Elevated CO2 affects embryonic development and larval phototaxis in a temperate marine fish

As an effect of anthropogenic CO2 emissions, the chemistry of the world's oceans is changing. Understanding how this will affect marine organisms and ecosystems are critical in predicting the impacts of this ongoing ocean acidification. Work on coral reef fishes has revealed dramatic effects of elevated oceanic CO2 on sensory responses and behavior. Such effects may be widespread but have almost exclusively been tested on tropical reef fishes. Here we test the effects elevated CO2 has on the reproduction and early life history stages of a temperate coastal goby with paternal care by allowing goby pairs to reproduce naturally in an aquarium with either elevated (ca 1400 µatm) CO2 or control seawater (ca 370 µatm CO2). Elevated CO2 did not affect the occurrence of spawning nor clutch size, but increased embryonic abnormalities and egg loss. Moreover, we found that elevated CO2 significantly affected the phototactic response of newly hatched larvae. Phototaxis is a vision-related fundamental behavior of many marine fishes, but has never before been tested in the context of ocean acidification. Our findings suggest that ocean acidification affects embryonic development and sensory responses in temperate fishes, with potentially important implications for fish recruitment.

Effects of elevated CO2 on early life history development of the yellowtail kingfish, Seriola lalandi, a large pelagic fish

An increasing number of studies have examined the effects of elevated carbon dioxide (CO2) and ocean acidification on marine fish, yet little is known about the effects on large pelagic fish. We tested the effects of elevated CO2 on the early life history development and behaviour of yellowtail kingfish, Seriola lalandi. Eggs and larvae were reared in current day control (450 µatm) and two elevated CO2 treatments for a total of 6 d, from 12 h post-fertilization until 3 d post-hatching (dph). Elevated CO2 treatments matched projections for the open ocean by the year 2100 under RCP 8.5 (880 µatm CO2) and a higher level (1700 µatm CO2) relevant to upwelling zones where pelagic fish often spawn. There was no effect of elevated CO2 on survival to hatching or 3 dph. Oil globule diameter decreased with an increasing CO2 level, indicating potential effects of elevated CO2 on energy utilization of newly hatched larvae, but other morphometric traits did not differ among treatments. Contrary to expectations, there were no effects of elevated CO2 on larval behaviour. Activity level, startle response, and phototaxis did not differ among treatments. Our results contrast with findings for reef fish, where a wide range of sensory and behavioural effects have been reported. We hypothesize that the absence of behavioural effects in 3 dph yellowtail kingfish is due to the early developmental state of newly hatched pelagic fish. Behavioural effects of high CO2 may not occur until larvae commence branchial acid-base regulation when the gills develop; however, further studies are required to test this hypothesis. Our results suggest that the early stages of kingfish development are tolerant to rising CO2 levels in the ocean.

Effects of pre-hatching pCO2 on development and survival of zoea stages of Arctic spider crab Hyas araneus

Sensitivity of marine crustaceans to anthropogenic CO2 emissions and the associated acidification of the oceans may be less than that of other, especially lower, invertebrates. However, effects on critical transition phases or carry-over effects between life stages have not comprehensively been explored. Here we report the impact of elevated seawater PCO2 values (3100 µatm) on Hyas araneus during the last 2 weeks of their embryonic development (pre-hatching phase) and during development while in the consecutive zoea I and zoea II larval stages (post-hatching phase). We measured oxygen consumption, dry weight, developmental time and mortality in zoea I to assess changes in performance. Feeding rates and survival under starvation were investigated at different temperatures to detect differences in thermal sensitivities of zoea I and zoea II larvae depending on pre-hatch history. When embryos were pre-exposed to elevated PCO2 during maternal care, mortality increased about 60% under continued CO2 exposure during the zoea I phase. The larvae that moulted into zoea II, displayed a developmental delay by about 20 days compared to larvae exposed to control PCO2 during embryonic and zoeal phases. Elevated PCO2 caused a reduction in zoea I dry weight and feeding rates, while survival of the starved larvae was not affected by the seawater CO2 concentration. In conclusion, CO2 effects on egg masses under maternal care carried over to the first larval stages of crustaceans and reduced their survival and development to levels below those previously reported in studies exclusively focussing on acute PCO2 effects on the larval stages.

Physiology, growth and development of larval krill ''Euphausia superba'' in autumn and winter in the Lazarev Sea, Antarctica

The physiological condition of larval Antarctic krill was investigated during austral autumn 2004 and winter 2006 in the Lazarev Sea, to provide better understanding of a critical period of their life cycle. The condition of larvae was quantified in both seasons by determining their body length (BL), dry mass (DM), elemental- and biochemical composition, as well as stomach content analysis, and rates of metabolism and growth. Overall the larvae in autumn were in better condition under the ice than in open water, and for those under the ice there was a decrease in condition from autumn to winter. Thus growth rates of furcilia larvae in open water in autumn were similar to winter values under the ice (mean 0.008 mm/d), whereas autumn, under ice values were higher: 0.015 mm/d. Equivalent larval stages had up to 30% lower BL and 70% lower DM in winter compared to autumn, with mean oxygen consumption 44% lower (0.54 µl O2 DM/h). However, their ammonium excretion rates doubled (from 0.03-0.06 µg NH4 DM/h) so their mean O:N ratio was 46 in autumn and 15 in winter. Thus differing metabolic substrates were used between autumn and winter, suggesting a flexible overwintering strategy, as suggested for adults. The larvae were eating small copepods (Oithona spp.) and/or protozoans as well as autotrophic food under the ice. However, pelagic Chlorophyll a (Chl a) was a good predictor for growth in both seasons. The physics (current speed/ice topography) probably has a critical part to play in whether larval krill can exploit the food that may be associated with sea ice or be advected away from such suitable feeding habitat.

Fertilisation and larval development in an Antarctic bivalve, Laternula elliptica, under reduced pH and elevated temperatures

Elevated temperatures associated with ocean warming and acidification can influence development and, ultimately, success of larval molluscs. The effect of projected oceanic changes on fertilisation and larval development in an Antarctic bivalve, Laternula elliptica, was investigated through successive larval stages at ambient temperature and pH conditions (-1.6°C and pH 7.98) and conditions representative of projections through to 2100 (-0.5°C to +0.4°C and pH 7.80 to pH 7.65). Where significant effects were detected, increased temperature had a consistently positive influence on larval development, regardless of pH level, while effects of reduced pH varied with larval stage and incubation temperature. Fertilisation was high and largely independent of stressors, with no loss of gamete viability. Mortality was unaffected at all development stages under experimental conditions. Elevated temperatures reduced occurrences of abnormalities in D-larvae and accelerated larval development through late veliger and D-larval stages, with D-larvae occurring 5 d sooner at 0.4°C compared to ambient temperature. Reduced pH did not affect occurrences of abnormalities in larvae, but it slowed the development of calcifying stages. More work is required to investigate the effects of developmental delays of the magnitude seen here in order to better determine the ecological relevance of these changes on longer term larval and juvenile success.

Maintained larval growth in mussel larvae exposed to acidified undersaturated seawater

Ocean acidification (OA) is known to affect bivalve early life-stages. We tested responses of blue mussel larvae to a wide range of pH in order to identify their tolerance threshold. Our results confirmed that decreasing seawater pH and decreasing saturation state increases larval mortality rate and the percentage of abnormally developing larvae. Virtually no larvae reared at average pHT 7.16 were able to feed or reach the D-shell stage and their development appeared to be arrested at the trochophore stage. However larvae were capable of reaching the D-shell stage under milder acidification (pHT=7.35, 7.6, 7.85) including in under-saturated seawater with omega Aragonite as low as 0.54±0.01 (mean±s. e. m.), with a tipping point for normal development identified at pHT 7.765. Additionally growth rate of normally developing larvae was not affected by lower pHT despite potential increased energy costs associated with compensatory calcification in response to increased shell dissolution. Overall, our results on OA impacts on mussel larvae suggest an average pHT of 7.16 is beyond their physiological tolerance threshold and indicate a shift in energy allocation towards growth in some individuals revealing potential OA resilience.

Seawater carbonate chemistry and skeletal development, size, weight, total lipid and symbiont density of coral Favia fragum in a laboratory experiment

Ocean acidification (OA) threatens the existence of coral reefs by slowing the rate of calcium carbonate (CaCO3) production of framework-building corals thus reducing the amount of CaCO3 the reef can produce to counteract natural dissolution. Some evidence exists to suggest that elevated levels of dissolved inorganic nutrients can reduce the impact of OA on coral calcification. Here, we investigated the potential for enhanced energetic status of juvenile corals, achieved via heterotrophic feeding, to modulate the negative impact of OA on calcification. Larvae of the common Atlantic golf ball coral, Favia fragum, were collected and reared for 3 weeks under ambient (421 µatm) or significantly elevated (1,311 µatm) CO2 conditions. The metamorphosed, zooxanthellate spat were either fed brine shrimp (i.e., received nutrition from photosynthesis plus heterotrophy) or not fed (i.e., primarily autotrophic). Regardless of CO2 condition, the skeletons of fed corals exhibited accelerated development of septal cycles and were larger than those of unfed corals. At each CO2 level, fed corals accreted more CaCO3 than unfed corals, and fed corals reared under 1,311 µatm CO2 accreted as much CaCO3 as unfed corals reared under ambient CO2. However, feeding did not alter the sensitivity of calcification to increased CO2; Delta calcification/Delta Omega was comparable for fed and unfed corals. Our results suggest that calcification rates of nutritionally replete juvenile corals will decline as OA intensifies over the course of this century. Critically, however, such corals could maintain higher rates of skeletal growth and CaCO3 production under OA than those in nutritionally limited environments.

Effects of ocean acidification on embryonic respiration and development of a temperate wrasse living along a natural CO2 gradient

Volcanic CO2 seeps provide opportunities to investigate the effects of ocean acidification on organisms in the wild. To understand the influence of increasing CO2 concentrations on the metabolic rate (oxygen consumption) and the development of ocellated wrasse early life stages, we ran two field experiments, collecting embryos from nesting sites with different partial pressures of CO2 [pCO2; ambient (400 µatm) and high (800-1000 µatm)] and reciprocally transplanting embryos from ambient- to high-CO2 sites for 30 h. Ocellated wrasse offspring brooded in different CO2 conditions had similar responses, but after transplanting portions of nests to the high-CO2 site, embryos from parents that spawned in ambient conditions had higher metabolic rates. Although metabolic phenotypic plasticity may show a positive response to high CO2, it often comes at a cost, in this case as a smaller size at hatching. This can have adverse effects because smaller larvae often exhibit a lower survival in the wild. However, the adverse effects of increased CO2 on metabolism and development did not occur when embryos from the high-CO2 nesting site were exposed to ambient conditions, suggesting that offspring from the high-CO2 nesting site could be resilient to a wider range of pCO2 values than those belonging to the site with present-day pCO2 levels. Our study identifies a crucial need to increase the number of studies dealing with these processes under global change trajectories and to expand these to naturally high-CO2 environments, in order to assess further the adaptive plasticity mechanism that encompasses non-genetic inheritance (epigenetics) through parental exposure and other downstream consequences, such as survival of larvae.