Results of this study provide first information on the growth of H. planatus in Southern South America. Specifically, we studied moult frequency in the field, moult increment in the laboratory and analysed the size frequency distributions of crabs from an intertidal zone of the Beagle Channel. Studies on growth of hymenosomatid crabs are very limited (e.g. Richer de Forges 1977; Gao et al. 1994), and the present article is the first one on Hymenosomatidae that links laboratory and field growth data. In a previous study, Richer de Forges (1977) shows the growth of H. planatus with animals kept in the laboratory. Our results demonstrate that this species has a variable growth pattern in both sexes which could be explained by the presence of both immature and mature individuals, in a same range size.
The Beagle Channel population of H.
planatus exhibits different moult temporal patterns according to size. Small crabs moult during early spring and late summer, which coincides with the period observed in the Kerguelen Islands population (Richer de Forges 1977). In the Beagle Channel, a typical sub-Antarctic environment, these periods are characterized by the beginning of an increase in sea surface temperature and primary productivity in early spring, reaching the maximum temperature in summer (Almandoz et al. 2011). Although in crustacean decapods endogenous factors impinge on frequency of moulting, environmental variables could affect the moult cycle (see Chang 1995 for a review). The seasonal pattern of moulting observed in small sizes of H. planatus has also been found in other cold water species, even in other decapods of the Beagle Channel (e.g. Paralomis granulosa, large juvenile and adult Lithodes santolla) (Lovrich and Vinuesa 1995; Lovrich et al. 2002).
During the studied period, all mature females were in intermoult stage, which indicates the absence of ecdysis once maturity is reached. Namely, the pubertal moult is a terminal moult. By contrast, morphometrically mature, large males of H. planatus show evidence of moulting after the size of morphometric maturity (ca. 9 mm CW, Diez and Lovrich 2010), particularly during summer months (February–March). In addition to the morphometric change at the pubertal moult, where chela shows a first allometric positive change, some males exhibit a second morphometric change in their chela, being significantly longer and wider at 10.6 mm CW (Diez and Lovrich 2010). This pattern suggests that males continue moulting, likely corresponding to modal groups 6 and 7 (Fig. 4), after the first morphometric change. However, from our variable data, it was difficult to determine the number of moults between these two morphometric changes. The terminal moult in males, if present, could occur at the moult stage corresponding to this second allometric change of the chela. By judging the size and abundance of these males in the population (10.1–13.6 mm CW, 6.2 % of male population; Diez and Lovrich 2010), it is probable that not all males pass through this moulting event. Furthermore, it is likely that the lifetime after the male terminal moult may be relatively brief and crabs die shortly afterwards.
In the Beagle Channel, the per cent size increment per moult of H. planatus was variable in small crabs and showed a tendency to decrease in larger sizes. This pattern is also observed in other crustacean decapods, both in species with indeterminate growth (e.g. Munida gregaria, L. santolla, Neohelice granulata, Ucides cordatus) (Vinuesa et al. 1990; Tapella 2002; Luppi et al. 2004; Mokhtari et al. 2008) as well as in species with determinate growth (e.g. Maja squinado) (Sampedro et al. 2003). Growth requires energetic resources before and after ecdysis, in order to moult and to develop gametes in reproductive organs, being antagonistic processes for a fixed energy budget (Hartnoll 1985).
In H. planatus females, this opposed relationship begins before reaching the maturity size. This involves a change in energy allocation: part of the energy assigned to growth during the immature phase is diverted to reproduction, with the consequent marked decrease in the per cent size increment per moult. In fact, H. planatus shows one of the highest reproductive output among Brachyura species (ca. 20 % of the body weight per egg batch; Hines 1982; Diez and Lovrich 2010) only exceeded by parasitic pinnotherids species (Hines 1992). Like other hymenosomatids (McLay and Van den Brink 2009), H. planatus females can only lay eggs after the pubertal moult, when the abdomen acquires the shape to accommodate the egg mass (Vinuesa and Ferrari 2008). Hence, its high reproductive output can be related with the presence of a terminal pubertal moult. We hypothesize that the terminal pubertal moult is an advantageous feature that allows females to maximize their investment in reproduction after their terminal moult. Having all the energy devoted to reproduction is particularly important in the sub-Antarctic environment that enables H. planatus to produce two egg batches per year, which, in turn, allow us to further postulate that determinate growth is an advantageous feature in case of invasion to the Antarctica (Diez and Lovrich 2010).
By contrast, H. planatus males attain the gonadal maturity at 3.6 mm CW (Diez and Lovrich 2010), and the process of sexual maturity competes with growth (Hartnoll 1985), as follows. This size at gonadal maturity corresponds to young animals: the smallest male with spermatozoa at deferens ducts is 2.2 mm CW, likely attributable to stages Crab II or Crab III. This is a size relatively small compared to female gonadal maturity or pubertal/terminal moult attained in the range of 7.0-9.6 mm CW (Diez and Lovrich 2010).
The analysis of the modal groups from size frequency distributions of the Beagle Channel population is novel for H. planatus. We preferred to use the term “modal groups” instead of instars or cohorts, because of the great variability of moulting increment. However, the first two smaller modal groups likely correspond to juvenile instars, because crabs of the same instar further larger could belong to different modal groups, as aforementioned. We recognize the limitation of our analysis since both applied methods (Bhattacharya’s and MIX) have subjective decisions on, for example, the number of modal groups. A formal and more objective modal analysis of the size structure of the H. planatus population (e.g. Smith and Jamieson 1989; Lovrich and Vinuesa 1995; Lovrich et al. 1995; Smith and Botsford 1998; Lovrich et al. 2002) was hampered by different factors. First, the high variability of size increment at moulting combined with the quadratic function that relates the moult increment with the crab size (Fig. 3) makes individuals that belong to a modal group could remain in this same modal group while others crabs could move to the next modal group, even after two moult periods. Alternatively at moulting, small crabs could “skip” a modal group and go fell into the next one. Second, modal groups were present at all samplings, without the possibility of identifying an instar that could have matched with a modal group, with the exception of the very small sizes. Third, the blurring modes, particularly in females, as a result of the accumulation of adult, terminally moulted individuals >7 mm CW from different size classes. Although modes remained in the same size range during all the studied period (Figs. 4, 5) suggesting that modes are instars, averages of modal groups (Tables 3, 4) contradict this perception, since for two contiguous modal groups, average sizes can be similar. Hence, the analysis of the modal displacements of any cohorts through the study period is complex and can be speculative, even though modal groups can be traced in the population.
Nevertheless, based on the high proportions of modal groups corresponding to small sizes, it is possible to confirm two recruitment periods or juvenile migrations from settlement places (Diez et al. 2011): summer (January–March) and early winter (June–July). Both periods coincide with the two spawning per year of this species (Diez and Lovrich 2010) and with the two larval cohorts found in the meroplankton assemblage of the Beagle Channel (Lovrich 1999). The existence of these two juvenile cohorts in two different periods, the high variability recorded in the moult increment in the laboratory (Fig. 3) and the presence of a terminal moult suggest that the modal groups could be composed by crabs of different ages and moult stages.
The presence of a terminal moult divides Hymenosomatidae into two groups of species: one maintains the ecdysis after the pubertal moult as H. orbiculare females and Elamenopsis lineata (Lucas 1980). Another fraction is composed of several species of Halicarcinus spp. and Amarinus spp. which have a pubertal terminal moult (Richer de Forges 1977; Lucas 1980; Vinuesa and Ferrari 2008). This pattern of development has been recorded for some families of decapods. For example, within the Majoidea group, the pubertal and terminal moults are one and the same moult (Hartnoll 2001). H. planatus arrives at the pubertal moult with ripe ovaries (Diez and Lovrich 2010), and although its mating system is still unknown, we suggest that this species probably has a mating strategy similar to the “Majoid” group established by McLay and López Greco (2011). Nevertheless, the presence of a terminal moult in males of certain majoid crabs has been largely controversial (Conan and Comeau 1986; Dawe et al. 1991) and was corroborated recently (Fonseca et al. 2008).
The terminal pubertal moult of H. planatus females could occur in two different periods: December and July (Diez and Lovrich 2010). The modal groups that contain the size corresponding to maturity (i.e. modal group 5, Fig. 5) presented the highest proportions in December and July. In this context, in which females vary in the number of moults to attain sexual maturity, it is complex to estimate the age of maturity, by calculating the time elapsed since the arrival to intertidal zone (~3.6 mm CW; Diez et al. 2011) to the maturity size (ca. 9 mm AC; Diez and Lovrich 2010). However, according to the variability in size increment (Table 1; Fig. 3) and an intermoult period of ca. 90 days (estimated from individuals that moulted twice in captivity, (Diez 2011)), females could take 5–9 moult instars (ca. 15–27 months) to attain the size at maturity. Females H. planatus of the Kerguelen Islands population take 27 months to reach the size at maturity of 14.1 mm CW, probably at crab instar 12 (Richer de Forges 1977). These differences in size at maturity between both populations could be related to differences in the temperature regimes between the Beagle Channel and Kerguelen Islands. Temperature may affect the growth pattern (Hartnoll 2001) altering the number and sizes of moults that precede the terminal moult as it occurs in, for example, Chionoecetes opilio (Burmeister and Sainte-Marie 2010).
Within Hymenosomatidae, the terminal moult may have evolved as part of a strategy of small size and a high reproductive rate (McLay and Van den Brink 2009). This is an important trait in the life history of the sub-Antarctic population of H. planatus. The cessation of growth allows allocating most resources to reproduction, favouring the reproductive success in a highly seasonal environment with constrained availability of energetic resources, such as the sub-Antarctic one.