Decline of freshwater gastropods exposed to recurrent interacting stressors implying cyanobacterial proliferations and droughts
Freshwater biota increasingly undergo multiple stressors, but we poorly understand to what extent they influence the dynamics of community structure. Here, we study the impact of combined stressor exposure on gastropods at 9-year interval, through a monthly 1-year (2013) monitoring, also providing data on the occurrence of other macroinvertebrate taxa. Previous study in 2004 showed the occurrence of cyanobacterial proliferations, drought, trematode parasites and invasive non-native pulmonate Physa acuta. During the year 2013, we always detected cyanobacterial microcystins (MCs) in gastropods, from 59 to 4149 ng g−1 fresh mass (vs. 0–246 ng g−1 in 2004), suggesting a continuous and increased MC intoxication. Environmental intracellular MC concentrations were high (8–41 µg L−1) from August to October 2013, whereas they were detected only in August 2004 (17 µg L−1). In 2013, we recorded no trematodes among the 2490 sampled gastropods, and P. acuta represented 94% of gastropods (vs. 58% in 2004). After August 2013, nearly all gastropods disappeared as most other macroinvertebrates (except Chironomidae, Ephemeroptera and Trichoptera). The whole decline of gastropods and other macroinvertebrates, and the absence of trematodes strongly suggest adverse conditions in the study site. Despite acute stressful conditions suggested above, gastropod abundance was 13-fold higher in June 2013 (vs. 2004), reflecting successful recolonization and efficient breeding. Most gastropods exposed to drought and toxic bloom were young vulnerable stages. Thus, we supposed alternation of local gastropod extinctions versus recolonization that could induce, on a long term, a loss of diversity to the detriment of the most sensitive species.
KeywordsGastropoda Co-occurring multiple stressors Toxic blooms Water withdrawal Invasive species Trematodes
We thank Valérie Briand for bibliographical assistance.
All of the authors read and approved the paper.
Compliance with ethical standards
Conflict of interest
The authors declare that there is no conflict of interest.
- Aldridge DW (1983) Physiological ecology of freshwater prosobranchs. In: Russell-Hunter WD (ed) The Mollusca, vol 6. Academic Press, New York, pp 329–358Google Scholar
- Brackenbury TD, Appleton CC (1993) Recolonization of the Umsindusi River, Natal, South Africa, by the invasive gastropod, Physa acuta (Basommatophora, Physidae). J Med Appl Malacol 5:39–44Google Scholar
- Chorus I, Bartram J (eds) (1999) Toxic cyanobacteria in water: a guide to public health consequences, monitoring and management, Published on bahalf of UNESCO, WHO and UNEP by E&FN Spon, LondonGoogle Scholar
- Codd GA, Beattie KA, Raggett SL (1997) The evaluation of Envirogard Microcystin plate and tube kits. Environ Agency 47Google Scholar
- Combes C (1995) Interactions durables. Ecologie et evolution du parasitisme. Editions Masson, ParisGoogle Scholar
- Dudgeon D (1983) The effects of water fluctuations on a gently shelving marginal zone of Plover Cove Reservoir, Hong Kong. Arch Hydrobiol Suppl 65(2/3):163–196Google Scholar
- Glöer P, Meier-Brook C (1994) Süsswassermollusken. Deutscher Jugendbund für Naturbeobachtung, HamburgGoogle Scholar
- Habdija I, Latjner J, Belinic I (1995) The contribution of gastropod biomass in microbenthic communities in a karstic river. Int Revue Gesamten Hydrobiol Hydrogr 80:03–110Google Scholar
- Holmstrup M, Bindesbøl AM, Osstingh GJ, Duschl A, Scheil V, Köhler HR, Loureiro S, Soares AMVM, Ferreira ALG, Kienle C, Gerhardt A, Laskowski R, Kramarz PE, Bayley M, Svendsen C, Spurgeon DJ (2010) Interactions between effects of environmental chemicals and natural stressors: a review. Sci Total Environ 408:3746–3762CrossRefGoogle Scholar
- Hudson PJ, Dobson AP, Lafferty KD (2006) Is a healthy ecosystem one that is rich in parasite species? TREE 21:381–385Google Scholar
- King KC, Mac Laughin JD, Gendron AD, Paul BD, Giroux I, Rondeau B, Boily M, Juneau P, Marcogliese DJ (2007) Impacts of agriculture on the parasite communities of northern leopard frogs (Rana pipiens) in southern Quebec, Canada. Parasitology 134:2063–2080Google Scholar
- Krzyzanek E, Kasza H, Pajak G (1993) The effect of water blooms caused by blue-green algae on the bottom macrofauna in the Goczalkowice Reservoir (southern Poland) in 1992. Acta Hydrobiol 35:221–230Google Scholar
- MacMahon RF (1983) Physiological ecology of freshwater pulmonates. In: Russell-Hunter WD (ed) The Mollusca, vol 6. Academic Press, New York, pp 359–430Google Scholar
- R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
- Strzelec M, Michalik-Kucharz A (2003) The gastropod fauna of an unstabilised dam reservoir in Southern Poland. Malakol Abh 21:43–47Google Scholar
- Sulmon C, van Baaren J, Cabello-Hurtado F, Gouesbet G, Hennion F, Mony C, Renault D, Bormans M, El Amrani A, Wiegand C, Gérard C (2015) Abiotic stressors and stress responses: what commonalities appear between species across biological organization levels? Environ Pollut 202:66–77CrossRefGoogle Scholar
- Tachet H, Richoux P, Bournaud M, Usseglio-Polatera P (2006) Invertébrés d’eau douce: systématique, biologie, écologie. CNRS Editions, ParisGoogle Scholar