Skip to main content
Log in

Interspecific associations between Hydrilla verticillata and three dominant native genera of submerged macrophytes are taxa dependent

  • Research Article
  • Published:
Aquatic Sciences Aims and scope Submit manuscript

Abstract

Hydrilla verticillata is a submerged macrophyte that has invaded every continent except Antarctica. In this study, we tested the predictions that (i) H. verticillata invades sites with a higher prevalence of native species; (ii) co-occurrences between the invasive and natives depend on their degree of similarity in morphology and resource use and that (iii) native species morphologically similar to H. verticillata decreases in sites colonized by H. verticillata overtime, while occurrences of morphologically dissimilar species increase post-invasion. The incidences of H. verticillata and three taxa of dominant natives were inspected across 87 sites in a reservoir in South Brazil before and after invasion by H. verticillata. The predictions were tested through co-occurrence metrics and logistic regression analyses. The logistic regression indicated that H. verticillata invaded sites independently of the occurrence of dominant natives, but it co-occurred more than expected by chance with the morphologically dissimilar native Characeae species, Nitella sp. and Chara cf. guairensis. On the other hand, Egeria spp. (morphologically similar to H. verticillata) occurrences were not correlated with the presence of H. verticillata. Moreover, the probability of occurrence of Characeae increased significantly overtime in sites invaded by H. verticillata. These results indicate that H. verticillata invaded sites independently of environmental suitability and likely facilitated more dissimilar taxa, such as Characeae, but there was no evidence that it influenced Egeria spp. occurrences. The patches of H. verticillata probably provide favorable habitats for the establishment of Characeae.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Barbosa M, Vinicius M, Kobayashi JT, Pelicice FM (2014) Morphometric and biotic variables as potential predictors of Ludwigia sedoides (Humb. & Bonpl.) Hara in a large Amazonian reservoir. Int J Limnol 50:163–171

    Article  Google Scholar 

  • Bianchini I Jr, Cunha-santino MB, Milan JAM (2010) Growth of Hydrilla verticillata (L.f.) Royle under controlled conditions. Hydrobiologia 644:301–312

    Article  Google Scholar 

  • Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trends Ecol Evol 18:119–125

    Article  Google Scholar 

  • Capers RS, Selsky R, Bugbee GI, White JC (2007) Aquatic plant community invasibility and scale-dependent patterns in native and invasive species richness. Ecology 88:3135–3143

    Article  Google Scholar 

  • Carey MP, Sethi SA, Larsen SJ, Rich CF (2016) A primer on potential impacts, management priorities, and future directions for Elodea spp. in high latitude systems: learning from the Alaskan experience. Hydrobiologia 777:1–19

    Article  Google Scholar 

  • Chesson P, Kuang JJ (2008) The interaction between predation and competition. Nature 456:235–238

    Article  CAS  Google Scholar 

  • Ciotir C, Freeland J (2016) Cryptic intercontinental dispersal, commercial retailers, and the genetic diversity of native and non-native cattails (Typha spp.) in North America. Hydrobiologia 768:137–150

    Article  CAS  Google Scholar 

  • Davies KF, Chesson P, Harrison S, Inouye BD, Melbourne BA, Rice KJ (2005) Spatial heterogeneity explains the scale dependence of the native–exotic diversity relationship. Ecology 86:1602–1610

    Article  Google Scholar 

  • dos Santos DA, Hoeinghaus DJ, Gomes LC (2018) Spatial scales and the invasion paradox: a test using fish assemblages in a Neotropical floodplain. Hydrobiologia 817:121–131

    Article  Google Scholar 

  • Ferrareze M, Nogueira MG (2015) Impact assessment of the introduction of Cichla kelberi in a large Neotropical reservoir and its lateral lagoons (Upper Parana River Basin, Brazil). Braz J Biol 75:1018–1026

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Gerard J, Triest L (2018) Competition between invasive Lemna minuta and native l-minor in indoor and field experiments. Hydrobiologia 812:57–65

    Article  CAS  Google Scholar 

  • Gidudu B, Copeland RS, Wanda F, Ochaya H, Cuda JP, Overholt WA (2011) Distribution, interespecific associations and abundance of aquatic plants in Lake Bisina, Uganda. J Aquat Plant Manag 49:19–27

    Google Scholar 

  • Gotelli NJ, Ellison AM (2004) A primer of ecological statistics. Sinauer Associates, Sunderland

    Google Scholar 

  • Hoyer MV, Jackson MW, Allen MS, Canfield DE Jr (2008) Lack of exotic hydrilla infestation effects on plant, fish and aquatic bird community measures. L Res Manag 24:331–338

    Google Scholar 

  • Kennedy TA, Naeem S, Howe KM, Knops JMH, Tilman D, Reich P (2002) Biodiversity as a barrier to ecological invasion. Nature 417:636–638

    Article  CAS  Google Scholar 

  • Lozano V, Brundu G (2018) Prioritisation of aquatic invasive alien plants in South America with the US Aquatic Weed Risk Assessment. Hydrobiologia 812:115–130

    Article  CAS  Google Scholar 

  • Martin GD, Coetzee JA, Stephen C (2018) Plant-herbivore-parasitoid interactions in an experimental freshwater tritrophic system: higher trophic levels modify competitive interactions between invasive macrophytes. Hydrobiologia 817:307–318

    Article  CAS  Google Scholar 

  • 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 86:236–242

    Article  Google Scholar 

  • Pereira LS, Neves RDF, Miyahira IC, Kozlowsky-Suzuki B, Branco CWC, de Paula JC, dos Santos LN (2018) Non-native species in reservoirs: how are we doing in Brazil? Hydrobiologia 817:71–84

    Article  Google Scholar 

  • Pierini SA, Thomaz SM (2009) Effects of Limnological and Morphometric Factors Upon Z (min), Z (max) and width of Egeria spp. Stands in a Tropical Reservoir. Braz Arch Biol Techn 52:387–396

    Article  Google Scholar 

  • R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org

  • Rejmánek M (2011) Invasiveness. In: Simberloff D, Rejmánek M (eds) Encyclopedia of biological invasions. University of California Press, Berkeley and Los Angeles, pp 379–385

    Google Scholar 

  • Rodriguez LF (2006) Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur. Biol Inv 8:927–939

    Article  Google Scholar 

  • Rybicki NB, Landwehr JM (2007) Long-term changes in abundance and diversity of macrophyte and waterfowl populations in an estuary with exotic macrophytes and improving water quality. Limnol Ocean 52:1195–1207

    Article  Google Scholar 

  • Sculthorpe D (1967) The biology of aquatic vascular plants. Edward Arnold Publishers, London

    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

    Article  Google Scholar 

  • 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 92:40–48

    Article  Google Scholar 

  • Stachowicz JJ, Byrnes JE, Jarret E (2006) Species diversity, invasion success, and ecosystem functioning: disentangling the influence of resource competition, facilitation, and extrinsic factors. Mar Ecol Prog Ser 311:251–262

    Article  Google Scholar 

  • Stohlgren TJ, Jarnevich C, Chong GW, Evangelista PH (2006) Scale and plant invasions: a theory of biotic acceptance. Preslia 78:5–426

    Google Scholar 

  • Szmeja J, Gałka A (2008) Phenotypic responses to water flow and wave exposure in aquatic plants. Acta Soc Bot Pol 59:59–65

    Google Scholar 

  • Thiebaut G, Martinez L (2015) An exotic macrophyte bed may facilitate the anchorage of exotic propagules during the first stage of invasion. Hydrobiologia 746:193–196

    Article  Google Scholar 

  • Thomaz SM, Michelan TS (2011) Associations between a highly invasive species and native macrophytes differ across spatial scales. Biol Inv 13:1881–1891

    Article  Google Scholar 

  • Thomaz SM, Chambers PA, Pierini SA, Pereira G (2007) Effects of phosphorus and nitrogen amendments on the growth of Egeria najas. Aquat Bot 86:191–196

    Article  CAS  Google Scholar 

  • Thomaz SM, Agostinho AA, Gomes LC, Silveira MJ, Rejmánek M, Aslan CE, Chow E (2012) Using space-for-time substitution and time sequence approaches in invasion ecology. Fresh Biol 13:2401–2410

    Article  Google Scholar 

  • Thouvenot L, Thiebaut G (2018) Regeneration and colonization abilities of the invasive species Elodea canadensis and Elodea nuttallii under a salt gradient: implications for freshwater invasibility. Hydrobiologia 817:193–203

    Article  CAS  Google Scholar 

  • Wallem PK, Anderson CB, Martínez-Pastur G, Lencinas MV (2010) Using assembly rules to measure the resilience of riparian plant communities to beaver invasion in subantarctic forests. Biol Invasions 12:325–335

    Article  Google Scholar 

  • Wang C, Zhang S, Li W, Wang PF, Li L (2011) Nitric oxide supplementation alleviates ammonium toxicity in the submerged macrophyte Hydrilla verticillata (L.f.) Royle. Ecotoxicol Environ Safe 74:67–73

    Article  CAS  Google Scholar 

  • Wang T, Hu JT, Liu CH, Yu D (2017) Soil type can determine invasion success of Eichhornia crassipes. Hydrobiologia 788:281–291

    Article  Google Scholar 

  • Xu X, Yang L, Huang XL, Li ZQ, Yu D (2018) Water brownification may not promote invasions of submerged non-native macrophytes. Hydrobiologia 817:215–225

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank E.R. Cunha (Universidade Estadual de Maringá) for the fruitful discussions and helping with data analyses. We also thank the Associate Editor and two anonymous reviewers whose comments improved the first version of this paper. S.M. Thomaz is especially thankful to the National Council for Scientific and Technological Development (CNPq) for providing continuous funding through a Research Productivity Grant. M.J. Silveira thanks CAPES, an organization of the Brazilian Government for the training of human resources, for providing a PhD scholarship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. J. Silveira.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

27_2018_614_MOESM1_ESM.doc

Figure S1: The map demonstrates the study areas in the Rosana Reservoir of Brazil investigated and the invaded (●) and non-invaded (○) sites by H. verticillata. We did not use the data of sites inside the square, because H. verticillata was not recorded in this region. Table S1: Results of the multiple regressions logistic using the data of presence/absence of Nitella sp, Chara cf. guairensis and Egeria spp as dependent variables, and the presence/absence (invasion) of H. verticillata, period (pre-invasion and post-invasion) and Secchi disk values as predicting variables. (DOC 472 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Silveira, M.J., Thomaz, S.M. Interspecific associations between Hydrilla verticillata and three dominant native genera of submerged macrophytes are taxa dependent. Aquat Sci 81, 21 (2019). https://doi.org/10.1007/s00027-018-0614-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00027-018-0614-z

Keywords

Navigation