Skip to main content
Log in

Didymosphenia geminata habitat requirements are unique and variable for cell establishment and mat accumulation

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Didymosphenia geminata is a freshwater diatom that can form thick mats that alter benthic habitat and community structure. In North America, mats now occur in streams outside historical observation ranges, necessitating a better understanding of conditions that support colonization and mat development to predict future occurrences and manage nuisance mats. A subbasin-level approach to relate D. geminata to habitat parameters was taken to minimize ecoregional and climatic differences among 24 sites in the geologically diverse upper Tennessee River basin, USA. Mat occurrence peaked at parameter concentrations slightly above those where D. geminata was absent; supporting previous studies that suggest nutrient limitation induces mat formation. However, unlike previous findings that suggest low dissolved phosphorus (P) is the main trigger of stalk formation, mat presence in this study was not correlated to dissolved P. Several water quality parameters, including water chemistry, temperature, and discharge, were correlated with D. geminata presence and abundance, but the strength of these relationships varied seasonally. These results support the idea that a hierarchical framework of habitat parameters is required for colonization and mat development, and that mat formation is related to stress. Differing conditions supporting cell proliferation and mat development may help explain the inconsistent nature of mats across a region. As parameters other than P may also be important in triggering stalk production, manipulating those may be useful in managing mat biomass.

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

Similar content being viewed by others

References

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

    Article  CAS  Google Scholar 

  • Alexander, R. B. & R. A. Smith, 2006. Trends in the nutrient enrichment of US rivers during the late 20th century and their relation to changes in probable stream trophic conditions. Limnology and Oceanography 51: 639–654.

    Article  CAS  Google Scholar 

  • Anderson, M. J., K. E. Ellingsen & B. H. McArdle, 2006. Multivariate dispersion as a measure of beta diversity. Ecology Letters 9: 683–693.

    Article  Google Scholar 

  • APHA, 2005. Standard methods for the examination of water and wastewater, 21st ed. American Public Health Association, Washington, DC.

    Google Scholar 

  • Bergey, E. A. & S. A. Spaulding, 2015. Didymosphenia: it’s more complicated. BioScience 65: 225.

    Article  Google Scholar 

  • Beville, S. T., G. N. Kerr & K. F. D. Hughey, 2012. Valuing impacts of the invasive alga Didymosphenia geminata on recreational angling. Ecological Economics 82: 1–10.

    Article  Google Scholar 

  • Biggs, B. J. F., R. A. Smith & M. J. Duncan, 1999. Velocity and sediment disturbance of periphyton in headwater streams: biomass and metabolism. Journal of the North American Benthological Society 18: 222–241.

    Article  Google Scholar 

  • Bothwell, M. L. & C. Kilroy, 2011. Phosphorus limitation of the freshwater benthic diatom Didymosphenia geminata determined by the frequency of dividing cells. Freshwater Biology 56: 565–578.

    Article  CAS  Google Scholar 

  • Bothwell, M. L. & B. W. Taylor, 2017. Blooms of benthic diatoms in phosphorus-poor streams. Frontiers in Ecology and the Environment 15: 110–111.

    Article  Google Scholar 

  • Bothwell, M. L., D. R. Lynch, H. Wright & J. Deniseger, 2009. On the boots of fishermen: the history of didymo blooms on Vancouver Island, British Columbia. Fisheries 34: 382–388.

    Article  Google Scholar 

  • Bothwell, M. L., B. W. Taylor & C. Kilroy, 2014. The Didymo story: the role of low dissolved phosphorus in the formation of Didymosphenia geminata blooms. Diatom Research 29: 229–236.

    Article  Google Scholar 

  • Bray, J., J. Harding, C. Kilroy, P. Broady & P. Gerbeaux, 2016. Physicochemical predictors of the invasive diatom Didymosphenia geminata at multiple spatial scales in New Zealand Rivers. Aquatic Ecology 50: 1–14.

    Article  CAS  Google Scholar 

  • Bray, J., C. Kilroy, P. Gerbeaux & J. S. Harding, 2017. Ecological eustress? Nutrient supply, bloom stimulation and competition determine dominance of the diatom Didymosphenia geminata. Freshwater Biology 62: 1433–1442.

    Article  CAS  Google Scholar 

  • Breiman, L., 2001. Random forests. Machine Learning 45: 5–32.

    Article  Google Scholar 

  • Burnham, K. P. & D. R. Anderson, 2002. Model Selection and Inference: A Practical Information-Theoretic Approach, 2nd ed. Springer, New York.

    Google Scholar 

  • Chu, S. P., 1942. The influence of the mineral composition of the medium on the growth of planktonic algae: part I. Methods and culture media. The Journal of Ecology 30: 284–325.

    Article  CAS  Google Scholar 

  • Cooksey, K. E., 1981. Requirement for calcium in adhesion of a fouling diatom to glass. Applied and Environmental Microbiology 41: 1378–1382.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cullis, J. D. S., C. A. Gillis, M. L. Bothwell, C. Kilroy, A. Packman & M. Hassan, 2012. A conceptual model for the blooming behavior and persistence of the benthic mat-forming diatom Didymosphenia geminata in oligotrophic streams. Journal of Geophysical Research 117(G2): 2156–2202. https://doi.org/10.1029/2011JG001891.

    Article  Google Scholar 

  • Cutler, D. R., T. C. Edwards, K. H. Beard, A. Cutler, K. T. Hess, J. Gibson & J. J. Lawler, 2007. Random forests for classification in ecology. Ecology 88: 2783–2792.

    Article  Google Scholar 

  • Davies, J. P. & A. R. Grossman, 1998. Responses to deficiencies in macronutrients. In Rochaix, J.-D., M. Goldschmidt-Clermont & S. Merchant (eds), The Molecular Biology of Chloroplasts and Mitochondria in Chlamydomonas. Kluwer Academic Publishers, Dordrecht: 613–633.

    Google Scholar 

  • Dodds, W. K., J. R. Jones & E. B. Welch, 1998. Suggested classification of stream trophic state: distributions of temperate stream types by chlorophyll, total nitrogen, and phosphorus. Water Research 32: 1455–1462.

    Article  CAS  Google Scholar 

  • Duncan, A. M., C. Kilroy, C. Vieglais & F. Velvin, 2007a. Protocol for the collection of samples for delimiting surveys for Didymosphenia geminata for microscopic analysis. Biosecurity New Zeland. NIWA Client Report: CHC2007-110.

  • Duncan, A. M., C. Kilroy, C. Vieglais & F. Velvin, 2007b. Protocol for the collection of samples for delimiting surveys for Didymosphenia geminata for microscopic and DNA analysis. Biosecurity New Zeland, NIWA Client Report: CHC2007-102.

  • Elwell, L. C., C. A. Gillis, L. A. Kunza & M. D. Modley, 2014. Management challenges of Didymosphenia geminata. Diatom Research 29: 303–305.

    Article  Google Scholar 

  • Flum, T. & S. C. Nodvin, 1995. Factors affecting streamwater chemistry in the Great Smoky Mountains, USA. Water, Air, and Soil Pollution 85: 1707–1712.

    Article  CAS  Google Scholar 

  • Geesey, G. G., B. Wigglesworth-Cooksey & K. E. Cooksey, 1999. Influence of calcium and other cations on surface adhesion of bacteria and diatoms: a review. The Journal of Bioadhesion and Biofilm Research 15: 195–205.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Gillis, C. A., S. J. Dugdale & N. E. Bergeron, 2018. Effect of discharge and habitat type on the occurrence and severity of Didymosphenia geminata mats in the Restigouche River, eastern Canada. Ecohydrology. https://doi.org/10.1002/eco.1959.

    Article  Google Scholar 

  • Giordano, M., A. Norici & R. Hell, 2005. Sulfur and phytoplankton: acquisition, metabolism and impact on the environment. New Phytologist 166: 317–382.

    Article  Google Scholar 

  • Gretz, M. R., 2008. The stalks of didymo, in Proceedings of the 2007 International Workshop on Didymosphenia geminata, Canadian Technical Report of Fisheries and Aquatic Sciences, 2795, 58 pp., Fish. and Oceans Can., Nanaimo, B. C., Canada.

  • Hastie, T., R. Tibshirani, & J. Friedman, 2001. The Elements of Statistical Learning: Data mining, Inference, and Prediction. Springer, New York.

    Book  Google Scholar 

  • Hawkesford, M. J. & J. L. Wray, 2000. Molecular genetics of sulfur assimilation. Advances in Botanical Research 33: 159–223.

    Article  CAS  Google Scholar 

  • Higgins, J. M. & K. Byung, 1981. Phosphorus retention models for Tennessee Valley Authority reservoirs. Water Resources Research 17(3): 571–576.

    Article  Google Scholar 

  • Jackson, L. J., L. Corbett & G. Scrimgeour, 2015. Environmental constraints on Didymosphenia geminata occurrence and bloom formation in Canadian Rocky Mountain lotic systems. Canadian Journal of Fisheries and Aquatic Sciences 73: 964–972.

    Article  Google Scholar 

  • James, D. A., M. L. Bothwell, S. R. Chipps & J. Carreiro, 2015. Use of phosphorus to reduce blooms of the benthic diatom Didymosphenia geminata in an oligotrophic stream. Freshwater Science 34: 1272–1281.

    Article  Google Scholar 

  • James, D. A. & S. R. Chipps, 2016. Influence of Didymosphenia geminata blooms on prey composition and associated diet and growth of brown trout. Transactions of the American Fisheries Society 145: 195–205.

    Article  CAS  Google Scholar 

  • James, D. A., K. Mosel & S. R. Chipps, 2014. The influence of light, stream gradient, and iron on Didymosphenia geminata bloom development in the Black Hills, South Dakota. Hydrobiologia 721: 117–127.

    Article  CAS  Google Scholar 

  • Jaramillo, A., D. Osman, L. Caputo & L. Cardenas, 2015. Molecular evidence of a Didymosphenia geminata (Bacillariophyceace) invasion in Chilean freshwater systems. Harmful Algae 49: 117–123.

    Article  CAS  Google Scholar 

  • Jellyman, P. G. & J. S. Harding, 2016. Disentangling the stream community impacts of Didymosphenia geminata: how are higher trophic levels affected? Biological Invasions 18: 3419–3435.

    Article  Google Scholar 

  • Kamil, B. 2018. MuMIn:Multi-Model Inference. R package version 1.40.4. https://Cran.R-project.org/package=MuMIn.

  • Kilroy, C., 2004. A New Alien Diatom, Didymosphenia geminata (Lyngbye) Schmidt: Its biology, distribution, effects and potential risks for New Zealand fresh waters. National Institute of Water & Atmospheric Research Ltd, Christchurch, New Zealand, Client Report: CHC2004-128.

  • Kilroy, C., 2007. Protocol for microscopic analysis of samples for the detection of Didymosphenia geminata. NIWA Client Report: CHC2007-071.

  • Kilroy, C. & M. L. Bothwell, 2011. Environmental control of stalk length in the bloom-forming, freshwater benthic diatom Didymosphenia geminata (Bacillariophyceae). Journal of Phycology 47: 981–989.

    Article  Google Scholar 

  • Kilroy, C. & M. L. Bothwell, 2012. Didymosphenia geminata growth rates and bloom formation in relation to ambient dissolved phosphorus concentration. Freshwater Biology 57: 641–653.

    Article  CAS  Google Scholar 

  • Kilroy, C. & M. L. Bothwell, 2014. Attachment and short-term stalk development of Didymosphenia geminata: effects of light temperature and nutrients. Diatom Research 29: 237–248.

    Article  Google Scholar 

  • Kilroy, C. & S. T. Larned, 2016. Contrasting effects of low-level phosphorus and nitrogen enrichment on growth of the mat-forming alga Didymosphenia geminata in an oligotrophic river. Freshwater Biology 61: 1550–1567.

    Article  CAS  Google Scholar 

  • Kilroy, C., S. T. Larned & B. J. F. Biggs, 2009. The non-indigenous diatom Didymosphenia geminata alters benthic communities in New Zealand. Freshwater Biology 54: 1990–2002.

    Article  Google Scholar 

  • Kilroy, C., T. H. Snelder, O. Floerl, C. C. Vieglais & K. L. Dey, 2008. A rapid technique for assessing the suitability of areas for invasive species applied to New Zealand’s rivers. Diversity and Distribution 14: 262–272.

    Article  Google Scholar 

  • Kirkwood, A. E., T. Shea, L. J. Jackson & E. McCauley, 2007. Didymosphenia geminata in two Alberta headwater rivers: an emerging invasive species that challenges conventional views on algal bloom development. Canadian Journal of Fisheries and Aquatic Sciences 64: 1703–1709.

    Article  CAS  Google Scholar 

  • Kirkwood, A. E., T. Shea, L. J. Jackson & E. McCauley, 2009. Are dams hotspots for Didymosphenia geminata blooms? Freshwater Biology 54: 1856–1863.

    Article  CAS  Google Scholar 

  • Kumar, S., S. A. Spaulding, T. J. Stiglgren, K. A. Hermann, T. S. Schmidt & L. L. Bahls, 2009. Potential habitat distribution for the freshwater diatom Didymosphenia Geminata in the continental U.S. Frontiers in Ecology and the Environment 7: 415–420.

    Article  Google Scholar 

  • Kunza, L. A., C. A. Gillis, J. Z. Haueter, J. N. Murdock & J. M. O’Brien, 2018. Declining phosphorus as a potential driver for the onset of Didymosphenia geminata mats in North American rivers. River Research and Applications. https://doi.org/10.1002/rra.3332.

    Article  Google Scholar 

  • Ladrera, R., J. Gomà & N. Prat, 2016. Regional distribution and temporal changes in density and biomass of Didymosphenia geminata in two Mediterranean river basins. Aquatic Invasions 11: 355–367.

    Article  Google Scholar 

  • Larned, S. & C. Kilroy, 2014. Effects of Didymosphenia geminata removal on river macroinvertebrate communities. Journal of Freshwater Ecology 29: 345–362.

    Article  Google Scholar 

  • Lavery, J. M., J. Kurek, K. M. Rühland, C. A. Gillis, M. F. Pisaric & J. P. Smol, 2014. Exploring the environmental context of recent Didymosphenia geminata proliferation in Gaspésie, Quebec, using paleolimnology. Canadian Journal of Fisheries and Aquatic Sciences 71: 616–626.

    Article  Google Scholar 

  • Lewis, W. M. & J. H. McCutchan, 2010. Ecological responses to nutrients in streams and rivers of the Colorado Mountains and foothills. Freshwater Biology 55: 1973–1983.

    Article  Google Scholar 

  • Liaw, A. & M. Wiener, 2002. Classification and regression by random forest. R News 2: 18–22.

    Google Scholar 

  • Maavara, T., C. T. Parsons, C. Ridenour, S. Stojanovic, H. H. Dürr, H. R. Powley & P. Van Cappellen, 2015. Global phosphorus retention by river damming. Proceedings of the National Academy of Sciences 112: 15603–15608.

    CAS  Google Scholar 

  • Miller, M. P., D. M. McKnight, J. D. Cullis, A. Greene, K. Vietti & D. Liptzin, 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 

  • Moffat, M. C., 1994. Ultrastructural study of Didymosphenia geminata (Bacillariophyceae). Transactions of the American Microscopical Society 113: 59–71.

    Article  Google Scholar 

  • Montecino, V., X. Molina, M. L. Bothwell, P. Muñoz, M. L. Carrevedo, F. Salinas, S. Kumar, M. L. Castillo, G. Bizama & R. O. Bustamante, 2016. Spatio temporal population dynamics of the invasive diatom Didymosphenia geminata in central-southern Chilean rivers. Science of the Total Environment 568: 1135–1145.

    Article  CAS  Google Scholar 

  • Oksanen, J., F. G. Blanchet, R. Kindt, P. Legendre, O’hara, G. L. Simpson & H. Wagner, 2010. Cegan: Community Ecology Package. R package version 1.17-2. R Development Core Team. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.

  • Pinheiro, J., D. Bates, S. DebRoy & D. Sarkar, 2018, nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-137. https://CRAN.R-project.org/package=nlme.

  • Poff, L. N., J. D. Allan, M. B. Bain, J. R. Karr, K. L. Prestegaard, B. D. Richter, R. E. Sparks & J. C. Stromberg, 1997. The natural flow regime. Bioscience 47: 769–784.

    Article  Google Scholar 

  • Potapora, M. & D. F. Charles, 2003. Distribution of benthic diatoms in U.S. rivers in relation to conductivity and ionic composition. Freshwater Biology 48: 1311–1328.

    Article  Google Scholar 

  • Root, S. & C. M. O’Reily, 2012. Didymo control: increasing the effectiveness of decontamination strategies and reducing spread. Fisheries 37: 440–448.

    Article  Google Scholar 

  • Rost, A. L., C. H. Fritsen & C. J. Davis, 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 

  • Sanmiguel, A., S. Blanco, I. Álvarez-Blanco, C. Cejudo-Figueiras, A. Escudero, M. E. Pérez, G. Noyon & E. Bécares, 2016. Recovery of the algae and macroinvertebrate benthic community after Didymosphenia geminata mass growths in Spanish rivers. Biological Invasions 18: 1467–1484.

    Article  Google Scholar 

  • Schneider, C. A., W. S. Rasband & K. W. Eliceiri, 2012. NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9: 671–675.

    Article  CAS  Google Scholar 

  • Schweiger, E. W, I. W. Ashton, C. C. Muhlfeld, L. A. Jones & L. L. Bahls, 2011. The distribution and abundance of a nuisance native alga, Didymosphenia geminata, in streams of Glacier National Park: Climate drivers and management implications. Park Science 28: 88–91.

    Google Scholar 

  • Schroeder, O., 2005. Invasive algae “Didymo” found in Tennessee River. Tennessee Wildlife Resources Agency. 2005-09-01.

  • Shelby, E. L., 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: 42 pp

  • Smith, D. J. & G. J. C. Underwood, 2000. The production of extracellular carbohydrates by estuarine benthic diatoms: the effects of growth phase and light and dark treatment. Journal of Phycology 36: 321–333.

    Article  CAS  Google Scholar 

  • Smith, F. W., M. J. Hawkesford, P. M. Ealing, D. T. Clarkson, P. J. Berg, A. R. Belcher & A. G. Warrilow, 1997. Regulation of expression of a cDNA from barley roots encoding a high affinity sulfate transporter. The Plant Journal 12: 875–884.

    Article  CAS  Google Scholar 

  • Spaulding, S. A & L. Elwell, 2007. Increase in nuisance blooms and geographic expansion of the freshwater diatom Didymosphenia geminata: recommendations for response. Joint publication from US EPA Region 8 and Federation of Fly Fishers, Livingston, Mont.

  • Staats, N., L. J. Stal, B. Winder & L. R. Mur, 2000. Oxygenic photosynthesis as driving process in exopolysaccharide production of benthic diatoms. Marine Ecology Press Series 193: 261–269.

    Article  CAS  Google Scholar 

  • Sun, C. J., G. E. Fantner, J. Adams, P. K. Hansma & J. H. Waite, 2007. The role of calcium and magnesium in the concrete tubes of the sandcastle worm. The Journal of Experimental Biology 210: 1481–1488.

    Article  CAS  Google Scholar 

  • Sundareshwar, P. V., S. Upadhayay, M. Abessa, S. Honomichl, B. Berdanier & S. A. Spaulding, 2011. Didymosphenia geminata: algal blooms in oligotrophic streams and rivers. Geophysical Research Letters 38: L10405.

    Article  Google Scholar 

  • Taylor, B. W. & M. L. Bothwell, 2014. The origin of invasive microorganisms matters for science, policy, and management: the case of Didymosphenia geminata. BioScience 64: 531–538.

    Article  Google Scholar 

  • Taylor, B. W. & M. L. Bothwell, 2015. Response to Bergey and Spaulding. BioScience 65: 226.

    Article  Google Scholar 

  • Tennessee Department of Environment and Conservation, 2010. Quality system standard operating procedure for periphyton stream surveys. Division of Water Pollution Control.

  • Tomas, P., C. Oscoz, C. Duran, D. Fernandez & J. P. Marin, 2010. Distribution of the bloom-forming diatom Didymosphenia geminata in the Ebro River basin (Northeast Spain) in the period 2006–2009. Aquatic Invasions 5: 285–289.

    Article  Google Scholar 

  • Wetzel, R. G., 2001. Limnology: lakes and river ecosystems. Academic Press, San Diego.

    Google Scholar 

  • Whitton, B., N. Ellwood & B. Kawecha, 2009. Biology of the freshwater diatom Didymosphenia: a review. Hydrobiologia 630: 1–37.

    Article  CAS  Google Scholar 

  • Wong, W. H., J. J. Dudula, T. Beaudoin, K. Groff, W. Kimball & J. Swigor, 2018. Declining ambient water phosphorus concentrations in Massachusetts’ rivers from 1999 to 2013: Environmental protection works. Water Research 139: 108–117.

    Article  CAS  Google Scholar 

  • Yildiz, F. H., J. P. Davies & A. R. Grossman, 1994. Characterization of sulfate transport in Chlamydomonas reinhardti during sulfur-limited and sulfur-sufficient growth. Plant Physiology 104: 981–987.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Matt Kulp for assistance with site selection and access to streams in Great Smoky Mountains National Park, and Natalie Knorp, Kate Henderson, Andrea Engle, Cole Harty, Matthew Padgett, James Barlow and Kelly Dunham for field and laboratory assistance. Research was funded by the National Park Service, the Tallasee Fund and the Tennessee Little River Chapter of Trout Unlimited, TN and NC.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lucas A. Hix.

Additional information

Handling editor: David Philip Hamilton

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 62 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hix, L.A., Murdock, J.N. Didymosphenia geminata habitat requirements are unique and variable for cell establishment and mat accumulation. Hydrobiologia 828, 147–164 (2019). https://doi.org/10.1007/s10750-018-3809-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-018-3809-3

Keywords

Navigation