Variation in shell morphology and life-history traits of Potamopyrgus antipodarum, a highly invasive freshwater snail in Chile
Gonzalo A. Collado
A B * , Ingrid Muñoz A , Ian S. Acuña-Rodríguez C and Moisés A. Valladares A B
+ Author Affiliations
- Author Affiliations
A Departamento de Ciencias Básicas, Facultad de Ciencias, Universidad del Bío-Bío, Avenida Andrés Bello 720, Chillán, PC 3780000, Chile.
B Grupo de Biodiversidad y Cambio Global (GBCG), Facultad de Ciencias, Universidad del Bío-Bío, Avenida Andrés Bello 720, Chillán, PC 3780000, Chile.
C Instituto de Investigaciones Interdisciplinarias (I3), Universidad de Talca, Campus Lircay, Talca, PC 3460000, Chile.
Marine and Freshwater Research 74(1) 65-74 https://doi.org/10.1071/MF22113
Submitted: 8 June 2022 Accepted: 7 November 2022 Published: 30 November 2022
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Context: The New Zealand mudsnail, Potamopyrgus antipodarum, has invaded numerous countries around the world, including Chile.
Aim: We aimed to determine variation in shell morphology and fecundity in 12 populations scattered in six hydrological basins in this country.
Methods: Populations were compared using shell morphometry, principal-component analysis (PCA), and brood size. Independent linear mixed models (LMM) were applied to study spatially correlated data.
Results: The morphometric analysis showed significant differences in shell variables, whereas the PCA showed a high degree of overlap of specimens as well as separation of populations in the morphometric space. Brood size differed significantly among populations, ranging from 0 to 63 offspring. Altitude and shell length had an effect on brood size, whereas shell length showed variation among basins. Latitude did not have a direct effect on any of the two variables.
Conclusions: Potamopyrgus antipodarum exhibits great morphological and life-history trait variation, which could be favouring its rapid expansion in Chile. The lack of genetic variation of this species, previously reported in the country, suggests that differences found in our study are likely to be due to environmental variation.
Implications: Further studies should be addressed to assess the origin of the variance.
Keywords: fecundity, freshwater snails, invasive species, New Zealand mudsnail, ovoviviparity, reproductive strategy, shell variation, Tateidae.
References
Alexandre da Silva, MV, Nunes Souza, JV, de Souza, JRB, and Vieira, LM (2019). Modelling species distributions to predict areas at risk of invasion by the exotic aquatic New Zealand mudsnail Potamopyrgus antipodarum (Gray 1843). Freshwater Biology 64, 1504–1518.| Modelling species distributions to predict areas at risk of invasion by the exotic aquatic New Zealand mudsnail Potamopyrgus antipodarum (Gray 1843).Crossref | GoogleScholarGoogle Scholar |
Alonso, A, and Castro-Díez, P (2008). What explains the invading success of the aquatic mud snail Potamopyrgus antipodarum (Hydrobiidae, Mollusca)? Hydrobiologia 614, 107–116.
| What explains the invading success of the aquatic mud snail Potamopyrgus antipodarum (Hydrobiidae, Mollusca)?Crossref | GoogleScholarGoogle Scholar |
Bennett, DM, Dudley, TL, Cooper, SD, and Sweet, SS (2015). Ecology of the invasive New Zealand mud snail, Potamopyrgus antipodarum (Hydrobiidae), in a Mediterranean-climate stream system. Hydrobiologia 746, 375–399.
| Ecology of the invasive New Zealand mud snail, Potamopyrgus antipodarum (Hydrobiidae), in a Mediterranean-climate stream system.Crossref | GoogleScholarGoogle Scholar |
Bowler, PA (1991). The rapid spread of the freshwater hydrobiidae snail Potamopyrgus antipodarum (Gray) in the Middle Snake River, southern Idaho. Proceedings of the Desert Fishes Council 21, 173–182.
Broekhuizen, N, Parkyn, S, and Miller, D (2001). Fine sediment effects on feeding and growth in the invertebrate grazers Potamopyrgus antipodarum (Gastropoda, Hydrobiidae) and Deleatidium sp. (Ephemeroptera, Leptophlebiidae). Hydrobiologia 457, 125–132.
| Fine sediment effects on feeding and growth in the invertebrate grazers Potamopyrgus antipodarum (Gastropoda, Hydrobiidae) and Deleatidium sp. (Ephemeroptera, Leptophlebiidae).Crossref | GoogleScholarGoogle Scholar |
Butkus, R, Šidagytė, E, and Arbačiauskas, K (2012). Two morphotypes of the New Zealand mud snail Potamopyrgus antipodarum (J.E. Gray, 1843) (Mollusca: Hydrobiidae) invade Lithuanian lakes. Aquatic Invasions 7, 211–218.
| Two morphotypes of the New Zealand mud snail Potamopyrgus antipodarum (J.E. Gray, 1843) (Mollusca: Hydrobiidae) invade Lithuanian lakes.Crossref | GoogleScholarGoogle Scholar |
Cheng, YW, and LeClair, LL (2011). A quantitative evaluation of the effect of freezing temperatures on the survival of New Zealand mudsnails (Potamopyrgus antipodarum Gray, 1843), in Olympia Washington’s Capitol Lake. Aquatic Invasions 6, 47–54.
| A quantitative evaluation of the effect of freezing temperatures on the survival of New Zealand mudsnails (Potamopyrgus antipodarum Gray, 1843), in Olympia Washington’s Capitol Lake.Crossref | GoogleScholarGoogle Scholar |
Collado, GA (2014). Out of New Zealand: molecular identification of the highly invasive freshwater mollusk Potamopyrgus antipodarum (Gray, 1843) in South American. Zoological Studies 53, 70.
| Out of New Zealand: molecular identification of the highly invasive freshwater mollusk Potamopyrgus antipodarum (Gray, 1843) in South American.Crossref | GoogleScholarGoogle Scholar |
Collado, GA (2016). Filling the gap: new records of the invasive New Zealand Mudsnail Potamopyrgus antipodarum in central Chile. The Journal of Zoology Studies 3, 13–19.
Collado, GA, and Fuentealba, CG (2020). Range extension of the invasive Potamopyrgus antipodarum (Gray, 1843) (Gastropoda, Tateidae) in Chile, and a summary of its distribution in the country. Check List 16, 621–626.
| Range extension of the invasive Potamopyrgus antipodarum (Gray, 1843) (Gastropoda, Tateidae) in Chile, and a summary of its distribution in the country.Crossref | GoogleScholarGoogle Scholar |
Collado, GA, Vidal, MA, Aguayo, KP, Méndez, MA, Valladares, MA, Cabrera, FJ, Pastenes, L, Gutiérrez Gregoric, DE, and Puillandre, N (2019a). Morphological and molecular analysis of cryptic native and invasive freshwater snails in Chile. Scientific Reports 9, 7846.
| Morphological and molecular analysis of cryptic native and invasive freshwater snails in Chile.Crossref | GoogleScholarGoogle Scholar |
Collado, GA, Aguayo, KP, Cazzaniga, NJ, Gutiérrez Gregoric, DE, de Lucía, M, and Haase, M (2019b). Systematic evaluation of cryptic freshwater snails from central Chile, including the enigmatic Littoridina santiagensis (Gastropoda, Truncatelloidea). European Journal of Taxonomy 524, 1–15.
| Systematic evaluation of cryptic freshwater snails from central Chile, including the enigmatic Littoridina santiagensis (Gastropoda, Truncatelloidea).Crossref | GoogleScholarGoogle Scholar |
Dorgelo, J (1987). Density fluctuations in populations (1982–1986) and biological observations of Potamopyrgus jenkinsi in two trophically differing lakes. Hydrobiological Bulletin 21, 95–110.
| Density fluctuations in populations (1982–1986) and biological observations of Potamopyrgus jenkinsi in two trophically differing lakes.Crossref | GoogleScholarGoogle Scholar |
Dorgelo, J, van der Geest, HG, and Hunting, ER (2014). Dynamics of natural populations of the dertitivorous mudsnail Potamopyrgus antipodarum (Gray) (Hydrobiidae) in two interconnected Lakes differing in trophic state. SpringerPlus 3, 739.
| Dynamics of natural populations of the dertitivorous mudsnail Potamopyrgus antipodarum (Gray) (Hydrobiidae) in two interconnected Lakes differing in trophic state.Crossref | GoogleScholarGoogle Scholar |
Drown, DM, Levri, EP, and Dybdahl, MF (2011). Invasive genotypes are opportunistic specialists not general purpose genotypes. Evolutionary Applications 4, 132–143.
| Invasive genotypes are opportunistic specialists not general purpose genotypes.Crossref | GoogleScholarGoogle Scholar |
Dybdahl, MF, and Kane, SL (2005). Adaptation vs. phenotypic plasticity in the success of a clonal invader. Ecology 86, 1592–1601.
| Adaptation vs. phenotypic plasticity in the success of a clonal invader.Crossref | GoogleScholarGoogle Scholar |
Dybdahl, MF, and Lively, CM (1995). Diverse, endemic and polyphyletic clones in mixed populations of a freshwater snail (Potamopyrgus antipodarum). Journal of Evolutionary Biology 8, 385–398.
| Diverse, endemic and polyphyletic clones in mixed populations of a freshwater snail (Potamopyrgus antipodarum).Crossref | GoogleScholarGoogle Scholar |
Gaino, E, Scoccia, F, Lancioni, T, and Ludovisi, A (2008). The invader mudsnail Potamopyrgus antipodarum in the Tiber River basin (central Italy). Italian Journal of Zoology 75, 253–261.
| The invader mudsnail Potamopyrgus antipodarum in the Tiber River basin (central Italy).Crossref | GoogleScholarGoogle Scholar |
Geist, JA, Mancuso, JL, Morin, MM, Bommarito, KP, Bovee, EN, Wendell, D, Burroughs, B, Luttenton, MR, Strayer, DL, and Tiegs, SD (2022). The New Zealand mud snail (Potamopyrgus antipodarum): autecology and management of a global invader. Biological Invasions 24, 905–938.
| The New Zealand mud snail (Potamopyrgus antipodarum): autecology and management of a global invader.Crossref | GoogleScholarGoogle Scholar |
Gust, M, Buronfosse, T, André, C, Mons, R, Gagné, F, and Garric, J (2011). Is exposure temperature a confounding factor for the assessment of reproductive parameters of New Zealand mudsnails Potamopyrgus antipodarum (Gray)? Aquatic Toxicology 101, 396–404.
| Is exposure temperature a confounding factor for the assessment of reproductive parameters of New Zealand mudsnails Potamopyrgus antipodarum (Gray)?Crossref | GoogleScholarGoogle Scholar |
Haase, M (2003). Clinal variation in shell morphology of the freshwater gastropod Potamopyrgus antipodarum along two hill-country streams in New Zealand. Journal of the Royal Society of New Zealand 33, 549–560.
| Clinal variation in shell morphology of the freshwater gastropod Potamopyrgus antipodarum along two hill-country streams in New Zealand.Crossref | GoogleScholarGoogle Scholar |
Hamada, K, Tatara, Y, Urabe, M, The Biology Club of Kojo High School (2013). Survey of mitochondrial DNA haplotypes of Potamopyrgus antipodarum (Caenogastropoda: Hydrobiidae) introduced into Japan. Limnology 14, 223–228.
| Survey of mitochondrial DNA haplotypes of Potamopyrgus antipodarum (Caenogastropoda: Hydrobiidae) introduced into Japan.Crossref | GoogleScholarGoogle Scholar |
Haynes A, Taylor BJR (1984) Food finding and food preference in Potamopyrgus jenkinsi (E. A. Smith) (Gastropoda: Prosobranchia). Archiv fur Hydrobiologie 100, 479–491.
Holomuzki, JR, and Biggs, BJF (2006). Habitat-specific variation and performance trade-offs in shell armature of New Zealand mudsnails. Ecology 87, 1038–1047.
| Habitat-specific variation and performance trade-offs in shell armature of New Zealand mudsnails.Crossref | GoogleScholarGoogle Scholar |
Jacobsen, R, and Forbes, VE (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.
| Clonal variation in life–history traits and feeding rates in the gastropod, Potamopyrgus antipodarum: performance across a salinity gradient.Crossref | GoogleScholarGoogle Scholar |
James, MR, Hawes, I, and Weatherhead, M (2000). Removal of settled sediments and periphyton from macrophytes by grazing invertebrates in the littoral zone of a large oligotrophic lake. Freshwater Biology 44, 311–326.
| Removal of settled sediments and periphyton from macrophytes by grazing invertebrates in the littoral zone of a large oligotrophic lake.Crossref | GoogleScholarGoogle Scholar |
Jokela, J, Lively, CM, Dybdahl, MF, and Fox, JA (1997). Evidence for a cost of sex in the freshwater snail Potamopyrgus antipodarum. Ecology 78, 452–460.
| Evidence for a cost of sex in the freshwater snail Potamopyrgus antipodarum.Crossref | GoogleScholarGoogle Scholar |
Kerans, BL, Dybdahl, MF, Gangloff, MM, and Jannot, JE (2005). Potamopyrgus antipodarum: distribution, density, and effects on native macroinvertebrate assemblages in the Greater Yellowstone ecosystem. Journal of the North American Benthological Society 24, 123–138.
| Potamopyrgus antipodarum: distribution, density, and effects on native macroinvertebrate assemblages in the Greater Yellowstone ecosystem.Crossref | GoogleScholarGoogle Scholar |
Kistner, EJ, and Dybdahl, MF (2013). Adaptive responses and invasion: the role of plasticity and evolution in snail shell morphology. Ecology and Evolution 3, 424–436.
| Adaptive responses and invasion: the role of plasticity and evolution in snail shell morphology.Crossref | GoogleScholarGoogle Scholar |
Kistner, EJ, and Dybdahl, MF (2014). Parallel variation among populations in the shell morphology between sympatric native and invasive aquatic snails. Biological Invasions 16, 2615–2626.
| Parallel variation among populations in the shell morphology between sympatric native and invasive aquatic snails.Crossref | GoogleScholarGoogle Scholar |
Larson, MD, and Ross Black, A (2016). Assessing interactions among native snails and the invasive New Zealand mud snail, Potamopyrgus antipodarum, using grazing experiments and stable isotope analysis. Hydrobiologia 763, 147–159.
| Assessing interactions among native snails and the invasive New Zealand mud snail, Potamopyrgus antipodarum, using grazing experiments and stable isotope analysis.Crossref | GoogleScholarGoogle Scholar |
Lassen, HH (1979). Reproductive effort in Danish mudsnails (Hydrobiidae). Oecologia 40, 365–369.
| Reproductive effort in Danish mudsnails (Hydrobiidae).Crossref | GoogleScholarGoogle Scholar |
Levri, EP, Kelly, AA, and Love, E (2007). The invasive New Zealand mud snail (Potamopyrgus antipodarum) in Lake Erie. Journal of Great Lakes Research 33, 1–6.
| The invasive New Zealand mud snail (Potamopyrgus antipodarum) in Lake Erie.Crossref | GoogleScholarGoogle Scholar |
Levri, EP, Krist, AC, Bilka, R, and Dybdahl, MF (2014). Phenotypic plasticity of the introduced New Zealand mud snail, Potamopyrgus antipodarum, compared to sympatric native snails. PLoS ONE 9, e93985.
| Phenotypic plasticity of the introduced New Zealand mud snail, Potamopyrgus antipodarum, compared to sympatric native snails.Crossref | GoogleScholarGoogle Scholar |
Lively, CM (1987). Evidence from a New Zealand snail for the maintenance of sex by parasitism. Nature 328, 519–521.
| Evidence from a New Zealand snail for the maintenance of sex by parasitism.Crossref | GoogleScholarGoogle Scholar |
Mazurová, E, Hilscherová, K, Jálová, V, Köhler, H-R, Triebskorn, R, Giesy, JP, and Bláha, L (2008). Endocrine effects of contaminated sediments on the freshwater snail Potamopyrgus antipodarum in vivo and in the cell bioassays in vitro. Aquatic Toxicology 89, 172–179.
| Endocrine effects of contaminated sediments on the freshwater snail Potamopyrgus antipodarum in vivo and in the cell bioassays in vitro.Crossref | GoogleScholarGoogle Scholar |
McKenzie, VJ, Hall, WE, and Guralnick, RP (2013). New Zealand mudsnails (Potamopyrgus antipodarum) in Boulder Creek, Colorado: environmental factors associated with fecundity of a parthenogenic invader. Canadian Journal of Zoology 91, 30–36.
| New Zealand mudsnails (Potamopyrgus antipodarum) in Boulder Creek, Colorado: environmental factors associated with fecundity of a parthenogenic invader.Crossref | GoogleScholarGoogle Scholar |
Neiman, M (2006). Embryo production in a parthenogenetic snail (Potamopyrgus antipodarum) is negatively affected by the presence of other parthenogenetic females. Invertebrate Biology 125, 45–50.
| Embryo production in a parthenogenetic snail (Potamopyrgus antipodarum) is negatively affected by the presence of other parthenogenetic females.Crossref | GoogleScholarGoogle Scholar |
Nentwig, W, Bacher, S, Kumschick, S, Pyšek, P, and Vilà, M (2018). More than ‘100 worst’ alien species in Europe. Biological Invasions 20, 1611–1621.
| More than ‘100 worst’ alien species in Europe.Crossref | GoogleScholarGoogle Scholar |
Pinheiro JC, Bates DM (2000) ‘Mixed-effects models in S and S-Plus.’ (Springer-Verlag: New York, NY, USA)
Ponder, WF (1988). Potamopyrgus antipodarum – a molluscan coloniser of Europe and Australia. Journal of Molluscan Studies 54, 271–285.
| Potamopyrgus antipodarum – a molluscan coloniser of Europe and Australia.Crossref | GoogleScholarGoogle Scholar |
Proctor T, Kerans B, Clancey P, Ryce E, Dybdahl M, Gustafson D, Hall R, Pickett F, Richards D, Waldeck RD, Chapman J, Wiltshire RH, Becker D, Anderson M, Pitman B, Lassuy D, Heimowitz P, Dwyer P, Levri EP (2007) National management and control plan for the New Zealand mudsnail (Potamopyrgus antipodarum). US Fish and Wildlife Service Report. (US Fish and Wildlife Service) Available at https://www.researchgate.net/publication/303364344_National_Management_and_Control_Plan_for_the_New_Zealand_Mudsnail_Potamopyrgus_antipodarum [Verified 18 May 2022]
Radea, C, Louvrou, I, and Economou-Amilli, A (2008). First record of the New Zealand mud snail Potamopyrgus antipodarum J.E. Gray 1843 (Mollusca: Hydrobiidae) in Greece – notes on its population structure and associated microalgae. Aquatic Invasions 3, 341–344.
| First record of the New Zealand mud snail Potamopyrgus antipodarum J.E. Gray 1843 (Mollusca: Hydrobiidae) in Greece – notes on its population structure and associated microalgae.Crossref | GoogleScholarGoogle Scholar |
Rakauskas, V, Šidagyté, E, Butkus, R, and Garbaras, A (2018). Effect of the invasive New Zealand mud snail (Potamopyrgus antipodarum) on the littoral macroinvertebrate community in a temperate mesotrophic lake. Marine and Freshwater Research 69, 155–166.
| Effect of the invasive New Zealand mud snail (Potamopyrgus antipodarum) on the littoral macroinvertebrate community in a temperate mesotrophic lake.Crossref | GoogleScholarGoogle Scholar |
Ribi, G (1986). Within-lake dispersal of the prosobranch snails, Viviparus ater and Potamopyrgus jenkinsi. Oecologia 69, 60–63.
| Within-lake dispersal of the prosobranch snails, Viviparus ater and Potamopyrgus jenkinsi.Crossref | GoogleScholarGoogle Scholar |
Richards, DC (2002). The New Zealand mudsnail invades the western United States. Aquatic Nuisance Species Digest 4, 42–44.
Richards, DC, Cazier, LD, and Lester, GT (2001). Spatial distribution of three snail species, including the invader Potamopyrgus antipodarum, in a freshwater spring. Western North American Naturalist 61, 375–380.
Riley, LA, Dybdahl, MF, and Hall, RO (2008). Invasive species impact: asymmetric interactions between invasive and endemic freshwater snails. Journal of the North American Benthological Society 27, 509–520.
| Invasive species impact: asymmetric interactions between invasive and endemic freshwater snails.Crossref | GoogleScholarGoogle Scholar |
Schreiber, ESG, Glaister, A, Quinn, GP, and Lake, PS (1998). Life history and population dynamics of the exotic snail Potamopyrgus antipodarum (Prosobranchia: Hydrobiidae) in Lake Purrumbete, Victoria, Australia. Marine and Freshwater Research 49, 73–78.
| Life history and population dynamics of the exotic snail Potamopyrgus antipodarum (Prosobranchia: Hydrobiidae) in Lake Purrumbete, Victoria, Australia.Crossref | GoogleScholarGoogle Scholar |
Shimada, K, and Urabe, M (2003). Comparative ecology of the alien freshwater snail Potamopyrgus antipodarum and the indigenous snail Semisulcospira spp. Venus 62, 39–53.
Strzelec, M (2005). Impact of the introduced Potamopyrgus antipodarum (Gastropods) on the snail fauna in post-industrial ponds in Poland. Biologia 60, 159–163.
Taybi, AF, Mabrouki, Y, and Glöer, P (2021). First record of the New Zealand mudsnail Potamopyrgus antipodarum (J.E. Gray, 1843) (Tateidae, Mollusca) in Africa. Graellsia 77, e140.
| First record of the New Zealand mudsnail Potamopyrgus antipodarum (J.E. Gray, 1843) (Tateidae, Mollusca) in Africa.Crossref | GoogleScholarGoogle Scholar |
Vergara, D, Fuentes, JA, Stoy, KS, and Lively, CM (2017). Evaluating shell variation across different populations of a freshwater snail. Molluscan Research 37, 120–132.
| Evaluating shell variation across different populations of a freshwater snail.Crossref | GoogleScholarGoogle Scholar |
Verhaegen, G, McElroy, KE, Bankers, L, Neiman, M, and Haase, M (2018a). Adaptive phenotypic plasticity in a clonal invader. Ecology and Evolution 8, 4465–4483.
| Adaptive phenotypic plasticity in a clonal invader.Crossref | GoogleScholarGoogle Scholar |
Verhaegen, G, Neiman, M, and Haase, M (2018b). Ecomorphology of a generalist freshwater gastropod: complex relations of shell morphology, habitat, and fecundity. Organisms Diversity & Evolution 18, 425–441.
| Ecomorphology of a generalist freshwater gastropod: complex relations of shell morphology, habitat, and fecundity.Crossref | GoogleScholarGoogle Scholar |
Verhaegen, G, von Jungmeister, K, and Haase, M (2021). Life history variation in space and time: environmental and seasonal responses of a parthenogenetic invasive freshwater snail in northern Germany. Hydrobiologia 848, 2153–2168.
| Life history variation in space and time: environmental and seasonal responses of a parthenogenetic invasive freshwater snail in northern Germany.Crossref | GoogleScholarGoogle Scholar |
Wallace, C (1985). On the distribution of the sexes of Potamopyrgus jenkinsi (Smith). Journal of Molluscan Studies 51, 290–296.
| On the distribution of the sexes of Potamopyrgus jenkinsi (Smith).Crossref | GoogleScholarGoogle Scholar |
Wallace, C (1992). Parthenogenesis, sex and chromosomes in Potamopyrgus. Journal of Molluscan Studies 58, 93–107.
| Parthenogenesis, sex and chromosomes in Potamopyrgus.Crossref | GoogleScholarGoogle Scholar |
Winterbourn, MJ (1970). The New Zealand species of Potamopyrgus (Gastropoda: Hydrobiidae). Malacologia 10, 283–321.
Winterbourn, MJ (1972). Morphological variation of Potamopyrgus jenkinsi (Smith) from England and a comparison with the New Zealand species, Potamopyrgus antipodarum (Gray). Proceedings of the Malacological Society of London 40, 133–145.
Zachar, N, and Neiman, M (2013). Profound effects of population density on fitness-related traits in an invasive freshwater snail. PLoS ONE 8, e80067.
| Profound effects of population density on fitness-related traits in an invasive freshwater snail.Crossref | GoogleScholarGoogle Scholar |
