Biol Invasions https://doi.org/10.1007/s10530-018-1776-2

ORIGINAL PAPER

Comparing residence time and natural enemies between low- and high- density invasions Emily W. Grason

. P. Sean McDonald . Jennifer L. Ruesink

Received: 19 November 2017 / Accepted: 29 May 2018 Ó Springer International Publishing AG, part of Springer Nature 2018

Abstract Ecological and historical factors influence the probability that a known invader will experience success in new locations. Using field and laboratory studies, we investigated how residence time and natural enemies (co-evolved castrating parasite, and native crabs) differ between two introduced populations of the intertidal snail, Batillaria attramentaria. The populations have substantially different invasion histories (* 10 vs. [ 80 years) and exhibit markedly different densities and tidal distributions. The lessdense, vertically-restricted population was recently introduced, and thus has potentially had less opportunity to fill the fundamental niche at that site. However, no increase in density or intertidal range occurred in this population over 10 years, suggesting that it had reached its realized niche. The newer population experienced much greater effects of native cancrid crabs than the older, high-density population, particularly below the minimum tidal elevation of observed E. W. Grason (&) Washington Sea Grant, University of Washington, 3716 Brooklyn Avenue N.E, Seattle, WA 98105-6716, USA e-mail: [email protected] P. SeanMcDonald Program on the Environment, University of Washington, Box 355679, Seattle, WA 98195-5679, USA J. L. Ruesink Department of Biology, University of Washington, Box 351800, 24 Kincaid Hall, Seattle, WA 98195-1800, USA

snail distribution, where crabs were found in the greatest densities. Prevalence of parasite infection did not differ between populations. This is the first study documenting effects of predators on this invasive snail, which is widespread along coastlines of the northeast Pacific, whereas previous studies have suggested that the primary restriction on population growth rate was likely to be parasitic castration. Further, this study supports the general understanding that, while novel predators can reduce the impacts or population growth rates of invasive species, such topdown effects are not likely to preclude persistence at a given site. Keywords Batillaria attramentaria
Biotic resistance
Invasive
Natural enemies
Predators
Residence time
Realized niche

Introduction Many risk assessments for invasive species rely on the observation that similar abiotic conditions between native and introduced ranges, and the species’ history of impact in prior invasions elsewhere should increase the probability of invasion (Moyle and Light 1996; Kolar and Lodge 2001; Peterson 2003; Thuiller et al. 2005). Exceptions to this rule, in which an introduction proves less successful than expected based on

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these factors, provide opportunities to examine the ecological and historical contexts that impede prediction. Invasion success can be defined both qualitatively, i.e., how a species progresses through the introduction, establishment, spread, and impact stages of invasion; and quantitatively, i.e. how vital rates, population parameters, and interaction strengths compare at each of those stages. A broad suite of factors can affect these outcomes for any newly-established non-native species: phenomenological factors such as propagule pressure (Lockwood et al. 2005; Colautti et al. 2006; Simberloff 2009), and residence time (Pysˇek and Jarosˇik 2005; Wilson et al. 2007); intrinsic characteristics of the introduced species, such as life history strategy, and dispersal ability (Sakai et al. 2001); and features of the novel range, such as abiotic conditions, and interactions with the resident community (Levine et al. 2004; Colautti et al. 2006; Suwa and Louda 2012; Zenni and Nun˜ez 2013). When a species performs differently in similar abiotic conditions, two non-mutually exclusive explanations for relatively poor performance of an otherwise successful invader are time since introduction (residence time) and natural enemies. Regarding the former, a recently-introduced population might fill only part of its total potential range if it is dispersallimited (Pysˇek and Jarosˇik 2005; Wilson et al. 2007) or might be present in small numbers if few propagules were initially introduced (Lockwood et al. 2005; Colautti et al. 2006; Simberloff 2009). Regarding the latter, biotic interactions with either co-evolved or local predators, pathogens, or competitors can limit the spread and population growth of non-native species (Levine et al. 2004; Colautti et al. 2006; Suwa and Louda 2012; Zenni and Nun˜ez 2013). Assessing the role that each of these factors plays in influencing the trajectory of an invasion is key to forecasting the impact of the invasion, as well as helping to determine the probability of other invasions by the same species. Here we explore the influence of natural enemies and residence time on the tidal range and abundance of a non-native marine snail, comparing the importance of each factor between two populations that differ in invasion history and relative success. The intertidal snail, Batillaria attramentaria (hereafter: Batillaria), is native to the northwestern Pacific Ocean but has established populations along shorelines in the northeastern Pacific from Monterey Bay, California to Boundary Bay, Canada (36.8°N to

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49.0°N; Byers 1999). Negative impacts have been demonstrated where Batillaria overlaps with a similar native snail in the southern part of its invaded range (Byers 1999), but in the northern part, some facilitative effects occur (Wonham et al. 2005). Whether positive or negative, these impacts emerge in part due to Batillaria’s high population densities ([ 3000 m-2) for an organism with a shell length up to 4 cm (Byers and Goldwasser 2001). The initial introduction appears to have accompanied imports of Pacific oysters (Crassostrea gigas) in the first part of the twentieth century (Wonham and Carlton 2005). This species lacks a pelagic larval stage, and crawlaway juveniles hatch from benthic egg capsules (Yamada and Sankurathri 1977); therefore, subsequent regional spread of Batillaria has been humanmediated. The history and ecology of this species sets up a scenario in which, within a region, sites can have populations with different initial introduction dates and distinct dynamics. Byers (1999), in comparing sites across the U.S. west coast, has observed that date of initial oyster import was not a good predictor of Batillaria presence or density. In this study, we

Fig. 1 Map of study sites. In Padilla Bay, surveying was conducted at the Padilla Bay National Estuarine Research Reserve (NERR) interpretive center, and the tethering study occurred adjacent to the Sullivan-Minor Gun Club. In Willapa Bay, both surveying and tethering were conducted at Oysterville, the only location in the bay at which Batillaria has been reported

Comparing residence time and natural enemies

compare two populations from Washington State (Fig. 1) to discern whether differences in abundance and tidal distribution are best explained by residence time or interactions with potential natural enemies. Batillaria has likely been present in Padilla Bay since the 1930s (Bulthuis 2013); we designate this the ‘‘older’’ site. By contrast, at the ‘‘newer’’ site, Willapa Bay, Batillaria was first observed in 2004 (JLR, personal observation) and was not listed as present there in a compilation of introduced species published about that time (Wonham and Carlton 2005). Batillaria is a likely hitchhiker on aquaculture material from Japan, especially shell and juvenile oysters imported to Washington annually from the early 1900s until 1977 (White et al. 2009). The ‘‘newer’’ site has substantially more shellfish aquaculture production than the ‘‘older’’ site, and, accordingly, a history of more imports that could have been a potential vector. Therefore, the timing of establishment of Batillaria at the two sites contradicts what might be expected from propagule pressure. Initial plantings of Pacific oysters at the ‘‘older’’ site occurred in 1932 (Dinnel 2000). Plantings at the ‘‘newer’’ site occurred as early as 1928 (Kincaid 1968), and were likely greater in total volume, but Batillaria did not appear until several decades after direct imports from Japan had ended. The establishment of the invasive snail in Willapa Bay, therefore, most assuredly results from a secondary introduction via transport of material from another shellfish growing location in Washington. To date, Batillaria has only been observed around a single location on the west side of Willapa Bay—Oysterville. Initial observations suggested that the newer population (Willapa Bay) is currently less successful than the older population (Padilla Bay): restricted to higher tidal elevations, and lower densities. A short residence time could explain a relatively small population of snails, with a narrow tidal distribution, simply because of the time it takes populations to grow and disperse. In addition to residence time, tidal distribution and abundance of Batillaria could be influenced by either co-evolved or novel natural enemies. In modeling studies Byers and Goldwasser (2001) found that low mortality rates (inclusive of intrinsic and extrinsic sources) governed both the dynamics and impacts of Batillaria in California, which were less sensitive to variability in reproduction. Reproduction is influenced in part by co-evolved parasitic trematodes, which infect Batillaria as the obligate first intermediate host,

ultimately castrating the snails by appropriating gonad tissue for their own reproduction (Torchin et al. 2005; Miura et al. 2006). Therefore, the population growth rate is influenced by the proportion of adult snails infected with trematodes. Infection not only castrates the snail, but causes the snail to grow as much as 50% larger and to migrate deeper into the intertidal zone (Torchin et al. 2005; Miura et al. 2006; Grason Unpublished Data). The top-down effects of predators on Batillaria are not well understood, in that no publications have documented predation on this species, but it seems likely that generalist crabs and molluscivorous fish opportunistically consume snails as they forage on the incoming tides. Using a combination of survey and experimental data, we explored three possible influences on the abundance and distribution of Batillaria, by comparing the tidal range, density, parasite prevalence, and local predator effects between snails in Padilla Bay (older population, broader tidal distribution and higher density) and Willapa Bay (newer population, restricted tidal distribution and lower density). 1.

2.

Residence time Variability in density and tidal range reflect the influence of different times since introduction for the two sites. If residence were the only factor limiting observed density and distribution, we would predict (1) that the newer population in Willapa Bay would experience greater population growth than the older invasion in Padilla Bay; and, (2) the lower limit of tidal distribution would become deeper over time for the newer, but not the older, invasion as the newer population progressively fills the fundamental niche. Co-evolved parasites Variability in density and tidal range reflect different rates of infection rates by the co-evolved, non-native, trematode. Parasitic castration, movement, and somatic growth of parasitized snails would generate opposing predictions about which population would have a higher infection rate. Firstly, because snails migrate deeper when infected, we would expect increased parasite prevalence to be associated with a deeper tidal distribution. This corresponds to current observations of distribution in Padilla Bay (older), and therefore generates the prediction that parasite prevalence would be higher in that population. Yet we would also expect that

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3.

increased infection rates would lead to a decreased population growth rate, and increased somatic growth rates and snail sizes that result from infection could reduce the carrying capacity of the site, resulting in relatively lower densities. This logic would result in the prediction that the Willapa Bay (newer) population has a higher infection prevalence. Native predators Variability in density and tidal range reflect a difference in top-down effects by native predators, due to variation in either predator abundance or assemblages. A relatively greater abundance of effective predators could result in increased predation pressure, and consequently decreased snail density, across the tidal range (i.e. biotic resistance, sensu stricto). A difference in tidal ranges could be caused by different assemblages of predators. Either case would result in a difference in realized niches between the two sites. This hypothesis generates two predictions: (1) increased abundance of effective predators in Willapa Bay (newer) relative to Padilla Bay (older); and, (2) snails in Willapa Bay experience greater predation rates than snails in Padilla Bay, particularly at or below their currently-observed lower limit of distribution.

Our hypotheses regarding mechanisms for differential invasion success between sites emphasize residence time and enemy release because the extensive softsediment tideflats and water temperatures are similar in the bays, and abiotic conditions are considered less likely than biotic conditions to determine lower limits of intertidal organisms (Connell 1961). Elucidating the mechanisms that influence abundance and distribution of this invasive snail will provide insight into the conditions which favor invasion for Batillaria and the extent to which the success of this species might vary over space and time.

Methods We used a combination of surveying, tethering studies, trapping, and laboratory predation studies to explore support for the hypothesized mechanisms determining the difference in density and distribution of the two populations of Batillaria attramentaria.

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Population surveys Batillaria density and parasite infection status were surveyed in vertical transects (i.e., along a tidal elevation gradient) in both bays in 2007, 2008, and 2011, and in Willapa Bay only in 2016 (Fig. 1). In Willapa Bay, the site of the newer population, all surveys were conducted at Oysterville, and surveys of the older population were conducted near the Padilla Bay National Estuarine Research Reserve interpretive center. Spanning the vertical range of observed snail distribution at each site, we sampled between 3 and 25 evenly-spaced (in linear distance) positions, estimating abundance by counting snails in 1–5 quadrats (0.25 m2, distribution of transect effort summarized in Table 1). To assess infection prevalence of trematodes across elevation, snail size, and between sites, we collected a subsample of snails from every elevation sampled during the 2011 transects (28 elevations in ‘‘older’’/ Padilla, 23 elevations at ‘‘newer’’/Willapa). For Padilla Bay, parasite data was supplemented with observations from an identically-designed transect approximately 1.3 km to the north, after verifying that prevalence was similar between the two sites. To reduce the potential for size bias of subsampled snails (because infection rates vary based on snail size), we collected all snails from each of the replicate quadrats until a minimum of 20 snails was collected. When the minimum was reached, the remaining snails for that quadrat were also collected and assessed. At the lowest elevation, it was occasionally impossible to find 20 snails, so all snails detected were assessed. Thus, sample sizes of snails for which infection was assessed varied somewhat with elevation and snail density. Snails were measured by shell length, and brought to the lab to assess parasite infection status (as in Torchin et al. 2005). Cercaria batillariae is reported to be the only species to infect Batillaria in the invaded range (Torchin et al. 2005), and, in concordance, we did not observe any of the other species that can infect Batillaria in the native range (Hechinger 2007). In Willapa Bay (newer), tidal height for each sampling location was determined by extracting elevation values (m above mean lower-low water, MLLW) from a digital elevation model of Willapa Bay (ONRC 2008) based on geographic position collected with a handheld geographic position system (GPS) unit (Garmin Geko 201). Because we were not

Comparing residence time and natural enemies Table 1 Summary of transect survey parameters for two study sites, Padilla Bay (older population), and Willapa Bay, Washington (newer population) Site

Survey year

No. transects

Padilla Bay

2007

3

2008 2011 Willapa Bay

No. positions (elevations) within each transect

No. quadrats at each position

4

1

5

5

1

2

25

2

2007 and 2008

3

3

1

2011

1

23

5

2016

1

20

5

able to obtain high-resolution elevation data for the intertidal zone in Padilla Bay (older), we measured elevation directly, using Real Time Kinematic (RTK) and Post-Processed Kinematic GPS. We derived tidal elevations from GPS measurements using VDatum (www.vdatum.noaa.gov). Intertidal distribution of Batillaria proved to be non-overlapping between the two sites based on vertical distance relative to MLLW (Fig. 2a). Otherwise, both sites were shallow-slope soft-sediment tideflats. To enable comparisons between the two sites using elevation as a predictor, we also defined elevation as position normalized to the local observed vertical extent of Batillaria, considering both the lower limit (0) and the upper limit (1) (relative elevation). We focused on the lower limit, even though the upper limit also differed, because physical

features, either a steep cliff or man-made dike fronting terrestrial conditions, restricted the upper limit at one site (Padilla/older).

Fig. 2 Inundation time (a) and horizontal distance from lower limit of Batillaria (b) of tethering sites in Padilla Bay (older population) and Willapa Bay (newer population) relative to elevation in meters above mean lower-low water (MLLW). Filled symbols represent tethering positions at Padilla Bay, while open symbols represent tethering positions at Willapa.

Grey symbols in panel a represent the tethering positions that were below the lower limit of observed snail distribution at that site. There are three such positions (overlapping points) in Padilla Bay and four in Willapa Bay, WA. Bars in panel b represent horizontal range extent of Batillaria for each site (Willapa Bay: white bar; Padilla Bay: black bar)

Analysis We tested the first hypothesis (i.e., residence time limits population size and spread) by examining changes in snail density over time (2007–2011) in both populations, as well as the variation in the lower limit at the site of the newer population in Willapa Bay. Density (snails m-2) was modeled as a function of year (continuous variable) and site (fixed factor: in a two-way generalized linear model (GLM) with a log link function and Poisson error distribution). We tested whether the lower vertical limit of distribution became deeper over time for the newer

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population (Willapa Bay) only. This observation would support the prediction of dispersal limitation in the first hypothesis, i.e., that a relatively short residence time had not provided sufficient opportunity for this direct-developing snail to migrate across the distance required to reach a similar depth as the older population in Padilla Bay. Only data from 2011 to 2016 were used to test this prediction, because observations in the first two sample years were not taken at tidal elevations low enough to directly observe the lower limit. To estimate the lower limit of distribution, snail density at this site was modeled separately for each year as a linear function of elevation for each of the 2 years. In these models, absolute elevation (meters above MLLW) was included as both a linear and a quadratic term, because we expected densities to be lower at the upper and lower limits of distribution (Whittaker 1967). We established 95% CI around each of the modeled relationships and, by assessing their overlap, determined whether the depth of the predicted lower limit differed between years. We tested the second hypothesis (i.e., parasitic infection prevalence influences tidal distribution and population growth) by determining whether the probability of being infected differed between the snail populations at the two sites during 2011. Because snails grow larger and migrate deeper when they become infected by C. batillariae (Miura et al. 2006), estimates of prevalence for a given site must account for both size of snails and elevations sampled. We modeled the probability that a given snail was infected with a binomial GLM (logit link) with site, size, relative elevation (ranging from 0 to 1, as described above), and their two-way interactions as predictors. Parasite prevalence was assessed in all survey years, but did not fluctuate appreciably during the observation period (P.S. McDonald, unpublished data). We present only the 2011 data because it had the highest spatial resolution. Predation studies We assessed the abundance of predators at each site with baited traps and evaluated predation on Batillaria using field-based tethering and a laboratory predation experiment. Field activities related to the predation study were done in the same locations as transect surveys (Fig. 1). The laboratory experiment was

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conducted in flow-through seawater aquaria at Shannon Point Marine Center (Anacortes, Washington). Trapping To compare the communities of probable predators of Batillaria, we trapped mobile epifauna across an elevation gradient at both sites, at a subset of positions used in the tethering study (below). At four regularlyspaced positions spanning the tidal heights across which snails were tethered (lowest, fourth, seventh, and highest positions), we deployed five rectangular Fukui fish traps (model FT-100, 60 9 45 9 20 cm with 12 mm mesh) separated by at least 20 m. These traps capture a wide variety of fish, including perch, sculpin, and flatfish, as well as invertebrates, and were baited with approximately 200 g of frozen mackerel (e.g., Holsman et al. 2006). Due to differences in tidal regimes and Batillaria distribution at the two sites, traps at Willapa Bay (newer) were more likely to be emersed on the higher-low tide of the mixed semidiurnal tide cycle. To avoid fish mortality, traps were retrieved after 11 h at the newer site (9 July 2013), and 20 h at the older site (8 July 2013). Despite this difference, trap soaks at both sites included an overnight high tide, when predators are most attracted to baited traps, and trap catches have been adjusted for the soak time and are therefore expressed as rates. At the end of each soak, all organisms in each trap were identified to species and counted. To estimate the size of crabs in the traps, we measured the carapace width of the first 10 crabs haphazardly selected from each trap. We attempted to reduce size bias of subsamples of crabs by mixing crabs before selecting them. Tethering To test whether the effects of native predators of Batillaria differed between sites, we conducted tethering studies in both bays during consecutive years (Padilla Bay/older in 2012; Willapa Bay/younger 2013). Tethered Batillaria of three size classes were deployed across a vertical transect for several weeks and observed for evidence of predation or predation attempts. At each of 10 positions along the vertical transects, 10 of each size class of snail were individually tethered to a single 1 m length of rebar with 20–30 cm of monofilament line and cyanoacrylate gel. The tethering did not appear to inhibit snails’ ability to

Comparing residence time and natural enemies

bury. Of the 10 elevations, the highest 7 were arrayed across the observed distribution of snails at that site such that the tethering stations were evenly spaced horizontally. In addition, because we were interested in whether subtidal predators influence the lower distribution limit as well as the overall density of Batillaria, the lowest 3 tethering positions were situated beyond the deepest observation of snails (Padilla Bay: 0.30 m MLLW; Willapa Bay: 1.35 m MLLW, Fig. 2), and separated from each other by the same horizontal distance as the higher 7 positions. We arrayed snails along the rebar in an order that haphazardly mixed individuals of different size classes, and laid the rebar flat in the mud, perpendicular to the elevation gradient. The density of tethered snails at each rebar position was 810 snails m-2 (30 snails in an area of approximately 0.4 m2), which is within natural observed densities at the higher elevations in Padilla Bay. Because snails are patchily distributed, we did not manipulate local density of untethered snails at the tethering site. Thus the actual local density of snails at tethering sites varied across elevation, and across time. We used only snails collected locally from a similar tidal elevation for each experiment. Very small snails were scarce in Willapa Bay. As a result, size classes differed slightly between the two bays in the study (Padilla/older: small: 11–16 mm, medium: 20–25 mm, large: 29–35 mm; Willapa/newer: small: \ 20 mm, medium: 22–25 mm, large: [ 28 mm). Tethered snails were deployed on the same tidal cycle in successive years (Padilla/older population: 23 May, 2012; Willapa/younger population: 24 May, 2013). For the duration of the study periods, we recorded observations of snail damage, death, and disappearance approximately every 2 weeks for 6 weeks. Missing and damaged shells, either with or without living snails in them, were interpreted as evidence of attempted predation. We believe this is a safe assumption as mechanical damage due to storms, waves, or beachgoers was unlikely at either of these low-energy beaches that are rarely visited by humans. To determine whether predators differentially affected the two populations, we compared the proportion of snails from each size class that were damaged by predators at the end of 6 weeks. To standardize elevations assayed between the two populations, we used relative elevation (as described above) as a continuous predictor, and restricted

observations in the analysis to the range for which relative elevation was similar. This removed the deepest three, and highest two, tethering positions for Willapa Bay. The deepest tethering positions in Willapa were substantially lower than those in Padilla because the relatively shallow vertical range limit of snails meant that elevations beyond the deepest vertical range limit were more accessible in Willapa but not Padilla Bay. In addition, the highest two thethering positions in Willapa were removed from the analysis, because tethered snails were not deployed all the way to the upper range limit in Padilla Bay. We modeled the proportion of snails that were damaged by predators using a GLM with binomial error distribution and a logit link function with relative elevation (as above), size class (small, medium, large), site (Padilla or Willapa Bay), and their two-way interactions as predictors. Laboratory experiment We evaluated size-selective predation of Batillaria by an abundant predator, Dungeness crab (Cancer magister (= Metacarcinus magister)), using a laboratory experiment. Prior to the start of the experiment, crabs (109–120 mm CW) were fed crushed Batillaria ad libitum for at least 24 h to ensure only crabs for which this prey item was acceptable were used in the experiment. This also enabled us to identify and remove pre-molt crabs, which typically do not engage in feeding. Crabs demonstrating normal feeding behavior were then starved for an additional 48 h prior to the experiment to increase motivation to feed. Individual crabs were enclosed in seven replicate plastic baskets enclosures (22 cm 9 35 cm 9 13 cm) fitted with mesh screen (0.33 mm) side walls and lids and placed in a flow-through table receiving a constant supply of sea water. A small amount of clean sand was added to each enclosure and ten Batillaria from each of three size classes (small: 12–15 mm, medium: 20–24 mm, large: 30–34 mm) were distributed haphazardly on the substrate surface (n = 30 snails) and allowed to acclimate for 1 h before the addition of the crab. An additional enclosure received no crab and functioned as a partial control for natural mortality. Crabs never consumed all of the snails available for a single size class, and no replacement was conducted. After 72 h, all Batillaria were removed and checked for obvious signs of crab predation, and the sand

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within each enclosure was sieved to collect all shell fragments. We tested whether crabs demonstrated size-selective predation using a binomial generalized linear mixed effects model (GLMM) with the number of snails killed or damaged of each size class as the response variable conditioned on the number of snails initially available. The model also included a randomly varying intercept for each individual replicate enclosure, to account for between–crab variation. No background mortality occurred in the partial control, and we therefore omitted this treatment from the analysis. Two enclosures where crabs did not consume any snails (i.e., no predation-related mortality) were also excluded from the analysis, as was an enclosure in which the position preferentially allowed small snails to crawl out of the water confounding the treatments, yielding 4 experimental replicates.

Results Population survey The present survey confirmed previous observations that the lower intertidal limit of Batillaria differs substantially between these two sites. Batillaria in Padilla Bay were observed as deep as 0.30 m above MLLW (Fig. 3), which is similar to observations made throughout that bay (Grason unpublished data). However, Batillaria in Willapa Bay were restricted to a higher elevation, and only occurred as deep as 1.4 m above MLLW (Fig. 3). Notably, the upper vertical elevation limit of Batillaria is also higher in Willapa (newer) than Padilla Bay (older), but this is primarily due to the extensive historical diking of Padilla Bay (PBNERR 2008), which has eliminated the higher elevation tide flats in the majority of that estuary. Averaged across all years, Batillaria in Padilla Bay were present in three-fold greater densities than in Willapa Bay, the site of the newer population (Figs. 3, 4; Table 2). Snail density was relatively stable from 2007 to 2011 in Willapa Bay, but was substantially lower in the final sampling year than the first 2 years in Padilla Bay (Table 2; Fig. 4). Though not included in the analysis, observations from 2016 in Willapa Bay suggest that the density of Batillaria has remained low (average ± SEM: 36.2 ±4.2) since the time period over which densities were compared.

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Fig. 3 Batillaria attramentaria density across tidal elevation gradients in three survey years (2007, black; 2008, red; 2011, blue) at Padilla Bay (older population, filled symbols) and Willapa Bay (newer population, open symbols), WA Table 2 Summary table for generalized linear model (Poisson error, log link) of Batillaria density across 3 years (2007, 2008, and 2011) and two introduction sites (Padilla/older and Willapa/newer populations) Factor

Estimate

SE

Z

p

5.313

0.007

761.77

\ 0.001

Site

- 1.279

0.012

- 104.89

\ 0.001

Year

- 0.166

0.003

- 51.41

\ 0.001

0.059

0.005

12.89

\ 0.001

Intercept

Site 9 year

Bold values indicate statistical significance at P \ 0.05

Batillaria in Willapa Bay (newer) did not extent their distribution to lower tidal elevations over time (Fig. 5). The 95% confidence limits of the lower limits of distribution for 2011 (r2 = 0.11) and 2016 (r2 = 0.27) overlap substantially, based on fitting each year’s data with linear and quadratic terms for elevation. Averaged across the entire transect, infection prevalence was similar between the two populations; 60% of Batillaria in Padilla Bay/older, and 57% in Willapa Bay/newer, were infected with parasitic trematodes. In the model, site was not supported as a significant factor influencing the probability that a given snail was infected (Fig. 6; Table 3). The two-

Comparing residence time and natural enemies

Fig. 4 Average density (± 1 SEM) of Batillaria attramentaria measured across vertical transects in 2007, 2008 and 2011 at Padilla Bay (older population, filled symbols) and Willapa Bay (newer population, open symbols), WA

Fig. 6 Proportion of a sample of 20 Batillaria attramentaria infected with trematode parasites as a function of average snail size (mm) in 2011. Filled symbols: Padilla Bay (older population); open symbols Willapa Bay (newer population)

Predation studies Trapping

Fig. 5 Batillaria attramentaria density across tidal elevation gradients at the site of the newer population, Willapa Bay, WA, for 2 years (2011 black/grey; and 2016 red/pink). Lines are predicted relationship between density and elevation (including a quadratic term) modeled separately for each year, with 95% confidence intervals in shaded portions

way interaction between relative elevation and size was also statistically supported, but this reflects the complex association between snail size, infection rates, and behavior (Miura et al. 2006) rather than any site-related differences.

There were striking differences in the communities of potential predators of Batillaria captured in the trapping survey (Fig. 7). Cancrid crabs (mean carapace width = 66.1 mm, standard deviation 10.2 mm, n = 97; primarily Cancer magister (= Metacarcinus magister), but also Cancer productus) were trapped only at Willapa Bay (newer), and only at the two deepest trapping positions (corresponding with the deepest and 4thdeepest tethering positions). Cancrids were entirely absent from traps deployed in Padilla Bay (older), despite the longer trap deployment and greater inundation time at that site relative to Willapa Bay, as well as a documented presence in the bay (Dinnel et al. 1986). The only crabs captured in traps at that site were small grapsid crabs (maximum carapace width = 30 mm, Hemigrapsus oregonensis); their abundance was low and did not appear to vary with tidal elevation. Staghorn sculpin (Leptocottus armatus) were captured at both sites. At Willapa Bay, they appeared in traps at all elevations, and were most abundant in the middle of the elevation gradient. The abundance of sculpins was lower overall at the older site, and they were captured only at the deepest two trapping positions.

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E. W. Grason et al. Table 3 Summary table for generalized linear model (binomial error, logit link) of probability of infection by trematodes in Batillaria surveyed in 2011, across relative elevation, size, and two introduction sites (Padilla/older and Willapa/newer populations) Factor

Estimate

SE

Z

Site

- 2.779

2.718

- 1.02

Relative elevation Size Site 9 relative elevation Site 9 size Relative elevation 9 size

p 0.301

11.615

5.425

2.14

0.032

0.720

0.092

7.86

\ 0.001

- 0.887

1.342

- 0.66

0.508

0.141

0.100

1.41

0.158

- 0.447

0.221

- 2.02

0.043

Bold values indicate statistical significance at P \ 0.05

Fig. 7 Average Fukui trap catches (1 SEM), standardized by effort, of four species of potential predators of Batillaria attramentaria as a function of tidal elevation relative to local observed distribution of snails (0 = lower limit, 1 = upper

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limit). Traps were set at lowest, fourth, seventh, and highest tethering positions at each site. Filled symbols represent catches at Padilla Bay (older population), and open symbols indicate catches in Willapa Bay, WA (newer population)

Comparing residence time and natural enemies

Tethering In the analysis of predator effects, which included only the tethering positions that overlapped in relative elevation between the two sites, the proportion of tethered snails attacked or consumed by predators differed between the two sites (Fig. 8a; Table 4). Overall, within the overlapping elevations 40.1% of snails at Willapa Bay (newer), and 9.6% of snails in Padilla Bay (older) were either damaged or consumed by predators. At the older site, with overall low predator effects, predators had the greatest effects on medium sized snails, 62% of damaged snails at that site were from the medium size class. By contrast, at the newer site, small snails showed the greatest frequency of damage or predation (62% of small snails, representing 43% of total damage) and large snails were significantly less damaged (34%). These results are indicated by a significant effect of the large size class for the reference site (Willapa/newer) and a significant interaction term for the medium size class with site (Table 4). While the model comparing sites necessarily excluded data from Willapa Bay outside the range of relative elevations assessed in Padilla Bay, qualitative evaluation of those observations indicate that effects of predators on snails in Willapa Bay (newer) increased substantially at deeper tidal elevations (Fig. 8b). At the lowest three positions, which were below the deepest limit of Batillaria’s vertical distribution at that site, 89 out 90 tethered snails were attacked or consumed by predators, while predator effects in the upper half of the elevation gradient, though patchy, averaged 30%. Laboratory experiment In the laboratory predation experiment, mortality and shell damage from was greatest for small and medium snails (Fig. 9), with an average 23 and 20% affected by predators, respectively. Mortality and shell damage for large snails (5%) was significantly lower than for small snails (Table 5). All dead Batillaria showed evidence of crab predation (e.g., broken/crushed shells), and no mortality occurred in the predator-free control enclosure.

Fig. 8 Proportion of 10 snails in each of three size classes of Batillaria attramentaria damaged or killed by predators in tethering study as a function of tidal elevation relative to local observed distribution of snails (0 = lower limit, 1 = upper limit). Panel a shows only overlapping relative elevations included in analysis, for visibility. Panel b shows full extent of tethering stations for both sites including sites that were removed from analysis in Willapa Bay (deepest three, and highest two). Open symbols are observations from Willapa Bay (newer population), filled symbols represent Padilla Bay, WA (older population). Size class: small = circle/dotted line, medium = triangle/dashed line, large = square/solid line)

Discussion We observed the strongest support for the hypothesis that two populations of Batillaria differ in distribution

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E. W. Grason et al. Table 4 Summary table for generalized linear model (binomial error, logit link) of number of Batillaria (n = 10) affected by predators based on site (Padilla/older and Willapa/newer Factor Intercept Relative elevation

populations), Batillaria size class, and relative elevation. The reference group for the GLM comparison of size was the small size class, and Willapa Bay for site

Estimate

SE

Z

p

1.106

0.474

2.335

0.020

- 2.582

1.430

- 1.806

0.071 \ 0.001

Site

- 4.338

0.848

- 5.114

Size class (medium)

- 0.715

0.621

- 1.150

0.250

Size class (large)

- 1.490

0.622

- 2.394

0.017

Relative elevation 9 site

0.120

- 4.201

2.704

- 1.554

Relative elevation 9 size (medium)

0.635

1.916

0.331

0.740

Relative elevation 9 size (large)

1.129

1.956

0.577

0.564

Site 9 size (medium)

2.167

0.985

2.200

0.028

Size 9 size (large)

1.854

1.085

1.709

0.088

Bold values indicate statistical significance at P \ 0.05

Table 5 Summary table for generalized linear mixed effects model (binomial error, logit link) of the number, out of 10, of Batillaria of each of three size classes affected by crabs, Cancer magister (= Metacarcinus magister)—predation-related damage and mortality—in the laboratory experiment (n = 4). The reference group for factor of size was the small size class Size class

Estimate

SEM

Z

p

Small (reference group)

- 1.237

0.379

- 3.266

0.001

Medium

- 0.150

0.547

- 0.273

0.785

Large

- 1.708

0.818

- 2.987

0.037

Bold values indicate statistical significance at P \ 0.05

Fig. 9 Proportion of 10 snails in each of three size classes of Batillaria attramentaria damaged or killed by Cancer magister (= Metacarcinus magister, n = 4) in size-selectivity laboratory experiment. Each symbol type represents a different individual replicate crab and x axis is jittered for visibility

and density due to top down effects of native predators, rather than an effect of residence time, or infection by co-evolved parasites. The importance of natural enemies is supported by data from a combination of surveys, tethering studies, trapping, and laboratory predation studies. Evidence from surveys did not support the first hypothesis that the differences in abundance and tidal distribution of the two populations are explained by residence time. Neither of the two predictions under

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this hypothesis were supported; the newer population (Willapa Bay) did not grow in density or expand its distribution deeper over the study period, suggesting that this population has likely filled its realized niche. Though this species is a direct-developing gastropod with no planktonic dispersal (Yamada and Sankurathri 1977), evidence from a prior study suggests that migration of adults could have enabled Batillaria to traverse the horizontal distance necessary to match the deeper vertical range limit of snails observed in the older, Padilla Bay population. Batillaria from the native range traveled an average of 15 cm per day in a mark-release-recapture study (Miura et al. 2006). At this rate, which is likely conservative, the population in Willapa Bay could have crawled at least 219 horizontal meters deeper, corresponding to a depth of 0.9 m MLLW, at which elevation 100% of snails in the tethering experiment were damaged or killed by

Comparing residence time and natural enemies

predators. In 2011 and 2016, Batillaria were never observed deeper than 1.35 m MLLW in Willapa Bay, either in quadrats or in additional searching outside of quadrats. The second hypothesis was also not supported by surveys. Infection by co-evolved parasitic trematodes does not explain differences in elevation or density of snails, as infection rates were similar in the two populations. Thus neither prediction (of higher or lower prevalence in the newer population) generated by this hypothesis was supported. Infection rates in both populations were also similar to those reported for the native range (52.6% Miura et al. 2006), and within the recently reported range for in another population on the west coast of the United States: 46–73% in Elkhorn Slough, California (Lin 2006; Fabian 2016). Notably, however, we observed a much lower frequency of infection than was reported for Padilla Bay in 2000 (86.2%), and much higher than other locations in California during that same year (2.7–14.0%, Torchin et al. 2005). Given that infection prevalence varies with depth, it is difficult to interpret these earliest observations, because the methods for collection are not reported. The observed infection prevalence would increase in collection areas at lower elevations or biased towards larger-sized snails (Fig. 6). Transect surveys in Padilla Bay in 2007 and 2008 also collected a small number of snails to assess parasite infection. While those observations are too sparse to provide a robust test of change over time, they generally indicate infection prevalence has been stable since 2007 (59%, P.S. McDonald, unpublished data). The infection prevalences observed in the present study are likely to reduce population growth rates relative to an uninfected population, but the inability to detect a difference in overall infection rates between the two sites does not support the hypothesis that parasites are driving current differential success. We observed the strongest support for the third hypothesis that predators, namely cancrid crabs, influence the abundance, elevation, and size distribution of the newer population of Batillaria in Willapa Bay, but have substantially weaker effects on the older population in Padilla Bay. The difference in predator communities has apparently resulted in different realized niches for Batillaria at the two sites. The effects of predators on tethered snails were, overall, greater in Willapa Bay, and increased sharply near the lower limit of observed snail distribution at that site. It

has been well established in intertidal marine habitats that predation can be influential in determining the deeper vertical extent of species’ distributions (Connell 1972). With respect to our sites, previous research has demonstrated that abundance of cancrids is highest near tidal channels in Willapa Bay (Rooper et al. 2002). These crabs reside in deeper channels during low tides and venture onto tideflats during high tide in search of food (Holsman et al. 2003, 2006). Holsman et al. (2006), working in Willapa Bay, observed Cancer magister (= Metacarcinus magister) commonly making forays of 0.6 km or more, but higher abundances, and thus more feeding, occurred closer to channels. In Padilla Bay, where tethered Batillaria experienced very low mortality or damage across the entire vertical gradient, cancrids are far less abundant overall than in Willapa Bay, and particularly so at higher intertidal elevations and far from channels (Dinnel et al. 1986). Yet tethering positions at the site in Padilla Bay were both deeper and closer to channels than those at the Willapa Bay site, making habitat configuration an inadequate explanation for differences in predation pressure between the sites. Predicting the influence of natural enemies for a future introduction relies on a mechanistic understanding of which species, native or non-native, are likely to impact vital rates of the invasive. Here we demonstrate that native cancrid crabs are responsible for the differential success of this species at two introduction sites, providing the first published evidence of native predation on Batillaria. Of the potential predators captured, only the vertical distribution of cancrid crabs corresponded to the rate at which snails were damaged and consumed in the tethering experiment. Based on distribution patterns, neither grapsid crabs (Hemigrapsus spp.), nor staghorn sculpin (L. armatus) are likely exerting strong predation pressure on Batillaria. The morphology and biomechanics of grapsid claws, unlike those of cancrids, are not well-suited for crushing snail prey (Yamada and Boulding 1998), and, though they could be used to peel the shell, we did not observe that many snails were killed this way. Additionally, gut content analyses have failed to detect evidence that L. armatus include Batillaria in their diet to a significant degree (McPeek et al. 2015), despite consuming other species of snail and co-occurring with high Batillaria densities in some areas (P.S. McDonald, pers. obs.). Results of the laboratory electivity experiment corroborated

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E. W. Grason et al.

patterns of size-dependent predation observed in the tethering experiment, further supporting C. magister as a predator contributing to biotic resistance to the newer population. Together with migration of infected snails to lower tidal elevations (Miura et al. 2006), the predation on small snails at low elevations in Willapa Bay explains observed patterns of increasing infection prevalence, and snail size at deeper tidal elevations, similar to observations from other systems (Byers et al. 2015a). Comparisons among other recently-established populations of Batillaria would strengthen our inference biotic resistance by cancrids, but we are aware of no published data that would enable such tests. In addition, predation rates on Batillaria in Elkhorn Slough have been observed to be temporally variable (K. Wasson, Pers. comm.), a component of predation that is untested here. Nevertheless, future risk analyses for this species could incorporate the local presence and abundance of cancrid crabs in intertidal elevations. It is generally understood that distinct processes influence success at each stage of an invasion (Williamson et al. 1996; Blackburn et al. 2011). Consistent with Colautti et al. (2006), we found that predation can be an important predictor of success at the abundance/ impact stage, determining the abundance and distribution of an invasive at a site following establishment. Our study also supports that, within a given stage of invasion (here, spread), distinct factors can influence success depending on the spatial scale considered (Theoharides and Dukes 2007). Though we have observed that predation, or lack thereof, is important at a local/site scale, the presence and high abundances of cancrid crabs across all of Washington’s shorelines does not preclude abundance and wide geographic range of Batillaria on the regional scale. Similarly, while residence time predicts size of an invader’s range on a regional scale (Byers et al. 2015b), and could be why Batillaria has not been noted beyond Oysterville in Willapa Bay, other processes can have a greater influence on distribution at the local scale, even for a species that disperses by crawling. We show that for local distribution of Batillaria within Willapa Bay, a short residence time is not as important as biotic resistance in determining the vertical intertidal range and population density. Several other possible influences on success are not addressed by this study, including competition, abiotic

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stresses, food availability and propagule pressure. In California, Batillaria outcompetes native Cerithidea californica (Byers 1999), which is not found in Washington State. Thus, the presence of a similar snail in California, albeit weakly competitive could cause differences in abundance between invasive populations of Batillaria in the two states, but not between the two sites assessed in this study. With respect to the other possible influences, over the elevation gradient and time period tested, we can only infer that abiotic stress was not associated with significant mortality rates of tethered snails relative to predation; only two of the 600 tethered snails appeared to have died without evidence of attempted predation. Our study was not designed to capture subtler effects of abiotic stressors on vital rates, such as changes in growth and reproductive rates, that might influence abundance and distribution. Third, while it seems clear that crabs prevent Batillaria from extending their distribution deeper in Willapa Bay, the possibility that food availability also limits the density and depth at which snails live remains untested. While sediment grain size and organic content—which would influence benthic diatom growth—was qualitatively similar between the two sites, further analysis would be required to rule this out as a factor influencing snail density and distribution. We would expect light limitation on growth of benthic diatoms to increase with depth and immersion time, as well as from shading by native eelgrass (Zostera marina). Observational evidence suggests that the lower limit of snails was often very close to the upper distributional limit of Z. marina in Padilla Bay, ca. 0 m MLLW (Grason unpublished data). The upper limit of Z. marina in Willapa Bay is higher (? 0.6 m MLLW, Ruesink et al. 2010), but still well below the lower limit of Batillaria distribution observed during any of the surveys reported in the present study. Thus it appears unlikely that eelgrass distribution explains differences in lower limit of Batillaria. Lastly, we have very little information from which to infer propagule pressure for each site. Over the course of the last century, Willapa Bay certainly received much greater quantities of shellfish than Padilla, but less is known about the precise origin and release points of those transfers, and thus whether they are likely to have contained Batillaria. Together our findings illustrate a scenario in which predation, rather than residence time or co-evolved

Comparing residence time and natural enemies

parasites, drives differential success of an invasive species. Concordant with previous studies, we observe that novel predators are not likely to preclude establishment at an invasion site, but they can influence local success at one or more later stages of invasion, both spread and impact (i.e. abundance) (Levine et al. 2004; Colautti et al. 2006). In many cases, biotic resistance is observed to be context dependent with implications for variability of invasion success (Kimbro et al. 2013). For instance, an estuarine gradient influences the abundance of native crabs (including Cancer productus, also in our study) that prey on invasive European green crab (Carcinus maenas), such that the invasive crab is only found in lowsalinity habitats which are more physiologically stressful for C. productus (Hunt and Yamada 2003; Jensen et al. 2007). In the San Juan Islands, the invasive clam, Nuttallia obscurata, is limited to softsubstrate habitats in which they can effectively bury to avoid predation by native C. productus (Byers 2002). Our observation that native predators can influence the success of an invader both within and across sites is consistent with these previous findings. Thus, in addition to abiotic factors typically used for invasion risk assessments, site-scale spatial variability in biotic interactions could be used to improve the resolution of invasion risk assessments. Acknowledgements The authors are very grateful for assistance provided by M. Hannam and S. Shull (GIS), J. Heckes (site access), R. Theobald (analysis), R. Davis, D. Grason, and M. Flora-Tostado (field assistance). We appreciate the efforts by E. Carrington, J. Olden, M. Hannam, K. Wasson, and two anonymous reviewers, who provided helpful suggestions for improvement of the manuscript. Students at Shannon Point Marine Center, and the University of Washington, assisted with field and laboratory data collection, particularly A. Gehman, and we thank them for their contributions. A portion of this research was conducted in the National Estuarine Research Reserve System under an award from the Estuarine Reserves Division, Office of Ocean and Coastal Resource Management, National Ocean Service, National Oceanic and Atmospheric Administration.

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