Diel and tidal pCO2?×?O2 fluctuations provide physiological refuge to early life stages of a coastal forage fish.
ABSTRACT: Coastal ecosystems experience substantial natural fluctuations in pCO2 and dissolved oxygen (DO) conditions on diel, tidal, seasonal and interannual timescales. Rising carbon dioxide emissions and anthropogenic nutrient input are expected to increase these pCO2 and DO cycles in severity and duration of acidification and hypoxia. How coastal marine organisms respond to natural pCO2?×?DO variability and future climate change remains largely unknown. Here, we assess the impact of static and cycling pCO2?×?DO conditions of various magnitudes and frequencies on early life survival and growth of an important coastal forage fish, Menidia menidia. Static low DO conditions severely decreased embryo survival, larval survival, time to 50% hatch, size at hatch and post-larval growth rates. Static elevated pCO2 did not affect most response traits, however, a synergistic negative effect did occur on embryo survival under hypoxic conditions (3.0?mg?L-1). Cycling pCO2?×?DO, however, reduced these negative effects of static conditions on all response traits with the magnitude of fluctuations influencing the extent of this reduction. This indicates that fluctuations in pCO2 and DO may benefit coastal organisms by providing periodic physiological refuge from stressful conditions, which could promote species adaptability to climate change.
Project description:Atmospheric CO2 levels have been increasing at an unprecedented rate due to anthropogenic activity. Consequently, ocean pCO2 is increasing and pH decreasing, affecting marine life, including fish. For many coastal marine fishes, selection of the adult habitat occurs at the end of the pelagic larval phase. Fish larvae use a range of sensory cues, including sound, for locating settlement habitat. This study tested the effect of elevated CO2 on the ability of settlement-stage temperate fish to use auditory cues from adult coastal reef habitats. Wild late larval stages of painted goby (Pomatoschistus pictus) were exposed to control pCO2 (532 ?atm, pH 8.06) and high pCO2 (1503 ?atm, pH 7.66) conditions, likely to occur in nearshore regions subjected to upwelling events by the end of the century, and tested in an auditory choice chamber for their preference or avoidance to nighttime reef recordings. Fish reared in control pCO2 conditions discriminated reef soundscapes and were attracted by reef recordings. This behaviour changed in fish reared in the high CO2 conditions, with settlement-stage larvae strongly avoiding reef recordings. This study provides evidence that ocean acidification might affect the auditory responses of larval stages of temperate reef fish species, with potentially significant impacts on their survival.
Project description:Coastal organisms reside in highly dynamic habitats. Global climate change is expected to alter not only the mean of the physical conditions experienced but also the frequencies and/or the magnitude of fluctuations of environmental factors. Understanding responses in an ecologically relevant context is essential for formulating management strategies. In particular, there are increasing suggestions that exposure to fluctuations could alleviate the impact of climate change-related stressors by selecting for plasticity that may help acclimatization to future conditions. However, it remains unclear whether the presence of fluctuations alone is sufficient to confer such effects or whether the pattern of the fluctuations matters. Therefore, we investigated the role of frequency and initial conditions of the fluctuations on performance by exposing larval sea urchin Heliocidaris crassispina to either constant or fluctuating pH. Reduced pH alone (pH 7.3 vs 8.0) did not affect larval mortality but reduced the growth of larval arms in the static pH treatments. Changes in morphology could affect the swimming mechanics for these small organisms, and geometric morphometric analysis further suggested an overall shape change such that acidified larvae had more U-shaped bodies and shorter arms, which would help maintain stability in moving water. The relative negative impact of lower pH, computed as log response ratio, on larval arm development was smaller when larvae were exposed to pH fluctuations, especially when the change was less frequent (48- vs 24-h cycle). Furthermore, larvae experiencing an initial pH drop, i.e. those where the cycle started at pH 8.0, were more negatively impacted compared with those kept at an initial pH of 7.3 before the cycling started. Our observations suggest that larval responses to climate change stress could not be easily predicted from mean conditions. Instead, to better predict organismal performance in the future ocean, monitoring and investigation of the role of real-time environmental fluctuations along the dispersive pathway is key.
Project description:Sand lances of the genus Ammodytes are keystone forage fish in coastal ecosystems across the northern hemisphere. Because they directly support populations of higher trophic organisms such as whales, seabirds or tuna, the current lack of empirical data and, therefore, understanding about the climate sensitivity of sand lances represent a serious knowledge gap. Sand lances could be particularly susceptible to ocean warming and acidification because, in contrast to other tested fish species, they reproduce during boreal winter months, and their offspring develop slowly under relatively low and stable pCO2 conditions. Over the course of 2 years, we conducted factorial pCO2?×?temperature exposure experiments on offspring of the northern sand lance Ammodytes dubius, a key forage species on the northwest Atlantic shelf. Wild, spawning-ripe adults were collected from Stellwagen Bank National Marine Sanctuary (Cape Cod, USA), and fertilized embryos were reared at three pCO2 conditions (400, 1000 and 2100 ?atm) crossed with three temperatures (5, 7 and 10 ?C). Exposure to future pCO2 conditions consistently resulted in severely reduced embryo survival. Sensitivity to elevated pCO2 was highest at 10 ?C, resulting in up to an 89% reduction in hatching success between control and predicted end-of-century pCO2 conditions. Moreover, elevated pCO2 conditions delayed hatching, reduced remaining endogenous energy reserves at hatch and reduced embryonic growth. Our results suggest that the northern sand lance is exceptionally CO2-sensitive compared to other fish species. Whether other sand lance species with similar life history characteristics are equally CO2-sensitive is currently unknown. But the possibility is a conservation concern, because many boreal shelf ecosystems rely on sand lances and might therefore be more vulnerable to climate change than currently recognized. Our findings indicate that life history, spawning habitat, phenology and developmental rates mediate the divergent early life CO2 sensitivities among fish species.
Project description:Assessing the potential of marine organisms to adapt genetically to increasing oceanic CO2 levels requires proxies such as heritability of fitness-related traits under ocean acidification (OA). We applied a quantitative genetic method to derive the first heritability estimate of survival under elevated CO2 conditions in a metazoan. Specifically, we reared offspring, selected from a wild coastal fish population (Atlantic silverside, Menidia menidia), at high CO2 conditions (∼2300 μatm) from fertilization to 15 days posthatch, which significantly reduced survival compared to controls. Perished and surviving offspring were quantitatively sampled and genotyped along with their parents, using eight polymorphic microsatellite loci, to reconstruct a parent-offspring pedigree and estimate variance components. Genetically related individuals were phenotypically more similar (i.e., survived similarly long at elevated CO2 conditions) than unrelated individuals, which translated into a significantly nonzero heritability (0.20 ± 0.07). The contribution of maternal effects was surprisingly small (0.05 ± 0.04) and nonsignificant. Survival among replicates was positively correlated with genetic diversity, particularly with observed heterozygosity. We conclude that early life survival of M. menidia under high CO2 levels has a significant additive genetic component that could elicit an evolutionary response to OA, depending on the strength and direction of future selection.
Project description:Despite the remarkable expansion of laboratory studies, robust estimates of single species CO2 sensitivities remain largely elusive. We conducted a meta-analysis of 20 CO2 exposure experiments conducted over 6 years on offspring of wild Atlantic silversides (Menidia menidia) to robustly constrain CO2 effects on early life survival and growth. We conclude that early stages of this species are generally tolerant to CO2 levels of approximately 2000 µatm, likely because they already experience these conditions on diel to seasonal timescales. Still, high CO2 conditions measurably reduced fitness in this species by significantly decreasing average embryo survival (-9%) and embryo+larval survival (-13%). Survival traits had much larger coefficients of variation (greater than 30%) than larval length or growth (3-11%). CO2 sensitivities varied seasonally and were highest at the beginning and end of the species' spawning season (April-July), likely due to the combined effects of transgenerational plasticity and maternal provisioning. Our analyses suggest that serial experimentation is a powerful, yet underused tool for robustly estimating small but true CO2 effects in fish early life stages.
Project description:Whether marine fish will grow differently in future high pCO2 environments remains surprisingly uncertain. Long-term and whole-life cycle effects are particularly unknown, because such experiments are logistically challenging, space demanding, exclude long-lived species, and require controlled, restricted feeding regimes-otherwise increased consumption could mask potential growth effects. Here, we report on repeated, long-term, food-controlled experiments to rear large populations (>4,000 individuals total) of the experimental model and ecologically important forage fish Menidia menidia (Atlantic silverside) under contrasting temperature (17°, 24°, and 28°C) and pCO2 conditions (450 vs. ~2,200 ?atm) from fertilization to ~ a third of this annual species' life span. Quantile analyses of trait distributions showed mostly negative effects of high pCO2 on long-term growth. At 17°C and 28°C, but not at 24°C, high pCO2 fish were significantly shorter [17°C: -5 to -9%; 28°C: -3%] and weighed less [17°C: -6 to -18%; 28°C: -8%] compared to ambient pCO2 fish. Reductions in fish weight were smaller than in length, which is why high pCO2 fish at 17°C consistently exhibited a higher Fulton's k (weight/length ratio). Notably, it took more than 100 days of rearing for statistically significant length differences to emerge between treatment populations, showing that cumulative, long-term CO2 effects could exist elsewhere but are easily missed by short experiments. Long-term rearing had another benefit: it allowed sexing the surviving fish, thereby enabling rare sex-specific analyses of trait distributions under contrasting CO2 environments. We found that female silversides grew faster than males, but there was no interaction between CO2 and sex, indicating that males and females were similarly affected by high pCO2. Because Atlantic silversides are known to exhibit temperature-dependent sex determination, we also analyzed sex ratios, revealing no evidence for CO2-dependent sex determination in this species.
Project description:The application of evolutionary principles to the management of fisheries has gained considerable attention recently. Harvesting of fish may apply directional or disruptive selection to key life-history traits, and evidence for fishery-induced evolution is growing. The traits that are directly selected upon are often correlated (genetically or phenotypically) with a suite of interrelated physiological, behavioral, and morphological characters. A question that has received comparatively little attention is whether or not, after cessation of fishery-induced selection, these correlated traits revert back to previous states. Here, we empirically examine this question. In experiments with the Atlantic silverside, Menidia menidia, we applied size-selective culling for five generations and then maintained the lines a further five generations under random harvesting. We found that some traits do return to preharvesting levels (e.g., larval viability), some partially recover (e.g., egg volume, size-at-hatch), and others show no sign of change (e.g., food consumption rate, vertebral number). Such correlations among characters could, in theory, greatly accelerate or decelerate the recovery of fish populations. These results may explain why some fish stocks fail to recover after fishing pressure is relaxed.
Project description:Ocean acidification (OA) may have varied effects on fish eco-physiological responses. Most OA studies have been carried out in laboratory conditions without considering the in situ pCO2/pH variability documented for many marine coastal ecosystems. Using a standard otolith ageing technique, we assessed how in situ ocean acidification (ambient, versus end-of-century CO2 levels) can affect somatic and otolith growth, and their relationship in a coastal fish. Somatic and otolith growth rates of juveniles of the ocellated wrasse Symphodus ocellatus living off a Mediterranean CO2 seep increased at the high- pCO2 site. Also, we detected that slower-growing individuals living at ambient pCO2 levels tend to have larger otoliths at the same somatic length (i.e. higher relative size of otoliths to fish body length) than faster-growing conspecifics living under high pCO2 conditions, with this being attributable to the so-called 'growth effect'. Our findings suggest the possibility of contrasting OA effects on fish fitness, with higher somatic growth rate and possibly higher survival associated with smaller relative size of otoliths that could impair fish auditory and vestibular sensitivity.
Project description:Coralline algae are susceptible to the changes in the seawater carbonate system associated with ocean acidification (OA). However, the coastal environments in which corallines grow are subject to large daily pH fluctuations which may affect their responses to OA. Here, we followed the growth and development of the juvenile coralline alga Arthrocardia corymbosa, which had recruited into experimental conditions during a prior experiment, using a novel OA laboratory culture system to simulate the pH fluctuations observed within a kelp forest. Microscopic life history stages are considered more susceptible to environmental stress than adult stages; we compared the responses of newly recruited A. corymbosa to static and fluctuating seawater pH with those of their field-collected parents. Recruits were cultivated for 16 weeks under static pH 8.05 and 7.65, representing ambient and 4× preindustrial pCO2 concentrations, respectively, and two fluctuating pH treatments of daily [Formula: see text] (daytime pH = 8.45, night-time pH = 7.65) and daily [Formula: see text] (daytime pH = 8.05, night-time pH = 7.25). Positive growth rates of new recruits were recorded in all treatments, and were highest under static pH 8.05 and lowest under fluctuating pH 7.65. This pattern was similar to the adults' response, except that adults had zero growth under fluctuating pH 7.65. The % dry weight of MgCO3 in calcite of the juveniles was reduced from 10% at pH 8.05 to 8% at pH 7.65, but there was no effect of pH fluctuation. A wide range of fleshy macroalgae and at least 6 species of benthic diatoms recruited across all experimental treatments, from cryptic spores associated with the adult A. corymbosa. There was no effect of experimental treatment on the growth of the benthic diatoms. On the community level, pH-sensitive species may survive lower pH in the presence of diatoms and fleshy macroalgae, whose high metabolic activity may raise the pH of the local microhabitat.
Project description:Anthropogenic activities are increasing ocean temperature and decreasing ocean pH. Some coastal habitats are experiencing increases in organic runoff, which when coupled with a loss of vegetated coastline can accelerate reductions in seawater pH. Marine larvae that hatch in coastal habitats may not have the ability to respond to elevated temperature and changes in seawater pH. This study examined the response of Florida stone crab (Menippe mercenaria) larvae to elevated temperature (30°C control and 32°C treatment) and CO2-induced reductions in pH (8.05 pH control and 7.80 pH treatment). We determined whether those singular and simultaneous stressors affect larval vertical movement at two developmental stages. Geotactic responses varied between larval stages. The direction and rate of the vertical displacement of larvae were dependent on pH rather than temperature. Stage III larvae swam upwards under ambient pH conditions, but swam downwards at a faster rate under reduced pH. There was no observable change in the directional movement of Stage V larvae. The reversal in orientation by Stage III larvae may limit larval transport in habitats that experience reduced pH and could pose challenges for the northward dispersal of stone crabs as coastal temperatures warm.