Abstract
Pomacea canaliculata, a freshwater snail native to tropical and temperate South America, has become an important invader and agricultural pest throughout tropical and subtropical regions around the world. Colonization of various aquatic habitats by P. canaliculata in coastal regions of South China and its establishment potential in estuaries have raised great concern, yet little is known about the biological response of the snail and its tolerance under saline environments. We first examined the salinity tolerance of P. canaliculata using a total of 30 experimental juvenile snails exposed to eight salinity levels (from 0 to 14 psu in 2 psu steps). Daily survival of the snails was measured for each salinity treatment over 30 days. Based on salinity exposure test, influence of salinity on snail reproduction was investigated for a period of 30 days using 30 adult snails exposed to four salinity treatments (0, 2, 4 and 6 psu). Each salinity test replicated three times. Pomacea canaliculata could tolerate salinity levels ranging from 0 to 6 psu in which probability of survival was greater than 72% during a 30 days exposure. Lethal time leading to 50% mortality (LT50) of the snail declined from 71 days at 0 psu to 27 days at 6 psu. Pomacea canaliculata could ingest and reproduce normally at salinities ranging from 0 to 4 psu. Average mass daily gain, specific growth rate, and the hatching of egg clutches decreased significantly with elevated salinities. Results show a general threshold response of P. canaliculata to salinity. This freshwater snail falls into “2nd degree” euryhaline limnobionts tolerating salinities of 3–8‰.
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References
Alonso, A. & J. A. Camargo, 2003. Short-term toxicity of ammonia, nitrite, and nitrate to the aquatic snail Potamopyrgus antipodarum (Hydrobiidae, Mollusca). Bulletin of Environmental Contamination and Toxicology 70: 1006–1012.
Bailer, A. J., & W. Piegorsch. 1997. Statistics for environmental biology and toxicology. CRC Press.
Bernatis, J. L., I. J. Mcgaw & C. L. Cross, 2007. Abiotic tolerances in different life stages of apple snails Pomacea canaliculata and Pomacea maculata and the implications for distribution. Journal of Shellfish Research 35: 1013–1025.
Carlsson, N. O. L., C. Brönmark & L. Hansson, 2004. Invading herbivory: the golden apple snail alters ecosystem functioning in Asian wetlands. Ecology 85: 1575–1580.
Chen, L., W. Wang, Y. Zhang & G. Lin, 2009. Recent progresses in mangrove conservation, restoration and research in China. Journal of Plant Ecology 2: 45–54.
Chen, Y. & Y. Ye, 2014. Effects of salinity and nutrient addition on mangrove Excoecaria agallocha. PLoS One 9: e93337.
Cheng, Q., Q. Jing, R. C. Spear, J. M. Marshall, Z. Yang & P. Gong, 2016. Climate and the timing of imported cases as determinants of the dengue outbreak in Guangzhou, 2014: evidence from a mathematical model. PLoS Neglected Tropical Diseases 10: e4417.
Cooke, G. M., A. G. King, L. Miller & R. N. Johnson, 2012. A rapid molecular method to detect the invasive golden apple snail Pomacea canaliculata (Lamarck, 1822). Conservation Genetics Resources 4: 591–593.
Costil, K., G. B. J. Dussart & J. Daguzan, 2001. Biodiversity of aquatic gastropods in the Mont St-Michel basin (France) in relation to salinity and drying of habitats. Biodiversity and Conservation 10: 1–18.
Cox, D. R., 1992. Regression models and life-tables. In Kotz, S. & N. L. Johnson (eds.), Breakthroughs in Statistics: Methodology and Distribution. Springer, New York: 527–541.
De Wolf, H., T. Backejau & R. Blust, 2004. Sensitivity to cadmium along a salinity gradient in populations of the periwinkle, Littorina littorea, using time-to-death analysis. Aquatic Toxicology 66: 241–253.
Facon, B., E. Machline, J. P. Pointier & P. David, 2004. Variation in desiccation tolerance in freshwater snails and its consequences for invasion ability. Biological Invasions 6: 283–293.
Fang, L., P. K. Wong, L. Lin, C. Lan & J. Qiu, 2010. Impact of invasive apple snails in Hong Kong on wetland macrophytes, nutrients, phytoplankton and filamentous algae. Freshwater Biology 55: 1191–1204.
Flomer, O., 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3: 294–299.
Gosselin, L. A. & F. S. Chia, 1995. Characterizing temperate rocky shores from the perspective of an early juvenile snail: the main threats to survival of newly hatched Nucella emarginata. Marine Biology 122: 625–635.
Halwart, M., 1994. The golden apple snail Pomacea canaliculata in Asian rice farming systems: present impact and future threat. International Journal of Pest Management 40: 199–206.
Hayes, K. A., R. C. Joshi, S. C. Thiengo & R. H. Cowie, 2008. Out of South America: multiple origins of non-native apple snails in Asia. Diversity and Distributions 14: 701–712.
Hayes, K. A., R. H. Cowie, S. C. Thiengo & E. E. Strong, 2012. Comparing apples with apples: clarifying the identities of two highly invasive Neotropical Ampullariidae (Caenogastropoda). Zoological Journal of the Linnean Society 166: 723–753.
Hayes, K. A., R. L. Burks, A. Castro-Vazquez, P. C. Darby, H. Heras, P. R. Martín, J. Qiu, S. C. Thiengo, I. A. Vega & T. Wada, 2015. Insights from an integrated view of the biology of apple snails (Caenogastropoda: Ampullariidae). Malacologia 58: 245–303.
Horgan, F. G., A. M. Stuart & E. P. Kudavidanage, 2014a. Impact of invasive apple snails on the functioning and services of natural and managed wetlands. Acta Oecologica 54: 90–100.
Horgan, F. G., M. Imelda Felix, D. E. Portalanza, L. Sanchez, W. M. Moya Rios, S. E. Farah, J. A. Wither, C. I. Andrade & E. B. Espin, 2014b. Responses by farmers to the apple snail invasion of Ecuador’s rice fields and attitudes toward predatory snail kites. Crop Protection 62: 135–143.
Hoy, M., B. L. Boese, L. Taylor, D. Reusser & R. Rodriguez, 2012. Salinity adaptation of the invasive New Zealand mud snail (Potamopyrgus antipodarum) in the Columbia River estuary (Pacific Northwest, USA): physiological and molecular studies. Aquatic Ecology 46: 249–260.
Hoyaux, J., R. Gilles & C. Jeuniaux, 1976. Osmoregulation in molluscs of the intertidal zone. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 53: 361–365.
Hutchinson, S. & L. E. Hawkins, 1992. Quantification of the physiological responses of the European flat oyster Ostrea edulis L. to temperature and salinity. Journal of Molluscan Studies 58: 215–226.
Jacobsen, R. & V. E. Forbes, 1997. Clonal variation in life-history traits and feeding rates in the gastropod, Potamopyrgus antipodarum: performance across a salinity gradient. Functional Ecology 11: 260–267.
Jia, H., X. Jian, W. U. Sangyun, & G. F. He, 2011. Temporal and spatial variations of salinity in Pearl River Estuary in recent years. Transactions of Oceanology and Limnology 2:142–146.
Jordan, P. J. & L. E. Deaton, 1999. Osmotic regulation and salinity tolerance in the freshwater snail Pomacea bridgesi and the freshwater clam Lampsilis teres. Comparative Biochemistry and Physiology A: Molecular & Integrative Physiology 122: 199–205.
Kefford, B. J. & D. Nugegoda, 2005. No evidence for a critical salinity threshold for growth and reproduction in the freshwater snail Physa acuta. Environmental Pollution 134: 377–383.
Kwong, K. L., P. K. Wong, S. S. S. Lau & J. W. Qiu, 2008. Determinants of the distribution of apple snails in Hong Kong two decades after their initial invasion. Malacologia 50: 293–302.
Liang, S., R. C. Zhou, S. S. Dong & S. H. Shi, 2008. Adaptation to salinity in mangroves: Implication on the evolution of salt-tolerance. Chinese Science Bulletin 11: 1708–1715.
Lv, S., Y. Zhang, H. X. Liu, L. Hu, Q. Liu, F. R. Wei, Y.H. Guo, P. Steinmann, W. Hu & X. N. Zhou, 2013. Phylogenetic evidence for multiple and secondary introductions of invasive snails: Pomacea species in the People′s Republic of China. Diversity and Distributions 19: 147–156.
Martin, C. W. & J. F. Valentine, 2014. Tolerance of embryos and hatchlings of the invasive apple snail Pomacea maculata to estuarine conditions. Aquatic Ecology 48: 321–326.
Matsukura, K., M. Okuda, K. Kubota & T. Wada, 2008. Genetic divergence of the genus Pomacea (Gastropoda: Ampullariidae) distributed in Japan, and a simple molecular method to distinguish P. canaliculata and P. insularum. Applied Entomology and Zoology 43: 535–540.
McAskill, S. & J. Douglass, 2017. Salinity and temperature alter Pomacea maculata herbivory rates on Vallisneria americana. Journal of Molluscan Studies 83: 481–483.
Miranda, N. A. F., R. Perissinotto & C. C. Appleton, 2010. Salinity and temperature tolerance of the invasive freshwater gastropod Tarebia granifera. South African Journal of Science 106: 1–7.
Muraeva, O. A., A. L. Maltseva, N. A. Mikhailova & A. I. Granovitch, 2016. Mechanisms of adaption to salinity stress in marine gastropods Littorina saxatilis: a proteomic analysis. Cell and Tissue Biology 10: 160–169.
Nielsen, T. V. & L. A. Gosselin, 2011. Can a scavenger benefit from environmental stress? Role of salinity stress and abundance of preferred food items in controlling population abundance of the snail Lirabuccinum dirum. Journal of Experimental Marine Biology and Ecology 410: 80–86.
Potts, W. T. W., 1954. The energetics of osmotic regulation in brackish- and fresh-water animals. Journal of Experimental Biology 31: 618–630.
Ramakrishnan, V., 2007. Salinity, pH, Temperature, Desiccation and Hypoxia Tolerance in the Invasive Freshwater Apple Snail Pomacea insularum. University of Texas at Arlington, Arlington, TX.
Rankin, J. C. & J. A. Davenport, 1981. Animal Osmoregulation. Blackie, Glasgow, London.
Remane, A. & C. Schlieper, 1971. Biology of Brackish Water. Wiley, New York.
Seuffert, M. E. & P. R. Martín, 2017. Thermal limits for the establishment and growth of populations of the invasive apple snail Pomacea canaliculata. Biological Invasions 19: 1169–1180.
Sogbesan, O. A., 2010. Nutritive potentials and utilization of garden snail (Limicolaria aurora) meat meal in the diet of Clarias gariepinus fingerlings. African Journal of Biotechnology 5: 1999–2003.
Song, H. M., 2010. Sequencing cytochrome oxidase subunit I of mitochondrial DNA and the taxonomic status of apple snails. Chinese Journal of Zoology 45: 1–7.
Sri-Aroon, P., C. Lohachit & M. Harada, 2005. Brackish-water mollusks of Surat Thani Province, southern Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 36: 180–188.
Suski, J. G., C. J. Salice & R. Patino, 2012. Species-specific and transgenerational responses to increasing salinity in sympatric freshwater gastropods. Environmental Toxicology and Chemistry 31: 2517–2524.
Tamburi, N. E. & P. R. Martín, 2009. Feeding rates and food conversion efficiencies in the apple snail Pomacea canaliculata (Caenogastropoda: Ampullariidae). Malacologia 51(221–232): 12.
Veiga, M. P. T., S. M. M. Gutierre, G. C. Castellano & C. A. Freire, 2016. Tolerance of high and low salinity in the intertidal gastropod Stramonita brasiliensis (Muricidae): behaviour and maintenance of tissue water content. Journal of Molluscan Studies 82: 154–160.
Wada, T., & K. Matsukura, 2007. Seasonal changes in cold hardiness of the invasive freshwater apple snail, Pomacea canaliculata (Lamarck) (Gastropoda: Ampullariidae). Malacologia 49: 383–392.
Xu, W., Q. Zhong, L. Li, J. Zhang & Q. Zhong, 2011. Differences of female and male Pomacea canaliculata in foraging and heterosexual choice. Chinese Journal of Ecology 30: 2528–2533.
Yang, Q. Q., S. W. Liu, C. He & X. P. Yu, 2018a. Distribution and the origin of invasive apple snails, Pomacea canaliculata and P. maculata (Gastropoda: Ampullariidae) in China. Scientific Reports 8: 1185.
Yang, S., J. R. Zhong, L. L. Zhao, H. Wu, Z. J. Du, Q. Liu, J. E. Zhang & T. M. Yan, 2018b. The salinity tolerance of the invasive golden apple snail (Pomacea canaliculata). Molluscan Research 38: 90–98.
Yang, S., J. R. Zhong, L. L. Zhao, J. W. Yang, W. Hao & J. E. Zhang, 2015. Acute toxicity effects of salinity stress on the invasive golden apple snails. Journal of South China Agricultural University 5: 31–35.
Yang, T. B., Z. D. Wu & Z. R. Lun, 2013. The apple snail Pomacea canaliculata, a novel vector of the rat lungworm, Angiostrongylus cantonensis: its introduction, spread, and control in China. Hawai’i Journal of Medicine & Public Health 72: 24–25.
Zhou, G., C. Zhai, X. Deng, J. Zhang, Z. Zhang, Q. Dai & S. Cui, 2018. Performance of yield, photosynthesis and grain quality of japonica rice cultivars under salinity stress in micro-plots. Chinese Journal of Rice Science 2: 146–154.
Zong, Y., F. Yu, G. Huang, J. M. Lloyd & W. W. S. Yim, 2010. The history of water salinity in the Pearl River estuary, China, during the Late Quaternary. Earth Surface Processes and Landforms 35: 1221–1233.
Acknowledgements
This work was supported by the National Natural Science Foundation of China (31870525, 41871034, U1131006), Guangdong Modern Agricultural Technology Innovation Team Construction Project (No. 2016LM1100). We thank anonymous reviewers for providing helpful comments on earlier versions of this manuscript.
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We conducted all experiments in adherence to institutional guidelines for animal welfare under the protocol approved by the Animal Ethics Committee of the South China Agricultural University. Pomacea snails used for testing were collected from locations in South China, where there are no endangered or protected species. No specific permits were required for the field study and the locations are not protected.
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Qin, Z., Yang, M., Zhang, JE. et al. Effects of salinity on survival, growth and reproduction of the invasive aquatic snail Pomacea canaliculata (Gastropoda: Ampullariidae). Hydrobiologia 847, 3103–3114 (2020). https://doi.org/10.1007/s10750-020-04320-z
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DOI: https://doi.org/10.1007/s10750-020-04320-z