Abstract. Recent records of lithodid crabs in deeper waters off the Antarctic continental slope raised the question of the return of crabs to Antarctic waters, following their extinction in the lower Miocene ϳ15 million years ago. Antarctic cooling may be responsible for the impoverishment of the marine high Antarctic decapod fauna, presently comprising only five benthic shrimp species. Effects of polar conditions on marine life, including lowered metabolic rates and short seasonal food availability, are discussed as main evolutionary driving forces shaping Antarctic diversity. In particular, planktotrophic larval stages should be vulnerable to the mismatch of prolonged development and short periods of food availability, selecting against complex life cycles. We hypothesize that larval lecithotrophy and cold tolerance, as recently observed in Subantarctic lithodids, represent, together with other adaptations in the adults, key features among the life-history adaptations of lithodids, potentially enabling them to conquer polar ecosystems. The return of benthic top predators to high Antarctic waters under conditions of climate change would considerably alter the benthic communities.
During the larval development of the subantarctic king crab, Lithodes santolla, and stone crab, Paralomis granulosa, we compared changes in the carbon, fatty acid and protein contents of larvae reared under constant conditions from hatching to metamorphosis, either in presence or absence of food (Artemia spp. nauplii). In both species the feeding condition had no influence on any of the chemical parameters studied, indicating a fully lecithotrophic (i.e. non-feeding) mode of development from hatching of the first zoea to metamorphosis of the late megalopa. Dry mass and carbon contents at hatching were similar in the larvae of both species, but L. santolla contained initially higher total amounts of fatty acids and protein than P. granulosa. Both species utilized considerable portions of their total fatty acid pool which decreased logarithmically throughout the time of development. At metamorphosis, it was almost exhausted in P. granulosa, while L. santolla had consumed only about 60%. Protein utilization, in contrast, was higher in L. santolla (40%) than in P. granulosa (20%). Triacylglycerol was the principal storage lipid in both species, accounting initially for about 75% of the lipid fraction; it was strongly utilized during larval development. Phospholipid constituted the second largest lipid class; it also decreased in P. granulosa, but to a lesser extent in L. santolla. The major fatty acids of both species were 18:1(n À 9), 20:5(n À 3) and 16:0 as well as, in lower proportions, 18:1(n À 7), 22:6(n À 3), 16:1(n À 7) and 18:0. Monounsaturated fatty acids represented the dominant group in L. santolla, whereas P. granulosa contained similar amounts of mono-and polyunsaturated fatty acids. In L. santolla, monounsaturated fatty acids, especially 16:1(n À 7), were preferentially utilized as compared to polyunsaturates. Due to a particularly strong lipid utilization in P. granulosa, all individual fatty acids were largely depleted at metamorphosis, showing similar extents of consumption. L. santolla had higher initial lipid and protein stores that seem to be used more economically as compared to P. granulosa. D
Changes in biomass and elemental composition (dry mass, W; carbon, C; nitrogen, N; hydrogen, H) were studied in the laboratory during complete larval and early juvenile development of the southern king crab, Lithodes santolla (Molina), formerly known as Lithodes antarcticus (Jacquinot). At 6 F 0.5 jC, total larval development from hatching to metamorphosis lasted about 10 weeks, comprising three demersal zoeal stages and a benthic megalopa, with mean stage durations of 4, 7, 11 and 47 days, respectively. No differences in development duration or mortality were observed in larvae either fed with Artemia sp. nauplii or unfed, indicating that all larval stages of L. santolla are lecithotrophic. First feeding and growth were consistently observed immediately after metamorphosis to the first juvenile crab stage. Regardless of the presence or absence of food, W, C, N and H decreased throughout larval development. Also the C:N mass ratio decreased significantly, from 7.7 at hatching to 4.1 at metamorphosis, indicating that a large initial lipid store remaining from the egg yolk was gradually utilized as an internal energy source, while proteins played a minor role as a metabolic substrate. In total, 56 -58% of the initial quantities of C and H present at hatching, and 20% of N were lost during nonfeeding larval development to metamorphosis. Nine to ten percent of the initially present C, N and H were lost with larval exuviae, half of these losses occurring in the three zoeal stages combined and another half in the megalopa stage alone. degradation accounted for losses of about 47 -50% in C and H but for only 10% in N. Hence, most of the losses in C and H reflected metabolic energy consumption (primarily lipid degradation), while about half of the losses in N and two thirds of those in W were due to larval exuviation. Complete independence from food throughout larval development is based on an enhanced maternal energy investment per offspring and on energy-saving mechanisms such as low larval locomotory activity and low exuvial losses. These traits are interpreted as bioenergetic adaptations to food-limited conditions in Subantarctic regions, where a pronounced seasonality of day length limits the period of primary production, while low temperatures enforce a long duration of pelagic development. D
The southern king crab, Lithodes santolla Molina, is distributed in cold-temperate and subantarctic waters ranging from the southeastern Pacific island of Chiloé (Chile) and the deep Atlantic waters off Uruguay, south to the Beagle Channel (Tierra del Fuego, Argentina/Chile). Recent investigations have shown that its complete larval development from hatching to metamorphosis, comprising three zoeal stages and a megalopa, is fully lecithotrophic, i.e. independent of food. In the present study, larvae were individually reared in the laboratory at seven constant temperatures ranging from 1 to 18 jC, and rates of survival and development through successive larval and early juvenile stages were monitored throughout a period of 1 year. The highest temperature (18 jC) caused complete mortality within 1 week; only a single individual moulted under this condition, 2 days after hatching, to the second zoeal stage, while all other larvae died later in the zoea I stage. At the coldest condition (1 jC), 71% of the larvae reached the zoea III stage, but none of these moulted successfully to a megalopa. A temperature of 3 jC allowed for some survival to the megalopa stage (17 -33% in larvae obtained from two different females), but only a single individual passed successfully, 129 days after hatching, through metamorphosis to the first juvenile crab instar. At all other experimental conditions (6, 9, 12 and 15 jC), survival through metamorphosis varied among temperatures and two hatches from 29% to 90% without showing a [T]). The same model was also used to describe the temperature dependence of cumulative periods of development from hatching to later larval or juvenile stages. One year after hatching, the 7th (6 jC) to 9th (15 jC) crab instar was reached. Under natural temperature conditions in the region of origin of our material (Beagle Channel, Argentina), L. santolla should reach metamorphosis in October -December, i.e. ca. 2 months after hatching (taking place in winter and early spring). Within 1 year from hatching, the crabs should grow approximately to juvenile instars VII -VIII. Our results indicate that the early life-history stages of L. santolla tolerate moderate cold stress as well as planktonic food-limitation in winter, implying that this species is well adapted to subantarctic environments with low temperatures and a short seasonal plankton production. D
Paralomis granulosa Jacquinot is a commercially fished lithodid crab species living in subantarctic and cold-temperate regions of southern South America. Its larval stages (Zoea I, II, Megalopa) are fully lecithotrophic, developing in the complete absence of food from hatching through metamorphosis; first feeding occurs in the first juvenile crab stage. In laboratory rearing experiments conducted at constant 1, 3, 6, 9, 12, and 15°C, we studied rates of larval and early juvenile survival and development in relation to temperature. At 1°C, many larvae (52%) reached the Megalopa stage almost 2 mo after hatching, but all died subsequently without passing through metamorphosis. Larval development was successfully completed at all other temperatures, with maximum survival at 6 to 9°C. The time of non-feeding larval development from hatching to metamorphosis lasted, on average, from 24 d (at 15°C) to almost 4 mo (117 d, at 3°C). When the experiment was terminated 1 yr after hatching, the 3rd (3°C) to 8th (15°C) juvenile crab instar had been reached. The relationship between the time of development through individual larval or juvenile stages (y) and temperature (T ) was described as a power function (y = a × T b , or log[y] = log[a] + b · log[T]; the same regression model was also used to describe the temperature-dependence of cumulative periods of development from hatching. The wide thermal tolerance window for successful larval development (at least 3 to 15°C) and the broad geographic range of this species show that the early life-cycle stages of P. granulosa are cold-eurythermal. This physiological trait together with larval independence of food indicate that this lithodid crab species is well adapted to severe conditions of cold in combination with the food-limitation in subantarctic regions. Since similar traits have been also observed in other Lithodidae, we suggest that early life-history adaptations to low temperatures and low planktonic productivity may explain the high number of lithodid species occurring at high latitudes and in the deep sea, i.e. in conditions under which other Decapoda show strongly reduced diversity.
The evolutionary history of the Anomura has long been controversially discussed. One aspect that has received little attention is the dissimilarity in physiological tolerances of the related families Paguridae and Lithodidae to environmental conditions, and how this may have determined the divergence and radiation of the families into different distribution ranges, in particular with regard to the limited penetration of the deep sea by the Paguridae. This study investigates the physiological tolerances of the temperate shallow-water hermit crab, Pagurus cuanensis, to various temperature (5, 10, 15, 20°C) and pressure regimes (1 to 100 atm) by measuring the standard metabolic rate (SMR) and behavioural changes. SMR was primarily affected by temperature, with a notably low rate at 5°C throughout all pressures. Behaviour was affected by pressure, with an increase in pressure from 50 to 100 atmospheres (atm) resulting in reduced activity. It is suggested that this species can tolerate hydrostatic pressures greater than those found in its natural bathymetric range. It is discussed that a lack of physiological cold tolerance and ecological factors, such as the need to find gastropod shells for protection, are the principal restrictions maintaining P. cuanensis to a maximum depth of approximately 250 m. We hypothesize that temperate shallow-water invertebrates could indeed be able to penetrate greater depths as continental shelf waters warm up in the course of global climate change.
The early ontogenetic stages of the sub-Antarctic king crab Lithodes santolla were analyzed for the presence and activities of a set of important digestive enzymes. The eggs and non-feeding larvae (zoea I-III, megalopa) showed high activities of esterases, phosphatases, and exopeptidases indicating the enzymatic ability to utilize endogeneous yolk reserves. SDS-PAGE showed a continuous decrease of proteins or proteids in the range of 59-81 kDa during ontogenetic development from the eggs through the zoeal stages to the first juvenile crab stage, CI. This reduction reflects the degradation of storage compounds during lecithotrophic larval development. Activities of the endopeptidases, trypsin and chymotrypsin, were low in eggs and larvae but increased significantly in the first juvenile crab stage. These enzymes typically facilitate the first steps of proteolysis in the extra-cellular spaces of the midgut gland and in the stomach. Their scarcity indicates that the larvae of L. santolla are physiologically not prepared to digest external food. This ability seems to appear first in the CI stage. Extracts of juvenile midgut glands and the gastric fluids of adults showed high activities of a variety of digestive enzymes including phosphatases, carbohydrases, as well as endo-and exopeptidases. High activities of digestive enzymes in adults may compensate for scarce food supply and rate-limiting low temperatures in the predominantly sub-Antarctic habitats of L. santolla.
Temporal pattern of hatching was studied in the subantarctic lithodid crabs Lithodes santolla (Molina) and Paralomis granulosa (Jaquinot) from the Argentine Beagle Channel. In both species, larval hatching occurred in low daily numbers over an extended period of up to several weeks, depending on hatch size. Low daily hatching activity and low oxygen-consumption rates in freshly hatched P. granulosa larvae are discussed as life history adaptations to, and/or physiological constraints by, the environmental conditions of high latitudes.
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