Predicting the impacts of Carcinus maenas predation on cultivated Mytilus edulis beds.
Article Type: Report
Subject: Crabs (Behavior)
Fishery management (Methods)
Invasive species (Behavior)
Predation (Biology)
Authors: Murray, L.G.
Seed, R.
Jones, T.
Pub Date: 12/01/2007
Publication: Name: Journal of Shellfish Research Publisher: National Shellfisheries Association, Inc. Audience: Academic Format: Magazine/Journal Subject: Biological sciences; Zoology and wildlife conservation Copyright: COPYRIGHT 2007 National Shellfisheries Association, Inc. ISSN: 0730-8000
Issue: Date: Dec, 2007 Source Volume: 26 Source Issue: 4
Topic: Computer Subject: Company growth
Product: Product Code: 0913040 Crabs; 9108581 Fisheries Management Programs NAICS Code: 114112 Shellfish Fishing; 92614 Regulation of Agricultural Marketing and Commodities SIC Code: 0913 Shellfish
Geographic: Geographic Scope: United Kingdom Geographic Code: 4EUUK United Kingdom
Accession Number: 195918068
Full Text: ABSTRACT Cultivated mussels may be subjected to heavy predation by several predators including the shore crab Carcinus maenas, and crab predation can result in substantial losses from commercial fisheries. In the present study methods were developed to quantify the effects of crab predation on mussel beds, with the aim of estimating losses of mussels to crabs in the mussel fishery located in the Menai Strait, United Kingdom. There were significant linear relationships between crab carapace width and the number and size of mussels consumed. Increases in the mean length of mussels presented to crabs resulted in an exponential decline in the number of mussels consumed. Consequently, there was a similar decline in the predicted losses of mussels during the cultivation process as mussels increased in body size. It was estimated that C. maenas consumed 10% of seed mussels laid in the Menai Strait during their growth to a marketable size. Although crab abundance and size, and seawater temperature substantially influenced the number of mussels eaten, the size of mussels was by far the dominant factor in determining losses. Therefore, efforts to control crab predation should focus on the early stages of the cultivation process and on areas where the smaller, more vulnerable, mussels are present. The coefficients and formulae presented here could be applied to other areas of Mytilus edulis cultivation subject to predation by C. maenas.

KEY WORDS: aquaculture, crabs, mussels, prey selection

INTRODUCTION

Of the 2.05 million tons of marine molluscs harvested worldwide in 2004, the blue mussel Mytilus edulis (Linnaeus) represented 50% of the catch, accounting for 6% of all aquaculture production (FAO 2006). Mussel cultivation may occur either on-bottom, where mussels are cultivated on the seabed, or off-bottom, where mussels are suspended in the water-column, usually on topes hanging from rafts. On-bottom cultivation involves growing mussels from seed of approximately 20 mm in shell length to a marketable size of approximately 50 mm, a process taking around 2.5 y. During this time mussels may be subject to heavy mortality, particularly from predators such as the shore crab Carcinus maenas (Linnaeus), the common starfish Asterias rubens (Linnaeus), the dogwhelk Nucella lapillus (Linnaeus), and many bird species including gulls, diving ducks, and waders (see Seed & Suchanek 1992 and references therein).

As an invasive species in many parts of the world, C. maenas is considered detrimental to molluscan (Walton et al. 2002, Miron et al. 2005) and crustacean (Rossong et al. 2006, Williams et al. 2006) fisheries. Yields of seed mussels may be increased 8-fold when protected from C. maenas predation (Davies et al. 1980). Carcinus maenas migrates with the tide during the spring and summer months (Hunter & Naylor 1993); it is thus found in the intertidal and shallow subtidal zones and has a preferred salinity range of around 20-40 (Thomas et al. 1981, Ameyaw-Akumfi & Naylor 1987, McGaw & Naylor 1992). The diet of C. maenas is dependent on the availability of prey. Ropes (1968) and Elner (1981) found bivalves to be the predominant items in the diet, whereas Brousseau & Baglivo (2005) found that mussels were always the preferred prey of the Asian shore crab Hemigrapsus sanguineus (De Haan). Moreover, juvenile and adult C. maenas and Cancer pagurus (Linnaeus) selected M. edulis more frequently than the oysters Crassostrea gigas (Thunberg) and Ostrea edulis (Linnaeus), whereas the cockle Cerastoderma edule (Linnaeus) was selected in similar numbers to M. edulis (Mascaro & Seed 2000, Mascaro & Seed 2001). Although cultivated mussel assemblages may be rich in associated species, mussels far exceed any other organism in abundance and biomass (Murray et al. 2007); mussels are thus likely to be the main food source for C. maenas on commercially exploited beds.

Prey selection by predators may vary as a result of preference for a particular prey item (Jackson & Underwood 2007), the way prey items are presented (Burch & Seed 2000), the physiology of either the predator (Kaiser et al. 1990, Reid et al. 1997) or prey (Arnold 1984, Cote 1995, Leonard et al. 1999), and different environmental conditions, including temperature. Acclimatization to different temperatures caused food consumption rates to increase by 2.4 times in C. maenas acclimated at 24[degrees]C compared with crabs acclimated at 10[degrees]C (Wallace 1973). However, Elner (1980) did not find any significant effects of temperature, between 10[degrees]C and 17[degrees]C, on feeding rates or prey size selection in C. maenas feeding on M. edulis.

The present study is based on mussel cultivation sites in the Menai Strait, North Wales, United Kingdom. The aim of the study is to develop methods to estimate losses of mussels attributable to crab predation throughout the period of cultivation. Field observations established the growth rate of mussels and abundance of crabs during the period between laying seed and the harvesting of mussels of marketable size (2-3 y). Laboratory experiments were conducted to determine the effects of varying prey presentation and predator and prey size using a single predator species (C. maenas) and prey species (M. edulis).

MATERIALS AND METHODS

General Methodology

Mussel cultivation in the Menai Strait follows a regular timetable under which seed mussels are imported annually during July and August, the exact timing depending on when natural stocks of newly settled mussels are located. These seed mussels are laid in the intertidal zone, where they are left to grow for approximately 2 y. The two-year-old mussels are then moved to the subtidal zone for a final period of more rapid growth for 6-12 mo. Mussels are harvested from October to March after between 28 and 33 mo of growth. To determine the growth of mussels during the cultivation process, mussels were collected from 3 cohorts, each representing a distinct year class of mussels, at sites 11, 12, and S1-3 (Fig. 1) from September 2005 to March 2007. Five 10-cm diameter cores of mussels were collected from the lower and upper limits of the intertidal mussel beds every three months. Subtidal mussels were collected haphazardly from commercial dredges. All mussels were measured along the antero-posterior axis to 0.1 mm.

All Carcinus maenas used in the current study were collected from the cultivated mussel beds in the Menai Strait, either by dredging or using baited traps, and only undamaged crabs were used in the feeding experiments. Crabs were fed to satiation on mussel flesh; food was then withheld for 48 h before feeding trials began to standardize hunger levels (Elner & Hughes 1978, Jubb et al. 1983) and allow a period for crabs to acclimatize. Crabs were kept individually in running seawater at 12 [+ or -] 1[degrees]C unless otherwise stated. In each experiment mussels were presented in sufficient quantities, based on pilot experiments, to prevent any one size class being eaten out during a feeding trial. Any fouling organisms were removed from the mussels, although numbers of fouling organisms were low. Crabs were kept in complete darkness while feeding to prevent disturbance; furthermore, C. maenas is not a visual predator (Crothers 1968, Ameyaw-Akumfi & Hughes 1987). One hundred mussels collected from the cultivated beds in the Menai Strait covering a size range of 15-60 mm were used to estimate the dry flesh biomass consumed ([C.sub.b]) in the feeding experiments based on the regression of length against dry flesh weight. Mussels were dried at 60[degrees]C until constant weight was reached (~48 h). The relationship between length and total wet weight was used to estimate the weight of mussels lost during the cultivation process.

[FIGURE 1 OMITTED]

Crab Population

To establish the abundance and size of C. maenas on the cultivated mussel beds in the Menai Strait, still images were extracted from video recordings of the seabed. A Mobitronic RV-2 Marine underwater camera was mounted on a steel frame at a height of 55 cm, giving a 50 cm [x] 50 cm field of view. The video images were recorded onto mini DV tape via an A/V cable using a Canon MV850i camcorder. Three sites on the subtidal mussel beds and three on intertidal mussel beds, together with three sites without mussels were identified (Fig. 1). Sampling was conducted during the 2 h before high water during tides intermediate between neaps and springs once per month from April 2006 to March 2007. Sites were located using a handheld GPS receiver. Seabed images were recorded by lowering the camera frame from a boat onto the seabed and lifting and relowering it at intervals as the boat drifted with the tide. Transects of ~100 m were recorded and 20 images extracted at random from the video. Still images were extracted using Video2Photo software. Image J software was used to enhance and analyze the images. Mussel coverage and crab abundance were recorded, and the CW of crabs measured using Image J. During the winter, from November until February, visibility on the subtidal mussel beds was poor because of a combination of high turbidity and low light levels. Crab abundance was estimated during these months by collecting samples from commercial mussel dredging vessels. Start and finish points of trawls (~250-1000 m) were recorded using a GPS receiver. Dredges were emptied into hoppers before mussels and crabs were passed up a conveyor belt where all visible crabs were removed, counted, and measured. Six trawls were conducted each month from October 2006 to March 2007. During October, abundance as measured by dredging was compared with abundance measured using the video system. The size-frequency distributions of crabs were predicted based on the mean and standard deviations of the CW width of crabs measured, assuming normal distribution.

Feeding Rates, Size and Prey Selection

Feeding rates of C. maenas were measured after 2, 4, 8, 12, 16, and 20 h and then daily for 6 days. A total of 12 male crabs of 60-75 mm carapace width (CW) were each presented with 45 mussels comprising 9 mussels in each of five length classes, which were: 20-22.4, 22.5 24.9, 25-27.4, 27.5-29.9, and 30-32.4 mm covering the range of mussel sizes commonly found on the intertidal beds. The number of mussels eaten ([C.sub.e]) or damaged in each size class were recorded and replaced every 24 h.

To determine the difference in prey size selection and consumption rates by crabs of different CW, 21 male crabs ranging from 22.2 mm to 68.3 mm CW were each presented with 42 mussels, consisting of seven mussels in each of six size classes which were: 17.5-19.9, 20-22.4, 22.5-24.9, 25-27.4, 27.5-29.9, and 30-32.4 mm. The number of mussels eaten from each size class was recorded after 8 h. Ali eaten or damaged mussels were then replaced. After a further 24 h the number of mussels eaten from each size class was again recorded.

To determine the difference in prey selection caused by changing the mussel sizes presented to C. maenas, 10 male crabs ranging from 58-60 mm CW were presented with 42 mussels in seven length classes. Mussels were presented in the proportions 3, 5, 8, 10, 8, 5, and 3, whereas the modal mussel length class presented to each crab was different, with length class midpoints ranging from 21.25 mm to 43.75 mm. At each of the four smallest size ranges, an additional four crabs were presented with mussels. The length distributions of mussels presented approximated the distributions of mussels on cultivated beds in the Menai Strait and covered the size range of mussels found during most of the cultivation process. The number of mussels consumed from each size class was noted after 24 h.

The effects of temperature on feeding rates was determined using a total of 18 male C. maenas of 60-70 mm CW kept at 6[degrees]C, 8[degrees]C, 10[degrees]C, 13[degrees]C, 16[degrees]C, and 18[degrees]C, with three crabs at each temperature. Each crab was presented with 35 mussels of 20-30 mm length. The number of mussels consumed by each crab was recorded after 24 h.

RESULTS

Crab Population

The mean number ([+ or -]1 S.E.) of C. maenas per hectare measured by dredging (n = 6) in the subtidal zone ranged from 1-949 [+ or -] 393 crabs [ha.sup.-1] (0.19 [+ or -] 0.04 crabs [m.sup.-2]) in October to 324 [+ or -] 37 crabs [ha.sup.-1] (0.03 [+ or -] 0.004 crabs [m.sup.-2]) in March. The mean number of crabs recorded in the video survey of the subtidal mussel beds one week before dredge sampling was 3,400 [+ or -] 1,410 crabs [ha.sup.-1] (0.34 [+ or -] 0.14 crabs [m.sup.-2]) and one week after dredge sampling in October 2006 was 2,536 [+ or -] 1,239 crabs [ha.sup.-1] (0.25 [+ or -] 0.12 crabs [m-.sup.-2]). Both intertidal and subtidal video surveys showed a decline in abundance between September and October; thus it was estimated that dredging underestimated crab abundance by 33% and abundance estimates were increased by a factor of 1.5 accordingly. The number of crabs on the intertidal mussel beds, and overall, peaked during July (Fig. 2a). There was an approximate inverse relationship between the number of crabs recorded in the intertidal and subtidal zones during the spring and summer months (Fig. 2b) reflecting tidal migration by C. maenas. There was a slight decrease in mean CW during July, probably because of the crabs imported along with seed mussels during this month. Overall, numbers of crabs decreased from July to December (Fig. 2c). No crabs were recorded on intertidal mussel beds from December to February and numbers remained steady in the subtidal zone during these months. During March, numbers of crabs increased sharply in the intertidal zone. Excluding the decrease in mean CW recorded during July, mean CW remained between 40 and 50 mm on both intertidal and subtidal beds. Crabs were absent from the sites without mussels during the spring, bur as total numbers increased crabs were found at N1 and N2 (Table 1). Site 12 had the highest abundance of crabs during any time of the year (13,846 crabs [ha.sup.-1] or 1.4 [m.sup.-2]), although sites I1 and S2 also exhibited abundances >10,000 crabs [ha.sup.-1] (>1 [m.sup.-2]) during the summer, and there were numbers in excess of 10,000 crabs [ha.sup.-1] at S3 during the fall.

[FIGURE 2 OMITTED]

Feeding Rates, Size, and Prey Selection

There was a significant correlation between time and the feeding rate of C. maenas ([F.sub.1,10] = 8,860.13, [R.sup.2] = 0.999, P < 0.0001). There was a sharp decline in feeding rates during the first 24 h after crabs had been presented with prey; feeding rates then leveled out (Fig. 3). Feeding rates of C. maenas during the first 2 h after being presented with mussels were almost 8 times greater than after 6 days. The mean number of mussels eaten per hour during the first 24 h of feeding was ~2 compared with ~1 after 48 h and <1 beyond 48 h.

There was a significant correlation between CW and the mean length of mussels consumed (Fig. 4). Residuals were normally distributed (K-S statistic = 0.103, P = 0.994) and variances were equal (P = 0.174). There was a weaker, but significant, correlation between CW and modal length consumed (y = 0.346x + 3.272, [R.sup.2] = 0.418). The smallest crab to consume any mussels had a CW of 34 mm. Crabs down to 22 mm CW were presented with mussels as small as 17.5 mm in length bur failed to eat.

Residuals of CW against [C.sub.e] regressions were normally distributed (K-S statistic <0.143, P > 0.848) and variances were equal (P > 0.207) There were significant linear correlations between CW and [C.sub.e] (Fig. 5a) and significant exponential correlations between CW and [C.sub.b] after 8 and 24 h (Fig. 5b). On average, only four mussels extra were consumed over 24 h compared with 8 h (Fig. 5a) reflecting the decline in feeding rates over time (Fig. 3). The slope of the relationship between CW and Co did not differ significantly between 8 and 24 h (ANCOVA, [F.sub.1,27] = 0.15, P = 0.706).

[FIGURE 3 OMITTED]

[FIGURE 4 OMITTED]

There was a highly significant negative exponential correlation between the mean length of mussels (MML) presented to crabs and [C.sub.e] (Fig. 6a). Residuals were normally distributed (K-S statistic = 0.313, P = 0.233) and variances were not significantly different (P = 0.127). [C.sub.e] decreased from a maximum of 29 at a MML of 21.25 mm to 1 at a MML of 36.75-43.75 mm. MML and [C.sub.b] were related by a cubic function (Fig. 6b). Residuals were normally distributed (K-S statistic = 0.253, P = 0.481) and variances were not significantly different (P 0.089). [C.sub.b] was greatest when crabs were presented with a MML of 21.25 mm. From 23.75 mm to 36.25 mm [C.sub.b] was lower, whereas above 36.25 mm [C.sub.b] increased as larger mussels were consumed.

Mussels from the most abundant size class presented to the crabs were consumed in the greatest numbers (Fig. 7a and b). The mean and modal length of mussels predicted to be consumed (Fig. 4) was 24 mm. When the MML presented was only slightly greater (26.25 mm; Figure 7c) mussels were still consumed predominantly from the most abundant size class. Once MML was increased beyond this value, to 28.75 mm, more mussels were consumed from the 25-27.5-mm size class, rather than the most abundant size class (Fig. 7d). As MML is increased further mussels are still selected from the smaller size classes until only a single mussel is consumed at the largest mussel sizes presented (Fig. 6a).

Predicting Prey Consumption

The number of mussels predicted to be eaten ([z.sub.e]; Fig. 8a) based on the relationships between CW and [C.sub.e], and MML and [C.sub.e] was calculated using the following equation:

[Z.sub.e] = ([y.sub.0] + [ae.sup.(-by)]) + [a.sub.c]x

where x = CW, and y = MML. The constant [a.sub.c] (0.539) is the slope of the regression line describing the relationship between CW and [C.sub.e] (averaged for 8 and 24 h feeding periods). The number of mussels consumed by crabs from 35-70 mm was predicted based on the curve (y = [ae.sup.-bx]) describing the relationship between MML and [C.sub.e], obtained from crabs of 60 mm CW (Fig. 6a). These values were adjusted by (CW-60)[a.sub.c] to account for differences in the CW of crabs, giving constants: [y.sub.0] = -32.3459, a (MML vs. CW constant) = 1517.8 and b = 0.18, which represent the theoretical relationship between MML and [C.sub.e] at = 0.

[FIGURE 5 OMITTED]

[FIGURE 6 OMITTED]

Over 24 h, [z.sub.e] ranged from 0-37 (Fig. 8a). The estimated number of mussels consumed by a crab of 70 mm CW was ~37 when presented with a MML of 21.25 mm, decreasing to ~6 when presented with a MML of 43.75 mm; for a crab of 35 mm the estimated number of mussels consumed ranged from 0 when presented with a MML >26.25 mm to ~16 when presented with a MML of 21.25 mm.

[FIGURE 7 OMITTED]

[FIGURE 8 OMITTED]

The predicted biomass consumed ([z.sub.b]) was calculated in a similar manner to [z.sub.e], using the exponential and three-parameter polynomial functions relating CW and [C.sub.b], and MML and [C.sub.b], respectively. Thus:

[MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII]

where, x = CW; y = MML; [a.sub.c] = CW v. [C.sub.b] constant (0.0791); a = 3.31204 x [10.sup.-6]; b = 3.03206 x [10.sup.-4]; c = 8.61571 x [10.sup.-3]; and [y.sub.0] = -0.07048.

The estimated biomass consumed by C. maenas individuals of 70 mm CW ranged from 0.88-1.90 g DFW [d.sup.-1] (Fig. 8b). For individuals of 35 mm CW, the biomass consumed ranged from 0-0.12 g DFW [d.sup.-1]. The biomass consumed by the largest crabs (70 mm CW) was greatest for small mussels (21.25-36.25 mm MML) and larger mussels (41.25-43.75 mm MML). Mussels between 36.25 and 41.25 mm MML yielded the least biomass for large crabs. Small crabs (35 mm) were only able to eat mussels <26.25 mm in length, consuming 0.1 g DFW [d.sup.-1].

There was a significant quadratic correlation between seawater temperature and the number of mussels eaten (Fig. 9). Residuals were normally distributed (K-S statistic = 0.151, P = 0.771) and variances were equal (P = 0.85). The number of mussels eaten was 6 times greater at 13[degrees]C than at 6[degrees]C. There was a decrease in the number of mussels eaten above 13[degrees]C, falling to a similar level at 18[degrees]C as was found at 9[degrees]C.

The mean height of the intertidal mussel beds in the Menai Strait above Chart Datum (Lowest Astronomical Tide) is 2.1 m (Admiralty 2004). Consequently, they are immersed, on average, for 79% of the time. Predicted losses of mussels to crabs were reduced accordingly, assuming the abundance of crabs recorded in the intertidal zone remained constant during this time. There was an exponential decline in the number of mussels consumed by C. maenas during the cultivation process (Fig. 10), reflecting the decrease in numbers eaten with mussel size (see Fig. 6a). Mussel losses decrease from 47,000-65,000 [ha.sup.-1] [d.sup.-1] (5-7 [m.sup.-2] [d.sup.-1]) during the first two months of growth to only 14 [ha.sup.-1] [d.sup.-1] (~1 mussel 700[m.sup.-2] [d.sup.-1]) in the final month of harvesting, when mussels are available only to crabs >60 mm CW. Peaks in predation occur in March and September because of increases in crab abundance and CW (Fig. 2) but mussel growth is the dominant factor in reducing losses, as mussels increase from <20 mm to >50 mm in length during their 2.5-3 y of growth. Total mussel losses caused by C. maenas predation throughout the cultivation process amount to 9.648 [x] [10.sup.6] mussels [ha.sup.-1], or 550 kg [ha.sup.-1] during the 33 mo between seeding and harvesting, equivalent to 168.06 tons final weight and 9.5% of the seed mussels laid. The weight of mussels consumed ranged from 52 kg [ha.sup.-1] [d.sup.-1] during August of the first year of cultivation, when mussels are much smaller, to only 0.2 kg [ha.sup.-1] [d.sup.-1] after 33 mo (Table 2).

[FIGURE 9 OMITTED]

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DISCUSSION

Carcinus maenas generally selects smaller sized prey items (<25 mm) in preference to larger prey items (Seed 1980, Sanchez-Salazar et al. 1987b, Walton et al. 2002, Floyd & Williams 2004), but will eat larger prey, and will also select mussels in preference to other molluscan prey (Miron et al. 2005). Mussels are therefore vulnerable to crabs at all stages of the cultivation process. However, mussels may attain refuge on the upper shore, where predator numbers are lower, or in the lower shore and subtidal zones where more rapid growth rates quickly lead to larger body size (Seed 1980). Seasonal migration of C. maenas into deeper water means that intertidal prey species may also attain refuge from crab predation for several months of the year (Sanchez-Salazar et al. 1987b).

Gascoigne et al. (2005) recorded low C. maenas abundances in the Menai Strait using an unbaited trap, with numbers ranging from 0-475 [ha.sup.-1] (<1 crab 21 [m.sup.-2]). However, the use of unbaited traps underestimates abundance, which is two orders of magnitude below the values recorded intertidally in the current study (0-10,500 crabs [ha.sup.-1], 0 ~ 1 crab [m.sup.-2]). Using a box-corer, Saier (2002) recorded a mean C. maenas abundance of 359 [+ or -] 116 [m.sup.-2] (3.59 [x] [10.sup.6] [ha.sup.-1]) in the intertidal zone and 144 [+ or -] 54 [m.sup.-2] (1.44 [x] [l0.sup.6] [ha.sup.-1]) in the subtidal zone of the Wadden Sea, although these values include juvenile crabs. The abundance estimates given in the present study reflect the minimum number of crabs present on the mussel beds, because juveniles and crabs buried in the sediment or under algae were not visible in the video recordings. However, visual surveys of the mussel beds were more effective for most of the year than removing crabs from commercial mussel dredges, which resulted in underestimates of abundance caused by crabs escaping the dredges and the limited ability to see crabs among the harvested mussels. Even at the abundances presented here C. maenas will have a major impact on the mussel beds during certain times of the year and stages of the mussel cultivation process.

Carcinus maenas is virtually absent from the intertidal zone in the Menai Strait during winter (Beadman et al. 2003, Gascoigne et al. 2005). Consequently, the impact of predation on intertidal mussel beds is likely to be small from January to March, when temperatures fall as low as 6[degrees]C and the metabolic rate of crabs will also be lower (Robertson et al. 2002). Therefore, the impact of C. maenas on commercial mussel beds will be highest during the warmer months. In addition, it is during the spring and summer months in the Menai Strait that new seed mussels are laid and partially on-grown mussels (mussels that have been grown from seed that has been relaid) are moved into the subtidal zone where they are more vulnerable to predation by virtue of their being continuously immersed.

Mussels of ~25-30 mm length provide the maximum profitability for C. maenas of 60 mm CW (Fig. 6b). Based on profitability, Elner & Hughes (1978) predicted a preferred mussel length of 22.5-25 mm for C. maenas of 60-65 mm CW, bur observed 17.5 mm as the most frequently selected length of mussels. Similarly, Smallegange & van der Meer (2003) predicted a preferred mussel length range of 20-22.5 mm for C. maenas of 60-65 mm CW but most mussels were selected from the 16-18 mm length class. In the current study, the smallest mussels presented to C. maenas were 17.5-20 mm in length yet the mean and modal mussel length selected was ~24 mm for crabs of 60 mm CW. In the studies by Elner & Hughes (1978) and Smallegange & van der Meer (2003) the smallest mussels presented to crabs were 3 mm in length. Therefore, the presence of smaller mussels may have resulted in ah apparent preference for smaller mussels because of encounters made by the crabs and experience gained while feeding on smaller mussels. The increases in MML selected with increasing MML presented observed in the current study (Fig. 4) strongly support this assertion. From Figure 4 it is apparent that despite the difference in regression equations between the current study and Elner (1980), the difference in predicted mean mussel length selected is very small, with the largest predicted difference in mean mussel size selected for the smallest and largest crabs, at 1.4 mm and 0.4 mm, respectively.

Rovero et al. (2000) showed that the energy cost for C. maenas consuming mussels increased from 1.6% of the energy gained from small mussels (13-16 mm) to 3.3% of the energy gained from larger mussels (27-30 mm). Therefore, even when consuming larger mussels C. maenas makes substantial energy gains. Carcinus maenas switches from crushing mussels to using a more time-consuming cutting technique when the mussel width to major chela length ratio is [greater than or equal to] 0.24 (Smallegange & Van der Meer 2003). Thus crabs more frequently select smaller mussels because of the greater rime required to open larger mussels combined with the greater risk of chelal damage (Smallegange & van der Meer 2003). The effect of varying chelal size also accounts for some of the variability in the size and number of mussels consumed by crabs in the present study (Figs. 4 and 5). However, carapace width is a more convenient measure that can be used to rapidly assess the potential levels of predation in the field. Furthermore, Elner (1980) found strong positive correlations between carapace width and master chelal height in both male (y = 0.48x-1.11, [R.sup.2] = 0.93) and female (y = 0.23x - 0.02, [R.sup.2] = 0.86) C. maenas.

It is important to note that in many studies (Elner & Hughes 1978, Smallegange & van der Meer 2003, Mistri 2004), a preference for a particular prey size is assumed where the proportion of prey consumed from a given size class is greater than the proportion presented. Jackson and Underwood (2007) challenge this assumption, defining preference as a difference in the prey selected when choice is available compared with when no choice is available, distinguishing preference from electivity. Thus the larger mussels selected by C. maenas in the current study should not be considered indicative of a difference in preference but of electivity, which in terms of assessing the effects of predators on bivalve populations is the more useful measure.

The time over which experiments are conducted is also important, as mean feeding rates during the first 24 h are three times greater than after 48 h or four times greater than after 6 days. During the first few hours of feeding trials commencing crabs will feed more rapidly because of the fact that food was previously withheld for 48 h to standardize hunger levels. After the initial period of feeding the continued decline in feeding rates may be caused by decreased metabolic rate in the laboratory (Wallace 1973); energy requirements will be greater in the wild because of tidal migration, foraging, breeding, encounters with other crabs, and predators. Feeding rates of crabs in the wild will presumably vary between the extremes recorded over time in the current study, and will be dependent on food availability, season, and environmental conditions.

In the present study, the number of mussels consumed decreased at the higher and lower temperatures (Fig. 9), which could explain the lack of any significant difference in feeding rates between 10[degrees]C and 17[degrees]C reported by Elner (1980). Sanchez-Salazar et al. (1987a) recorded much higher energy consumption at 15.5[degrees]C compared with 9.5[degrees]C, but found no significant effect of temperature on the size of C. edule selected by C. maenas. Feeding rates in C. maenas are not entirely dependent on metabolic rate, which changes by a factor 1.4 between crabs acclimatized at 10[degrees]C and 24[degrees]C, compared with feeding rates, which may change by a factor of 2.4 (Wallace 1973). Furthermore, the effects of short-term temperature changes experienced by C. maenas because of weather conditions and tidal migration are uncertain. Temperatures in the Menai Strait range from 6[degrees]C to 17[degrees]C and C. maenas will feed within this range, although feeding rates are substantially reduced at the lower temperatures.

The critical mussel length over which size preference became more important than prey abundance in terms of the mussel size selected was 26 mm, approximately 2 mm above the size most often selected by 60 mm CW crabs when mussels were presented in equal size proportions (Fig. 4). In the current study, the mussel size selected most often by C. maenas of 60 mm CW was also the MML that was most profitable to the crabs (Fig. 6b). When making their selection crabs investigate the prey sizes available, handling several mussels before selecting one to eat (Elner & Hughes 1978, Ameyaw-Akumfi & Hughes 1987). Furthermore, Jubb et al. (1983) suggests a relative-stimulus hypothesis in which the size of prey sensed by the crabs' pereiopods influences the prey selected or rejected. Consequently, foraging time, along with handling time, will be greatly increased by increasing the numbers of mussels above the preferred size causing an exponential decline in numbers eaten.

Losses of mussels to C. maenas will decrease exponentially with mussel growth (Fig. 6a). Thus to minimize the number of mussels lost to crabs, it is during the first year of growth that most effort should be expended on protecting the mussels, either by increasing predator removal or using physical barriers to exclude predators. Reducing seed mussel losses will also require less exploitation of natural seed mussel stocks. However, it is only once mussels reach a marketable size, around 45 mm length, that they have any commercial value. Whereas it is clear that only the largest crabs are able to feed on mussels of a marketable size, losses of these mussels may amount to six per crab per day, amounting to 540 mussels per crab during the final six-month growing period in the subtidal zone.

Seed mussels are laid at a density of 50 t [ha.sup.-1] at a mean length 18.75 mm. If no mussels were lost throughout the cultivation process and mussels reached a mean length of 56.25 mm their weight would have increased 36-fold, reaching 1,775 t [ha.sup.-1]. However, only two to three times the weight laid remain once they have attained a marketable size (pers. comm.); thus, losses amount to ~92-4%. Based on the population size of C. maenas from April 2006 to March 2007 and the monthly averages of the number of mussels consumed (Fig. 10), it is estimated that predation by C. maenas accounts for 10.3% of the losses (9.5% of the seed mussels laid) during the entire cultivation process. Annual variations in the C. maenas population size will alter total losses suffered but mussel size is likely to remain the most important factor in determining crab induced mortality. Disease, competition, smothering, storm damage and predation by birds, starfish, and other crab species will account for the other losses.

The present study has provided the first estimates of the effects of C. maenas predation on the commercial mussel beds in the Menai Strait. The constants derived could also be applied to other mussel cultivation sites and the methods used to predict predator effects on bivalve populations in general. Measurements of predation in the field, using caging experiments or measurements of prey losses, would be of interest to compare with feeding rates and prey selection in the laboratory. The predictions made here can be refined with further studies into the effects of environmental conditions, predator interactions, and the population structure and diet of C. maenas.

ACKNOWLEDGMENTS

This work was funded by a European Social Fund Ph.D. studentship (LGM). The authors thank Kim Mould, and the staff of Myti Mussels Ltd and Extramussel Ltd; Tom Gallagher, Dr Chris Richardson, Dr James Bussell, Gwynne P Jones, and Berwyn Roberts.

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L. G. MURRAY, (1) * R. SEED (1) AND T. JONES (2)

(1) School of Ocean Sciences, University of Wales, Bangor, Menai Bridge LL59 5AB, United Kingdom;

(2) Extramussel Ltd., Refail, Llanfinan, Llangefni LL77 7SN, United Kingdom

* Corresponding author. E-mail: leegmurray@hotmail.com
TABLE 1.
Mean abundance [+ or -] 1 SE (crabs [m.sup.-1]) of Carcinus
maenas at subtidal (S) and intertidal (I) mussel beds, and
sites without mussels (N).

Site           Spring                  Summer

N1       0               --     0.11 [+ or -] 0.05
N2       0               --     0.13 [+ or -] 0.06
N3       0               --     0.00 [+ or -] 0.00
I1       0.29 [+ or -] 0.20     1.08 [+ or -] 0.31
I2       1.38 [+ or -] 0.63     0.50 [+ or -] 0.21
I3       0.00 [+ or -] 0.00     0.16 [+ or -] 0.07
S1       0.52 [+ or -] 0.52     0.10 [+ or -] 0.10
S2       0.36 [+ or -] 0.22     1.06 [+ or -] 0.20
S3       0.38 [+ or -] 0.15     0.52 [+ or -] 0.12

Site             Autumn                  Winter

N1         ND                  ND
N2         ND                  ND
N3       0.36 [+ or -] 0.31    ND
I1       0.31 [+ or -] 0.09    0               --
I2       0.11 [+ or -] 0.06    0               --
I3       0.39 [+ or -] 0.11    0               --
S1       0.15 [+ or -] 0.15    0.10 [+ or -] 0.03
S2       0.23 [+ or -] 0.16    0.09 [+ or -] 0.01
S3       1.07 [+ or -] 0.35    0.11 [+ or -] 0.01

ND indicates no data.

TABLE 2.
Mussel losses to Carcinus maenas in the Menai
Strait during the mussel cultivation process.

                         Losses
Time     Length      (kg [ha.sup.-1]
(mo)    class (mm)      [d.sup.-1]

 1      17.5-20.0        25.20
 2      20.0-22.5        51.77
 4      25.0-27.5        13.72
 9      27.5-30.0        10.54
13      30.0-32.5        18.29
15      32.5-35.0        25.92
17      37.5-40.0        23.40
21      37.5-40.0         8.45
22      37.5-40.0        11.30
28      47.5-50.0        18.42
30      52.5-55.0         0.33
33      55.0-57.5         0.24
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