Ecophysiological studies on developing eggs and ovigerous females of intertidal crabs (1996)
AuthorsLeelapiyanart, Nongnudshow all
Morphological, ecological and physiological adaptations of ovigerous crabs and their developing eggs to conditions on shore were compared in two species of New Zealand intertidal crabs. Newly-laid eggs of both Heterozius rotundifrons and Cyclograpsus lavauxi are ellipsoidal, with initial mean volume of 204 and 10 nL respectively, increasing to 360 and 19 nL respectively before hatching. The incubation periods of eggs of H. rotundifrons and C. lavauxi were 194±3 and 56±1 days respectively at constant 15°C. Morphological criteria and timing of the 5 major developmental stages are reported: (1) Newly laid egg stage (2) Blastula stage (3) Gastrula stage (4) Eyespot and pigmentation stage and (5) Heart-beating stage. Two major membranes surround developing eggs at both early and late stages of H. rotundifrons. The thickness of the outer and inner membranes are approximately 3.4-4.8 and 0.6-0.9 µm respectively and are separated by a perivitelline space. The timing of larval release was examined during continuous immersion (and continuing light/dark cycle) in ovigerous H. rotundifrons and C. lavauxi entrained to experimental tidal and light/dark cycles. For H. rotundifrons, larval release occurred over 4-6 consecutive days only during the dark phase at times related to both the light/dark and tidal cycles. For C. lavauxi, larval release was a single event occurring during high tide period at both light and dark phases. Detached eggs of both crab species were able to hatch into larvae independently of the female although the percentage hatching was low. In H rotundifrons, at 15°C, resting mass-specific Mo2 of non-ovigerous and ovigerous crabs was of similar magnitude in air and water but for C. lavauxi, M02 was about two times higher in air. In both species, in air and in water, the mass-specific Mo2 of ovigerous crabs (adults and eggs combined) was higher than in non-ovigerous crabs, the difference being greatest in crabs with late stage eggs. Mo2 of developing eggs of H. rotundifrons and C. lavauxi was measured in seawater at 15°C. In both species, Mo2 of eggs increased 10-12 times, the major increase being toward the end of their development. The cost of development, estimated from total O2 consumption of single eggs of H. rotundifrons and C. lavauxi, was 1.517 and 0.077 µmol O2 respectively. The 20-fold ratio is approximately equal to the ratio of their masses (about 19 times). The elevated metabolic rates of ovigerous crabs can largely be accounted for by the increased metabolism of the eggs. However, a significant unexplained component of the elevation in H rotundifrons suggests a small metabolic cost of bearing eggs. In response to declining oxygen tension, eggs of H rotundifrons and C. lavauxi exhibited characteristics of oxygen conformers and regulators respectively. The Pcrit value for eggs at stage 5D of C. lavauxi was approximately 45 mmHg. The lactate concentration in eggs of H rotundifrons increased from about 0.602 mmol.L-1 in normoxic eggs to about 10.20 mmol.L-1 after 3 hours hypoxic exposure. The rate of lactate accumulation during hypoxia suggests that the eggs are not sustaining metabolism by anaerobiosis, but are allowing metabolic depression. In H rotundifrons, no specific respiratory behaviour was associated with egg-bearing. Upon exposure to hypoxia, non-ovigerous and ovigerous crabs showed similar "emersion behaviour" (initial agitation, followed by leg extension and abdominal elevation and later quiescence). There was no difference in heart rates and scaphognathite activities between non-ovigerous and ovigerous H rotundifrons. Both non-ovigerous and ovigerous crabs of this species showed decreased heart and ventilation rates in response to hypoxia which is similar to the behaviour found in other shore crabs. Both early and late stage eggs of H rotundifrons and C. lavauxi survived 24 hours exposure to dilute seawater and fresh water. Late stage eggs were more tolerant of reduced salinity than early stage eggs. Similar relationships existed when these eggs were acclimated for 96 hours to 50% seawater. In both species, eggs were hyperosmotic to the external medium in all salinities. The osmolalities of eggs were relatively insensitive to the external salinity and, even in fresh water,' maintained osmolality equivalent to 70% seawater. Eggs exhibited remarkably little volume change over the same range of ambient salinities. Measurements of four cations (Na+, K+, Ca2+, Mg2+) in eggs at different stages after 24 hours exposure to a range of salinities, at 15°C, demonstrated that internal ions are retained and regulated differently at different egg stages. The overall concentrations of all four cations increased during development and decreased as salinities decreased. Sodium and potassium are the main cations in the eggs. Sodium was consistently hypo-ionic and potassium hyper-ionic compared with seawater. Sodium and magnesium concentrations changed at a proportionally greater rate with dilution than did potassium and calcium. These observations are consistent with location for most of the sodium and magnesium in a small compartment between the permeable outer egg membrane and the embryo itself and with an embryonic (in the cells, blastocoel or yolk) location for most of the potassium and calcium. Water and sodium influx studies suggested that egg membranes of H. rotundifrons are very permeable to water and salt throughout their development. Eggs at the early stage are more permeable to water but less permeable to sodium than eggs at the late stage. There are two components of water and sodium exchange in all egg stages of H. rotundifrons: a small rapidly exchanging or "fast pool" (outer pool) and a much larger, slowly exchanging or "slow pool" (inner pool). The outer pool is thought to represent the perivitelline space of eggs (4-8% of volume throughout development). The volume of exchangeable water in the inner pool increased with egg development. Eggs at stage 2 and 5D acclimated to 50% seawater showed a permeability to water and sodium less than eggs acclimated to 100% seawater. Such a mechanism would be advantageous in an intertidal environment by limiting the work required to balance the osmotic influx of water and the loss of sodium. The results of this study provided information on the ecology and physiology of ovigerous crabs and developing eggs and suggested that the eggs of both H. Rotundifrons and C. lavauxi could survive periods of hypoxia that might be encountered when the female is partially buried at low tide or in shallow pools. Additionally, the eggs could cope physiologically with periods of dilution of the surface water by precipitation or freshwater seepage. Measurements of sodium and water fluxes indicated that, contrary to earlier suggestions, the eggs are highly permeable and are in dynamic exchange with the seawater at all stages.