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The Effect of Sacculina Carcini Infections on the Fouling, Burying Behaviour and Condition of the Shore Crab, Carcinus Maenas

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The Effect of Sacculina Carcini Infections on the Fouling, Burying Behaviour and Condition of the Shore Crab, Carcinus Maenas Marine Biology Research, 2006; 2: 270Á275 ORIGINAL ARTICLE The effect of Sacculina carcini infections on the fouling, burying behaviour and condition of the shore crab, Carcinus maenas KIM N. MOURITSEN1 & TOMAS JENSEN2 1Department of Marine Ecology, Institute of Biological Sciences, University of Aarhus, Finlandsgade 14, DK-8200 Aarhus N, Denmark & 2Wadden Sea Centre, Okholmvej 5, DK-6760 Ribe, Denmark Abstract Crabs infected by rhizocephalans usually do not moult. Because moulting is the ultimate defence against fouling epibionts, infected as opposed to uninfected crabs can be expected to harbour a diversity of hard-bottom organisms on their cuticula. Here we provide unequivocal evidence that this is the case in the Carcinus maenasÁSacculina carcini association. In a Danish sample of shore crabs, 75% of sacculinized individuals harboured macroscopic epibionts, whereas only 29% of the uninfected crabs were colonized. The mean numbers of fouling barnacles and serpulid tubeworms per individual were 7.7 and 47.3 for uninfected and infected crabs, respectively, corresponding to coverage of the cuticula by 0.7 and 5.4%. Infected crabs were 12% lower in tissue dry weight than uninfected individuals, which may be a factor causing the moult of sacculinized crabs to be postponed. Finally, a laboratory experiment suggested that infected crabs are less likely to bury than uninfected specimens. Because burying is an important fouling defence, such a parasite-induced behavioural change will favour the colonization by epibionts. It is argued that rhizocephalans infecting crabs from soft-bottom communities may indirectly affect the structure of the free-living benthic community by adding hard-bottom species that otherwise would be absent. Key words: Barnacles, community structure, epibionts, parasitism, rhizocephalans, serpulids Introduction coastal areas, and that the prevalence of rhizocepha- lans is often substantial (10Á50%; e.g. Alvarez & Rhizocephalans are morphologically modified crus- Caldero´n 1996; Mathieson et al. 1998; Mouritsen tacean parasites infecting, among other crustaceans, & Poulin 2002), this can be envisaged to impact the often ecologically important brachyurans. The the structure of the benthic community as a whole main body of the parasite is a root-like system of (see Poulin 1999; Thomas et al. 1999). However, branches that extends into most of the host’s tissue, the evidence that Rhizocephala-infected crabs in fact whereas the gonads of the parasites emerge exter- do harbour a better-developed community of epi- nally under the abdomen of the crab (e.g. Høeg & bionts than uninfected individuals is weak and Lu¨tzen 1995). Two important consequences of largely circumstantial, particularly regarding the infection are that the host is castrated and (if a green shore crab Carcinus maenas (see Giard 1874; male) feminized behaviourally and morphologically, Phillips & Cannon 1978; Shields 1992; Thomas and that externally infected crabs in most cases et al. 1999; Isaeva et al. 2001; Gaddes & Sumpton cease moulting (Høeg & Lu¨tzen 1995; Werner 2004). 2001). The latter means that the cuticula of infected Using the Carcinus maenasÁSacculina carcini asso- crabs can serve as a more permanent substrate for ciation as the model system, we here provide epibionts, which in turn should lead to a consider- unequivocal evidence that Sacculina-infected crabs ably higher abundance of fouling organisms on are more heavily fouled by certain unspecialized infected than on uninfected animals. If true, and epibionts than uninfected individuals. In addition, considering the generally high abundance of crabs in we present data on the burying behaviour and Correspondence: K. N. Mouritsen, Department of Marine Ecology, Institute of Biological Sciences, University of Aarhus, Finlandsgade 14, DK-8200 Aarhus N, Denmark. E-mail: [email protected] Published in collaboration with the University of Bergen and the Institute of Marine Research, Norway, and the Marine Biological Laboratory, University of Copenhagen, Denmark (Accepted 14 June 2006; Printed 12 September 2006) ISSN 1745-1000 print/ISSN 1745-1019 online # 2006 Taylor & Francis DOI: 10.1080/17451000600874752 Parasitism and fouling of crabs 271 general condition of infected versus uninfected crabs, half uninfected and half sacculinized, but specimens, which may partly explain the mechanism pairwise matched according to both carapace width by which the difference in fouling between the two and gender (i.e. equal size distribution and sex groups of crabs is established. The potential indirect ratio), were individually transferred to 44 l experi- community impact of the hostÁparasite association mental aquaria with a ca. 0.15 m2 bottom covered is discussed. by 5 cm of fine sand. The animals were left undisturbed for 2 min, after which time it was recorded whether or not the animals had buried Material and methods into the substrate. Study site, animal collection and standard protocol The study was carried out at Rønbjerg Harbour in Infection and condition the central part of the Limfjord, Denmark (56853?N 9810?E) during August 1997, 1999 and 2000. Shore Parasites subsist on nutrition provided by their host, crabs, Carcinus maenas, were caught by eel traps at a and infected crabs may therefore be in poorer water depth of approximately 1Á3 m, and the catch condition than uninfected individuals. Because crabs was divided into two groups according to whether or in poor condition may have a slower growth rate and not they were infected by Sacculina carcini. This was hence fewer moults per unit time, epibionts might be determined by the presence or absence of the allowed to accumulate for a longer period of time. parasite’s external gonads (externae) on the abdo- This could be an additional explanation for a more men of the host. Using this criterion of infection developed fouling community on sacculinized crabs means that the group of ‘uninfected’ crabs may than on uninfected crabs. Hence, to test the condi- include individuals that were only internally in- tion of infected versus uninfected crabs, 30 pairs of fected, which ensures a conservative analysis. The crabs, matched according to infection status and animals were kept in large storage tanks supplied carapace width (size range 25.9Á58.9 mm) were with running sea water until processed 1 or 2 days collected in 1999. Although males predominated, after capture. both sexes were represented in the two groups of animals. The crabs were killed, cleaned for macro- scopic epibionts, dried at 1008C for 36 h and Infection and epibiota subsequently weighed. The Sacculina externae pre- In 1997, the carapace width of 938 uninfected and sent on infected crabs were removed prior to drying 196 sacculinized crabs was measured with callipers. in order to approximate host tissue dry weight only. During measurements, the presence or absence of The internal part of the parasite could not easily be macroscopic epibionts on each animal was recorded. removed and therefore the dry weight of the infected Because the size distribution of the infected and host also included some parasite tissue. This means uninfected crabs differed significantly (see Results), that any quantitative difference in dry weight be- an additional sample of 12 uninfected and 12 tween uninfected and infected crabs is a conservative infected individuals, chosen at random (no visual estimate. contact) but matched according to carapace width (B/1 mm deviation), were killed and their legs Results removed. The number of macroscopic epibionts present on both the dorsal and ventral side of the Apart from a few records of attached macroalgae cuticula of each crab was recorded, and the propor- and mussels (Mytilus edulis), the majority of un- tion of the surface area occupied by these organisms specialized epibionts found on the shore crabs was then estimated from photographs taken of both were species of barnacles and the serpulid tube- sides: transparent graph paper was placed on each worm Pomatoceros triqueter (Figure 1). Based on the photograph and areas covered by fouling organisms 1997 sample of 1134 crabs, sacculinized hosts were marked, added, and then related to the entire significantly more likely (almost three-fold) to be projected surface area of the crab. fouled than uninfected individuals (Fisher’s exact test, PB/0.0005) (Figure 2). However, the mean carapace width of infected crabs (48.19/0.83) Infection and burying behaviour was significantly larger than that of uninfected Burying by crabs can influence the process of fouling crabs (44.59/0.86; Student’s t-test, t1132 /5.61, (e.g. Becker & Wahl 1996; Wahl et al. 1998), and in PB/0.0005). This could suggest that the group order to investigate whether Sacculina infection of infected animals was on average slightly older affects the burying behaviour of the host, a labora- than uninfected ones, and because the frequency tory experiment was carried out in 2000. Sixty-two of moulting decreases with age this might have 272 K. N. Mouritsen & T. Jensen test, P/0.049, Figure 2). Moreover, the dry weight of infected crabs was generally lower (approximately 12%, based on back-transformed grand means) than that of uninfected crabs (Figure 3). A full model ANCOVA indicated homogeneity of error variance across groups (Levene’s test, F1,58 /2.25, P/0.14) and the absence of a significant interaction between the two weightÁsize relationships (Figure 3) (F1,56 /0.19, P/0.66). The reduced model demon- strated a highly significant effect of infection status (F1,57 /18.64, PB/0.0005). Discussion Figure 1. A sacculinized shore crab, Carcinus maenas (1997 The present results demonstrate that Sacculina sample), fouled by tubeworms, Pomatoceros triqueter. Note the carcini-infected shore crabs are more likely to slightly protruding abdomen caused by the presence of Sacculina carcini externae beneath the abdomen. Apart from the tube- harbour epibionts than uninfected individuals, and worms, a few barnacles were also attached ventrally. that the average abundance of obligate hard-bottom species such as barnacles and the tubeworm Poma- toceros triqueter is several fold higher on infected contributed to the higher proportion of fouled crabs.
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