Aquatic Ecology

, Volume 53, Issue 1, pp 79–96 | Cite as

Decline of freshwater gastropods exposed to recurrent interacting stressors implying cyanobacterial proliferations and droughts

  • Claudia GérardEmail author
  • Emilie Lance


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.


Gastropoda Co-occurring multiple stressors Toxic blooms Water withdrawal Invasive species Trematodes 



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.


  1. 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
  2. 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
  3. 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
  4. 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
  5. 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
  6. 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
  7. 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
  8. Botana LM (2016) Toxicological perspective on climate change: aquatic toxins. Chem Res Toxicol 29:619–625CrossRefGoogle Scholar
  9. 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
  10. 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
  11. 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
  12. 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
  13. 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
  14. 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
  15. 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
  16. Codd GA, Beattie KA, Raggett SL (1997) The evaluation of Envirogard Microcystin plate and tube kits. Environ Agency 47Google Scholar
  17. Combes C (1995) Interactions durables. Ecologie et evolution du parasitisme. Editions Masson, ParisGoogle Scholar
  18. Connell JH, Sousa WP (1983) On the evidence needed to judge ecological stability or persistence. Am Nat 121:789–824CrossRefGoogle Scholar
  19. De Tallarico LF (2016) Freshwater gastropods as a tool for ecotoxicology assessments in Latin America. Am Malacol Bull 33:330–336CrossRefGoogle Scholar
  20. 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
  21. Dillon RT (2000) The ecology of freshwater molluscs. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  22. 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
  23. Esch GW, Fernandez JC (1994) Snail-trematode interactions and parasite community dynamics in aquatic systems: a review. Am Midl Nat 131:209–237CrossRefGoogle Scholar
  24. 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
  25. Gérard C (2000) Dynamics and structure of a benthic macroinvertebrate community in a lake after drought. J Freshw Ecol 15:65–69CrossRefGoogle Scholar
  26. Gérard C (2001a) Consequences of a drought on freshwater gastropod and trematode communities. Hydrobiologia 459:9–18CrossRefGoogle Scholar
  27. Gérard C (2001b) Structure and temporal variation on trematode and gastropod communities in a freshwater ecosystem. Parasite 8:275–287CrossRefGoogle Scholar
  28. 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
  29. 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
  30. 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
  31. 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
  32. 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
  33. Glöer P, Meier-Brook C (1994) Süsswassermollusken. Deutscher Jugendbund für Naturbeobachtung, HamburgGoogle Scholar
  34. 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
  35. 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
  36. 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
  37. 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
  38. 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
  39. 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
  40. 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
  41. Hudson PJ, Dobson AP, Lafferty KD (2006) Is a healthy ecosystem one that is rich in parasite species? TREE 21:381–385Google Scholar
  42. Huspeni TC, Lafferty KD (2004) Using larval trematodes that parasitize snails to evaluate a salt marsh restoration project. Ecol Appl 14:795–804CrossRefGoogle Scholar
  43. Kappes H, Hause P (2012) Slow, but steady: dispersal of freshwater mollusks. Aquat Sci 74:1–14CrossRefGoogle Scholar
  44. 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
  45. 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
  46. Kotak BG, Zurawell RW (2007) Cyanobacterial toxins in Canadian freshwaters: a review. Lake Reserv Manag 23:109–122CrossRefGoogle Scholar
  47. 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
  48. 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
  49. Lake PS (2000) Disturbance, patchiness, and diversity in streams. J N Am Benthol Soc 19:573–592CrossRefGoogle Scholar
  50. 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
  51. 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
  52. 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
  53. 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
  54. 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
  55. 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
  56. Lemm JU, Feld CK (2017) Identification and interaction of multiple stressors in central European lowland rivers. Sci Total Environ 603–604:148–154CrossRefGoogle Scholar
  57. 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
  58. 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
  59. Marcogliese DJ (2005) Parasites of the superorganism: are they indicators of ecosystem health? Int J Parasitol 35:705–716CrossRefGoogle Scholar
  60. 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
  61. Marcogliese DJ, Pietrock M (2011) Combined effects of parasites and contaminants on animal health: parasites do matter. Trends Parasitol 27:123–130CrossRefGoogle Scholar
  62. 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
  63. 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
  64. 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
  65. 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
  66. 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
  67. Morley NJ (2010) Interactive effects of infectious diseases and pollution in aquatic molluscs. Aquat Toxicol 96:27–36CrossRefGoogle Scholar
  68. 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
  69. Morley NJ, Irwin SWB, Lewis JW (2003) Pollution toxicity to the transmission of larval digeneans through their molluscan hosts. Parasitology 126:S5–S26CrossRefGoogle Scholar
  70. Newcombe RG (1998) Two-sided confidence intervals for the single proportion: comparison of seven methods. Stat Med 17:857–872CrossRefGoogle Scholar
  71. 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
  72. 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
  73. Paerl HW, Otten TG (2013) Harmful cyanobacterial blooms: causes, consequences, and controls. Microb Ecol 65:995–1010CrossRefGoogle Scholar
  74. Pardo I, García L (2016) Water abstraction in small lowland streams: unforeseen hypoxia and anoxia effects. Sci Total Environ 568:226–235CrossRefGoogle Scholar
  75. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  76. Relyea R, Hoverman J (2006) Assessing the ecology in ecotoxicology: a review and synthesis in freshwater systems. Ecol Lett 9:1157–1171CrossRefGoogle Scholar
  77. Richardson J (1997) Acute ammonia toxicity for eight New Zealand indigenous freshwater species. N Z J Mar Freshw 31:185–190CrossRefGoogle Scholar
  78. Schwarz SS, Jenkins DG (2000) Temporary aquatic habitats: constraints and opportunities. Aquat Ecol 34:3–8CrossRefGoogle Scholar
  79. 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
  80. 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
  81. Strzelec M, Michalik-Kucharz A (2003) The gastropod fauna of an unstabilised dam reservoir in Southern Poland. Malakol Abh 21:43–47Google Scholar
  82. 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
  83. Sumpter JP (2009) Protecting aquatic organisms from chemicals: the harsh realities. Philos Trans R Soc A 367:3877–3894CrossRefGoogle Scholar
  84. Tachet H, Richoux P, Bournaud M, Usseglio-Polatera P (2006) Invertébrés d’eau douce: systématique, biologie, écologie. CNRS Editions, ParisGoogle Scholar
  85. Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628–630CrossRefGoogle Scholar
  86. Turner AM, Montgomery SL (2009) Hydroperiod, predators and the distribution of physid snails across the freshwater habitat gradient. Freshw Biol 54:1189–1201CrossRefGoogle Scholar
  87. 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
  88. 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
  89. 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
  90. Żbikowski J, Żbikowska E (2009) Invaders of an invader—trematodes in Potamopyrgus antipodarum in Poland. J Invertebr Pathol 101:67–70CrossRefGoogle Scholar
  91. 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
  92. 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
  93. 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
  94. 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

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.UMR CNRS 6553 ECOBIOUniversité de Rennes 1Rennes CedexFrance
  2. 2.UMR-I 02 SEBIOUniversité de Reims Champagne-ArdenneReims CedexFrance
  3. 3.UMR 7245 MNHN/CNRS Molécules de Communication et Adaptation des Microorganismes, équipe Cyanobactéries Cyanotoxines et EnvironnementMuséum National d’Histoire NaturelleParisFrance

Personalised recommendations