Abiotic conditions in cephalopod (Sepia officinalis) eggs: embryonic development at low pH and high pCO2

Low pO(2) values have been measured in the perivitelline fluids (PVF) of marine animal eggs on several occasions, especially towards the end of development, when embryonic oxygen consumption is at its peak and the egg case acts as a massive barrier to diffusion. Several authors have therefore suggested that oxygen availability is the key factor leading to hatching. However, there have been no measurements of PVF pCO(2) so far. This is surprising, as elevated pCO(2) could also constitute a major abiotic stressor for the developing embryo. As a first attempt to fill this gap in knowledge, we measured pO(2), pCO(2) and pH in the PVF of late cephalopod (Sepia officinalis) eggs. We found linear relationships between embryo wet mass and pO(2), pCO(2) and pH. pO(2) declined from > 12 kPa to less than 5 kPa, while pCO(2) increased from 0.13 to 0.41 kPa. In the absence of active accumulation of bicarbonate in the PVF, pH decreased from 7.7 to 7.2. Our study supports the idea that oxygen becomes limiting in cephalopod eggs towards the end of development; however, pCO(2) and pH shift to levels that have caused significant physiological disturbances in other marine ectothermic animals. Future research needs to address the physiological adaptations that enable the embryo to cope with the adverse abiotic conditions in their egg environment

Ecological pressures and the contrasting scaling of metabolism and body shape in coexisting taxa: cephalopods versus teleost fish

Metabolic rates are fundamental to many biological processes, and commonly scale with body size with an exponent ( bR) between 2/3 and 1 for reasons still debated. According to the 'metabolic-level boundaries hypothesis', bR depends on the metabolic level ( LR). We test this prediction and show that across cephalopod species intraspecific bR correlates positively with not only LR but also the scaling of body surface area with body mass. Cephalopod species with high LR maintain near constant mass-specific metabolic rates, growth and probably inner-mantle surface area for exchange of respiratory gases or wastes throughout their lives. By contrast, teleost fish show a negative correlation between bR and LR. We hypothesize that this striking taxonomic difference arises because both resource supply and demand scale differently in fish and cephalopods, as a result of contrasting mortality and energetic pressures, likely related to different locomotion costs and predation pressure. Cephalopods with high LR exhibit relatively steep scaling of growth, locomotion, and resource-exchange surface area, made possible by body-shape shifting. We suggest that differences in lifestyle, growth and body shape with changing water depth may be useful for predicting contrasting metabolic scaling for coexisting animals of similar sizes. This article is part of the theme issue 'Physiological diversity, biodiversity patterns and global climate change: testing key hypotheses involving temperature and oxygen'

Analysis of cutaneous and internal gill gas exchange morphology in early larval amphibians, Pseudophryne bibronii and Crinia georgiana

This study uses stereological techniques to examine body, internal gill and cardiovascular morphology of two larval amphibians, Pseudophryne bibronii and Crinia georgiana, to evaluate the roles of diffusive and convective gas exchange. Gosner stage 27 specimens were prepared for light microscopy and six parallel sections of equal distance taken through the body as well as a further six through the heart and internal gills. Body, internal gill and heart volume as well as body and internal gill surface areas were determined. The harmonic mean distance across the internal gills was also measured and used to estimate oxygen diffusive conductance, DO2. The species were of similar body size and surface area, but the heart and internal gills were larger in P. bibronii, which may represent precursors for greater growth of the species beyond stage 27. The much larger surface area of the skin compared to the internal gills in both species suggests it is the main site for gas exchange, with the gills supplementing oxygen uptake. The sparse cutaneous capillary network suggests diffusion is the main oxygen transport mechanism across the skin and directly into deeper tissues. A numerical model that simplifies larval shape, and has an internal (axial vessels) and external oxygen source, confirms that diffusion is able to maintain tissue oxygen with limited convective input.Casey A. Mueller, Roger S. Seymou

The energy cost of embryonic development in fishes and amphibians, with emphasis on new data from the Australian lungfish, Neoceratodus forsteri

The rate of oxygen consumption throughout embryonic development is used to indirectly determine the ‘cost’ of development, which includes both differentiation and growth. This cost is affected by temperature and the duration of incubation in anamniote fish and amphibian embryos. The influences of temperature on embryonic development rate, respiration rate and energetics were investigated in the Australian lungfish, Neoceratodus forsteri, and compared with published data. Developmental stage and oxygen consumption rate were measured until hatching, upon which wet and dry gut-free masses were determined. A measure of the cost of development, the total oxygen required to produce 1 mg of embryonic dry tissue, increased as temperature decreased. The relationship between the oxygen cost of development (C, ml mg−1) and dry hatchling mass (M, mg) in fishes and amphibians is described by C = 0.30 M0.22 ± 0.13 (95% CI), r 2 = 0.52. The scaling exponent indicates that the cost of embryonic development increases disproportionally with increasing hatchling mass. At 15 and 20°C, N. forsteri cost of development is significantly lower than the regression mean for all species, and at 25°C is lower than the allometrically scaled data set. Unexpectedly, incubation of N. forsteri is long, despite natural development under relatively warm conditions, and may be related to a large genome size. The low cost of development may be associated with construction of a rather sluggish fish with a low capacity for aerobic metabolism. The metabolic rate is lower in N. forsteri hatchlings than in any other fishes or amphibians at the same temperature, which matches the extremely low aerobic metabolic scope of the juveniles.Casey A. Mueller, Jean M. P. Joss and Roger S. Seymou