Intellectual merit: Ocean acidification has the potential to affect a broad spectrum of marine organisms and thereby transform the composition and function of our oceans. In contrast to calcifying marine invertebrates, marine fish are widely believed to be unaffected by the CO2 concentrations projected for the future. While this may be so for juvenile and adult fish stages, the fate of fish embryos and larvae in high CO2 oceans is less certain as CO2-sensitivity data for these stages are largely unavailable. Recognizing this knowledge gap and inspired by the findings of two recent studies on clownfish and sea bass larvae (Munday et al. PNAS 107 (2010); Checkley et al. Science 324 (2009)), the investigators performed a series of experiments exposing eggs and early larvae of inland silversides (Menidia beryllina) to elevated CO2 levels while strictly adhering to current "best practice" guidelines for ocean acidification research. At 1,000 ppm CO2, average M. beryllina survival ~1wk post-hatch significantly and consistently (five experiments) declined by ~75% compared to current day CO2 levels (390 ppm), while average length of newly hatched larvae decreased by 22%. Together with prior studies, these results suggest a surprisingly high susceptibility of fish early life stages to the CO2 increases that are projected to occur this century. Given that the abundance of many fish stocks, including most commercial species, is often regulated by processes affecting early life history growth and survival, ocean acidification may impact the dynamics of future fish populations and become yet another challenge to sustainable fisheries.

The investigators believe that there is now a pressing need to better understand how CO2 affects the viability of fish embryos and larvae in the ocean. This requires novel approaches involving longer-term, larger-scale experiments across multiple species. The investigators will comprehensively examine the impacts of current and future CO2 levels (400 - 1,000 ppm) during the egg and larval stages of three model fish species: Atlantic silversides (M. menidia), inland silversides (M. beryllina) and sheepshead minnows (Cyprinodon variegatus). They will also investigate populations of the same species (M. menidia) from differing latitudes. These species/populations are ecologically important due to their intermediate trophic position, have comparable life histories to commercial marine fish, offer differences in genetic growth capacity and presumed sensitivity, and are highly amenable to laboratory experimentation. Survival and growth (weight- and length-based) will be measured in experiments performed at different CO2, temperature (21, 27°C) and feeding conditions (low, ad libitum), thus permitting the affects of CO2 to be considered in parallel with thermal stress and food limitation. Quantification of feeding rates, gross growth efficiency, and oxygen consumption will characterize the physiological costs of high CO2 environments. Changes in calcification of larval fish otoliths and skeletal elements will be determined from weights and a Ca45 radiotracer approach. Finally, surviving M. menidia (or M. beryllina) will be reared to maturity and their offspring will be challenged with differing levels of CO2. Repeating this approach over several generations will demonstrate the extent to which CO2 resistance may evolve through natural selection. Collectively, this study will make significant advances toward understanding how ocean acidification may challenge the world's most valuable marine resource, fish.

Broader Impacts: This investigation will serve as the dissertation topic for a doctoral student at Stony Brook University and will support a female post-doctoral researcher. The PIs have a strong record of supporting diversity in education and in enriching undergraduate and secondary school education and research and will continue these practices for this project. A novel outreach program has the potential to reach one million aquarium patrons during the project.

Project Report

Forage fish such as silversides and minnows are key components of temperate coastal marine ecosystems because they act as predators of zooplankton and prey for larger trophic organisms like striped bass, bluefish or piscivorous birds. The sensitivity of coastal forage fish to ocean acidification was largely unexplored and thus became the focus of this NSF-funded research project. Based on a series of independent experiments, our first discovery was that growth and survival of Inland silverside (Menidia beryllina) embryos and early larvae were significantly reduced in direct response to CO2 concentrations (~ 1,000 µatm) that are predicted in the average open ocean for the end of this century (Fig.1). This spurred on a wide range of experimental approaches; one consisted of novel, multi-year experiments that combined high-frequency pH monitoring in a temperate tidal salt marsh with repetitive sampling of a wild fish population (Atlantic silverside, M. menidia) spawning in there and standardized CO2 exposure experiments on offspring over of two years. This demonstrated for the first time an interannually consistent, seasonal change in offspring CO2 tolerance in a marine organism. The shifting response strikingly coincided with the rapid seasonal acidification pattern typical for this and many other coastal habitats (Fig.2 - primary image). This project further led to a new quantitative genetic approach to determine the evolutionary adaptation potential of fish to high CO2 environments; while demonstrating a viable method to better understand the long-term vulnerabilities of marine organisms to unfolding ocean acidification. In addition, this NSF grant facilitated the measurement and analysis of pH, dissolved oxygen (DO) and in situ pCO2 levels in a wide range of New England bays and estuaries (Fig.3), hence broadening the current understanding of the spatio-temporal variability of these factors. For example, it clearly indicated that in productive coastal habitats, pH and DO covary on tidal, diel, seasonal and interannual time scales (Fig.4), because respiration due to microbial degradation of organic matter necessarily consumes oxygen while producing CO2. Stressfully low pH and oxygen conditions are therefore particularly prevalent in coastal ecosystem that are also affected by eutrophication. Consequently, this project started to explore the additive and synergistically negative effects of co-occurring hypoxia and acidification on the early life stages of coastal organisms such bay scallops and quahogs (Fig.5), or silversides and sheepshead minnows (Fig.6). This NSF project trained three Master students, who successfully graduated from Stony Brook University in 2014. It involved numerous undergraduate and highschool students from diverse backgrounds in field and experimental work, thereby conveying the challenges and opportunities of this research field. The PI’s used their experiences and findings to actively reach out to stakeholders, members of congress, academic and governmental researchers and the general public – using print and electronic media, lectures, seminar and conference talks.

Agency
National Science Foundation (NSF)
Institute
Division of Ocean Sciences (OCE)
Type
Standard Grant (Standard)
Application #
1129622
Program Officer
David L. Garrison
Project Start
Project End
Budget Start
2011-09-01
Budget End
2014-08-31
Support Year
Fiscal Year
2011
Total Cost
$649,856
Indirect Cost
Name
State University New York Stony Brook
Department
Type
DUNS #
City
Stony Brook
State
NY
Country
United States
Zip Code
11794