Skip to main content
Log in

Recovery of the algae and macroinvertebrate benthic community after Didymosphenia geminata mass growths in Spanish rivers

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

This study aims to assess the ecological profile of the invasive alga Didymosphenia geminata in NW Spain, analysing the biotic and abiotic factors related to the presence of massive colonies and their effect on river benthos. Physical and chemical parameters were measured in three infested rivers during 2009 and 2010, and biological samples of benthic community were taken according to standard protocols. Collected data was compared with that of control stations located in the same rivers but presenting no evident infestations. The autoecology shown by D. geminata in this study supports former observations reporting the expansion of its ecological niche, with current velocity and nutrients concentrations the environmental variables that best explain the establishment and development of mats in the studied rivers. Regarding its impact, it was observed that the mass growths of this diatom produced a dramatic change in the composition of the algae and macroinvertebrate benthic community which persisted after their disappearance. These results led to the development of a geostatistical predictive model to identify potential risk of dispersion of this diatom in Spanish rivers. The expected distribution of this algae according to this model agreed in general with the actual observed infestations, thus validating it as a tool to prevent and manage future infestations.

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
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Abbreviations

AFDW:

Phytobenthic ash-free dry weight

Chla :

Phytobenthic chlorophyll a

Cond:

Specific electric conductivity

CV:

Current velocity

DGEM:

Didymosphenia geminata

DW:

Phytobenthic dry weight

TKN:

Kjeldahl nitrogen

Phae:

Phytobenthic photosynthetically active phaeopigments

SRP:

Soluble reactive phosphorus

T:

Temperature

TOC:

Total organic carbon

TP:

Total phosphorus

References

  • Aboal M, Marco S, Chaves E, Mulero I, García-Ayala A (2012) Ultrastructure and function of stalks of the diatom Didymosphenia geminata. Hydrobiologia 695:17–24

    Article  CAS  Google Scholar 

  • AENOR (2004) Norma española UNE–EN 13946:2004. Calidad del agua. Guía para el muestreo en rutina y el pretratamiento de diatomeas bentónicas de ríos. AENOR, Madrid

    Google Scholar 

  • AENOR (2005) Norma española UNE–EN 14407:2005. Calidad del agua. Guía para la identificación, recuento e interpretación de muestras de diatomeas bentónicas de ríos. AENOR, Madrid

    Google Scholar 

  • Alba Tercedor J, Jáimez-Cuéllar P, Álvarez M, Avilés J, Bonada N, Casas J, Mellado A, Ortega M, Pardo I, Prat N, Rieradevall M, Robles S, Sáinz-Cantero CE, Sánchez-Ortega A, Suárez ML, Toro M, Vidal-Abarca MR, Vivas S, Zamora-Muñoz C (2002) Caracterización del estado ecológico de ríos mediterráneos ibéricos mediante el índice IBMWP (antes BMWP’). Limnetica 21:175–185

    Google Scholar 

  • Álvarez I, Escudero A, Cejudo C, Pérez M, Blanco S, Bécares E (2010) Control y seguimiento del alga invasora Didymosphenia geminata. CHD, Valladolid

    Google Scholar 

  • APHA (2005) Standard methods for the examination of water and wastewater. American Water Works Association, Washington

    Google Scholar 

  • Beeby J (2012) Water quality and survivability of Didymosphenia geminata. Colorado State University, Fort Collins

    Google Scholar 

  • Beltrami ME, Blanco S, Ciutti F, Cappelletti C, Monauni C, Pozzi S, Rimet F, Ector L (2008) Distribution and ecology of Didymosphenia geminata (Lyngbye) M. Schmidt (Bacillariophyta) in Trentino watercourses (northern Italy). Cryptogam Algol 29:141–160

    Google Scholar 

  • Berkson J (1944) Application of the logistic function to bio-assay. J Am Stat Assoc 39:357–365

    CAS  Google Scholar 

  • Beville ST, Kerr GN, Hughey KFD (2012) Valuing impacts of the invasive alga Didymosphenia geminata on recreational angling. Ecol Econ 82:1–10

    Article  Google Scholar 

  • Blanco S, Ector L (2008) Didymosphenia geminata (Bacillariophyta, Gomphonemataceae), una amenaza para nuestros ríos. Cuad Biodivers 26:3–6

    Article  Google Scholar 

  • Blanco S, Ector L (2009) Distribution, ecology and nuisance effects of the freshwater invasive diatom Didymosphenia geminata (Lyngbye) M. Schmidt: a literature review. Nova Hedwig 88:347–422

    Article  Google Scholar 

  • Blanco S, Ector L, Huck V, Monnier O, Cauchie HM, Hoffmann L, Bécares E (2008) Diatom assemblages and water quality assessment in the Duero basin (NW Spain). Belg J Bot 141:39–50

    Google Scholar 

  • Bland JM, Kerry SM (1998) Weighted comparison of means. BMJ 316:129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campbell ML (2005) Organism impact assessment (OIA) for potential impacts of Didymosphenia geminata. All Oceans Ecology, Melbourne

    Google Scholar 

  • CHE (2005) Metodología para el establecimiento del estado ecológico, según la Directiva Marco del Agua: protocolos de muestreo y análisis para fitobentos (microalgas bentónicas). CHE, Zaragoza

    Google Scholar 

  • Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Austr J Ecol 18:117–143

    Article  Google Scholar 

  • Corbett LM (2013) Relationships between Didymosphenia geminata occurrence, blooms and environmental conditions. Ph.D. Thesis, Univ Calgary

  • Coste M (1982) Etude des méthodes biologiques d’appréciation quantitative de la qualité des eaux. Report (CEMAGREF) QE Lyon–AF Bassin Rhône–Méditérannée–Corse

  • Coste M, Ector L (2000) Diatomées invasives exotiques ou rares en France: principales observations effectuées au cours des dernières décennies. Syst Geograph Plants 70:373–400

    Article  Google Scholar 

  • Cullis JDS, Gillis C-A, Bothwell ML, Kilroy C, Packman A, Hassan M (2012) A conceptual model for the blooming behavior and persistence of the benthic mat-forming diatom Didymosphenia geminata in oligotrophic streams. J Geophys Res 117:G00N03

    Google Scholar 

  • Cullis JDS, Crimaldi JP, McKnight DM (2013) Hydrodynamic shear removal of the nuisance stalk-forming diatom Didymosphenia geminata. Limnol Oceanogr 3:256–268

    Article  Google Scholar 

  • Cullis JDS, McKnight DM, Spaulding SA (2015) Hydrodynamic control of benthic mats of Didymosphenia geminata at the reach scale. Can J Fish Aquat Sci 72:902–914

    Article  Google Scholar 

  • Ellwood NTW, Whitton BA (2007) Importance of organic phosphate hydrolyzed in stalks of the lotic diatom Didymosphenia geminata and the possible impact of atmospheric and climatic changes. Hydrobiologia 592:121–133

    Article  CAS  Google Scholar 

  • Elwell L (2006) Increase in nuisance blooms and geographic expansion of the freshwater diatom Didymosphenia geminata: recommendations for response. Federation of Fly Fishers, Livingston

    Google Scholar 

  • Elwell LC, Gillis C-A, Kunza LA, Modley MD (2014) Management challenges of Didymosphenia geminata. Diatom Res 29:303–305

    Article  Google Scholar 

  • Falasco E, Bona F (2013) Recent findings regarding non-native or poorly known diatom taxa in north-western Italian rivers. J Limnol 72:e4

    Article  Google Scholar 

  • Freeman C, Lock MA (1995) The biofilm polysaccharide matrix: A buffer against changing organic substrate supply? Limnol Oceanogr 40:273–278

    Article  CAS  Google Scholar 

  • Furey PC, Kupferberg SJ, Lind AJ (2014) The perils of unpalatable periphyton: Didymosphenia and other mucilaginous stalked diatoms as food for tadpoles. Diatom Res 29:267–280

    Article  Google Scholar 

  • Gillis C-A, Chalifour M (2010) Changes in the macrobenthic community structure following the introduction of the invasive algae Didymosphenia geminata in the Matapedia River (Québec, Canada). Hydrobiologia 647:63–70

    Article  Google Scholar 

  • Gillis C-A, Lavoie I (2014) A preliminary assessment of the effects of Didymosphenia geminata nuisance growths on the structure and diversity of diatom assemblages of the Restigouche River basin, Quebec, Canada. Diatom Res 29:281–292

    Article  Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Palaeontological Statistics software package for education and data analysis. Palaeontol Electron 4:1–9

    Google Scholar 

  • Hansson LA, Gyllström M, Ståhl-Delbanco A, Svensson M (2004) Responses to fish predation and nutrients by plankton at different levels of taxonomic resolution. Freshw Biol 49:1538–1550

    Article  Google Scholar 

  • Hoagland KD, Rosowski JR, Gretz MR, Roemer SC (1993) Review—diatom extracellular polymeric substances: function, fine structure, chemistry, and physiology. J Phycol 29:537–566

    Article  CAS  Google Scholar 

  • Holderman C, Hardy R (2004) Kootenai River Ecosystem Project: an ecosystem approach to evaluate and rehabilitate a degraded, large riverine ecosystem. Final Report to Bonneville Power Administration, pp 49–99

  • Hustedt F (1930) Bacillariophyta (Diatomeae). Die Süsswasser-Flora Mitteleuropas. Gustav Fischer, Jena, pp 1–466

    Google Scholar 

  • James DA (2013) Risk potential for the aquatic invasive species Didymosphenia geminata to bloom in selected streams of the Black Hills, South Dakota. U.S. Fish and Wildlife Service, Colorado

    Google Scholar 

  • James DA, Ranney SH, Chipps SR, Spindler BD (2010) Invertebrate composition and abundance associated with Didymosphenia geminata in a montane stream. J Freshw Ecol 25:235–241

    Article  Google Scholar 

  • Kawecka B, Sanecki J (2003) Didymosphenia geminata in running waters of southern Poland—symptoms of change in water quality? Hydrobiologia 495:193–201

    Article  Google Scholar 

  • Kilroy C, Bothwell ML (2012) Didymosphenia geminata growth rates and bloom formation in relation to ambient dissolved phosphorus concentration: ambient phosphorus and Didymosphenia geminata blooms. Freshw Biol 57:641–653

    Article  CAS  Google Scholar 

  • Kilroy C, Bothwell ML (2014) Attachment and short-term stalk development of Didymosphenia geminata: effects of light, temperature and nutrients. Diatom Res 29:237–248

    Article  Google Scholar 

  • Kilroy C, Unwin M (2011) The arrival and spread of the bloom-forming, freshwater diatom, Didymosphenia geminata, in New Zealand. Aquat Invas 6:249–262

    Article  Google Scholar 

  • Kilroy C, Biggs B, Blair N, Lambert P, Jarvie B, Dey K, Smale D (2005) Ecological studies on Didymosphenia geminata. National Institute for Water and Atmospheric Research, Christchurch

    Google Scholar 

  • Kilroy C, Lagerstedt A, Davey A, Robinson K (2006) Studies on the survivability of the invasive diatom Didymosphenia geminata under a range of environmental and chemical conditions. National Institute of Water & Atmospheric Research, Christchurch

    Google Scholar 

  • Kilroy C, Snelder TH, Floerl O, Vieglais CC, Dey KL (2007) A rapid technique for assessing the suitability of areas for invasive species applied to New Zealand’s rivers: rapid assessment of environmental suitability. Divers Distrib 14:262–272

    Article  Google Scholar 

  • Kilroy C, Larned ST, Biggs BJF (2009) The non-indigenous diatom Didymosphenia geminata alters benthic communities in New Zealand rivers. Freshw Biol 54:1990–2002

    Article  Google Scholar 

  • Kirkwood AE, Jackson LJ, McCauley E (2009) Are dams hotspots for Didymosphenia geminata blooms? Freshw Biol 54:1856–1863

    Article  CAS  Google Scholar 

  • Kumar S, Spaulding SA, Stohlgren TJ, Hermann KA, Schmidt TS, Bahls LL (2008) Potential habitat distribution for the freshwater diatom Didymosphenia geminata in the continental US. Front Ecol Environ 7:415–420

    Article  Google Scholar 

  • Ladrera R, Rieradevall M, Prat N (2014) Massive growth of the invasive algae Didymosphenia geminata associated with discharges from a mountain reservoir alters the taxonomic and functional structure of macroinvertebrate community. River Res Appl 31:216–227

    Article  Google Scholar 

  • Lagerstedt MA (2007) Didymosphenia geminata; an example of a biosecurity leak in New Zealand. Thesis in partial fulfilment of requirements for M.Sc. in Environmental Sciences, University of Canterbury

  • Larned ST, Kilroy C (2014) Effects of Didymosphenia geminata removal on river macroinvertebrate communities. J Freshw Ecol 29:345–362

    Article  Google Scholar 

  • Larned S, Arscott D, Blair N, Jarvie B, Jellyman D, Lister K, Wilcock B (2007) Ecological studies of Didymosphenia geminata in New Zealand, 2006–2007. National Institute of Water and Atmospheric Research, New Zealand. NIWA Client Report CHC2007–070

  • Larson AM, Carreiro J (2008) Relationship between nuisance blooms of Didymosphenia geminata and measures of aquatic community composition in Rapid Creek, South Dakota. In: Proceedings of the 2007 International Workshop on Didymosphenia geminata. Canad Techn Rep Fish Aquat Sci 2795, pp 45–49

  • Lecointe C, Coste M, Prygiel J, Ector L (1999) Le logiciel OMNIDIA version 2, une puissante base de données pour les inventaires de diatomées et pour le calcul des indices diatomiques européens. Cryptogam Algol 20:132–134

    Google Scholar 

  • Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280

    Article  Google Scholar 

  • Mack RN, Simberloff D, Mark Lonsdale W, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710

    Article  Google Scholar 

  • Metzeltin D, Lange-Bertalot H (2014) The genus Didymosphenia M. Schmidt. A critical evaluation of established and description of 11 new taxa. Iconogr Diatomol 25:1–293

    Google Scholar 

  • Miller MP, McKnight DM, Cullis JD, Greene A, Vietti K, Liptzin D (2009) Factors controlling streambed coverage of Didymosphenia geminata in two regulated streams in the Colorado Front Range. Hydrobiologia 630:207–218

    Article  CAS  Google Scholar 

  • Montecino V, Molina X, Kumar S, Castillo MLC, Bustamante RO (2014) Niche dynamics and potential geographic distribution of Didymosphenia geminata (Lyngbye) M. Schmidt, an invasive freshwater diatom in Southern Chile. Aquat Invas 9:507–519

    Article  Google Scholar 

  • Patrick RM, Reimer CW (1975) The diatoms of the United States exclusive of Alaska and Hawaii. Volume 2. Part 2. Entomoneidaceae, Cymbellaceae, Gomphonemaceae, Epithemiaceae. Monogr Acad Nat Sci Phila 13:1–213

    Google Scholar 

  • Richardson DC, Oleksy IA, Hoellein TJ, Arscott DB, Gibson CA, Root SM (2014) Habitat characteristics, temporal variability, and macroinvertebrate communities associated with a mat-forming nuisance diatom (Didymosphenia geminata) in Catskill mountain streams, New York. Aquat Sci 76:553–564

    Article  CAS  Google Scholar 

  • Rost AL, Fritsen CH (2014) Influence of a tributary stream on benthic communities in a Didymosphenia geminata impacted stream in the Sierra Nevada, USA. Diatom Res 29:249–257

    Article  Google Scholar 

  • Rost AL, Fritsen CH, Davis CJ (2011) Distribution of freshwater diatom Didymosphenia geminata in streams in the Sierra Nevada, USA, in relation to water chemistry and bedrock geology. Hydrobiologia 665:157–167

    Article  CAS  Google Scholar 

  • Schmidt A (1874) Atlas der Diatomaceenkunde. Reisland, Leipzig

    Google Scholar 

  • Shannon CE, Weaver W (1949) The mathematical theory of communication. University of Illinois Press, Urbana, IL

    Google Scholar 

  • Shearer J, Erickson J (2006) Didymosphenia geminata and the Rapid Creek brown trout fishery, South Dakota. Current Knowledge of Didymosphenia geminata: Developing a Research and Management Response. Federation of Fly Fishers and EPA Region 8 celebrated in association with Western Division American Fisheries Society Annual Meeting, Bozeman. United States of America, pp 15–16

  • Shelby EL (2006) An assessment and analysis of benthic macroinvertebrate communities associated with the appearance of Didymosphenia geminata in the White River below Bull Shoals Dam. Arkansas Department of Environmental Quality, Little Rock

    Google Scholar 

  • Sournia A (1978) Phytoplankton manual. United Nations Educational, Scientific and Cultural Organization, Paris

    Google Scholar 

  • Spaulding SA, Elwell L (2007) Increase in nuisance blooms and geographic expansion of the freshwater diatom Didymosphenia geminata: Recommendations for response. US EPA, Denver

    Google Scholar 

  • Spaulding SA, Hermann K, Steuven G, Erickson KW (2005) A nuisance diatom species: Didymosphenia geminata in western streams. US EPA, Denver

    Google Scholar 

  • StatSoft I (2007) STATISTICA (data analysis software system). StatSoft, Inc., Tulsa

    Google Scholar 

  • Stevenson RJ, Bothwell ML, Owe RL (1996) Algal ecology. Academic Press, San Diego

    Google Scholar 

  • Suren AM, Biggs BJF, Duncan MJ, Bergey L, Lambert P (2003) Benthic community dynamics during summer low-flows in two rivers of contrasting enrichment 2. Invertebrates. N Z J Mar Freshw Res 37:71–83

    Article  Google Scholar 

  • Ter Braak CJF, Smilauer P (2002) Canoco. Biometris. Plant Research International, Wageningen

    Google Scholar 

  • Ter Braak CJ, Van Dam H (1989) Inferring pH from diatoms: a comparison of old and new calibration methods. Hydrobiologia 178:209–223

    Article  Google Scholar 

  • Tomás P, Oscoz J, Durán C, Fernández D, Marín JP, Miranda R, Leunda PM (2010) Distribution of the bloom-forming diatom Didymosphenia geminata in the Ebro River basin (North–East Spain) in the period 2006–2009. Aquat Invas 5:285–289

    Article  Google Scholar 

  • Turner JT, Tester PA (1997) Toxic marine phytoplankton, zooplankton grazers, and pelagic food webs. Limnol Oceanogr 42:1203–1214

    Article  Google Scholar 

  • URS (2006) Investigación del origen de depósitos sobre sustratos sumergidos en el río Ara (cuenca del Cinca). Confederación Hidrográfica del Ebro, Barcelona

    Google Scholar 

  • Van Dam H, Mertens A, Sinkeldam J (1994) A coded checklist and ecological indicator values of freshwater diatoms from the Netherlands. Neth J Aquat Ecol 28:117–133

    Article  Google Scholar 

  • Vitousek VM (1990) Biological invasions and ecosystem processes: towards an integration of population biology and ecosystem studies. Oikos 57:7–13

    Article  Google Scholar 

  • Whitton BA, Ellwood NTW, Kawecka B (2009) Biology of the freshwater diatom Didymosphenia: a review. Hydrobiologia 630:1–37

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was funded by the Duero Basin Authority (CHD, Spain). Authors are grateful to M. López and H.L. Astiárraga who contributed to field and laboratory work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Saúl Blanco.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sanmiguel, A., Blanco, S., Álvarez-Blanco, I. et al. Recovery of the algae and macroinvertebrate benthic community after Didymosphenia geminata mass growths in Spanish rivers. Biol Invasions 18, 1467–1484 (2016). https://doi.org/10.1007/s10530-016-1095-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-016-1095-4

Keywords

Navigation