our results not only evidenced that the dispersal of ciliate protists was improved when mediated by biological vectors, but also demonstrated that the impact depends on the animal vector, and that the effect is even more relevant when propagules are carried by both animal vectors. Our findings support the importance of animal vectors in the dispersal and structuring of ciliates, and highlight the potential differences in the effectiveness of amphibians and odonates for the dispersal of this group.

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References

  1. Abellán, P., J. Tella, M. Carrete, L. Cardador & J. D. Anadón, 2017. Climatic matching drives spread rate but not establishment success in recent unintentional bird introductions. Proceedings of the National Academy of Sciences of the United States of America 35: 9385–9390.

    Google Scholar 

  2. Alahuhta, J., S. Kosten, M. Akasaka, D. Auderset, M. M. Azzella, R. Bolpagni, C. P. Bove, P. A. Chambers, E. Chappuis, J. Clayton, M. de Winton, F. Ecke, E. Gacia, G. Gecheva, P. Grillas, J. Hauxwell, S. Hellsten, J. Hjort, M. V. Hoyer, C. Ilg, A. Kolada, M. Kuoppala, T. Lauridsen, E. H. Li, B. A. Lukács, M. Mjelde, A. Mikulyuk, R. P. Mormul, J. Nishihiro, B. Oertli, L. Rhazi, M. Rhazi, L. Sass, C. Schranz, M. Søndergaard, T. Yamanouchi, Q. Yu, H. Wang, N. Willby, X. K. Zhang & J. Heino, 2017. Global variation in the beta diversity of lake macrophytes is driven by environmental heterogeneity rather than latitude. Journal of Biogeography 44: 1758–1769.

    Google Scholar 

  3. Allen, M. R., 2007. Measuring and modelling dispersal of adult zooplankton. Oecologia 153: 135–143.

    PubMed  Google Scholar 

  4. Anderson, M. J., 2005. Permanova: a FORTRAN computer program for permutational multivariate analysis of variance. Department of Statistics, University of Auckland, Auckland, NZL.

    Google Scholar 

  5. Andrushchyshyn, O. P., A. K. Magnusson & D. D. Williams, 2006. Responses of intermittent pond ciliate populations and communities to in situ bottom-up and top-down manipulations. Aquatic Microbial Ecology 42(3): 293–310.

    Google Scholar 

  6. Araújo, A. P., A. H. C. Marques, A. P. Dantas, M. Melo Junior, G. J. B. Moura & M. S. Tinoco, 2020. Assisted phoresy of invertebrates by anurans in tank bromeliads: interspecific relationship. Aquatic Sciences 82(3): 1–11.

    Google Scholar 

  7. Artolozaga, I., E. Santamaria, A. Lopez, B. Ayo & J. Irriberri, 1997. Succession of bacterivorous protists on laboratory-made marine snow. Journal of Plankton Research 19: 1429–1440.

    Google Scholar 

  8. Beckman, N. G., J. M. Bullock & R. Salguero-Gómez, 2018. High dispersal ability is related to fast life-history strategies. Journal of Ecology 106: 1349–1362.

    Google Scholar 

  9. Beladjal, L. & J. Mertens, 2009. Diaspore dispersal of Anostraca by flying insects. Journal of Crustacean Biology 29(2): 266–268.

    Google Scholar 

  10. Bharti, D., S. Kumar, A. La Terza & K. Chandra, 2020. Dispersal of ciliated protist cysts: mutualism and phoresy on mites. Ecology 24: e03075.

    Google Scholar 

  11. Biddanda, J. J. A. & L. R. Pomeroy, 1988. Microbial aggregation and degradation of phytoplankton derived detritus in seawater. I Microbial succession. Marine Ecology Progress Series 42: 79–88.

    Google Scholar 

  12. Bilton, D. T., J. R. Freeland & B. Okamura, 2001. Dispersal in freshwater invertebrates: mechanisms and consequences. Annual Review of Ecology and Systematics 32: 159–181.

    Google Scholar 

  13. Blackburn, T. M., J. L. Lockwood & P. Cassey, 2015. The influence of numbers on invasion success. Molecular ecology 24(9): 1942–1953.

    PubMed  Google Scholar 

  14. Bohonak, A. J. & H. H. Whiteman, 1999. Dispersal of the fairy shrimp Branchinecta coloradensis (Anostraca): effects of hydroperiod and salamanders. Limnology and Oceanography 44: 487–493.

    Google Scholar 

  15. Buosi, P. R. B., G. M. Pauleto, F. A. Lansac-Tôha & L. F. M. Velho, 2011. Ciliate community associated with aquatic macrophyte roots: effects of nutrient enrichment on the community composition and species richness. European Journal of Protistology 47(2): 86–102.

    PubMed  Google Scholar 

  16. Buosi, P., A. Cabral, L. Utz, C. Ludgero, G. Vieira & L. Velho, 2015. Effects of seasonality and dispersal on the ciliate community inhabiting bromeliad phytotelmata in riparian vegetation of a large tropical river. Journal of Eukaryotic Microbiology 62: 737–749.

    Google Scholar 

  17. Cadotte, M. W., 2006. Dispersal and species diversity: a Meta analysis. The American Naturalist 167: 913–924.

    PubMed  Google Scholar 

  18. Cassey, P., S. Delean, J. L. Lockwood, J. S. Sadowski & T. M. Blackburn, 2018. Dissecting the null model for biological invasions: a meta-analysis of the propagule pressure effect. PLoS Biology 16(4): e2005987.

    PubMed  PubMed Central  Google Scholar 

  19. Chen, J., A. D. Del Genio, B. E. Carlson & M. G. Bosilovich, 2008. The spatio temporal structure of twentieth-century climate variations in observations and reanalyses. Part I: long-term trend. Journal of Climate 21: 2611–2633.

    Google Scholar 

  20. Cohen, G. M. & J. B. Shurin, 2003. Scale-dependence and mechanisms of dispersal in freshwater zooplankton. Oikos 103: 603–617.

    Google Scholar 

  21. Corliss, J. O. & S. C. Esser, 1974. Comments on the role of the cyst in the life cycle and survival of free-living protozoa. Transactions of the American Microscopical Society 3: 578–593.

    Google Scholar 

  22. De Bie, T., L. De Meester, L. Brendonck, K. Martens, B. Goddeeris & D. Ercken, 2012. Body size and dispersal mode as key traits determining metacommunity structure of aquatic organisms. Ecology Letters 15: 740–747.

    PubMed  Google Scholar 

  23. Deitmer, J. W., 1987. Loss of electrical excitability during encystment of the hypotrichous ciliate Stylonychia mytilus. Naturwissenschaften 74: 140–142.

    Google Scholar 

  24. Evans, S., J. B. Martiny & S. D. Allison, 2017. Effects of dispersal and selection on stochastic assembly in microbial communities. The ISME Journal 11(1): 176–185.

    PubMed  Google Scholar 

  25. Finlay, B. J., 2002. Global dispersal of free-living microbial eukaryote species. Science 296: 1061–1063.

    CAS  PubMed  Google Scholar 

  26. Finlay, B. J. & G. F. Esteban, 1998. Freshwater protozoa: biodiversity and ecological function. Biodiversity Conservation 7: 1163–1186.

    Google Scholar 

  27. Foissner, W., 2006. Biogeography and dispersal of microorganisms: a review emphasizing protists. Acta Protozoologica 45: 111–136.

    Google Scholar 

  28. Foissner, W., 2011. Dispersal of protists: the role of cysts and human introductions. In Fontaneto, D. (ed.), Biogeography of microscopic organisms: is everything small everywhere?. Cambridge University Press, Cambridge: 61–87.

    Google Scholar 

  29. Foissner, W. & H. Berger, 1996. A user-friendly guide to the ciliates (Protozoa Ciliophora) commonly used by hydrobiologists as bioindicators in rivers, lakes and wastewaters, with notes on their ecology. Freshwater Biology 35: 375–482.

    Google Scholar 

  30. Foissner, W., H. Berger & J. Schaumburg, 1999. Identification and ecology of limnetic plankton ciliates. Imformations berichte des Bayer. Bayerisches Landesamtes fur Wasserwirtschaft Heft 3(99): 1–793.

    Google Scholar 

  31. Fontaneto, D., 2019. Long-distance passive dispersal in microscopic aquatic animals. Movement Ecology 7: 1–10.

    Google Scholar 

  32. Freiry, R. F., Weber, V., Bonecker, C. C., Lansac-Tôha, F. A., Pires, M. M., Stenert, C., Maltchik, L. 2020. Additive partitioning of the diversity of the dormant zooplankton communities in intermittent ponds along a forest–grassland transition. Hydrobiologia 847 (5):1327–1342.

    Google Scholar 

  33. Frisch, D., K. Cottenie, A. Badosa & A. J. Green, 2012. Strong spatial influence on colonization rates in a pioneer zooplankton metacommunity. PLoS ONE 7: 40205.

    Google Scholar 

  34. García-Girón, J., J. Heino, F. García-Criado, C. Fernández-Aláez & J. Alahuhta, 2020. Biotic interactions hold the key to understanding metacommunity organisation. Ecography 43: 1180–1190.

    Google Scholar 

  35. Gianluca, A. T., S. A. J. Declerck, P. Lemmens & L. De Meester, 2017. Effects of dispersal and environmental heterogeneity on the replacement and nestedness components of β-diversity. Ecology 98(2): 525–533.

    Google Scholar 

  36. Gilbert, J. J. & T. Schroder, 2003. The ciliate epibiont Epistylis pygmaeum: selection for zooplankton hosts, reproduction and effect on two rotifers. Freshwater Biology 48: 878–893.

    Google Scholar 

  37. Grainger, T. N. & B. Gilbert, 2016. Dispersal and diversity in experimental metacommunities: linking theory and practice. Oikos 125: 1213–1223.

    Google Scholar 

  38. Hill, M. J., J. Heino, I. Thornhill, D. B. Ryves & P. J. Wood, 2017. Effects of dispersal mode on the environmental and spatial correlates of nestedness and species turnover in pond communities. Oikos 126: 1575–1585.

    Google Scholar 

  39. Incagnone, G., F. Marrone, R. Barone, L. Robba & L. Naselli-Flores, 2015. How do freshwater organisms cross the “dry ocean”? A review on passive dispersal and colonization processes with a special focus on temporary ponds. Hydrobiologia 750(1): 103–123.

    Google Scholar 

  40. Kneitel, J. M. & J. M. Chase, 2004. Disturbance, predator, and resource interactions alter container community composition. Ecology 85: 2088–2093.

    Google Scholar 

  41. Korhonen, J. J., J. Soininen & H. Hillebrand, 2010. A quantitative analysis of temporal turnover in aquatic species assemblages across ecosystems. Ecology 91: 508–517.

    PubMed  Google Scholar 

  42. Kristiansen, J., 1996. Dispersal of freshwater algae: a review. Hydrobiologia 336: 151–157.

    Google Scholar 

  43. Lansac-Tôha, F. M., B. R. Meira, B. T. Segovia, F. A. Lansac-Tôha & L. F. M. Velho, 2016. Hydrological connectivity determining metacommunity structure of planktonic heterotrophic flagellates. Hydrobiologia 781: 81–94.

    Google Scholar 

  44. Lansac-Tôha, F. M., J. Heino, B. A. Quirino, G. A. Moresco, O. Peláez, B. R. Meira, L. C. Rodrigues, S. Jati, F. A. Lansac-Tôha & L. F. M. Velho, 2019. Differently dispersing organism groups show contrasting beta diversity patterns in a dammed subtropical river basin. Science of the Total Environment 691: 1271–1281.

    Google Scholar 

  45. Leibold, M. A., M. Holyoak, N. Mouquet, P. Amarasekare, J. M. Chase, M. F. Hoopes, R. D. Holt, J. B. Shurin, R. Law, D. Tilman, M. Loreau & A. Gonzalez, 2004. The metacommunity concept: a framework for multi-scale community ecology. Ecology Letters 7: 601–613.

    Google Scholar 

  46. Leturque, H. & F. Rousset, 2002. Dispersal, kin competition, and the ideal free distribution in a spatially heterogeneous population. Theoretical Population Biology 62: 169–180.

    PubMed  Google Scholar 

  47. Lockwood, J. L., P. Cassey & T. M. Blackburn, 2009. The more you introduce the more you get: the role of colonization pressure and propagule pressure in invasion ecology. Diversity and Distributions 15: 904–910.

    Google Scholar 

  48. Logue, J. B., N. Mouquet, H. Peter, H. Hillebran & Metacommunity Working Group, 2011. Empirical approaches to metacommunities: a review and comparison with theory. Trends in Ecology & Evolution 26: 482.

    Google Scholar 

  49. Louette, G. & L. De Meester, 2005. High dispersal capacity of cladoceran zooplankton in newly founded communities. Ecology 86: 353–359.

    Google Scholar 

  50. Lynn, D. 2008. The ciliated protozoa: characterization, classification, and guide to the literature. Springer Science & Business Media.

  51. Madoni, P., 1984. Estimation of the size of freshwater ciliate populations by a sub-sampling technique. Hydrobiologia 111(3): 201–206.

    Google Scholar 

  52. Maguire Jr., B., 1959. Passive overland transport of small aquatic organisms. Ecology 40: 312.

    Google Scholar 

  53. Maguire Jr., B., 1963. The passive dispersal of small aquatic organisms and their colonization of isolated bodies of water. Ecology 33: 161–185.

    Google Scholar 

  54. McGrady-Steed, J. & P. J. Morin, 2000. Biodiversity, density compensation, and the dynamics of populations and functional groups. Ecology 81: 361–373.

    Google Scholar 

  55. Messikommer, E. L., 1943. Untersuchungen über die passive Verbreitung der Algen. Zeitschrift für Hydrologie 9: 310–316.

    Google Scholar 

  56. Morais Júnior, C. S. D., L. P. Diniz, S. L. D. Nascimento Filho, M. T. Brito, A. D. O. Silva, G. J. Moura & M. D. Melo Júnior, 2019. Zooplankton associated with phytotelms and treefrogs in a neotropical forest Iheringia. Série Zoologia 109: e2019020.

    Google Scholar 

  57. Mouquet, N. & M. Loreau, 2003. Community patterns in source sink metacommunities. The American Naturalist 162: 544–557.

    PubMed  Google Scholar 

  58. Naselli-Flores, L. & J. Padisák, 2016. Blowing in the wind: how many roads can a phytoplanktont walk down? A synthesis on phytoplankton biogeography and spatial processes. Hydrobiologia 764: 303–313.

    Google Scholar 

  59. Negreiros, O. P., B. T. Segovia, F. M. Lansac-Tôha, B. R. Meira, P. R. B. Buosi, A. F. Cabral & L. F. M. Velho, 2017. Structure and dynamic of planktonic ciliate community in a large Neotropical river: the relevance of the pluviosity and tributaries in the biodiversity maintenance. Acta Limnologica Brasiliensia 29: 1–17.

    Google Scholar 

  60. Oksanen, J., F. G. Blanchet, M. Friendly, R. Kindt, P. Legendre, D. Mcglinn & H. Wagner, 2017. Vegan: Community Ecology Package. R package version 2.4 × 2. https://CRAN.R-project.org/package=vegan.

  61. Padial, A. A., F. Ceschin, S. A. J. Declerck, L. De Meester & C. C. Bonecker, 2014. Dispersal ability determines the role of environmental, spatial and temporal drivers of metacommunity structure. PLoS ONE 9(10): e111227.

    PubMed  PubMed Central  Google Scholar 

  62. Panov, V. E. & C. Caceres, 2007. Role of diapause in dispersal of aquatic invertebrates. Springer 87: 195.

    Google Scholar 

  63. Parsons, W. M., H. E. Schlichting & K. W. Stewart, 1966. In-flight transport of Algae and Protozoa by selected Odonata. Transactions of the American Microscopical Society 85: 520–527.

    Google Scholar 

  64. Pauleto, G. M., F. R. D. Oliveira, B. T. Segovia, B. R. Meira, F. Lansac-Tôha, P. R. B. Buosi & L. F. M. Velho, 2017. Intra-annual variation in planktonic ciliate species composition (Protista: Ciliophora) in different strata in a shallow floodplain lake. Acta Limnologica Brasiliensia 29: e107.

    Google Scholar 

  65. Petchey, O. L., T. J. Casey, L. Jiang, P. T. Mc Phearsonm & J. Price, 2002. Species richness, environmental fluctuations, and temporal change in total community biomass. Oikos 99: 231–240.

    Google Scholar 

  66. R Core Team, 2017. R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria.

    Google Scholar 

  67. Railkin, A. I., 1995. Heterotrophic flagellates on artificial substrates in the White Sea. Cytology 37: 951–957.

    Google Scholar 

  68. Rocha, M. P., L. M. Bini, T. Siqueira, J. Hjort, M. Grönroos, M. Lindholm, S. M. Karjalainen & J. Heino, 2018. Predicting occupancy and abundance by niche position, niche breadth and body size in stream organisms. Oecologia 186: 205–216.

    PubMed  Google Scholar 

  69. Rogers, D. C., 2014. Larger hatching fractions in avian dispersed anostracan eggs (Branchiopoda). Journal of Crustacean Biology 34(135–143): 2014.

    Google Scholar 

  70. Rosa, J., R. Campos, K. Martens & J. Higuti, 2020. Spatial variation of ostracod (Crustacea, Ostracoda) egg banks in temporary lakes of a tropical flood plain. Marine and Freshwater Research. https://doi.org/10.1071/MF19081.

    Article  Google Scholar 

  71. Rundle, S. D., D. T. Bilton & A. Foggo, 2007. By wind, wings or water: body size, dispersal and range size in aquatic invertebrates. In Hildrew, A. G., D. G. Raffaelli, R. Edmonds-Brown. Body size: the structure and function of aquatic ecosystems. Ecological Reviews, Cambridge University Press, Cambridge, 186–209.

  72. Russo, S. E., S. Portnoy & C. K. Augspurger, 2006. Incorporating animal behavior into seed dispersal models: implications for seed shadows. Ecology 87: 3160–3174.

    PubMed  Google Scholar 

  73. Sabagh, L. T., R. J. P. Dias, C. W. Branco & C. F. Rocha, 2011. News records of phoresy and hyperphoresy among treefrogs, ostracods, and ciliates in bromeliad of Atlantic forest. Biodiversity and Conservation 20(8): 1837.

    Google Scholar 

  74. Segovia, B. T., F. M. Lansac-Toha, B. R. de Meira, A. F. Cabral, F. A. Lansac-Tôha & L. F. M. Velho, 2016. Anthropogenic disturbances influencing ciliate functional feeding groups in impacted tropical streams. Environmental Science and Pollution Research Environmental Science and Pollution Research 23: 20003–20016.

    CAS  PubMed  Google Scholar 

  75. Segovia, B. T., J. D. Dias, A. F. Cabral, B. R. Meira, F. M. Lansac-Tôha, F. A. Lansac-Tôha, L. M. Bini & L. F. M. Velho, 2017. Common and rare taxa of planktonic ciliates: influence of flood events and biogeographic patterns in Neotropical floodplains. Microbial Ecology 74(3): 522–533.

    PubMed  Google Scholar 

  76. Shurin, J. B. & E. G. Allen, 2001. Effects of competition, predation and dispersal on species richness at local and regional scales. The American Naturalist 158: 624–637.

    CAS  PubMed  Google Scholar 

  77. Soininen, J., 2016. Spatial structure in ecological communities a quantitative analysis. Oikos 125: 160–166.

    Google Scholar 

  78. Stewart, K. W. & H. E. Schlichting, 1966. Dispersal of algae and protozoa by selected aquatic insects. The Journal of Ecology 54: 551–562.

    Google Scholar 

  79. Tonn, W. M. & J. J. Magnuson, 1982. Patterns in the species composition and richness of fish assemblages in northern Wisconsin lakes. Ecology 63: 1149–1166.

    Google Scholar 

  80. Tulloch, J. B. G., 1929. Dragonfly migration. Entomologist 62: 213.

    Google Scholar 

  81. Vanschoenwinkel, B., A. Waterkeyn, T. Vandecaetsbeek, O. Pineau, P. Grillas & L. Brendonck, 2008a. Dispersal of freshwater invertebrates by large terrestrial mammals: a case study with wild boar (Sus scrofa) in Mediterranean wetlands. Freshwater Biology 53: 2264–2273.

    Google Scholar 

  82. Vanschoenwinkel, B., S. Gielen, H. Vandewaerde, M. Seaman & L. Brendonck, 2008b. Relative importance of different dispersal vectors for small aquatic invertebrates in a rock pool metacommunity. Ecography 31: 567–577.

    Google Scholar 

  83. Velho, L. F. M., D. G. Pereira, T. A. Pagioro, V. D. Santos, M. C. Z. Perenha & F. A. Lansac-Tôha, 2005. Abundance, biomass and size structure of planktonic ciliates in reservoirs with distinct trophic states. Acta Limnologica Brasiliensia 17(4): 361–371.

    Google Scholar 

  84. Velho, L. F. M., F. M. Lansac-Tôha, P. R. B. Buosi, B. R. Meira, A. F. Cabral & F. A. Lansac-Tôha, 2013. Structure of planktonic ciliates community (Protist, Ciliophora) from an urban lake of southern Brazil. Acta Scientiarum: Biological Sciences 35: 531–539.

    Google Scholar 

  85. Weisse, T., 2008. Distribution and diversity of aquatic protists: an evolutionary and ecological perspective. Biodiversiry and Conservation 17(2): 243–259.

    Google Scholar 

  86. Weisse, T., 2014. Ciliates and the rare biosphere-community ecology and population dynamics. Journal of Eukaryotic Microbiology 61(4): 419–433.

    Google Scholar 

  87. Winegardner, A. K., B. K. Jones, I. S. Y. Ng, T. Siqueira & K. Cottenie, 2012. The terminology of metacommunity ecology. Trends in Ecology and Evolution 27: 253–254.

    PubMed  Google Scholar 

  88. Xu, M. Q., H. Chao, D. G. Deng, W. S. Feng & H. Xu, 2005. The temporal and spatial distribution, composition and abundance of Protozoa in Chaohu Lake, China: relationship with eutrophication. European Journal of Prostistology 41: 183–192.

    Google Scholar 

  89. Zenni, R. D. & D. Simberloff, 2013. Number of source populations as a potential driver of pine invasions in Brazil. Biological Invasions 15: 1623–1639.

    Google Scholar 

  90. Zhong, X., G. Xu & H. Xu, 2017. An approach to analysis of colonization dynamics in community functioning of protozoa for bioassessment of marine pollution. Ecological Indicators 78: 526–530.

    Google Scholar 

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Acknowledgements

We thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for financial support and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), for granting the scholarship and to the Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura (Nupelia) and the Postgraduate Program in Ecology of Continental Aquatic Environments (PEA) of the Universidade Estadual de Maringá (UEM), for the support and infrastructure.

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Cochak, C., de Oliveira, F.R., Lansac-Tôha, F.M. et al. Relative contributions of disparate animal vectors to the development of freshwater ciliate communities. Hydrobiologia 848, 1121–1135 (2021). https://doi.org/10.1007/s10750-021-04518-9

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Keywords

  • Microorganisms
  • Protists
  • Aquatic colonization
  • Ecological succession