New additions to the feeding ecology of Carcinus maenas

Cah. Biol. Mar. (2010) 51 : 229-238

New additions to the feeding ecology of Carcinus maenas (L., 1758) in a South-western Europe estuary (Portugal) Maria Luísa CHAVES1, Manuel Santos HORTA1, Paula CHAINHO1, Maria José COSTA1,2 and José Lino COSTA1* (1) Faculdade de Ciências da Universidade de Lisboa, Instituto de Oceanografia, Campo Grande, 1749-016 Lisboa, Portugal. (2) Faculdade de Ciências da Universidade de Lisboa, Departamento de Biologia Animal, Lisboa, Campo Grande, 1749-016 Lisboa, Portugal. *E-mail: [email protected]

Abstract: The feeding ecology of the green crab Carcinus maenas was studied across all the estuarine gradient of the Mondego River, located within the species natural distribution range, adding information on the Northern branch of this estuary. A total of 683 specimens of C. maenas was collected at nine sampling stations during four seasonal surveys, using a 2 mm mesh size otter trawl. Stomach contents analyses of 578 specimens showed bivalves, crustaceans, polychaetes and algae as the most frequent food items; cannibalism and piscivory were also reported. Isopods and the gastropods Littorinidae were new additions to the listed items of C. maenas diet in this estuary. Spatial and temporal variations were found for the diet of C. maenas, with differences found between the Southern branch and all other estuarine areas and showing higher diet similarities during summer and autumn. Differences in the diet of C. maenas related with ontogeny “(size and sex)” were identified, which confirms the species potential to reduce intraspecific competition. The type and diversity of prey found in the diet of C. maenas suggest that it is an important predator in the food web of the Mondego river estuary, particularly in the adult phase, and confirm its ability to adopt an opportunistic feeding strategy. Résumé : Nouvelles données sur l’écologie alimentaire de Carcinus maenas (L., 1758) dans un estuaire du sud-ouest de l’Europe (Portugal). L’écologie alimentaire du crabe vert Carcinus maenas a été étudiée dans l’estuaire du Mondego, situé dans la zone de distribution naturelle de l’espèce, permettant d’ajouter de l’information sur la branche nord de cet estuaire. Un total de 683 individus de C. maenas a été recueilli à neuf stations d’échantillonnage lors de quatre campagnes saisonnières. Les analyses du contenu stomacal de 578 individus montraient que les bivalves, crustacés, polychètes et les algues sont les éléments alimentaires les plus fréquents. On a aussi constaté du cannibalisme et de la consommation de poissons. Isopodes et gastéropodes Littorinidés sont également des éléments de la diète de C. maenas dans cet estuaire. On a trouvé des variations spatiales et temporelles qui différencient la diète du crabe vert de la branche sud de l’estuaire d’autres régions estuariennes et qui montrent une similarité plus grande de cette diète pendant l’été et l’automne. Des variations de la diète de C. maenas avec l’ontogénie ont été observées, confirmant le potentiel de cette espèce pour réduire la compétition intraspécifique. Le type et la diversité des proies trouvées dans l’alimentation de C. maenas suggèrent que cette espèce de crabe est un prédateur important dans la chaîne alimentaire de l’estuaire du Mondego, en particulier à l’âge adulte, et confirment sa capacité à adopter une stratégie alimentaire opportuniste. Keywords: Green crab strategy

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Diet

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Mondego estuary

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Size/sex classes

Reçu le 9 septembre 2009 ; accepté après révision le 10 mai 2010. Received 9 September 2009; accepted in revised form 10 May 2010.

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Spatial and temporal variations

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Opportunistic

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FEEDING ECOLOGy OF CArCINUS mAENAS

Introduction The green crab Carcinus maenas (Linnaeus, 1758) (Decapoda: Portunidae) is the most characteristic crustacean decapod that inhabits European estuaries and rocky shores (Crothers, 1968). A wide geographical distribution (from the Scandinavian Peninsula to the Gibraltar strait and further South into Mauritania) and high local abundances (Klein-Breteler, 1976; Beukema et al., 1978) place C. maenas as a species of prime ecological importance. The green crab is an omnivorous predator, feeding on a wide variety of prey items (Crothers, 1968), in particular molluscs (Ropes, 1968; Elner, 1981), crustaceans (Baeta et al., 2006), and polychaetes (Le Calvez, 1987). C. maenas has successfully invaded intertidal habitats in several regions of the world (Cohen et al., 1995). This success is due, to some extent, to its adaptable diet and voracity (Griffiths et al., 1992). In spite of the very important role of C. maenas on structuring ecosystems by changing marine and estuarine communities through its feeding habits (Crothers, 1968; Ropes, 1968; Elner, 1981; Sanchez-Salazar et al., 1987a; Le Roux et al., 1990) few studies on the feeding ecology of this species are available in the biogeographic transitional area of South-western Europe (Le Calvez, 1987; Martins, 1995; Pestana, 1997; Baeta et al., 2005). Even though there is profuse literature on this species’ biology/ecology for other regions of the Globe, much of the information on C. maenas ecology is still based on laboratory experiments (Baeta et al., 2005). Studies on its natural diet, taking into account the prey’s ecology and its trophic relations are still uncommon and tremendously necessary to support an accurate management of green crab populations and natural resources in general. Feeding habits of the green crab were investigated across all the estuarine gradient of the Mondego River, included in its natural distributional range, to further improve knowledge on its feeding ecology. Unlike previous studies, emphasis was given to the ontogenic/sex, spatial and temporal variations of C. maenas diet.

Materials and Methods Study area The Mondego estuary is a mesotidal and well-mixed intertidal estuary, located in the central Portuguese Atlantic coast (40º08´N-8º50´W) (Fig. 1). This is a temperate-warm region influenced both by Atlantic and Mediterranean climates and characterised by a rainfall period extending from November to May and a drought period with very low water flow between June and October (Lima & Lima, 2002).

Figure 1. Carcinus maenas. Cartographic representation of the Mondego estuary, including the nine sampling stations established in this study. Figure 1. Carcinus maenas. Représentation cartographique de l’estuaire du Mondego et des neuf stations d’échantillonnage.

The estuary is divided in two branches that diverge 7.5 km upstream from the river mouth (Fig. 1), with different hydrological characteristics: (1) the Northern branch receives most of the freshwater input from the Mondego River, and is therefore, strongly influenced by seasonal freshwater fluctuations (Chainho et al., 2006), and has depths of 5-10 m during high tide, and a tidal range of approximately 2-3 m; (2) the Southern branch (2-4 m deep during high tide) drains a small tributary, the Pranto River, and is more strongly influenced by tidal cycles than the Northern branch. Due to differences in depth, the tidal excursion is longer in the Northern branch, causing stronger daily changes in salinity, whereas daily temperature changes are higher in the Southern branch (Lima & Lima, 2002). In the Northern branch, the sediment grain-size decreases towards the estuary mouth (gravel to fine sand). Fine sediments, like mud and very fine muddy sand, gather on areas of reduced hydrodynamics at margins and tidal flats. The area of marine influence of the Southern branch is dominated by sand with some shell gravel, whereas the upstream area is mainly muddy. As a consequence of lower hydrodynamism, Zostera noltii Hornemann, 1832 beds are only present in the Southern branch, and seasonal intertidal macroalgae blooms of Ulva spp. have been reported for this area, due to a high level of euthrophication (Cardoso et al., 2004). Thus, the two branches of the estuary can be considered different subsystems. The Mondego estuary is characterized by relatively fine sediments and high biomass of aquatic vegetation, which provide food resources and also adequate refuge areas for crabs, supporting an important population of C. maenas (Baeta et al., 2005). Most part of the green crab population of the Mondego estuary is located in the Southern branch due to reduced hydrodynamism, presence of muddy

M.L. CHAVES, M. SANTOS HORTA, P. CHAINHO, M.J. COSTA, J.L. COSTA

bottoms and important algal and Zostera beds (Cardoso et al., 2004; Baeta et al., 2005). Abiotic and biotic conditions in the Northern branch (higher hydrodynamism, coarser sediments and reduced vegetation cover) seem to be less favourable to C. maenas, with decreasing abundance of this species upstream due to reduced salinity (Horta, 2006). Sampling A total of nine sampling stations was established for this study (Fig. 1) covering the salinity gradient between the vicinity of the river mouth and the upper tidal reaches of both branches of the estuary. Seasonal sampling was carried out in July (summer) and October (autumn) 2000 and February (winter) and early June (spring) 2001, using a commercial fishing vessel. Crabs were collected using an otter trawl with a 2 mm mesh size at cod-end. Two hauls of 15 minutes each were conducted in each sampling station during ebb tide from upstream to downstream. Samples of C. maenas were stored in ice and later frozen at - 20ºC. Laboratory procedures and data analysis All crabs were counted, sexed and measured (carapace width – CW) to the nearest mm. Following Berrill (1982) and Baeta et al. (2005), specimens were divided into 8 discrete classes according to their sex (F: females, M: males) and size: F1/M1, CW ≤ 35 mm; F2/M2, 35 < CW ≤ 45 mm; F3/M3, 45 < CW ≤ 55 mm; F4/M4: CW > 55 mm. Female individuals in classes F3 and F4 were aggregated (into F34) to analyze size/sex variations in the species feeding ecology due to the low number of F4 individuals. The stomach contents of a random subsample (578) of C. maenas specimens were sorted and identified to the lowest possible taxonomic level using a dissecting microscope. Due to the diversity of organisms and high degree of disintegration of the food items found in the stomachs, their importance to the species diet had to be analysed exclusively using the relative Occurence Index (OI). The OI is the proportion of non-empty stomachs that contain a particular item (Hyslop, 1980). The Kendall Coefficient of Concordance test (W2) (Siegel & Castellan, 1988) was applied to these OI values to test for the significance of concordance in diet considering the size/sex classes, sampling stations and seasons. Following this procedure, a cluster analysis using squared Euclidean distances and group average linking was conducted for size/sex classes, sampling stations and seasons to identify relatively homogeneous groups in terms of diet. Considering the recommendations of Field et al. (1982), Stergiou & Fourtouni (1991) and Costa (2004) to improve the reliability of this analysis, that technique was complemented by a Correspondence Analysis (CA) (ter

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Braak & Šmilauer, 2002) and both outputs interpreted together. However, only the ontogenetic/sex variations CA diagram is shown because other CA diagrams do not provide additional information. An RxC independence Gtest with Williams’ correction (GW) and the respective a posteriori simultaneous test procedure (Sokal & Rohlf, 1995) were performed to determine whether the ingestion of the most important food items depended on the size/sex of the individuals, sampling areas or seasons, considering the homogeneous groups defined in the previous cluster analyses. All mathematical procedures were performed using the SPSS statistical package (Anonymous, 1997) with the exception of the G-tests and the CA, which were conducted using BIOMstat (Rohlf & Slice, 1995) and CANOCO (ter Braak & Šmilauer, 2002) programs, respectively.

Results Distribution, abundance and population structure A total of 683 crabs was captured. Highest abundance values were found in the Southern branch and medium size individuals (from 35 to 55 mm) were the most abundant (Fig. 2). High homogeneity in the relative abundance of size/sexual classes was found in the entire estuary, except for the proportion of F3 and F4 females, which were more common in the mouth of the estuary.

Figure 2. Carcinus maenas. Population structure in the Mondego estuary. Symbols for sampling stations and size/sexual classes are indicated in Figure 1 and in the methods section, respectively. N = 683 (308 females, 375 males). Figure 2. Carcinus maenas. Structure démographique dans l’estuaire du Mondego. Symboles pour les stations d’échantillonnage et pour les classes de taille/sexe comme indiqués dans la Figure 1 et dans la section de méthodes, respectivement. N = 683 (308 femelles, 375 mâles).

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Diet

Ontogenic and sex variations

A total of 578 crabs was considered for feeding ecology analyses and around 30% of individuals had empty stomachs (Table 1). Overall, Bivalvia were the most frequent food item (OI = 0.38) identified in the diet of C. maenas in the Mondego estuary, followed by Crustacea, Polychaeta and Algae (with OI = 0.28, 0.26 and 0.22, respectively) (Table 2). Gastropoda and Teleostei prey groups were also present in stomach contents (Table 2).

The Kendall test revealed no significant concordance in the diet of size/sex classes (W2 = 54.42, df = 6, p > 0.05). Two major ontogenic groups were identified by the cluster analysis based on their diet: smaller and larger individuals (F1, M1 and M4) and medium size individuals (M2, M3, F2 and F34) (Fig. 3). However, the CA diagram shows that the cluster linkage between small (F1 and M1) and larger individuals (M4) is artificial, resulting from the lower diversity of preys consumed by these extreme size classes when compared to medium size individuals (Fig. 4). In fact, in this diagram, larger crabs (M4) are associated with preys of higher dimensions like Scrobiculariidae, Teleostei and C. maenas (cannibalism) whereas smaller individuals (F1 and M1) are highly associated to Algae. G-tests confirmed significant ontogenic variations in the intake of Scrobiculariidae (GW = 7.179, df = 2, p < 0.05), preferred by the largest crabs, and Algae (GW = 6.019, df = 2, p < 0.05), the most important food item for smaller crabs (Table 2). A more generalist diet was identified for medium size crabs, which showed an intermediate position in the CA diagram (Fig. 4) and relative higher values of consumption of some other preys, such as Polychaeta, Crustacea and Gastropoda, when compared to the diet of larger and smaller crabs (Table 2). In general, male and female crabs of the same size class had similar diets (Figs 3 & 4).

Table 1. Carcinus maenas. Number of individuals with stomach contents and empty stomachs, by size and sex classes. Tableau 1. Carcinus maenas. Nombre d’individus avec l’estomac rempli et vide par classes de taille et par sexe. CW

≤ 35 mm 35-45 mm 45-55 mm > 55 mm Total

Size/Sex Class

Stomach with contents

Empty stomachs

Total

F1 M1 F2 M2 F3 M3 F4 M4

36 37 75 73 59 75 5 41 401

14 10 35 27 33 39 4 15 177

50 47 110 100 92 114 9 56 578

CW- Carapace width

Prey items Algae Total Polychaeta Nereididae Polychaeta n.i. Total Gastropoda Littorinidae Gastropoda n.i. Total Bivalvia Cardiidae Mytilidae Scrobiculariidae Bivalvia n.i. Total Crustacea Mysidacea Isopoda Amphipoda Crangon crangon (Linnaeus, 1758) Carcinus maenas (Linnaeus, 1758) Crustacea n.i. Teleostei

Total sample 0.22 0.26 0.07 0.21 0.05 0.02 0.03 0.38 0.13 0.04 0.08 0.13 0.28 0.02 0.02 0.08 0.06 0.02 0.07 0.04

Size/sex classes F1/M1 F2/F34/M2/M3 0.29 0.26 0.05 0.21 0.01 0.00 0.01 0.27 0.14 0.04 0.01 0.08 0.19 0.03 0.00 0.08 0.04 0.00 0.04 0.01

0.22 0.29 0.07 0.22 0.06 0.02 0.04 0.40 0.12 0.04 0.09 0.15 0.31 0.02 0.02 0.09 0.07 0.02 0.09 0.04

M4 0.10 0.24 0.07 0.17 0.02 0.02 0.00 0.44 0.20 0.05 0.12 0.07 0.27 0.02 0.02 0.07 0.05 0.05 0.05 0.05

F3 and F4 were aggregated into F34 due to the low number of F4 individuals. Symbols for size/sex classes as indicated in the methods section.

Table 2. Carcinus maenas. Relative Occurrence Index (OI) for all food items found in stomach contents from the Mondego estuary. The total sample and homogenous size/sex classes in terms of feeding habits (identified by the cluster analysis, Fig. 3) were considered (N = 401). Tableau 2. Carcinus maenas. Indice d’Occurrence Relative (OI) pour tous les items alimentaires trouvés dans le contenu des estomacs de l’estuaire du Mondego. Tous les individus et classes homogènes de taille/sexe, en terme d’habitudes alimentaires (identifiées par l’analyse de groupement, Fig. 3) ont été considérés (N = 401).


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Spatial variations

Figure 3. Carcinus maenas. Cluster analysis of the size/sex classes according to their diet in the Mondego estuary. Symbols for size/sex classes as indicated in methods section. F3 and F4 were aggregated into F34 due to the low number of F4 individuals. Figure 3. Carcinus maenas. Analyse de groupement des classes de taille/sexe selon leur diète dans l’estuaire du Mondego. Symboles pour classes de taille/sexe comme indiqués dans la section de méthodes. F3 et F4 ont été agrégés en F34 dû au fait d’un très petit nombre d’individus F4.

No significant spatial concordance was found in the diet of C. maenas in the Mondego estuary (W2 = 84.07, df = 8, p > 0.05). Cluster analysis revealed two major spatial groups: specimens collected in the Southern branch of the estuary (E1 and E2) and specimens from all other estuarine areas (E3 to E9) (Fig. 5). Polychaeta, Crustacea, Bivalvia and Algae were the most representative preys in both areas (Table 3). However, G-tests revealed significant spatial variations in diet for two groups of preys: Nereididae (GW = 8.523, df = 1, p < 0.01) and Crangon crangon (Linnaeus, 1758) (GW = 4.153, df = 1, p < 0.05). Both taxa were more frequent in the stomach of specimens from the Southern branch. Seasonal variations No significant seasonal concordance was also found in the diet of C. maenas in the Mondego estuary (W2 = 15.48, df = 3, p > 0.05). The cluster analysis evidenced a higher similarity in the diet of this crab during summer and

Figure 4. Carcinus maenas. Correspondence analysis (CA) diagram considering the diet of different size/sex classes in the Mondego estuary. Symbols for size/sex classes as indicated in the methods section. F3 and F4 were aggregated into F34 due to the low number of F4 individuals. Prey items designations correspond to the lowest taxonomical level of identification (see Table 2). Figure 4. Carcinus maenas. Diagramme d’analyse de correspondance (CA) en considérant la diète de différentes classes de taille/sexe dans l’estuaire du Mondego. Symboles pour classes de taille/sexe comme indiqués dans la section de méthodes. F3 et F4 ont été agrégés en F34 dû au fait d’un très petit nombre d’individus F4. Les désignations des proies correspondent au niveau d’identifications taxonomique le plus bas (voir Tableau 2).

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Figure 5. Carcinus maenas. Cluster analysis of the Mondego estuary sampling stations according to the diet. Symbols for sampling stations as indicated in Figure 1. Figure 5. Carcinus maenas. Analyse de groupement des stations d’échantillonnage de l’estuaire du Mondego selon la diète. Les symboles pour les stations d’échantillonnage comme indiqués dans la Figure 1.

Table 3. Carcinus maenas. Relative Occurrence Indices (OI) for all food items of C. maenas in homogeneous areas of the Mondego estuary in terms of feeding habits (based on cluster analysis, Fig. 5) (N = 401). Tableau 3. Carcinus maenas. Les indices d’Occurrence Relative (Ol) pour tous les items alimentaires du C. maenas dans les zones homogènes de l’estuaire du Mondego concernant les habitudes alimentaires (en fonction de l’analyse de groupement, Fig. 5) (N = 401). Prey items Algae Total Polychaeta Nereididae Polychaeta n.i. Total Gastropoda Littorinidae Gastropoda n.i. Total Bivalvia Cardiidae Mytilidae Scrobiculariidae Bivalvia n.i. Total Crustacea Mysidacea Isopoda Amphipoda Crangon crangon Carcinus maenas Crustacea n.i. Teleostei

Sampling stations E 1-2 E 3-9 0.20 0.31 0.10 0.22 0.05 0.01 0.04 0.37 0.14 0.05 0.07 0.11 0.30 0.03 0.02 0.09 0.08 0.02 0.05 0.04

Symbols for sampling stations as indicated in Figure 1.

0.24 0.23 0.03 0.21 0.04 0.02 0.02 0.41 0.11 0.04 0.10 0.16 0.26 0.01 0.02 0.08 0.03 0.03 0.11 0.04

Figure 6. Carcinus maenas. Cluster analysis of the sampling seasons according to the diet in the Mondego estuary. Figure 6. Carcinus maenas. Analyse de groupement des stations d’échantillonnage selon la diète dans l’estuaire du Mondego.

autumn (Fig. 6). Similarly to what was found for spatial patterns, Polychatea, Crustacea, Bivalvia and Algae were the main food items all over the year (Table 4). Nevertheless, significant seasonal variations in the diet of C. maenas were revealed by G-tests for four prey groups: Nereididae (GW = 12.664, df = 3, p < 0.01), Bivalvia n.i. (GW = 17.048, df = 3, p < 0.001), Cardiidae (GW = 12.497, df = 3; p < 0.01) and Scrobiculariidae (GW = 12.412, df = 3, p < 0.01). Consumption of Nereididae was higher in winter and spring than in summer. For Cardiidae and Scrobiculariidae, significant differences were found between winter and autumn and summer and autumn, respectively. Unidentified Bivalvia were most common in the diet of C. maenas during autumn and less common in the summer, though the consumption of total Bivalvia was homogenous along the year.

Discussion Stomach content analyses of C. maenas in the Mondego estuary showed a large prey spectrum, with Bivalvia, Crustacea, Polychaeta and Algae as the most representative groups. Studies on natural feeding habits of the green crab from similar and distinct geographic locations evidenced differences on preferential food items. Baeta et al. (2006) found Crustacea, Polychaetes and Teleostei as preferential prey of C. maenas in the Southern branch and mouth of the Mondego estuary. Data from the Mira estuary, located in the Portuguese South-western coast and approximately identical to the Mondego estuary in size, revealed Crustacea, Bivalvia and Teleostei as the main food items in the diet of this crab (Martins, 1995). Similar results were referred by Pestana (1997) in the Tagus estuary, located in the central region of Portugal. Some of these authors considered that most Algae and Bivalvia items found in green crabs stomachs were accidentally ingested when these crabs attack other prey (Martins, 1995; Baeta et al., 2006). However, the large amount of these prey groups


Table 4. Carcinus maenas. Relative Occurrence Indices (OI) for all food items in different seasons in the Mondego estuary (N = 401). Tableau 4. Carcinus maenas. Indices d’Occurrence Relative (Ol) pour tous les items alimentaires pendant l’année dans l’estuaire du Mondego (N = 401). Prey items Algae Total Polychaeta Nereididae Polychaeta n.i. Gastropoda total Littorinidae Gastropoda n.i. Total Bivalvia Cardiidae Mytilidae Scrobiculariidae Bivalvia n.i. Total Crustacea Mysidacea Isopoda Amphipoda Crangon crangon Carcinus maenas Crustacea n.i. Teleostei

Seasons Summer Autumn Winter 0.18 0.19 0.00 0.19 0.04 0.01 0.03 0.33 0.10 0.01 0.16 0.05 0.31 0.03 0.04 0.12 0.03 0.00 0.09 0.07

0.18 0.22 0.05 0.17 0.01 0.00 0.01 0.36 0.05 0.05 0.03 0.23 0.26 0.01 0.01 0.07 0.03 0.02 0.11 0.03

0.16 0.38 0.11 0.27 0.03 0.01 0.02 0.45 0.21 0.05 0.12 0.06 0.37 0.01 0.03 0.12 0.10 0.04 0.06 0.04

Spring 0.29 0.29 0.08 0.21 0.08 0.03 0.05 0.38 0.13 0.05 0.05 0.15 0.23 0.03 0.01 0.05 0.06 0.02 0.05 0.02

found in crabs’ stomachs during the present study is not consistent with an accidental consumption. Studies in Portuguese estuaries revealed a diversified diet, similarly to what was found by Le Calvez (1987) for the Rance Basin (Brittany, France) and Griffiths et al. (1992) for the South African coast. In contrast, in works by Crothers (1968) at Dale Peninsula, Wales, Ropes (1968) at Rhode Island, USA, or Elner (1981) at Port Hebert, Canada, the diet of C. maenas consisted almost exclusively of Bivalvia. C. maenas diet variations in different geographical areas and the large amount of Algae found in stomachs during the present study emphasize the omnivorous and opportunistic feeding strategy of this species. However, in the Mondego estuary specimens of C. maenas consume preys over a certain size within the available species. As shown by Chainho et al. (2006), the benthic invertebrate communities in the Mondego estuary during the same sampling period were numerically dominated by small sized opportunistic polychaetes, most of which not included in the diet of C. maenas. On the contrary, invertebrate biomass was dominated by bivalves (Cardiidae and Scrobiculariidae) and large polychaete species such as Nereis diversicolor (O.F. Müller, 1776)

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(unpublished data), which were highly consumed by C. maenas. Therefore, a certain degree of food selection based on size seems to exist even in smaller crabs. In the Mondego estuary all size/sex classes of C. maenas ingested mainly Bivalvia, Crustacea, Polychaeta and Algae, which seems to confirm the results obtained by Baeta et al. (2006) of no ontogenic or sex differences in the species diet. However, important variations in the diet according to animal size were observed, with higher Algae intake by smaller crabs than adults. This is probably due to the reduced capacity of smaller crabs to capture and crush hard preys as their claws are less developed than in older crabs. According to Rangeley & Thomas (1987), juvenile C. maenas feed on a narrow size range of preys, constrained by their chelal strength, dexterity, and time required to open prey over a certain size. In the present study larger crabs were associated with larger preys such as Scrobiculariidae, C. maenas and Teleostei most probably because these crabs are able to open larger bivalve shells and handle prey of any size (Sanchez-Salazar et al., 1987b). Further, the experiments by Walne & Dean (1972) on predation of bivalves by C. maenas show that prey size is correlated to predator size. That seems to be the reason for having more Teleostei in the diet of larger crabs than in smaller ones, although consumption of dead fish by C. maenas has also been reported (Berghahn; 1990; Martins, 1995). It should be noticed however that many molluscivorous predators such as C. maenas, despite being able to consume larger and more profitable preys, show a preference for smaller, less profitable preys, most likely to minimize the risk of damaging feeding extremities (Smallegange et al., 2008). Diet variations according to size confirmed C. maenas ability to reduce intraspecific competition. Nonetheless, the occurrence of conspecifics in the stomach contents of these crabs was common, similarly to what was found by Martins (1995) in the Mira estuary, Pestana (1997) in the Tagus estuary and Baeta et al. (2006) in the Mondego estuary. Klein-Breteler (1976) also referred predation by larger shore crabs on smaller ones as a common occurrence in the Wadden Sea, Netherlands. According to Baeta et al. (2006), the incidence of cannibalism may be enhanced by high densities that favour encounters between conspecifics. Medium size crabs seem to capture a larger spectrum of prey sizes. Contrarily to larger specimens, which have less mechanical restrictions to attack and handle larger preys and can be more species selective, crabs of intermediate size seem to be more limited in terms of prey size and thus constrained to be less selective regarding prey species (Mascaró & Seed, 2001). A feeding strategy that includes a wide variety of prey species, even of smaller size, might allow these crabs to ingest sufficient biomass to meet the energy requirements for their growth and maturation. Therefore, capturing small prey may still be a rewarding

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investment in terms of energy spending for these medium size crabs, although they also hunt larger preys, within the limits imposed by the risk of claw damage. Despite the relative homogeneity in the diet of C. maenas along the Mondego estuary, some spatial variations were found regarding its feeding habits. Since no important spatial variations were observed in the population structure of C. maenas in the estuary, such differences in diet cannot be related to differential distribution of size classes in each area. Considering the opportunistic foraging behavior of these crabs, differences in diet between the Southern branch and other areas of the estuary probably reflect food availability in each particular habitat (Baeta et al., 2006). Nereididae and C. crangon were more consumed in the Southern branch of the estuary than near the mouth and in the Northern branch. Abrantes et al. (1999) refers that the distribution of Nereididae can be correlated with warmer waters, higher salinity and higher abundance of fine particles and organic matter. Pardal et al. (1993), in a study on Polychaeta populations in the Mondego estuary, also stressed that the distribution of these animals appeared to be primarily controlled by physicochemical conditions like sediment type, salinity and currents. The Southern branch presents lower hydrodynamic conditions, less influence of river discharges and higher salinity (Chainho et al., 2006), and higher abundances of N. diversicolor were found there in comparison to the Northern branch (unpublished data). Therefore, higher consumption of Nereididae by C. maenas in this area of the estuary might be related with higher abundance of these invertebrates in the Southern branch. References to C. crangon in literature suggest that this species also prefers areas with finer sediments (most adequate to its burrowing habits) without the influence of strong currents to avoid the displacement to less favorable areas (Pinn & Ansell, 1993; Calado & Narciso, 2002). Therefore, highest consumption of this species in the same area might have an identical reason as for Nereididae. C. maenas diet did not differ markedly along the year and seasonal variations in the diet possibly reflected seasonal fluctuations in the abundance of certain food items corroborating Martins (1995) and Baeta et al. (2006) findings. In the present study Nereididae was more frequent in C. maenas stomachs in winter and spring, coinciding with higher biomasses registered for this family in the Mondego estuary (unpublished data). In Canal de Mira, a branch of Ria de Aveiro (Portugal) with environmental conditions similar to the Mondego estuary, densities of Nerididae increased from late winter through spring (Abrantes et al., 1999). In the estuary of ythan, Scotland, Chambers & Milne (1975) also found higher densities of Nereididae in that period of the year. Seasonal differences were also found for the intake of Cardiidae, Scrobiculariidae and unidentified Bivalvia. These

differences may be related to the difficulty of identifying preys in the stomach contents, since they are previously crushed and fragmented by the crabs’ claws (Pestana, 1997). This could be confirmed by the high percentage of unidentified bivalves and also by the fact that no seasonal significant differences were found for consumption of total bivalves. Cardoso et al. (2004) and Baeta et al. (2005) reported the occurrence of spring macroalgal blooms at the Mondego estuary. A tendency for a higher consumption of Algae by C. maenas in spring was observed but that variation was not statistically significant. Higher similarity in the species diet in summer and autumn was probably related to the occurrence of a severe flood in the winter of 2000/01, which changed significantly prey availability during winter and spring (Chainho et al., 2006). This study emphasizes the plasticity of C. maenas concerning the use of the available resources, both spatially and seasonally, but also that different size classes have different diets, reducing the potential occurrence of intraspecific competition. On the other hand, this crab seems to have an important role in the estuarine food webs, not only because it feeds on surface and subsurface organisms, with different feeding strategies, but also because it is preyed by fish (Jorge et al., 2002) and birds (Lopes et al., 2002). The dietary importance of bivalves for C. maenas in the Mondego estuary substantiates the reputation of the green crab as a potential pest for bivalve fisheries (Elner, 1981). Furthermore, in some specific areas it may be an indirect and direct competitor of young lobsters and other crab species (McDonald et al., 2001; Walton et al., 2002; yamada et al., 2005). No significant differences were found in the diet of C. maenas between areas where the species is endemic and an invader, being major variations apparently related to particular characteristics of each location. Therefore, it seems that its impact in newly colonized systems will depend on the natural abiotic and biotic conditions. The understanding of the feeding habits of C. maenas might be very important to prevent future impacts of this species on local communities where this crab is introduced. Modelling the distribution and abundance of this species could also be very interesting, as a support for predicting areas that can be affected in a near future (Smallegange et al., 2009). Acknowledgments The field work was undertaken with the financial support of the project “Methodological Basis for Water Quality Analysis in Portuguese Rivers and Estuaries (QUERE)” funded by the Instituto do Ambiente (IA). This work was also financially supported by the RECONNECT project (PTDC/MAR/64627/2006) funded by FCT and two grants


to M.L.C. (SFRH/BPD/34741/2007) and P.C. (SFRH/BPD/ 29579/2006) from FCT and ESF in the aim of the III European Community Support Framework.

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