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

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

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Journal of Experimental Marine Biology and Ecology 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 / j e m b e

Cannibalistic interactions in two co-occurring decapod species: Effects of density, food, alternative prey and habitat Valter Amaral a,b,⁎, José Paula a, Stephen Hawkins b,1, Stuart Jenkins b,1 a b

Laboratório Marítimo da Guia, Faculdade de Ciências da Universidade de Lisboa, Avenida Nossa Senhora do Cabo 939, 2750-374 Cascais, Portugal Marine Biological Association of the UK, Citadel Hill, Plymouth, PL1 2PB, UK

a r t i c l e

i n f o

Article history: Received 19 February 2008 Received in revised form 22 October 2008 Accepted 24 October 2008 Keywords: Agonistic behaviour Cancer pagurus Cannibalism Mesocosms Mutual interference Porcellana platycheles

a b s t r a c t Cannibalism is a potentially important factor in the regulation of populations in a range of habitats. The intensity of this biotic factor may be determined by both intra and interspecific interactions. Cancer pagurus and Porcellana platycheles are two co-occurring decapods on Atlantic rocky shores. In laboratory mesocosms, 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. No agonistic behaviour was noted in P. platycheles, suggesting a non-aggressive co-existence between gregarious individuals. Predation of C. pagurus on P. platycheles was intense, possibly accounting for the spatial segregation observed in the natural environment. Cannibalism among C. pagurus juveniles was low and only on vulnerable prey (i.e. at moulting), suggesting a non-aggressive co-existence among juveniles. 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 crab species at low tide. © 2008 Elsevier B.V. All rights reserved.

1. Introduction Cannibalism is a potentially important factor in population regulation and in the generation of fluctuations in population structure and stock-recruitment relationships in both terrestrial and marine systems (Fox, 1975; Polis, 1981; Sainte-Marie and Lafrance, 2002; Moksnes, 2004; Wise, 2006). It is generally recognized as a density-dependent event, capable of population regulation through both intra and intersize class cannibalism (Fox, 1975; Polis, 1981; Smith and Reay, 1991; Moksnes, 2004). In marine environments, intra and intersize class cannibalism can be major sources of postsettlement mortality in fish and marine benthic invertebrates, especially crabs, which aggregate in nursery habitats (Moksnes et al., 1997; Bystrom et al., 2003; Wahle, 2003; Moksnes, 2004).

⁎ Corresponding author. Laboratório Marítimo da Guia, Faculdade de Ciências da Universidade de Lisboa, Avenida Nossa Senhora do Cabo 939, 2750-374 Cascais, Portugal. Tel.: +351 214869211; fax: +351 214869720. E-mail address: [email protected] (V. Amaral). 1 Present address: School of Ocean Sciences, Bangor University, Menai Bridge, Anglesey, LL59 5EY, UK. 0022-0981/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2008.10.025

Determining the occurrence and magnitude of cannibalism, among, and on, juvenile stages may thus be of crucial importance in understanding population dynamics. Predator-prey size ratio, food availability, predator starvation, alternative prey, habitat type and interspecific interactions may significantly affect the occurrence of cannibalism and its intensity in marine environments (e.g. Polis, 1981; Smith and Reay, 1991; Moksnes et al., 1998). Our understanding of cannibalistic behaviour and intensity mainly results from combined information gathered from different studies, each focusing on a few environmental factors, and many times using distinct experimental designs. This study evaluates the effects of prey and predator densities, food availability, predator starvation, alternative prey and habitat type on juvenile cannibalistic interactions in two coexisting decapod species, the edible crab Cancer pagurus (L.) and the broad-clawed porcelain crab Porcellana platycheles (Pennant, 1777). Cancer pagurus is a large and active omnivorous predator inhabiting hard and soft substrata from the low intertidal to ~100 m depth, in the Northeastern Atlantic and Mediterranean Sea (Ingle, 1980; Lawton, 1989). In addition to its importance in coastal food webs it is also an important commercial species; there are important fisheries

V. Amaral et al. / Journal of Experimental Marine Biology and Ecology 368 (2009) 88–93

for C. pagurus and attempts have been made to rear it (Woll et al., 2006). Strong cannibalistic behaviour has been reported for several decapod species including Carcinus maenas (Moksnes, 2004), Callinectes sapidus (Moksnes et al., 1997) and Cancer magister (Fernandez, 1999). Interestingly, avoidance of dead conspecifics has also been reported for several others, including C. pagurus (Hancock, 1974; Chapman and Smith, 1978; Zimmerfaust et al., 1985; Richards, 1992). This raises questions as to the cannibalistic behaviour of C. pagurus, which to the authors' knowledge, has not yet been consistently investigated (Chapman and Smith, 1978; Lawton, 1989). Porcellana platycheles is a conspicuous small, mainly microphagous, filter feeder, occurring in the low intertidal fringe from the Shetlands to the Canary Islands, and the Mediterranean Sea (Smaldon, 1972; Stevcic, 1988). Evidence of alternative macrophagic feeding has been reported, including the presence of sand grains and polychaeta setae in stomach contents (Stevcic, 1988). Furthermore, their characteristic large chelipeds suggest that aggressive behaviour may occur among conspecifics, but information is lacking. Cancer pagurus and P. platycheles co-occur in areas of fucoid– covered boulders and pebbles in the low intertidal and shallow subtidal zones, although individuals of C. pagurus over two years of age tend to live at greater depths (Smaldon, 1972; Ingle, 1980; Lawton, 1989; Sheehy and Prior, 2008). Little data exist on interspecific interactions, although C. pagurus predation on P. platycheles has been noted in laboratory experiments (Lawton, 1989). We conducted a series of laboratory, mesocosm experiments to study juvenile cannibalistic interactions in C. pagurus and P. platycheles. Specifically, we addressed: (1) Is intrasize class cannibalism in juvenile C. pagurus determined by density, food supply or lack of alternative prey? (2) Is intrasize class cannibalism and predation in juvenile P. platycheles dependent on density and food supply? (3) Can intersize class cannibalism be controlled by prey (juvenile) and predator (adult) densities in each species? (4) And, what are the effects of food, alternative prey and habitat type on such cannibalistic behaviour? 2. Materials and methods 2.1. Animal and substrata collection Animals and substrata were collected from May to June 2007 (spring season), from four coastal sites around Plymouth, UK: Mount Batten, Jenny Cliff and Heybrook Bay in Plymouth Sound, and Wembury Bay in the adjacent coast. These sites are characterized by platforms of laminated rocks with uneven series of gaps that create numerous ridges and pools where beach material, from sand to boulders, accumulate (M.B.A., 1957). There is a rich algal flora, particularly in the low shore, where Fucus serratus dominates (M.B.A., 1957). Cancer pagurus and P. platycheles occurred spatially together in the low intertidal and shallow subtidal areas, and were most abundant under pebbles, particularly under F. serratus. The natural density of each crab species at low water was estimated from 15 quadrats (0.5 × 0.5 m), randomly deployed in the low intertidal. Individuals encountered in these surveys were retained for laboratory experiments. Whilst this approach lacks information on densities during high water, these data were used as an approximation to inform experiments. Juvenile C. pagurus, between 20 and 27 mm carapace width (CW), corresponding to 1+ yr crabs (Sheehy and Prior, 2008), and late juveniles of P. platycheles, between 5 and 7.5 mm CW (Smaldon, 1972), were most abundant and were selected for experimentation. Adults from 85 to 95 mm and 12 to 13.5 mm CW of C. pagurus and P. platycheles, respectively, were also retained. Only active and undamaged individuals, free of parasites and in intermoult (evaluated by hardness of the carapace) were collected. In order to replicate the natural environment, sieved (b1.0 mm) beach sand was used in experimental mesocosms. Pebbles of two size

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ranges dominated the low intertidal, and were used as different habitats in the experiments: small and large pebbles, 8-12 and 16-22 cm long, respectively. Fronds of F. serratus were selected to fit mesocosm height. 2.2. Animal and substrata maintenance Animals were kept in flow-through 120 L containers with natural seawater and fed fresh blue mussel, fish and shrimp for at least 5 d before being used. Despite different feeding habits, the same food was given to each species to standardise conditions and hence allow direct comparison of results. Photoperiod, water temperatures and salinities were similar to those in the mesocosms (see below). Adults maintained 3 d without food were considered “starved”. Animals undergoing moulting were discarded. Substrata were rinsed with seawater and cleaned of epiphytes and fauna prior to use. Sand and pebbles were additionally sun-dried. 2.3. Mesocosms Mesocosms were small flow-through rectangular tanks with round corners (0.27 × 0.27 × 0.18 m; 13 L), provided with a 2 cm deep layer of sand, which allowed burrowing of juvenile crabs. Mussel shell debris was added to provide a more natural environment. Running (~ 1.5 L min- 1) natural, filtered (b750 μm) seawater from Plymouth Sound entered at the bottom and left each tank at the surface. Water temperature was 16 ± 1 °C and salinity 34± 2. Photoperiod was 16 h light: 8 h dark, provided by 2 white florescent tubes (~80 lux), approximating natural conditions in southwest Britain at the time of the experiments. 2.4. General experimental procedures Mesocosm experimentation was conducted at the Marine Biological Association, Plymouth, UK (50°18-22′N, 4°5-13′W). All experiments had a full factorial design with a replication level of 3. The animal densities used for experimentation are considered in relation to each other, and thus the terms low, medium and high are relative. In 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, respectively, although when juvenile density was not a factor, the medium juvenile density was used. Unless stated otherwise, excess food (fresh blue mussel, fish and shrimp) was provided daily, scaled to crab density so foraging opportunities were equal; uneaten remains were siphoned out daily. Adult predators were allowed to adapt to mesocosms for 8 h prior to prey addition. No control of moulting was made during trials, so its effects could be as natural as possible. The duration of experimental trials (Table 1) was set pragmatically based on preliminary work, allowing time for the studied effects to be noted and avoiding unnecessary stress and death on individuals. Experiments on intrasize class cannibalism had two different durations: 5 days for experiments involving interspecific interactions and 15 d for those evaluating effects of density. Preliminary experiments on intersize class cannibalism were stopped after 6 h of no prey mortality and appendage loss, yielding a total trial duration of 80 h. Throughout all experiments, animal behavior was observed to provide insight into the mechanisms leading to mortality and appendage loss and on termination of each trial, habitats were carefully removed from the tanks and surveyed for animals. Animals and substrata were used only once. 2.5. Experiments 2.5.1. Intrasize class cannibalism in C. pagurus juveniles In order to assess the density dependent nature of cannibalism in C. pagurus and the way it is mediated by availability of food and/or alternative prey, two experiments were conducted. The first experiment (Exp.1) tested the effects of juvenile density (low, medium, high)

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Table 1 Summary of all experiments conducted

Table 2 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. L/M/H M L/M/H M L/M/H

Food Alt. prey Pred.

1 2 3 4 5

C. pagurus C. pagurus P. platycheles P. platycheles C. pagurus

6

P. platycheles L/M/H Y

-

7 8 9

C. pagurus C. pagurus C. pagurus

Y/N -

M M M

Y Y/N Y Y/N Y

Y/N Y/N Y/N

Y/N -

Y/N Consp. 1/2 Consp. 1/2 Consp. 1 Consp. 1 Consp. 1

Starv. Habitat Treat. Dur.

C. pagurus

-

-

3 4 3 4 6

15d 5d 15d 5d 80h

df

MS

F

p

df

MS

F

p

2 6

0.04 0.03

1.26

0.35

2 6

0.003 0.003

1.0

0.42

-

-

6

80h

Y/N -

S/Ps/ Pl/F

4 4 8

80h 80h 80h

All experiments had a full factorial design. For each experiment is indicated the crab species focused, the factors under test, the total number of treatments and the duration of the experiment. Legend of column heads: Exp. – Experiment; Sp. – Species; Dens. – Density; Alt. prey – Alternative prey; Pred. – Predators; Starv. – Predator starvation; 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 pebbles, F. serratus.

and food (yes, no) over a 15 d period, under the hypothesis that cannibalism was more intense at high density. The second (Exp.2) determined rates of cannibalism at a constant juvenile density whilst varying food availability (yes, no) and alternative prey (P. platycheles at 6 juvenile ind.tank- 1, versus none) (Table 1). The hypothesis tested was that cannibalism was more intense when no food or alternative prey was supplied. 2.5.2. Intrasize class cannibalism and predation in P. platycheles Experiment 1 was repeated for P. platycheles (Exp.3, Table 1). We tested the hypothesis that predation of P. platycheles by juvenile C. pagurus is mediated by the presence of alternative food in a 5 d experiment by varying the presence of the potential predator (yes, no) and food (yes, no) (Exp.4, Table 1). 2.5.3. Intersize class cannibalism: effects of prey and predator densities, food, alternative prey and habitat type Intersize class cannibalism was assessed in both target species in five experiments. Initially factorial experiments were run for both C. pagurus (Exp.5) and P. platycheles (Exp.6) to evaluate whether intersize class cannibalism was dependant on both prey and predator densities. The hypothesis under test was that intersize class cannibalism was higher at high prey (juveniles) and predator densities. Juvenile density (low, medium and high) and predator density (1 or 2) were varied and mortality assessed after 80 hours. Control trials were ran without predators, and average results subtracted to other treatments. 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 (starved, not starved) affected intersize class cannibalism in C. pagurus was examined in Experiment 7. We hypothesized that starved predators yielded higher cannibalism rates, especially when no food was supplied. The effects of the presence of alternative prey (P. platycheles at 6 juvenile ind.tank- 1, versus none), together with food availability (yes, no) in intersize class cannibalism in C. pagurus were investigated in Experiment 8. Specifically, the hypothesis was that the presence of alternative prey resulted in lower intersize class cannibalism, especially in the absence of food. Finally, the hypothesis that cannibalism is more important where refugia are sparse, was tested by varying habitat type from simple to increasingly complex (sand, small pebbles, large pebbles and F. serratus). The availability of food (yes, no) was also manipulated to determine to what extent this mediated the level of cannibalism.

Density Error

P. platycheles

2.6. Statistical analyses Proportional mortality (number of missing crabs / total number) and appendage loss (number of appendage missing / total number) were used as dependent variables in ANOVA models on intrasize class cannibalism and interspecific predation. ANOVA models were also used on intersize class cannibalism, with proportional prey mortality (number of prey missing / total number) as the dependent variable. Experimental factors (density, food, alternative prey, predators, predator starvation and habitat) were used as independent variables 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 tests. STATISTICA software, v. 6 (StatSoft) was used. 3. Results 3.1. Intrasize class cannibalism in C. pagurus: effects of density, food and alternative prey Although agonistic behaviour, characterized by brief fighting events (b10 s), was noted several times, cannibalism was relatively low and was independent of density (Cochran's C = 0.95, df = 1, p N 0.26) (Exp.1). Only crabs that moulted were cannibalized and overall, proportional mortality was similar among the different density treatments: 17, 0 and 21% at low, medium and high densities, respectively (ANOVA Tukey's test, p N 0.3) (Table 2). The presence of food, and alternative prey had no effect on cannibalistic interactions, and mortality remained below 19% in all treatments (Cochran's C = 0.5, df = 1, p N 0.99; Exp.2, Table 3). No appendage loss was found in either experiment in live crabs. 3.2. Intrasize class cannibalism and predation in P. platycheles: effects of density and food In P. platycheles observations showed some agonistic behaviour; display of chelipeds was noted on some occasions, but did not result in fighting. Virtually no cannibalism was detected (Exp.3); mortality rates were zero at low and high densities, and ~ 6% at medium density,

Table 3 Results of two-way ANOVA analyses on the effects of food supply and presence of other crab species on intrasize class cannibalism as proportional mortality and appendage loss on C. pagurus (Exp.2) and P. platycheles (Exp.4) df

Proportional mortality

Proportional appendage loss

MS

MS

F

p

F

p

C. pagurus Food (A) Alternative prey (B) A×B Error

1 1 1 8

0.01 0.05 0.01 0.01

0.50 4.50 0.50

0.50 0.07 0.50

0.001 0.48 0.01 0.01

0.08 4.75 1.06

0.78 0.06 0.33

P. platycheles Food (A) Predator (B) A×B Error

1 1 1 8

0.17 0.42 0.10 0.01

16.76 41.71 9.70

b0.01 b0.001 b0.05

0.11 0.55 0.05 0.01

10.96 56.12 5.40

b0.05 b0.001 b0.05

V. Amaral et al. / Journal of Experimental Marine Biology and Ecology 368 (2009) 88–93

Fig. 1. Results of the effects of C. pagurus predator (yes, no) and food (yes, no) on survival, as proportional mortality, of P. platycheles (Exp.4). Error bars represent SE, being absent when SE = 0.

and ANOVA showed no effect of juvenile density (Cochran's C = 1; ANOVA Tukey's test, p N 0.4) (Table 2). Again, at the end of the experiment, no appendages were missing in live crabs. Juvenile individuals of C. pagurus attacked P. platycheles based on encounter, but not all encounters resulted in attacks (Exp.4). In all observed attacks, juvenile P. platycheles resisted by exposing their chelipeds, which sometimes resulted in attack failure and escape. Fighting events between C. pagurus juveniles were less common than in Exp.1 and 2. Mortality rates of P. platycheles were highest (67%) in the presence of juvenile C. pagurus predators and absence of food (Cochran's C = 0.52, df = 2, p N 0.99; ANOVA Tukey's test, p b 0.01) (Table 3). Appendage loss was highest when predators were present, with and without food supply (35 and 68%, respectively; Cochran's C = 0.44, df = 3, p N 0.86; ANOVA Tukey's test, p b 0.05 in all cases) (Fig. 1).

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afterwards, although not significantly (ANOVA Tukey's test, p N 0.5) (Fig. 2A). With two predators, prey mortality was inversely densitydependent, but only decreased significantly from low to medium prey density (ANOVA Tukey's test, p b 0.05) (Fig. 2A). Prey consumption was significantly affected by interaction of prey and predator densities (Cochran's C = 0.8, df = 1, p N 0.99; ANOVA: F = 39.8, df = 2,17, p b 0.001) (Exp.5). With one predator, consumption increased significantly from low to medium prey density (ANOVA Tukey's test, p b 0.001), although not further on (ANOVA Tukey's test, p N 0.6) (Fig. 2B). When two predators were present, no difference in prey consumption was noted among prey densities (ANOVA Tukey's test, p N 0.9) (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 5. Mortality of juvenile C. pagurus was significantly affected by interaction of food with predator starvation (Cochran's C = 0.5, df = 1, p N 0.99) (Table 4) (Exp.7). All juveniles were killed by starved predators to which no food was supplied (100%, ANOVA Dunnett's test, p b 0.001). The presence of P. platycheles, as alternative prey (Exp.8), significantly decreased mortality of juvenile C. pagurus (from 58 to 13%; Cochran's C = 0.33, df = 2, p N 0.99, ANOVA Tukey's test, p b 0.001), with or without food (Table 4). In the habitat experiment (Exp.9), juveniles sought refuge under pebbles of each size and by grabbing to F. serratus fronds higher in the mesocosms. Adults were observed to find refuge (other than burrowing) only under large pebbles. In some occasions, F. serratus fronts restrained movements of adults, but not of juveniles, by becoming embraced around walking appendices. Adults attacked conspecific juveniles based on encounter, but also through ambush tactics, by rising suddenly from

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, p N 0.99; Table 4) (Exp.5). With one predator, prey mortality increased significantly from low to medium prey density (ANOVA Tukey's test, p b 0.01) 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

A B A×B Error Factor

A B A×B Error

Experiment 5

Experiment 7

Prey (A) & predator (B) densities

Starvation (A) & food (B)

df

MS

F

p

df

MS

F

p

2 2 4 18

0.01 0.11 0.23 0.02

0.51 5.82 11.54

0.61 b 0.05 b 0.001

1 1 1 8

0.05 0.42 0.13 0.01

4.50 40.50 12.50

b0.07 b0.001 b0.01

Experiment 8

Experiment 9

Alternative prey (A) & food (B)

Habitat type (A) & food (B)

df

MS

F

p

df

MS

F

p

1 1 1 8

0.63 0.05 0.01 0.02

40.33 3.00 0.33

b 0.001 0.12 0.58

3 1 3 16

0.35 0.42 0.09 0.02

22.44 2.67 5.78

b0.001 0.12 b0.01

Fig. 2. Results of the effects of predator (1, 2) and prey densities (low, medium, high) on intersize class cannibalism of C. pagurus (A) as proportional prey mortality and (B) prey consumption rates (Exp.6). Error bars represent SE, being absent when SE = 0.

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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

Fig. 3. Results of the effects of habitat type (sand, small pebbles, big pebbles, F. serratus) and food (yes, no) on intersize class cannibalism of C. pagurus as proportional prey mortality (Exp.9). Error bars represent SE, being absent when SE = 0.

under pebbles. The majority of the attacks observed in F. serratus and small pebble habitats was not successful, and prey often escaped without injury. Mortality of C. pagurus juveniles was affected by interaction of habitat type with food supply (Cochran's C = 0.17, df = 5, p N 0.99) (Table 4). With no food supply, a higher proportion of juveniles (~67%) were cannibalized in sand and large pebble habitats (ANOVA Tukey's test, p N 0.99), than in F. serratus and small pebble habitats (b17%, ANOVA Tukey's test, p b 0.05) (Fig. 3). When food was supplied, the F. serratus habitat provided the best survival rates of juvenile C. pagurus (ANOVA Tukey's test, p b 0.05), yielding 100% survival (Fig. 3). 4. Discussion Cannibalism has been suggested as the main cause of juvenile mortality in size-structured populations of crabs, and hence is likely to affect several aspects of population dynamics (Moksnes et al., 1997; Fernandez, 1999; Moksnes, 2004). In this study, several factors underlying cannibalistic behaviours and interspecific interactions in juvenile crabs were addressed in simulations of natural conditions in laboratory mesocosms. Such an approach benefits from tight control of experimental factors but clearly will be affected by an unnatural environment. One such factor, the density at which crabs are stocked, will have a significant impact on the experimental results. We sampled the natural environment at low tide to assess natural variation in crab densities. Cancer pagurus juveniles of 1+ yr probably remain between tidal marks until later stages (N2+ yr), when subtidal/intertidal migrations occur (Sheehy and Prior, 2008). This is common in the ontogeny of intertidal crab populations, including the congener C. magister (McMillan et al., 1995; Holsman et al., 2006) and C. maenas (Hunter and Naylor, 1993; Burrows et al., 1999). Porcellana platycheles only undergo limited migrations inside the habitat, thus generally remaining between tidal marks the entire life (Stevcic, 1988). Hence, experimentation with the crab densities obtained at low tide allowed realistic, natural levels of interactions to be assessed. 4.1. Intrasize class cannibalism No evidence of agonistic behaviour was detected in P. platycheles, and cannibalism between juvenile C. pagurus was always low (only moulting crabs were cannibalized). In the wild, juveniles of each species were often found at high densities under respective rocks, suggesting a passive conspecific existence. Lack of aggressive interactions among juveniles allows gregarious behaviour, with all the benefits that this entails. For example, increased vigilance reducing response time to a predator attack (Zimmerfaust et al., 1985; Moksnes and Heck, 2006). Although similar low levels of cannibalism within

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. platycheles were maintained at a range of densities from low to high, suggests that this is not the case. Indeed the pattern of mortality (only P. platycheles juveniles were eaten) shows that C. pagurus juveniles are an effective predator of this species. These results are in accordance with those reported by Lawton (1989), also from laboratory conditions. On the shore, few specimens, usually less than 3, of each species sometimes occurred under the same pebbles and boulders, but not at high densities (more than 5 individuals of each species). At low tide, juvenile C. pagurus were most abundant near the low water level, while P. platycheles were abundant in the mid-low intertidal. This study suggests that interspecific predation may account for the spatial distributions on the shore, but extrapolation of mesocosm results to natural distribution patterns must be viewed with caution. 4.3. Intersize class cannibalism There was no evidence of cannibalism between different size classes of P. platycheles. The characteristic large chelipeds thus do not seem to be involved in aggressive behaviour between conspecifics, but display of chelipeds without fighting suggests that they could serve mating purposes. Under laboratory conditions, therefore, P. platycheles appears to be a non-aggressive species and in the field, natural distributions support this conclusion. Larger P. platycheles were always found in association with juvenile conspecifics on the shore, frequently at high densities, apparently reflecting a non-aggressive and gregarious nature. In contrast, cannibalism in C. pagurus was intense between different size classes, with strong dependence on prey and predator densities. These results somehow contradict the distinct rejection behavior of conspecifics by adult C. pagurus reported by Lawton (1989). Nevertheless, a similar ontogenetic change, from low to high intensity cannibalism, is known for the congener C. borealis, (Richards, 1992). In the natural environment, adult C. pagurus are mainly found subtidally, and more frequently in the presence of N2+ yr than smaller juveniles (Ingle, 1980; Lawton, 1989; Sheehy and Prior, 2008). Just as interspecific predation may be a factor in determining spatial patchiness in the distributions of P. platycheles and C. pagurus juveniles on the shore, intersize class cannibalism may act in the same manner for different cohorts of C. pagurus. Mortality of C. pagurus juveniles by a single adult predator increased with prey density, possibly indicating saturation at high prey density, 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 result of a decrease in habitat heterogeneity, leading to higher encounter rates (Lipcius and Hines, 1986; Moksnes et al., 1997). In our study, the addition of a second predator could have resulted in higher preypredator encounter rates, leading to a similar effect to that of reduced habitat heterogeneity (Hassel, 1978). Prey consumption did not increased proportionally with increased predator density. Dependence of prey consumption on predator intensity suggests the occurrence of mutual interference among adult C. pagurus (Moksnes et al., 1997; Fernandez, 1999; Moksnes, 2004).

V. Amaral et al. / Journal of Experimental Marine Biology and Ecology 368 (2009) 88–93

Although predator starvation had no effect on the level of predation of conspecifics, greater availability of food did diminish prey mortality. Food availability is for many organisms the most important factor affecting the intensity of cannibalism (Fox, 1975; Polis, 1981; Smith and Reay, 1991; Wise, 2006). In fact, the level of cannibalism was also significantly reduced by P. platycheles as alternative prey. Although adding P. platycheles adds a potentially confounding effect (increased crab density) this was likely not relevant, since we showed in Experiment 1 that cannibalism between juvenile C. pagurus was low and independent of crab density. Consumption of alternative prey rather than conspecifics is a common behaviour observed in a range of organisms (Fox, 1975; Polis, 1981; Smith and Reay, 1991). On the other hand, adult C. pagurus may have preyed preferentially on P. platycheles due to the smaller body size of this prey type, and thus easier to capture and handle, when compared to that of C. pagurus juveniles. Furthermore, food supply reduced predation rates on alternative prey, suggesting that adult C. pagurus may chose the most cost-effective type of food/prey. Habitat type had a strong influence on the level of intersize class cannibalism. Juvenile mortality was lower within small pebbles and under F. serratus, than in the sand and large pebbles habitats, with habitat type showing more impact on cannibalism rates than food supply. Observations on the shore showed that adults were always found under large pebbles, and hence this habitat provided a poor refuge to prey. In contrast, on the shore and in the mesocosms, juveniles were observed to hide within the fronds of F. serratus, which may restrain movements of larger crabs (Moksnes et al., 1998; pers. obs.) and also limit visual predation. Studies of C. magister have shown that habitats of higher structural complexity generally provide more valuable refuges to prey (Fox, 1975; Polis, 1981; Moksnes and Heck, 2006). Our mesocosm results seem to corroborate this tendency for C. pagurus. In conclusion, we showed no evidence of aggressive behaviour in P. platycheles but significant levels of cannibalistic mortality in C. pagurus. Intersize class cannibalism in C. pagurus was more important for juvenile mortality than intrasize class cannibalism, and we speculate it may be involved in driving the intertidal distribution of this species at low tide. Additional factors including, prey and predator densities, food and habitat type modified the outcome of cannibalistic interactions. We did not control the energetic supply of food, conspecifics and alternative prey in our experiments. In order to evaluate the choice between food types by C. pagurus, specific experiments controlling this factor must yet be conducted. Field studies will allow validation of mesocosm results and further clarify the role of intra and interspecific aggressive interactions on the dynamics of intertidal crab communities. Acknowledgements We are indebted to A. Silva for her help with crab collection. We acknowledge a PhD grant to V.A. (SFRH/BD/10471/2002) funded by Fundação para a Ciência e a Tecnologia. We thank four Hanonymous referees for critical comments that greatly improved the manuscript. [RH]

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