Responses of a tropical micro-crustacean, Daphnia lumholtzi, upon exposures to dissolved toxins and living cells of cyanobacteria
Graphical abstract
Introduction
Climate change and anthropogenic activities promote the global expansion and mass development of harmful cyanobacteria in the aquatic environment (Huisman et al., 2018). In freshwater ecosystems, bloom forming of cyanobacteria, especially Microcystis spp., causes serious problems to organisms and wildlife due to oxygen depletion during their decay and the synthesis of bioactive secondary metabolites (e.g. microcystins; Chorus and Bartram, 1999, Paerl and Fulton III, 2006, Li et al., 2010). During blooms, cyanobacteria can remain in high densities in the aquatic environment for several weeks; thus they can severely impact aquatic animals especially phytoplanktivorous zooplankton, an intermediated position in the aquatic food chain (Lampert, 2006). Cyanobacteria colonies or filaments are difficult to ingest, toxic and of low nutritional values for zooplankton as they have low content of polyunsaturated fatty acids (PUFA) and lack sterols necessary for Daphnia growth, development and reproduction (Martin-Creuzburg et al., 2008). As a consequence, the abundance of cyanobacteria and their toxins correlates negatively with zooplankton biomass and also induces a shift in zooplankton size and community composition (Hansson et al., 2007, Ger et al., 2016).
Acute and chronic toxicity of cyanobacteria and their toxins and their detrimental impacts on behaviors, biochemical responses, and life-history traits of zooplankton (e.g., Daphnia) are well known (e.g., Ghadouani et al., 2004, Dao et al., 2010, Dao et al., 2013, Ger et al., 2016). Tests for median lethal concentration (LC50) of dissolved cyanotoxins to micro-crustaceans have been mainly conducted with species of temperate regions. DeMott et al. (1991) treated temperate micro-crustaceans with pure MC-LR and reported the 48h-LC50 values ranging from 450 (Diaptomus birgei) to 21,400 g MC-LR L−1 (Daphnia pulicaria). Other studies revealed the 48h-LC50 values from 84–2550 g MCE L−1 for different clones of Daphnia magna, or from 34–1906 g MCE g−1 dry weight (DW) for Daphnia similis (Jungmann and Benndorf, 1994, Sotero-Santos et al., 2006, Okumura et al., 2007, Smutna et al., 2014). Similar studies with tropical micro-crustaceans are rare, with the 48h-LC50 values of 80–460 g MCE L−1 for Moina micrura, and 120–180 g MCE L−1 for Daphnia laevis (Herrera et al., 2015). Sprague (1971) suggested using 48h-LC50 to calculate safe concentrations (SC) of pollutants, which would not diminish the life-sustaining of aquatic organisms such as fish. The authors suggested the SC value based on the 48h-LC50 multiplied with an application factor of 0.01–0.04. Recently, Shen et al. (2019) calculated SC for D. magna exposed to the dibutyl phthalate basing on the 24h- and 48-LC50 values and the application factor of 0.3. We will calculate SC for the investigated toxins and evaluate it in terms of life trait consequences.
Likewise, investigations of chronic toxicity including life traits of cyanobacteria and their toxins to Daphnia species have focused rather on temperate Daphnia (e.g., D. magna, D. pulex, D. similis) than tropical Daphnia (e.g., D. lumholtzi) species (e.g., Hietala et al., 1997, Rohrlack et al., 2001, Lürling and Van der Grinten, 2003, Dao et al., 2010, Smutna et al., 2014, Herrera et al., 2015). Survival, body size, maturation, fecundity and reproduction of D. magna and D. pulex were significantly reduced when they were fed with cyanobacterial isolates such as Microcystis aeruginosa or Cylindrospermopsis raciborskii (Laurén-Määttä et al., 1997, Hietala et al., 1997, Gustafsson and Hansson, 2004, Nogueira et al., 2004, Trubetskova and Haney, 2006).
The responses of tropical Daphnia chronically exposed to cyanobacterial toxins have only been investigated recently. Living cells of M. aeruginosa impaired growth and survival of the tropical micro-crustaceans D. lumholtzi during 10 days of incubation (Semyalo et al., 2009). Moreover, D. lumholtzi suffered increasing impairment of life history traits over 3 generations exposed to cyanobacterial toxins and very low recovery (Dao et al., 2018). Two other tropical cladocerans (e.g. D. laevis, M. micrura) significantly reduced reproduction and enzymatic activity (catalase, glutathione S-transferase) upon exposures to toxic cyanobacterial species, M. aeruginosa and C. raciborskii (Ferrao-Filho et al., 2017).
In toxicity tests, widely distributed species M. aeruginosa, Planktothrix agardhii and C. raciborskii are often used as living cyanobacterial cultures to test the toxicity on micro-crustaceans via ingestions. Also, in tropical regions including Asia Microcystis sp. and Cylindrospermopsis sp. are dominant, and alternating between wet and dry seasons (Mowe et al., 2015). The cyanobacterium Cylindrospermopsis curvispora is a tropical and sub-tropical species, found in Zambia, Botswana, Sri Lanka, Japan, Vietnam, and Southern Africa, and can produce the toxic metabolite anatoxin-a (Cronberg and Komarek, 2004, Dao et al., 2016). However, the toxicity of the cyanobacterium C. curvispora, to tropical cladocerans has not been reported. Investigating effects of common cyanobacteria or cyanotoxins of tropical cyanobacteria (e.g. C. curvispora) on the tropical cladocerans such as D. lumholtzi would enable us to have a more comprehensive understanding and a better ecological risk assessment of cyanobacteria in tropical ecosystems. Therefore, this study investigates the survivorship, fecundity, and reproduction of D. lumholtzi upon both acute and chronic exposures to purified MC-LR, a crude extract of a water bloom sample with dominance of M. aeruginosa, and living cells of the cyanobacterium C. curvispora.
Section snippets
Chemicals and organisms for the tests
The cyanobacterium Cylindrospermopsis curvispora (Fig. 1a, b) was isolated from a pond in District 7, Hochiminh City during its mass development and cultured in Z8 medium (Kotai, 1972). The isolated strain is coiled with a diameter of between 20 – , which is ingestable for D. lumholtzi, and was a non-microcystin-producing strain (Dao et al., 2016). Microcystin-LR was purchased from Enzo Life Science Inc. (USA). It was dissolved in reversed osmosis water prior to the acute test and in
Acute effects of dissolved MCs on D. lumholtzi
In the acute test, pH and dissolved oxygen of the test solutions ranged from 6.6 – 7.6, and 6.5 – 7.7 mg L−1, respectively, which is within the suitable range for Daphnia (APHA, 2012). Any negative influences of the test solution characteristics on the survival of D. lumholtzi were unlikely. The 24h- and 48h-LC50 values for MC-LR exposures were 299 and 247 g L−1 and for MCE were 409 and 331 g L−1, respectively (Table 2). The cyanobacterial extract was presumably less toxic to D. lumholtzi
Conclusions and perspectives
In conclusion, upon exposure to dissolved microcystins, the tropical D. lumholtzi seems more sensitive than many other Daphnia species from temperate regions, in terms of survival, fecundity, and reproduction. Because survival of D. lumholtzi was strongly impaired at low microcystins concentrations, this species is recommended as a model species in studying the impacts of cyanobacteria on tropical lakes. Living cells of C. curvispora, a non-microcystins-producing strain from Vietnam, potently
CRediT authorship contribution statement
TSD raised the conceptualization and did the funding acquisition. TMCV and BTB did the investigation, methodology and data curation. TMCV wrote the original draft. All authors wrote the final manuscript. CW and VKD edited, structured the manuscript and polished the language.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
We would like to thank Prof. Tham Hoang from Loyola University Chicago for his assistance on the calculation of median lethal concentration (24h- and 48h-LC50). This research is funded by Vietnam National Foundation for Science and Technology Development (NAFOSTED) under grant number 106-NN.04-2014.69.
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