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Long-Term Population Fluctuations of the Exotic New Zealand Mudsnail

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Long-Term Population Fluctuations of the Exotic New Zealand Mudsnail Long-term population fluctuations of the exotic New Zealand mudsnail Potamopyrgus antipodarum and its introduced aporocotylid trematode in northwestern France Claudia Gérard, Maxime Hervé, Ryan Hechinger To cite this version: Claudia Gérard, Maxime Hervé, Ryan Hechinger. Long-term population fluctuations of the exotic New Zealand mudsnail Potamopyrgus antipodarum and its introduced aporocotylid trematode in northwestern France. Hydrobiologia, Springer, 2018, 817 (1), pp.253-266. 10.1007/s10750-017-3406- x. hal-01827551 HAL Id: hal-01827551 https://hal-univ-rennes1.archives-ouvertes.fr/hal-01827551 Submitted on 3 Sep 2018 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Long-term population fluctuations of the exotic New Zealand mudsnail Potamopyrgus antipodarum and its introduced aporocotylid trematode in northwestern France Claudia Gérard, 1✉ Phone 332-23-23-50-37 Email [email protected] Maxime Hervé, 2 Ryan F. Hechinger, 3 1 Ecosystèmes, Biodiversité, Evolution (UMR ECOBIO 6553), Université de Rennes, 35042 Rennes, France 2 IGEPP, Université de Rennes 1, Avenue du Général Leclerc, 35042 Rennes, France 3 Scripps Institution of Oceanography-Marine Biology Research Division, University of California, San Diego, La Jolla, CA, 92093 USA Received: 30 March 2017 / Accepted: 4 October 2017 Abstract Long-term studies of invasive populations are rare, which is unfortunate because important aspects of their dynamics may only be detected over long term. For instance, invasive populations can experience substantial population declines, or even crashes, sometime after their introduction and invasion. Potamopyrgus antipodarum (Caenogastropoda) is a successful invader, and is rarely parasitized in introduced areas. In France, the snail is parasitized as first intermediate host by only one trematode species (Aporocotylid sp. I), native to the snail’s home range, New Zealand. Here, we examined the dynamics of the molluscan assemblage in a French stream 1 sur 31 24/10/2017 09:35 on a 14-year interval (2000–2004 and 2009–2013), focusing on this introduced host-parasite association. Overall, P. antipodarum was numerically dominant (90.80%) among molluscs, also including sphaeriid clams (9.12%) and pulmonate snails (0.08%). However, during the last monitoring period, we found a substantial population decline of P. antipodarum, potentially driven by environmental change, such as decreased water temperature and depth, and possibly competitive interactions with sphaeriids, which became numerically dominant (56.34%). P. antipodarum was the only mollusc found infected and only by Aporocotylid sp. I. Interestingly, despite low monthly prevalence (from 0 to 1.52%) and snail host population decline, the P. antipodarum-aporocotylid relationship appeared to be persistent over time. Keywords Invasive Potamopyrgus antipodarum Introduced aporocotylid Long-term population dynamics Decline Abiotic parameters Sphaeriids Electronic supplementary material The online version of this article (doi:10.1007/s10750-017-3406-x) contains supplementary material, which is available to authorized users. Guest editors: John E. Havel, Sidinei M. Thomaz, Lee B. Kats, Katya E. Kovalenko & Luciano N. Santos / Aquatic Invasive Species II Introduction Long-term studies of species invasions are relatively rare. This is unfortunate, because although invasive species do undergo periods of rapid population growth and spread [when we deem them “invasive” (Kolar & Lodge, 2001)], they can then strongly fluctuate in abundance over time, and sometimes even spontaneously collapse (Simberloff & Gibbons, 2004; Strayer et al., 2006; Simberloff, 2013 for reviews). Hence, the preponderance of short-term studies of introduced species will not provide the full understanding of the impacts of invasive species. The demographic success of invasive species can be affected 2 sur 31 24/10/2017 09:35 by many factors such as abiotic stresses due to environmental change (e.g., drought, pollution), impacts of parasitism (by parasites introduced after the host introduction and/or native parasites acquired after introduction), and other interactions (Simberloff & Gibbons, 2004; Strayer et al., 2006; Simberloff, 2013 for reviews). The freshwater snail, Potamopyrgus antipodarum (Gray, 1843) (Caenogastropoda), is a globally invasive species, which is a member of the largely Australasian family Tateidae [previously a subfamily of the Hydrobiidae, but now recognized as being a separate family (Zielske et al., 2011; Wilke et al., 2013)]. Native to New Zealand, P. antipodarum has invaded streams and lakes of most of the world’s continents including Australia, Europe, America, and Asia (Alonso & Castro-Díez, 2012; Collado, 2014). Its introduction on these different continents likely has multiple independent origins, but has involved only a small number of parthenogenetic clones (e.g., Hughes, 1996; Jacobsen & Forbes, 1997; Städler et al., 2005; Hoy et al., 2012). In Europe, only two haplotypes have been reported to date: “t” and “z.” The most widely distributed is haplotype t, which appears to be a generalist in fresh waters, whereas haplotype z is restricted to brackish waters (Städler et al., 2005). As for many invasive species, the successful spread of P. antipodarum is at least partly explained by inadvertent human introductions, but also by the snail’s mode of reproduction (i.e., ovoviviparity and parthenogenesis), wide physiological tolerances (e.g., euryhalinity), efficient dispersal, and enemy release (predators, parasites) (Alonso & Castro-Díez, 2008, 2012 for reviews). In its native range, P. antipodarum is first intermediate host for as many as 20 species of highly host-specific trematodes (Hechinger, 2012), which, as parasitic castrators, generally can substantially impact host populations (e.g., Lafferty, 1993; Gérard, 1997, 2001; Negovetich & Esch, 2008). In contrast, in Europe, populations are rarely parasitized. Previous studies in France and Poland revealed that P. antipodarum was infected as first intermediate host by only a single trematode species and at very low levels (≤ 0.48% in France, 0.007% in Poland) ( Gérard & Dussart, 2003; Gérard & Le Lannic, 2003; Gérard et al., 2003; Zbikowski & Zbikowska, 2009). This trematode was reported for the first time in 1999 in western France (Gérard et al., 2003), where P. antipodarum was first recorded in 1912 (Lucas, 1965). DNA sequence analyses indicate that the trematode from French P. antipodarum corresponds to Aporocotylid sp. I (sensu Hechinger, 2012), a New Zealand blood fluke with a two-host life cycle that infects fishes as final hosts (Gérard et al., 3 sur 31 24/10/2017 09:35 e. 2017). Both in New Zealand and in Europe, the average prevalence of Aporocotylid sp. I in P. antipodarum is very low (0.07%), suggesting that this trematode probably does not regulate native or introduced snail host populations (Gérard et al., 2017). Here, we investigate the long-term population dynamics of P. antipodarum and its aporocotylid parasite in a French stream over a 14-year period, with intensive sampling during 2000–2004 [just after the first record in 1999 of the parasite in the same region (Gérard et al., 2003)] and 2009–2013 (10 years after). We had three aims. First, we sought to better understand temporal fluctuations of the introduced population of P. antipodarum in relation with abiotic and biotic conditions. Therefore, we examine the temporal fluctuations of two major abiotic parameters; water temperature, which is crucial for ectotherms such as molluscs and which can correlate with other physicochemical parameters, and depth, which reflects the availability of habitat/space resources. We also examine the long-term dynamics of the whole molluscan assemblage, which may include potential competitors with the invasive snail. Second, we wished to observe whether there was a delayed regulation or even a crash of the invasive mudsnail following its introduction. Third, we sought to examine details of parasitism by the introduced aporocotylid parasite in the P. antipodarum population. Gérard et al. (2017) presented limited information concerning the parasite’s prevalence, using pooled samples from this same dataset. Here, we reported higher-resolution details of the prevalence of Aporocotylid sp. I in P. antipodarum throughout the entire 14-year time period, and we examined the occurrence of parasitic trematodes (including Aporocotylid sp. I) in the rest of the molluscan assemblage. Materials and methods Study site We conducted monitoring in a fourth-order oligotrophic stream (Le Petit Hermitage, in Ille-et-Vilaine, eastern Brittany, France, 48°32′N, 1°34′W) draining a 10 ha-catchment area in a riparian wetland at an altitude of ca. 20 m above sea level (see Clément et al., 2002; Lefebvre et al., 2004; Gruau et al., 2004 for site details). Stream flow is characterized by a base-flow −1 period from June to November (mean monthly discharge ≤ 40 L s ), and a −1 high-flow period from December to May (> 40 L s ). Stream substratum is primarily schist, consisting
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