Energy metabolism during embryonic development and larval growth of an Antarctic sea urchin

1999 ◽  
Vol 202 (15) ◽  
pp. 2041-2050 ◽  
Author(s):  
A.G. Marsh ◽  
P.K. Leong ◽  
D.T. Manahan

Developmental energetics of an Antarctic sea urchin, Sterechinus neumayeri, were quantified to describe the physiological bases underlying ontogenetic changes in metabolic rate at extreme cold temperatures (−1.5 degrees C). Rates of development from a four-arm to a six-arm larval stage were not affected by food availability. The respiratory cost of development to the six-arm larval stage (day 60) was 14.0 mJ for fed larvae and 8.2 mJ for unfed larvae. We observed three phases of metabolic regulation during development. During embryogenesis (day 0–22), increasing metabolic rates were proportional to increases in cell numbers. During early larval development (day 22–47), the differences in respiratory rate between fed and unfed larvae were not accounted for by cell number, but by cell-specific metabolic rate (respiratory rate normalized to DNA content). Once an advanced larval stage had been reached (day 47–60), cell-specific respiratory rate and mitochondrial densities (citrate synthase activity normalized to DNA content) were more equivalent between fed and unfed larvae, suggesting that size-specific metabolic rates were determined at a level of physiological regulation that was independent of cell numbers or feeding history.

1999 ◽  
Vol 202 (18) ◽  
pp. 2485-2493
Author(s):  
R.E. Bishop ◽  
J.J. Torres

Leptocephali are the unusual transparent larvae that are typical of eels, bonefish, tarpon and ladyfish. Unlike the larvae of all other fishes, leptocephali may remain in the plankton as larvae for several months before metamorphosing into the juvenile form. During their planktonic phase, leptocephali accumulate energy reserves in the form of glycosaminoglycans, which are then expended to fuel metamorphosis. The leptocephalus developmental strategy is thus fundamentally different from that exhibited in all other fishes in two respects: it is far longer in duration and energy reserves are accumulated. It was anticipated that the unusual character of leptocephalus development would be reflected in the energy budget of the larva. This study describes the allocation of energy to metabolism and excretion, two important elements of the energy budget. Metabolic rates were measured directly in four species of leptocephali, Paraconger caudilimbatus, Ariosoma balearicum, Gymnothorax saxicola and Ophichthus gomesii, using sealed-jar respirometry at sea. Direct measurements of metabolic rates were corroborated by measuring activities of lactate dehydrogenase and citrate synthase, two key enzymes of intermediary metabolism, in addition to that of Na(+)/K(+)-ATPase, a ubiquitous ion pump important in osmotic regulation. Excretion rates were determined by subsampling the sea water used in the respiratory incubations. The entire premetamorphic size range for each species was used in all assays. Mass-specific oxygen consumption rate, excretion rate and all enzyme activities (y) declined precipitously with increasing mass (M) according to the equation y=aM(b), where a is a species-specific constant and −1.74<b<-0.44. In leptocephali, the highly negative slope of the familiar allometric equation describing the relationship between mass-specific metabolic rate and mass, normally between −0.33 and 0, showed that a massive decline in metabolic rate occurs with increasing size. The result suggests that the proportion of actively metabolizing tissue also declines with size, being replaced in large measure by the metabolically inert energy depot, the glycosaminoglycans. Leptocephali can thus grow to a large size with minimal metabolic penalty, which is an unusual and successful developmental strategy.


2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Eric Ste-Marie ◽  
Yuuki Y. Watanabe ◽  
Jayson M. Semmens ◽  
Marianne Marcoux ◽  
Nigel E. Hussey

Abstract Metabolic rate is intricately linked to the ecology of organisms and can provide a framework to study the behaviour, life history, population dynamics, and trophic impact of a species. Acquiring measures of metabolic rate, however, has proven difficult for large water-breathing animals such as sharks, greatly limiting our understanding of the energetic lives of these highly threatened and ecologically important fish. Here, we provide the first estimates of resting and active routine metabolic rate for the longest lived vertebrate, the Greenland shark (Somniosus microcephalus). Estimates were acquired through field respirometry conducted on relatively large-bodied sharks (33–126 kg), including the largest individual shark studied via respirometry. We show that despite recording very low whole-animal resting metabolic rates for this species, estimates are within the confidence intervals predicted by derived interspecies allometric and temperature scaling relationships, suggesting this species may not be unique among sharks in this respect. Additionally, our results do not support the theory of metabolic cold adaptation which assumes that polar species maintain elevated metabolic rates to cope with the challenges of life at extreme cold temperatures.


2011 ◽  
Vol 69 (3) ◽  
pp. 460-464 ◽  
Author(s):  
Steve S. Doo ◽  
Symon A. Dworjanyn ◽  
Shawna A. Foo ◽  
Natalie A. Soars ◽  
Maria Byrne

Abstract Doo, S. S., Dworjanyn, S. A., Foo, S. A., Soars, N. A., and Byrne, M. 2012. Impacts of ocean acidification on development of the meroplanktonic larval stage of the sea urchin Centrostephanus rodgersii. – ICES Journal of Marine Science, 69: 460–464. The effects of near-future ocean acidification/hypercapnia on larval development were investigated in the sea urchin Centrostephanus rodgersii, a habitat-modifying species from eastern Australia. Decreased pH (−0.3 to −0.5 pH units) or increased pCO2 significantly reduced the percentage of normal larvae. Larval growth was negatively impacted with smaller larvae in the pH 7.6/1800 ppm treatments. The impact of acidification on development was similar on days 3 and 5, indicating deleterious effects early in development. On day 3, increased abnormalities in the pH 7.6/1600 ppm treatment were seen in aberrant prism stage larvae and arrested/dead embryos. By day 5, echinoplutei in this treatment had smaller arm rods. Observations of smaller larvae in C. rodgersii have significant implications for this species because larval success may be a potential bottleneck for persistence in a changing ocean.


Author(s):  
D L Swanson ◽  
T J Agin ◽  
Y Zhang ◽  
P Oboikovitz ◽  
S DuBay

Abstract The climatic variability hypothesis (CVH) posits that more flexible phenotypes should provide a fitness advantage for organisms experiencing more variable climates. While typically applied across geographically separated populations, whether this principle applies across seasons or other conditions (e.g., open vs. sheltered habitats) which differ in climatic variability remains essentially unstudied. In north-temperate climates, climatic variability in winter usually exceeds that in summer, so extending the CVH to within-population seasonal variation predicts that winter phenotypes should be more flexible than summer phenotypes. We tested this prediction of the within-season extension of the CVH by acclimating summer and winter-collected house sparrows (Passer domesticus) to 24, 5 and -10 °C and measuring basal (BMR) and summit (Msum = maximum cold-induced) metabolic rates before and after acclimation. To examine mechanistic bases for metabolic variation, we measured flight muscle and heart masses and citrate synthase and β-hydroxyacyl coA-dehydrogenase activities. BMR and Msum were higher for cold-acclimated than for warm-acclimated birds and BMR was higher in winter than in summer birds. Contrary to our hypothesis of greater responses to cold acclimation in winter birds, metabolic rates generally decreased over the acclimation period for winter birds at all temperatures but increased at cold temperatures for summer birds. Flight muscle and heart masses were not significantly correlated with season or acclimation treatment, except for supracoracoideus mass, which was lower at -10 °C in winter, but flight muscle and heart masses were positively correlated with BMR and flight muscle mass was positively correlated with Msum. Catabolic enzyme activities were not clearly related to metabolic variation. Thus, our data suggest that predictions of the CVH may not be relevant when extended to seasonal temperature variability at the within-population scale. Indeed, these data suggest that metabolic rates are more prominently upregulated in summer than in winter in response to cold. Metabolic rates tended to decrease during acclimation at all temperatures in winter, suggesting that initial metabolic rates at capture (higher in winter) influence metabolic acclimation for captive birds.


1995 ◽  
Vol 198 (1) ◽  
pp. 19-30 ◽  
Author(s):  
O Hoegh-Guldberg ◽  
D Manahan

Determining the metabolic rate of larval invertebrates from aquatic habitats is complicated by the problems of small size and the scarcity of suitable measurement techniques. In this study, coulometric respirometry (a new technique for the study of marine embryos and larvae) was used to explore several issues associated with the rate of energy use during embryonic and larval development of marine invertebrates from three phyla. Coulometric respirometry measures rates of oxygen consumption under normoxic conditions by electrochemically replacing the oxygen consumed by organisms during an experiment. This technique is based on the assumption that all electrons consumed by the anodic reactions result in the production of oxygen. We verify this assumption using direct measurements of oxygen production and show that the technique is sensitive enough (1 nmol O2 h-1) to quantify the oxygen consumption of a single individual swimming freely in a relatively large volume (2 ml). Continuous measurements can span days, and embryos in the coulometric respiration chambers develop to the larval stage at normal rates of differentiation. Measurements of metabolic rates were made with the coulometric respirometer during the complete life-span of larvae of three species (asteroid, Asterina miniata; bivalve, Crassostrea gigas; echinoid, Dendraster excentricus). For these species, metabolic power equations had mass exponents near unity (0.9­1.1), showing that metabolic rate scales isometrically with mass during larval growth. Metabolic rates were independent of the concentration of larvae used in the respirometer chambers for a range of larval concentrations from 4 to 400 larvae ml-1 (coulometric respirometer) and from 241 to 809 larvae ml-1 (polarographic oxygen sensor). Metabolic rates were measured using coulometric respirometry and two other commonly used techniques, polarographic oxygen sensors and Winkler's titration. Polarographic oxygen sensors in small, sealed chambers (100 µl) consistently gave the lowest values (by as much as 80 %) for the asteroid, echinoid and molluscan larvae. By comparison, rates of oxygen consumption measured using coulometric respirometry and Winkler's titration (to measure the change in oxygen concentration over time) were similar and consistently higher. Although the polarographic oxygen sensor is the most widely used method for measuring the metabolism of small animals in sealed 100­1000 µl chambers, it appears that the metabolism of some larvae is adversely affected by the conditions within these respirometers.


1977 ◽  
Vol 68 (1) ◽  
pp. 69-87
Author(s):  
BLOCK WILLIAM

Analysis of 148 measurements of individual respiration rate showed that although respiration was linearly related to live weight on a double log10 scale, there were significant differences between rates at 0°, + 50° and +10 °C. Proto- and deutonymphal metabolic rates were higher than other stages, especially at +10 °C. Q10 values ranged from 2.07 to 3.83 over 0° to +10 °C. Equations relating individual respiratory rate to live weight and temperature for A. antarcticus, and metabolic rate to temperature for 10 species of Antarctic terrestrial invertebrates were developed. Comparison with temperate data indicated considerable cold adaptation in the Antarctic species with 3–5 times increased metabolism. It was calculated that 78–82 % of the energy assimilated may be used in respiration by A. antarcticus.


2020 ◽  
Vol 8 (1) ◽  
Author(s):  
Louise C Archer ◽  
Stephen A Hutton ◽  
Luke Harman ◽  
W Russell Poole ◽  
Patrick Gargan ◽  
...  

Abstract Metabolic rates vary hugely within and between populations, yet we know relatively little about factors causing intraspecific variation. Since metabolic rate determines the energetic cost of life, uncovering these sources of variation is important to understand and forecast responses to environmental change. Moreover, few studies have examined factors causing intraspecific variation in metabolic flexibility. We explore how extrinsic environmental conditions and intrinsic factors contribute to variation in metabolic traits in brown trout, an iconic and polymorphic species that is threatened across much of its native range. We measured metabolic traits in offspring from two wild populations that naturally show life-history variation in migratory tactics (one anadromous, i.e. sea-migratory, one non-anadromous) that we reared under either optimal food or experimental conditions of long-term food restriction (lasting between 7 and 17 months). Both populations showed decreased standard metabolic rates (SMR—baseline energy requirements) under low food conditions. The anadromous population had higher maximum metabolic rate (MMR) than the non-anadromous population, and marginally higher SMR. The MMR difference was greater than SMR and consequently aerobic scope (AS) was higher in the anadromous population. MMR and AS were both higher in males than females. The anadromous population also had higher AS under low food compared to optimal food conditions, consistent with population-specific effects of food restriction on AS. Our results suggest different components of metabolic rate can vary in their response to environmental conditions, and according to intrinsic (population-background/sex) effects. Populations might further differ in their flexibility of metabolic traits, potentially due to intrinsic factors related to life history (e.g. migratory tactics). More comparisons of populations/individuals with divergent life histories will help to reveal this. Overall, our study suggests that incorporating an understanding of metabolic trait variation and flexibility and linking this to life history and demography will improve our ability to conserve populations experiencing global change.


BMC Biology ◽  
2021 ◽  
Vol 19 (1) ◽  
Author(s):  
Isabella Loughland ◽  
Alexander Little ◽  
Frank Seebacher

Abstract Background Thermal plasticity is pivotal for evolution in changing climates and in mediating resilience to its potentially negative effects. The efficacy to respond to environmental change depends on underlying mechanisms. DNA methylation induced by DNA methyltransferase 3 enzymes in the germline or during early embryonic development may be correlated with responses to environmental change. This developmental plasticity can interact with reversible acclimation within adult organisms, which would increase the speed of response and could alleviate potential mismatches between parental or early embryonic environments and those experienced at later life stages. Our aim was to determine whether there is a causative relationship between DNMT3 enzyme and developmental thermal plasticity and whether either or both interact with short-term acclimation to alter fitness and thermal responses in zebrafish (Danio rerio). Results We developed a novel DNMT3a knock-out model to show that sequential knock-out of DNA methyltransferase 3a isoforms (DNMT3aa−/− and DNMT3aa−/−ab−/−) additively decreased survival and increased deformities when cold developmental temperatures in zebrafish offspring mismatched warm temperatures experienced by parents. Interestingly, short-term cold acclimation of parents before breeding rescued DNMT3a knock-out offspring by restoring survival at cold temperatures. DNMT3a knock-out genotype interacted with developmental temperatures to modify thermal performance curves in offspring, where at least one DNMT3a isoform was necessary to buffer locomotion from increasing temperatures. The thermal sensitivity of citrate synthase activity, an indicator of mitochondrial density, was less severely affected by DNMT3a knock-out, but there was nonetheless a significant interaction between genotype and developmental temperatures. Conclusions Our results show that DNMT3a regulates developmental thermal plasticity and that the phenotypic effects of different DNMT3a isoforms are additive. However, DNMT3a interacts with other mechanisms, such as histone (de)acetylation, induced during short-term acclimation to buffer phenotypes from environmental change. Interactions between these mechanisms make phenotypic compensation for climate change more efficient and make it less likely that thermal plasticity incurs a cost resulting from environmental mismatches.


1978 ◽  
Vol 35 (6) ◽  
pp. 816-821 ◽  
Author(s):  
J. R. Brett ◽  
J. M. Blackburn

The metabolic rate of spiny dogfish, Squalus acanthias, was determined in both a tunnel respirometer and a large, covered, circular tank (mass respirometer). Swimming performance was very poor in the respirometer, so that a power–performance curve could not be established. Instead, resting metabolic rates were determined, with higher rates induced by causing heavy thrashing (active metabolism). Routine metabolic rates were measured for the spontaneous activity characterizing behavior in the circular tank. For fish of 2 kg mean weight, the metabolic rates at 10 °C were 32.4 ± 2.6 SE (resting), 49.2 ± 5.0 SE (routine), and 88.4 ± 4.6 SE (active) mg O2∙kg−1∙h−1. Assuming that the routine rate represents a general energy expenditure in nature, this is equivalent to metabolizing about 3.8 kcal∙kg−1∙d−1 (15.9 × 103 J∙kg−1∙d−1). Key words: dogfish, metabolic rates, energetics, respiration


2018 ◽  
Vol 75 (6) ◽  
pp. 2117-2128 ◽  
Author(s):  
Samuel P S Rastrick ◽  
Victoria Collier ◽  
Helen Graham ◽  
Tore Strohmeier ◽  
Nia M Whiteley ◽  
...  

Abstract Climate change driven alterations in salinity and carbonate chemistry are predicted to have significant implications particularly for northern costal organisms, including the economically important filter feeders Mytilus edulis and Ciona intestinalis. However, despite a growing number of studies investigating the biological effects of multiple environmental stressors, the combined effects of elevated pCO2 and reduced salinity remain comparatively understudied. Changes in metabolic costs associated with homeostasis and feeding/digestion in response to environmental stressors may reallocate energy from growth and reproduction, affecting performance. Although these energetic trade-offs in response to changes in routine metabolic rates have been well demonstrated fewer studies have investigated how these are affected by changes in feeding plasticity. Consequently, the present study investigated the combined effects of 26 days’ exposure to elevated pCO2 (500 µatm and 1000 µatm) and reduced salinity (30, 23, and 16) on the energy available for growth and performance (Scope for Growth) in M. edulis and C. intestinalis, and the role of metabolic rate (oxygen uptake) and feeding plasticity [clearance rate (CR) and absorption efficiency] in this process. In M. edulis exposure to elevated pCO2 resulted in a 50% reduction in Scope for Growth. However, elevated pCO2 had a much greater effect on C. intestinalis, with more than a 70% reduction in Scope for Growth. In M. edulis negative responses to elevated pCO2 are also unlikely be further affected by changes in salinity between 16 and 30. Whereas, under future predicted levels of pCO2C. intestinalis showed 100% mortality at a salinity of 16, and a >90% decrease in Scope for Growth with reduced biomass at a salinity of 23. Importantly, this work demonstrates energy available for production is more dependent on feeding plasticity, i.e. the ability to regulate CR and absorption efficiency, in response to multiple stressors than on more commonly studied changes in metabolic rates.


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