The first record of Mytilus galloprovincialis (Lamarck, 1819) on Carcinus aestuarii Nardo, 1847 in the Çardak Lagoon, Turkey

Epibiosis is a common phenomenon observed between many sessile marine species (Wahl 1989). For many epibiont species it is very important to attach to the biological substrate in order to survive either through the adaptation of their morphological structures or the population dynamics. Most of the epibiont species are characterized by high growth rates, short life cycles and high reproductive rates (Jackson 1977; Seed 1985). This is an example of a model ecological development in the early stages of development. The exoskeleton of decapod crustaceans is well known as a substrate for epibionts/symbionts. Since many epibionts are mostly suspension feeders (e.g. barnacles, tube-dwelling polychaetes, bryozoans), this settlement is favorable for them because the movement of crabs and their feeding activity increase the availability of food. This relationship may have benefits to their hosts via camouflage and protect them from predators and parasites. Nevertheless, some relationships may negatively affect their hosts. Certain symbiotic organisms increase the host’s attractiveness to predators and they may prey on eggs or embryos of their hosts (Dvoretsky & Dvoretsky 2010). Several species such as a rhizocephalan parasitic castrator, Sacculina carcini, can generally parasitize C. aestuarii (Kuris et al. 2003).

C. aestuarii has been known from all Turkish coasts (Bakır et al. 2014). There are no detailed data showing a parasite/host relationship between M. galloprovincialis and C. aestuarii. In this study, the occurrence of Mytilus galloprovincialis on the Mediterranean green crab C. aestuarii has been reported for the first time.

C. aestuarii samples were collected in April 2015 and March 2016 from 6 sites of the Çardak Lagoon (Fig. 1). The crab specimens were sampled using single-entry fyke nets at an average depth of 1.5-2 m. Firstly, crab specimens were grouped by sex. A digital caliper was used for morphometric measurements of the crabs (carapace width and length) and the mussels (shell length). Next, the body parts of the crabs with the Mediterranean mussels attached were separated. Mediterranean mussels observed in different parts of the crab body were photographed to determine whether their removal from the holding parts caused any damage to the crusts of C. aestuarii specimens. All the crab specimens carrying the mussels on their bodies were recorded.

Figure 1

A total of 125 female and 469 male crabs were collected in the Çardak Lagoon. Specimens carrying epibiont mussels were encountered only at station 3 in samples collected in August and September 2015. Only four male individuals (average carapace width 38.5±4.69 mm, carapace length 44.82±5.76 mm) of C. aestuarii with carapaces infested by the mussels were collected in the sampling area. A total of 22 mussel specimens (1-9 ind. per single crab) were observed on the body parts of C. aestuarii. The mean length of the mussels observed as epibionts on different parts of the crab body was 8.77±0.40 mm. Specimens of M. galloprovincialis were found attached mainly to the abdomen, eyestalk, maxilliped, mouth, and propods of pereiopods (Fig. 2). These mussels were attached to the crab specimens by their byssus. All crab specimens collected in this study were males. Table 1 shows the number of mussel species and their frequency on the crab body.

Figure 2

Barnacles, bryozoans, hydrozoans, and bivalves are common epibionts attached to different body parts of the crabs (Dvoretsky & Dvoretsky 2008). Successful larval settlement and metamorphosis of Mytilidae depend on the availability of appropriate substrate (Branch & Steffani 2004). Branch et al. (2004) reported that M. galloprovincialis larvae lead to mass mortalities of the swimming crab Ovalipes trimaculatus. Larvae settled onto the eyestalks and mouthparts of the crab specimens can lead to their starvation or even death. It is not known whether large populations of the Mediterranean mussel may be similarly affected by other crab species (Branch et al. 2004). Wahl et al. (1997) studied the effects of epibiosis by Carcinus maenas preying on the mussel Mytilus edulis. Epibenthic species have strong effects on the community dynamics and this direct and indirect effects are involved in determining these epibiont prey-consumer interactions. Some epibionts strongly affect the feeding behavior of the consumers. When epibionts are more attractive than their host, the consumer pressure on the former increased (Wahl et al. 1997). Isaeva et al. (2001) have also recorded that Mytilus trossulus and Hiatella arctica are epibionts on the crab Hemigrapsus sanguineus in Vostok Bay, the Sea of Japan. The same authors described these species as facultative epibionts on the crab body. In the same study, the authors have reported that these species were found attached to the sacculinized crabs rather than the unsacculinized ones. We couldn’t find any Sacculina individuals on the crabs. The sex of the crabs has the major effect on the attachment places of the mussels. McGaw (2006) has reported another mytilid, Mytilus californiensis, on the crabs Cancer magister and Cancer productus. McGaw has also found a large number of species as epibionts on the male crabs. Similarly, we have observed the epibiont mussels only on the male specimens of C. aestuarii. Gili et al. (1993) performed a study on epibionts found on the deep sea crab Bathynectes piperitus and found only 4 male specimens invaded by epibionts of a total of 318 males. Similarly, we observed the male dominance in the male/female ratio, i.e. 3.75:1. Therefore, the epibiosis among crab males could be higher because they significantly dominated among the collected specimens.

Attaching to crabs is a useful strategy for many epibionts to feed and avoid predators (Wahl 1989). Mussel individuals found in this study were observed to attach to different parts of the crab specimens such as the abdomen and pereipods of the crab. Nevertheless, the mussels observed on eyes and maxillipeds of crabs may affect the feeding and orientation capacity of the crab specimens.

We believe that mussels attaching to C. aestuarii specimens as epibiont is a rare behavioral pattern. Despite the large number of crabs caught, the number of mussels observed on crabs was small. Therefore, it can be assumed that this observation may be coincidental. The reproduction period of mussel specimens was observed in spring. Based on the shell length of the analyzed mussels, it seems that they were ca. 6 month old. It is most likely that the mussels had attached to crabs already in their veliger stages and grew together with them. However, it is also possible that the duration of epibiosis would be shorter if juvenile bivalves, not veligers, settled on crabs. According to Ompi (2010) small specimens of Mytilidae are able to move until they finally settle on the proper substrate. The size is a significant factor in the movement of other mollusk species – smaller individuals tend to move greater distances than the larger ones (Uryu et al. 1996). On the other hand, crabs with epibionts were of medium size, therefore it is likely that they may get rid of them during the next molt. A higher incidence of epibionts on larger crabs, which do not molt so frequently, appears to be a common pattern among these crustaceans (Key et al. 1999).

This study includes the first data on epibiosis patterns of M. galloprovincialis attached to C. aestuarii found in the Çardak Lagoon.