Abstract
Harmful algal blooms (HABs) can disrupt aquatic communities through a variety of mechanisms, especially through toxin production. Herbivorous and omnivorous zooplankton may be particularly susceptible to HAB toxins, due to their close trophic relationship to algae as grazers. In this study, the acute toxigenic effects of the haptophyte Prymnesium parvum on a zooplankton community were investigated under laboratory conditions. Total zooplankton abundances decreased during 48-h exposure, although species responses to P. parvum densities varied. Changes in community composition were driven by declines in Daphnia mendotae and Keratella spp. abundances, which resulted in an average shift in copepod abundance from 47.1 to 72.4%, and rotifer abundance from 35.0 to 7.1%. Total cladocerans were relatively unchanged in relative abundance (11.1–10.4%), though the dominant cladoceran shifted from Daphnia mendotae (61.3% of cladocerans) to Bosmina longirostris (81.5% of cladocerans). Daphnia mendotae and Keratella spp. are known to be non-selective or generalist feeders and were likely harmed through a combination of ingestion of and contact by P. parvum. Proportional increases in copepod and Bosmina abundances in the presence of P. parvum likely reflect selective or discriminate feeding abilities in these taxa. This study corroborates previous field studies showing that P. parvum can negatively affect zooplankton, reflecting species-specific differences in zooplankton-P. parvum interactions. Such changes can alter zooplankton community composition, leading to substantial food-web consequences and potential long-term ecosystem-level impacts in lakes that experience blooms.
Similar content being viewed by others
Data accessibility
Data will be made available on PANGAEA upon publication.
References
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46. https://doi.org/10.1111/j.1442-9993.2001.01070
Baker JW, Grover JP, Brooks BW, Urena-Boeck F, Roelke DL, Errera R, Kiesling RL (2007) Growth and toxicity of Prymnesium parvum (Haptophyta) as a function of salinity, light, and temperature. J Phycol 43:219–227
Barreiro A et al (2005) Relative importance of the different negative effects of the toxic haptophyte Prymnesium parvum on Rhodomonas salina and Brachionus plicatilis. Aquat Microb Ecol 38:259–267
Bednarska A, Pietrzak B, Pijanowska J (2014) Effect of poor manageability and low nutritional value of cyanobacteria on Daphnia magna life history performance. J Plankton Res 36:838–847
Beyer JE, Hambright KD (2017) Maternal effects are no match for stressful conditions: a test of the maternal match hypothesis in a common zooplankter. Funct Ecol. https://doi.org/10.1111/1365-2435.12901
Blossom HE, Rasmussen SA, Andersen NG, Larsen TO, Nielsen KF, Hansen PJ (2014) Prymnesium parvum revisited: relationship between allelopathy, ichthyotoxicity, and chemical profiles in 5 strains. Aquat Toxicol 157:159–166. https://doi.org/10.1016/j.aquatox.2014.10.006
Boyd CM (1976) Selection of particle sizes by filter-feeding copepods: a plea for reason. Limnol Oceanogr 21:175–180
Colin SP, Dam HG (2002) Testing for toxic effects of prey on zooplankton using sole versus mixed diets. Limnol Oceanogr 47:1430–1437
Dam HG (2013) Evolutionary adaptation of marine zooplankton to global change. Annu Rev Mar Sci 5:349–370. https://doi.org/10.1146/annurev-marine-121211-172229
DeMott WR (1982) Feeding selectivities and relative ingestion rates of Daphnia and Bosmina. Limnol Oceanogr 27:518–527
DeMott WR (1990) Retention efficiency, perceptual bias, and active choice as mechanisms of food selection by suspension-feeding zooplankton. In: Hughes RN (ed) Behavioural mechanisms of food selection. Springer, Berlin, pp 569–594
DeMott WR (1995) Food selection by calanoid copepods in response to between-lake variation in food abundance. Freshw Biol 33:171–180
DeMott WR, Mueller-Navarra DC (1997) The importance of highly unsaturated fatty acids in zooplankton nutrition: evidence from experiments with Daphnia, a cyanobacterium and lipid emulsions. Freshw Biol 38:649–664
Dufrêne M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–366
Edvardsen B, Paasche E (1998) Bloom dynamics and physiology of Prymnesium and Chrysochromulina. In: Anderson DM, Cemballa AD, Hallegraeff GM (eds) NATO ASI Series, Vol. G 41, Physiological ecology of harmful algal blooms, vol 41, vol G. Springer, Heildelberg, pp 193–209
Errera RM et al (2008) Effect of imbalanced nutrients and immigration on Prymnesium parvum community dominance and toxicity: results from in-lake microcosm experiments. Aquat Microb Ecol 52:33–44. https://doi.org/10.3354/ame01199
Glibert PM, Anderson DM, Gentien P, Graneli E, Sellner KG (2005) The global, complex phenomena of harmful algal blooms. Oceanography 18:136–147
Granéli E, Johansson N (2003a) Effects of the toxic haptophyte Prymnesium parvum on the survival and feeding of a ciliate: the influence of different nutrient conditions. Mar Ecol Prog Ser 254:49–56
Granéli E, Johansson N (2003b) Increase in the production of allelopathic substances by Prymnesium parvum cells grown under N- or P-deficient conditions. Harmful Algae 2:135–145
Granéli E, Turner JT (eds) (2006) Ecology of harmful algae. Springer, Berlin
Guo MX, Harrison PJ, Taylor FJR (1996) Fish kills related to Prymnesium parvum N Carter (Haptophyta) in the People’s Republic of China. J Appl Phycol 8:111–117
Gustafsson S, Rengefors K, Hansson LA (2005) Increased consumer fitness following transfer of toxin tolerance to offspring via maternal effects. Ecology 86:2561–2567. https://doi.org/10.1890/04-1710
Hallegraeff GM (1993) A review of harmful algal blooms and their apparent global increase. Phycologia 32:79–99
Hambright KD, Hairston NG, Schaffner WR, Howarth RW (2007a) Grazer control of nitrogen fixation: phytoplankton taxonomic composition and ecosystem functioning. Fundam Appl Limnol 170:103–124
Hambright KD, Hairston NG, Schaffner WR, Howarth RW (2007b) Grazer control of nitrogen fixation: synergisms in the feeding ecology of two freshwater crustaceans. Fundam Appl Limnol 170:89–101
Hambright KD, Zamor RM, Easton JD, Glenn KL, Remmel EJ, Easton AC (2010) Temporal and spatial variability of an invasive toxigenic protist in a North American subtropical reservoir. Harmful Algae 9:568–577. https://doi.org/10.1016/j.hal.2010.04.006
Hambright KD, Easton JD, Zamor RM, Beyer J, Easton AC, Allison B (2014) Regulation of growth and toxicity of a mixotrophic microbe: implications for understanding range expansion in Prymnesium parvum. Freshw Sci 33:745–754. https://doi.org/10.1086/677198
Hambright KD, Beyer JE, Easton JD, Zamor RM, Easton AC, Hallidayschult TC (2015) The niche of an invasive marine microbe in a subtropical freshwater impoundment. ISME J 9:256–264. https://doi.org/10.1038/ismej.2014.103
Hansson L-A, Gustafsson S, Rengefors K, Bomark L (2007) Cyanobacterial chemical warfare affects zooplankton community composition. Freshw Biol 52:1290–13301
Hudnell HK (ed) (2008) Cyanobacterial harmful algal blooms: state of the science and research needs, vol 619. Advances in experimental medicine and biology. Springer, New York
Huisman J, Matthijs HCP, Visser PM (eds) (2005) Harmful cyanobacteria. Springer, New York
James T, De La Cruz A (1989) Prymnesium parvum Carter (Chrysophyceae) as a suspect of mass mortalities of fish and shellfish communities in western Texas. Tex J Sci 41:429–430
Johansson N, Granéli E (1999) Influence of different nutrient conditions on cell density, chemical composition and toxicity of Prymnesium parvum (Haptophyta) in semi-continuous cultures. J Exp Mar Biol Ecol 239:243–258
Jonsson PR, Pacvia H, Toth G (2009) Formation of harmful algal blooms cannot be explained by allelopathic interactions. Proc Natl Acad Sci 106:11177–11182
Kilham SS, Kreeger DA, Lynn SG, Goulden CE, Herrera L (1998) COMBO: a defined freshwater culture medium for algae and zooplankton. Hydrobiologia 377:147–159. https://doi.org/10.1023/A:1003231628456
Lampert W (1987) Laboratory studies on zooplankton-cyanobacteria interactions. N Z J Mar Freshwat Res 21:483–490
Landsberg JH (2002) The effects of harmful algal blooms on aquatic organisms. Rev Fish Sci 10:113–390
Legrand C, Johansson N, Johnsen G, Borsheim KY, Granéli E (2001) Phagotrophy and toxicity variation in the mixotrophic Prymnesium patelliferum (Haptophyceae). Limnol Oceanogr 46:1208–1214
Lewis WMJ (1986) Evolutionary interpretations of allelochemical interactions in phytoplankton algae. Am Nat 127:184–194
Leys C, Ley C, Klein O, Bernard P, Licata L (2013) Detecting outliers: do not use standard deviation around the mean, use absolute deviation around the median. J Exp Soc Psychol 49:764–766
Michaloudi E, Moustaka-Gouni M, Gkelis S, Pantelidakis K (2009) Plankton community structure during an ecosystem disruptive algal bloom of Prymnesium parvum. J Plankton Res 31:301–309. https://doi.org/10.1093/plankt/fbn114
Nejstgaard JC, Solberg PT (1996) Repression of copepod feeding and fecundity by the toxic haptophyte Prymnesium patelliferum. Sarsia 81:339–344
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2018) vegan: community ecology package. R package version 2.5-2. https://CRAN.R-project.org/package=vegan. Accessed 7 Aug 2018
R Core Development Team (2018) R: a language and environment for statistical computing. Version 3.5.1. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. http://www.r-project.org/. Accessed 7 Aug 2018
Rashel RH, Patiño R (2017) Influence of genetic background, salinity, and inoculum size on growth of the ichthyotoxic golden alga (Prymnesium parvum). Harmful Algae 66:97–104. https://doi.org/10.1016/j.hal.2017.05.010
Remmel EJ, Hambright KD (2012) Toxin-assisted micropredation: experimental evidence shows that contact micropredation rather than exotoxicity is the role of Prymnesium toxins. Ecol Lett 15:126–132. https://doi.org/10.1111/j.1461-0248.2011.01718.x
Remmel EJ, Kohmescher N, Larson JH, Hambright KD (2011) Experimental study of harmful algae-zooplankton interactions and the ultimate grazing defense. Limnol Oceanogr 56:461–470
Roberts DW (2016) labdsv: ordination and multivariate analysis for ecology. R package version 1.8-0. https://CRAN.R-project.org/package=labdsv. Accessed 7 Aug 2018
Roelke DL et al (2007) Effects of nutrient enrichment on Prymnesium parvum population dynamics and toxicity: results from field experiments, Lake Possum Kingdom, USA. Aquat Microb Ecol 46:125–140
Roelke DL et al (2016) A chronicle of a killer alga in the west: ecology, assessment, and management of Prymnesium parvum blooms. Hydrobiologia 764:29–50. https://doi.org/10.1007/s10750-015-2273-6
Schwierzke L et al (2010) Prymnesium parvum population dynamics during bloom development: a role assessment of grazers and virus. J Am Wat Resour Assoc 46:63–75
Shumway SE, Allen SM, Boersma PD (2003) Marine birds and harmful algal blooms: sporadic victims or under-reported events? Harmful Algae 2:1–17
Shumway SE, Burkholder JM, Morton SL (eds) (2018) Harmful algal blooms: a compendium desk reference. Wiley, New York
Sikora A, Dawidowicz P (2014) Do the presence of filamentous cyanobacteria and an elevated temperature favor small-bodied Daphnia in interspecific competitive interactions? Fundam Appl Limnol 185:307–314. https://doi.org/10.1127/fal/2014/0641
Skovgaard A, Hansen PJ (2003) Food uptake in the harmful alga Prymnesium parvum mediated by excreted toxins. Limnol Oceanogr 48:1161–1166
Sommer U, Sommer F, Santer B, Jamieson C, Boersma M, Becker C, Hansen T (2001) Complementary impact of copepods and cladocerans on phytoplankton. Ecol Lett 4:545–550
Sopanen S, Koski M, Uronen P, Kuuppo P, Lehtinen S, Legrand C, Tamminen T (2008) Prymnesium parvum exotoxins affect the grazing and viability of the calanoid copepod Eurytemora affinis. Mar Ecol Prog Ser 361:191–202
Starkweather PL (1980) Aspects of the feeding behavior and trophic ecology of suspension-feeding rotifers. Hydrobiologia 73:63–72
Sunda WG, Graneli E, Gobler CJ (2006) Positive feedback and the development and persistence of ecosystem disruptive algal blooms. J Phycol 42:963–974
Tillmann U (1998) Phagotrophy by a plastidic haptophyte, Prymnesium patelliferum. Aquat Microb Ecol 14:155–160
Tillmann U (2003) Kill and eat your predator: a winning strategy of the planktonic flagellate Prymnesium parvum. Aquat Microb Ecol 32:73–84
Zamor RM, Glenn KL, Hambright KD (2012) Incorporating molecular tools into routine HAB monitoring programs: using qPCR to track invasive Prymnesium. Harmful Algae 15:1–7
Zamor RM, Franssen NR, Porter C, Patton TM, Hambright KD (2014) Rapid recovery of a fish assemblage following an ecosystem disruptive algal bloom. Freshw Sci 33:390–401
Acknowledgements
We would like to thank James Easton, Anne Easton, Richard Zamor, and Emily Remmel for early discussions that led to the development of this project, Caryn Vaughn, Lara Souza, and Dani Glidewell for comments on earlier versions of this manuscript, and Gary Wellborn, Richard Page, and Donna Cobb for assisting with coordination and facility usage at the University of Oklahoma Biological Station. This study was funded, in part, by Grants from the Oklahoma Department of Wildlife Conservation through the Sport Fish Restoration Program (Grant F-61-R), the Oklahoma Water Resources Research Institute, and the Office of the University of Oklahoma Vice President for research to KDH. BAW was funded, in part, by the University of Oklahoma Biological Station. An earlier version of this paper was submitted in partial fulfillment of the requirements for the Master of Science in Biology by BAW.
Author information
Authors and Affiliations
Contributions
BAW and KDH conceived and designed the experiment; BAW, JEB, and TCH conducted the experiment; BAW performed all sample analysis; BAW, JEB, and TCH conducted data analysis; BAW, JEB, and KDH wrote the manuscript.
Corresponding author
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.
Rights and permissions
About this article
Cite this article
Witt, B.A., Beyer, J.E., Hallidayschult, T.C. et al. Short-term toxicity effects of Prymnesium parvum on zooplankton community composition. Aquat Sci 81, 55 (2019). https://doi.org/10.1007/s00027-019-0651-2
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00027-019-0651-2