Seasonal changes in dry mass and energetic content of Munida subrugosa (crustacea: decapoda) in the beagle channel, Argentina.

ABSTRACT Munida subrugosa is the most abundant benthic species in the Beagle Channel (55[degrees]S, 68[degrees]W), Tierra del Fuego. Moreover, this species has two simultaneous but different feeding habits: predator and deposit feeder. Because of its high abundance (100 ind x 100 [m.sup.-2]) and trophic position, this species plays a key role in the subantarctic benthic ecosystems. However, little is known about its energetic content and changes in dry mass during its reproductive cycle. Samples of M. subrugosa were obtained in 2000 to 2001 by means of an epibenthic trawl. The relative water content (WC) and the energetic content (EC) (kJ x [g.sup.-1] ash free dry mass [AFDM]) of whole adult animals, and the relative dry mass (RDM) and EC of tissues and organs of females were measured throughout one year. The EC investment of adults at the time of maximum gonadal development was evaluated. The EC was measured using a bomb calorimeter. The mean WC and EC for M. subrugosa was 59% [+ or -] 7% and 19 [+ or -] 2 kJ x [g.sup.-1] AFDM, respectively. WC and EC for whole adult animals varied significantly throughout the year, attaining maximum values in autumn or summer respectively, after the pattern of seasonal reproduction and feeding. Moreover, the EC of M. subrugosa varied by 30% annually. The RDM and EC investment in gonadal development was significant higher in females. The hepatopancreas in M. subrugosa is used as an energetic storage organ, because RDM and EC increased before vitellogenesis and moulting.

KEY WORDS: subantarctic, Anomura, reproductive cycle, squat lobster, Munida gregaria

INTRODUCTION

The anomuran crab, Munida subrugosa (White, 1847) attains length 5-7 cm, and nearly 15-g wet mass, that lives off southern South America, New Zealand and southern Australia (Boschi et al. 1992). In South America, the Beagle Channel represents the southern distributional limit for this species. Munida subrugosa constitutes up to 50% of the macrobenthic community biomass and the 85% of the density of anomuran and brachyuran decapods at the eastern entrance to (Arntz et al. 1996, Gorny et al. 1996), and in, the Beagle Channel (Perez-Barros et al. 2004). The bycatch of the hake fishery from the Atlantic shelf off Argentina during 2000 was dominated by Munida spp. and yielded 6674 t (Villarino et al. 2002). A second sympatric and morphological similar species, M. gregaria Fabricius 1973 also occurs in the Beagle Channel (Tapella et al. 2002a). The specific identity of both species is still controversial and molecular studies suggest that both are the same species probably undergoing speciation (Perez-Barros et al. submitted). Hence, results presented in this study may be extensive and valid also for M. gregaria.

Currently, the only galatheids that are commercially exploited are Pleuroncodes monodon (H. Milne Edwards, 1837) and Cervimunida johni Porter, 1903 off Chile, ca. 35[degrees]S. Landings peaked 60,000 t in 1972, varied around 10,000 t during the 1980s and between 2,000 and 12,000 t during the 1990s. Munida spp. prospectively constitutes an exploitable shellfish at the southern tip of South America (Rayner 1935, Lovrich et al. 1998). High abundance of Munida spp. and its potential economical applications are comparable to those of other galatheids. Commercial uses can be as cocktail shrimp, source of natural astaxantins for coloration of cultured salmons or chicken eggs, digestive proteases for cheese manufacture, or milled as source of proteins of balanced food (Aurioles Gamboa & Balart 1995, Lovrich et al. 1998). Meat yield of M. subrugosa is 7.5% wet weight (Lovrich et al. 1998).

Munida subrugosa plays an important linking role in subantarctic benthic ecosystems, mainly due its trophic position (Romero et al. 2004). In one respect as predator and deposit feeder, M. subrugosa feeds on lower trophic level organisms, crustaceans and algae and on detritus and sediments (Romero et al. 2004). Hence, M. subrugosa is responsible for incorporating organic matter into the trophic web by passing saprophytic biodegradation (Romero et al. 2004). On the other hand, M. subrugosa, being very abundant, is prey of several top predators. Particularly in the Beagle Channel, galateid crabs are fed on by king crabs, fishes, cormorants, penguins and whales (Romero et al. 2004). Munida subrugosa participates in short trophic chains, which are probably efficient in the energetic transfer, because the shorter the chain, the less energetic losses (Pianka 1982). Hence the importance of studies related to energetic contents of this species.

The study of the energetic transfer between populations is an important step in the analysis and understanding of the functioning of an ecosystem. All energy that passes through a population is either transformed to heat or to other forms of energy, or is available to pass to another trophic level. Accurate values for the energetic content of both tissues of organisms or whole organisms are essential for a better understanding of energetic relations in ecosystems. Moreover, measures of whole body energy are useful in quantifying consumption of species by their predators (Paul 1997). Hitherto, the only data for the energetic content of related species, M. valida Smith, 1883 and M. iris A. Milne Edwards, 1880, are from the deep-sea continental slope (Steimle & Terranova 1988), in the northwest Atlantic.

In decapods, bioenergetic studies of variation in energetic content during the reproductive cycle are scarce. In the shrimp Crangon crangon (Fabricius, 1795) a cycle of progressive and retrogressive changes between the dry mass of the ovary and hepatopancreas occurs during ovarian development (Haefner & Spaargaren 1993). Other studies report on both seasonal variations and general descriptions of the lipid content and its relation with the reproductive cycle (Clarke 1977, Teshima et al. 1989, Styrishave & Andersen 2000, Wen et al. 2001, Mourente & Rodriguez 1991).

This study analyzes temporal variation in the dry mass and energetic content of Munida subrugosa in the Beagle Channel throughout a year. The dry mass and energetic content of females and males is compared on a monthly basis. In females, the energetic changes in the ovary, hepatopancreas and abdominal muscle are analyzed on a bimonthly basis. Furthermore, the energetic investment of females and males at the maximum stage of gonadic development before mating is documented.

MATERIALS AND METHODS

Study Site and Sampling

The field work was carried out in Bahfa Ushuaia, in the Beagle Channel (55[degrees]S; 68[degrees]W). Samples of M. subrugosa were obtained from waters shallower than 40-m depth with an epibenthic trawl net of 10-mm mesh size and 1.7-m mouth width (see Tapella 2002 for details). Crabs used for the analyses were preserved alive onboard, and dissected or frozen at -20[degrees]C on arrival at the laboratory.

The standard measure of body size, the carapace length (CL), was determined to the nearest 0.1 mm with a dial caliper. Crabs >10 mm CL are gonadal mature and therefore considered as adult individuals (Tapella et al. 2002b) as such, only crabs of >10 mm were used for this study. Average sizes for females and males used in this study were 19.9 [+ or -] 2.6 and 19.9 [+ or -] 2.4 mm CL, respectively, which is coincident with the modal sizes of the Beagle Channel population (c.f. Tapella 2002). Water content (%) and energetic content (EC) of whole M. subrugosa individuals, both males and females, were studied from monthly samples obtained between February and December 2000. From the total monthly catch, 12 males and 12 females were randomly selected and frozen.

The relative dry mass (RDM) and EC of different organs or tissues of female M. subrugosa were studied from samples taken once every second month from December 2000 to November 2001. At each sampling, 8-22 females were randomly selected from the total catch for analysis. Animals were kept in tanks with running seawater for a few hours until the dissection, then the carapace was removed, and ovaries, hepatopancreas and abdominal muscle were dissected.

To compare the energetic investment in reproduction in males and females, an additional sample of 15 male M. subrugosa was taken in May of 2001, when gonadosomatic indexes are near to reach their maximal values (Tapella et al. 2002b). Both testicles and vasa deferentia were used for the energetic measurements.

Water Content and Dry Mass Determination

Wet mass (WM) of the whole animals, stomach contents, hepatopancreas, abdominal muscles and ovaries of females, and testicles and vasa deferentia in males were recorded to 0.0001 g precision. Samples were dried to constant weight at 60[degrees]C, and the dry mass (DM) recorded.

The percentage water content of the animals was calculated as (WM-DM) x W[M.sup.-1] x 100. Because the DM is dependent on the animal size, we calculated the RDM of organs and tissues, which was the D[M.sub.organ] standardized by the D[M.sub.whole animal]. The RDM of all animals was calculated from the animal size (CL) and according to their sex and ovigerous condition. Lineal regressions between log RDM and log CL were calculated from a different sample of several nonovigerous females, ovigerous females and males (Table 1), obtained in July and December of 2001. The equality of the slopes was checked with an analysis of covariance (Sokal & Rohlf 1995).

Calorimetric Determination

After obtaining the DM, samples were ground and pelletized with a press model Parr 2812. The caloric content of each sample was obtained by burning pellets of 20-200 mg in a calorimeter Parr model 1425 with a microbomb Parr model 1341. Energy values were calculated using standard equations (Parr Instrument Co. 1991, 1993). The values obtained were corrected for ash and acid content and were expressed as kJ x [g.sup.-1] ash free dry mass (AFDM). Benzoic acid calibrations were done periodically.

RESULTS

The ingestion in Munida subrugosa was clearly seasonal, being maximum in December (Fig. 1; ANOVA F = 25.4, P < 0.001). Food uptake in M. subrugosa follows the same pattern as surface water temperature (Fig. 1; r = 0.66, P = 0.02): in autumn and winter, ingestion was almost 4 times less than in spring or summer.

[FIGURE 1 OMITTED]

For the whole adult animals values of water content and EC of male and female M. subrugosa varied significantly throughout the year (Fig. 2, Table 2). Overall, the mean water content and EC for both sexes were 59% [+ or -] 7% and 19 [+ or -] 2 kJ x [g.sup.-1], respectively. The minimum and maximum values of water content were registered in autumn and winter, respectively (Fig. 2A). The minimum of EC was recorded in winter (Fig. 2B). The interaction between month and sex for the water content was statistically significant (Table 2). Particularly, the water content of females was the lowest in June (ANOVA F = 6.24, P = 0.01).

[FIGURE 2 OMITTED]

RDM and EC in Organs and Tissues

Ovaries

The ovarian RDM and EC varied significantly throughout the year (Fig. 3, Table 3). Both RDM and EC reached their maximum values in May: afterwards, RDM and EC gently decreased and in November attained values similar to December (Fig. 3).

[FIGURE 3 OMITTED]

Hepatopancreas

The hepatopancreas RDM and EC varied significantly throughout the year (Fig. 3, Table 3). RDM and EC showed two maximum values around 140 [+ or -] 40 [mg.sub.org] x [g.sub.animal.sup.-1] and 32 [+ or -] 2 kJ x [g.sup.-1], respectively, in March and November (Fig. 3). No significant differences in RDM and EC between these months were found (Tukey test, P = 0.33 and P = 0.99 for RDM and EC, respectively).

Abdominal Muscle

The abdominal muscle RDM varied significantly throughout the year (Fig. 3, Table 3), principally because of a single maximum RDM recorded in March (80 + 10 [mg.sub.org] x [g.sub.animal.sup.-1]). This value duplicated the others recorded during the study period. The EC of the abdominal muscle was similar throughout the year (Fig. 3, Table 2), with an annual mean EC of 22 [+ or -] 2 kJ x [g.sup.-1].

Relationship Among Ovary, Hepatopancreas and Abdominal Muscle

Maxima in RDM of hepatopancreas and muscle and in EC of the hepatopancreas preceded that of the ovary (Fig. 3). In terms of RDM, the hepatopancreas and muscle were positive and significantly correlated (partial correlation, [r.sub.HxM] = 0.82, n = 109, P < 0.05). However, in terms of EC the hepatopancreas and muscle were uncorrelated (partial correlation, [r.sub.HxM] = 0.088, n = 59, P > 0.05). Hepatopancreas and ovary RDM were positive and significantly correlated (partial correlation, [r.sub.HxO] = 0.55, n = 109, P < 0.05), whereas the EC of these organs was positive but not significantly correlated (partial correlation, [r.sub.HxO] = 0.178, n = 109, P > 0.05). Ovary and muscle RDM and EC were negatively correlated, and none of these correlations were significant (partial correlation, [r.sub.OxM] = -0.31, n = 109, and [r.sub.OxM] = -0.184, n = 59, both P > 0.05, respectively).

Gonad Energy and Mass at the End of the Gonadal Development

The gonad RDM was significantly higher in females (40 [+ or -] 10 [mg.sub.org] x [ganimal.sup.-1]) than in males (6 [+ or -] 2 [mg.sub.org] x [ganimal.sup.-1]) (Student t = 12.91, P < 0.001). The gonad EC was also significantly higher in females (26 [+ or -] 2 kJ x [g.sup.-1]) than in males (22 [+ or -] 2 kJ x [g.sup.-1]) (Student t = 4.20, P = 0.002). Hepatopancreatic RDM (80 [+ or -] 28 [mg.sub.org] x [g.sub.animal.sup.-1]) and EC (30 [+ or -] 3 kJ x [g.sup.-1]) were similar in both sexes (Student t = 0.22, P = 0.82, and t = -1.07, P = 0.30, respectively). Similarly, muscle RDM (50 [+ or -] 9 [mg.sub.org] x [g.sup.animal.sub.-1]) and EC (21 [+ or -] 2 kJ x [g.sup.-1]) were also similar in both sexes (Student t = -0.08, P = 0.93 and t = 0.56, P = 0.58, respectively).

DISCUSSION

Our results depict a typical annual energetic cycle of a decapod in subantarctic latitudes (Thatje 2004 and references therein). Over the year, variations in energetic content can be divided into three different periods. During summer and autumn, the total energetic content is fairly constant (Fig. 2B), yet with a high flow of matter and energy from the hepatopancreas and muscle towards ovaries (Fig. 3B). Growth of the ovary is indicated by a maximum RDM and EC in May (Fig. 3A), which coincides with the lowest water content in the whole individuals (Fig. 2A). Subsequently during winter, the total energy content decreases after the egg-extrusion (c.f. Tapella et al. 2002b), and is coincident with a period of low ingestion (Fig. 1) and the lowest values of energy and mass in organs and tissues (Fig. 3). Finally, the energy accumulation phase occurs during the spring (Fig. 3B), when the food intake increases (Fig. 1), and the hepatopancreas grows for a second time in the year (Fig. 3). We attribute these variations to a seasonal feeding pattern and ultimately to physiological events such as reproduction.

The seasonal variations in somatic energetic content of M. subrugosa probably reflect its temporal feeding patterns. Development and physiological events in ectotherms from high latitudes may be regulated by the seasonal availability of food, and the degree of food dependence given their position in the food web (Clarke 1988). Particularly, the environment of the Beagle Channel is subantarctic with a marked seasonality in surface temperature (4.5[degrees]C-9[degrees]C in August and January, respectively) and photoperiod (18:6 light:dark in summer and vice versa). Munida subrugosa feeds on small macroalgae, small crustaceans and particulate organic matter (Romero et al. 2004). Food uptake in M. subrugosa follows the same pattern as water temperature. In turn, this could also reflect the different seasonal availability of producers (macroalgae and phytoplankton) and other prey with an annual life span.

In female Munida subrugosa maximum somatic energetic values recorded between February and May can be related to the reproductive cycle. In February, oocytes begin their secondary vitellogenesis (i.e., yolk accumulation) (Tapella et al. 2002b). This coincides first, with an increase in EC and RDM of the hepatopancreas in February and March and second with the increase in ovary EC during March and May. The ovary RDM drastically drops in July, right after the egg extrusion in June (Tapella et al. 2002b). Furthermore, the ovary EC gently decreases after egg extrusion, probably because of the presence of nonextruded oocytes and the reorganization of nutritional material associated with vitellogenesis (c.f. Johnson 1980).

The water content of M. subrugosa presents two maxima, in August and December. The latter is coincident with one of the peaks in RDM and EC of the hepatopancreas. These changes can be attributed to the moulting period. Tapella (2002) showed that M. subrugosa >10 mm CL has 2 periods of moult during the year, in spring and in summer. At moulting, decapods absorb a great quantity of water, which is later replaced by the organic matter that constitutes tissues (Vernet & Charmantier-Daures 1994). Nevertheless, the hepatopancreatic energetic increase during February is probably associated with the energy gained for summer moulting and ovarian growth.

Munida subrugosa uses its hepatopancreas to store energy, because this organ increases its RDM and EC before vitellogenesis (peaking in March) and moulting (peaking in November). Flexibility in storage and mobilization of nutrient reserves confers an evolutionary advantage, enabling an organism to stay active during periods of starvation (Crawford 1979), such as the moulting period (O'Halloran & O'Dor 1988). In crustaceans, the hepatopancreas is the principal energy supplier, and a large part of this energy is stored as lipids (e.g., Chapelle 1977, Mourente & Rodriguez 1991, Albessard et al. 2001, Ravid et al. 1999). The main functions of these stored lipids are as reserves for vitellogenesis and moulting (Dall 1981). The material accumulated by the hepatopancreas is converted to other compounds that are released into the hemolymph for an eventual use by the ovary (Haefner & Spaargaren 1993). In high latitude species, the energy stored in the hepatopancreas may be also used during winter when less food is available (Styrishave & Andersen 2000); this holds true for M. subrugosa, where reduced food consumption during winter (Fig. 1) is accompanied by the utilization of energy stored in the hepatopancreas (Fig. 3B) and a general decline in its energetic content (Fig. 2B).

Somatic energetic values of Munida subrugosa in the Beagle Channel compare with those of other related species and benthic crustaceans in general. During summer, spring and autumn, somatic EC of M. subrugosa was 20.6, 18.9 and 19.5 kJ x [g.sup.-1], respectively. These values are similar to other galatheids from the continental slope of the northwest Atlantic. Munida valida presents values of 19.9 kJ x [g.sup.-1] in summer; M. iris has 19.0 kJ x [g.sup.-1] in spring, and Eumunida picta Smith 1883, has 20.6 kJ x [g.sup.-1] in autumn (Steimle & Terranova 1988). The mean EC for M. subrugosa from the Beagle Channel was 18.9 [+ or -] 1.4 kJ x [g.sup.-1], similar to the decapod value from the English Channel of 20.5 [+ or -] 1.5 kJ x [g.sup.-1] (Dauvin & Joncourt 1989) but significantly lower than the reported EC of 22.7 kJ x [g.sup.-1] for benthic crustaceans and the general somatic EC of 23 kJ x [g.sup.-1] for macrobenthic invertebrates (Brey et al. 1988).

The somatic EC of M. subrugosa varies throughout the year between 16 and 21 kJ x [g.sup.-1]. Hence, calculations of consumption rates of predators should consider these seasonal variations carefully. Similarly, studies on energetic budgets of prey of M. subrugosa should take into account such seasonal variations. Munida subrugosa is one of the main prey of about 30 species of top predators in the Southwestern Atlantic (Romero et al. 2004). In the Straits of Magellan and its channel system, the density of M. subrugosa is as high as 27 individuals x [m.sup.-2] (Gutt et al. 1999). The Beagle Channel presents the highest biomass and productivity of macrozoobenthos of the Magellanic Region (Thatje & Mutschke 1999). Particularly at <40 m depth, the biomass of M. subrugosa is on average 3.4 g x [m.sup.-2] (Tapella et al. 2002a), which implies 64 kJ x [m.sup.-2] of energy easily accessible to predators above the sea-bottom. This characteristic is important from an ecological point of view, because Munida spp. are part of numerous trophic chains; for example, in the Beagle Channel food consumption among populations of nine seabird species is high, and estimated to be between 1.71 and 3.42 t x [d.sup.-1] (Raya Rey & Schiavini 2001). Hence, M. subrugosa probably contribute a large proportion of the high energetic flow towards the seabirds, especially diving species like penguins and cormorants. A contrasting potential prey species in the same location is the clam Eurhomalea exalbida (Chemnitz, 1795), which lives buried 20 cm in the substrate and is very abundant. Patches of this clam have an average abundance of 83 ind x [m.sup.-2] and an annual biomass of 186.4 g x [m.sup.-2] (Lomovasky et al. 2002), which represents 3914.4 kJ x [m.sup.-2], 60-fold that of M. subrugosa. Eurhomalea exalbida is a filter feeder that consumes particulate organic matter. This food is converted into clam tissue and retained under the sea bottom and is unavailable to predators. This clam is a long-lived species, with a life-span of 70 y (Lomovasky et al. 2002). Animals with such life-strategies capture and retain nutrients in living tissue for decades, so that energy transfer to other trophic levels is very low compared with Munida spp.

ACKNOWLEDGMENTS

The authors thank A. Chizzini, M. Gutierrez, C. Boy, C. de Roccis and E. Beckwith for field and laboratory assistance and J. Calcagno for statistical help. M. Robson corrected the English language. This study was financed by the Fundacion Antorchas, Argentina (project 13817/4). Additional funds were from the Agencia de Promocion Cientifica y Tecnologica (PICT 01-10042) and CONICET (PIP 02944). M.C. Romero and F. Tapella have a research fellowship for graduates from the CONICET.

LITERATURE CITED

Albessard, E., P. Mayzaud & J. Cuzin-Roudy. 2001. Variation of lipid classes among organs of the Northern krill Meganyctiphanes norvegica, with respect to reproduction. Comp. Biochem. Physiol. 129A: 373-390.

Arntz, W. E., M. Gorny, I. Wehrtmann, M. A. Lardies & R. Soto. 1996. Crustacea Decapoda: summary report. In: W. E. Arntz & M. Gorny, editors. Cruise report of the Joint Chilean-German-Italian Magellan "Victor Hensen" Campaign in 1994. Ber. Polarforsch. 190:57-60.

Aurioles Gamboa, D. & E. F. Balart. 1995. La langostilla: biologia, ecologia y aprovechamiento. Centro de Investigaciones Biologicas del Noroeste, S.C. La Paz, Baja California, Mexico. 233 pp.

Balestrini, C., G. Manzella & G. Lovrich. 1998. Simulacion de corrientes en el Canal Beagle y Bahia Ushuaia mediante un modelo bidimensional. Servicio de Hidrografia Naval. Departamento de Oceanografia. Informe Tecnico 98. 58 pp.

Brey, T., H. Rumohr & S. Ankar. 1988. Energy content of macrobenthic invertebrates: general conversion factors from weight to energy. J. Exp. Mar. Biol. Ecol. 117:271-278.

Boschi, E. E., C. E. Fischbach & M. I. Iorio. 1992. Catalogo ilustrado de los Crustaceos Estomatopodos y Decapodos marinos de Argentina. Frente Maritimo 10A:7-94.

Chapelle, S. 1977. Lipid composition of tissues of marine crustaceans. Biochem. Syst. Ecol. 5:241-249.

Clarke, A. 1977. Seasonal variations in the total lipid content of Chorismus antarcticus (Pfeffer) (Crustacea: Decapoda) at South Georgia. J. Exp. Mar. Biol Ecol. 27:93-106.

Clarke, A. 1988. Seasonality in the Antarctic marine environment. Comp. Biochem. Physiol. 90A:461-473.

Crawford, R. E. 1979. Effect of starvation and experimental feeding on the proximate composition and caloric content of an Antarctic teleost, Notothenia coriiceps neglecta. Comp. Biochem. Physiol. 62A:321-326.

Dall, W. 1981. Lipid absorption in the Norwegian lobster, Nephrops norvegicus (L.). J. Exp. Mar. Biol Ecol. 50:33-45.

Dauvin, J. C. & M. Joncourt. 1989. Energy values of marine benthic invertebrates from the western English Channel. J. Mar. Biol Ass. U.K. 69:589-595.

Gorny, M., W. E. Arntz & R. Soto. 1996. Crustacea Decapoda: Report on the anomuran and brachyuran crabs. In: W.E. Arntz & M. Gorny, editors. Cruise report of the joint Chilean-German-Italian Magellan "Victor Hensen" campaign in 1994. Ber. Polarforsch. 190. pp. 60-63.

Gun, J., E. Helsen, W. E. Arntz & A. Buschmann. 1999. Biodiversity and community structure of the mega-epibenthos in the Magellan region (South America). In: W.E. Arntz & C. Rios, editors. Magellan-Antarctic: ecosystems that drifted apart. Sc. Mar. 63. pp. 155-170.

Haefner, P. A. & D. H. Spaargaren. 1993. Interactions of ovary and hepatopancreas during the reproductive cycle of Crangon crangon (L.). I. Weight and volume relationships. J. Crustacean Biol. 13:523-531.

Johnson, P. T. 1980. Histology of the blue crab, Callinectes sapidus: a model for the Decapoda. New York, New York: Praeger. 440 pp.

Lomovasky, B. J., T. Brey, E. Morriconi & J. Calvo. 2002. Growth and production of the venerid bivalve Eurhomalea exalbida in the Beagle Channel, Tierra del Fuego. J. Sea Res. 48:209-216.

Lovrich, G. A., M. A. Casalinuovo, S. L Molina, C. Carcamo & R. Pierotti. 1998. Las langostillas Munida subrugosa y M. gregaria (Decapoda, Anomura) como potencial recurso economico patagonico. Nat. Pat. Cs. Biol. (Comodoro Rivadavia) 6:89-92.

Mourente, G. & A. Rodriguez. 1991. Variation in the lipid content of wild-caught females of the marine shrimp Penaeus kerahturus during sexual maturation. Mar. Biol. 110:21-28.

O'Halloran, M. J. & R. K. O'Dor. 1988. Molt cycle of male snow crabs, Chionoecetes opilio, from observations of external features, setal changes, and feeding behavior. J. Crustacean Biol. 8:164-176.

Parr Instrument Company. 1991. 1425 semimicro bomb calorimeter. Operating instruction manual. Moline, IL USA. 13 pp.

Parr Instrument Company. 1993. 1672 thermometer. Operating instruction manual. Moline, IL USA. 33 pp.

Paul, A. J. 1997. The use of bioenergetic measurements to estimate prey consumption, nutritional status and thermal habitat requirements for marine organisms reared in the sea. Bull. Nat. Res. Inst. Aquacult. (Suppl. 3):59-68.

Perez-Barros, P., F. Tapella, M. C. Romero, J. Calcagno & G. A. Lovrich. 2004. Benthic decapod crustaceans associated to captures of Munida spp. (Decapoda: Anomura) in the Beagle Channel, Argentina. Sc. Mar. 68:237-246.

Perez-Barros, P., E. Damato & G. A. Lovrich. Taxonomic status of two South American sympatric squat lobsters, Munida gregaria and M. subrugosa (Crustacea: Decapoda: Galatehidae), challenged by DNA sequence information. Zool. J. Linn. Soc-brad. (submitted).

Pianka, E. R. 1982. Ecologia evolutiva. Omega ediciones, S.A., Barcelona, Espana. 365 pp.

Ravid, T., A. Tietz, M. Khayat, E. Boehm, R. Michelis & E. Lubzens. 1999. Lipid accumulation in the ovaries of a marine shrimp Penaeus semisulcatus (De Haan). J. Exp. Biol. 202:1819-1829.

Raya Rey, A. & A. Schiavini. 2001. Filling the groove: energy flow to seabirds in the Beagle channel, Tierra del Fuego, Argentina. Ecologia Austral 11:115-122.

Rayner, G. W. 1935. The Falkland species of the crustacean genus Munida. Discovery Report. 10:212-245.

Romero, M. C., G. A. Lovrich, F. Tapella & S. Thatje. 2004. Feeding ecology of the crab Munida subrugosa (Decapoda: Anomura: Galatheidae) in the Beagle Channel, Argentina. J. Mar. Biol. Ass. U.K. 84:359 365.

Sokal, R. R. & F. J. Rohlf. 1995. Biometry. The principles and practice of statistics in biological research, 3rd ed. New York, New York: W. H. Freeman & Co. 887 pp.

Steimle, F. W., Jr. & R. J. Terranova. 1988. Energy contents of northwest Atlantic continental slope organisms. Deep-Sea Res. 35:415-423.

Styrishave, B. & O. Andersen. 2000. Seasonal variations in hepatopancreas fatty acid profiles of two colour forms of shore crabs, Carcinus maenas. Mar. Biol. 137:415-422.

Tapella, F. 2002. Reproduccion, crecimiento, distribucion y abundancia de la langostilla Munida subrugosa (Anomura: Galatheidae) del Canal Beagle, Tierra del Fuego, Argentina. Doctoral degree thesis, Universidad Nacional de Cordoba, Argentina. 154 pp.

Tapella, F., M. C. Romero, G. A. Lovrich & A. Chizzini. 2002a. Life history of the galatheid crab Munida subrugosa in subantarctic waters of the Beagle Channel, Argentina. In: A. J. Paul et al. editor. Crabs in cold water regions: biology, management and economics. Alaska Sea Grant College Program. AK-SG-02-01. pp. 115-134.

Tapella, F., G. A. Lovrich, M. C. Romero & S. Thatje. 2002b. Reproductive biology of the crab Munida subrugosa (Decapoda: Anomura: Galatheidae) in the Beagle Channel, Argentina. J. Mar. Biol. Ass. U.K. 82:589-595.

Thatje, S. 2004. Reproductive trade-offs in benthic decapod crustaceans of high southern latitudes: tolerance of cold and food limitation. Ber. Polar Meeresforsch 483:1-183.

Thatje, S. & E. Mutschke. 1999. Distribution of abundance, biomass, production and productivity of macrozoobenthos in the sub-Antarctic Magellan Province (South America). Polar Biol. 22:31-37.

Teshima, S. I., A. Kanazawa, S. Koshio & K. Horinouchi. 1989. Lipid metabolism of the prawn Penaeus japonicus during maturation: variation in lipid profiles of the ovary and hepatopancreas. Comp. Biochem. Physiol. 92B:45-49.

Vernet, G. & M. Charmantier-Daures. 1994. Mue, autotomie et regeneration. In: J. Forest, editor. Traite de Zoologie, Crustaces 7. pp. 107-194.

Villarino, M. F., M. A. Simonazzi, M. A. Renzi & G. R. Cafiete. 2002. Estimacion de la captura de merluza (Merluccius hubbsi) y de la fauna acompanante obtenida como bycatch en la Pesqueria del langostino patagonico (Pleoticus muelleri) durante el ano 2000. INIDEP. Informe N[degrees] 62/02. 14 pp.

Wen, X., L. Chen, C. Ai, Z. Zhou & H. Jiang. 2001. Variation in lipid composition of Chinese mitten-handed crab, Eriocheir sinensis during ovarian maturation. Comp. Biochem. Physiol. 130B:95-104.

M. CAROLINA ROMERO, * GUSTAVO A. LOVRICH AND FEDERICO TAPELLA

Consejo Nacional de Investigaciones Cientificas y Tecnicas, CONICET. Centro Austral de Investigaciones Cientificas, CADIC. CC 92, V9410BFD, Ushuaia, Tierra del Fuego, Argentina

* Corresponding author. E-mail: [e-mail]

TABLE 1.

Predictive regression of relative dry mass (RDM) on crab size (carapace
length, CL, in mm) in different sexes and ovigerous condition of
Munida subrugosa.

                                                      CL Range
  Sex and Condition       Equation of Regression        (mm)        N

Non-ovigerous females   Log RDM = 2.5 log CL - 3.09     13-25      106
Ovigerous females       Log RDM = 2.7 log CL - 3.24     15-26       45
Males                   Log RDM = 3.0 log CL - 3.71     16-24      151
                        [H.sub.0]: [b.sub.NOF] =
                          [b.sub.OF] = [b.sub.m]
                        [H.sub.0]: [b.sub.NOF] =
                          [b.sub.OF]
                        [H.sub.0]: [b.sub.NOF] =
                          [b.sub.M]
                        [H.sub.0]: [b.sub.OF] =
                          [b.sub.M]

  Sex and Condition       Equation of Regression      [R.sup.2]     F

Non-ovigerous females   Log RDM = 2.5 log CL - 3.09     0.75      316.5
Ovigerous females       Log RDM = 2.7 log CL - 3.24     0.72      106.8
Males                   Log RDM = 3.0 log CL - 3.71     0.78      545.4
                        [H.sub.0]: [b.sub.NOF] =
                          [b.sub.OF] = [b.sub.m]                    3.5
                        [H.sub.0]: [b.sub.NOF] =
                          [b.sub.OF]                                0.2
                        [H.sub.0]: [b.sub.NOF] =
                          [b.sub.M]                                 6.7
                        [H.sub.0]: [b.sub.OF] =
                          [b.sub.M]                                 1.6

Sex and Condition       Equation of Regression            P

Non-ovigerous females   Log RDM = 2.5 log CL - 3.09   [much less than]
                                                        0.001
Ovigerous females       Log RDM = 2.7 log CL - 3.24   [much less than]
                                                        0.001
Males                   Log RDM = 3.0 log CL - 3.71   [much less than]
                                                        0.001
                        [H.sub.0]: [b.sub.NOF] =
                          [b.sub.OF] = [b.sub.m]        0.031
                        [H.sub.0]: [b.sub.NOF] =
                          [b.sub.OF]                    0.700
                        [H.sub.0]: [b.sub.NOF] =
                          [b.sub.M]                     0.010
                        [H.sub.0]: [b.sub.OF] =
                          [b.sub.M]                     0.210

References: NOF and OF, non-ovigerous and ovigerous females,
respectively. N, sample size; [r.sup.2] coefficient of determination.
M, males; F, F-statistic.

TABLE 2.

Two-way analyses of variance (ANOVA) to detect differences in
percentage of water content and energetic content (kJ x [g.sup.-1])
in adult Munida subrugosa between sexes and throughout the year.

                Water Content (%)          Energetic Content

Source         d.f.     MS       F       d.f.     MS       F

Month            10   776.36   35.5 *     10    41.63   12.66 *
Sex               1    10.43    0.5        1    16.65    5.06 *
Month x sex      10    45.53    2.1 *     10     3.30    1.01
Error           242    21.87             242     3.29

References: MS, mean square; EC, energetic content; F, F-statistic.
Significant differences (P < 0.05) are indicated by asterisk.

TABLE 3.

One-way analysis of variance (ANOVA) to detect differences in
relative dry mass ([mg.sub.org] x [[g.sub.animal].sup.-1]) (RDM) and
energetic content (kj x [g.sup.-1] AFDM) (EC) of three different
tissues of female Munida subrugosa throughout the year.

                     Relative Dry Mass           Energetic Content

    Source       d.f.      MS          F       d.f.     MS       F

Ovary               6    3,345.51   114.02*       6    29.52   10.70*
Error             102       29.34                55     2.76
Hepatopancreas      6   32,192.20    36.47*       6   150.07   29.91*
Error             102      882.63                91     5.02
Abd. muscle         6    2,193.30    22.36*       6     3.09    1.19
Error             102       98.08                89     2.59

References: Abd. muscle, abdominal muscle; F, F-statistic. Significant
differences (P < 0.05) are indicated by asterisk.