Crassostrea Gigas) Impacts on Native Periwinkles (Littorina Littorea)

Aquatic Invasions (2011) Volume 6, Issue 3: 281–290 doi: 10.3391/ai.2011.6.3.05 Open Access

Research Article

Alien epibiont (Crassostrea gigas) impacts on native periwinkles (Littorina littorea)

Nina Eschweiler* and Christian Buschbaum Alfred Wegener Institute for Polar and Marine Research, Wadden Sea Station Sylt, Hafenstrasse 43, 25992 List/Sylt, Germany E-mail: [email protected] (NE), [email protected] (CB) *Corresponding author

Received: 27 January 2011 / Accepted: 28 March 2011 / Published online: 11 May 2011

Abstract

In marine sedimentary coastal environments such as the Wadden Sea (coastal south-eastern North Sea) shells of epibenthic molluscs are the only major available settlement substrate for an increasing number of alien sessile organisms. We investigated the effects of Pacific oyster Crassostrea gigas epibionts on body weight, mobility and fecundity of the native common periwinkle Littorina littorea. Body dry weight of snails without oyster overgrowth was twice as high compared to periwinkles covered with oysters. Also crawling speed of snails with oyster epigrowth was significantly slowed down and about ten times lower than in unfouled periwinkles. Additionally, oyster epibionts caused a strong decrease in reproductive output. In laboratory experiments, egg production of fouled L. littorea was about 100-fold lower than in periwinkles free of oysters. Field surveys in different years and habitats demonstrated that up to 10% of periwinkles occurring on epibenthic bivalve beds and up to 25% of snails living on sand flats may be fouled by C. gigas. However, oysters are not the only epibionts on L. littorea in the area. In previous studies it was shown that periwinkles can also be strongly overgrown by other alien epibionts such as Australian barnacles Austrominius modestus and American slipper limpets Crepidula fornicata. These epibiotic structures may cause similar effects as revealed for C. gigas. Thus, we conclude that an alien epibiont accumulation on L. littorea may have a significant impact on periwinkle population dynamics and its ecological functions in the Wadden Sea. Key words: Littorina littorea, epibiosis, alien species, Crassostrea gigas, Wadden Sea

Introduction responsible for the largest number of associated established introductions (Wolff 2005; Haydar In recent decades, an increasing number of 2010). Apart from its own epibionts, C. gigas biological invasions have been observed in itself represents a sessile organism and its larvae Atlantic European waters due to the growing require hard substrates for settlement (Reise magnitude of global trade and associated 1998). transport vectors (Galil et al. 2009). The In the northern Wadden Sea (south-eastern predominant vectors for transportation of alien North Sea), C. gigas were first detected in the species are aquaculture, ballast water and hull field in the beginning of the 1990s (Reise 1998; fouling (Carlton 1985; Minchin and Gollasch Diederich et al. 2005), attached to shells of blue 2003). In the North Sea about the half of the mussels Mytilus edulis Linnaeus, 1758, because non-native species were introduced via hull mussel beds provided the only major hard fouling and aquaculture activities explaining the substrate available in an otherwise sedimentary high share of sessile alien macroalgae and dominated environment. In recent years, a invertebrates occurring in the area (Gollasch et dramatic increase in oyster abundance has been al. 2008). For example, Haydar (2010) identified observed (Wehrmann et al. 2000; Diederich et al. 35 species that have been introduced together 2005; Nehls and Büttger 2007; Kochmann et al. with non-native oysters to the Netherlands and 2008; Markert et al. 2010). Consequently most found a high number of epibiont species attached former mussel beds have turned into oyster reefs to the oyster shells. In particular, the imports of with high numbers of oysters on every hard Pacific oysters Crassostrea gigas (Thunberg, substrate available including shells of the 1793) since the beginning of the 1960s are gastropod Littorina littorea (Linnaeus, 1758).

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Periwinkles L. littorea may achieve high of the List basin along the east coast of the abundances of several hundred individuals per island of Sylt, including the sampled m2 in the area (Buschbaum 2000). They are Diedrichsenbank (55°2′N and 8°26′E), the important structuring elements because their bivalve bed in the Oddewatt (55°01′N and grazing activity has a strong influence on benthic 8°25′E) and Leghörn (54°57′N and 8°23′E). community composition and recruitment success of macroalgae and sessile invertebrates Pacific oyster overgrowth on Littorina littorea (Wilhelmsen and Reise 1994; Albrecht 1998; Buschbaum 2000). As L. littorea lacks anti- Live periwinkles were collected on three fouling substances (Wahl and Sönnichsen 1992) intertidal mixed beds of mussels and oysters it is a suitable hard bottom surface for many during low tide in September/October 2007, marine organisms. Previous investigations 2008 and 2010. To determine abundance of revealed that overgrowth with native organisms overgrown snails a frame (30 cm × 30 cm) was such as barnacles causes detrimental effects such randomly placed on the bottom. All periwinkles as reducing snail mobility, fecundity, growth and with and without oyster epigrowth (Figure 2) survival (Dittmann and Robles 1991; Wahl 1996, inside the frame were counted and size of snails 1997; Buschbaum and Reise 1999; Thieltges and and oysters was measured to the nearest 1mm Buschbaum 2007). Therefore, barnacle epibionts using a calliper. At each mussel bed six replicate may affect population dynamics in L. littorea samples were taken. Next to bivalve beds, and indirectly influence its ecological function in samples were also taken from an adjacent sand the Wadden Sea. An increasing number of non- flat area in September 2010. Due to lower snail native epibionts attached to periwinkles may densities, an area of 5 × 5 m was searched for intensify this effect and may cause similar periwinkles and all L. littorea with and without harmful impacts on L. littorea. Therefore, in this oyster epibionts were counted. For all study we investigated the occurrence and the investigations on oyster overgrowth only snails > effects of Pacific oyster C. gigas epibionts on the 10 mm were used. periwinkle L. littorea and hypothesized that snail mobility, body weight and reproductive output is Body weight of Littorina littorea reduced in overgrown snails. To examine soft tissue weight in periwinkles with and without oyster epibionts, we collected Methods live snails (n = 32) of the same size class (17–18 mm shell height measured from base to apex) Study area with and without oyster epigrowth in September Investigations were conducted in the intertidal 2007. After detaching oysters (mean size 3.6 ± zone of the List tidal basin (54°50′– 55°10′N and 0.4 cm) from the shells, snails were boiled in 08°20′ – 08°40′E) near the island of Sylt, located water for 2 minutes and then soft bodies were in the northern Wadden Sea (Figure 1). The List carefully removed from shells and dried for three basin captures an area of about 404 km² and is days at 70°C up to weight constancy. Weight partly enclosed in the south and north by dams. was determined to the nearest of 0.01 g. The only connection to the open North Sea is the Lister Deep, a slender tidal inflow of 2.8 km Mobility of Littorina littorea width (Reise and Riethmüller 1998). Mean water temperature is about 9°C, with a winter average To investigate the effects of oyster epigrowth on of 5°C and a summer average of 15°C. Tides are periwinkle mobility we measured crawling speed semi-diurnal and the mean tidal range is 2 m. of periwinkles i) with oyster epigrowth, ii) Average salinity is 30 PSU. More detailed without oysters and iii) with removed oysters in descriptions of geology, sediments and September 2007. Mean size of attached and hydrography of the study area are given by Reise previously removed oysters was 3.6 ± 0.5 cm. (1985), Austen (1992, 1994a, b) Bayerl and For each treatment 40 periwinkles of the same Higelke (1994), Reise et al. (1994) and Gätje and size (17 – 18 mm shell height) were used. Snails Reise (1998). A number of mixed beds of native were placed in line on a sand flat at low tide, blue mussels M. edulis and introduced Pacific each with its own numbered starting point, oyster C. gigas are situated in the intertidal zone marked with a flag with the snail code number.

282 Crassostrea gigas impacts on Littorina littorea

Figure 1. Study area in the south-eastern North Sea. Investigations and field experiments were performed on mixed beds of invasive oysters Crassostrea gigas and native blue mussels Mytilus edulis [Diedrichsenbank (DB), Oddewatt (OW), Leghörn (LH)] and sand flat regions in the Oddewatt (OW) in the List basin of the island of Sylt, 2007–2010.

After one hour crawled distance was recorded by the egg release of L. littorea i) without oyster measuring the length of the crawling track. epibionts ii) with C. gigas overgrowth iii) with In a second experiment, we analyzed the oysters removed. Mean size of attached and capability of snails to return to crawling position previously removed oysters was 3.7 ± 0.6 cm. once turned upside down in three treatments: (i) For each treatment we used six cylindrical snails with oyster epigrowth (n = 40), (ii) boxes (n=6) which were covered with a 125µm periwinkles without oysters (n = 40) and (iii) gauze to prevent losses of egg capsules. At the L. littorea of which oysters had been removed bottom the boxes were supplied with running from the shells (n = 15). Snails were placed in seawater of ambient temperature and salinity. supine position into basins, filled with a 1 cm Each box contained five females and five males. wet sediment layer, representing low tide Because of low densities of male periwinkles conditions. After one hour all snails which had covered with oysters, we used only males turned around were counted. Experiment was repeated with a new number of L. littorea of the without epibionts. Depending on the specific same size class (17–18 mm shell height) and treatment females were overgrown or free of with the same replicate number to imitate high oysters. Snail sex was determined just before the tide conditions with a 5 cm water layer. beginning of the experiment. Thalli of the green algae Ulva lactuca Linnaeus served as food for L. littorea. The experiment lasted 12 days. Daily, Egg production of Littorina littorea the content of each box was filtered through a Periwinkle reproductive output with and without 125µm sieve. Snails and algae were carefully oyster epibionts was investigated with a method washed and transferred back into the boxes. similar to that described in Buschbaum and Reise Retained egg capsules per box were counted. For (1999) (Figure 3) in May 2009. We determined further details see Buschbaum and Reise (1999).

283 N. Eschweiler and C. Buschbaum

Figure 2. Periwinkle Littorina littorea with Crassostrea gigas (left) and without oyster epigrowth (right). Photo by N. Eschweiler.

Figure 3 Schematic drawing of the experimental set-up to investigate egg production of Littorina littorea with and without oyster overgrowth and periwinkles from which oysters were removed.

following Wilcoxon´s matched pairs signed rank Statistical analyses test. Comparisons between abundances of periwinkles were tested by using a Mann- Results are presented as arithmetic means ± Whitney U–test, comparisons between standard deviation. Differences in body dry abundances of fouled and uncovered periwinkles weight were analyzed by Mann-Whitney U–test. were tested using Kruskal-Wallis ANOVA Chi-Square-test was used to analyse differences followed by the Dunn´s method for unequal in snail ability to return to normal crawling treatment group sizes. If P < 0.05 effects were position. Crawling speed and egg production in considered to be statistically significant. All periwinkles with and without oyster epibionts computer analyses were carried out with the were verified using Kruskal-Wallis H–test, software package SigmaStat 3.5 by Statcon.

284 Crassostrea gigas impacts on Littorina littorea

Figure 4. Mean abundance of Littorina littorea (± sd) with (black bars) and without Pacific oyster epigrowth (grey bars) on mixed beds of mussels and oysters and on a sand flat area in different years. Mean percentage of snails overgrown with oysters are diagrammed via black dots (± sd).

Table 1. Mean abundance (±sd) of Littorina littorea on mixed mussel/oyster beds in August 2007, September 2008 and September 2010 (average over three different beds) and mean abundance (±sd) of periwinkles on a sandflat area in September 2010.

Snails > 10mm/m² 2007 mixed bed 2008 mixed bed 2010 mixed bed 2010 sandflat total 212.17 (176.21) 219.35 (81.11) 440.12 (168.76) 15.35 (5.91) overgrown 2.83 (5.72) 20.00 (12.30) 23.46 (29.98) 3.61 (1.51) % overgrown 3.08 (6.03) 11.14 (9.07) 7.33 (9.85) 24.42 (7.81)

Results Body weight and mobility of Littorina littorea Abundance of Littorina littorea and oyster with and without oyster epigrowth epigrowth Tissue dry weight in uncovered snails (0.14 g ± Abundance of snails on mixed mussel/oyster 0.17 g/snail) was significantly higher than in beds was 212.17 ± 176.21 ind./m² in 2007 and L. littorea with oyster fouling (0.06 g ± 0.02 219.35 ± 81.11 ind./m² in 2008 with no g/snail) (Mann-Whitney U-test, P < 0.001). significant difference (Mann-Whitney U–test, p Crawling speed of periwinkles differed = 0.1). In 2010 density (440.12 ± 168.76 ind./m²) significantly between the three treatments was twice as high as in previous years and (Kruskal-Wallis H–test, p < 0.001) (Figure 5A). significantly different (Mann-Whitney U–test, It was lowest in snails with oysters (6.2 ± 2.5cm (2007) p < 0.001), (2008), p < 0.001) (Table 1, h‾¹) and significantly different from periwinkles Figure 4). Abundance of snails overgrown with free of oysters (96.6 ± 73.0 cm h‾1, Wilcoxon´s oysters, by contrast, increased significantly from matched pairs signed rank test, p < 0.001) and 2007 (3.08 ± 6.03%) to 2008 (11.14 ± 9.07%) conspecifics from which oysters were removed (Tukey`s test, p < 0.05) but decreased in 2010 (62.5 ± 58.6 cm h‾1, Wilcoxon´s matched pairs (7.33 ± 9.85%). In comparison to mixed signed rank test, p < 0.01). There was also an mussel/oyster beds, sand flat areas revealed a apparent difference in crawling speed between significantly higher mean percentage of fouled periwinkles without oysters and snails with snails (mixed beds: 6.29 ± 8.62%, sand flat: removed epigrowth, however, it was not 24.42 ± 7.81%) (Kruskal-Wallis ANOVA, statistically significant (Wilcoxon´s matched Dunn´s-method, p < 0.001). pairs signed rank test, p = 0.0736, n = 15).

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Ability to return to crawling position also differed significantly between the treatments. At low tide situation 42.5 % of snails without oyster epigrowth returned while none of the L. littorea with oyster cover (Chi-Square-test, p < 0.001) and only 13.3% of periwinkles from which oysters were removed (Chi-Square-test, p < 0.05) were observed at crawling position after one hour experimental period (Figure 5B). There was a significant difference in the number of snails which turned over between fouled and cleaned individuals as well (Chi-Square-test, p < 0.05). At submersed conditions we observed the same pattern with most unfouled periwinkles being able to return to crawling position (45%) (Figure 5C). Ability was significantly lower in overgrown snails (2.5 %, Chi-Square-test, p < 0.001) and in periwinkles from which oysters were removed (13.3%, Chi-Square-test, p < 0.05). The difference between fouled periwinkles and snails with removed oysters was not significantly different (Chi-Square-test, p > 0.05).

Reproduction of Littorina littorea There was a significant difference of mean egg production between the treatments (Kruskal- Wallis H-test, p < 0.001) (Figure 6). Snails without oyster epigrowth (109 ± 83 eggs day‾1 1 female ‾ ) released significantly more eggs than Figure 5. Mean crawling speed (± sd) of Littorina littorea fouled snails (1 ± 2 eggs day‾1 female ‾1) and at low tide (A) and percentage of Littorina littorea, which periwinkles from which oysters were removed (2 turned from upside down to normal crawling position within 1 1 one hour at low tide (B) and high tide simulation (C), with ± 2 eggs day‾ female ‾ ) (Wilcoxon´s matched and without oyster cover and with removed oysters in pairs signed rank test, p < 0.01). Fouled summer 2007. L. littorea and snails with removed epigrowth showed no significant difference in egg production (Wilcoxon´s matched pairs signed rank test, p > 0.05).

Discussion Effects of oyster epigrowth There are a number of detrimental effects on Littorina littorea, caused by epibionts. In the present case, oysters considerably impaired snail mobility. Crawling was either extensively slowed down or considered impossible, as was the capability to return to normal position once turned upside down. Crawling is an essential requirement for food ingestion, as L. littorea grazes on diatoms, germlings, ephemeral Figure 6. Mean egg production per day and female (± sd) of Littorina littorea with and without oyster cover and with macroalgae and small invertebrates such as removed oysters in a ten day experiment in summer 2008. juvenile barnacles by bulldozing and crawling (Lubchenco 1978; Denley and Underwood 1979;

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Hawkins 1983; Petraitis 1983; Farrell 1988; snails due to their heavy load. Thus, every Wilhelmsen and Reise 1994; Fenske 1997; overgrown L. littorea is strongly impacted after a Albrecht 1998; Buschbaum 2000). Often short period of time, which, in many cases, will periwinkles are naturally dislodged by wave and end in the death of the snail. currents and may be positioned upside down in unfavorable habitats. This is especially true for Increasing alien epibionts overgrown snails that are subjected to increased drag (Witman and Suchanek 1984; Wahl 1996, Oyster density continues to increase in the 1997). In that case returning to crawling position Wadden Sea (Nehls et al. 2009) and although is necessary for normal feeding and for returning percentage of fouled snails on mixed beds of to preferred habitats, activities which are blue mussels and Pacific oysters showed strongly hampered by a heavy epibiotic load. fluctuations over the last four years, a trend The consequence of a reduced food intake in could be observed towards an increasing amount snails with attached epibionts is a decline in of oyster fouling on periwinkles. As indicated in tissue weight (Wahl 1996, 1997) followed by a this study, up to 10 % of snails on mixed bivalve reduced overall fitness (Chan and Chan 2005), beds and up to 25 % of snails on sandflats were which may result in lower reproduction rates. In covered with oysters. On sandflat areas, drift of our experiment, egg production of periwinkles snails with and without oyster cover by waves ceased almost entirely when overgrown with did not differ and was even significantly lower oysters, what was also true for the treatment in for infested periwinkles when placed in an area which oysters had been previously removed. with comparatively high current velocities Buschbaum and Reise (1999) suggest that a (Eschweiler, unpublished data). Nevertheless, reduced general fitness of snails with epibionts dislodgment of fouled snails from mixed beds to and a disability in copulation by the voluminous sandflats may be an explanation for the higher epigrowth may be responsible for reduced egg amount of oyster covered snails on sandflat production in overgrown L. littorea. This study areas, as they would be unable to crawl back to revealed the same effects, but additionally the shellfish bed. If dislodged by waves above or showed, that even oyster cover solely on female below their preferred habitat, L. littorea could be snails suffices to constrain copulation, as male observed to return to that habitat (Alexander periwinkles were not fouled in our experiments. 1960; Gendron 1977; Petraitis 1982). Two other Therefore, gonadal analyses of fouled snails are factors may also be responsible for the recommended for further studies. It may be differences in distribution. (i) On sand flat areas, assumed that the oysters attached to the snails in where no other hard substrate is available, our experimental treatment preyed on released periwinkle shells are a proper settlement surface egg capsules. However, egg production of for oyster larvae. (ii) The high abundance of periwinkles from which oysters were removed L. littorea on mixed beds of mussel and oysters before the experiment had started hardly ever results in a high mutual grazing pressure, as they differed from the number of released eggs of are crawling over each other, simultaneously overgrown snails, indicating a reduced overall bulldozing and grazing and disengaging fitness followed by a decline in gonad themselves from sessile organisms such as oyster development and low egg production of larvae (Lubchenco 1978; Wahl and Sönnichsen L. littorea with oyster epigrowth. As Buschbaum 1992; Albrecht 1998). In general, oyster fouling and Reise (1999) previously showed, barnacle on snails is not very high. Could oyster epibionts cover [Balanus crenatus (Bruguière, 1789)] on still be able to impair not only the activity of a periwinkle shells, which was removed before the single individual but also of entire benthic egg production measurements, did not negatively communities? Certainly, oyster cover alone is affect reproductive output of periwinkles. not sufficient to affect the entire periwinkle However, the weight of one oyster is apparently population dynamics and ecological functions. much higher than that of a multitude of However, oyster densities may still increase barnacles, and may, therefore, cause a higher and many other sessile alien species have been energy loss in L. littorea. Additionally, Pacific introduced into the Wadden Sea (Reise et al. oysters are fast growing organisms reaching a 1999). For example, the American slipper limpet size of about 50-80 mm shell length after two Crepidula fornicata (Linnaeus, 1758) was first years (Reise 1998), with the capacity, to almost observed at the island of Sylt in 1934 and stop any movement and reproductive success of nowadays it occurs on almost all mixed bivalve

287 N. Eschweiler and C. Buschbaum beds. The Australian barnacle Astrominius to mortality, caused by high epibiotic load on modestus (Darwin, 1854), formerly known as L. littorea in the subtidal area. The recent Elminius modestus (Buckeridge and Newman increase of Pacific oysters is also responsible for 2010), has been introduced in 1955 and shows a intertidal snails now being exposed to high strong increase in the last decade, with numbers epibiotic loads. Additionally, other non- dominating over the native barnacles indigenous epibiotic species successfully [Semibalanus balanoides (Linnaeus, 1767) and established in the Wadden Sea, are facilitated by Balanus crenatus]. Presumably, both species rising temperatures, and we assume that this profit from increasing water temperatures and process will continue. Although no profound milder winters in the southern North Sea, detrimental effect could be observed on the resulting in increasing abundances and higher periwinkle population so far, it seems to be only occurrence of epibionts on L. littorea in the a question of time until the combination of a Wadden Sea in recent years (Harms 1999; multitude of epibiotic alien species might Franke and Gutow 2004; Wiltshire and Manly strongly impair periwinkle population dynamics 2004; Reichert and Buchholz 2006; Witte et al. and consequently its ecological function in the 2010). Wadden Sea. Second to oysters, A. modestus especially shows highest occurrence on bivalve and Acknowledgements periwinkle shells (Witte et al. 2010) and may cause similar detrimental impacts as revealed for We are deeply grateful to Sonja Endres and Kathrin native barnacles B. crenatus (Buschbaum and Ackermann for essential help with field and lab experiments. We thank Caroline Eschweiler for help with Reise 1999) and alien oysters C. gigas. graphical design and Eric Fee for proof reading of earlier Slipper limpet overgrowth causes increasing versions of the manuscript. Two anonymous reviewers gave byssus thread production in blue mussels valuable comments on the manuscript. Christian Buschbaum M. edulis. The required energy lacks for other and Nina Eschweiler were financed by the Alfred Wegener processes such as growth and reproduction Institute for Polar and Marine Research. (Thieltges and Buschbaum 2007). A similar effect of overgrowth by the slipper limpet could References be expected for periwinkles fitness, as C. fornicata was also detected in high Alexander DG (1960) Directional movements of the abundances on shells of L. littorea (pers. obs.). intertidal snail, Littorina littorea. Biological Bulletin 119: 301–302 Each mentioned epibiont has an influence on Albrecht AS (1998) Soft bottom versus hard rock: the snail as an individual and may implicate Community ecology of macroalgae on intertidal mussel appreciable diseases in its living conditions. beds in the Wadden Sea. Journal of Experimental Although one alien sessile species alone might Marine Biology and Ecology 229: 85–109, doi:10.1016/ S0022-0981(98)00044-6 not cause a profound effect on the entire Austen I (1992) Geologisch-sedimentologische Kartierung periwinkle population, the sum of all alien des Königshafens (List/Sylt). Meyniana 44: 45–52 epibionts together might tip the balance towards Austen G (1994a) Hydrodynamics and particulate matter extensive changes in population dynamics and budget of Königshafen, southeastern North Sea. Helgoländer Meeresuntersuchungen 48: 183–200, subsequently influence benthic community doi:10.1007/BF02367035 structures. Austen I (1994b) The surficial sediments of Königshafen variations over the last past 50 years. Helgoländer Meeresuntersuchungen 48: 163–171, doi:10.1007/BF0236 Conclusion 7033 Bayerl KA, Higelke B (1994) The development of northern Sylt during the latest Holocene. Helgoländer Epibionts in general strongly decrease Meeresuntersuchungen 48: 145–162, doi:10.1007/BF023 reproductive output and hamper snail mobility, 67032 Buckeridge JS, Newman WA (2010) A review of the which results in reduced body weight of subfamily Elminiinae (Cirripedia: Thoracica: Littorina littorea. Austrobalanidae), including a new genus, Protelminius Periwinkles predominantly occur in the nov., from the Oligocene of New Zealand. Zootaxa intertidal zone of the Wadden Sea, whereas 2349: 39–54 Buhs F, Reise K (1997) Epibenthix fauna dredged from tidal compara-tively low snail densities were observed channels in the Wadden Sea of Schleswig-Holstein: in the adjacent subtidal zone (Buhs and Reise spatial patterns and a long-term decline. Helgoländer 1997; Saier 2000). Buschbaum and Reise (1999) Meeresuntersuchungen 51: 343–359, doi:10.1007/BF02 to some extent attributed this distribution pattern 908719

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