Journal of Experimental Marine Biology and Ecology 368 (2009) 88–93

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Journal of Experimental Marine Biology and Ecology

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Cannibalistic interactions in two co-occurring decapod : Effects of density, food, alternative prey and habitat

Valter Amaral a,b,⁎, José Paula a, Stephen Hawkins b,1, Stuart Jenkins b,1 a Laboratório Marítimo da Guia, Faculdade de Ciências da Universidade de Lisboa, Avenida Nossa Senhora do Cabo 939, 2750-374 Cascais, Portugal b Marine Biological Association of the UK, Citadel Hill, Plymouth, PL1 2PB, UK article info abstract

Article history: Cannibalism is a potentially important factor in the regulation of populations in a range of habitats. The Received 19 February 2008 intensity of this biotic factor may be determined by both intra and interspecific interactions. Received in revised form 22 October 2008 and platycheles are two co-occurring decapods on Atlantic rocky shores. In laboratory mesocosms, Accepted 24 October 2008 we investigated intra and intersize class cannibalistic and interspecific predatory behaviours in those species. We addressed the effects of prey and predator densities, food, starvation, alternative prey and habitat type. Keywords: No agonistic behaviour was noted in P. platycheles, suggesting a non-aggressive co-existence between Agonistic behaviour Cancer pagurus gregarious individuals. Predation of C. pagurus on P. platycheles was intense, possibly accounting for the Cannibalism spatial segregation observed in the natural environment. Cannibalism among C. pagurus juveniles was low Mesocosms and only on vulnerable prey (i.e. at moulting), suggesting a non-aggressive co-existence among juveniles. Mutual interference However, intersize class cannibalism in C. pagurus was intense (ontogenetic shift), possibly reflecting the juvenile-adult segregation in the natural environment. Prey and predator densities, food and habitat type strongly influenced this behaviour. Possible interference among cannibals was noted, with lower prey consumption at high predator density. Food supply alone had more effect on cannibalistic rate than did alternative prey (P. platycheles) and predator starvation. Structurally complex habitats (small pebble and Fucus serratus habitats) yielded higher prey survival than the sandy habitat, and the behaviours of both prey and cannibals reflected the small-scale spatial distribution of individuals in the wild. Intersize class cannibalism and interspecific agonistic relationships may account for the intertidal distribution of species at low tide. © 2008 Elsevier B.V. All rights reserved.

1. Introduction Determining the occurrence and magnitude of cannibalism, among, and on, juvenile stages may thus be of crucial importance in under- Cannibalism is a potentially important factor in population standing population dynamics. regulation and in the generation of fluctuations in population Predator-prey size ratio, food availability, predator starvation, structure and stock-recruitment relationships in both terrestrial and alternative prey, habitat type and interspecific interactions may marine systems (Fox, 1975; Polis, 1981; Sainte-Marie and Lafrance, significantly affect the occurrence of cannibalism and its intensity in 2002; Moksnes, 2004; Wise, 2006). It is generally recognized as a marine environments (e.g. Polis, 1981; Smith and Reay, 1991; Moksnes density-dependent event, capable of population regulation through et al., 1998). Our understanding of cannibalistic behaviour and in- both intra and intersize class cannibalism (Fox, 1975; Polis, 1981; tensity mainly results from combined information gathered from Smith and Reay, 1991; Moksnes, 2004). In marine environments, intra different studies, each focusing on a few environmental factors, and and intersize class cannibalism can be major sources of post- many times using distinct experimental designs. This study evaluates settlement mortality in fish and marine benthic invertebrates, the effects of prey and predator densities, food availability, predator especially , which aggregate in nursery habitats (Moksnes starvation, alternative prey and habitat type on juvenile cannibalistic et al., 1997; Bystrom et al., 2003; Wahle, 2003; Moksnes, 2004). interactions in two coexisting decapod species, the edible crab Cancer pagurus (L.) and the broad-clawed Porcellana platycheles (Pennant, 1777). ⁎ Corresponding author. Laboratório Marítimo da Guia, Faculdade de Ciências da Cancer pagurus is a large and active omnivorous predator inha- Universidade de Lisboa, Avenida Nossa Senhora do Cabo 939, 2750-374 Cascais, biting hard and soft substrata from the low intertidal to ~100 m depth, Portugal. Tel.: +351 214869211; fax: +351 214869720. in the Northeastern Atlantic and Mediterranean Sea (Ingle, 1980; E-mail address: [email protected] (V. Amaral). 1 Present address: School of Ocean Sciences, Bangor University, Menai Bridge, Lawton, 1989). In addition to its importance in coastal food webs it is Anglesey, LL59 5EY, UK. also an important commercial species; there are important fisheries

0022-0981/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2008.10.025 V. Amaral et al. / Journal of Experimental Marine Biology and Ecology 368 (2009) 88–93 89 for C. pagurus and attempts have been made to rear it (Woll et al., ranges dominated the low intertidal, and were used as different habitats 2006). Strong cannibalistic behaviour has been reported for several in the experiments: small and large pebbles, 8-12 and 16-22 cm long, decapod species including (Moksnes, 2004), Calli- respectively. Fronds of F. serratus were selected to fitmesocosmheight. nectes sapidus (Moksnes et al., 1997) and Cancer magister (Fernandez, 1999). Interestingly, avoidance of dead conspecifics has also been 2.2. and substrata maintenance reported for several others, including C. pagurus (Hancock, 1974; Chapman and Smith, 1978; Zimmerfaust et al., 1985; Richards, 1992). were kept in flow-through 120 L containers with natural This raises questions as to the cannibalistic behaviour of C. pagurus, seawater and fed fresh blue , fish and for at least 5 d which to the authors' knowledge, has not yet been consistently before being used. Despite different feeding habits, the same food was investigated (Chapman and Smith, 1978; Lawton, 1989). given to each species to standardise conditions and hence allow direct Porcellana platycheles is a conspicuous small, mainly micropha- comparison of results. Photoperiod, water temperatures and salinities gous, filter feeder, occurring in the low intertidal fringe from the were similar to those in the mesocosms (see below). Adults Shetlands to the Canary Islands, and the Mediterranean Sea (Smaldon, maintained 3 d without food were considered “starved”. Animals 1972; Stevcic, 1988). Evidence of alternative macrophagic feeding has undergoing moulting were discarded. Substrata were rinsed with been reported, including the presence of sand grains and polychaeta seawater and cleaned of epiphytes and fauna prior to use. Sand and setae in stomach contents (Stevcic, 1988). Furthermore, their pebbles were additionally sun-dried. characteristic large chelipeds suggest that aggressive behaviour may occur among conspecifics, but information is lacking. 2.3. Mesocosms Cancer pagurus and P. platycheles co-occur in areas of fucoid– covered boulders and pebbles in the low intertidal and shallow Mesocosms were small flow-through rectangular tanks with round subtidal zones, although individuals of C. pagurus over two years of corners (0.27×0.27×0.18 m; 13 L), provided with a 2 cm deep layer of age tend to live at greater depths (Smaldon, 1972; Ingle, 1980; Lawton, sand, which allowed burrowing of juvenile crabs. Mussel shell debris 1989; Sheehy and Prior, 2008). Little data exist on interspecific was added to provide a more natural environment. Running interactions, although C. pagurus predation on P. platycheles has been (~1.5 L min-1) natural, filtered (b750 μm) seawater from Plymouth noted in laboratory experiments (Lawton, 1989). Sound entered at the bottom and left each tank at the surface. Water We conducted a series of laboratory, mesocosm experiments to temperature was 16±1 °C and salinity 34±2. Photoperiod was 16 h light: study juvenile cannibalistic interactions in C. pagurus and P. platy- 8 h dark, provided by 2 white florescent tubes (~80 lux), approximating cheles. Specifically, we addressed: (1) Is intrasize class cannibalism in natural conditions in southwest Britain at the time of the experiments. juvenile C. pagurus determined by density, food supply or lack of alternative prey? (2) Is intrasize class cannibalism and predation in 2.4. General experimental procedures juvenile P. platycheles dependent on density and food supply? (3) Can intersize class cannibalism be controlled by prey (juvenile) and Mesocosm experimentation was conducted at the Marine Biolo- predator (adult) densities in each species? (4) And, what are the gical Association, Plymouth, UK (50°18-22′N, 4°5-13′W). All experi- effects of food, alternative prey and habitat type on such cannibalistic ments had a full factorial design with a replication level of 3. The behaviour? animal densities used for experimentation are considered in relation to each other, and thus the terms low, medium and high are relative. In 2. Materials and methods all cases low, medium and high densities of juvenile crabs were 2, 4 and 6, and 2, 6 and 18 ind.tank-1 of C. pagurus and P. platycheles, 2.1. Animal and substrata collection respectively, although when juvenile density was not a factor, the medium juvenile density was used. Animals and substrata were collected from May to June 2007 (spring Unless stated otherwise, excess food (fresh blue mussel, fish and season), from four coastal sites around Plymouth, UK: Mount Batten, shrimp) was provided daily, scaled to crab density so foraging Jenny Cliff and Heybrook Bay in Plymouth Sound, and Wembury Bay in opportunities were equal; uneaten remains were siphoned out daily. the adjacent coast. These sites are characterized by platforms of Adult predators were allowed to adapt to mesocosms for 8 h prior to laminated rocks with uneven series of gaps that create numerous ridges prey addition. No control of moulting was made during trials, so its and pools where beach material, from sand to boulders, accumulate effects could be as natural as possible. The duration of experimental (M.B.A., 1957). There is a rich algal flora, particularly in the low shore, trials (Table 1) was set pragmatically based on preliminary work, where Fucus serratus dominates (M.B.A., 1957). allowing time for the studied effects to be noted and avoiding Cancer pagurus and P. platycheles occurred spatially together in the unnecessary stress and death on individuals. Experiments on intrasize low intertidal and shallow subtidal areas, and were most abundant class cannibalism had two different durations: 5 days for experiments under pebbles, particularly under F. serratus. The natural density of each involving interspecific interactions and 15 d for those evaluating crab species at low water was estimated from 15 quadrats (0.5×0.5 m), effects of density. Preliminary experiments on intersize class canni- randomly deployed in the low intertidal. Individuals encountered in balism were stopped after 6 h of no prey mortality and appendage these surveys were retained for laboratory experiments. Whilst this loss, yielding a total trial duration of 80 h. Throughout all experiments, approach lacks information on densities during high water, these data animal behavior was observed to provide insight into the mechanisms were used as an approximation to inform experiments. leading to mortality and appendage loss and on termination of each Juvenile C. pagurus, between 20 and 27 mm carapace width (CW), trial, habitats were carefully removed from the tanks and surveyed for corresponding to 1+ yr crabs (Sheehy and Prior, 2008), and late juveniles animals. Animals and substrata were used only once. of P. platycheles, between 5 and 7.5 mm CW (Smaldon, 1972), were most abundant and were selected for experimentation. Adults from 85 to 2.5. Experiments 95 mm and 12 to 13.5 mm CW of C. pagurus and P. platycheles, respectively, were also retained. Only active and undamaged indivi- 2.5.1. Intrasize class cannibalism in C. pagurus juveniles duals, free of parasites and in intermoult (evaluated by hardness of the In order to assess the density dependent nature of cannibalism in carapace) were collected. C. pagurus and the way it is mediated by availability of food and/or In order to replicate the natural environment, sieved (b1.0 mm) alternative prey, two experiments were conducted. The first experi- beach sand was used in experimental mesocosms. Pebbles of two size ment (Exp.1) tested the effects of juvenile density (low, medium, high) 90 V. Amaral et al. / Journal of Experimental Marine Biology and Ecology 368 (2009) 88–93

Table 1 Table 2 Summary of all experiments conducted Results of ANOVA analyses on the effects of density on intrasize class cannibalism as proportional mortality on C. pagurus (Exp.1) and P. platycheles (Exp.3) Factors Exp. Sp. Dens. Food Alt. prey Pred. Starv. Habitat Treat. Dur. C. pagurus P. platycheles 1 C. pagurus L/M/H Y - - - - 3 15d df MS FpdfMS Fp 2 C. pagurus M Y/N Y/N - - - 4 5d Density 2 0.04 1.26 0.35 2 0.003 1.0 0.42 3 P. platycheles L/M/H Y - - - - 3 15d Error 6 0.03 6 0.003 4 P. platycheles M Y/N - Y/N - - 4 5d 5 C. pagurus L/M/H Y - Consp. - - 6 80h 1/2 6 P. platycheles L/M/H Y - Consp. - - 6 80h 2.6. Statistical analyses 1/2 7 C. pagurus M Y/N - Consp. 1 Y/N - 4 80h 8 C. pagurus M Y/N Y/N Consp. 1 - - 4 80h Proportional mortality (number of missing crabs / total number) 9 C. pagurus M Y/N - Consp. 1 - S/Ps/ 8 80h and appendage loss (number of appendage missing / total number) Pl/F were used as dependent variables in ANOVA models on intrasize class All experiments had a full factorial design. For each experiment is indicated the crab cannibalism and interspecific predation. ANOVA models were also species focused, the factors under test, the total number of treatments and the duration used on intersize class cannibalism, with proportional prey mortality of the experiment. Legend of column heads: Exp. – Experiment; Sp. – Species; Dens. – (number of prey missing / total number) as the dependent variable. – – – Density; Alt. prey Alternative prey; Pred. Predators; Starv. Predator starvation; Experimental factors (density, food, alternative prey, predators, Treat. – Treatments; Dur. – Duration. Legend of column cells: L/M/H – Low, Medium, High; Y/N – Yes, No; Consp. – Conspecifics; S/Ps/Pb/F – Sand, Small pebbles, Large predator starvation and habitat) were used as independent variables pebbles, F. serratus. and were considered fixed throughout. Cochran's tests revealed homoscedasticity of variances in all cases (Sokal and Rohlf, 1995). A posteriori comparisons were done by Tukey's HSD and Dunnett's and food (yes, no) over a 15 d period, under the hypothesis that tests. STATISTICA software, v. 6 (StatSoft) was used. cannibalism was more intense at high density. The second (Exp.2) determined rates of cannibalism at a constant juvenile density whilst 3. Results varying food availability (yes, no) and alternative prey (P. platycheles at -1 6 juvenile ind.tank , versus none) (Table 1). The hypothesis tested 3.1. Intrasize class cannibalism in C. pagurus: effects of density, food and was that cannibalism was more intense when no food or alternative alternative prey prey was supplied. Although agonistic behaviour, characterized by brief fighting 2.5.2. Intrasize class cannibalism and predation in P. platycheles events (b10 s), was noted several times, cannibalism was relatively Experiment 1 was repeated for P. platycheles (Exp.3, Table 1). We low and was independent of density (Cochran's C=0.95, df =1,pN0.26) tested the hypothesis that predation of P. platycheles by juvenile (Exp.1). Only crabs that moulted were cannibalized and overall, C. pagurus is mediated by the presence of alternative food in a 5 d proportional mortality was similar among the different density experiment by varying the presence of the potential predator (yes, no) treatments: 17, 0 and 21% at low, medium and high densities, and food (yes, no) (Exp.4, Table 1). respectively (ANOVA Tukey's test, pN0.3) (Table 2). The presence of food, and alternative prey had no effect on cannibalistic interactions, 2.5.3. Intersize class cannibalism: effects of prey and predator densities, and mortality remained below 19% in all treatments (Cochran's C=0.5, food, alternative prey and habitat type df=1, pN0.99; Exp.2, Table 3). No appendage loss was found in either Intersize class cannibalism was assessed in both target species in experiment in live crabs. five experiments. Initially factorial experiments were run for both C. pagurus (Exp.5) and P. platycheles (Exp.6) to evaluate whether 3.2. Intrasize class cannibalism and predation in P. platycheles: effects of intersize class cannibalism was dependant on both prey and predator density and food densities. The hypothesis under test was that intersize class cannibalism was higher at high prey (juveniles) and predator densities. Juvenile In P. platycheles observations showed some agonistic behaviour; density (low, medium and high) and predator density (1 or 2) were display of chelipeds was noted on some occasions, but did not result in varied and mortality assessed after 80 hours. Control trials were ran fighting. Virtually no cannibalism was detected (Exp.3); mortality without predators, and average results subtracted to other treatments. rates were zero at low and high densities, and ~6% at medium density, No intersize class cannibalism was detected in P. platycheles (see Results), and so no further experiments were conducted on this species. The extent to which food availability (yes, no) and predator state Table 3 (starved, not starved) affected intersize class cannibalism in C. pagurus Results of two-way ANOVA analyses on the effects of food supply and presence of other was examined in Experiment 7. We hypothesized that starved crab species on intrasize class cannibalism as proportional mortality and appendage predators yielded higher cannibalism rates, especially when no food loss on C. pagurus (Exp.2) and P. platycheles (Exp.4) was supplied. df Proportional mortality Proportional appendage loss The effects of the presence of alternative prey (P. platycheles at 6 MS Fp MS Fp juvenile ind.tank-1, versus none), together with food availability (yes, no) C. pagurus in intersize class cannibalism in C. pagurus were investigated in Food (A) 1 0.01 0.50 0.50 0.001 0.08 0.78 Experiment 8. Specifically, the hypothesis was that the presence of Alternative prey (B) 1 0.05 4.50 0.07 0.48 4.75 0.06 alternative prey resulted in lower intersize class cannibalism, especially A×B 1 0.01 0.50 0.50 0.01 1.06 0.33 in the absence of food. Error 8 0.01 0.01

Finally, the hypothesis that cannibalism is more important where P. platycheles refugia are sparse, was tested by varying habitat type from simple to Food (A) 1 0.17 16.76 b0.01 0.11 10.96 b0.05 increasingly complex (sand, small pebbles, large pebbles and F. serratus). Predator (B) 1 0.42 41.71 b0.001 0.55 56.12 b0.001 The availability of food (yes, no) was also manipulated to determine to A×B 1 0.10 9.70 b0.05 0.05 5.40 b0.05 what extent this mediated the level of cannibalism. Error 8 0.01 0.01 V. Amaral et al. / Journal of Experimental Marine Biology and Ecology 368 (2009) 88–93 91

afterwards, although not significantly (ANOVA Tukey's test, pN0.5) (Fig. 2A). With two predators, prey mortality was inversely density- dependent, but only decreased significantly from low to medium prey density (ANOVA Tukey's test, pb0.05) (Fig. 2A). Prey consumption was significantly affected by interaction of prey and predator densities (Cochran's C=0.8, df =1, pN0.99; ANOVA: F=39.8, df=2,17, pb0.001) (Exp.5). With one predator, consumption increased significantly from low to medium prey density (ANOVA Tukey's test, pb0.001), although not further on (ANOVA Tukey's test, pN0.6) (Fig. 2B). When two predators were present, no difference in prey consumption was noted among prey densities (ANOVA Tukey's test, pN0.9) (Fig. 2B). Non-aggressive display of chelipeds among P. platycheles was noted in some occasions, but no mortality and appendage loss were noted (Exp.6). Statistical tests were thus not conducted. Animal behaviour in Exp.7 and 8 was similar to that of Exp.4 and Fig. 1. Results of the effects of C. pagurus predator (yes, no) and food (yes, no) on 5. Mortality of juvenile C. pagurus was significantly affected by inter- survival, as proportional mortality, of P. platycheles (Exp.4). Error bars represent SE, being absent when SE=0. action of food with predator starvation (Cochran's C=0.5, df =1, pN0.99) (Table 4) (Exp.7). All juveniles were killed by starved predators to which no food was supplied (100%, ANOVA Dunnett's and ANOVA showed no effect of juvenile density (Cochran's C=1; test, pb0.001). The presence of P. platycheles, as alternative prey ANOVA Tukey's test, pN0.4) (Table 2). Again, at the end of the (Exp.8), significantly decreased mortality of juvenile C. pagurus (from experiment, no appendages were missing in live crabs. 58 to 13%; Cochran's C=0.33, df=2, pN0.99, ANOVA Tukey's test, Juvenile individuals of C. pagurus attacked P. platycheles based on pb0.001), with or without food (Table 4). encounter, but not all encounters resulted in attacks (Exp.4). In all In the habitat experiment (Exp.9), juveniles sought refuge under observed attacks, juvenile P. platycheles resisted by exposing their pebbles of each size and by grabbing to F. serratus fronds higher in the chelipeds, which sometimes resulted in attack failure and escape. mesocosms. Adults were observed to find refuge (other than burrowing) Fighting events between C. pagurus juveniles were less common than in only under large pebbles. In some occasions, F. serratus fronts restrained Exp.1 and 2. Mortality rates of P. platycheles were highest (67%) in the movements of adults, but not of juveniles, by becoming embraced presence of juvenile C. pagurus predators and absence of food (Cochran's around walking appendices. Adults attacked conspecific juveniles based C=0.52, df =2, p N0.99; ANOVA Tukey's test, p b0.01) (Table 3). on encounter, but also through ambush tactics, by rising suddenly from Appendage loss was highest when predators were present, with and without food supply (35 and 68%, respectively; Cochran's C=0.44, df=3, pN0.86; ANOVA Tukey's test, pb0.05 in all cases) (Fig. 1).

3.3. Intersize class cannibalism: effects of prey and predator densities, food, alternative prey and habitat type

Adult C. pagurus attacked conspecific juveniles based on encounter. All attacks observed were successful, resulting in prey death or appendage loss. Intersize class cannibalism was common, and prey mortality was significantly affected by interaction of prey and predator densities (Cochran's C=0.47, df =3, pN0.99; Table 4) (Exp.5). With one predator, prey mortality increased significantly from low to medium prey density (ANOVA Tukey's test, pb0.01) decreasing

Table 4 Results of two-way ANOVA analyses on the effects of prey and predator densities, predator starvation and food supply, alternative prey and food supply and habitat type and food supply on intersize class cannibalism in C. pagurus, as proportional prey mortality (Exp.5, 7, 8 and 9)

Factor Experiment 5 Experiment 7 Prey (A) & predator (B) densities Starvation (A) & food (B) df MS Fp dfMS Fp A 2 0.01 0.51 0.61 1 0.05 4.50 b0.07 B 2 0.11 5.82 b0.05 1 0.42 40.50 b0.001 A×B 4 0.23 11.54 b0.001 1 0.13 12.50 b0.01 Error 18 0.02 8 0.01

Factor Experiment 8 Experiment 9 Alternative prey (A) & food (B) Habitat type (A) & food (B) df MS Fp dfMS Fp A 1 0.63 40.33 b0.001 3 0.35 22.44 b0.001 B 1 0.05 3.00 0.12 1 0.42 2.67 0.12 Fig. 2. Results of the effects of predator (1, 2) and prey densities (low, medium, high) on A×B 1 0.01 0.33 0.58 3 0.09 5.78 b0.01 intersize class cannibalism of C. pagurus (A) as proportional prey mortality and (B) prey Error 8 0.02 16 0.02 consumption rates (Exp.6). Error bars represent SE, being absent when SE=0. 92 V. Amaral et al. / Journal of Experimental Marine Biology and Ecology 368 (2009) 88–93

juvenile size classes have been reported in Cancer borealis (Richards, 1992), the opposite pattern is common among intertidal crab populations (e.g. C. magister (Fernandez, 1999), C. sapidus (Moksnes et al., 1997), C. maenas (Moksnes, 2004)). The reasons for the stark contrast in behavior among similar species is not clear, but is likely to have implications for species-specific population dynamics.

4.2. Interspecific juvenile predation

Despite the low intensity of juvenile cannibalism in each species, juvenile C. pagurus preyed heavily on P. platycheles, especially in the absence of food. The design of this experiment means that addition of predators increased stock-density (a potential confounding factor). In theory, enhanced density only of P. platycheles could have led to similar levels of mortality. However, output from Experiment 3, where P. platy- cheles were maintained at a range of densities from low to high, suggests Fig. 3. Results of the effects of habitat type (sand, small pebbles, big pebbles, F. serratus) that this is not the case. Indeed the pattern of mortality (only P. platy- and food (yes, no) on intersize class cannibalism of C. pagurus as proportional prey cheles juveniles were eaten) shows that C. pagurus juveniles are an mortality (Exp.9). Error bars represent SE, being absent when SE=0. effective predator of this species. These results are in accordance with those reported by Lawton (1989), also from laboratory conditions. On under pebbles. The majority of the attacks observed in F. serratus and the shore, few specimens, usually less than 3, of each species sometimes small pebble habitats was not successful, and prey often escaped occurred under the same pebbles and boulders, but not at high densities without injury. Mortality of C. pagurus juveniles was affected by (more than 5 individuals of each species). At low tide, juvenile C. pagurus interaction of habitat type with food supply (Cochran's C=0.17, df=5, were most abundant near the low water level, while P. platycheles were pN0.99) (Table 4). With no food supply, a higher proportion of juveniles abundant in the mid-low intertidal. This study suggests that inter- (~67%) were cannibalized in sand and large pebble habitats (ANOVA specific predation may account for the spatial distributions on the shore, Tukey's test, pN0.99), than in F. serratus and small pebble habitats (b17%, but extrapolation of mesocosm results to natural distribution patterns ANOVA Tukey's test, pb0.05) (Fig. 3). When food was supplied, the must be viewed with caution. F. serratus habitat provided the best survival rates of juvenile C. pagurus (ANOVA Tukey's test, pb0.05), yielding 100% survival (Fig. 3). 4.3. Intersize class cannibalism

4. Discussion There was no evidence of cannibalism between different size classes of P. platycheles. The characteristic large chelipeds thus do not seem to be Cannibalism has been suggested as the main cause of juvenile involved in aggressive behaviour between conspecifics, but display of mortality in size-structured populations of crabs, and hence is likely to chelipeds without fighting suggests that they could serve mating affect several aspects of population dynamics (Moksnes et al., 1997; purposes. Under laboratory conditions, therefore, P. platycheles appears Fernandez, 1999; Moksnes, 2004). In this study, several factors under- to be a non-aggressive species and in the field, natural distributions lying cannibalistic behaviours and interspecific interactions in juvenile support this conclusion. Larger P. platycheles were always found in crabs were addressed in simulations of natural conditions in laboratory association with juvenile conspecifics on the shore, frequently at high mesocosms. Such an approach benefits from tight control of experi- densities, apparently reflecting a non-aggressive and gregarious nature. mental factors but clearly will be affected by an unnatural environment. In contrast, cannibalism in C. pagurus was intense between different One such factor, the density at which crabs are stocked, will have a size classes, with strong dependence on prey and predator densities. significant impact on the experimental results. We sampled the natural These results somehow contradict the distinct rejection behavior of environment at low tide to assess natural variation in crab densities. conspecifics by adult C. pagurus reported by Lawton (1989). Never- Cancer pagurus juveniles of 1+ yr probably remain between tidal theless, a similar ontogenetic change, from low to high intensity marks until later stages (N2+ yr), when subtidal/intertidal migrations cannibalism, is known for the congener C. borealis,(Richards, 1992). In occur (Sheehy and Prior, 2008). This is common in the ontogeny of the natural environment, adult C. pagurus are mainly found subtidally, intertidal crab populations, including the congener C. magister (McMil- and more frequently in the presence of N2+ yr than smaller juveniles lan et al., 1995; Holsman et al., 2006)andC. maenas (Hunter and Naylor, (Ingle, 1980; Lawton, 1989; Sheehy and Prior, 2008). Just as interspecific 1993; Burrows et al., 1999). Porcellana platycheles only undergo limited predation may be a factor in determining spatial patchiness in the migrations inside the habitat, thus generally remaining between tidal distributions of P. platycheles and C. pagurus juveniles on the shore, marks the entire life (Stevcic, 1988). Hence, experimentation with the intersize class cannibalism may act in the same manner for different crab densities obtained at low tide allowed realistic, natural levels of cohorts of C. pagurus. interactions to be assessed. Mortality of C. pagurus juveniles by a single adult predator increased with prey density, possibly indicating saturation at high prey density, 4.1. Intrasize class cannibalism while with two, it was inversely density-dependent. A similar shift in predator responses to prey density has been reported for blue crabs as a No evidence of agonistic behaviour was detected in P. platycheles, result of a decrease in habitat heterogeneity, leading to higher encounter and cannibalism between juvenile C. pagurus was always low (only rates (Lipcius and Hines, 1986; Moksnes et al., 1997). In our study, the moulting crabs were cannibalized). In the wild, juveniles of each addition of a second predator could have resulted in higher prey- species were often found at high densities under respective rocks, predator encounter rates, leading to a similar effect to that of reduced suggesting a passive conspecific existence. Lack of aggressive interac- habitat heterogeneity (Hassel, 1978). Prey consumption did not tions among juveniles allows gregarious behaviour, with all the increased proportionally with increased predator density. Dependence benefits that this entails. For example, increased vigilance reducing of prey consumption on predator intensity suggests the occurrence of response time to a predator attack (Zimmerfaust et al., 1985; Moksnes mutual interference among adult C. pagurus (Moksnes et al., 1997; and Heck, 2006). Although similar low levels of cannibalism within Fernandez, 1999; Moksnes, 2004). V. Amaral et al. / Journal of Experimental Marine Biology and Ecology 368 (2009) 88–93 93

Although predator starvation had no effect on the level of predation References of conspecifics, greater availability of food did diminish prey mortality. Food availability is for many organisms the most important factor Burrows, M.T., Kawai, K., Hughes, R.N., 1999. Foraging by mobile predators on a rocky shore: underwater TV observations of movements of blennies Lipophrys pholis and affecting the intensity of cannibalism (Fox,1975; Polis,1981; Smith and crabs Carcinus maenas. Mar. Ecol. Prog. Ser. 187, 237–250. Reay, 1991; Wise, 2006). In fact, the level of cannibalism was also Bystrom, P., Persson, L., Wahlstrom, E., Westman, E., 2003. Size- and density-dependent fi significantly reduced by P. platycheles as alternative prey. Although habitat use in predators: consequences for habitat shifts in young sh. J. Anim. Ecol. 72 (1), 156–168. adding P. platycheles adds a potentially confounding effect (increased Chapman, C.J., Smith, G.L., 1978. 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Fish. 1, 41–64. validation of mesocosm results and further clarify the role of intra and Sokal, R.R., Rohlf, F.J., 1995. Biometry: the principles and practice of statistics in interspecific aggressive interactions on the dynamics of intertidal crab biological research, 3rd edition. W. H. Freeman and Co., New York. Stevcic, Z., 1988. Autecological investigations of the porcelain crab Porcellana platycheles communities. (Pennant) (, ) in the Rovinj Area (northern Adriatic). Crustaceana 55, 242–252. Acknowledgements Wahle, R.A., 2003. Revealing stock-recruitment relationships in and crabs: is experimental ecology the key? Fish. Res. 65 (1-3), 3–32. Wise, D.H., 2006. Cannibalism, food limitation, intraspecific competition and the We are indebted to A. Silva for her help with crab collection. We regulation of spider populations. Annu. Rev. Entomol. 51, 441–465. acknowledge a PhD grant to V.A. (SFRH/BD/10471/2002) funded by Woll, A.K., van der Meeren, G.I., Tuene, S., 2006. Quality improvement by feeding wild- – Fundação para a Ciência e a Tecnologia. We thank four Hanonymous caught edible crab (Cancer pagurus L.): a pilot study. Aquac. Res. 37 (14), 1487 1496. Zimmerfaust, R.K., Tyre, J.E., Case, J.F., 1985. Chemical attraction in the spiny , referees for critical comments that greatly improved the manuscript. Panulirus interruptus (Randall), and its probable ecological significance. Biol. Bull. [RH] 169 (1), 106–118.