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 nongenetic inheritance (epigenetics) through parental exposure and other downstream consequences, such as survival of larvae

Nest-mediated parental care in a marine fish: Are large-scale nesting habitats selected and do these habitats respond to small-scale requirements?

Fishes have evolved various reproductive strategies including mechanisms that involve parental care and demersal eggs laid into nests. Symphodus ocellatus has a seasonal reproduction period during which large, dominant males become territorial and build nests with fragments of algae, where they attract females to spawn and provide care to the developing eggs. Based on the hypothesis that the S. ocellatus males choose the reproductive habitat based on some characteristics of the substrate, here we assessed whether, on a coastal area scale, the distribution of this species changes during the reproductive period because of the selection of some suitable sites or substrates, and whether the nesting microhabitat used by this species responding to certain requirements in relation to different characteristics. From April to September 2010, at four locations and on three substrate types, the fish were counted in three periods related to different stages of reproduction. Furthermore, several physical and biological variables have been recorded around numerous nests to select those with more recurrence. We found that S. ocellatus prefers to live on rocky substrates populated by photophilic algae, regardless of the phases of the reproductive cycle. We identified depth (1.7–3.2 m), the presence of a hole, a 10–20 cm algal canopy, and high algal coverage of Dyctiotales as nest requirements. S. ocellatus is mostly distributed in coastal sites sheltered from the action of waves. This allows the construction and maintenance of nests and the possibility to remain in a water temperature range similar to the reproductive physiological constraints

CO2 effects on behaviour and reproduction of nesting fish species

Ocean acidification is a global phenomenon linked to the CO2 absorption by the surface of the sea. This increasing process leads to a rise of the CO2 partial pressure (pCO2) that changes the seawater chemistry. It is known that such changes have negative consequences for many marine organisms. However, the effects of acidification on fishes are yet poorly understood. Fishes have been hypothesized to be more physiologically tolerant to elevated CO2. Nevertheless, many researches have described severe effects of altered pCO2 levels on fish behaviour, especially during early life history stages, and only few authors have focused on fish reproduction. The aim of my Ph.D. research is to investigate the effects of different pCO2 levels on the reproduction of nesting fish species, with particular emphasis on reproductive behaviour and reproductive success, and on early life stages development. This research will be conducted in the Vulcano Island coast where a natural gradient of pH and CO2 exists, due to underwater volcanic emissions dominated by CO2. Preliminary observations on fish community composition in this place have shown different distribution patterns of the species along the pCO2 gradient. In particular, some species belonging to genus Symphodus display the same distribution pattern in high pCO2 levels (= ca. 1100 µatm) and in normal pCO2 levels (= ca. 400 µatm). The males of these species build elaborate nests in which several females spawn, and they could be more sensitive to the acidification effects due to territorial habits shown during their reproductive period

Living in a high CO2 world: a global meta-analysis shows multiple trait-mediated fish responses to ocean acidification

Understanding how marine organisms will be affected by global change is of primary importance to ensure ecosystem functioning and nature contributions to people. This study meets the call for addressing how life-history traits mediate effects of ocean acidification on fish. We built a database of overall and trait-mediated responses of teleost fish to future CO2 levels by searching the scientific literature. Using a meta-analytical approach, we investigated the effects of projected CO2 levels by IPCC for 2050–2070 and 2100 on fish eco-physiology and behavior from 320 contrasts on 42 species, stemming from polar to tropical regions. Moreover, since organisms may experience a mosaic of carbonate chemistry in coastal environments (e.g., in estuaries, upwelling zones and intertidal habitats), which may have higher pCO2 values than open ocean waters, we assessed responses from additional 103 contrasts on 21 fish species using pCO2 levels well above IPCC projections. Under mid-century and end-of-century CO2 emission scenarios, we found multiple CO2-dose-dependent effects on calcification, resting metabolic rate, yolk, and behavioral performances, along with increased predation risk and decreased foraging, particularly for larvae. Importantly, many of the traits considered will not confer fish tolerance to elevated CO2 and far-reaching ecological consequences on fish population replenishment and community structure will likely occur. Extreme CO2 levels well above IPCC projections showed effects on fish mortality and calcification, while growth, metabolism, and yolk were unaffected. CO2 exposures in short-term experiments increased fish mortality, which in turn decreased in longer-term exposures. Whatever the elevated CO2 levels considered, some key biological processes (e.g., reproduction, development, habitat choice) were critically understudied. Fish are an important resource for livelihoods in coastal communities and a key component for stability of marine ecosystems. Given the multiple trait-mediated effects evidenced here, we stress the need to fill the knowledge gap on important eco-physiological processes and to expand the number and duration of ocean acidification studies to multi-generational, multiple stressor (e.g., warming, hypoxia, fishing), and species interactions experiments to better elucidate complex ecosystem-level changes and how these changes might alter provisioning of ecosystem services

Data from: Living in a high CO2 world: a global meta-analysis shows multiple trait-mediated responses of fish to ocean acidification

Understanding how marine organisms will be affected by global change is of primary importance to ensure ecosystem functioning and nature contributions to people. This study meets the call for addressing how life-history traits mediate effects of ocean acidification on fish. We built a database of overall and trait-mediated responses of teleost fish to future CO2 levels by searching the scientific literature. Using a meta-analytical approach, we investigated the effects of projected CO2 levels by IPCC for 2050-2070 and 2100 on fish eco-physiology and behavior from 320 contrasts on 42 species, stemming from polar to tropical regions. Moreover, since organisms may experience a mosaic of carbonate chemistry in coastal environments (e.g. in estuaries, upwelling zones and intertidal habitats), which may have higher pCO2 values than open ocean waters, we assessed responses from additional 103 contrasts on 21 fish species using pCO2 levels well above IPCC projections. Under mid- and end-of-century CO2 emission scenarios, we found multiple CO2-dose dependent effects on calcification, resting metabolic rate, yolk, behavioral performances, along with increased predation risk and decreased foraging, particularly for larvae. Importantly, many of the traits considered will not confer fish tolerance to elevated CO2 and far-reaching ecological consequences on fish population replenishment and community structure will likely occur. Extreme CO2 levels well above IPCC projections showed effects on fish mortality and calcification, while growth, metabolism and yolk were unaffected. CO2 exposures in short-term experiments increased fish mortality, which in turn decreased in longer-term exposures. Whatever the elevated CO2 levels considered, some key biological processes (e.g. reproduction, development, habitat choice) resulted critically understudied. Fish are an important resource for livelihoods in coastal communities and a key component for stability of marine ecosystems. Given the multiple trait-mediated effects evidenced here, we stress the need to fill the knowledge gap on important eco-physiological processes and to expand the number and duration of ocean acidification studies to multi-generational, multiple stressor (e.g. warming, hypoxia, fishing) and species interactions experiments to better elucidate complex ecosystem-level changes and how these changes might alter provisioning of ecosystem services

Seawater carbonate chemistry and nest guarding behaviour of a temperate wrasse

Organisms may respond to changing environmental conditions by adjusting their behaviour (i.e., behavioural plasticity). Ocean acidification (OA), resulting from anthropogenic emissions of carbon dioxide (CO2), is predicted to impair sensory function and behaviour of fish. However, reproductive behaviours, and parental care in particular, and their role in mediating responses to OA are presently overlooked. Here, we assessed whether the nesting male ocellated wrasse Symphodus ocellatus from sites with different CO2 concentrations showed different behaviours during their breeding season. We also investigated potential re-allocation of the time-budget towards different behavioural activities between sites. We measured the time period that the nesting male spent carrying out parental care, mating and exploring activities, as well as changes in the time allocation between sites at ambient (400 μatm) and high CO2 concentrations (1000 μatm). Whilst the behavioural connectance (i.e., the number of linkages among different behaviours relative to the total amount of linkages) was unaffected, we observed a significant reduction in the time spent on parental care behaviour, and a significant decrease in the guarding activity of fish at the high CO2 sites, with a proportional re-allocation of the time budget in favour of courting and wandering around, which however did not change between sites. This study shows behavioural differences in wild fish living off volcanic CO2 seeps that could be linked to different OA levels, suggesting that behavioural plasticity may potentially act as a mechanism for buffering the effects of ongoing environmental change. A reallocation of the time budget between key behaviours may play a fundamental role in determining which marine organisms are thriving under projected OA

CO2 EFFECTS ON SPAWNING RATES OF A MEDITERRANEAN NESTING WRASSE

Some aspects of the reproductive behaviour of the ocellated wrasse Symphodus ocellatus (Forsskål 1775) were investigated in wild conditions along a pCO2 gradient. Our results show no differences in the number of females, sneakers and satellite males involved in the spawning phase under two pCO2 conditions. However, the spawning rate of nesting males was negatively affected in high pCO2, whilst exerted a normal reproductive pattern in ambient pCO2

Impiego dei BRUV (Baited Remote Underwater Video) per la valutazione del popolamento ittico nell'area marina protetta Capo Gallo-Isola delle Femmine (Palermo)

A Baited Remote Underwater Video (BRUV) system was used to assess fish assemblages on detritic bottoms (40 m) inside and outside the Capo Gallo - Isola delle Femmine MPA. Our study investigated the suitability of Baited Remote Underwater Video to describe fish (relative) abundance and diversity between sites at different protection levels. The fish assemblages relative abundance and species richness significantly differed between the three different location (A, B e CTL) considered. The largest difference occurred at CTL site position outside the MPA, where 2-fold increase in the number of species was recorded relative to the A and B sites

Influence of Fish Aggregating Devices (FADs) On Anti-Predator Behaviour Within Experimental Mesocosms

Commercial fishers have used fish aggregating devices throughout the Mediterranean Sea for over 40 years. These devices attract numerous predatory and forage species in both coastal and offshore environments. This study examined the influence of fish aggregating devices on schooling and aggregating behaviour by small forage fish in quasi-natural mesocosms. Anti-predator behaviour was evaluated for juvenile Caranx crysos under a variety of treatment conditions. Results suggest that, in the absence of physical structure, C. crysos first respond to a predatory threat by forming a school. When a physical structure is present, however, C. crysos show an occasional tendency to aggregate near the structure. These results suggest that a threatened prey species can change their defensive strategy against predatory behaviour. Further examination is required to explain if fish aggregating devices can increase survival rates of post-larval and juvenile prey species in the southern Mediterranean Sea. Management agencies should consider the relationship between the use of fish aggregating devices by commercial fisheries and the potential influence such devices possess on population dynamics of aggregating fish species

Appendices 2-5 Cattano et al DRYAD

Literature data used for the meta-analyses to assess eco-physiological and behavioural responses, along with response variables, category levels, CO2 treatment (range), duration, metrics and effect sizes. File type: .xls. Data are presented in four different excel sheets: Ap 2 Summary table; Ap 3 Ecophysiological response; Ap 4 Behavioral response; Ap 5 extreme pCO