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Ecological interactions between invasive and native fouling species in the reservoir of a hydroelectric plant

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Abstract

In this study, we investigate the main ecological interactions between fouling aquatic organisms (both invasive and native) present in the reservoir of the Governador José Richa hydroelectric plant, located in southern Brazil, and to identify the most suitable period for the interruption of machinery operation for cleaning and maintenance of the hydraulic systems of this plant. A total of 32 experimental plates were fixed to a metallic structure positioned close to the plant's water intake. Three species of invasive fouling were identified in our samples (Limnoperna fortunei [Mollusca], Cordylophora sp., and Hydra sp. [Cnidaria]) and six native taxa belonging to the phyla Protozoa, Ciliophora, Amoebozoa, and Arthropoda. Spring and summer were the seasons with the highest fouling rates, as well as densities of fouling organisms. The highest levels of diversity were recorded during the colder seasons. Several interactions between the organisms were identified, such as mutualism, commensalism, competition, epibiosis, cannibalism, and predation. The data obtained suggest that, from the biological point of view, the most suitable period for machine shutdown destined for the removal of biological fouling in the hydraulic systems of the studied plant is between the end of spring and the beginning of summer.

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Data availability

Raw data used in our analyses are available from the authors upon request.

References

  • Abarzua, S. & S. Jakubowski, 1995. Biotechnological investigation for the prevention of biofouling. I. Biological and biochemical principles for the prevention of biofouling. Marine Ecology Progress Series 123:301-312.

    Article  CAS  Google Scholar 

  • Ackerman, J. D., B. Sim, S. J. Nichols & R. Claudi, 1994. A review of the early life history of zebra mussels (Dreissena polymorpha): comparisons with marine bivalves. Canadian Journal of Zoology 72(7):1169-1179.

    Article  Google Scholar 

  • Albano, M. J. & S. M. Obenat, 2019. Fouling assemblages of native, non-indigenous and cryptogenic species on artificial structures, depths and temporal variation. Journal of Sea Research 144:1-15.

    Article  Google Scholar 

  • Aneel, A. N. E. E., 2016. Plano de Dados Abertos, Informações Gerenciais – Tópico: Geração.

  • Armour, A., J. Tsou & P., 1993. Wiancko, Zebra mussels: the industrial impact. In: Proceedings of the 3rd international zebra mussel conference, Toronto.

  • Belz, C. E., G. Darrigran, N. Bonel & O. S. Mäder Netto, 2010. Density, Recruitment, and Shell Growth of Limnoperna fortunei (Mytilidae), an lnvasive Mussel in Tropical South America. Journal of Freshwater Ecology 25(2):227-233.

    Article  Google Scholar 

  • Berntsson, K. M. & P. R. Jonsson, 2003. Temporal and spatial patterns in recruitment and succession of a temperate marine fouling assemblage: a comparison of static panels and boat hulls during the boating season. Biofueling 19(3):187-195.

    Article  CAS  Google Scholar 

  • Boltovskoy, D., 2015. Limnoperna fortunei: the ecology, distribution and control of a swiftly spreading invasive fouling mussel, vol 10. Springer.

    Book  Google Scholar 

  • Boltovskoy, D., 2017. Traits and impacts of invasive species: Myths and evidences from the perspective of introduced freshwater mussels. Aquatic Ecosystem Health & Management 20(4):334-343.

    Article  Google Scholar 

  • Boltovskoy, D. & N. Correa, 2015. Ecosystem impacts of the invasive bivalve Limnoperna fortunei (golden mussel) in South America. Hydrobiologia 746(1):81-95.

    Article  CAS  Google Scholar 

  • Boltovskoy, D., N. Correa, D. Cataldo & F. Sylvester, 2006. Dispersion and Ecological Impact of the Invasive Freshwater Bivalve Limnoperna fortunei in the Río de la Plata Watershed and Beyond. Springer.

    Article  Google Scholar 

  • Boltovskoy, D., F. Sylvester, A. Otaegui, V. Leites & D. H. Cataldo, 2009. Environmental modulation of reproductive activity of the invasive mussel Limnoperna fortunei: implications for antifouling strategies. Austral Ecology 34(7):719-730.

    Article  Google Scholar 

  • Boltovskoy, D., B. Morton, N. Correa, D. Cataldo, C. Damborenea, P. E. Penchaszadeh & F. Sylvester, 2015a. Reproductive output and seasonality of Limnoperna fortunei. In Limnoperna Fortunei. Springer: 77–103.

  • Boltovskoy, D., M. Xu & D. Nakano, 2015b. Impacts of Limnoperna fortunei on man-made structures and control strategies: general overview. In Limnoperna fortunei :375–393.

  • Booy, O., L. Cornwell, D. Parrott, M. Sutton-Croft & F. Williams, 2017. Impact of biological invasions on infrastructure. In Impact of Biological Invasions on Ecosystem Services. Springer: 235–247.

  • Borges, P. D., 2013. Aspectos do ciclo de vida da espécie invasora Cordylophora caspia (Cnidaria) no reservatório da Usina Hidrelétrica Governador José Richa, Rio Iguaçu, Paraná.

  • Borges, P. D., 2014. Limnoperna fortunei (Bivalvia: Mytilidae) e o setor elétrico brasileiro: distribuição, impactos, estudo de caso da dispersão no Rio Iguaçu e teste de protocolo de uso de larvas na caracterização do perfil genético de populações.

  • Borges, P. D., S. Ludwig & W. A. Boeger, 2017. Testing hypotheses on the origin and dispersion of Limnoperna fortunei (Bivalvia, Mytilidae) in the Iguassu River (Paraná, Brazil): molecular markers in larvae and adults. Limnology 18(1):31-39.

    Article  CAS  Google Scholar 

  • Burlakova, L. E., A. Y. Karatayev & V. A. Karatayev, 2012. Invasive mussels induce community changes by increasing habitat complexity. Hydrobiologia 685(1):121-134.

    Article  Google Scholar 

  • Callow, M. E., 1993. A review of fouling in freshwaters. Biofouling 7(4):313-327.

    Article  CAS  Google Scholar 

  • Canzi, C., L. Bortoluzzi & D. Rodriguez Fernandez, 2005. Ocorrência e situação atual do mexilhão dourado (Limnoperna fortunei) no reservatório da central hidrelétrica de Itaipu. I Simpósio Brasileiro sobre Espécies Exóticas Invasoras, Brasilia (Brazil).

  • Cataldo, R., 2001. 'Musseling'in on the Ninth District economy. Fedgazette 13(1):15-15.

    Google Scholar 

  • Cataldo, D. & D. Boltovskoy, 1999. Population dynamics of Corbicula fluminea (Bivalvia) in the Paraná River Delta. Hydrobiologia 153–163.

  • Cataldo, D., D. Boltovskoy & M. Pose, 2003. Toxicity of chlorine and three nonoxidizing molluscicides to the pest mussel Limnoperna fortunei. Journal‐American Water Works Association 95(1):66-78.

    Article  CAS  Google Scholar 

  • Characklis, W. G., 1981. Bioengineering report: fouling biofilm development: a process analysis. Biotechnology and Bioengineering 23(9):1923-1960.

    Article  CAS  Google Scholar 

  • Chen, X., X. Xiong, X. Jiang, H. Shi & C. Wu, 2019. Sinking of floating plastic debris caused by biofilm development in a freshwater lake. Chemosphere 222:856-864.

    Article  CAS  PubMed  Google Scholar 

  • Cifuentes, M., I. Krueger, C. P. Dumont, M. Lenz & M. Thiel, 2010. Does primary colonization or community structure determine the succession of fouling communities? Journal of Experimental Marine Biology and Ecology 395(1-2):10-20.

    Article  Google Scholar 

  • Coetser, S. & T. E. Cloete, 2005. Biofouling and biocorrosion in industrial water systems. Critical reviews in microbiology 31(4):213-232.

    Article  CAS  PubMed  Google Scholar 

  • Cummings, K. S. & D. L. Graf, 2010. Mollusca: bivalvia. In Ecology and Classification of North American Freshwater Invertebrates. Elsevier: 309–384.

  • Damborenea, C. & P. Penchaszadeh, 2006. Biología reproductiva de Limnoperna fortunei. Bio-invasión del mejillón dorado en el continente americano:71–84.

  • Danrigran, G. & I. E. De Drago, 2000. Invasion of the exotic freshwater mussel Limnopema fortunei (Dunker, 1857)(Bivalvia: Mytilidae) in South America. The Nautilus 114:69-73.

    Google Scholar 

  • Darrigran, G., 2002. Potential impact of filter-feeding invaders on temperate inland freshwater environments. Biological invasions 4(1-2):145-156.

    Article  Google Scholar 

  • Darrigran, G. & C. Damborenea, 2011. Ecosystem engineering impact of Limnoperna fortunei in South America. Zoological science 28(1):1-8.

    Article  PubMed  Google Scholar 

  • Darrigran, G., S. M. Martin, B. Gullo & L. Armendariz, 1998. Macroinvertebrates associated with Limnoperna fortunei (Dunker, 1857)(Bivalvia, Mytilidae) in Rio de la Plata, Argentina. Hydrobiologia 367(1-3):223-230.

    Article  Google Scholar 

  • Darrigran, G. & C. Damborenea, 2006. Bio-invasión del mejillón dorado en el continente americano. Editorial de la Universidad Nacional de La Plata (EDULP).

  • David, P., E. Thebault, O. Anneville, P.-F. Duyck, E. Chapuis & N. Loeuille, 2017. Impacts of invasive species on food webs: a review of empirical data. In Advances in Ecological Research, Vol 56. Elsevier: 1–60.

  • Dehmordi, L. M., L. Karami, N. Safarpor & B. Alesadi, 2011. Taxonomic identification and distribution of biofouling organisms in Deilam port in Iran. Journal of Ecology and the Natural Environment 3(14):441-445.

    Google Scholar 

  • Deserti, M. I., K. S. Esquius, A. H. Escalante & F. H. Acuña, 2017. Trophic ecology and diet of Hydra vulgaris (Cnidaria; Hydrozoa). Animal Biology 67(3-4):287-300.

    Article  Google Scholar 

  • Emery‐Butcher, H. E., S. J. Beatty & B. J. Robson, 2020. The impacts of invasive ecosystem engineers in freshwaters: A review. Freshwater Biology.

    Article  Google Scholar 

  • Farhat, N., L. Javier, M. Van Loosdrecht, J. Kruithof & J. S. Vrouwenvelder, 2019. Role of feed water biodegradable substrate concentration on biofouling: Biofilm characteristics, membrane performance and cleanability. Water research 150:1-11.

    Article  CAS  PubMed  Google Scholar 

  • Fernandez, M. O. & S. A. Navarrete, 2015. A comparison of temporal turnover of species from benthic cnidarian assemblages in tropical and subtropical harbours. Taylor & Francis.

    Article  Google Scholar 

  • Flemming, H.-C., 2002. Biofouling in water systems–cases, causes and countermeasures. Applied microbiology and biotechnology 59(6):629-640.

    Article  CAS  PubMed  Google Scholar 

  • Flemming, H. C., 2011. Microbial biofouling: unsolved problems, insufficient approaches, and possible solutions. Springer.

  • Flemming, H.-C. & E. Cloete, 2010. Environmental impact of controlling biofouling and biocorrosion in cooling water systems. In Operational and Environmental Consequences of Large Industrial Cooling Water Systems :365–380.

  • Folino-Rorem, N. C., 2000. The freshwater expansion and classification of the colonial hydroid Cordylophora (Phylum Cnidaria, Class Hydrozoa). . In Pederson, J. (ed.) Marine Bioinvasions: Proceedings of the First National Conference. Massachusetts Institute of Technology Sea Grant College Program, Cambridge MA.

  • Folino-Rorem, N. C., J. Stoeckel, E. Thorn & L. Page, 2006. Effects of artificial filamentous substrate on zebra mussel (Dreissena polymorpha) settlement. Biological invasions 8(1):89-96.

    Article  Google Scholar 

  • Fortunato, L., S. Jeong & T. Leiknes, 2017. Time-resolved monitoring of biofouling development on a flat sheet membrane using optical coherence tomography. Scientific reports 7(1):1-9.

    Article  CAS  Google Scholar 

  • Frota, M. N., E. M. Ticona, A. V. Neves, R. P. Marques, S. L. Braga & G. Valente, 2014. On-line cleaning technique for mitigation of biofouling in heat exchangers: A case study of a hydroelectric power plant in Brazil. Experimental thermal and fluid science 53:197-206.

    Article  Google Scholar 

  • Gaino, T. L. E., 2005. Competition between the freshwater sponge Ephydatia fluviatilis and the zebra mussel Dreissena polymorpha in Lake Trasimeno (central Italy). Italian Journal of Zoology 72(1):27-32.

    Article  Google Scholar 

  • Gallardo, B. & D. C. Aldridge, 2018. Inter-basin water transfers and the expansion of aquatic invasive species. Elsevier.

    Article  CAS  PubMed  Google Scholar 

  • Green, P. T., D. J. O'Dowd, K. L. Abbott, M. Jeffery, K. Retallick & R. Mac Nally, 2011. Invasional meltdown: invader–invader mutualism facilitates a secondary invasion. Ecology 92(9):1758-1768.

    Article  PubMed  Google Scholar 

  • Grohmann, P. A., 2008a. Bioencrustration in the turbine cooling system at the funil hydroelectric power plant, Itatiaia, Rio de Janeiro, Brazil. Naturalia.

  • Grohmann, P. A., 2008b. Bioincrustation caused by a hydroid species in the turbine cooling system at the Funil hydroelectric power plant. Naturalia 31:16-21.

    Google Scholar 

  • Grohmann, P. A., 2008c. Bioincrustation caused by a hydroid species in the turbine cooling system at the funil hydroelectric power plant, Itatiaia Naturalia, Rio Claro 31:16-21.

    Google Scholar 

  • Gutiérrez, J. L., C. G. Jones, D. L. Strayer & O. O. Iribarne, 2003. Mollusks as ecosystem engineers: the role of shell production in aquatic habitats. Oikos 101(1):79-90.

    Article  Google Scholar 

  • Hacker, S. a. D. & S. D. Gaines, 1997. Some implications of direct positive interactions for community species diversity. Wiley Online Library.

    Article  Google Scholar 

  • Hobmayer, B., M. Jenewein, D. Eder, M.-K. Eder, S. Glasauer, S. Gufler, M. Hartl & W. Salvenmoser, 2012. Stemness in Hydra-a current perspective. International Journal of Developmental Biology 56(6-7-8):509-517.

    Article  CAS  PubMed  Google Scholar 

  • Jackson, M. C., 2015. Interactions among multiple invasive animals. Ecology 96(8):2035-2041.

    Article  CAS  PubMed  Google Scholar 

  • Jernelöv, A., 2017. The long‐term fate of invasive species. Aliens forever or integrated immigrants with time.

    Book  Google Scholar 

  • Jones, E. I., J. L. Bronstein & R. Ferrière, 2012. The fundamental role of competition in the ecology and evolution of mutualisms. Wiley Online Library.

    Article  PubMed  Google Scholar 

  • Karatayev, A. Y., L. E. Burlakova & D. K. Padilla, 2005. Contrasting distribution and impacts of two freshwater exotic suspension feeders, Dreissena polymorpha and Corbicula fluminea. In The comparative roles of suspension-feeders in ecosystems. Springer: 239–262.

  • Karatayev, A. Y., D. K. Padilla, D. Minchin, D. Boltovskoy & L. E. Burlakova, 2007. Changes in global economies and trade: the potential spread of exotic freshwater bivalves. Springer.

    Article  Google Scholar 

  • Kéfi, S., M. Holmgren & M. Scheffer, 2016. When can positive interactions cause alternative stable states in ecosystems? Functional Ecology 30(1):88-97.

    Article  Google Scholar 

  • Kuebbing, S. E. & M. A. Nuñez, 2015. Negative, neutral, and positive interactions among nonnative plants: patterns, processes, and management implications. Global Change Biology 21(2):926-934.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Latombe, G., P. Pyšek, J. M. Jeschke, T. M. Blackburn, S. Bacher, C. Capinha, M. J. Costello, M. Fernández, R. D. Gregory & D. Hobern, 2017. A vision for global monitoring of biological invasions. Biological Conservation 213:295-308.

    Article  Google Scholar 

  • Lauer, T. E., D. K. Barnes, A. Ricciardi & A. Spacie, 1999. Evidence of recruitment inhibition of zebra mussels (Dreissena polymorpha) by a freshwater bryozoan (Lophopodella carteri). Journal of the North American Benthological Society 18(3):406-413.

    Article  Google Scholar 

  • Liu, W., M. Xu, J. Zhang & T. Zhang, 2020. Survival and attachment of biofouling freshwater mussel (Limnoperna fortunei) to environmental conditions: potential implications in its invasion, infection and biofouling control. Limnology:1-11.

    Article  Google Scholar 

  • Ludwig, S., M. K. Tschá, R. Patella, A. J. Oliveira & W. A. Boeger, 2014. Looking for a needle in a haystack: molecular detection of larvae of invasive Corbicula clams. Management of biological Invasions 5(2):143.

    Article  Google Scholar 

  • MacIsaac, H. J., 1996. Potential abiotic and biotic impacts of zebra mussels on the inland waters of North America. American zoologist 36(3):287-299.

    Article  Google Scholar 

  • Maclsaac, H. J., W. G. Sprules & J. Leach, 1991. Ingestion of small-bodied zooplankton by zebra mussels (Dreissena polymorpha): can cannibalism on larvae influence population dynamics? Canadian journal of fisheries and aquatic sciences 48(11):2051-2060.

    Article  Google Scholar 

  • Magara, Y., Y. Matsui, Y. Goto & A. Yuasa, 2001. Invasion of the non-indigenous nuisance mussel, Limnoperna fortunei, into water supply facilities in Japan. Journal of Water Supply: Research and Technology – AQUA 50(3):113-124.

    Article  Google Scholar 

  • Mansur, M. C. D., C. P. Santos, D. Pereira, P. E. A. Bergonci & C. T. Callil, 2016. Moluscos límnicos - bivalves.

  • Martin, R. A. M., D. V. Obrecht, G. A. Stoner, R. A. O'Hearn, S. W. Lanning & W. R. Mabee, 2016. First record of occurrence of the invasive hydroid Cordylophora caspia (Cnidaria: Hydrozoa) in Missouri. The Southwestern Naturalist 61(3):260-264.

    Article  Google Scholar 

  • Martín-Rodríguez, A. J., J. M. Babarro, F. Lahoz, M. Sansón, V. S. Martín, M. Norte & J. J. Fernández, 2015. From broad-spectrum biocides to quorum sensing disruptors and mussel repellents: Antifouling profile of alkyl triphenylphosphonium salts. PLoS One 10(4).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Masi, B. P., I. Zalmon & R. Coutinho, 2016. Effects of structural factors on upwelling fouling community, Southeast Brazil. Brazilian Journal of Oceanography 64(4):387-400.

    Article  Google Scholar 

  • McPherson, B. F., W. H. Sonntag & M. Sabanskas, 1984. Fouling community of the Loxahatchee River estuary, Florida, 1980–81. Estuaries 7(2):149-157.

    Article  Google Scholar 

  • Melo, L. & T. Bott, 1997. Biofouling in water systems. Experimental thermal and fluid science 14(4):375-381.

    Article  CAS  Google Scholar 

  • Mieczan, T. & N. Rudyk-Leuska, 2019. Seasonal dynamics of the epibiont food web on Unio tumidus (Philipsson, 1788) in a eutrophic reservoir. European journal of protistology 69:138-150.

    Article  PubMed  Google Scholar 

  • Molina, F. R., S. B. J. de Paggi & J. C. Paggi, 2015. Impacts of Limnoperna fortunei on Zooplankton. Limnoperna Fortunei. Springer: 177–190.

  • Molloy, D. P., A. Y. Karatayev, L. E. Burlakova, D. P. Kurandina & F. Laruelle, 1997. Natural enemies of zebra mussels: predators, parasites, and ecological competitors. Taylor & Francis.

    Article  Google Scholar 

  • Morton, B., 1977. Freshwater fouling bivalves. In: Symposium, held at Texas Christian University, Fort Worth, Texas, Texas Christian University.

  • Nakano, D. & D. L. Strayer, 2014. Biofouling animals in fresh water: biology, impacts, and ecosystem engineering. Frontiers in Ecology and the Environment 12(3):167-175.

    Article  Google Scholar 

  • Nakano, D., T. Kobayashi, N. Endo & I. Sakaguchi, 2011. Growth rate and settlement of Limnoperna fortunei in a temperate reservoir. Journal of Molluscan Studies 77(2):142-148.

    Article  Google Scholar 

  • Navarrete, S. A., M. Parragué, N. Osiadacz, F. Rojas, J. Bonicelli, M. Fernández, C. Arboleda-Baena, A. Perez-Matus & R. Finke, 2019. Abundance, composition and succession of sessile subtidal assemblages in high wave-energy environments of Central Chile: Temporal and depth variation. Journal of experimental marine biology and ecology 512:51-62.

    Article  Google Scholar 

  • Nelson, N. M., 2019. Enumeration of potential economic costs of dreissenid mussel infestation in montana.

  • Olenin, S. & E. Leppäkoski, 1999. Non-native animals in the Baltic Sea: alteration of benthic habitats in coastal inlets and lagoons. Hydrobiologia 393:233-243.

    Article  Google Scholar 

  • Oliveira, M. D., M. C. S. Campos, E. M. Paolucci, M. C. D. Mansur & S. K. Hamilton, 2015. Colonization and spread of Limnoperna fortunei in South America. In Limnoperna Fortunei. Springer: 333–355.

  • Oreska, M. P. & D. C. Aldridge, 2011. Estimating the financial costs of freshwater invasive species in Great Britain: a standardized approach to invasive species costing. Biological Invasions 13(2):305-319.

    Article  Google Scholar 

  • Pamplin, P., T. Almeida & O. Rocha, 2006. Composition and distribution of benthic macroinvertebrates in Americana Reservoir(SP, Brazil). Acta Limnologica Brasiliensia 18(2):121-132.

    Google Scholar 

  • Papadopulos, F., M. Spinelli, S. Valente, L. Foroni, C. Orrico, F. Alviano & G. Pasquinelli, 2007. Common tasks in microscopic and ultrastructural image analysis using ImageJ. Ultrastructural pathology 31(6):401-407.

    Article  PubMed  Google Scholar 

  • Patil, J. S. & A. C. Anil, 2005. Biofilm diatom community structure: influence of temporal and substratum variability. Biofouling 21(3-4):189-206.

    Article  CAS  PubMed  Google Scholar 

  • Pielou, E. C., 1966. Shannon's formula as a measure of specific diversity: its use and misuse. The American Naturalist 100(914):463-465.

    Article  Google Scholar 

  • Pimentel, D., S. McNair, J. Janecka, J. Wightman, C. Simmonds, C. O’connell, E. Wong, L. Russel, J. Zern & T. Aquino, 2001. Economic and environmental threats of alien plant, animal, and microbe invasions. Agriculture, Ecosystems & Environment 84(1):1-20.

    Article  Google Scholar 

  • Pinto-Coelho, R. M., 2004. Métodos de coleta, preservação, contagem e determinação de biomassa em zooplâncton de aguas continentais. In Bicudo, C. E. (ed.) Amostragem em limnologia: 149–167.

  • Poloczanska, E., A. B.-. Biofouling, U. 2010 & A. Butler, 2010. Biofouling and climate change. booksgooglecom.

  • Portella, K. F., A. Joukoski, A. S. d. Silva, N. M. Brassac & C. E. Belz, 2009. Biofouling and chemical biodeterioration in hydroeletric power plant portland cement mortar. Quimica Nova 32(4):1047-1051.

    Article  CAS  Google Scholar 

  • Pörtner, H.-O., 2002. Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 132(4):739-761.

    Article  Google Scholar 

  • Pu, H., G.-l. Ding, X.-k. Ma, H.-t. Hu & Y.-f. Gao, 2009. Effects of biofouling on air-side heat transfer and pressure drop for finned tube heat exchangers. International journal of refrigeration 32(5):1032-1040.

    Article  CAS  Google Scholar 

  • Pucherelli, S. F., J. Keele, Y. J. Passamaneck, J. R. Beaver & T. R. Renicker, 2016. Range expansion of the invasive hydroid, Cordylophora caspia (Pallas, 1771), in Colorado River reservoirs. BioInvasions Records 5(3):133-137.

    Article  Google Scholar 

  • Pucherelli, S. F., R. Claudi & T. Prescott, 2018. Control of biofouling in hydropower cooling systems using HOD ultraviolet light. Management of Biological Invasions 9(4):451.

    Article  Google Scholar 

  • Rajagopal, S. & G. van der Velde, 2012. Invasive species: implications for industrial cooling water systems. In Operational and Environmental Consequences of Large Industrial Cooling Water Systems. Springer, Boston: 127–162.

  • Ricciardi, A., 2005. Facilitation and Synergistic Interactions Between Introduced Aquatic Species Scope-Scientific Committeeon Problems of the Environment Intertnational Council of Scientific Unions, Vol. 63: 162.

  • Ricciardi, A., 2001. Facilitative interactions among aquatic invaders: is an" invasional meltdown" occurring in the Great Lakes? Canadian journal of fisheries and aquatic sciences 58(12):2513-2525.

    Article  Google Scholar 

  • Ricciardi, A., 2015. Ecology of Invasive Alien Invertebrates Thorp and Covich's Freshwater Invertebrates (Fourth Edition). Elsevier: 83–91.

  • Ricciardi, A. & H. J. MacIsaac, 2000. Recent mass invasion of the North American Great Lakes by Ponto–Caspian species. Trends in Ecology & Evolution 15(2):62-65.

    Article  CAS  Google Scholar 

  • Ricciardi, A. & H. J. MacIsaac, 2008. The book that began invasion ecology. Nature 452(7183):34-34.

    Article  CAS  Google Scholar 

  • Ricciardi, A. & H. J. MacIsaac, 2011. Impacts of biological invasions on freshwater ecosystems. Fifty years of invasion ecology: the legacy of Charles Elton 1:211-224.

    Google Scholar 

  • Ricciardi, A. & H. M. Reiswig, 1994. Taxonomy, distribution, and ecology of the freshwater bryozoans (Ectoprocta) of eastern Canada. Canadian Journal of Zoology 72(2):339-359.

    Article  Google Scholar 

  • Ricciardi, A., F. G. Whoriskey & J. Rasmussen, 1996. Impact of the invasion on native unionid bivalves in the upper St. Lawrence River. Canadian Journal of Fisheries and Aquatic Sciences 53:1434-1444. https://doi.org/10.1139/cjfas-53-6-1434.

    Article  Google Scholar 

  • Rodrigues, L. C., N. R. Simões, V. M. Bovo-Scomparin, S. Jati, N. F. Santana, M. C. Roberto & S. Train, 2015. Phytoplankton alpha diversity as an indicator of environmental changes in a neotropical floodplain. Ecological Indicators 48:334-341.

    Article  CAS  Google Scholar 

  • Rodrigues, M., T. Ostermann, L. Kremeser, H. Lindner, C. Beisel, E. Berezikov, B. Hobmayer & P. Ladurner, 2016. Profiling of adhesive-related genes in the freshwater cnidarian Hydra magnipapillata by transcriptomics and proteomics. Biofouling 32(9):1115-1129.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodriguez, L. F., 2006. Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur. Springer.

    Article  Google Scholar 

  • Rolla, M., S. Consuegra, E. Carrington, D. Hall & C. G. de Leaniz, 2019. Experimental evidence of invasion facilitation in the zebra mussel-killer shrimp system. bioRxiv:626432.

  • Sardiña, P., D. Cataldo & D. Boltovskoy, 2008. The effects of the invasive mussel, Limnoperna fortunei, on associated fauna in South American freshwaters: importance of physical structure and food supply. ingentaconnectcom.

  • Schneider, C. A., W. S. Rasband & K. W. Eliceiri, 2012. NIH Image to ImageJ: 25 years of image analysis. Nature methods 9(7):671.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silknetter, S., R. P. Creed, B. L. Brown, E. A. Frimpong, J. Skelton & B. K. Peoples, 2019. Positive biotic interactions in freshwaters: A review and research directive. Freshwater Biology doi:https://doi.org/10.1111/fwb.13476.

    Article  Google Scholar 

  • Simberloff, D., 2006. Invasional meltdown 6 years later: important phenomenon, unfortunate metaphor, or both? Ecology Letters 9(8):912-919.

    Article  PubMed  Google Scholar 

  • Simberloff, D. & J. R. Vitule, 2014. A call for an end to calls for the end of invasion biology. Oikos 123(4):408-413.

    Article  Google Scholar 

  • Simberloff, D. & B. Von Holle, 1999. Positive interactions of nonindigenous species: invasional meltdown? Biological invasions 1(1):21-32.

    Article  Google Scholar 

  • Simberloff, D. & A. Ricciardi, 2020. I n Chap. 3, Elton invoked the notion of a homogenized world owing. In The Ecology of Invasions by Animals and Plants :53.

  • Singh, M. P., P. Singh, H.-B. Li, Q.-Q. Song & R. K. Singh, 2020. Microbial biofilms: Development, structure, and their social assemblage for beneficial applications. In New and Future Developments in Microbial Biotechnology and Bioengineering: Microbial Biofilms. Elsevier: 125–138.

  • Spaccesi, F. & C. A. Rodrigues, 2012. Benthic communities on hard substrates covered by Limnoperna fortunei Dunker (Bivalvia, Mytilidae) at an estuarine beach (Río de la Plata, Argentina). Journal of Limnology 71.

    Article  Google Scholar 

  • Stewart, T. W., J. G. Miner & R. L. Lowe, 1998. Quantifying mechanisms for zebra mussel effects on benthic macroinvertebrates: organic matter production and shell-generated habitat. Journal of the North American Benthological Society 17(1):81-94.

    Article  Google Scholar 

  • Sylvester, F., D. Boltovskoy & D. Cataldo, 2007. The invasive bivalve Limnoperna fortunei enhances benthic invertebrate densities in South American floodplain rivers. Springer.

    Article  Google Scholar 

  • Sylvester, F., O. Kalaci, B. Leung, A. Lacoursière‐Roussel, C. C. Murray, F. M. Choi, M. A. Bravo, T. W. Therriault & H. J. MacIsaac, 2011. Hull fouling as an invasion vector: can simple models explain a complex problem? Journal of Applied Ecology 48(2):415-423.

    Article  Google Scholar 

  • Uliano-Silva, M., F. F. C. F. Fernandes, I. B. B. Holanda & M. F. Rebelo, 2013. Invasive species as a threat to biodiversity: the golden mussel Limnoperna fortunei approaching the Amazon River basin. Exploring Themes on Aquatic Toxicology Kerala P135–148.

  • Underwood, A. & M. Anderson, 1994. Seasonal and temporal aspects of recruitment and succession in an intertidal estuarine fouling assemblage. Journal of the Marine Biological Association of the United Kingdom 74(3):563-584.

    Article  Google Scholar 

  • Velde, G. v. d. & S. Rajagopal, 2006. Biological invasions: concepts to understand and predict a global threat. Springer.

    Google Scholar 

  • Venkatesan, R. & P. S. Murthy, 2008. Macrofouling control in power plants. Series on Biofilms doi:https://doi.org/10.1007/7142_2008_14.

    Article  Google Scholar 

  • Wegner, B., A. L. Kronsbein, M. Gillefalk, K. Van de Weyer, J. Köhler, E. Funke, M. T. Monaghan & S. Hilt, 2019. Mutual facilitation among invading Nuttall’s waterweed and quagga mussels. Frontiers in plant science 10.

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank the National Council for Scientific and Technological Development (CNPq) for granting funding to AO (Grant 381091/2014-7).

Funding

This paper presents part of the results of the P&D project, code PD-06491-0383/2015, executed by the Federal University of Paraná and Aliança Prestadora de Serviços Ltda. and funded by COPEL Geração e Transmissão SA, under the Research and Technological Development Program of Electricity Sector, regulated by the National Electric Energy Agency (Aneel).

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Authors and Affiliations

  1. Universidade Federal do Paraná - Graduate Program in Animal Science, Curitiba, Brazil

    Ana Paula da Silva Bertão, Raissa Vitória Vieira Leite & Antonio Ostrensky

  2. Universidade Federal do Paraná - Integrated Group of Aquaculture and Environment – GIA, R. dos Funcionários, 1540, Juvevê, Curitiba, PR, 80035-050, Brazil

    Ana Paula da Silva Bertão, Raissa Vitória Vieira Leite, Aline Horodesky & Antonio Ostrensky

  3. Universidade Federal do Paraná - Graduate Program in Zoology, Curitiba, Brazil

    Aline Horodesky, Marcio Roberto Pie & Antonio Ostrensky

  4. COPEL Geração e Transmissão S/A, GeT/SGE/DPEG/VECM, Rua José Izidoro Biazetto, 158 - Mossunguê, Curitiba, PR, 82305-240, Brazil

    Thiago Luis Zanin

  5. Alianca Prestadora de Serviços Ltda, Av. Sete de Setembro, 5402, Cj. 41 Batel, Curitiba, PR, 80240-000, Brazil

    Otto Samuel Mader Netto

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  1. Ana Paula da Silva Bertão
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  2. Raissa Vitória Vieira Leite
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Contributions

Conceptualization: AB, RL, and AO; methodology and field collection: AB, AO, RL, and AH, and ON; software: AO and AB; writing—preparing the manuscript: AB, AO, RL, and AH; writing—review and editing: AB, AO, AH, RL, and MP; supervision: AO, MP, and TZ.

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Correspondence to Ana Paula da Silva Bertão.

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da Silva Bertão, A.P., Leite, R.V.V., Horodesky, A. et al. Ecological interactions between invasive and native fouling species in the reservoir of a hydroelectric plant. Hydrobiologia 848, 5169–5185 (2021). https://doi.org/10.1007/s10750-021-04706-7

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  • DOI: https://doi.org/10.1007/s10750-021-04706-7

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