Reproductive potential of the lithodids Lithodes santolla and Paralomis granulosa (Anomura, Decapoda) in the Beagle Channel, Argentina*

Lithodidae is the only group of reptant decapods that occurs in Antarctic waters and has been particularly abundant in the Beagle Channel, Straits of Magellan and south to 50o S. Because of their abundance in coastal waters, the sympatric Lithodes santolla and Paralomis granulosa have constituted a mixed fishery since the 1930s. The two species differ markedly in their reproductive potential. Lithodes santolla is large (maximum size of 190 mm carapace length, CL, and 8 kg weight), has a generation time of 6 yrs., the reproductive cycle is annual and females carry between 5,000-60,000 eggs per female per clutch. In their life span, L. santolla females produce 6 times more eggs than P. granulosa females. Paralomis granulosa is smaller than its relative (maximum 115 mm CL and 1.5 kg weight), and has a slower growth rate, resulting in a generation time of 12 yrs. The reproductive cycle is biennial and females carry between 800-10,000 eggs per female per clutch. Moreover, the reproductive potential of P. granulosa is reduced because an important proportion of the largest and more prolific females of the population do not carry eggs. In other terms, in one generation time of P. granulosa, two complete generations of L. santolla are produced, and compared to other Subantarctic lithodids L. santolla is the most prolific species. The higher reproductive potential of L. santolla probably confers to this species the ability to recover more rapidly from an overfishing situation.


INTRODUCTION
Lithodidae is the only group of reptant decapods that occurs in Antarctic waters.Only one species, Lithodes murrayi Henderson, 1888 was found in the Bellingshausen Sea (Klages et al., 1995) and in the Subantarctic waters off the Crozet Islands (Arnaud, 1971).By contrast, lithodids -stone or king crabswere very abundant in the Subantarctic benthos, especially in the Magellan region.Among the 11 species of lithodid crabs that occur on Antarctic and Subantarctic waters, 7 species occur in the southern tip of South America.Lithodes santolla (Molina, 1782) and Paralomis granulosa Jacquinot, 1847 occurred at high densities between 2 and 50 m deep in the Straits of Magellan, Beagle Channel, and the Pacific channels south to 50º S. Such high densities have encouraged the development of a fishery since the 1930s, which affected negatively the populations (Campodonico et al., 1983;Campodonico and Hernández, 1983;Bertuche et al., 1990;Lovrich, 1997a and references therein).Lithodes turkayi Macpherson, 1988 is the third species that rarely occurs in the Magellan Straits and the Beagle Channel, at >70 m depth (identified as L. murrayi by Campodonico and Guzmán, 1972;Vinuesa et al., this issue).Lithodes confundens, Macpherson 1988 occurs on the Atlantic continental shelf near the eastern entrance of the Straits of Magellan (Lovrich et al., 1998b) and off the Islas Malvinas (Falkland Is.), and in the Straits of Magellan near Punta Arenas (Macpherson, 1988).Paralomis spinosissima Birstein and Vinogradov, 1972, P. formosa Henderson, 1888, and Neolithodes diomedeae (Benedict, 1894) occur south of the Antarctic Convergence, off South Georgia Islands (Macpherson, 1988;Otto and MacIntosh, 1996).However, N. diomedae is the only one of these species that occurs further north off the Pacific coast up to 5º S, and has been landed and sold in Puerto Montt at about 42º S (Vinuesa pers. obs.).
Knowledge on the biology of lithodids has arisen from the interest in their fishing and with the purpose of an efficient management of the populations.Therefore, most of the available information is related with the reproduction and life history of the current or potentially exploited species.By contrast, only the occurrences of less abundant or smaller species with no commercial interest were reported, as for example the other Subantarctic lithodids Paralomis birsteini Macpherson, 1988, P. aculeata Henderson, 1888or P. anamerae Macpherson, 1988.In this article, we summarize the available information on the life history and reproductive potential of Lithodes santolla and Paralomis granulosa in the Beagle Channel, Argentina.

The biology of the lithodids in the Beagle Channel
Both species are very different in their morphology.The body of Lithodes santolla is covered with spines and males may attain a maximum size of 190 mm of carapace length (CL) and 8 kg weight (Vinuesa, 1990).By contrast, P. granulosa is smaller, its body is covered by clusters of granules and males reach a maximum size of 115 mm CL and 1.5 kg weight (unpublished data).In the following, we summarize the main life history traits for both species.Literature sources from where the information proceeds are detailed in Table 1.

The biology of Lithodes santolla
In late November-early December, the reproductive cycle of L. santolla begins with female molting (Vinuesa, 1990).The precopulatory embrace and mating occur between a male with an old shell and a female recently molted and slightly smaller than her couple.Mating pairs may be found in the population for approximately a month (unpubl.data).As in other lithodids (Powell and Nickerson, 1965), fertilization is external and occurs immediately after female oviposition.Eggs are carried by females and the embryogenesis lasts approximately 9-10 mo.Fecundity (number of eggs per brood) increases with female size, between 5,500 and 60,000 eggs (Table 1).Larval hatching occurs between mid September and October, without significant annual variation (unpubl.data).Larvae are lecithotrophic (Oyarzún, 1992) or facultative lecithotrophic (Comoglio and Vinuesa, 1991), pass through three zoeal and one glaucothoe -or megalopal-stages (Campodonico, 1971), and metamorphose to the first benthic crab stage, which is about 1.5 mm CL (Oyarzún, 1992).The entire larval period lasts about 35-55 days at 7-8ºC (Vinuesa et al., 1985;Oyarzún, 1992).At temperatures <7ºC, the glaucothoe does not succeed in molting to the juvenile stage (Oyarzún, 1992).
Molt frequency of L. santolla decreases with age: during the first year, crabs molt 6-7 times, during the second year, 4-5 times, and during the third year, 3 times.Three years old crabs are about 50 mm CL (Vinuesa et al., 1990).Thereafter, males molt twice a year until they reach morphometric maturity (defined as the change in the allometric relationship between carapace and claw size), i.e., at 5 yrs.age, and 90-99 mm CL (Table 1).In the fourth year, females begin the ovarian maturation and thus, molt annually (Vinuesa et al., 1991).Gonadal maturity (in males defined as the presence of spermatozoa in the deferent ducts, and in females as the presence of embryos attached to pleopods) is reached at 60-75 mm CL in males, and at 66-87 mm CL in females (Table 1; Vinuesa, 1984).In females, oogenesis lasts ca.24 mo (Vinuesa and Labal, in press).After gonadal maturity, females continue to molt annually (Vinuesa et al., 1991), and after morphometric maturity males apparently continue molting biannually until they reach 110 mm CL (pers.obs.).Males enter the fishery at 110 mm CL and males >150 mm CL probably molt biennially (Geaghan, 1973).

The biology of Paralomis granulosa
During October-November, the reproductive cycle begins with courtship and mating, between an old-shelled male and a recently molted female that is smaller than her couple (unpubl.data).The fertilization is external and the female broods the embryos attached to pleopods between 18 and 22 mo (Table 1).Fecundity varies between 800 and 10,000 eggs, increasing with female size.However, ca.50% of the females >80 mm CL do not carry eggs although their ovaries are well developed (Hoggarth, 1993;Lovrich, 1997a).In the Beagle Channel, larval hatching occurs mainly during winter (June to August), almost two years after mating (Lovrich and Vinuesa, 1993).Larval development seems to be shorter than in L. santolla, since the 2 zoeal stages last 18-21 days at 8 or 5ºC, respectively (Table 1).However, there is no information about the duration of the glaucothoe stage, the entire larval development in the natural environment, and growth from the first crab stage to the stage of ca. 10 mm CL.During the immature phase, growth is slow.The smaller crabs (10-40 mm CL) molt twice a year: in winter and summer, while crabs >40 mm CL molt only in summer.During the immature phase, percentage of growth per molt is constant and 12.4 % irrespective of crab size (Lovrich and Vinuesa, 1995).At this rate of growth, we suspect that gonadal maturity would be reached at ca. 10 yrs age (Lovrich, 1997a).
Several indirect evidences indicate that fishing has been the main factor of mortality and the cause of the density reduction in the populations of lithodid crabs of the Beagle Channel (Campodonico and Hernández, 1983;Bertuche et al., 1990;Vinuesa, 1990;Lovrich, 1997a).Since L. santolla has been continuously fished, the effects of the fishery on its population were more evident than on P. granulosa.Between 1975 and 1996 the population of L. santolla underwent significant decreases in (1) the relative abundance (Table 1), ( 2) the proportion of legal males, (3) the proportion of ovigerous females, and (4) the mean size of the size frequency distributions of males and females.The only stock assessment of the population of the Beagle Channel was done in 1980-1981 after 14 yrs of annual landings of ≥ 200 t (Boschi et al., 1984), and was roughly coincident with the start of the decline of landings.Hence in 1980-81, crabs were probably less abundant than before the fishery developed, i.e., in the 1950s.On average, the density of L. santolla ≥ 60 mm CL was 3.1 crab • 100 m -2 and the relative abundance was 9.3 crabs per trap (Boschi et al., 1984).
Density estimations of P. granulosa are still needed, and reported relative abundances are scarce.In 1970, the relative abundance in the Beagle Channel was 38 crabs per trap (González, 1971), whereas in 1996 and 1997 it was 66 and 105 crabs ≥55 mm CL per trap, and 19 and 16 legal crabs per trap, respectively (Table 1; Lovrich 1997b;Lovrich et al., 1998a).However, there is some evidence of the negative influence of the fishery on the population.In the Straits of Magellan between 1979 and 1984-86, after intensive fishing, there were decreases in (1) the ~60% of the biomass of legal sized-crabs, (2) the relative abundance of landed crabs (probably > 75 cm CL) from 9.5 to 4 kg per trap, and (3) the mode of male size distributions from 92 to 74 mm CL (Campodonico et al., 1983;Díaz and Alvarado, 1986).

Reproductive potential
In crustaceans, the reproductive potential has been quantified in terms of fecundity, age at maturity, fishing mortality, proportion of females in each size class, and growth of individuals in a population (Campbell and Robinson, 1983;Shields, 1991).In this study the reproductive potential was calculated as the cumulative fecundity of a given female along her reproductive life-span (see Shields, 1991 p. 207).The size of each molt stage was derived from data of L. santolla female growth (Vinuesa and Lombardo, 1982), and the size-fecundity relationship was calculated from data of Vinuesa (1982).
The size of each molt stage of P. granulosa was assumed to be 5 mm CL (Campodonico et al., 1983 and unpubl. data), and the fecundity at size was calculated according to the function reported by Lovrich and Vinuesa (1993).
For an individual female and along her life span, L. santolla produces 6 times more eggs than P. granulosa (Fig 2).This is determined by two factors: first, L. santolla is larger and thus may carry more eggs than P. granulosa.Second, the embryogenesis of L. santolla lasts 9-10 mo, which allows females to have an annual reproductive cycle.Thus, a single female molts every year, increases her size and the total productivity.By contrast, the biennial reproductive cycle constrains P. granulosa females to molt once every two years, and thus prevents the increase of productivity.Moreover, if the female becomes large, e.g., >85 mm CL, she probably does not find a male of the appropriate size to mate, does not carry eggs, and thus the reproductive potential will not increase (Lovrich 1997a;1997b and unpubl. data).Finally, in population terms, in one generation time of P. granulosa (i.e., when one egg produces another egg), two generations of L. santolla are already produced, and the third one begins to produce eggs (Fig 2).
From the preceding observations, we advance two different hypotheses.First, life history traits of L. santolla, such as having more eggs that are pro-duced annually, annual molt, and reaching larger sizes, suggest that this species has more energetic requirements than its sympatric P. granulosa.Hence, L. santolla has probably occupied grounds of better quality than those used by P. granulosa, as occurs with king crabs of the Bering Sea Paralithodes camtschaticus and P. platypus (Jensen and Armstrong, 1989).So far, only anecdotal observations sustain that grounds formerly occupied by L. santolla were colonized by P. granulosa, once L. santolla was removed by fishing.Second, we suggest that the higher reproductive potential of L. santolla confers to this species the ability to recover more rapidly from an overfishing situation.By contrast, the longer generation time, the lower fecundity and the correspondingly lower reproductive potential of P. granulosa suggest that this species cannot support heavy rates of fishing for many years, as has occurred in the Islas Malvinas-Falkland Is. (Hoggarth, 1991).In the case of overfishing, the population recovery to pre-fishery levels will be relatively slow.However, much work is needed to estimate pre-fishery abundances, interactions between both species and niche overlapping, and effects of fishing on the competition between the two populations.Therefore, data acquisition from virgin stocks should be a priority for lithodid research in the Magellan region.
FIG. 1. -Landings of Lithodes santolla (u) and Paralomis granulosa (m ) in Ushuaia, Argentina.Landings for 1998 were forecasted with the available data until July 1998, i.e., 6 out of 10 mo of the fishing season.Source: Dirección de Recursos Naturales, Province of Tierra del Fuego.

TABLE 1 .
-Summary of life-history traits of the sympatric Lithodes santolla and Paralomis granulosa mainly in the Beagle Channel, Argentina.Numbers in superscript indicate bibliographic references: 1: