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The invasive macrophyte Hydrilla verticillata causes taxonomic and functional homogenization of associated Chironomidae community

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Abstract

Exotic species have invaded freshwater ecosystems, causing biodiversity loss of associated communities. We investigated the influence of the invasive macrophyte Hydrilla verticillata on taxonomic and functional richness, and on taxonomic and functional beta diversity of associated Chironomidae community, comparing this macrophyte with the structurally similar native macrophyte, Egeria najas. We conducted a field experiment where the native and invasive plants were kept side-by-side and colonized by invertebrates. We used accumulation curves to test if richness differed between macrophytes. We used multivariate dispersion to investigate whether taxonomic and functional composition differed between both macrophytes and to test if beta diversity was higher among individuals of the native than among individuals of the invasive macrophytes. We measured beta diversity values as an average distance of the compositions to the centroid in a multidimensional space (taxonomic and functional) given by a Principal Coordinates Analysis. We found similar taxonomic richness and similar taxonomic and functional Chironomidae composition between macrophytes. However, functional richness as well as taxonomic and functional beta diversity of Chironomidae were higher among the native than among the invasive macrophytes. Thus, although H. verticillata did not cause changes neither in Chironomidae taxonomic richness nor on taxonomic and functional composition, its spread may drive the simplification of species and functional traits of associated Chironomidae communities.

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References

  • Agostinho AA, Thomaz SM, Gomes LC (2004) Threats for biodiversity in the floodplain of the Upper Paraná River: effects of hydrological regulation by dams. Ecohydrol Hydrobiol 4(3):267–280

    Google Scholar 

  • Agostinho AA, Bonecker CC, Gomes LC (2009) Effects of water quantity on connectivity: the case of the upper Paraná River floodplain. Ecohydrol Hydrobiol 9:99–113

    Google Scholar 

  • Amorim SR, Umetsu CA, Camargo AFM (2015) Effects of a non-native species of Poaceae on aquatic macrophyte community composition: a comparison with a native species. J Aquat Plant Manage 53:191–196

    Google Scholar 

  • Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62:245–253

    PubMed  Google Scholar 

  • Armitage PD, Cranston PS, Pinder LCV (1995) The Chironomidae. Springer, Netherlands

    Google Scholar 

  • Barrientos CA, Allen MS (2008) Fish abundance and community composition in native and non-native plants following hydrilla colonisation at Lake Izabal. Guatemala Fisheries Manag Ecol 15(2):99–106

    Google Scholar 

  • Behrend RDL, Teixeira MC, Fernandes SEP, Camargo JC, Rosin GC, Takeda AM (2013) Effects of a native and a non-native macrophyte species of Hydrocharitaceae on Chironomidae and Oligochaeta assemblages structure. Acta Sci Biol Sci 35:351–358

    Google Scholar 

  • Bilia CG, Pinha GD, Petsch DK, Takeda AM (2015) Influência da heterogeneidade ambiental sobre os atributos da comunidade de Chironomidae em lagoas de inundação neotropicais. Iheringia Ser Zool 105(1):20–27

    Google Scholar 

  • Blaustein L, Kotler BP (1993) Oviposition habitat selection by the mosquito, Culiseta longiareolata: effects of conspecifics, food and green toad tadpoles. Ecol Entomol 18:104–108

    Google Scholar 

  • Buchholz S, Tietze H, Kowarik I, Schirmel J (2015) Effects of a major tree invader on urban woodland arthropods. PLoS ONE 10:1–15

    Google Scholar 

  • Burghardt KT, Tallamy DH (2015) Not all non-natives are equally unequal: reductions in herbivore b-diversity depend on phylogenetic similarity to native plant community. Ecol Lett 18:1087–1098

    PubMed  Google Scholar 

  • Butakka CMM, Ragonha FH, Takeda AM (2014) Chironomidae larvae (Diptera) of Neotropical floodplain: overlap niche in different habitats. Braz J Biol 74:363–370

    CAS  PubMed  Google Scholar 

  • Butakka CMM, Ragonha FH, Train S, Pinha GD, Takeda AM (2016) Chironomidae feeding habits in different habitats from a Neotropical floodplain: exploring patterns in aquatic food webs. Braz J Biol 76:117–125

    CAS  PubMed  Google Scholar 

  • Carey N, Strachan SR, Robson BJ (2018) Impacts of Indian waterfern (Ceratopteris thalictroides (L.) Brongn.) infestation and removal on macroinvertebrate biodiversity and conservation in spring-fed streams in the Australian arid zone. Aquat Conserv 28(2):466–475

    Google Scholar 

  • Carniatto N, Fugi R, Thomaz SM, Cunha ER (2014) The invasive submerged macrophyte Hydrilla verticillata as a foraging habitat for small-sized fish. Nat Conservação 12(1):30–35

    Google Scholar 

  • Chase JM (2010) Stochastic community assembly causes higher biodiversity in more productive environments. Science 328:1388–1391

    CAS  PubMed  Google Scholar 

  • Colon-Gaud JC, Kelso WE, Rutherford DA (2004) Spatial distribution of macroinvertebrates inhabiting Hydrilla and coontais beds in the Atchafalaya Basin, Louisiana. J Aquat Plant Manage 42:85–91

    Google Scholar 

  • Cook CDK, Lüond R (1982) A revision of the genus Hydrilla (Hydrocharitaceae). Aquat Bot 13:485–504

    Google Scholar 

  • Cox GW (1999) Alien species in North American and Hawaii. Island Press, Washington

    Google Scholar 

  • Cunha ER, Thomaz SM, Evangelista HBA, Carniato J, Souza CF, Fugi R (2011) Small-sized fish assemblages do not differ between a native and a recently established non-indigenous macrophyte in a Neotropical ecosystem. Nat Conservação 9(1):61–66

    Google Scholar 

  • De Bello F, Lep SJ, Lavorel S, Moretti M (2007) Importance of species abundance for assessment of trait composition: an example based on pollinator communities. Community Ecol 8:163–170

    Google Scholar 

  • Dray S, Dufour A (2007) The ade4 Package: implementing the duality diagram for ecologists. J Stat Softw 22(4):1–20

    Google Scholar 

  • Epler JH (2001) Identification Manual for the Larval Chironomidae (Diptera) of North and South Carolina. Special Publication, Crawfordville

    Google Scholar 

  • Fasoli JVB, Mormul RP, Cunha ER, Thomaz SM (2018) Plasticity responses of an invasive macrophyte species to inorganic carbon availability and to the interaction with a native species. Hydrobiologia 817(1):227–237

    CAS  Google Scholar 

  • Ferrington LC (2008) Global diversity of non-biting midges (Chironomidae; Insecta-Diptera) in freshwater. Hydrobiologia 595:447–445

    Google Scholar 

  • Fleming JP, Dibble ED (2015) Ecological mechanisms of invasion success in aquatic Macrophytes. Hydrobiologia 746:23–37

    Google Scholar 

  • Fontaneto D, Melone G, Ricci C (2005) Connectivity and nestedness of the meta-community structure of moss dwelling bdelloid rotifers along a stream. Hydrobiologia 542:131–136

    Google Scholar 

  • Frouz J, Kindlmann P (2001) The role of sink to source re-colonisation in the population dynamics of insects living in unstable habitats: an example of terrestrial chironomids. Oikos 93:50–58

    Google Scholar 

  • Gower JC (1966) Some distance properties of latent root and vector methods used in multivariate analysis. Biometrika 53:325–338

    Google Scholar 

  • Henriques-Oliveira AL, Nessimian JL, Dorvillé LFM (2003) Feeding habits of chironomid larvae (Insecta: Diptera) from a stream in the floresta da Tijuca, Rio de Janeiro. Brazil Braz J Biol 63:269–281

    CAS  PubMed  Google Scholar 

  • Hofstra D, Clayton J (2014) Native flora and fauna response to removal of the weed Hydrilla verticillata (Lf) Royle in Lake Tutira. Hydrobiologia 737(1):297–308

    Google Scholar 

  • Hussner A, Weyer KV, Gross EM, Hilt S (2010) Comments on increasing number and abundance of non-indigenous aquatic macrophyte species in Germany. Weed Res 50:519–526

    Google Scholar 

  • Jenkins M (2003) Prospects for biodiversity. Science 302:1175–1177

    CAS  PubMed  Google Scholar 

  • Kornijów R, Strayer DL, Caraco NF (2010) Macroinvertebrate communities of hypoxic habitats created by an invasive plant (Trapa natans) in the freshwater tidal Hudson River. Fund Appl Limnol 176:199–207

    Google Scholar 

  • Lambdon PH, Lloret F, Hulme PE (2008) Do non-native species invasions lead to biotic homogenization at small scales? The similarity and functional diversity of habitats compared for alien and native components of Mediterranean floras. Divers Distrib 14:774–785

    Google Scholar 

  • Mamani A, Koncurat ML, Boveri M (2019) Combined effects of fish and macroinvertebrate predation on zooplankton in a littoral mesocosm experiment. Hydrobiologia 829:19–29

    CAS  Google Scholar 

  • Matena J (1990) Succession of Chironomus Meigen species (Diptera: Chironomidae) in newly filled ponds. Int Rev Ges Hydrobiol 75:45–57

    Google Scholar 

  • Matthews J, Koopman KR, Beringen R, Odé B, Pot R, Velde G, van Valkenburg JLCH, Leuven RSEW (2014) Knowledge document for risk analysis of the non-native Brazilian waterweed (Egeria densa) in the Netherlands. Radboud University Nijmegen, Nijmegen

    Google Scholar 

  • Michelan TS, Silveira MJ, Petsch DK, Pinha GD, Thomaz SM (2014) The invasive aquatic macrophyte Hydrilla verticillata facilitates the establishment of the invasive mussel Limnoperna fortunei in Neotropical reservoirs. J Limnol 73:598–602

    Google Scholar 

  • Milošević D, Stojanović K, Djurdjević A, Marković Z, Stojković Piperac M, Živić M, Živić I (2018) The response of chironomid taxonomy- and functional trait-based metrics to fish farm effluent pollution in lotic systems. Environ Pollut 242:1058–1066

    PubMed  Google Scholar 

  • Mormul RP, Vieira LA, JrS P, Monkolski A, Santos AM (2006) Sucessão de invertebrados durante o processo de decomposição de duas plantas aquáticas (Eichhornia azurea e Polygonum ferrugineum). Acta Scie Biol Sci 28:109–115

    Google Scholar 

  • Mormul RP, Thomaz SM, Higuti J, Martens K (2010a) Ostracod (Crustacea) colonization of a native and a non-native macrophyte species of Hydrocharitaceae in the Upper Paraná floodplain (Brazil): an experimental evaluation. Hydrobiologia 644:185–193

    Google Scholar 

  • Mormul RP, Thomaz SM, Silveira MJ, Rodrigues L (2010b) Epiphyton or macrophyte: which primary producer attracts the snail Hebetancylus moricandi? Am Malacol Bull 28:127–133

    Google Scholar 

  • Naeem S (1998) Species redundancy and ecosystem reliability. Conserv Biol 12:39–45

    Google Scholar 

  • Novakowski GC, Hahn NS, Fugi R (2008) Diet seasonality and food overlap of the fish assemblage in a pantanal pond. Neotrop Ichthyol 6:567–576

    Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, et al (2015) Vegan: Community Ecology Package. R package version 2.2–1. https://CRAN.R-project.org/package=vegan

  • Olden JD (2006) Biotic homogenization: a new research agenda for conservation biogeography. J Biogeogr 33:2027–2039

    Google Scholar 

  • Olden JD, Rooney TP (2006) On defining and quantifying biotic homogenization. Global Ecol Biogeogr 15:113–120

    Google Scholar 

  • Olden JD, Poff NL, Douglas MR, Douglas ME, Fausch KD (2004) Ecological and evolutionary consequences of biotic homogenization. Trends Ecol Evol 19(1):18–24

    PubMed  Google Scholar 

  • Owens CS, Madsen JD (1998) Phenological studies of carbohydrate allocation in Hydrilla. J Aquat Plant Manage 36:40–44

    Google Scholar 

  • Pavoine S, Ricotta C (2014) Functional and phylogenetic similarity among communities. Methods Ecol Evol 5:666–675

    Google Scholar 

  • Pavoine S, Vallet J, Dufour AB, Gachet S, Daniel H (2009) On the challenge of treating various types of variables: application for improving the measurement of functional diversity. Oikos 118(3):391–402

    Google Scholar 

  • Petsch DK (2016) Causes and consequences of biotic homogenization in freshwater ecosystems. Int Rev Hydrobiol 101(3–4):113–122

    Google Scholar 

  • Petsch DK, Pinha GD, Dias JD, Takeda AM (2015) Temporal nestedness in Chironomidae and the importance of environmental and spatial factors in species rarity. Hydrobiologia 745(1):181–193

    Google Scholar 

  • Petsch DK, Schneck F, Melo AS (2017) Substratum simplification reduces beta diversity of stream algal communities. Freshw Biol 62:205–213

    CAS  Google Scholar 

  • Piazzi L, Balata D (2008) The spread of Caulerpa racemosa var cylindracea in the Mediterranean Sea: an example of how biological invasions can influence beta diversity. Mar Environ Res 65(1):50–61

    CAS  PubMed  Google Scholar 

  • Pillar VD, Blanco CC, Müller SC et al (2013) Functional redundancy and stability in plant communities. J Veg Sci 24:963–974

    Google Scholar 

  • Pinder LCV (1995) The habitats of chironomid larvae. In: Armitage PD, Cranston PS, Pinder LCV (eds) The Chironomidae. Biology and ecology of non-biting midges, Chapman and Hall, London, pp 107–135

    Google Scholar 

  • Pinha GD, Aviz D, Lopes Filho DR, Petsch DK, Marchese MR, Takeda AM (2013) Longitudinal distribution of Chironomidae (Diptera) downstream from a dam in a neotropical river. Braz J Biol 73(3):549–558

    CAS  PubMed  Google Scholar 

  • Pinha GD, Tramonte RP, Bilia CG, Takeda AM (2017) Differences in environmental heterogeneity promote the nestedness of Chironomidae metacommunity in Neotropical floodplain lakes. Acta Limnol Bras 29:e118

    Google Scholar 

  • Poff NL, Olden JD, Vieira NK, Finn DS, Simmons MP, Kondratieff BC (2006) Functional trait niches of North American lotic insects: traits-based ecological applications in light of phylogenetic relationships. J N Am Benthol Soc 25(4):730–755

    Google Scholar 

  • Puhl LE, Perelman SB, Batista WB, Burkart SE, León RJC (2014) Local and regional long-term diversity changes and biotic homogenization in two temperate grasslands. J Veg Sci 25:1278–1288

    Google Scholar 

  • R Development Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • Ragonha FH, Pinha GD, Bilia CG, Silva RG, Tramonte RP, Takeda AM (2013) Shoreline development from neotropical floodplain lakes on the density and richness of Chironomidae larvae. Bioikos 27:67–77

    Google Scholar 

  • Ribas LGS, Cássia-Silva C, Petsch DK, Silveira MJ, Lima-Ribeiro MS (2018) The potential invasiveness of an aquatic macrophyte reflects founder effects from native niche. Biol Invasions 20(11):3347–3355

    Google Scholar 

  • Ricciardi A, Kipp R (2008) Predicting the number of ecologically harmful exotic species in an aquatic system. Divers Distrib 14:374–380

    Google Scholar 

  • Ricotta C, Pavoine S, Bacaro G, Acosta AT (2012) Functional rarefaction for species abundance data. Methods Ecol Evol 3:519–525

    Google Scholar 

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

    Google Scholar 

  • Rosin GC, Oliveira-Mangarotti DP, Takeda AM, Butakka CMM (2009) Consequences of dam construction upstream of the Upper Parana River floodplain (Brazil): a temporal analysis of the Chironomidae community over an eight-year period. Braz J Biol 69(2):591–608

    CAS  PubMed  Google Scholar 

  • Saulino HHL, Trivinho-Strixino S (2018) Native macrophyte leaves influence more specialization of neotropical shredder chironomids than invasive macrophyte leaves. Hydrobiologia 813:189–198

    Google Scholar 

  • Schultz R, Dibble E (2012) Effects of invasive macrophytes on freshwater fish and macroinvertebrate communities: the role of invasive plant traits. Hydrobiologia 684:1–14

    Google Scholar 

  • Serra SR, Cobo F, Graca MA, Doledec S, Feio MJ (2016) Synthesising the trait information of European Chironomidae (Insecta: Diptera): towards a new database. Ecol Indic 61:282–292

    Google Scholar 

  • Serra SR, Graça MA, Dolédec S, Feio MJ (2017) Discriminating permanent from temporary rivers with traits of chironomid genera. Ann. Limnol. – Int. J Lim 53:161–174

    Google Scholar 

  • Sousa WTZ (2011) Hydrilla verticillata (Hydrocharitaceae), a recent invader threatening Brazil’s freshwater environments: a review of the extent of the problem. Hydrobiologia 669:1–20

    Google Scholar 

  • Sousa WTZ, Thomaz SM, Murphy KJ (2010) Response of native Egeria najas planch and invasive Hydrilla verticillata (Lf) royle to altered hydroecological regime in a subtropical river. Aquat Bot 92(1):40–48

    Google Scholar 

  • Souza-Filho EE, Stevaux JC (1997) Geologia e geomorfologia do complexo rio Baia, Curutuba, Ivinhema. In: Vazzoler AEAM, Agostinho AA, Hanh NS (eds) A Planície de Inundação do Alto Rio Paraná. Eduem, Maringá, Nupelia, pp 73–102

    Google Scholar 

  • Statsoft (2005) Statistica (data analysis software system), version 7.1. https://www.statsoft.de/en/home

  • Takeda AM, Souza-Franco GM, Melo SM, Monkolski A (2003) Invertebrados associados às macrófitas aquáticas da planície de inundação do (Brasil). In: Thomaz SM, Bini LM (eds) Ecologia e Manejo de Macrófitas Aquáticas. Eduem, Maringá, pp 243–260

    Google Scholar 

  • Taniguchi H, Nakano S, Tokeshi M (2003) Influences of habitat complexity on the diversity and abundance of epiphytic invertebrates on plants. Freshw Biol 48:718–728

    Google Scholar 

  • Theel HJ, Dibble ED, Madsen JD (2008) Differential influence of a monotypic and diverse native aquatic plant bed on a macroinvertebrate assemblage: an experimental implication of exotic plant induced habitat. Hydrobiologia 600:77–87

    Google Scholar 

  • Thomaz SM, Cunha ER (2010) The role of macrophytes in habitat structuring in aquatic ecosystems: methods of measurement, causes and consequences on animal assemblages' composition and biodiversity. Acta Limnol Bras 22(2):218–236

    Google Scholar 

  • Trivinho-Strixino S (2011) Larvas de Chironomidae: Guia de identificação Departamento de Hidrobiologia. Laboratório de entomologia Aquática/ UFSCar, São Carlos

    Google Scholar 

  • Warfe DM, Barmuta LA (2006) Habitat structural complexity mediates food web dynamics in a freshwater macrophyte community. Oecologia 150:141–154

    PubMed  Google Scholar 

  • Wolters JW, Verdonschot RCM, Schoelynck J, Verdonschot PFM, Meire P (2018) The role of macrophyte structural complexity and water flow velocity in determining the epiphytic macroinvertebrate community composition in a lowland stream. Hydrobiologia 806:157–173

    CAS  Google Scholar 

  • Zhang Y, Pennings SC, Li B, Wu J (2019) Biotic homogenization of wetland nematode communities by exotic Spartina alterniflora in China. Ecology 100(4):e02596

    PubMed  Google Scholar 

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Acknowledgements

CGB and GDP are thankful to the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES/PROEX) and DKP to Conselho Nacional de Desenvolvimento Científico e Tecnológico (PDJ/CNPq) by providing postdoctoral fellowship (#155580/2018-3) and financial field support. We would like to thank Dr. Márcio Silveira for contributions in earlier versions, Dr. Eduardo Cunha for all assistance and Sebastião Rodrigues, Ms. Rafael Tramonte, Dr. Márcio Silveira and Dr. Emanuel Silva for field assistance.

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  1. Programa de Biologia Comparada, Universidade Estadual de Maringá, Av. Colombo, 5790, Maringá, PR, CEP: 87020-900, Brazil

    Camila Gentilin-Avanci

  2. Programa de Pós-Graduação Em Ecologia de Ambientes Aquáticos Continentais, Universidade Estadual de Maringá, Av. Colombo, 5790, Maringá, PR, CEP: 87020-900, Brazil

    Gisele D. Pinha & Danielle K. Petsch

  3. Universidade Estadual de Maringá/DBI/NUPELIA/PEA, Av. Colombo, 5790, Maringá, PR, CEP: 87020-900, Brazil

    Roger P. Mormul & Sidinei M. Thomaz

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Gentilin-Avanci, C., Pinha, G.D., Petsch, D.K. et al. The invasive macrophyte Hydrilla verticillata causes taxonomic and functional homogenization of associated Chironomidae community. Limnology 22, 129–138 (2021). https://doi.org/10.1007/s10201-020-00641-z

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