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Nonindigenous and Cryptogenic Freshwater Bryozoa and Entoprocta in the St. Lawrence River

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Nonindigenous and Cryptogenic Freshwater Bryozoa and Entoprocta in the St. Lawrence River Biol Invasions (2016) 18:1737–1744 DOI 10.1007/s10530-016-1116-3 ORIGINAL PAPER Cryptic invaders: nonindigenous and cryptogenic freshwater Bryozoa and Entoprocta in the St. Lawrence River Kayla M. Hamelin . Rowshyra A. Castan˜eda . Anthony Ricciardi Received: 7 September 2015 / Accepted: 10 March 2016 / Published online: 18 March 2016 Ó Springer International Publishing Switzerland 2016 Abstract The distributions of most cosmopolitan power plant at Be´cancoeur, Quebec. Local densities invertebrate species are assumed to result from natural of both U. gracilis and L. carteri increased by an order processes. Cryptic invertebrates with obscure biogeo- of magnitude at sites closer to the power plant. The graphic origins are often considered native by default, occurrence of Lophopus crystallinus statoblasts in St. resulting in potentially severe underestimation of the Lawrence River sediments is the first documented extent of human-assisted invasions. This problem is physical evidence of the species in North America. exemplified by freshwater Bryozoa (Ectoprocta) and Contrary to the presumed natural Holarctic distribu- Entoprocta—small and widely distributed inverte- tion of L. crystallinus, our literature review found that brates commonly found in lakes and rivers. A benthic published historical records of L. crystallinus in the survey of a thermally modified section of the St. United States are erroneous or unsubstantiated. We Lawrence River revealed the presence of two non- propose that L. crystallinus is a western Palearctic indigenous bryozoans: Carter’s moss animal Lopho- species recently introduced to the St. Lawrence River, podella carteri (Hyatt) and the crystal moss animal most likely as statoblasts discharged with ballast water Lophopus crystallinus Pallas. Also discovered was a from transoceanic ships. cryptogenic entoproct, the goblet worm Urnatella gracilis Leidy. These species were collected as Keywords Biogeography Á Bryozoa Á Ectoprocta Á statoblasts and (in the case of U. gracilis) colonial Entoprocta Á Kamptozoa Á Lophopus crystallinus Á fragments downstream of the Gentilly-2 nuclear Lophopodella carteri Á Urnatella gracilis Electronic supplementary material The online version of Introduction this article (doi:10.1007/s10530-016-1116-3) contains supple- mentary material, which is available to authorized users. Nonindigenous species—organisms that have spread K. M. Hamelin Á R. A. Castan˜eda Á A. Ricciardi (&) beyond their historical range directly or indirectly as a Redpath Museum, McGill University, 859 Sherbrooke result of human activities—are being discovered at Street West, Montreal, QC H3A 0C4, Canada e-mail: [email protected] increasing rates in inland waters worldwide. In most large lakes and rivers, dozens of nonindigenous Present Address: invertebrate taxa have been recorded (Ricciardi R. A. Castan˜eda 2015). These numbers must certainly fall short of Department of Ecology and Evolutionary Biology, University of Toronto- Scarborough, 1265 Military Trail, Toronto, reality, as a result of insufficient monitoring, inade- ON M1C 1A4, Canada quate taxonomic expertise, and incomplete knowledge 123 1738 K. M. Hamelin et al. of the historical biogeography of many species nearly one million statoblasts, which could potentially (Carlton 2009). Indeed, numerous freshwater inverte- be re-suspended and released during ballasting oper- brate taxa are cryptogenic (that is, their native or ations of ships that visit multiple ports within the nonindigenous origins cannot be confirmed) and basin. A few statoblasts from these ships were hatched perhaps many more are misidentified as natives successfully in informal laboratory trials (S.A. Bailey, (‘‘pseudoindigenous’’, sensu Carlton 2009). Conse- Fisheries and Oceans Canada, personal communica- quently, the true extent and impacts of freshwater tion). Given the potentially high propagule pressure invasions may have been profoundly underestimated. imposed by ballast water release, among myriad other Small-bodied taxa—such as bryozoans (Ecto- human vectors, it is rather incredible that only one procta), entoprocts, annelids and rotifers, among nonindigenous bryozoan species has been recorded in others that are ubiquitous in lakes and rivers—are the Great Lakes-St. Lawrence River system to date remarkably absent from most freshwater nonindige- (Ricciardi and Reiswig 1994; Ricciardi 2006). nous species lists (e.g. Mills et al. 1993; Karatayev Here, we report the abundance and distribution of et al. 2009). Two reasons for this are: (1) their nonindigenous freshwater bryozoan and entoproct taxonomic resolution is problematic and thus impedes species in a 4-km thermally modified section of the recognition of nonindigenous taxa; and (2) they are St. Lawrence River downstream of a nuclear power believed to be easily transported by processes such as plant. wind and water currents, or carried by migrating waterfowl (e.g. Figuerola et al. 2004), such that they are often assumed to have naturally cosmopolitan Methods and site description distributions (Carlton 2009). Nevertheless, some freshwater bryozoans have well-documented invasion Invertebrate samples were collected within a broader histories (Balounova´ et al. 2013; Ricciardi and survey assessing the structure of benthic communi- Reiswig 1994; Wood and Okamura 1998), and several ties downstream of the Gentilly-2 nuclear power other species have disjunct, expanding distributions plant (G2NPP) on the south shore of the St. that suggest recent introductions (Wood 2002; Tatic- Lawrence River (46°2303800N, 7282101200W) near chi et al. 2008). Be´cancour, Que´bec (Fig. 1). The G2NPP facility One would expect bryozoan species introductions began operation in 1983 and remained functional to be far more common than records indicate, given until it was decommissioned at the end of December that phylactolaemate bryozoans possess highly resis- 2012. For decades, the heated discharge from tant and abundant resting eggs (statoblasts) that can G2NPP was released at temperatures *11 °C higher individually generate a population (Wood 2010). than the ambient river temperature, which prevented Statoblasts are moved through human activities a multi-kilometer section of the river from freezing including inadvertent transport with stocked fish and during winter months (Langlois and Vaillancourt aquatic plants (e.g. Masters 1940) and ship ballast 1990; Castan˜eda and Hamelin unpublished data). tanks (Bailey et al. 2005; Kipp et al. 2010). Contrary to Using a petite Ponar grab (231 cm2 area), we the classical view that the cosmopolitanism of bry- sampled the benthos along a 3.2 km transect down- ozoans is the result of natural processes (Bushnell stream of G2NPP (Fig. 1). This distance encompassed 1973), there is evidence that human-mediated disper- the artificial discharge canal (mean depth 2–3 m) and sal has played a major role in shaping their contem- most of the thermal plume, defined by year-round open porary global distributions. For example, transoceanic water of variable depth ([3 m) driven by both shipping traffic is the most plausible vector for the seasonal and tidal influences (Table 1). We collected introduction of an Asian bryozoan into the Panama samples along the length of the transect perpendicular Canal region (Wood and Okamura 1998). Statoblasts to the isotherms of the thermal gradient. Two benthic of eleven bryozoan species, comprising more than grabs were taken at each of 10 stations in June and 10 % of all described taxa (!), were found in the ballast August 2011, and 30 stations in May and September tank sediments of 33 transoceanic ships visiting the 2012. Samples were sieved through 0.5 mm mesh and Great Lakes over a two-year period (Kipp et al. 2010); all invertebrates and coarse sediments retained in the each of these ships was estimated to carry, on average, sieve were fixed in 75 % ethanol. 123 Nonindigenous and cryptogenic freshwater Bryozoa and Entoprocta 1739 Quebec *G2NPP * Montreal St. Lawrence River United States Lake Ontario Fig. 1 Map of the study site and location of the Gentilly-2 nuclear power plant (G2NPP) on the St. Lawrence River Table 1 Physico-chemical variables in the Gentilly-2 discharge canal (‘‘Canal’’) and downstream of the discharge canal (‘‘Rest of Plume’’), recorded in situ along the sampling transect in August 2011 and May 2012 Variable Canal Rest of Plume May August May August Depth (m) 2.2 ± 0.9 2.6 ± 0.4 4.8 ± 1.1 3.1 ± 1.4 Temperature (°C) 24.3 ± 0.6 30.2 ± 4.8 16.2 ± 2.2 24.8 ± 0.6 Dissolved oxygen (mg/L) 10.7 ± 0.43 7.7 ± 1.0 10.6 ± 0.4 8.4 ± 0.4 Flow velocity (m/s) 0.07 ± 0.04 0.23 ± 0.16 0.07 ± 0.07 0.11 ± 0.14 Sediment grain size (Phi) 2.28 ± 3.22 -0.89 ± 1.75 2.28 ± 2.31 1.27 ± 2.44 Values reported as Mean ± SD At each station, we measured temperature and Ricciardi (2005). During our sampling period, tem- dissolved oxygen (mg/L) using a YSI probe, water peratures were elevated in the canal (mean 24.3 °Cin velocity using a digital flow meter (Swoffer Model May 2012, mean 30.2 °C in August 2011), and 3000), and depth using either a digital depth sounder represented an average temperature enhancement of or weighted measuring tape. The mean grain size (Phi 6–8 °C relative to downstream sites. Large sediments scale) of sediments was estimated following Jones and (gravel) were observed close to the power plant 123 1740 K. M. Hamelin et al. outflow, with smaller sediments and organic debris worm Urnatella gracilis Leidy (Fig. 2). Bryozoan found throughout the canal, and mixed sediments statoblasts were encountered in greater density near downstream. the G2NPP discharge source (Fig. 3). Their abun- Using a dissection microscope, we manually dance in the discharge canal was largely dominated by removed statoblasts and colony fragments from sed- L. carteri, an Asian species that has an invasion history iments, and identified species following Wood (2010). in North America and Europe (e.g., Sanzhak et al. The analysis of sediment samples is considered to be a 2012; Walker et al. 2013) and is the only nonindige- reliable method of gaining information on the distri- nous bryozoan previously recorded in the Great Lakes- butions of bryozoan species that release statoblasts, St.
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