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Biological Invasions

, Volume 17, Issue 7, pp 2123–2138 | Cite as

Effects of Elodea nuttallii on temperate freshwater plants, microalgae and invertebrates: small differences between invaded and uninvaded areas

  • Ruth KellyEmail author
  • Chris Harrod
  • Christine A. Maggs
  • Neil Reid
Original Paper

Abstract

The invasive aquatic plant species Elodea nuttallii could pose a considerable risk to European freshwater ecosystems based on its current distribution, rate of spread and potential for high biomass. However, little research has been conducted on the impacts of this species on native biota. This study takes an ecosystem-wide approach and examines the impact of E. nuttallii on selected physicochemical parameters (dissolved oxygen and pH), algae, invertebrate and macrophyte communities. Elodea nuttallii had small but significant impacts on plant, invertebrate and algal species. The richness of algal periphyton was lower on E. nuttallii than on native macrophytes. The taxonomic composition of invertebrate communities associated with E. nuttallii differed from that associated with similar native plant species, but did not differ in terms of total biomass or species richness. Macrophyte species richness and total cover were positively correlated with percentage cover of E. nuttallii. Not all macrophyte species responded in the same way to E. nuttallii invasion; cover of the low-growing species, Elodea canadensis and charophytes were negatively correlated with E. nuttallii cover, whilst floating-rooted plants were positively correlated with E. nuttallii cover. All observed differences in the macrophyte community were small relative to other factors such as nutrient levels, inter-annual variation and differences between sites. Despite this, the observed negative association between E. nuttallii and charophytes is a key concern due to the rarity and endangered status of many charophyte species.

Keywords

Algae Aquatic Invasion Limnology Macroinvertebrate Macrophyte 

Notes

Acknowledgments

This research was funded by the Natural Heritage Research Partnership (NHRP) between the Northern Ireland Environment Agency (NIEA) and Quercus, Queen’s University Belfast (QUB) under a PhD studentship (QU08-05). Water chemistry analyses for the field study were conducted by the Agri-Food and Biosciences Institute, Newforge Lane, Belfast. Data from Lough Erne surveys were kindly supplied by Brenda Walker of the NIEA. Thanks to Irena Tománková for her assistance with invertebrate identification. We also thank our NIEA client officers, John Early and Tony Waterman, for their support. Thanks also to two anonymous reviewers whose advice substantially improved this manuscript.

Supplementary material

10530_2015_865_MOESM1_ESM.pdf (244 kb)
Supplementary material 1 (PDF 244 kb)

References

  1. Angelstein S, Schubert H (2008) Elodea nuttallii: uptake, translocation and release of phosphorus. Aquat Biol 3:209–216CrossRefGoogle Scholar
  2. Angelstein S, Schubert H (2009) Light acclimatisation of Elodea nuttallii grown under ambient DIC conditions. Plant Ecol 202:91–101CrossRefGoogle Scholar
  3. Barrat-Segretain M (2001) Invasive species in the Rhone River floodplain (France): replacement of Elodea canadensis Michaux by E. nuttallii St. John in two former river channels. Archiv Fur Hydrobiologie 152:237–251Google Scholar
  4. Barrat-Segretain M (2005) Competition between invasive and indigenous species: impact of spatial pattern and developmental stage. Plant Ecol 180:153–160CrossRefGoogle Scholar
  5. Barrat-Segretain M, Elger A, Sagnes P, Puijalon S (2002) Comparison of three life-history traits of invasive Elodea canadensis Michx. and Elodea nuttallii (Planch.) H. St. John. Aquat Bot 74:299–313Google Scholar
  6. Barrs JR, Keenan EA, O’Callaghan P, Caffrey J (2008) Research and control programme for Lagarosiphon major (Hydrocharitaceae). Central Fisheries Board, IrelandGoogle Scholar
  7. Barton K (2013) MuMIn: multi-model inference. R package version 1(9):11Google Scholar
  8. Bellinger EG, Sigee DC (2010) Freshwater algae: identification and use as bioindicators. Wiley-Blackwell, UKCrossRefGoogle Scholar
  9. Burks R, Lodge D (2002) Cued in: advances and opportunities in freshwater chemical ecology. J Chem Ecol 28:1901–1917PubMedCrossRefGoogle Scholar
  10. Burks R, Jeppesen E, Lodge D (2000) Macrophyte and fish chemicals suppress Daphnia growth and alter life-history traits. Oikos 88:139–147Google Scholar
  11. Caffrey JM, Baars J-R, Barbour JH, Boets P, Boon P, Davenport K, Dick J, Early J, Edsman L, Gallagher C, Gross J, Heinimaa P, Horrill C, Hudin S, Hulme PE, Hynes S, MacIsaac HJ, McLoone P, Millane M, Moen TL, Moore N, Newman J, O’Conchuir R, O’Farrell M, Colette O’Flynn, Oidtmann B, Renals T, Ricciardi A, Roy H, Shaw R, van Valkenburg JLCH, Olaf Weyl, Williams F, Lucy FE (2014) Tackling invasive alien species in Europe: the top 20 issues. Manag Biol Invasion 5:1–20CrossRefGoogle Scholar
  12. Capers RS, Selsky R, Bugbee GJ, White JC (2007) Aquatic plant community invasibility and scale-dependent patterns in native and invasive species richness. Ecology 88:3135–3143PubMedCrossRefGoogle Scholar
  13. Carniatto N, Thomaz SM, Cunha ER, Fugi R, Ota RR (2013) Effects of an invasive alien Poaceae on aquatic macrophytes and fish communities in a neotropical reservoir. Biotropica 45:747–754CrossRefGoogle Scholar
  14. Carvalho L, Dudley B, Dodkins I, Clarke R, Jones I, Thackeray S, Maberly S (2007) Final report project WFD80 Phytoplankton classification tool (Phase 2). SNIFFER, EdinburghGoogle Scholar
  15. Chaloner DT, Hershey AE, Lamberti GA (2009) Benthic invertebrate fauna. Elsevier, New YorkCrossRefGoogle Scholar
  16. Champion PD, Clayton JS, Hofstra DE (2010) Nipping aquatic plant invasions in the bud: weed risk assessment and the trade. Hydrobiologia 656:167–172CrossRefGoogle Scholar
  17. Compin A, Cereghino R (2007) Spatial patterns of macroinvertebrate functional feeding groups in streams in relation to physical variables and land-cover in Southwestern France. Landsc Ecol 22:1215–1225CrossRefGoogle Scholar
  18. Cox EJ (1996) Identification of freshwater diatoms from live material. Chapman and Hall, LondonGoogle Scholar
  19. Cummins KW, Klug MJ (1979) Feeding ecology of stream invertebrates. Annu Rev Ecol Syst 10:147–172CrossRefGoogle Scholar
  20. DAISIE (2015) 100 of the worst. http://www.europe-aliens.org/speciesTheWorst.do. Accessed 16 Jan 2015
  21. Declerck S, Vanderstukken M, Pals A, Muylaert K, de Meester L (2007) Plankton biodiversity along a gradient of productivity and its mediation by macrophytes. Ecology 88:2199–2210PubMedCrossRefGoogle Scholar
  22. deWinton MD, Clayton JS (1996) The impact of invasive submerged weed species on seed banks in lake sediments. Aquat Bot 53:31–45CrossRefGoogle Scholar
  23. Edington JM, Hildrew AG (1995) Sp. 53 caseless cadis larvae (Trichoptera): a revised key to the caseless cadis larvae of the British Isles, with notes on their ecology. Freshwater Biological Association, AmblesideGoogle Scholar
  24. Elliott JM, Mann KH (1998) Sp. 40 Leeches. A key to the British Freshwater Leeches, with notes on their life cycles and ecology. Freshwater Biological Association, AmblesideGoogle Scholar
  25. Erhard D, Gross EM (2006) Allelopathic activity of Elodea canadensis and Elodea nuttallii against epiphytes and phytoplankton. Aquat Bot 85:203–211Google Scholar
  26. Erhard D, Pohnert G, Gross EM (2007) Chemical defense in Elodea nuttallii reduces feeding and growth of aquatic herbivorous Lepidoptera. J Chem Ecol 33:1646–1661PubMedCrossRefGoogle Scholar
  27. Evangelista HBA, Thomaz SM, Umetsu CA (2014) An analysis of publications on invasive macrophytes in aquatic ecosystems. Aquat Invasions 9:521–528CrossRefGoogle Scholar
  28. Fitter R, Manuel R (1986) Field guide to lakes, rivers, streams and ponds of north-west Europe. Harper Collins, Hong KongGoogle Scholar
  29. Fournier D, Skaug H, Ancheta J, Ianelli J, Magnusson A, Maunder MN, Nielsen A, Sibert J (2012) AD Model Builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optim Methods Softw 27:233–249CrossRefGoogle Scholar
  30. Friday LE (1998) A key to the adults of British water beetles. J Field Stud Counc 7:1–152Google Scholar
  31. Gledhill T, Sutcliffe DW, Williams WD (1993) British freshwater Crustacea Malacostraca: a key with ecological notes. Freshwater Biological Association, CumbriaGoogle Scholar
  32. Gross EM, Johnson RL, Hairston NG (2001) Experimental evidence for changes in submersed macrophyte species composition caused by the herbivore Acentria ephemerella (Lepidoptera). Oecologia 127:105–114CrossRefGoogle Scholar
  33. Hamilton G (2010) The determination of Chlorophyll a in freshwater. Agri-food and biosciences standard operating procedure. Agri-food and Biosciences Institute, BelfastGoogle Scholar
  34. Hamilton SK, Lewis WM, Sippel SJ (1992) Energy-sources for aquatic animals in the Orinoco River floodplain—evidence from stable isotopes. Oecologia 89:324–330CrossRefGoogle Scholar
  35. Heegaard E, Birks H, Gibson C, Smith SJ, Wolfe-Murphy S (2001) Species–environmental relationships of aquatic macrophytes in Northern Ireland. Aquat Bot 70:175–223CrossRefGoogle Scholar
  36. Heino J (2008) Patterns of functional biodiversity and function-environment relationships in lake littoral macroinvertebrates. Limnol Oceanogr 53:1446–1455CrossRefGoogle Scholar
  37. Herault B, Bornet A, Tremolieres M (2008) Redundancy and niche differentiation among the European invasive Elodea species. Biol Invasions 10:1099–1110Google Scholar
  38. Hillebrand H, Durselen C, Kirschtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424CrossRefGoogle Scholar
  39. Hogsden K, Sager E, Hutchinson T (2007) The impacts of the non-native macrophyte Cabomba caroliniana on littoral biota of Kasshabog Lake, Ontario. J Great Lakes Res 33:497–504CrossRefGoogle Scholar
  40. Hulme PE (2012) Weed risk assessment: a way forward or a waste of time? J Appl Ecol 49:10–19CrossRefGoogle Scholar
  41. Hussner A (2012) Alien aquatic plant species in European countries. Weed Res 52:297–306CrossRefGoogle Scholar
  42. James C, Eaton J, Hardwick K (1999) Competition between three submerged macrophytes, Elodea canadensis Michx, Elodea nuttallii (Planch.) St John and Lagarosiphon major (Ridl.) moss. Hydrobiologia 415:35–40CrossRefGoogle Scholar
  43. John DM, Whitton BA, Brook AJ (2002) The freshwater algal flora of the British Isles: An identification guide to freshwater and terrestrial algae. Cambridge University Press, CambridgeGoogle Scholar
  44. Kelly D, Hawes I (2005) Effects of invasive macrophytes on littoral-zone productivity and foodweb dynamics in a New Zealand high-country lake. J N Am Benthol Soc 24:300–320CrossRefGoogle Scholar
  45. Kelly R, Leach K, Cameron A, Maggs CA, Reid N (2014a) Combining global climate and regional landscape models to improve prediction of invasion risk. Divers Distrib 20:884–894CrossRefGoogle Scholar
  46. Kelly R, Lundy MG, Mineur F, Harrod C, Maggs CA, Humphries NE, Sims DW, Reid N (2014b) Historical data reveal power-law dispersal patterns of invasive aquatic species. Ecography 37:581–590CrossRefGoogle Scholar
  47. Kennedy T, Naeem S, Howe K, Knops JMH, Tilman D, Reich P (2002) Biodiversity as a barrier to ecological invasion. Nature 417:636–638PubMedCrossRefGoogle Scholar
  48. Kornijow R, Vakkilainen K, Horppila J, Luokkanen E, Kairesalo T (2005) Impacts of a submerged plant (Elodea canadensis) on interactions between roach (Rutilus rutilus) and its invertebrate prey communities in a lake littoral zone. Freshw Biol 50:262–276CrossRefGoogle Scholar
  49. Kovalenko KE, Dibble ED (2014) Invasive macrophyte effects on littoral trophic structure and carbon sources. Hydrobiologia 721:23–34CrossRefGoogle Scholar
  50. Kruk C, Huszar V, Peeters E, Bonilla S, Costa L, Lurling M, Reynolds CS, Scheffer M (2010) A morphological classification capturing functional variation in phytoplankton. Freshw Biol 55:614–627CrossRefGoogle Scholar
  51. Leung B, Roura-Pascual N, Bacher S, Heikkila J, Brotons L, Burgman MA, Dehnen-Schmutz K, Essl F, Hulme PE, Richardson DM, Sol D, Vila M (2012) TEASIng apart alien species risk assessments: a framework for best practices. Ecol Lett 15:1475–1493PubMedCrossRefGoogle Scholar
  52. Levine J (2000) Species diversity and biological invasions: Relating local process to community pattern. Science 288:852–854PubMedCrossRefGoogle Scholar
  53. Lonsdale W (1999) Global patterns of plant invasions and the concept of invasibility. Ecology 80:1522–1536CrossRefGoogle Scholar
  54. Michelan T, Thomaz S, Mormul R, Carvalho P (2010) Effects of an exotic invasive macrophyte (tropical signalgrass) on native plant community composition, species richness and functional diversity. Freshwater Biol 55:1315–1326CrossRefGoogle Scholar
  55. Mjelde M, Lombardo P, Berge D, Johansen SW (2012) Mass invasion of non-native Elodea canadensis Michx. in a large, clear-water, species-rich Norwegian lake—impact on macrophyte biodiversity. Int J Limnol 48:225–240CrossRefGoogle Scholar
  56. Montgomery WI, Lundy MG, Reid N (2012) ‘Invasional meltdown’: evidence for unexpected consequences and cumulative impacts of multispecies invasions. Biol Invasions 14:1111–1125CrossRefGoogle Scholar
  57. Netten J, Arts G, Gylstra R, Roijackers RMM (2010) Effect of temperature and nutrients on the competition between free-floating Salvinia natans and submerged Elodea nuttallii in mesocosms. Fundam Appl Limnol 177:125–132CrossRefGoogle Scholar
  58. O’Hare M, Gunn I, Chapman D, Dudley BJ, Purse BV (2012) Impacts of space, local environment and habitat connectivity on macrophyte communities in conservation lakes. Divers Distrib 18:603–614CrossRefGoogle Scholar
  59. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013) vegan: Community Ecology Package. R Package Version 2.0-9Google Scholar
  60. R Core Development Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  61. Rybicki N, Landwehr J (2007) Long-term changes in abundance and diversity of macrophyte and waterfowl populations in an estuary with exotic macrophytes and improving water quality. Limnol Oceanogr 52:1195–1207CrossRefGoogle Scholar
  62. Sala OE, Chapin FS III, Armesto JJ, Eric Berlow, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Oesterheld M, Poff NL, Sykes MT, Walker BH, Walker M, Wall DH (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774PubMedCrossRefGoogle Scholar
  63. Savage AA (1989) Adults of the British Aquatic Hemiptera Heteroptera: a key with ecological notes. Freshwater Biological Association, AmblesideGoogle Scholar
  64. Schultz R, Dibble E (2012) Effects of invasive macrophytes on freshwater fish and macroinvertebrate communities: the role of invasive plant traits. Hydrobiologia 684:1–14CrossRefGoogle Scholar
  65. Simberloff D (2006) Invasional meltdown 6 years later: important phenomenon, unfortunate metaphor, or both? Ecol Lett 9:912–919PubMedCrossRefGoogle Scholar
  66. Stiers I, Crohain N, Josens G, Triest L (2011) Impact of three aquatic invasive species on native plants and macroinvertebrates in temperate ponds. Biol Invasions 13:2715–2726CrossRefGoogle Scholar
  67. Strayer D (2010) Alien species in fresh waters: ecological effects, interactions with other stressors, and prospects for the future. Freshw Biol 55:152–174CrossRefGoogle Scholar
  68. Szabo S, Scheffer M, Roijackers R, Waluto B, Braun M, Nagy PT, Borics G, Zambrano L (2010) Strong growth limitation of a floating plant (Lemna gibba) by the submerged macrophyte (Elodea nuttallii) under laboratory conditions. Freshw Biol 55:681–690CrossRefGoogle Scholar
  69. Thiébaut G, Di Nino F, Peltre M-C, Wagner P (2008) Management of aquatic exotic plants: the case of Elodea species. In: Sengupta M, Dalwani R (eds) The 12th world lake conference. Taal, pp 1058–1066Google Scholar
  70. Thomaz SM, Silveira MJ, Michelan TS (2012) The colonization success of an exotic Poaceae is related to native macrophyte richness, wind disturbance and riparian vegetation. Aquat Sci 74:809–815CrossRefGoogle Scholar
  71. Thouvenot L, Puech C, Martinez L, Haury J, Thiebaut G (2013) Strategies of the invasive macrophyte Ludwigia grandiflora in its introduced range: Competition, facilitation or coexistence with native and exotic species? Aquat Bot 107:8–16CrossRefGoogle Scholar
  72. Toporowska M, Pawlik-Skowronska B, Wojtal AZ (2008) Epiphytic algae on Stratiotes aloides L., Potamogeton lucens L., Ceratophyllum demersum L. and Chara spp. in a macrophyte-dominated lake. Oceanol Hydrobiol St 37:51–63Google Scholar
  73. Valinoti C, Ho C, Armitage A (2011) Native and exotic submerged aquatic vegetation provide different nutritional and refuge values for macroinvertebrates. J Exp Mar Biol Ecol 409:42–47CrossRefGoogle Scholar
  74. van Donk E, van de Bund W (2002) Impact of submerged macrophytes including charophytes on phyto- and zooplankton communities: allelopathy versus other mechanisms. Aquat Bot 72:261–274Google Scholar
  75. Wallace ID, Wallace B, Philipson GN (1990) A key to the case-bearing caddis larvae of Britain and Ireland. Freshwater Biological Association, AmblesideGoogle Scholar
  76. Warfe DM, Barmuta LA (2006) Habitat structural complexity mediates food web dynamics in a freshwater macrophyte community. Oecologia 150:141–154PubMedCrossRefGoogle Scholar
  77. Wu Z, Gao Y, Wang J, Liu BY, Zhou QH, Zhang YY (2009) Allelopathic effects of phenolic compounds present in submerged macrophytes on Microcystis aeruginosa. Allelopathy J 23:403–410Google Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Ruth Kelly
    • 1
    Email author
  • Chris Harrod
    • 2
    • 3
  • Christine A. Maggs
    • 2
  • Neil Reid
    • 1
    • 2
    • 4
  1. 1.Quercus, School of Biological SciencesQueen’s University BelfastBelfastUK
  2. 2.School of Biological SciencesQueen’s University BelfastBelfastUK
  3. 3.Instituto de Ciencias Naturales Alexander Von HumboldtUniversidad de AntofagastaAntofagastaChile
  4. 4.Institute of Global Food Security (IGFS)Queen’s University BelfastBelfastUK

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