Decline of freshwater gastropods exposed to recurrent interacting stressors implying cyanobacterial proliferations and droughts
Abstract
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.
Keywords
Gastropoda Co-occurring multiple stressors Toxic blooms Water withdrawal Invasive species TrematodesNotes
Acknowledgments
We thank Valérie Briand for bibliographical assistance.
Author’s contribution
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.
References
- Acou A, Robinet T, Lance E, Gérard C, Mounaix B, Brient L, Le Rouzic B, Feunteun E (2008) Evidence of silver eels contamination by microcystin-LR at the onset of their seaward migration: what consequences for their breeding potential? J Fish Biol 72:753–762CrossRefGoogle Scholar
- Albrecht C, Kroll O, Moreno Terrazas E, Wilke T (2009) Invasion of ancient Lake Titicaca by the globally invasive Physa acuta (Gastropoda: Pulmonata: Hygrophila). Biol Invasions 11:1821–1826CrossRefGoogle Scholar
- 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
- Alonso A, Camargo JA (2003) Short-term toxicity of ammonia, nitrite, and nitrate to the aquatic snail Potamopyrgus antipodarum (Hydrobiidae, Mollusca). Bull Environ Contam Toxicol 70:1006–1012CrossRefGoogle Scholar
- Banha F, Marques M, Anastacio PM (2014) Dispersal of two freshwater invasive macroinvertebrates, Procambarus clarkii and Physella acuta, by off-road vehicles. Aquat Conserv 24:582–591CrossRefGoogle Scholar
- Baudrimont M, de Montaudouin X (2007) Evidence of an altered protective effect of metallothioneins after cadmium exposure in the digenean parasite-infected cockle (Cerastoderma edule). Parasitology 134:237–245CrossRefGoogle Scholar
- Blakely TJ, Harding JS (2005) Longitudinal patterns in benthic communities in an urban stream under restoration. N Z J Mar Freshw 39:17–28CrossRefGoogle Scholar
- Botana LM (2016) Toxicological perspective on climate change: aquatic toxins. Chem Res Toxicol 29:619–625CrossRefGoogle Scholar
- Bousset L, Pointier JP, David P, Jarne P (2014) Neither variation loss, nor change in selfing rate is associated with the worldwide invasion of Physa acuta from its native North America. Biol Invasions 16:1769–1783CrossRefGoogle 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
- Briand JF, Robillot C, Quiblier-Llobéras C, Bernard C (2002) A perennial bloom of Planktothrix agardhii (Cyanobacteria) in a shallow eutrophic French lake: limnological and microcystin production studies. Arch Hydrobiol 153:605–622CrossRefGoogle Scholar
- Buktus R, Šidagytė E, Rakauskas V, Arbačiauskas K (2014) Distribution and current status of non-indigenous mollusc species in Lithuanian inland waters. Aquat Invasions 9:95–103CrossRefGoogle Scholar
- Bush AO, Lafferty KD, Lotz JM, Shostak AW et al (1997) Parasitology meets ecology on its own terms: Margolis, revisited. J Parasitol 83:575–583CrossRefGoogle Scholar
- Cabuk Y, Arslan N, Yilmaz V (2004) Species composition and seasonal variations of the gastropoda in Upper Sakarya River system (Turkey) in relation to water quality. Acta Hydrochim Hydrobiol 32:393–400CrossRefGoogle 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
- Connell JH, Sousa WP (1983) On the evidence needed to judge ecological stability or persistence. Am Nat 121:789–824CrossRefGoogle Scholar
- De Tallarico LF (2016) Freshwater gastropods as a tool for ecotoxicology assessments in Latin America. Am Malacol Bull 33:330–336CrossRefGoogle Scholar
- Dewson ZS, James ABW, Death RG (2007) A review of the consequences of decreased flow for instream habitat and macroinvertebrates. J N Am Benthol Soc 26:401–415CrossRefGoogle Scholar
- Dillon RT (2000) The ecology of freshwater molluscs. Cambridge University Press, CambridgeCrossRefGoogle 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
- Esch GW, Fernandez JC (1994) Snail-trematode interactions and parasite community dynamics in aquatic systems: a review. Am Midl Nat 131:209–237CrossRefGoogle Scholar
- Fischer BB, Pomati F, Eggen RIL (2013) The toxicity of chemical pollutants in dynamic natural systems: the challenge of integrating environmental factors and biological complexity. Sci Total Environ 449:253–259CrossRefGoogle Scholar
- Gérard C (2000) Dynamics and structure of a benthic macroinvertebrate community in a lake after drought. J Freshw Ecol 15:65–69CrossRefGoogle Scholar
- Gérard C (2001a) Consequences of a drought on freshwater gastropod and trematode communities. Hydrobiologia 459:9–18CrossRefGoogle Scholar
- Gérard C (2001b) Structure and temporal variation on trematode and gastropod communities in a freshwater ecosystem. Parasite 8:275–287CrossRefGoogle Scholar
- Gérard C, Poullain V (2005) Variation in the response of the invasive species Potamopyrgus antipodarum (Smith) to natural (cyanobacterial toxin) and anthropogenic (herbicide atrazine) stressors. Environ Pollut 138:28–33CrossRefGoogle Scholar
- Gérard C, Brient L, Le Rouzic B (2005) Variation in the response of juvenile and adult gastropods (Lymnaea stagnalis) to cyanobacterial toxin (microcystin-LR). Environ Toxicol 20:592–596CrossRefGoogle Scholar
- Gérard C, Carpentier A, Paillisson JM (2008) Long-term dynamics and community structure of freshwater gastropods exposed to parasitism and other environmental stressors. Freshw Biol 53:1–21CrossRefGoogle Scholar
- Gérard C, Poullain V, Lance E, Acou A, Brient L, Carpentier A (2009) Influence of toxic cyanobacteria on community structure and microcystin accumulation of freshwater molluscs. Environ Pollut 157:609–617CrossRefGoogle Scholar
- Gilroy DJ, Kauffman KW, Hall RA, Huang X, Chu FS (2000) Assessing potential health risks from microcystin toxins in blue-green algae dietary supplements. Environ Health Persp 108:435–439CrossRefGoogle Scholar
- Glöer P, Meier-Brook C (1994) Süsswassermollusken. Deutscher Jugendbund für Naturbeobachtung, HamburgGoogle Scholar
- Gordy MA, Kish L, Tarrabain M, Hanington PC (2016) A comprehensive survey of larval digenean trematodes and their snail hosts in central Alberta, Canada. Parasitol Res 115:3867–3880CrossRefGoogle 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
- Head RM, Jones RI, Bailey-Watts AE (1999) An assessment of the influence of recruitment from the sediment on the development of plaktonic populations of cyanobacteria in a temperate mesotrophic lake. Freshw Biol 41:759–769CrossRefGoogle Scholar
- Hechinger RF, Lafferty KD, Huspeni TC, Brooks AJ, Kuris AM (2007) Can parasites be indicators of free-living diversity? Relationships between species richness and the abundance of larval trematodes and of local benthos and fishes. Oecologia 151:82–92CrossRefGoogle Scholar
- Heinonen J, Kukkonen JVK, Holopainen IJ (1999) The effects of parasites and temperature on the accumulation of xenobiotics in a freshwater clam. Ecol Appl 9:475–481CrossRefGoogle Scholar
- Höckendorff S, Früh D, Hormel N, Haase P, Stoll S (2015) Biotic interactions under climate warming: temperature-dependent and species-specific effects of the oligochaete Chaetogaster limnaei on snails. Freshw Sci 34:1304–1311CrossRefGoogle 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
- Huspeni TC, Lafferty KD (2004) Using larval trematodes that parasitize snails to evaluate a salt marsh restoration project. Ecol Appl 14:795–804CrossRefGoogle Scholar
- Kappes H, Hause P (2012) Slow, but steady: dispersal of freshwater mollusks. Aquat Sci 74:1–14CrossRefGoogle Scholar
- Keas BE, Blankespoor HD (1997) The prevalence of cercariae from Stagnicola emarginata (Lymnaeidae) over 50 years in Northern Michigan. J Parasitol 83:536–540CrossRefGoogle 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
- Kotak BG, Zurawell RW (2007) Cyanobacterial toxins in Canadian freshwaters: a review. Lake Reserv Manag 23:109–122CrossRefGoogle 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
- Lagrue C, Poulin R (2016) The scaling of parasite biomass with host biomass in lake ecosystems: are parasites limited by host resources? Ecography 39:507–514CrossRefGoogle Scholar
- Lake PS (2000) Disturbance, patchiness, and diversity in streams. J N Am Benthol Soc 19:573–592CrossRefGoogle Scholar
- Lance E, Brient L, Bormans M, Gérard C (2006) Interactions between Cyanobacteria and Gastropods. I. Ingestion of toxic Planktothrix agardhii by Lymnaea stagnalis and kinetics of microcystin bioaccumulation and detoxification. Aquat Toxicol 70:140–148CrossRefGoogle Scholar
- Lance E, Brient L, Bormans M, Gérard C (2007) Interactions between Cyanobacteria and Gastropods. II. Impact of toxic Planktothrix agardhii on the life-history traits of Lymnaea stagnalis. Aquat Toxicol 81:389–396CrossRefGoogle Scholar
- Lance E, Bugajny E, Bormans M, Gérard C (2008) Consumption of toxic cyanobacteria by Potamopyrgus antipodarum (Gastropoda, Prosobranchia) and consequences on life traits and microcystin accumulation. Harmful Algae 7:464–472CrossRefGoogle Scholar
- Lance E, Brient L, Carpentier A, Acou A, Marion L, Bormans M, Gérard C (2010) Impact of toxic cyanobacteria on gastropods and microcystin accumulation in a eutrophic lake (Grand-Lieu, France) with special reference to Physa (= Physella) acuta. Sci Total Environ 408:3560–3568CrossRefGoogle Scholar
- Lance E, Alonzo F, Tanguy M, Gérard C, Bormans M (2011) Impact of microcystin-producing cyanobacteria on reproductive success of Lymnaea stagnalis (Gastropoda, Pulmonata) and predicted consequences at the population level. Ecotoxicology 20:719–730CrossRefGoogle Scholar
- Lance E, Petit A, Sanchez W, Paty C, Gérard C, Bormans M (2014) Evidence of trophic transfer of microcystins from the gastropod Lymnaea stagnalis to the fish Gasterosteus aculeatus. Harmful Algae 31:9–17CrossRefGoogle Scholar
- Lemm JU, Feld CK (2017) Identification and interaction of multiple stressors in central European lowland rivers. Sci Total Environ 603–604:148–154CrossRefGoogle Scholar
- MacKenzie K, Williams MH, Williams B, MacVicar AH, Siddall R (1995) Parasites as indicators of water quality and the potential use of helminth transmission in marine pollution studies. Adv Parasitol 35:85–144CrossRefGoogle Scholar
- Mankiewicz-Boczek J, Gągała I, Kokociński M, Jurczak T, Stefaniak K (2011) Perennial toxigenic Planktothrix agardhii bloom in selected lakes of Western Poland. Environ Toxicol 26:10–20CrossRefGoogle Scholar
- Marcogliese DJ (2005) Parasites of the superorganism: are they indicators of ecosystem health? Int J Parasitol 35:705–716CrossRefGoogle Scholar
- Marcogliese DJ (2016) The distribution and abundance of parasites in aquatic ecosystems in a changing climate: more than just temperature. Integr Comp Biol 56:611–619CrossRefGoogle Scholar
- Marcogliese DJ, Pietrock M (2011) Combined effects of parasites and contaminants on animal health: parasites do matter. Trends Parasitol 27:123–130CrossRefGoogle Scholar
- Martiguez L, Buronfosse T, Beisel JN, Giambérini L (2012) Parasitism can be a confounding factor in assessing the response of zebra mussels to water contamination. Environ Pollut 162:234–240CrossRefGoogle 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
- Merlo MJ, Etchegoin JA (2010) Testing temporal stability of the larval digenean community in Heleobia conexa (Mollusca: Cochliopidae) and its possible use as an indicator of environmental fluctuations. Parasitology 138:249–256CrossRefGoogle Scholar
- Mitchell DR, Leung TLF (2016) Sharing the load: a survey of parasitism in the invasive freshwater pulmonate, Physa acuta (Hygrophila: Physidae) and sympatric native snail populations. Hydrobiologia 766:165–172CrossRefGoogle Scholar
- Morley NJ (2006) Parasitism as a source of potential distortion in studies on endocrine disrupting chemicals in molluscs. Mar Pollut Bull 52:1330–1332CrossRefGoogle Scholar
- Morley NJ (2010) Interactive effects of infectious diseases and pollution in aquatic molluscs. Aquat Toxicol 96:27–36CrossRefGoogle Scholar
- Morley NJ, Lewis JW (2007) Anthropogenic pressure on a molluscan-trematode community over a long-term period in the Basingstoke Canal, UK, and its implications for ecosystem health. EcoHealth 3:269–280CrossRefGoogle Scholar
- Morley NJ, Irwin SWB, Lewis JW (2003) Pollution toxicity to the transmission of larval digeneans through their molluscan hosts. Parasitology 126:S5–S26CrossRefGoogle Scholar
- Newcombe RG (1998) Two-sided confidence intervals for the single proportion: comparison of seven methods. Stat Med 17:857–872CrossRefGoogle Scholar
- Nunes AL, Tricarico E, Panov VE, Cardoso AC, Katsanevakis S (2015) Pathways and gateways of freshwater invasions in Europe. Aquat Invasions 10:359–370CrossRefGoogle Scholar
- Oberholster PJ, Botha AM, Ashton PJ (2009) The influence of a toxic cyanobacterial bloom and water hydrology on algal populations and macroinvertebrate abundance in the upper littoral zone of Lake Krugersdrift, South Africa. Ecotoxicology 18:34–46CrossRefGoogle Scholar
- Paerl HW, Otten TG (2013) Harmful cyanobacterial blooms: causes, consequences, and controls. Microb Ecol 65:995–1010CrossRefGoogle Scholar
- Pardo I, García L (2016) Water abstraction in small lowland streams: unforeseen hypoxia and anoxia effects. Sci Total Environ 568:226–235CrossRefGoogle 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/
- Relyea R, Hoverman J (2006) Assessing the ecology in ecotoxicology: a review and synthesis in freshwater systems. Ecol Lett 9:1157–1171CrossRefGoogle Scholar
- Richardson J (1997) Acute ammonia toxicity for eight New Zealand indigenous freshwater species. N Z J Mar Freshw 31:185–190CrossRefGoogle Scholar
- Schwarz SS, Jenkins DG (2000) Temporary aquatic habitats: constraints and opportunities. Aquat Ecol 34:3–8CrossRefGoogle Scholar
- Skulberg OM, Wayne WW, Codd GA, Skulberg R (1993) Taxonomy of toxic Cyanophyceae (Cyanobacteria). In: Falconer IR (ed) Algal toxins in seafood and drinking water. Academic Press Ltd, Cambridge, pp 145–164CrossRefGoogle Scholar
- Strayer DL (2010) Alien species in fresh waters: ecological effects, interactions with other stressors, and prospects for the future. Freshw Biol 55:152–174CrossRefGoogle Scholar
- 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
- Sumpter JP (2009) Protecting aquatic organisms from chemicals: the harsh realities. Philos Trans R Soc A 367:3877–3894CrossRefGoogle Scholar
- Tachet H, Richoux P, Bournaud M, Usseglio-Polatera P (2006) Invertébrés d’eau douce: systématique, biologie, écologie. CNRS Editions, ParisGoogle Scholar
- Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628–630CrossRefGoogle Scholar
- Turner AM, Montgomery SL (2009) Hydroperiod, predators and the distribution of physid snails across the freshwater habitat gradient. Freshw Biol 54:1189–1201CrossRefGoogle Scholar
- Van Leeuwen CHA, Huig N, Van Der Velde G, Van Alen TA, Wagemaker CAM, Sherman CDH, Klaassen M, Figuerola J (2013) How did this snail get here? several dispersal vectors inferred for an aquatic invasive species. Freshw Biol 58:88–99CrossRefGoogle Scholar
- Vinebrook RD, Cottingham KL, Norberg J, Scheffer M, Dodson SI, Maberly SC, Sommer U (2004) Impacts of multiple stressors on biodiversity and ecosystem functioning: the role of species co-tolerance. Oikos 104:451–457CrossRefGoogle Scholar
- White SH, Duivenvoorden LJ, Fabbro LD (2005) Impacts of a toxic Microcystis bloom on the macroinvertebrate fauna of Lake Elphinstone, Central Queensland, Australia. Hydrobiologia 548:117–126CrossRefGoogle Scholar
- Żbikowski J, Żbikowska E (2009) Invaders of an invader—trematodes in Potamopyrgus antipodarum in Poland. J Invertebr Pathol 101:67–70CrossRefGoogle Scholar
- Zhang D, Xie P, Liu Y, Chen J, Liang G (2007) Bioaccumulation of the hepatotoxic microcystins in various organs of a freshwater snail from a subtropical Chinese lake, Taihu Lake, with dense toxic Microcystis blooms. Environ Toxicol Chem 26:171–176CrossRefGoogle Scholar
- Zukowski S, Walker KF (2009) Freshwater snails in competition: alien Physa acuta (Physidae) and native Glyptophysa gibbosa (Planorbidae) in the River Murray, South Australia. Mar Freshw Res 60:999–1005CrossRefGoogle Scholar
- Zurawell RW, Kotak BG, Prepas EE (1999) Influence of lake trophic status on the occurrence of microcystin-LR in the tissue of pulmonate snails. Freshw Biol 42:707–718CrossRefGoogle Scholar
- Zurawell RW, Chen H, Burke JM, Prepas EE (2005) Hepatotoxic cyanobacteria: a review of the biological importance of microcystins in freshwater environments. J Toxicol Environ Health B 8:1–37CrossRefGoogle Scholar