Fecundity of the Invasive Marine Gastropod Crepidula Fornicata Near the Current Northern Extreme of Its Range

Home , Bostrycapulus odites, Crepidula, Crepidula fornicata, Crepipatella

Fecundity of the invasive marine gastropod Crepidula fornicata near the current northern extreme of its range

Jan A. Pechenik,1,a Casey M. Diederich,1 Howard I. Browman,2 and Anders Jelmert3

1 Department of Biology, Tufts University, Medford, Massachusetts 02155, USA 2 Institute of Marine Research, Austevoll Research Station, Storebø, Norway 3 Institute of Marine Research, 5817 Bergen, Norway

Abstract. The calyptraeid gastropod Crepidula fornicata is native to the eastern coast of the United States but has now become an extremely successful invader along much of the Euro- pean coastline. As the northern limit of its spread is thought to be determined by an inability of adults to tolerate prolonged exposure to low winter temperatures, this study sought to compare the fecundity of females collected from two sites along the Norwegian coastline with that of females collected from Rhode Island, USA. Few other studies have compared the fecundities of marine invertebrates from invasive populations with those found in native populations. For both populations studied, fecundities increased with increasing shell length. However, contrary to expectations, size-related fecundities were signiﬁcantly higher for Norwegian females than for Rhode Island females, with Norwegian females producing larger egg capsules and a greater number of embryos per capsule, but not a greater number of egg capsules per brood. Current evidence suggests that at the northern extreme of its invaded range, the fecundity of C. fornicata is increased rather than compromised. Additional key words: Calyptraeidae, fecundity, biological invasions, reproductive success

The suspension-feeding marine gastropod Crepi- compare the features of successful invasives with dula fornicata (LINNAEUS 1758), native to the eastern those of native species in the invaded habitat coast of North America (Blanchard 1997), has (Brousseau & McSweeney 2016; reviewed by Alpert become a highly successful invasive species in many 2006; van Kleunen et al. 2010a; Parker et al. 2013). other parts of the world. First inadvertently intro- Few studies have made intraspecific comparisons duced into the coastal waters of the UK with oyster between populations of invasive species in the shipments in the 1870s, the species is now common invaded range and those in the native range (see van along the coasts of France, the Netherlands, Ger- Kleunen et al. 2010a,b; Parker et al. 2013), and many, Denmark, and Norway, with adult densities many of the studies that have been conducted con- of thousands of individuals per m2 in some locations cern terrestrial plant species (reviewed by Grosholz (reviewed by Blanchard 1997, 2009; Thieltges et al. & Ruiz 2003; Parker et al. 2013); the limited, related 2004; Bohn et al. 2012). The species has now been marine research has focused largely on vertebrates reported from Irish waters as well (McNeill et al. (reviewed by Grosholz & Ruiz 2003; van Kleunen 2010). et al. 2010b). What enables such invasions to take place? Why Thieltges et al. (2004) suggested that the northern are some species so much more successful as inva- range of C. fornicata was limited by the inability of ders than other, closely related species? What factors the adults to tolerate prolonged exposure to low limit the future spread of invasive species from winter temperatures. Although this must indeed play invaded areas? Most studies concerned with such an important role, fecundity is also a major determi- questions have sought to compare the biological fea- nant of a species’ ability to spread successfully (re- tures of successful invasives with those of related viewed by van Kleunen et al. 2010a; Parker et al. species that have not become invasive, or to 2013). Nobody has yet documented the fecundity of C. fornicata at the northern limits of its range. aAuthor for correspondence. Southern Norway is currently at that limit (Blan- E-mail: [email protected] chard 1997; Sjøtun 1997; Bohn et al. 2012). The first Crepidula fornicata fecundity in Norway 395 living representative of this species in Norway was at those sites is found only subtidally. The speci- reported in 1962 (Sjøtun 1997). mens were then transported in coolers to the Insti- In this study, we compared the fecundity of tute of Marine Research’s laboratory at Austevoll, females in a Norwegian population with that of Norway, for examination. Most stacks consisted of females collected from a coastal site in Rhode <4 individuals. For each stack, an individual was Island, USA, to determine whether living near the pried off the individual below it with a metal putty northern edge of its current range negatively impacts knife until a brooding female was found. The intact fecundity; such comparisons of reproductive attri- egg mass was then removed from the female and set butes between invasives and members of the same aside for examination; the female was then carefully species in their home range are rare (Parker et al. removed from her shell, quickly rinsed three times 2013). Crepidula fornicata, however, is particularly in distilled water to remove exterior salt, and placed well suited for such studies. This species, like other into a pre-weighed foil pan. Shell length was mea- calyptraeid gastropods, is a protandric hermaphro- sured to the nearest 0.1 mm using calipers, and the dite, with males eventually transitioning to females shell was then rinsed in distilled water to remove (Coe 1936; Collin 1995; Henry et al. 2010; Cahill salt. Both shell and tissue samples were then kept in et al. 2015; Carrillo-Baltodano & Collin 2015). Fol- a drying oven at 55°C for 96 h and weighed to the lowing internal fertilization by the male, females nearest 0.1 mg. Care was taken to sample brooding encapsulate their fertilized eggs within a series of females from a wide range of shell sizes. Females small, transparent, balloon-like triangular egg cap- are smaller near the top of each stack and larger sules; this collection of capsules—the egg mass—is toward the bottom (Coe 1936). then maintained beneath the shell at the front of the To estimate individual fecundity, the number of mantle cavity (e.g., Richard et al. 2006; Mardones egg capsules per egg mass was determined and ten et al. 2013) for several weeks until free-living veliger representative egg capsules were then set aside from larvae emerge. Thus, it is easy to determine fecun- each egg mass. Each egg capsule was carefully dity simply by counting the number of egg capsules opened with forceps, and all embryos were then within a brood, and the number of embryos within counted in each of the ten sampled capsules. Each the egg capsules. Most embryos develop to hatching capsule typically contained between 300 and 850 in this species (Pechenik, unpubl. data), and there is embryos (see below). Brood sizes were estimated no evidence of cannibalism. The Rhode Island col- from nine females in 2012 and seven females in lecting site is near the midpoint of the species’ native 2013. range, which extends from Florida well into Canada The data from this study were compared with (Blanchard 1997; Rawlings et al. 2011). reproductive data collected previously from Bissel Cove in Narragansett Bay, Rhode Island (41°32050″ N, 71°25053″W) (Pechenik et al. 2017). Brooding Methods females in that study were sampled ten times between April and September during 2010–2013 Collecting water temperature data (Pechenik et al. 2017). Because the fecundity of Water temperatures near our Norwegian study sites intertidal individuals sampled in that study was sig- were collected at 1-min intervals from December 1, nificantly greater than that of subtidal individuals 2011, through May 1, 2013. We used an Aanderaa collected at the same location, in some of our analy- Instruments (Nesttun, Norway) Conductivity Sensor ses we compared results from the Norwegian sam- Model 4120, and sampled at a water depth of 1 m. ples (all of which were collected subtidally) with those from subtidally collected Rhode Island individuals. In the Rhode Island study, there was no Sampling methods significant relationship between habitat (intertidal Adults of C. fornicata commonly occur as mixed- vs. subtidal) and any of the other measured repro- sex groups (stacks), in which smaller individuals are ductive characteristics, so that in the present study typically attached to the shells of other, larger indi- we included data from both subtidal and intertidal viduals below them (Coe 1936). Stacks of adults Rhode Island individuals in the other analyses. were collected in approximately 1 m of water at low We also estimated egg capsule sizes using capsules tide in two sheltered coves about 400 m apart in the obtained from females collected in Norway in 2013. Arendal municipality of Norway (58°31014.3″N, The lengths and widths of ten typical egg capsules 8°56045.3″E and 58°31029.6″N, 8°56028.9″E) in mid- from each egg mass were determined at a magnifica- May 2012 and early June 2013. Crepidula fornicata tion of 509; we later estimated egg capsule sizes by

Invertebrate Biology vol. 136, no. 4, December 2017 396 Pechenik, Diederich, Browman, & Jelmert computing the triangular surface area of each capsule (Pechenik et al. 2017).

Statistical methods Data were analyzed by standard linear regression, using GraphPad Prism 6.0 software. All data were log-transformed before analysis, except for the data presented in Supporting information Fig. S1. For examining relationships between female shell length and embryos per capsule or capsule surface area, linear regressions were conducted using the mean values for each sampled female.

Results The coldest recorded water temperature at our Norwegian study site in 2012 was 0.1°C (February 20), and the coldest average weekly water temperature was 1.1°C (February 14–20). In 2013, the coldest recorded water temperature was 0.5°C (January 26), and the coldest average weekly water temperature was 0.3°C (January 22–28). For the 16 brooding females sampled from Nor- wegian waters, covering a range of shell lengths between 31.8 and 53.0 mm, maximum individual fecundity (55,541 embryos) was nearly five times greater than the minimum recorded fecundity (11,136 embryos) (Fig. 1). Although Fig. 1 shows plots of untransformed values for fecundity (number of embryos per egg mass) versus female dry tissue weight (Fig. 1A), female dry shell weight (Fig. 1B), and female shell length (Fig. 1C), the regression equations shown for each were derived from analysis of log-transformed data. These analyses indicate that fecundity was not well predicted by female dry tissue weight (p=0.27) or by dry shell weight (p=0.06), but was well predicted by differences in female shell length (p=0.025); conducting the same analyses on untransformed data produced analogous results (Supporting information Fig. S1). The slopes of the lines relating fecundity to shell length were not significantly different for the Norwegian and Rhode Island populations, whether or not the data for intertidal Rhode Island individuals were included in the analyses (Fig. 2A,B); however, the intercepts did differ significantly in both cases, with the Norwegian females showing the greater increase in fecundity with increasing shell length (Fig. 2A,B). Fig. 1. Degree to which individual fecundity scales with (A) Similar results were obtained when we ran the same dry tissue weight, (B) dry shell weight, or (C) shell length in analysis including only those data for individuals females of Crepidula fornicata. All individuals were collected with shell lengths that overlapped between the Nor- in shallow water at low tide in the Arendal municipality of Norway, in 2012 and 2013. The regression statistics shown wegian and Rhode Island females (shell lengths are based on analyses of log-transformed data. between 32 and 44 mm); again, the slopes were not

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Fig. 2. Fecundity in Crepidula fornicata: comparisons between Norwegian females (blue dots) sampled in 2012 and 2013 and females sampled from a native population in Wickford, Rhode Island, USA (open circles), in 2012 and 2013. A. Comparison with data from Rhode Island females sampled both intertidally and subtidally; B. comparison including data from subtidal Rhode Island females only.

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significantly different (F1,87=0.86, p=0.36), but the Norwegian females was a much better predictor of intercepts differed significantly (F1,88=7.63, p=0.007). fecundity than was tissue weight, possibly because Larger Norwegian females did not produce signifi- shell length is a better indicator of the size of the cantly more egg capsules per egg mass than smaller space beneath the shell in which the egg capsules are individuals did (p=0.85; Fig. 3), a result different brooded. The importance of this correlation could from that observed for Rhode Island females be examined in future studies. (p<0.0001; Fig. 3). Although larger females sampled from both populations produced egg masses with 4 Norway more embryos per egg capsule, Norwegian females Y = 1.734X - 0.2330, R2 = 0.33 showed a significantly greater increase in embryos per F1,158 = 79.20 p < 0.0001 egg capsule with increased shell length than Rhode 3 Island females did; the two lines were not significantly different in slope (F1,278=0.21, p=0.64), but the intercepts were significantly different (F1,279=76.46, p<0.0001; Fig. 4). Although mean egg capsule size 2 increased significantly with increased female size in both sampled populations, larger Norwegian females Rhode Island of a given size tended to have disproportionately lar- 1 2 ger egg capsules than the Rhode Island females did Y = 1.862X - 0.6493, R = 0.42 F1,120 = 87.56 (comparison of slopes, F1,76=0.12, p=0.73; compar- Log mean embryos per egg capsule p < 0.0001 ison of intercepts, F1,77=10.30, p=0.002; Fig. 5). 0 Graphs of untransformed data relating female shell 1.01 .2 1. 41 .6 1. 82.0 length to fecundity, mean number of egg capsules per Log shell length mm egg mass, mean number of embryos per egg capsule, Fig. 4. The influence of sampling location (Norway vs. and mean capsule surface area are shown in Support- – Rhode Island) on the mean number of embryos per egg ing information Figs. S2 S5. capsule in females of Crepidula fornicata. For Norwegian samples, error bars show one SD. Standard deviations Discussion were similar for the Rhode Island samples, but for clarity are not shown. As indicated in the text, the slopes of the As in a previous study of this species in its native two lines did not differ significantly, but the x-axis range (Pechenik et al. 2017), shell length of intercepts did.

2.5 Rhode Island Norway 1.5 Y = 1.224X - 00.2214 Y = 0.1206X +1.549 Norway Y = 1.414X - 1.393, R2 = 0.61 F1,120 = 26.08, p < 0.0001 F1,14 = 0.037, p = 0.85 2 2 F1,5 = 7.855, p = 0.038 2.0 R = 0.1785 R = 0.0026

) Rhode Island 2 Y = 1.258 - 1.257, R2 = 0.4850 F1,71 = 66.86, p < 0.0001 1.0 1.5

1.0

0.5

0.5 Log number egg capsules per egg mass Log mean egg capsule area (mm

Slopes: F1,76 = 0.12, p = 0.73 Intercepts: F1,77 = 10.30, p = 0.0019 0.0 1.01 .2 1. 41 .6 1. 82.0 0.0 Log shell length (mm) 1.01 .2 1. 41 .6 1. 82.0 Fig 3. Relationship between number of egg capsules per Log shell length (mm) egg mass and female size for sampled Norwegian (blue Fig. 5. Effect of location on the relationship between dots) and Rhode Island (open circles) females of Crepi- female size and mean egg capsule sizes for the two sam- dula fornicata. For Norwegian females, the slope of the pled populations of Crepidula fornicata (Norway, blue line shown did not differ signiﬁcantly from zero (p=0.85). dots, meanSD; Rhode Island, open circles).

Invertebrate Biology vol. 136, no. 4, December 2017 Crepidula fornicata fecundity in Norway 399

Although the Norwegian site from which we col- to become sexually mature at a larger size in colder lected adults of C. fornicata for this study is only environments (the Bergmann “temperature–size about 160 km south of the current northern limit of rule;” e.g., Angilletta et al. 2004). Although this the species’ range (Blanchard 1997; Sjøtun 1997; would presumably delay the onset of female repro- Richard et al. 2006; Bohn et al. 2012), and the ductive activity, the benefits of higher fecundity may major factor presumed to be preventing the spread be especially great in an invaded region (Keller et al. of the species further north is intolerance to pro- 2007; Rigal et al. 2010; Janes€ et al. 2015; Brousseau longed freezing winter temperatures (Thieltges et al. & McSweeney 2016; Howeth et al. 2016). 2004), fecundity does not seem to be compromised Females in these northern invasive populations for these invaders. Our Norwegian sample sizes were may also be growing to a larger size. In an analysis not large, and the size distributions of brooding of the literature on the sizes of various marine inver- females from the two populations were dissimilar, tebrates in their native and invaded ranges but certainly there is no indication that the fecundi- (Grosholz & Ruiz 2003), body sizes were generally ties for Norwegian females were lower than those larger for invaders than for members of the same recorded for females collected from Rhode Island; species in their native populations; the same result indeed, size-related fecundity in the Norwegian pop- has recently been reported for invasive and native ulation was significantly higher than that recorded green crabs, Carcinus maenus (Kelley et al. 2015). for females from the Rhode Island population, even The mechanisms accounting for such shifts remain when the analyzed data included only females from largely unexplored, although for C. maenas the the two populations in the shared range of shell increased size was correlated with cooler tempera- sizes. Moreover, the maximum fecundity recorded tures in the invaded range (Kelley et al. 2015). was far higher than anything recorded previously Exactly why C. fornicata has become such a suc- for C. fornicata in the species’ home range (Fig. 2; cessful invader while most other members of the Pechenik et al. 2017). In several terrestrial plant family Calyptraeidae have not (Collin et al. 2010; studies (reviewed by Parker et al. 2013), introduc- Henry et al. 2010) is unclear. The production of tions into novel regions led to increased fecundity long-lived planktonic larvae is likely an important for the invaders. We know of no comparable pub- factor in mediating successful invasions (Collin et al. lished studies for marine invertebrates, possibly 2010), although many other calyptraeid species also because fecundities are more difficult to assess for produce planktonic larvae (Collin 2003); even so, most invertebrates than for calpytraeid gastropods the elevated or at least uncompromised fecundity like C. fornicata. For C. fornicata, the higher size- demonstrated here in C. fornicata near the northern specific fecundity found in our study for Norwegian limit of the species’ invasive range would clearly be females was mediated by an increase in the sizes of an asset. All calyptraeids are generalist suspension individual egg capsules, allowing Norwegian females feeders, so species-specific differences in dietary to include more embryos per capsule, rather than by requirements should not be related to invasion suc- an increase in the number of egg capsules per egg cess. As with all other calyptraeids, adults of C. for- mass. nicata are sedentary, so that different degrees of In sampling brooding females from the Norwe- adult dispersal ability (Brousseau & McSweeney gian population, we attempted to obtain as wide a 2016) should also not be related to ecological inva- range of shell sizes as possible, and so it is intriguing sion success. Some species become successful inva- that the smallest individual found with an egg mass sives by leaving behind their parasites (Torchin in our samples had a shell length of nearly 32 mm et al. 2003); however, C. fornicata, C. plana, and C. (Fig. 2), whereas in the Rhode Island population convexa do not seem to serve as first host species egg masses were commonly brooded by much smal- for trematodes (Pechenik et al. 2001, 2012), ler females (Fig. 2). It should also be noted that the although one related South American species (Crepi- largest Norwegian female sampled was about 20% patella dilatata) does (Gilardoni et al. 2012). More- larger than the largest brooding female that we over, many individuals of C. fornicata found in encountered in Rhode Island. Similarly large brood- French waters are infected by the French shell borer ing females have been found in samples taken from Cliona celata, although the infestation does not the Bay of Brest, France (Richard et al. 2006). appear to be harmful (Le Cam & Viard 2011). Indi- Future studies might examine this issue further, to viduals of C. fornicata also seem to be very tolerant see if Norwegian and French males of C. fornicata of a variety of physical stresses (Diederich & Peche- are transitioning to females at significantly larger nik 2013; Diederich et al. 2015), which may (e.g., average shell sizes. It is not unusual for ectotherms Lenz et al. 2011) or may not (McMahon 2002) play

Invertebrate Biology vol. 136, no. 4, December 2017 400 Pechenik, Diederich, Browman, & Jelmert a role in the species’ success as an invader; there is HIB. We are also grateful to Jon Albretsen (Institute of little comparable data on the physical tolerance of Marine Research) for extracting and graphing the temper- related species. ature data for the Norwegian collecting site from the The pronounced stacking behavior among indi- IMR database, and to Louise Page and the two anony- viduals of C. fornicata may also be a factor in the mous reviewers who provided excellent suggestions for improving the manuscript. The authors confirm that they unusual success of this species as an invasive, as it have no conflicts of interest. reduces competition with other benthic invertebrates for space, and provides perpetual access to mates (Dupont et al. 2006); indeed, Richard et al. (2006, p References 799) refer to such stacks as “self-sufficient reproductive units.” Having multiple males and females in Alpert P 2006. The advantages and disadvantages of each stack may also be beneficial in producing a being introduced. Biol. Invas. 8: 1523–1534. high genetic diversity in offspring; in one study Angilletta MJ, Steury TD, & Sears MW 2004. Temperature, growth rate, and body size in ectotherms: fitting pieces of (Dupont et al. 2006), nearly 80% of broods exam- – ined had been fertilized by two to five males, nearly a life-history puzzle. Integr. Comp. Biol. 44: 498 509. Beninger PG, Valdizan A, Decottigies P, & Cognie B all of which were still resident on the same stack at 2010. Field reproductive dynamics of the invasive slip- the time of sampling. Sperm storage may also be a per limpet, Crepidula fornicata. J. Exp. Mar. Biol. 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The invasive gastropod Crepidula fornicata: reproduction and individuals in a native population in Rhode Island, recruitment in the intertidal at its northernmost range USA; there is certainly no indication of a stress- in Wales, UK, and implications for its secondary induced decline in egg production by the Norwegian spread. Mar. Biol. 159: 2091–2103. females. Both the number of embryos per egg cap- ———— 2013. The importance of larval supply, larval sule and the number of embryos per egg mass were habitat selection and post-settlement mortality in deter- significantly greater for sampled Norwegian females mining intertidal adult abundance of the invasive gas- than for their more southern Rhode Island counter- tropod Crepidula fornicata. J. Exp. Mar. Biol. Ecol. parts. The mechanisms accounting for these differ- 440: 132–140. ences remain to be explored. 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Sjøtun K 1997. A new observation of Crepidula fornicata Fig. S1. Relationship between fecundity of Norwegian (Prosobranchia, Calyptraeidae) in western Norway. females and (A) female dry tissue weight, (B) dry shell Sarsia 82: 275–276. weight, and (C) shell length, showing the statistical results Thieltges DW, Strasser M, van Beusekom JE, & Reise K of regression analyses on the untransformed data. 2004. Too cold to prosper—winter mortality prevents Fig. S2. Fecundity in C. fornicata: comparisons between population increase of the introduced American slipper the Norwegian females (blue dots) sampled in 2012 and limpet Crepidula fornicata in northern Europe. J. Exp. 2013 and those sampled from a native population in Mar. Biol. Ecol. 311: 375–391. Wickford, Rhode Island, USA (open circles), in 2012 and Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, & 2013. Kuris AM 2003. Introduced species and their missing Fig. S3. Relationship between number of egg capsules per parasites. Nature 421: 628–630. egg mass and female size for sampled Norwegian (blue Valdizan A, Beninger PG, Decottignies P, Chantrel M, & dots) and Rhode Island (open circles) females of C. forni- Cognie B 2011. Evidence that rising coastal seawater cata. The plotted data have not been transformed. temperatures increase reproductive output of the inva- Fig. S4. The inﬂuence of sampling location (Norway vs. sive gastropod Crepidula fornicata. Mar. Ecol. Prog. Rhode Island) on the mean number of embryos per egg Ser. 438: 153–165. capsule in females of C. fornicata. Fig. S5. Effect of location on the relationship between female size and mean egg capsule sizes for the two sam- Supporting information pled populations of C. fornicata (Norway, blue dots, Additional Supporting information may be found in the mean SD; Rhode Island, open circles). The plotted online version of this article: data have not been transformed.

Invertebrate Biology vol. 136, no. 4, December 2017