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Factors Influencing the Deterioration of the Carapace Surface During the Moult Cycle of Carcinus Maenas (Linnaeus, 1758)

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Factors Influencing the Deterioration of the Carapace Surface During the Moult Cycle of Carcinus Maenas (Linnaeus, 1758) Contributions to Zoology, 83 (3) 167-175 (2014) Factors influencing the deterioration of the carapace surface during the moult cycle of Carcinus maenas (Linnaeus, 1758) Giuliano Greco1, 2, 3, Marco Faimali2, John Davenport1 1 School of Biological, Earth and Environmental Sciences, Enterprise Centre, Distillery Fields, North Mall Campus, University College Cork Cork, Ireland 2 CNR - ISMAR Via De Marini 6, 16149 Genoa, Italy 3 E-mail: [email protected] Key words: antifouling, crustaceans, epibiosis, green crab, moulting process, SEM Abstract Discussion and conclusion .......................................................... 172 Acknowledgements ...................................................................... 173 During its life cycle Carcinus maenas (Decapoda, Portunidae) References ...................................................................................... 173 goes through several phases of the moulting process (ecdysis) which allow it to grow despite having a rigid, non-living outer surface. As an individual approaches ecdysis, the exoskeletal Introduction calcium is solubilized (decalcification) from the shell and trans- ferred through the integumentary epithelium to the blood, where much of it is transported to cells, tissues and organs of Ecdysis (moulting), the process by which the inelastic temporary storage where it is later mobilized for deposition into cuticle is shed and renewed, is a defining feature of the the new exoskeleton. We hypothesised that the decalcification life history of arthropods, including crustaceans. Dur- process caused deterioration of the features and structures (e.g. ing moulting, the entire outer surface (including that of tubercles and setae) characterizing the crab carapace, but that this can be reversed by moulting. We also tested whether wear gills, eyes, grooming structures and sensilla) is re- and tear caused by abiotic and biotic influences between moults placed. Normally, moulting is associated with growth, might also cause surface deterioration. Any such deterioration which is saltatory rather than continuous in these in- would be detrimental to C. maenas. For example, compromise vertebrates, and also with regeneration of lost append- of the function of these structures could influence the settle- ages. However, moulting is also known to be important ment rate of epibionts on the crab surface as well as interfering with sensory and regulatory physiology. In this study, animals in removing fouling organisms (epibionts) in aquatic characterized as intermoult, premoult and postmoult crabs, crustaceans (e.g. Bauer, 2002). Less well understood were selected and their carapace surfaces analysed to evaluate are the effects of wear and tear between moults. In this the relationship between deterioration and moulting stage. Data study we address this deficiency using a convenient showed that the outer surfaces of Carcinus maenas were sub- ject to deterioration of their fine microtopographies throughout model. their life, probably influencing epibiotic settlement. Further- Carcinus maenas (Linnaeus, 1758) (Decapoda, more, the moulting process, already recognized as crucial for Portunidae) is a widely distributed epibenthic crab that growth and removal of fouling epibionts, also proved to be nec- inhabits hard and soft intertidal shallow habitats of the essary for the periodic restoration of surface microtopography. European coast and estuaries. During its life cycle it These findings, besides providing new insights into details of the crab life cycle, indicate a likely antifouling property for goes through several phases of the moulting process. carapace microtopography in C. maenas. This can be divided into five main stages (A, B, C, D, E) from newly moulted (A) to ecdysis (E), passing through several postmoult (B, C) and premoult stages Contents (D); each stage can be further divided into several sub- stages (Passano, 1960). Frequency of moulting is influ- Introduction ................................................................................... 167 enced by factors closely related to the metabolism of Material and methods .................................................................. 169 the crab, as well as by environmental conditions (Hart- Statistical analysis ................................................................. 169 noll, 2001; Styrishave, 2004). C. maenas, after several Results ............................................................................................. 171 Carapace deterioration before and after moult ............. 171 moults, can reach the C4T stage of the moulting cycle. Carapace deterioration after different intermoult This is characterized by cessation of moulting (anec- phase durations ...................................................................... 172 dysis) (Hartnoll, 1982). This stage generally occurs in Downloaded from Brill.com10/09/2021 12:19:58PM via free access 168 Greco et al. – Factors influencing carapace deterioration inC. maenas crustaceans that reach a large size, and represents a Any deterioration of tubercles and bristles, the main shift from a growing to a reproductive life strategy structures occurring on the crab carapace (Bottari et (Styrishave, 2004); crabs in anecdysis are generally al., 2003), under the influence of biotic and abiotic fac- characterized by a dark red colour. Carcinus maenas tors and not simply the decalcification process, could can be found in two different colour morphotypes be detrimental for C. maenas. For example, compro- (green and red) depending on the intermoult phase du- mise of the function of these structures could influence ration (Reid et al., 1997). This change in colour is due the settlement rate of epibionts on the crab surface, to the photodegradation of the integumental pigment since the topography and features of the carapace are astaxanthin that occurs during the intermoult stage known to have an important role in preventing the (Jencks and Buten, 1964; Lee, 1977) . settlement of organisms as reported for the crab Crabs spend most of their time in intermoult; dur- Cancer pagurus (Bers and Wahl, 2004) and for other ing this period they feed, reproduce and carry out day- marine organisms by several authors (Dyrynda, 1986; to-day activities. As an individual approaches pre- Baum et al., 2002; Scardino and de Nys, 2004; Guen- moult, the exoskeletal calcium is solubilized (decalci- ther and De Nys, 2007; Ralston and Swain, 2009; fication) from the shell and transferred through the Scardino et al., 2009; Bixler and Bhushan, 2012). The integumentary epithelium to the blood, where much of settlement of epibionts is one of the major issues influ- it is transported to cells, tissues and organs of tempo- encing the life of C. maenas. In some crab species, rary storage where it is later mobilized for deposition including spider crabs of the genus Maja, epibionts into the new exoskeleton (Ahearn et al., 2004). Decal- have a beneficial role (Parapar et al., 1997; Fernandez cification is one of the main events of the premoult et al., 1998), since the crabs take advantage of the stage (Roer and Dillaman, 1984). settlement of epibionts on their surfaces to camouflage Even though the moulting process has been studied themselves from predators. However, in C. maenas, as by many research groups in the last half century (Drach in many other active and predatory species, the settle- and Tchernigovtzeff, 1967; Engel and Brouwer, 1987, ment of epibionts on the crab outer surface is a serious 1991; McGaw et al., 1992; Groeneveld and Branch, problem leading to several harmful effects. These in- 2001; Godbout et al., 2002; Styrishave, 2004; Dam et clude: increases in weight, drag and friction, mechani- al., 2006; Ziegler et al., 2007), no studies of the external cal and chemical damage, degraded gas exchange, de- morphological changes that characterize the crab outer creased excretory capability and reduced sensory per- surface during the moult cycle (including any degrada- formance. These various effects, in turn, cause an en- tion of the carapace structures) have been performed. hanced susceptibility to predation and a weakened Fig. 1. SEM image of intact Carcinus maenas carapace 2 weeks Fig. 2. SEM image of a damaged tubercle of Carcinus maenas; after moult showing the two main structures characterizing its the black line indicates the projected area of the exposed exocu- surface: tubercles (T) and bristles (B); scale bar = 200 μm, ticle, the white line indicates the overall projected area of the magnification: 500×. tubercle; scale bar = 100 μm, magnification: 600×. Note dam- aged bristles (B) surrounding tubercle (T). Downloaded from Brill.com10/09/2021 12:19:58PM via free access Contributions to Zoology, 83 (3) – 2014 169 competitive ability (e.g. to capture food items) (Mc- fects of time on the crabs’ outer surfaces. After the Kenzie and Grigolava, 1996; Wahl, 1997, 2008). In ad- peelers had moulted, the exuviae (moulted integu- dition to effects on epibiont colonisation, any deterio- ments) were collected and the newly-moulted soft ration of the outer surface likely affects the integrity of crabs were left in sea water for 2 weeks before analysis the numerous sensors that are mounted on hairs and to allow sufficient shell hardening. They were killed bristles (e.g. chemosensory funnel canal organs of leg with clove oil (Gardner, 1997). Pieces of carapace sensilla; Schmidt and Gnatzy, 1989). (from exuviae and 2-weeks post moult) 1×1 cm in size Our study tested
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