Biological Invasions

, Volume 21, Issue 1, pp 59–66 | Cite as

Herbivory can mitigate, but not counteract, the positive effects of warming on the establishment of the invasive macrophyte Hydrilla verticillata

  • Clementina CalvoEmail author
  • Roger P. Mormul
  • Bruno R. S. Figueiredo
  • Eduardo R. Cunha
  • Sidinei M. Thomaz
  • Mariana Meerhoff
Original Paper


Hydrilla verticillata is a submerged, rooted macrophyte native to Asia and Australia, but currently attains broad distribution across all continents. Its success as an invasive species depends on the simultaneous influence of abiotic and biotic factors on different components of its performance. We conducted a factorial experiment to test the short-term responses of Hydrilla, present since 2005 in the upper Parana River (Brazil), to a native herbivore (apple snail Pomacea canaliculata) and increased water temperature, using two different spatial arrangements of macrophyte fragments (one simulating early establishment phase and other simulating late establishment phase). Temperature, herbivory and plant spatial arrangement individually, and in some cases through their interactions, caused changes in the growth likely indicating impacts for the ecological responses of Hydrilla´s establishment. Snail herbivory decreased plant growth thus exerting biotic resistance, while higher temperature increased Hydrilla´s invasiveness. According to our results and other pieces of evidence, invasions of Hydrilla might worsen under the future climate warming scenario, but herbivores might locally mitigate invasion speed or magnitude.


Invasion process Temperature Spatial aggregation Pomacea canaliculata Grazing Aquatic plant 



Clementina Calvo acknowledges the Agencia Nacional de Investigación e Innovación (ANII, Uruguay) for funding her MSc. We are also grateful to the State University of Maringá (UEM, Brazil) for supplies and facilities provided to perform the experiment. Mariana Meerhoff thanks the support of ANII and PEDECIBA. Roger P. Mormul and Sidinei M. Thomaz acknowledge the National Council for Scientific and Technological Development (CNPq) for providing continuous funding through a Scientific Productivity grant.

Supplementary material

10530_2018_1803_MOESM1_ESM.pdf (104 kb)
Supplementary material 1 (PDF 103 kb)


  1. Alofs KM, Jackson DA (2014) Meta-analysis suggests biotic resistance in freshwater environments is driven by consumption rather than competition. Ecology 95:3259–3270CrossRefGoogle Scholar
  2. Barrat-Segretain MH, Gudrun B, Hering-Vilas-Bôas A (1998) Comparative abilities of vegetative regeneration among aquatic plants growing in disturbed habitats. Aquat Bot 60:201–211CrossRefGoogle Scholar
  3. Blackburn TM, Pyšek P, Bacher S, Carlton JT, Duncan RP, Jarošik V, Wilson JRU, Richardson DM (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26:333–339CrossRefGoogle Scholar
  4. Carlsson NOL, Brönmark C, Hansson LA (2004) Invading herbivory: the golden apple snail alters ecosystem functioning in Asian wetlands. Ecology 85:1575–1580CrossRefGoogle Scholar
  5. Chadwell TB, Engelhardt KAM (2008) Effects of pre-existing submersed vegetation and propagule pressure on the invasion success of Hydrilla verticillata. J Appl Ecol 45:515–523CrossRefGoogle Scholar
  6. Coetzee JA, Hill MP (2012) The role of eutrophication in the biological control of water hyacinth, Eichhornia crassipes, in South Africa. Biocontrol 57:247–261CrossRefGoogle Scholar
  7. Cook CDK, Lüönd R (1982) A revision of the genus Hydrilla (Hydrocharitaceae). Aquat Bot 13:485–504CrossRefGoogle Scholar
  8. Cruz C, Silva AF, Venturini FP, Garlich N, Pitelli RLCM, Pitelli RA (2015) Food preference and consumption of aquatic macrophytes submerged by snail Pomacea canaliculata. Planta Daninha 33:433–439CrossRefGoogle Scholar
  9. Cuda JP, Coon BR, Dao YM, Center TD (2011) Effect of an herbivorous stem-mining midge on the growth of Hydrilla. J Aquat Plant Manag 49:83–89Google Scholar
  10. Dong B-C, Yu G-L, Guo W, Zhang M-X, Dong M, Yu F-H (2010) How internode length, position and presence of leaves affect survival and growth of Alternanthera philoxeroides after fragmentation? Evol Ecol 24:1447–1461CrossRefGoogle Scholar
  11. Fleming JP, Dibble ED (2015) Ecological mechanisms of invasion success in aquatic macrophytes. Hydrobiologia 746:23–37CrossRefGoogle Scholar
  12. Hahn PG, Orrock JL (2015) Spatial arrangement of canopy structure and land use history alter the effect that herbivores have on plant growth. Ecosphere 6:1–16CrossRefGoogle Scholar
  13. Heiler KCM, von Oheimb PV, Ekschmitt K, Albrecht C (2008) Studies on the temperature dependence of activity and on the diurnal activity rhythm of the invasive Pomacea canaliculata (Gastropoda: Ampullariidae). Mollusca 26:73–81Google Scholar
  14. Hofstra DE, Clayton J, Green JD, Auger M (1999) Competitive performance of Hydrilla verticillata in New Zealand. Aquat Bot 63:305–324CrossRefGoogle Scholar
  15. Jiang J, Kong F, Gu X, Chen K, Zhao S, Wang J (2010) Influence of intraspecific interaction and substrate type on initial growth and establishment of Hydrilla verticillata. Hydrobiologia 649:255–265CrossRefGoogle Scholar
  16. Langeland KA (1996) Hydrilla verticillata (L. F.) Royle (Hydrocharitaceae), “The perfect aquatic weed”. Castanea 61:293–304Google Scholar
  17. Lemoine NP, Burkepile DE, Parker JD (2014) Variable effects of temperature on insect herbivory. Peer J 2:e376CrossRefGoogle Scholar
  18. Li Z, He L, Zhang H, Urrutia-Cordero P, Ekvall MK, Hollander J, Hansson L-A (2017) Climate warming and heat waves affect reproductive strategies and interactions between submerged macrophytes. Glob Change Biol 23:108–116CrossRefGoogle Scholar
  19. Lin H-F, Alpert P, Yu F-H (2012) Effects of fragment size and water depth on performance of stem fragments of the invasive, amphibious, clonal plant Ipomoea aquatica. Aquat Bot 99:34–40CrossRefGoogle Scholar
  20. Luque GM, Bellard C, Bertelsmeier C, Bonnaud E, Genovesi P, Simberloff D, Courchamp F (2014) The 100th of the world’s worst invasive alien species. Biol Invasions 16:981–985CrossRefGoogle Scholar
  21. Madsen JD, Owens CS (2000) Factors contributing to the spread of Hydrilla in lakes and reservoirs. Aquatic plant control technical notes collection (ERDC TN-APCRP-EA-01). US Army Engineer Research and Development Center, Vicksburg, pp 1–11Google Scholar
  22. Madsen JD, Smith DH (1999) Vegetative spread of dioecious Hydrilla colonies in experimental ponds. J Aquat Plant Manag 37:25–29Google Scholar
  23. Marengo JA, Ambrizzi T, da Rocha RP, Alves LM, Cuadra SV, Valverde MC, Torres RR, Santos DC, Ferraz SET (2010) Future change of climate in South America in the late twenty-first century: intercomparison of scenarios from three regional climate models. Clim Dyn 35:1073–1097CrossRefGoogle Scholar
  24. McKee D, Hatton K, Eaton JW, Atkinson D, Atherton A, Harvey I, Moss B (2002) Effects of simulated climate warming on macrophytes in freshwater microcosm communities. Aquat Bot 74:71–83CrossRefGoogle Scholar
  25. Mony C, Koschnick TJ, Haller WT, Muller S (2007) Competition between two invasive Hydrocharitaceae (Hydrilla verticillata (L.f.) (Royle) and Egeria densa (Planch)) as influenced by sediment fertility and season. Aquat Bot 86:236–242CrossRefGoogle Scholar
  26. O´Connor MI (2009) Warming strengthens an herbivore-plant interaction. Ecology 90:388–398CrossRefGoogle Scholar
  27. Owens CS, Grodowitz MJ, Smart RM, Harms NE, Nachtrieb JM (2006) Viability of Hydrilla fragments exposed to different levels of insect herbivory. J Aquat Plant Manag 44:145–147Google Scholar
  28. Owens CS, Smart RM, Dick GO (2008) Resistance of Vallisneria to invasion from Hydrilla fragments. J Aquat Plant Manag 46:113–116Google Scholar
  29. P´yankov VI, Ivanov LA (2000) Biomass allocation in boreal plants with different ecological strategies. Russ J Ecol 31:1–7CrossRefGoogle Scholar
  30. Pesacreta GJ (1990) Aquatic plant control research program: pilot study: carbohydrate allocation in Hydrilla biotypes. No. WES/MP/A-90-2. Environmental Lab, Army Engineer Waterways Experiment Station, VicksburgCrossRefGoogle Scholar
  31. Pieczynska E (2003) Effect of damage by the snail Lymnaea (Lymnaea) stagnalis (L.) on the growth of Elodea canadensis Michx. Aquat Bot 75:137–145CrossRefGoogle Scholar
  32. Ribas LGS, Cunha ER, Vitule JRS, Mormul RP, Thomaz SM, Padial AA (2017) Biotic resistance by snails and fish to an exotic invasive aquatic plant. Fresh Biol 62:1266–1275CrossRefGoogle Scholar
  33. Riis T, Sand-Jensen K (2006) Dispersal of plant fragments in small streams. Freshw Biol 51:274–286CrossRefGoogle Scholar
  34. Roberts DA, Poore AGB (2006) Habitat configuration affects colonization of epifauna in a marine algal bed. Biol Conserv 127:18–26CrossRefGoogle Scholar
  35. Silveira MJ, Thomaz SM, Mormul RP, Pereira F (2009) Effects of desiccation and sediment type on early regeneration of plant fragment of three species of aquatic macrophyte. Intern Rev Hydrobiol 94:169–178CrossRefGoogle Scholar
  36. Sousa WTZ (2011) Hydrilla verticillata (Hydrocharitaceae), a recent invader threatening Brazil´s freshwater environments: a review of the extent of the problem. Hydrobiologia 669:1–20CrossRefGoogle Scholar
  37. Sousa WTZ, Thomaz SM, Murphy KJ (2010) Response of native Egeria najas Planch. and invasive Hydrilla verticillata (L.f.) Royle to altered hydroecological regime in a subtropical river. Aquat Bot 92:40–48CrossRefGoogle Scholar
  38. 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
  39. Thiébaut G, Martinez L (2015) An exotic macrophyte bed may facilitate the anchorage of exotic propagules during the first stage of invasion. Hydrobiologia 746:183–196CrossRefGoogle Scholar
  40. Umetsu CA, Evangelista HBA, Thomaz SM (2012) The colonization, regeneration, and growth rates of macrophytes from fragments: a comparison between exotic and native submerged aquatic species. Aquat Ecol 46:443–449CrossRefGoogle Scholar
  41. Underwood AJ (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. University Press, Cambridge, p 504Google Scholar
  42. Wang J-W, Yu D, Xiong W, Han Y-Q (2008) Above- and belowground competition between two submersed macrophytes. Hydrobiologia 607:113–122CrossRefGoogle Scholar
  43. Wu J, Cheng S, Liang W, Wu Z (2009) Effects of organic-rich sediment and below-ground sulfide exposure on submerged macrophyte, Hydrilla verticillata. Bull Environ Contam Toxicol 83:497–501CrossRefGoogle Scholar
  44. Yu H, Ye C, Song X, Liu J (2010) Comparative analysis of growth and physio-biochemical responses of Hydrilla verticillata to different sediments in freshwater microcosms. Ecol Eng 36:1285–1289CrossRefGoogle Scholar
  45. Yvon-Durocher G, Montoya JM, Trimmer M, Woodward G (2011) Warming alters the size spectrum and shifts the distribution of biomass in aquatic ecosystems. Global Change Biol 17:1681–1694CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Departamento de Ecología y Gestión AmbientalCentro Universitario Regional del Este (CURE) - Universidad de la República (UdelaR)MaldonadoUruguay
  2. 2.Núcleo de Pesquisa em LimnologiaIctiologia e Aquicultura (Nupélia) - Universidade Estadual de Maringá (UEM)MaringáBrazil
  3. 3.Department of BioscienceAarhus UniversitySilkeborgDenmark

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