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Positive feedback fishery: Population consequences of ‘crab-tiling’ on the green crab Carcinus maenas
Journal of Sea Research 60 (2008) 303–309
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Journal of Sea Research j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / s e a r e s
Positive feedback fishery: Population consequences of ‘crab-tiling’ on the green crab Carcinus maenas E.V. Sheehan ⁎, R.C. Thompson, R.A. Coleman 1, M.J. Attrill Marine Biology and Ecology Research Centre, School of Biological Sciences, Marine Institute, University of Plymouth, Drake Circus, Plymouth, PL4 8AA, UK
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Article history: Received 15 March 2008 Received in revised form 26 August 2008 Accepted 2 September 2008 Available online 13 September 2008 Keywords: Crab fishery Habitat provision Population structure Estuary Commercial species Bait collection
a b s t r a c t Collection of marine invertebrates for use as fishing bait is a substantial activity in many parts of the world, often with unknown ecological consequences. As new fisheries develop, it is critical for environmental managers to have high quality ecological information regarding the potential impacts, in order to develop sound management strategies. Crab-tiling is a largely unregulated and un-researched fishery, which operates commercially in the south-west UK. The target species is the green crab Carcinus maenas. Those crabs which are pre-ecdysis and have a carapace width greater than 40 mm are collected to be sold to recreational anglers as bait. Collection involves laying artificial structures on intertidal sandflats and mudflats in estuaries. Crabs use these structures as refugia and are collected during low tide. However, the effect that this fishery has on populations of C. maenas is not known. The impact of crab-tiling on C. maenas population structure was determined by sampling crabs from tiled estuaries and non-tiled estuaries using baited drop-nets. A spatially and temporarily replicated, balanced design was used to compare crab abundance, sizes and sex ratios between estuaries. Typically, fisheries are associated with a reduction in the abundance of the target species. Crab-tiling, however, significantly increased C. maenas abundance. This was thought to be a result of the extra habitat in tiled estuaries, which probably provides protection from natural predators, such as birds and fish. Although crabs were more abundant in tiled estuaries than non-tiled estuaries, the overall percentage of reproductively active crabs in non-tiled estuaries was greater than in tiled estuaries. As with most exploited fisheries stocks, crabs in exploited (tiled) estuaries tended to be smaller, with a modal carapace width of 20–29 mm rather than 30–39 mm in non-tiled estuaries. The sex ratio of crabs however; was not significantly different between tiled and non-tiled estuaries. These results illustrate the potential to manage fished populations using habitat provision to mitigate the effects of fishing pressure. © 2008 Elsevier B.V. All rights reserved.
1. Introduction Collecting invertebrates for use as fishing bait is widespread worldwide (Fairweather, 1991; Wynberg and Branch, 1991; Olive, 1993), and affects target organisms and other ecosystem components (Underwood, 1993; Thompson et al., 2002). When evaluating the sustainability of recreational fishing, Skilleter et al. (2005) highlighted the need to consider the impacts of bait collection as well as the sustainability of fish stocks, as this component is often ignored (McPhee and Skilleter, 2002). The addition of man-made structures to the marine environment is also of increasing concern, due to the rise in the number of coastal defences (Glasby and Connell, 1999), renewable energy related structures such as wind turbines (Wilhelmsson et al., 2006a), artificial reefs, and semi-permanent fishing equipment e.g. oyster trestles in ⁎ Corresponding author. Tel.: +44 1752 232906; fax: +44 1752 232970. E-mail address: [email protected] (E.V. Sheehan). 1 Present Address: Centre for Research on Ecological Impacts of Coastal Cities, Marine Ecology Laboratories (A11), The University of Sydney, NSW 2006, Australia. 1385-1101/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.seares.2008.09.002
estuaries (Nugues, 1996; Rilov and Benayahu, 2000; Hilgerloh et al., 2001). These structures add habitat complexity to often, soft sediment environments thereby altering species assemblages (Moschella et al., 2005; Wilhelmsson et al., 2006b). The present study examines a crab fishery ‘crab-tiling’, which involves not only collecting crustacea for bait, but also, installing semi-permanent man-made structures into estuarine mudflats. Over 1 million green crabs Carcinus maenas (L.) (Decapoda, Portunidae), are removed annually from estuaries in south-west UK to be sold as bait (Fowler, 1998; Black, 2004). To collect C. maenas, bait collectors known as ‘crab-tilers’, lay hard, stable structures, such as roof tiles, pieces of half round guttering, and car tyres on estuarine intertidal mudflats or sandflats to provide shelter that crabs will burrow beneath (Fig. 1). Crab-tilers only collect and sell those crabs which are (i) over 40 mm carapace width (CW), (ii) not brooding eggs (‘berried females’) and (iii) in a stage of pre-ecdysis. Crabs which are in this moulting stage are known within the angling community as ‘peeler crab’ and make excellent bait for bass Dicentrachus labrax (L.) and other species of fish. Qualifying crabs usually represent about 10 % of the crabs found under ‘crab-tiles’. The number of crab-tiles in
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affect the density and size structure of populations of other marine organisms (Wahle and Steneck, 1991; Hixon and Beets, 1993; Shervette et al., 2004). Lohrer et al. (2000) experimentally removed shelter in mudflats and detected a significant reduction in the total number of crabs. Adding hard substrata in an estuary may also increase potential food supply for crabs since crab-tiles also provide substratum for settlement of their prey, such as: Littorina littorea and Gibbula sp. (Sheehan, 2007; Cook et al., 2002). Finally, the insertion of the crab-tiles and the subsequent increase in substratum complexity may influence the recruitment of crabs through an increased abundance of sites for settling megalopae stages of C. maenas (Moksnes, 2002). Concerns were raised that due to the extent of crab-tiling activity in south-west UK, that crab population abundances may have been adversely affected (Sheehan, 2007). Due to the selective nature of this fishery, it was also expected that crab-tiling would have an effect on the sex ratio and on the size frequency of crabs in estuaries. The following hypotheses were therefore examined: (1) The abundance of C. maenas differs between tiled and non-tiled estuaries, (2) The size distribution of C. maenas populations will be different between tiled and non-tiled estuaries, and (3) Tiled estuaries would have different C. maenas sex ratios when compared to non-tiled estuaries. 2. Materials and methods 2.1. Study sites and experimental design
Fig. 1. a) Crab-tiles in the Teign Estuary, which are the numerous dark structures on the foreshore. b) Carcinus maenas being collected from a crab-tile.
south-west UK is particularly high, as the mild climate allows crabs to moult all year round (moulting threshold ≥8 °C, Crothers, 1967). In other parts of the UK, crabs will only moult over the summer months; therefore, crab-tilers can only operate for part of the year (Sheehan, 2007). The location of where crab-tiles can be laid is also limited. There is a public right to fish shellfish for personal use and/or commercial sale; however, the right to fish includes the right to lay fishing gear, by definition, fishing gear must ‘entrap’ the target species. Crab-tiles however, do not entrap the crabs and so permission must be gained from the landowner to lay crab-tiles. There are approximately 77,000 crab-tiles laid in south-west UK (Sheehan, 2007), yet the ecological consequence of laying these structures in soft-sediment habitats is not yet understood. This study focuses on the impact of the crab-tiling fishery on the population structure of the target species, and increases our understanding of the importance of habitat provision on exploited fisheries stocks. There are a number of mechanisms by which crab-tiling could affect crab-populations and these may have contrasting outcomes. For example, the effect of the selective removal of crabs from beneath crab-tiles could reduce local populations of C. maenas. Alternatively, the introduction of crab-tiles which increase the structural complexity of soft-sediment shorelines could indirectly increase the abundance of crabs. Increased habitat complexity increases the relative abundance of micro-habitats which reduce physiological stress e.g. heat, desiccation, freezing (Peterson, 1991) and provide refugia from predators (Klein-Breteler, 1976; Peterson, 1991; Moksnes et al., 1998; Lohrer et al., 2000). The availability of suitable refugia has been found to
Six estuaries in south-west UK were selected (Fig. 2), three estuaries where commercial crab-tiling takes place and three estuaries which have very few or no crab-tiles (Sheehan, 2007). Estuaries which were non-tiled are not exploited by crab-tilers as access to the foreshore is limited and often because landowners have not granted appropriate permission, rather than because of a lack of C. maenas (Tim Robbins, Devon Sea Fisheries Committee, pers. comm.). The three non-tiled estuaries were the Rivers Yealm (50° 19 N, 04° 02 W), Fowey (50° 21 N, 04° 38 W) and Salcombe (50° 14 N, 03° 44 W). The three tiled estuaries were the Rivers Plym (50° 22 N, 04° 05 W), Teign (50° 32 N, 03° 33 W) and Exe (50° 37 N, 03° 25 W). The average tidal range in these estuaries is 5.2 m during spring tides; the intertidal substrata were typically mudflats. Data were collected on two sampling occasions: October-November 2004 (sampling occasion 1) and May-June 2005 (sampling occasion 2). Sampling occasions were selected to detect generality of the patterns observed. Two times of the year were therefore selected, before and after winter, when both male and female crabs were likely to be present and active in the population (Naylor, 1962; Crothers, 1968; Atkinson and Parsons, 1973). To minimise potential confounding effects of tide (Crothers, 1968; Hunter and Naylor, 1993; Warman et al., 1993); daylight (Naylor, 1958; Aagaard et al., 1995) and lunar cycles (Aagaard et al., 1995) on crab activity, estuaries were sampled during daytime neap high tides. For each estuary, two sites were chosen based on the following criteria: 1. mid-estuary (mid-way between the river and the mouth), 2. covered by approximately 2 m of water during high tide, and 3. away (N30 m) from existing crab-tiles or other physical structures, such as moorings or boardwalks, which may cause crabs to aggregate (Kelaher et al., 1997; Lohrer et al., 2000). When sites are referred to as ‘tiled sites’, this means that the sites were within estuaries which were tiled, not that the sampling locations themselves were tiled. At each site on each sampling occasion, eight drop nets (drop net = 80 cm diameter, 0.5 cm mesh size) were deployed independently of each other, over two tidal cycles. Each net was baited with two small (length approximately 15 cm) freshly defrosted squid Loligo opalescens Berry, deployed and left in place for 15 minutes. Crabs were collected, sexed, measured (maximum carapace width CW) and returned to the estuary.
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Fig. 2. a) Location of estuaries sampled in England. b) Schematic diagram of the experimental design used to compare crabs in ‘non-tiled estuaries’ with crabs in ‘tiled estuaries’. Eight replicate nets were used to sample crabs at each site.
2.2. Data analyses 2.2.1. Abundance A four-factor ANOVA was performed using WinGMAV5 (EICC, The University of Sydney), followed by post-hoc Student Newman-Keuls (SNK) comparisons, to test the hypothesis relating to crab abundance. ‘Tiled’ had two levels (non-tiled and tiled), ‘sampling occasion’ which also had two levels (time 1 and time 2), were both orthogonal and fixed. The two remaining factors were both nested and random. ‘Estuary’ had three levels (three different estuaries, nested within ‘tiled’), and ‘site’ had two levels (site 1 and site 2, nested in ‘estuary’ and ‘tiled’). Each ‘site’ had eight replicate drop nets. The assumption of homogeneity of variance was tested with Cochran's C test (Underwood, 1997). Where heteroscedasticity could not be resolved through transformation, analyses were performed on untransformed data as ANOVA is robust to heterogeneous data from relatively large, balanced experimental designs (Underwood, 1997).
2.2.2. Size frequency distribution Carapace width measurements were separated into 10 mm size classes (e.g. 20 mm= 20–29 mm, 30 mm= 30–39 etc.). A KolmogorovSmirnov test (Sokal and Rohlf, 1995) was used to test the null hypothesis of no difference in size frequency distributions between tiled and nontiled estuaries for all of the populations of crabs collected. In addition to detecting any overall differences in the size frequency distribution between crab populations in tiled estuaries to those in non-tiled estuaries, it was also important to discriminate between the effects of crab-tiling on different functional size classes. The first size class were those crabs which are not taken by crab-tilers (juvenile and young crabs b40 mm CW), the second was those crabs which are taken by crab-tilers and reproductively active (‘medium’ 40–59 mm CW), the third were the largest crabs in the population (60 + mm). These larger crabs are usually competitively dominant and have a higher reproductive output (Crothers, 1968, Yamanda, 2001), and therefore are important to differentiate from the ‘medium’ sized crabs. Specific
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Table 1 Analysis of variance to compare the abundance of crabs between non-tiled and tiled estuaries Source of variation
df
MS
F
p
F versus
Tiled Tld Sampling occasion Sa Estuary Es (Tld) Site Si (Tld X Es) Tld X Sa Sa X Es (Tld) Sa X Si (Tld X Es) Residual Total
1 1 4 6 1 4 6 168 191
45448.52 21.33 2765.08 3075.95 841.69 3075.17 498.16 257.22
16.44 0.01 0.90 11.96 0.27 6.17 1.94
b 0.02 0.94 0.52 b 0.001 0.63 b 0.03 0.08
Es(Tld) Sa X Es(Tld) Si(Tld X Es) Residual Sa X Es(Tld) Sa X Si(TldX Es) Residual
Note: Factors were ‘tiled Tld’ (non-tiled and tiled), ‘Sampling occasion Sa’ (1 and 2), ‘Estuary Es’ (three estuaries for each treatment), and ‘Site Si’ (2 in each estuary) with 8 replicates. C = 0.27 (P b 0.01).
patterns in the relative proportions of crabs in the different size categories between tiled and non-tiled estuaries were examined using ANOVA. Data from nets within sites were combined to provide sufficient individuals for comparisons, such that ‘sites’ became the replicate unit of comparison. There were only 2 sites in each estuary, therefore the term ‘estuary’ was removed to keep a balanced design with sufficient replication for meaningful tests. Hence, the design here was two factor: ‘Tiled’ had two levels (non-tiled and tiled) and ‘sampling occasion’, which also had two levels (time 1 and time 2). Both factors were orthogonal and fixed, and there were six replicates. The relative proportion of each size class was calculated so that the demographic of the crab populations could be compared between tiled and non-tiled estuaries, by dividing the number of crabs in that size class by the total number of crabs in a site. 2.2.3. Proportion of females The hypothesis that tiled estuaries would have different sex ratios than non-tiled estuaries was examined by comparing the relative difference in the proportion of female C. maenas using ANOVA, following the same experimental design as above for size class. The proportion of females in each site was determined by dividing the number of females by the total number of crabs for each site, data were arcsin transformed (Sokal and Rohlf, 1995). 3. Results 3.1. Abundance
Fig. 3. Crab abundance between tiled and non-tiled estuaries. The graph indicates the variation of mean crab abundance (+ SE) for the interaction term Occasion X Estuary (Tiled) (see Table 1.). Non-tiled estuaries: Y = Yealm, F = Fowey, S = Salcombe; Tiled estuaries: P = Plym, T = Teign E = Exe. The feature to note is that the mean abundance of crabs from tiled estuaries (the average of the grey bars) was 39.72 (± 2.97 SE), this was significantly greater than the mean abundance of crabs from non-tiled estuaries (the average of the white bars), which was 8.95 (± 0.96 SE).
P b 0.01) (Sokal and Rohlf, 1995). For all size classes (apart from the largest ≥60 mm), tiled estuaries had greater numbers of crabs than nontiled estuaries. The greatest difference was observed for the 30–39 mm category. There were at least six times more 30 mm size class crabs and four times as many 40–49 mm and 50–59 mm size class crabs caught in tiled estuaries compared to non-tiled estuaries. For larger crabs (N60 mm), nearly 60% were captured in non-tiled estuaries, while for crabs of the smallest size class (10–19 mm) more than 85% were caught in tiled estuaries (Fig. 4). The abundance of small crabs (per site) differed with respect to time of sampling (Table 2, mean crab abundance; sampling occasion: (1) 42.2± 3.53 SE; (2) 32.5 ± 3.45 SE). There was a significant interaction between tiled/non-tiled estuaries and the time of sampling (Table 2.), in that medium-sized crabs were significantly more abundant in non-tiled estuaries compared to tiled estuaries at sampling occasion 1; but at sampling occasion 2 there were more medium sized crabs in tiled estuaries than non-tiled (Fig. 5). The mean abundance of large crabs differed significantly between sampling occasion 1 and 2 (Table 2, mean crab abundance; sampling occasion: (1) 9.91 ± 1.77 SE; (2) 18.1 ± 3.43 SE)
A total of 4672 C. maenas were caught, sexed and measured. The abundance of crabs varied significantly between tiled and non-tiled estuaries on each sampling occasion (Table 1; Fig. 3). Abundance also varied between sites within estuaries. Since both estuary and site were random factors with no associated a priori hypotheses, these were not interpreted further. Tiled estuaries had more than 4 times as many crabs as non-tiled estuaries (Table 1; Fig. 3). The non-tiled estuaries, Yealm, Fowey and Salcombe contained just 7.5%, 4.8% and 6.4% of the total number of crabs caught, whilst the number of crabs caught in the tiled estuaries, Plym, Teign and Exe, represented respectively 28.9%, 35.9% and 17.6% of the total number of crabs caught. 3.2. Size frequency Crab carapace widths ranged from 14 mm to 74 mm for females and from 9 mm to 80 mm for males. The modal size class in non-tiled estuaries was 30–39 mm whilst modal size class in tiled estuaries was 20–29 mm (Fig. 4). The size frequency of crabs caught in non-tiled estuaries and crabs caught in tiled estuaries both exhibited bell-shaped distributions but were significantly different from each other (Kolmogorov–Smirnov test, n1 = 777, n2 = 3895, D = 0.106 NN D0.01 = 0.061,
Fig. 4. Size frequency distribution of crabs in non-tiled and tiled estuaries (maximum carapace width CW).
E.V. Sheehan et al. / Journal of Sea Research 60 (2008) 303–309 Table 2 ANOVA comparing relative proportional differences for ‘small’, ‘medium’ and ‘large’ crabs, between crabs caught in non-tiled estuaries to crabs caught in tiled estuaries
Source of variation
df
Tiled Tld 1 Sampling 1 occasion Sa Tld × Sa 1 Residual 20 Total 23
307
Table 3 Analysis of variance to compare the proportion of female C. maenas in crab populations, between tiled estuaries and non-tiled estuaries
Small b40 mm
Medium 40–59 mm
LargeN60 mm
Source of variation
df
MS
F
P
MS
MS
MS
Tiled Tld Sampling occasion Sa Tld X Sa Residual Total
1 1 1 20 23
0.06 0.004 0.07 0.02
2.84 0.22 3.20
0.11 0.65 0.09
F
P
257.59 2.04 0.17 563.08 4.45 b 0.05 441.92 3.49 126.56
1.99 85.33
F
P 0.03 1.08
0.88 0.31
0.08 832.38 10.57 b0.005 78.75
F
P
431.92 5.76 b 0.03 401.19 5.35 b 0.04 40.15 0.54 75.01
0.47
Note: Size classes: b 40 mm (C = 0.38 ns), b) 40–59 mm (C = 0.33 ns) , c) 60+ mm (C = 0.71 p b 0.01), all data are arcsin (proportional) transformed.
and independently, between non-tiled and tiled estuaries (Table 2; nontiled= 18.24 ± 3.5 SE; tiled = 9.76 ± 1.53 SE). 3.3. Proportion of females In total 2086 male crabs and 2586 female crabs were caught; there was no significant difference (Table 3.) between the proportion of female crabs between non-tiled (mean = 0.44 ± 0.05 SE) and tiled estuaries (mean = 0.54 ± 0.04 SE). In tiled estuaries; however, the proportion of females did tend to be greater than the males in the populations (Fig. 6.). 4. Discussion Crab-tiling was clearly shown to affect C. maenas populations, though counter-intuitively, from what would normally be expected in a fished population. In that tiled estuaries had significantly 63% more crabs than non-tiled estuaries. Crab populations in estuaries which were tiled also had a different size structure compared to crab populations in non tiled estuaries; such that tiled estuaries had a smaller proportion of large crabs and a smaller modal size class of 20– 29 mm compared to 30–39 mm in non-tiled estuaries. The sex-ratio of C. maenas was not significantly affected by crab tiling. From a commercial point of view, stock enhancement of the target species may be considered a positive effect of this fishery, though from an environmental perspective, the increased abundance of a predator, such as C. maenas, may have adverse ecological effects. As crab-tiling involves the installation of refugia to relatively homogenous sedimentary habitats, the mechanism explaining the difference in the
Fig. 5. Differences in mean abundance (+SE) of medium sized crabs (40-59 mm CW) between non-tiled (white bars) and tiled estuaries (grey bars) for each of the two sampling occasions.
Note: Data were ArcSin (proportion) transformed. C = 0.35 ns.
abundance of crabs is most probably the increased habitat provision in the tiled estuaries. The selective nature of the fishery however, is likely to be driving the change in the size distribution of crabs. Fisheries worldwide are responsible for the substantial depletion of the target species (Haedrich and Barnes, 1997; Pauly et al., 1998; Jennings et al., 2001); however, this is not the case for the crab-tiling fishery, where the abundance of C. maenas in tiled estuaries (exploited) was found to be over four times greater than in estuaries which were non-tiled. It would appear that the consequences of increased habitat provision had a greater effect on crab abundance than the effects of their removal by crab-tilers. This unpredicted effect on the abundance of C. maenas could still, however, have adverse effects for associated estuarine fauna and their habitats. Elevated abundance of C. maenas can have various effects. Estuaries are important nursery areas for many commercially important fishes, such as plaice Pleuronectes platessa L., bass D. labrax and turbot Scophthalmus maximus (L.). C. maenas are a food resource for some fish species (Kelley, 1987), and therefore an increase in the abundance of juvenile C. maenas is likely to increase the size and abundance of the predatory fish. Conversely, an increase in the abundance of larger crabs may pose a threat to fish, as predation of juvenile fin-fish by C. maenas is documented for flounder Pseudopleuronectes americanus Walbaum, and cod Gadus morhua L. (Burrows et al., 1994; Fairchild and Howell, 2000; Taylor, 2005). Of primary interest to other commercial shellfisheries in crab-tiled estuaries, such as mussels Mytilus edulis L., oysters Crassostrea gigas (Thunberg) and Ostrea edulis L., and other types of bait collection e.g. lug worm Arenicola marina (L.) (Spencer, 2000) will be the potential detrimental effects that might be caused by an increase of C. maenas. These molluscs and polychaetes are an important part of the diet of C. maenas (Reise, 1978; Scherer and Reise, 1981; Gee et al., 1985; Raffaelli et al., 1989) and increases in the abundance of C. maenas can have a detrimental effect on fisheries of cultured Pacific oysters C. gigas (Walne and Davies, 1977); mussels M. edulis (Dare and Edwards, 1976; Davies et al., 1980) and hard clams Mercenaria mercenaria (L.) (Walne and Dean, 1972).
Fig. 6. Differences in mean abundance (+ SE) of male crabs (m) and female crabs (f) between non-tiled (white bars) and tiled estuaries (grey bars). n = 6 sites.
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Estuarine food webs are characterized by multi-level species interactions, which can be variable both spatially and temporally. Hence, it is difficult to make general predictions about the effects of elevated densities of C. maenas. The presence of other burrowing crab species, such as Chasmagnathus granulates (Dana), has been shown to indirectly cause opposing effects on predators of infauna, depending on the state of the tide. During low tide their burrows inhibited the foraging capacity of birds and ants on polychaetes (Palomo et al., 2003; Escapa et al., 2004); however, during high tide, fishes consumed more benthic prey when foraging in areas with crab burrows (Martinetto et al., 2005). Sometimes negative effects caused by the presence of C. maenas on one species have been coupled with further positive effects on another species. For example, in California Bay, the abundance of gammaridean amphipods (Eohaustorius spp., Paraphoxus spp.) declined in the presence of C. maenas, whilst the abundance of two polychaete taxa Lumbrineris spp. and Exogene spp., and a tanaid Leptochelia dubia (Krøyer) increased. These increases were attributed to strong top-down control from C. maenas, which removed co-occurring potential competitors and predators of the polychaetes and the tanaid (Grosholz et al., 2000). It could also be that the digging activity of C. maenas whilst foraging for prey aerated the top layer of the stable and often anoxic mud, creating a more favourable habitat for infauna (Schratzberger and Warwick, 1998). However, over a 9 year study no effect of the establishment of C. maenas was found on the abundance of 13 species of predatory shorebirds. Therefore, whilst there was a strong influence of this crab on its prey, there was no evidence of a bottom-up effect on C. maenas predators. (Grosholz et al., 2000). Collectively, these studies suggest that elevated numbers of C. maenas in estuaries which are crab-tiled are likely to have significant direct and indirect effects on estuarine communities. Fisheries, which are size and/or sex selective, either due to demand or because of legislation, can cause a population demographic that is not representative of natural populations (Carver et al., 2005). The selective removal of larger size categories of males from a population can significantly alter the mating dynamics, and hence also reduce overall reproductive success (Hines et al., 2003). Although crabs were more abundant in crab-tiled estuaries than non-tiled estuaries, the overall percentage of reproductively active crabs in non-tiled estuaries was greater than in tiled estuaries (reproductively active crabs : nontiled 62%, tiled 53%). Also, as crabs tended to be larger, it is likely that that the larger crabs would be more fecund than the smaller crabs. Nevertheless, C. maenas recruitment and offspring survivorship may increase in tiled estuaries due to the extra habitat provision. A significant difference between the size frequency distribution and smaller modal size of crab populations between tiled and non-tiled estuaries was observed. It is well documented that the diet of C. maenas may alter according to its size (Crothers, 1968). Young crabs feed on infauna; such as nematodes, flatworms, ostracods (Scherer and Reise, 1981), small cockles Cerastoderma edule (L.), and epifauna; such as, barnacles Semibalanus balanoides (L.) (Jensen and Jensen, 1985). Larger C. maenas tend to eat larger prey items, such as mussels M. edulis, clams Mya arenaria L., gastropods (Littorina spp.), algae and juvenile conspecifics (Crothers, 1968; Elner, 1977). Dare and Edwards (1981) showed that the size of oysters and mussels that a crab could open increased with the crab's carapace width. Therefore, changes in crab population structure could cause an ecosystem response, potentially changing the abundance and size distribution of prey species. For example, Gee et al. (1985) found that juvenile crabs in the River Lynher (UK) reduced the abundance of polychaetes, whilst adult crabs had a positive effect on the abundance of various small polychaete worms. Also in the UK, large crayfish Pacifastacus leniusculus (Dana) are selectively fished over their smaller conspecifics. As a result of P. leniusculus being a cannibalistic species, the lack of top down control on juvenile P. leniusculus from the larger adults has resulted in an abundance increase of juveniles. This has provided increased numbers of prey for predatory fish in the systems, which have been reported to have grown to unprecedented sizes (Sibley et al., 2002). For these
reasons it is important to investigate how fisheries affect the relative proportions of the different size classes of target organism as well as the overall abundance. Creating habitat in order to attract fauna is not limited to crab-tiling. For example, the use of fish aggregation devices (Rountree, 1989; Kawamura et al., 1996) or artificial reefs (Grove et al., 1991) to attract fishes to improve catches at a local scale. Crab-tiling, however, not only aggregates C. maenas to a specific area to facilitate collection, but also enhances the abundance of crabs in estuaries as a whole. Laying refugia to attract crustaceans is also used as a fishing practice in South America, where corrugated iron ‘tiles’ known as ‘casitas’ are laid on seagrass beds to attract rock lobsters Panulirus argus (Latreille) for collection (Karnofsky et al., 1989; Briones-Fourzán and Lozano-Álvarez, 2001). This fishery also increases the abundance of the target organism; however, similar to crab-tiling, the environmental effects of the fishery are likely to extend beyond the effects on the target organism. For example, the physical presence of the people collecting the crustaceans may disturb foraging birds and potentially cause trampling impacts, which could have an effect on infaunal assemblages. 5. Conclusions Crab-tiling is a highly lucrative fishery, which is expanding across the UK. As a consequence of the artificial habitat provision employed, the fishery in terms of crab abundance does not currently appear to be limited by the direct effects of crab removal. The fishery however, substantially reduces the average size of individuals and most probably also reduces overall reproductive output. At present it is not clear if recruitment of juveniles to crab-tiled estuaries is subsidised by larval import form adjacent areas and more work is required to establish this. It may be possible to manage these effects for example by introducing a minimum catch size and/or restricting the number of tiles in estuaries. However, before appropriate strategies can be developed at an ecosystem level (Shannon et al., 2006; Jennings and Revill, 2007), a more complete understanding of the indirect effects on the benthos and other mobile predators, such as birds and fish are also required. Acknowledgements This work was funded by the Holly Hill Charitable Trust with additional support from Natural England. We thank Tim Robbins (Devon Sea Fisheries Committee), Nigel Mortimer (Salcombe Conservation Officer), Jane Smith (Environmental Officer for Fowey Harbour Commissioners), Graeme Smithe (Teign Estuary Officer), Sarah Clark (Teign Estuary Partnership), Ken, Fred and Stuart (LEMA) for advice and logistical assistance. Rodney Bastard provided access to the River Yealm. Many thanks to Richard Ticehurst, Roger Haslam and Alex Abel for technical support. References Aagaard, A., Warman, C.G., Depledge, M.H., 1995. Tidal and seasonal changes in the temporal and spatial distribution of foraging Carcinus maenas in the weakly tidal littoral zone of Kerteminde Fjord, Denmark. Marine Ecology Progress Series 122 (1-3), 165–172. Atkinson, R., Parsons, A., 1973. Seasonal patterns of migration and locomotor rhythmicity in populations of Carcinus. Netherlands Journal of Sea Research 7, 81–93. Black, G., 2004. Report on surveys in 2003/04 of crab-tiling activity on Devon's estuaries and comparison with 2000/01 crab-tile survey data. Devon Biodiversity Records Centre. Briones-Fourzán, P., Lozano-Álvarez, E., 2001. Effects of artificial shelters (Casitas) on the abundance and biomass of juvenile spiny lobsters Panulirus argus in a habitatlimited tropical reef lagoon. Marine Ecology Progress Series 221, 221–232. Burrows, M.T., Gibson, R.N., Robb, L., Comely, C.A., 1994. Temporal patterns of movement in juvenile flatfishes and their predators: underwater television observations. Journal of Experimental Marine Biology and Ecology 177, 251–268. Carver, A.M., Wolcott, T.G., Wolcott, D.L., Hines, A.H., 2005. Unnatural selection: effects of a male-focused size-selective fishery on reproductive potential of a blue crab population. Journal of Experimental Marine Biology and Ecology 319 (1-2), 29–41.
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Journal of Sea Research j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / s e a r e s
Positive feedback fishery: Population consequences of ‘crab-tiling’ on the green crab Carcinus maenas E.V. Sheehan ⁎, R.C. Thompson, R.A. Coleman 1, M.J. Attrill Marine Biology and Ecology Research Centre, School of Biological Sciences, Marine Institute, University of Plymouth, Drake Circus, Plymouth, PL4 8AA, UK
a r t i c l e
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Article history: Received 15 March 2008 Received in revised form 26 August 2008 Accepted 2 September 2008 Available online 13 September 2008 Keywords: Crab fishery Habitat provision Population structure Estuary Commercial species Bait collection
a b s t r a c t Collection of marine invertebrates for use as fishing bait is a substantial activity in many parts of the world, often with unknown ecological consequences. As new fisheries develop, it is critical for environmental managers to have high quality ecological information regarding the potential impacts, in order to develop sound management strategies. Crab-tiling is a largely unregulated and un-researched fishery, which operates commercially in the south-west UK. The target species is the green crab Carcinus maenas. Those crabs which are pre-ecdysis and have a carapace width greater than 40 mm are collected to be sold to recreational anglers as bait. Collection involves laying artificial structures on intertidal sandflats and mudflats in estuaries. Crabs use these structures as refugia and are collected during low tide. However, the effect that this fishery has on populations of C. maenas is not known. The impact of crab-tiling on C. maenas population structure was determined by sampling crabs from tiled estuaries and non-tiled estuaries using baited drop-nets. A spatially and temporarily replicated, balanced design was used to compare crab abundance, sizes and sex ratios between estuaries. Typically, fisheries are associated with a reduction in the abundance of the target species. Crab-tiling, however, significantly increased C. maenas abundance. This was thought to be a result of the extra habitat in tiled estuaries, which probably provides protection from natural predators, such as birds and fish. Although crabs were more abundant in tiled estuaries than non-tiled estuaries, the overall percentage of reproductively active crabs in non-tiled estuaries was greater than in tiled estuaries. As with most exploited fisheries stocks, crabs in exploited (tiled) estuaries tended to be smaller, with a modal carapace width of 20–29 mm rather than 30–39 mm in non-tiled estuaries. The sex ratio of crabs however; was not significantly different between tiled and non-tiled estuaries. These results illustrate the potential to manage fished populations using habitat provision to mitigate the effects of fishing pressure. © 2008 Elsevier B.V. All rights reserved.
1. Introduction Collecting invertebrates for use as fishing bait is widespread worldwide (Fairweather, 1991; Wynberg and Branch, 1991; Olive, 1993), and affects target organisms and other ecosystem components (Underwood, 1993; Thompson et al., 2002). When evaluating the sustainability of recreational fishing, Skilleter et al. (2005) highlighted the need to consider the impacts of bait collection as well as the sustainability of fish stocks, as this component is often ignored (McPhee and Skilleter, 2002). The addition of man-made structures to the marine environment is also of increasing concern, due to the rise in the number of coastal defences (Glasby and Connell, 1999), renewable energy related structures such as wind turbines (Wilhelmsson et al., 2006a), artificial reefs, and semi-permanent fishing equipment e.g. oyster trestles in ⁎ Corresponding author. Tel.: +44 1752 232906; fax: +44 1752 232970. E-mail address: [email protected] (E.V. Sheehan). 1 Present Address: Centre for Research on Ecological Impacts of Coastal Cities, Marine Ecology Laboratories (A11), The University of Sydney, NSW 2006, Australia. 1385-1101/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.seares.2008.09.002
estuaries (Nugues, 1996; Rilov and Benayahu, 2000; Hilgerloh et al., 2001). These structures add habitat complexity to often, soft sediment environments thereby altering species assemblages (Moschella et al., 2005; Wilhelmsson et al., 2006b). The present study examines a crab fishery ‘crab-tiling’, which involves not only collecting crustacea for bait, but also, installing semi-permanent man-made structures into estuarine mudflats. Over 1 million green crabs Carcinus maenas (L.) (Decapoda, Portunidae), are removed annually from estuaries in south-west UK to be sold as bait (Fowler, 1998; Black, 2004). To collect C. maenas, bait collectors known as ‘crab-tilers’, lay hard, stable structures, such as roof tiles, pieces of half round guttering, and car tyres on estuarine intertidal mudflats or sandflats to provide shelter that crabs will burrow beneath (Fig. 1). Crab-tilers only collect and sell those crabs which are (i) over 40 mm carapace width (CW), (ii) not brooding eggs (‘berried females’) and (iii) in a stage of pre-ecdysis. Crabs which are in this moulting stage are known within the angling community as ‘peeler crab’ and make excellent bait for bass Dicentrachus labrax (L.) and other species of fish. Qualifying crabs usually represent about 10 % of the crabs found under ‘crab-tiles’. The number of crab-tiles in
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affect the density and size structure of populations of other marine organisms (Wahle and Steneck, 1991; Hixon and Beets, 1993; Shervette et al., 2004). Lohrer et al. (2000) experimentally removed shelter in mudflats and detected a significant reduction in the total number of crabs. Adding hard substrata in an estuary may also increase potential food supply for crabs since crab-tiles also provide substratum for settlement of their prey, such as: Littorina littorea and Gibbula sp. (Sheehan, 2007; Cook et al., 2002). Finally, the insertion of the crab-tiles and the subsequent increase in substratum complexity may influence the recruitment of crabs through an increased abundance of sites for settling megalopae stages of C. maenas (Moksnes, 2002). Concerns were raised that due to the extent of crab-tiling activity in south-west UK, that crab population abundances may have been adversely affected (Sheehan, 2007). Due to the selective nature of this fishery, it was also expected that crab-tiling would have an effect on the sex ratio and on the size frequency of crabs in estuaries. The following hypotheses were therefore examined: (1) The abundance of C. maenas differs between tiled and non-tiled estuaries, (2) The size distribution of C. maenas populations will be different between tiled and non-tiled estuaries, and (3) Tiled estuaries would have different C. maenas sex ratios when compared to non-tiled estuaries. 2. Materials and methods 2.1. Study sites and experimental design
Fig. 1. a) Crab-tiles in the Teign Estuary, which are the numerous dark structures on the foreshore. b) Carcinus maenas being collected from a crab-tile.
south-west UK is particularly high, as the mild climate allows crabs to moult all year round (moulting threshold ≥8 °C, Crothers, 1967). In other parts of the UK, crabs will only moult over the summer months; therefore, crab-tilers can only operate for part of the year (Sheehan, 2007). The location of where crab-tiles can be laid is also limited. There is a public right to fish shellfish for personal use and/or commercial sale; however, the right to fish includes the right to lay fishing gear, by definition, fishing gear must ‘entrap’ the target species. Crab-tiles however, do not entrap the crabs and so permission must be gained from the landowner to lay crab-tiles. There are approximately 77,000 crab-tiles laid in south-west UK (Sheehan, 2007), yet the ecological consequence of laying these structures in soft-sediment habitats is not yet understood. This study focuses on the impact of the crab-tiling fishery on the population structure of the target species, and increases our understanding of the importance of habitat provision on exploited fisheries stocks. There are a number of mechanisms by which crab-tiling could affect crab-populations and these may have contrasting outcomes. For example, the effect of the selective removal of crabs from beneath crab-tiles could reduce local populations of C. maenas. Alternatively, the introduction of crab-tiles which increase the structural complexity of soft-sediment shorelines could indirectly increase the abundance of crabs. Increased habitat complexity increases the relative abundance of micro-habitats which reduce physiological stress e.g. heat, desiccation, freezing (Peterson, 1991) and provide refugia from predators (Klein-Breteler, 1976; Peterson, 1991; Moksnes et al., 1998; Lohrer et al., 2000). The availability of suitable refugia has been found to
Six estuaries in south-west UK were selected (Fig. 2), three estuaries where commercial crab-tiling takes place and three estuaries which have very few or no crab-tiles (Sheehan, 2007). Estuaries which were non-tiled are not exploited by crab-tilers as access to the foreshore is limited and often because landowners have not granted appropriate permission, rather than because of a lack of C. maenas (Tim Robbins, Devon Sea Fisheries Committee, pers. comm.). The three non-tiled estuaries were the Rivers Yealm (50° 19 N, 04° 02 W), Fowey (50° 21 N, 04° 38 W) and Salcombe (50° 14 N, 03° 44 W). The three tiled estuaries were the Rivers Plym (50° 22 N, 04° 05 W), Teign (50° 32 N, 03° 33 W) and Exe (50° 37 N, 03° 25 W). The average tidal range in these estuaries is 5.2 m during spring tides; the intertidal substrata were typically mudflats. Data were collected on two sampling occasions: October-November 2004 (sampling occasion 1) and May-June 2005 (sampling occasion 2). Sampling occasions were selected to detect generality of the patterns observed. Two times of the year were therefore selected, before and after winter, when both male and female crabs were likely to be present and active in the population (Naylor, 1962; Crothers, 1968; Atkinson and Parsons, 1973). To minimise potential confounding effects of tide (Crothers, 1968; Hunter and Naylor, 1993; Warman et al., 1993); daylight (Naylor, 1958; Aagaard et al., 1995) and lunar cycles (Aagaard et al., 1995) on crab activity, estuaries were sampled during daytime neap high tides. For each estuary, two sites were chosen based on the following criteria: 1. mid-estuary (mid-way between the river and the mouth), 2. covered by approximately 2 m of water during high tide, and 3. away (N30 m) from existing crab-tiles or other physical structures, such as moorings or boardwalks, which may cause crabs to aggregate (Kelaher et al., 1997; Lohrer et al., 2000). When sites are referred to as ‘tiled sites’, this means that the sites were within estuaries which were tiled, not that the sampling locations themselves were tiled. At each site on each sampling occasion, eight drop nets (drop net = 80 cm diameter, 0.5 cm mesh size) were deployed independently of each other, over two tidal cycles. Each net was baited with two small (length approximately 15 cm) freshly defrosted squid Loligo opalescens Berry, deployed and left in place for 15 minutes. Crabs were collected, sexed, measured (maximum carapace width CW) and returned to the estuary.
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Fig. 2. a) Location of estuaries sampled in England. b) Schematic diagram of the experimental design used to compare crabs in ‘non-tiled estuaries’ with crabs in ‘tiled estuaries’. Eight replicate nets were used to sample crabs at each site.
2.2. Data analyses 2.2.1. Abundance A four-factor ANOVA was performed using WinGMAV5 (EICC, The University of Sydney), followed by post-hoc Student Newman-Keuls (SNK) comparisons, to test the hypothesis relating to crab abundance. ‘Tiled’ had two levels (non-tiled and tiled), ‘sampling occasion’ which also had two levels (time 1 and time 2), were both orthogonal and fixed. The two remaining factors were both nested and random. ‘Estuary’ had three levels (three different estuaries, nested within ‘tiled’), and ‘site’ had two levels (site 1 and site 2, nested in ‘estuary’ and ‘tiled’). Each ‘site’ had eight replicate drop nets. The assumption of homogeneity of variance was tested with Cochran's C test (Underwood, 1997). Where heteroscedasticity could not be resolved through transformation, analyses were performed on untransformed data as ANOVA is robust to heterogeneous data from relatively large, balanced experimental designs (Underwood, 1997).
2.2.2. Size frequency distribution Carapace width measurements were separated into 10 mm size classes (e.g. 20 mm= 20–29 mm, 30 mm= 30–39 etc.). A KolmogorovSmirnov test (Sokal and Rohlf, 1995) was used to test the null hypothesis of no difference in size frequency distributions between tiled and nontiled estuaries for all of the populations of crabs collected. In addition to detecting any overall differences in the size frequency distribution between crab populations in tiled estuaries to those in non-tiled estuaries, it was also important to discriminate between the effects of crab-tiling on different functional size classes. The first size class were those crabs which are not taken by crab-tilers (juvenile and young crabs b40 mm CW), the second was those crabs which are taken by crab-tilers and reproductively active (‘medium’ 40–59 mm CW), the third were the largest crabs in the population (60 + mm). These larger crabs are usually competitively dominant and have a higher reproductive output (Crothers, 1968, Yamanda, 2001), and therefore are important to differentiate from the ‘medium’ sized crabs. Specific
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Table 1 Analysis of variance to compare the abundance of crabs between non-tiled and tiled estuaries Source of variation
df
MS
F
p
F versus
Tiled Tld Sampling occasion Sa Estuary Es (Tld) Site Si (Tld X Es) Tld X Sa Sa X Es (Tld) Sa X Si (Tld X Es) Residual Total
1 1 4 6 1 4 6 168 191
45448.52 21.33 2765.08 3075.95 841.69 3075.17 498.16 257.22
16.44 0.01 0.90 11.96 0.27 6.17 1.94
b 0.02 0.94 0.52 b 0.001 0.63 b 0.03 0.08
Es(Tld) Sa X Es(Tld) Si(Tld X Es) Residual Sa X Es(Tld) Sa X Si(TldX Es) Residual
Note: Factors were ‘tiled Tld’ (non-tiled and tiled), ‘Sampling occasion Sa’ (1 and 2), ‘Estuary Es’ (three estuaries for each treatment), and ‘Site Si’ (2 in each estuary) with 8 replicates. C = 0.27 (P b 0.01).
patterns in the relative proportions of crabs in the different size categories between tiled and non-tiled estuaries were examined using ANOVA. Data from nets within sites were combined to provide sufficient individuals for comparisons, such that ‘sites’ became the replicate unit of comparison. There were only 2 sites in each estuary, therefore the term ‘estuary’ was removed to keep a balanced design with sufficient replication for meaningful tests. Hence, the design here was two factor: ‘Tiled’ had two levels (non-tiled and tiled) and ‘sampling occasion’, which also had two levels (time 1 and time 2). Both factors were orthogonal and fixed, and there were six replicates. The relative proportion of each size class was calculated so that the demographic of the crab populations could be compared between tiled and non-tiled estuaries, by dividing the number of crabs in that size class by the total number of crabs in a site. 2.2.3. Proportion of females The hypothesis that tiled estuaries would have different sex ratios than non-tiled estuaries was examined by comparing the relative difference in the proportion of female C. maenas using ANOVA, following the same experimental design as above for size class. The proportion of females in each site was determined by dividing the number of females by the total number of crabs for each site, data were arcsin transformed (Sokal and Rohlf, 1995). 3. Results 3.1. Abundance
Fig. 3. Crab abundance between tiled and non-tiled estuaries. The graph indicates the variation of mean crab abundance (+ SE) for the interaction term Occasion X Estuary (Tiled) (see Table 1.). Non-tiled estuaries: Y = Yealm, F = Fowey, S = Salcombe; Tiled estuaries: P = Plym, T = Teign E = Exe. The feature to note is that the mean abundance of crabs from tiled estuaries (the average of the grey bars) was 39.72 (± 2.97 SE), this was significantly greater than the mean abundance of crabs from non-tiled estuaries (the average of the white bars), which was 8.95 (± 0.96 SE).
P b 0.01) (Sokal and Rohlf, 1995). For all size classes (apart from the largest ≥60 mm), tiled estuaries had greater numbers of crabs than nontiled estuaries. The greatest difference was observed for the 30–39 mm category. There were at least six times more 30 mm size class crabs and four times as many 40–49 mm and 50–59 mm size class crabs caught in tiled estuaries compared to non-tiled estuaries. For larger crabs (N60 mm), nearly 60% were captured in non-tiled estuaries, while for crabs of the smallest size class (10–19 mm) more than 85% were caught in tiled estuaries (Fig. 4). The abundance of small crabs (per site) differed with respect to time of sampling (Table 2, mean crab abundance; sampling occasion: (1) 42.2± 3.53 SE; (2) 32.5 ± 3.45 SE). There was a significant interaction between tiled/non-tiled estuaries and the time of sampling (Table 2.), in that medium-sized crabs were significantly more abundant in non-tiled estuaries compared to tiled estuaries at sampling occasion 1; but at sampling occasion 2 there were more medium sized crabs in tiled estuaries than non-tiled (Fig. 5). The mean abundance of large crabs differed significantly between sampling occasion 1 and 2 (Table 2, mean crab abundance; sampling occasion: (1) 9.91 ± 1.77 SE; (2) 18.1 ± 3.43 SE)
A total of 4672 C. maenas were caught, sexed and measured. The abundance of crabs varied significantly between tiled and non-tiled estuaries on each sampling occasion (Table 1; Fig. 3). Abundance also varied between sites within estuaries. Since both estuary and site were random factors with no associated a priori hypotheses, these were not interpreted further. Tiled estuaries had more than 4 times as many crabs as non-tiled estuaries (Table 1; Fig. 3). The non-tiled estuaries, Yealm, Fowey and Salcombe contained just 7.5%, 4.8% and 6.4% of the total number of crabs caught, whilst the number of crabs caught in the tiled estuaries, Plym, Teign and Exe, represented respectively 28.9%, 35.9% and 17.6% of the total number of crabs caught. 3.2. Size frequency Crab carapace widths ranged from 14 mm to 74 mm for females and from 9 mm to 80 mm for males. The modal size class in non-tiled estuaries was 30–39 mm whilst modal size class in tiled estuaries was 20–29 mm (Fig. 4). The size frequency of crabs caught in non-tiled estuaries and crabs caught in tiled estuaries both exhibited bell-shaped distributions but were significantly different from each other (Kolmogorov–Smirnov test, n1 = 777, n2 = 3895, D = 0.106 NN D0.01 = 0.061,
Fig. 4. Size frequency distribution of crabs in non-tiled and tiled estuaries (maximum carapace width CW).
E.V. Sheehan et al. / Journal of Sea Research 60 (2008) 303–309 Table 2 ANOVA comparing relative proportional differences for ‘small’, ‘medium’ and ‘large’ crabs, between crabs caught in non-tiled estuaries to crabs caught in tiled estuaries
Source of variation
df
Tiled Tld 1 Sampling 1 occasion Sa Tld × Sa 1 Residual 20 Total 23
307
Table 3 Analysis of variance to compare the proportion of female C. maenas in crab populations, between tiled estuaries and non-tiled estuaries
Small b40 mm
Medium 40–59 mm
LargeN60 mm
Source of variation
df
MS
F
P
MS
MS
MS
Tiled Tld Sampling occasion Sa Tld X Sa Residual Total
1 1 1 20 23
0.06 0.004 0.07 0.02
2.84 0.22 3.20
0.11 0.65 0.09
F
P
257.59 2.04 0.17 563.08 4.45 b 0.05 441.92 3.49 126.56
1.99 85.33
F
P 0.03 1.08
0.88 0.31
0.08 832.38 10.57 b0.005 78.75
F
P
431.92 5.76 b 0.03 401.19 5.35 b 0.04 40.15 0.54 75.01
0.47
Note: Size classes: b 40 mm (C = 0.38 ns), b) 40–59 mm (C = 0.33 ns) , c) 60+ mm (C = 0.71 p b 0.01), all data are arcsin (proportional) transformed.
and independently, between non-tiled and tiled estuaries (Table 2; nontiled= 18.24 ± 3.5 SE; tiled = 9.76 ± 1.53 SE). 3.3. Proportion of females In total 2086 male crabs and 2586 female crabs were caught; there was no significant difference (Table 3.) between the proportion of female crabs between non-tiled (mean = 0.44 ± 0.05 SE) and tiled estuaries (mean = 0.54 ± 0.04 SE). In tiled estuaries; however, the proportion of females did tend to be greater than the males in the populations (Fig. 6.). 4. Discussion Crab-tiling was clearly shown to affect C. maenas populations, though counter-intuitively, from what would normally be expected in a fished population. In that tiled estuaries had significantly 63% more crabs than non-tiled estuaries. Crab populations in estuaries which were tiled also had a different size structure compared to crab populations in non tiled estuaries; such that tiled estuaries had a smaller proportion of large crabs and a smaller modal size class of 20– 29 mm compared to 30–39 mm in non-tiled estuaries. The sex-ratio of C. maenas was not significantly affected by crab tiling. From a commercial point of view, stock enhancement of the target species may be considered a positive effect of this fishery, though from an environmental perspective, the increased abundance of a predator, such as C. maenas, may have adverse ecological effects. As crab-tiling involves the installation of refugia to relatively homogenous sedimentary habitats, the mechanism explaining the difference in the
Fig. 5. Differences in mean abundance (+SE) of medium sized crabs (40-59 mm CW) between non-tiled (white bars) and tiled estuaries (grey bars) for each of the two sampling occasions.
Note: Data were ArcSin (proportion) transformed. C = 0.35 ns.
abundance of crabs is most probably the increased habitat provision in the tiled estuaries. The selective nature of the fishery however, is likely to be driving the change in the size distribution of crabs. Fisheries worldwide are responsible for the substantial depletion of the target species (Haedrich and Barnes, 1997; Pauly et al., 1998; Jennings et al., 2001); however, this is not the case for the crab-tiling fishery, where the abundance of C. maenas in tiled estuaries (exploited) was found to be over four times greater than in estuaries which were non-tiled. It would appear that the consequences of increased habitat provision had a greater effect on crab abundance than the effects of their removal by crab-tilers. This unpredicted effect on the abundance of C. maenas could still, however, have adverse effects for associated estuarine fauna and their habitats. Elevated abundance of C. maenas can have various effects. Estuaries are important nursery areas for many commercially important fishes, such as plaice Pleuronectes platessa L., bass D. labrax and turbot Scophthalmus maximus (L.). C. maenas are a food resource for some fish species (Kelley, 1987), and therefore an increase in the abundance of juvenile C. maenas is likely to increase the size and abundance of the predatory fish. Conversely, an increase in the abundance of larger crabs may pose a threat to fish, as predation of juvenile fin-fish by C. maenas is documented for flounder Pseudopleuronectes americanus Walbaum, and cod Gadus morhua L. (Burrows et al., 1994; Fairchild and Howell, 2000; Taylor, 2005). Of primary interest to other commercial shellfisheries in crab-tiled estuaries, such as mussels Mytilus edulis L., oysters Crassostrea gigas (Thunberg) and Ostrea edulis L., and other types of bait collection e.g. lug worm Arenicola marina (L.) (Spencer, 2000) will be the potential detrimental effects that might be caused by an increase of C. maenas. These molluscs and polychaetes are an important part of the diet of C. maenas (Reise, 1978; Scherer and Reise, 1981; Gee et al., 1985; Raffaelli et al., 1989) and increases in the abundance of C. maenas can have a detrimental effect on fisheries of cultured Pacific oysters C. gigas (Walne and Davies, 1977); mussels M. edulis (Dare and Edwards, 1976; Davies et al., 1980) and hard clams Mercenaria mercenaria (L.) (Walne and Dean, 1972).
Fig. 6. Differences in mean abundance (+ SE) of male crabs (m) and female crabs (f) between non-tiled (white bars) and tiled estuaries (grey bars). n = 6 sites.
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Estuarine food webs are characterized by multi-level species interactions, which can be variable both spatially and temporally. Hence, it is difficult to make general predictions about the effects of elevated densities of C. maenas. The presence of other burrowing crab species, such as Chasmagnathus granulates (Dana), has been shown to indirectly cause opposing effects on predators of infauna, depending on the state of the tide. During low tide their burrows inhibited the foraging capacity of birds and ants on polychaetes (Palomo et al., 2003; Escapa et al., 2004); however, during high tide, fishes consumed more benthic prey when foraging in areas with crab burrows (Martinetto et al., 2005). Sometimes negative effects caused by the presence of C. maenas on one species have been coupled with further positive effects on another species. For example, in California Bay, the abundance of gammaridean amphipods (Eohaustorius spp., Paraphoxus spp.) declined in the presence of C. maenas, whilst the abundance of two polychaete taxa Lumbrineris spp. and Exogene spp., and a tanaid Leptochelia dubia (Krøyer) increased. These increases were attributed to strong top-down control from C. maenas, which removed co-occurring potential competitors and predators of the polychaetes and the tanaid (Grosholz et al., 2000). It could also be that the digging activity of C. maenas whilst foraging for prey aerated the top layer of the stable and often anoxic mud, creating a more favourable habitat for infauna (Schratzberger and Warwick, 1998). However, over a 9 year study no effect of the establishment of C. maenas was found on the abundance of 13 species of predatory shorebirds. Therefore, whilst there was a strong influence of this crab on its prey, there was no evidence of a bottom-up effect on C. maenas predators. (Grosholz et al., 2000). Collectively, these studies suggest that elevated numbers of C. maenas in estuaries which are crab-tiled are likely to have significant direct and indirect effects on estuarine communities. Fisheries, which are size and/or sex selective, either due to demand or because of legislation, can cause a population demographic that is not representative of natural populations (Carver et al., 2005). The selective removal of larger size categories of males from a population can significantly alter the mating dynamics, and hence also reduce overall reproductive success (Hines et al., 2003). Although crabs were more abundant in crab-tiled estuaries than non-tiled estuaries, the overall percentage of reproductively active crabs in non-tiled estuaries was greater than in tiled estuaries (reproductively active crabs : nontiled 62%, tiled 53%). Also, as crabs tended to be larger, it is likely that that the larger crabs would be more fecund than the smaller crabs. Nevertheless, C. maenas recruitment and offspring survivorship may increase in tiled estuaries due to the extra habitat provision. A significant difference between the size frequency distribution and smaller modal size of crab populations between tiled and non-tiled estuaries was observed. It is well documented that the diet of C. maenas may alter according to its size (Crothers, 1968). Young crabs feed on infauna; such as nematodes, flatworms, ostracods (Scherer and Reise, 1981), small cockles Cerastoderma edule (L.), and epifauna; such as, barnacles Semibalanus balanoides (L.) (Jensen and Jensen, 1985). Larger C. maenas tend to eat larger prey items, such as mussels M. edulis, clams Mya arenaria L., gastropods (Littorina spp.), algae and juvenile conspecifics (Crothers, 1968; Elner, 1977). Dare and Edwards (1981) showed that the size of oysters and mussels that a crab could open increased with the crab's carapace width. Therefore, changes in crab population structure could cause an ecosystem response, potentially changing the abundance and size distribution of prey species. For example, Gee et al. (1985) found that juvenile crabs in the River Lynher (UK) reduced the abundance of polychaetes, whilst adult crabs had a positive effect on the abundance of various small polychaete worms. Also in the UK, large crayfish Pacifastacus leniusculus (Dana) are selectively fished over their smaller conspecifics. As a result of P. leniusculus being a cannibalistic species, the lack of top down control on juvenile P. leniusculus from the larger adults has resulted in an abundance increase of juveniles. This has provided increased numbers of prey for predatory fish in the systems, which have been reported to have grown to unprecedented sizes (Sibley et al., 2002). For these
reasons it is important to investigate how fisheries affect the relative proportions of the different size classes of target organism as well as the overall abundance. Creating habitat in order to attract fauna is not limited to crab-tiling. For example, the use of fish aggregation devices (Rountree, 1989; Kawamura et al., 1996) or artificial reefs (Grove et al., 1991) to attract fishes to improve catches at a local scale. Crab-tiling, however, not only aggregates C. maenas to a specific area to facilitate collection, but also enhances the abundance of crabs in estuaries as a whole. Laying refugia to attract crustaceans is also used as a fishing practice in South America, where corrugated iron ‘tiles’ known as ‘casitas’ are laid on seagrass beds to attract rock lobsters Panulirus argus (Latreille) for collection (Karnofsky et al., 1989; Briones-Fourzán and Lozano-Álvarez, 2001). This fishery also increases the abundance of the target organism; however, similar to crab-tiling, the environmental effects of the fishery are likely to extend beyond the effects on the target organism. For example, the physical presence of the people collecting the crustaceans may disturb foraging birds and potentially cause trampling impacts, which could have an effect on infaunal assemblages. 5. Conclusions Crab-tiling is a highly lucrative fishery, which is expanding across the UK. As a consequence of the artificial habitat provision employed, the fishery in terms of crab abundance does not currently appear to be limited by the direct effects of crab removal. The fishery however, substantially reduces the average size of individuals and most probably also reduces overall reproductive output. At present it is not clear if recruitment of juveniles to crab-tiled estuaries is subsidised by larval import form adjacent areas and more work is required to establish this. It may be possible to manage these effects for example by introducing a minimum catch size and/or restricting the number of tiles in estuaries. However, before appropriate strategies can be developed at an ecosystem level (Shannon et al., 2006; Jennings and Revill, 2007), a more complete understanding of the indirect effects on the benthos and other mobile predators, such as birds and fish are also required. Acknowledgements This work was funded by the Holly Hill Charitable Trust with additional support from Natural England. We thank Tim Robbins (Devon Sea Fisheries Committee), Nigel Mortimer (Salcombe Conservation Officer), Jane Smith (Environmental Officer for Fowey Harbour Commissioners), Graeme Smithe (Teign Estuary Officer), Sarah Clark (Teign Estuary Partnership), Ken, Fred and Stuart (LEMA) for advice and logistical assistance. Rodney Bastard provided access to the River Yealm. Many thanks to Richard Ticehurst, Roger Haslam and Alex Abel for technical support. References Aagaard, A., Warman, C.G., Depledge, M.H., 1995. Tidal and seasonal changes in the temporal and spatial distribution of foraging Carcinus maenas in the weakly tidal littoral zone of Kerteminde Fjord, Denmark. Marine Ecology Progress Series 122 (1-3), 165–172. Atkinson, R., Parsons, A., 1973. Seasonal patterns of migration and locomotor rhythmicity in populations of Carcinus. Netherlands Journal of Sea Research 7, 81–93. Black, G., 2004. Report on surveys in 2003/04 of crab-tiling activity on Devon's estuaries and comparison with 2000/01 crab-tile survey data. Devon Biodiversity Records Centre. Briones-Fourzán, P., Lozano-Álvarez, E., 2001. Effects of artificial shelters (Casitas) on the abundance and biomass of juvenile spiny lobsters Panulirus argus in a habitatlimited tropical reef lagoon. Marine Ecology Progress Series 221, 221–232. Burrows, M.T., Gibson, R.N., Robb, L., Comely, C.A., 1994. Temporal patterns of movement in juvenile flatfishes and their predators: underwater television observations. Journal of Experimental Marine Biology and Ecology 177, 251–268. Carver, A.M., Wolcott, T.G., Wolcott, D.L., Hines, A.H., 2005. Unnatural selection: effects of a male-focused size-selective fishery on reproductive potential of a blue crab population. Journal of Experimental Marine Biology and Ecology 319 (1-2), 29–41.
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