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Abstract The theory describing the evolution of offspring size often assumes that the production cost per unit volume is the same for small and large offspring. However, this may not be true if indirect costs of reproduction (e.g., material and energetic costs of supporting offspring development) scale disproportionately with offspring size. Here we show how direct and indirect costs of reproduction can be explicitly modeled within the Smith–Fretwell framework and how observations of size-number relationships can thus be used to evaluate indirect costs. We applied this analysis to measures of egg volume and fecundity for over 300 individuals of a coastal fish species and found that the tradeoff was much stronger than the expected inverse (fecundity scaled with volume−1.843). Larger offspring were thus more expensive to produce. For our study species, an important indirect cost was that larger eggs were accompanied by disproportionately more ovarian fluid. Calorimetry and removal experiments were used to further measure both the energetic costs and fitness benefits of ovarian fluid. In addition, we show that indirect costs of reproduction can intensify size-number tradeoffs in a variety of fishes. Indirect costs of reproduction can be large and may therefore play an important role in the evolution of offspring size. 

Ocean acidification (OA) presents a unique challenge to early life stages of marine species. Developing organisms must balance the need to grow rapidly with the energetic demands of maintaining homeostasis. The small sizes of early life stages can make them highly sensitive to changes in environmental CO₂levels, but studies have found wide variation in responses to OA. Thus far most OA studies have manipulated CO₂only, and modifying factors need to be considered in greater detail. We investigated the effects of high pCO₂and food ration on rates of growth and mortality of a coastal fish, the California Grunion (Leuresthes tenuis). We also examined how CO₂and food levels affected feeding success, metabolic rate, and swimming activity – processes reflective of energy acquisition and expenditure. In general, exposure to high CO₂decreased energy intake by reducing feeding success, and increased energy expenditure by increasing metabolic rate and routine swimming speed, though the magnitudes of these effects varied somewhat with age. Despite these changes in energetics, growth of biomass was not affected significantly by pCO₂level but was reduced by low ration level, and we did not detect an interactive effect of food ration and pCO₂on growth. However, under OA conditions, larvae were in poorer condition (as evaluated by the mass to length ratio) by the end of the experiment and our analysis of mortality revealed a significant interaction in which the effects of OA were more lethal when food energy was limited. These results are consistent with the idea that although energy can be reallocated to preserve biomass growth, increased energetic demand under ocean acidification may draw energy away from maintenance, including those processes that foster homeostasis during development. Overall, these results highlight both the need to consider the availability of food energy as a force governing species’ responses to ocean acidification and the need to explicitly consider the energy allocated to both growth and maintenance as climate changes. 

Rising temperatures have important consequences for somatic growth, but observed relationships between temperature and growth can vary in both magnitude and direction. The key to understanding such variation is knowing how temperature affects both the amount of energy available for growth and the efficiency with which surplus energy is assimilated into the body. We tested the hypothesis that patterns of temperature-dependent growth are driven by differential sensitivities of energy intake and expenditure to temperature. Larvae of California grunion Leuresthes tenuis were reared across a range of temperatures and 2 levels of food availability. Energy intake was measured from feeding rate, and energy expenditure was evaluated by measuring respiration and excretion rates. When food was abundant, both intake and expenditure increased with temperature, but intake increased more rapidly. These results suggest that high temperatures should lead to faster growth, and these predictions were confirmed by a separate experiment. In contrast, when food was restricted, the increase in energetic demand with temperature outpaced energy intake, suggesting a dwindling surplus of energy at high temperatures. This predicted reversal of the effects of temperature on growth was also confirmed experimentally. Finally, we compared patterns of energetics and growth to test the effects of temperature on food assimilation efficiency. When food was unlimited, assimilation efficiency decreased rapidly with temperature. When food was restricted, assimilation efficiency remained relatively high. Overall, our results emphasize the value of a bioenergetic perspective for illuminating why and how growth rates are likely to change in a warming ocean.