A traits-based approach to assess aquaculture's contributions to food, climate change, and biodiversity goals.

Aquaculture has the potential to support a sustainable and equitable food system in line with the United Nations Sustainable Development Goals (SDG) on food security, climate change, and biodiversity (FCB). Biological diversity amongst aquaculture organisms can drive diverse contributions to such goals. Existing studies have assessed the performance of a limited number of taxa in the general context of improving aquaculture production, but few explicitly consider the biological attributes of farmed aquatic taxa at the FCB nexus. Through a systematic literature review, we identify key traits associated with FCB and evaluate the potential of aquaculture to contribute to FCB goals using a fuzzy logic model. The majority of identified traits are associated with food security, and two-thirds of traits linked with food security are also associated with climate change or biodiversity, revealing potential co-benefits of optimizing a single trait. Correlations between FCB indices further suggest that challenges and opportunities in aquaculture are intertwined across FCB goals, but low mean FCB scores suggest that the focus of aquaculture research and development on food production is insufficient to address food security, much less climate or biodiversity issues. As expected, production-maximizing traits (absolute fecundity, the von Bertalanffy growth function coefficient K, macronutrient density, maximum size, and trophic level as a proxy for feed efficiency) highly influence a species' FCB potential, but so do species preferences for environmental conditions (tolerance to phosphates, nitrates, and pH levels, as well as latitudinal and geographic ranges). Many highly farmed species that are typically associated with food security, especially finfish, score poorly for food, climate, and biodiversity potential. Algae and mollusc species tend to perform well across FCB indices, revealing the importance of non-fish species in achieving FCB goals and potential synergies in integrated multi-trophic aquaculture systems. Overall, this study provides decision-makers with a biologically informed assessment of desirable aquaculture traits and species while illuminating possible strategies to increase support for FCB goals. Our findings can be used as a foundation for studying the socio-economic opportunities and barriers for aquaculture transitions to develop equitable pathways toward FCB-positive aquaculture across nuanced regional contexts.

Air exposure moderates ocean acidification effects during embryonic development of intertidally spawning fish.

Ocean acidification can negatively impact the early life-stages of marine fish, due to energetic costs incurred by the maintenance of acid-base homeostasis, leaving less energy available for growth and development. The embryos of intertidally spawning fishes, such as Pacific herring, are often air exposed for hours. We hypothesized that air exposure would be beneficial to the developing embryo due to a higher oxygen availability (and thus reduced metabolic costs to secure adequate oxygen) and permitting excess CO2 associated with ocean acidification to be off-gassed during emersion. To investigate this, we reared Pacific herring (Clupea pallasii) embryos under three tidal regimes (subtidal: fully immersed, low intertidal: 2 × 2 h air exposure, and high intertidal: 5 + 9 h air exposure) fully crossed with three aquatic CO2 levels (400, 1500 and 3200 µatm) at a water temperature of 9.5 °C and naturally fluctuating air temperature during air exposure. We measured the effects on embryonic development and hatch, as well as carry-over effects on larval development and survival. Air exposure during embryonic development had significant positive effects on growth, condition and survival in larval Pacific herring, with some interactive effects with CO2. Interestingly, CO2 by itself in the fully immersed treatment had no effect, but had significant interactions with air exposure. Our research suggests that air exposure during low tide can be highly beneficial to intertidally spawning fishes and needs to be taken into account in climate change studies and modeling.

Changes in gill and air-breathing organ characteristics during the transition from water- to air-breathing in juvenile Arapaima gigas.

The obligate air-breathing Amazonian fish, Arapaima gigas, hatch as water-breathing larvae but with development, they modify their swim bladder to an air-breathing organ (ABO) while reducing their gill filaments to avoid oxygen loss. Here, we show that significant changes already take place between 4 weeks (1.6 g) and 11 weeks (5 g) post hatch, with a reduction in gill lamellar surface area, increase in gill diffusion distance, and proliferation of the parenchyma in the ABO. By using a variety of methods, we quantified the surface area and diffusion distances of the gills and skin, and the swim bladder volume and anatomical complexity from hatch to 11-week-old juveniles. In addition, we identified the presence of two ionocyte types in the gills and show how these change with development. Until 1.6 g, A. gigas possess only the H+ -excreting/Na+ -absorbing type, while 5-g fish and adults have an additional ionocyte which likely absorbs H+ and Cl- and excretes HCO3- . The ionocyte density on the gill filaments increased with age and is likely a compensatory mechanism for maintaining ion transport while reducing gill surface area. In the transition from water- to air-breathing, A. gigas likely employs a trimodal respiration utilizing gills, skin, and ABO and thus avoid a respiratory-ion regulatory compromise at the gills.

Physiological resilience of pink salmon to naturally occurring ocean acidification.

Pacific salmon stocks are in decline with climate change named as a contributing factor. The North Pacific coast of British Columbia is characterized by strong temporal and spatial heterogeneity in ocean conditions with upwelling events elevating CO2 levels up to 10-fold those of pre-industrial global averages. Early life stages of pink salmon have been shown to be affected by these CO2 levels, and juveniles naturally migrate through regions of high CO2 during the energetically costly phase of smoltification. To investigate the physiological response of out-migrating wild juvenile pink salmon to these naturally occurring elevated CO2 levels, we captured fish in Georgia Strait, British Columbia and transported them to a marine lab (Hakai Institute, Quadra Island) where fish were exposed to one of three CO2 levels (850, 1500 and 2000 µatm CO2) for 2 weeks. At ½, 1 and 2 weeks of exposure, we measured their weight and length to calculate condition factor (Fulton's K), as well as haematocrit and plasma [Cl-]. At each of these times, two additional stressors were imposed (hypoxia and temperature) to provide further insight into their physiological condition. Juvenile pink salmon were largely robust to elevated CO2 concentrations up to 2000 µatm CO2, with no mortality or change in condition factor over the 2-week exposure duration. After 1 week of exposure, temperature and hypoxia tolerance were significantly reduced in high CO2, an effect that did not persist to 2 weeks of exposure. Haematocrit was increased by 20% after 2 weeks in the CO2 treatments relative to the initial measurements, while plasma [Cl-] was not significantly different. Taken together, these data indicate that juvenile pink salmon are quite resilient to naturally occurring high CO2 levels during their ocean outmigration.

Organ health and development in larval kingfish are unaffected by ocean acidification and warming.

Anthropogenic CO2 emissions are causing global ocean warming and ocean acidification. The early life stages of some marine fish are vulnerable to elevated ocean temperatures and CO2 concentrations, with lowered survival and growth rates most frequently documented. Underlying these effects, damage to different organs has been found as a response to elevated CO2 in larvae of several species of marine fish, yet the combined effects of acidification and warming on organ health are unknown. Yellowtail kingfish, Seriola lalandi, a circumglobal subtropical pelagic fish of high commercial and recreational value, were reared from fertilization under control (21 °C) and elevated (25 °C) temperature conditions fully crossed with control (500 µatm) and elevated (1,000 µatm) pCO2 conditions. Larvae were sampled at 11 days and 21 days post hatch for histological analysis of the eye, gills, gut, liver, pancreas, kidney and liver. Previous work found elevated temperature, but not elevated CO2, significantly reduced larval kingfish survival while increasing growth and developmental rate. The current histological analysis aimed to determine whether there were additional sublethal effects on organ condition and development and whether underlying organ damage could be responsible for the documented effects of temperature on survivorship. While damage to different organs was found in a number of larvae, these effects were not related to temperature and/or CO2 treatment. We conclude that kingfish larvae are generally vulnerable during organogenesis of the digestive system in their early development, but that this will not be exacerbated by near-future ocean warming and acidification.

Organ damage in Atlantic herring larvae as a result of ocean acidification.

The dissolution of anthropogenically emitted excess carbon dioxide lowers the pH of the world's ocean water. The larvae of mass spawning marine fishes may be particularly vulnerable to such ocean acidification (OA), yet the generality of earlier results is unclear. Here we show the detrimental effects of OA on the development of a commercially important fish species, the Atlantic herring (Clupea harengus). Larvae were reared at three levels of CO2: today (0.0385 kPa), end of next century (0.183 kPa), and a coastal upwelling scenario (0.426 kPa), under near-natural conditions in large outdoor tanks. Exposure to elevated CO2 levels resulted in stunted growth and development, decreased condition, and severe tissue damage in many organs, with the degree of damage increasing with CO2 concentration. This complements earlier studies of OA on Atlantic cod larvae that revealed similar organ damage but at increased growth rates and no effect on condition.

The proteome of Atlantic herring (Clupea harengus L.) larvae is resistant to elevated pCO2.

Elevated anthropogenic pCO2 can delay growth and impair otolith structure and function in the larvae of some fishes. These effects may concurrently alter the larva's proteome expression pattern. To test this hypothesis, Atlantic herring larvae were exposed to ambient (370 µatm) and elevated (1800 µatm) pCO2 for one-month. The proteome structure of the larvae was examined using a 2-DE and mass spectrometry. The length of herring larvae was marginally less in the elevated pCO2 treatment compared to the control. The proteome structure was also different between the control and treatment, but only slightly: the expression of a small number of proteins was altered by a factor of less than 2-fold at elevated pCO2. This comparative proteome analysis suggests that the proteome of herring larvae is resilient to elevated pCO2. These observations suggest that herring larvae can cope with levels of CO2 projected for near future without significant proteome-wide changes.