Hidden impacts of ocean warming and acidification on biological responses of marine animals revealed through meta-analysis.

Conflicting results remain on the impacts of climate change on marine organisms, hindering our capacity to predict the future state of marine ecosystems. To account for species-specific responses and for the ambiguous relation of most metrics to fitness, we develop a meta-analytical approach based on the deviation of responses from reference values (absolute change) to complement meta-analyses of directional (relative) changes in responses. Using this approach, we evaluate responses of fish and invertebrates to warming and acidification. We find that climate drivers induce directional changes in calcification, survival, and metabolism, and significant deviations in twice as many biological responses, including physiology, reproduction, behavior, and development. Widespread deviations of responses are detected even under moderate intensity levels of warming and acidification, while directional changes are mostly limited to more severe intensity levels. Because such deviations may result in ecological shifts impacting ecosystem structures and processes, our results suggest that climate change will likely have stronger impacts than those previously predicted based on directional changes alone.

Multiple interannual records of young-of-the-year identify an important area for the protection of the shortfin mako, Isurus oxyrinchus.

The shortfin mako (Isurus oxyrinchus) is the second most fishery-exploited pelagic shark in the Mediterranean Sea, thus its conservation status is a cause for concern. Despite the species has been listed in fishery and trade regulations to hinder its population decline, the lack of knowledge on its distribution patterns and habitats essential for its persistence still hampers the implementation of sound conservation actions. Combining data from local expert knowledge, opportunistic catch records, and Baited Remote Underwater Videos, we show evidence of the interannual presence of young-of-the-year (YOY) I. oxyrinchus in the Pelagie Archipelago (Central Mediterranean Sea). A total of twenty-one individuals ranging 71-92.5 cm FL were incidentally caught (on average 2.3 YOY/1000 hooks) or documented on BRUVS in July and August over three consecutive years. These data coupled with questionnaires administered to longline fishers identify one specific area used by YOY in the summer months. Our study presents the most abundant record of YOY shortfin makos in the Mediterranean Sea within such a restricted time and limited area providing important information for improving the protection of this critically endangered species.

Limited behavioural effects of ocean acidification on a Mediterranean anemone goby (Gobius incognitus) chronically exposed to elevated CO2 levels.

An in situ reciprocal transplant experiment was carried around a volcanic CO2 vent to evaluate the anti-predator responses of an anemone goby species exposed to ambient (∼380 µatm) and high (∼850 µatm) CO2 sites. Overall, the anemone gobies displayed largely unaffected behaviors under high-CO2 conditions suggesting an adaptive potential of Gobius incognitus to ocean acidification (OA) conditions. This is also supported by its 3-fold higher density recorded in the field under high CO2. However, while fish exposed to ambient conditions showed an expected reduction in the swimming activity in the proximity of the predator between the pre- and post-exposure period, no such changes were detected in any of the other treatments where fish experienced acute and long-term high CO2. This may suggest an OA effect on the goby antipredator strategy. Our findings contribute to the ongoing debate over the need for realistic predictions of the impacts of expected increased CO2 concentration on fish, providing evidence from a natural high CO2 system.

Small-scale fisheries catch more threatened elasmobranchs inside partially protected areas than in unprotected areas.

Elasmobranchs are heavily impacted by fishing. Catch statistics are grossly underestimated due to missing data from various fishery sectors such as small-scale fisheries. Marine Protected Areas are proposed as a tool to protect elasmobranchs and counter their ongoing depletion. We assess elasmobranchs caught in 1,256 fishing operations with fixed nets carried out in partially protected areas within Marine Protected Areas and unprotected areas beyond Marine Protected Areas borders at 11 locations in 6 Mediterranean countries. Twenty-four elasmobranch species were recorded, more than one-third belonging to the IUCN threatened categories (Vulnerable, Endangered, or Critically Endangered). Catches per unit of effort of threatened and data deficient species were higher (with more immature individuals being caught) in partially protected areas than in unprotected areas. Our study suggests that despite partially protected areas having the potential to deliver ecological benefits for threatened elasmobranchs, poor small-scale fisheries management inside Marine Protected Areas could hinder them from achieving this important conservation objective.

Nest guarding behaviour of a temperate wrasse differs between sites off Mediterranean CO2 seeps.

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.

Environmental DNA effectively captures functional diversity of coastal fish communities.

Robust assessments of taxonomic and functional diversity are essential components of research programmes aimed at understanding current biodiversity patterns and forecasting trajectories of ecological changes. Yet, evaluating marine biodiversity along its dimensions is challenging and dependent on the power and accuracy of the available data collection methods. Here we combine three traditional survey methodologies (underwater visual census strip transects [UVCt], baited underwater videos [BUV] and small-scale fishery catches [SSFc]), and one novel molecular technique (environmental DNA metabarcoding [eDNA]-12S rRNA and cytochrome oxidase subunit 1 [COI]) to investigate their efficiency and complementarity in assessing fish diversity. We analysed 1,716 multimethod replicates at a basin scale to measure the taxonomic and functional diversity of Mediterranean fish assemblages. Taxonomic identities were investigated at species, genus and family levels. Functional identities were assessed using combinations of morphological, behavioural and trophic traits. We show that: (a) SSFc provided the higher taxonomic diversity estimates followed by eDNA, and then UVCt and BUV; (b) eDNA was the only method able to gather the whole spectrum of considered functional traits, showing the most functionally diversified and least redundant fish assemblages; and (c) the effectiveness of eDNA in describing functional structure reflected its lack of selectivity towards any considered functional trait. Our findings suggest that the reach of eDNA analysis stretches beyond taxon detection efficiency and provides new insights into the potential of metabarcoding in ecological studies.

Changes in fish communities due to benthic habitat shifts under ocean acidification conditions.

Ocean acidification will likely change the structure and function of coastal marine ecosystems over coming decades. Volcanic carbon dioxide seeps generate dissolved CO2 and pH gradients that provide realistic insights into the direction and magnitude of these changes. Here, we used fish and benthic community surveys to assess the spatio-temporal dynamics of fish community properties off CO2 seeps in Japan. Adding to previous evidence from ocean acidification ecosystem studies conducted elsewhere, our findings documented shifts from calcified to non-calcified habitats with reduced benthic complexity. In addition, we found that such habitat transition led to decreased diversity of associated fish and to selection of those fish species better adapted to simplified ecosystems dominated by algae. Our data suggest that near-future projected ocean acidification levels will oppose the ongoing range expansion of coral reef-associated fish due to global warming.

Ocean acidification affects somatic and otolith growth relationship in fish: evidence from an in situ study.

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.

Ocean acidification does not impair predator recognition but increases juvenile growth in a temperate wrasse off CO2 seeps.

Fish behavioural effects under Ocean Acidification (OA) rely on changes expected to occur in brain function, which can be reversed by gabazine, a GABA-A antagonist. Here, using standard two-channel choice flume, we assessed OA effects on the predator recognition ability of both gabazine-treated and -untreated Symphodus ocellatus post-settlers living off CO2 seeps in the Mediterranean Sea. To estimate the post-settlers background predation risk we evaluated the density of their predator in the wild and through otolith aging techniques we assessed their post-settlement growth. Results showed that: 1) post-settlers predator recognition was unaffected under OA; 2) post-settlers living in elevated CO2 were on average 15% bigger in size than those from ambient conditions. Our results support fish behavioural tolerance to OA, potentially mediated by pre-exposure to high-risk predation levels, and speculate that by increasing body size, juvenile fish might more efficiently avoid their predators.

Ocean acidification affects fish spawning but not paternity at CO2 seeps.

Fish exhibit impaired sensory function and altered behaviour at levels of ocean acidification expected to occur owing to anthropogenic carbon dioxide emissions during this century. We provide the first evidence of the effects of ocean acidification on reproductive behaviour of fish in the wild. Satellite and sneaker male ocellated wrasse (Symphodus ocellatus) compete to fertilize eggs guarded by dominant nesting males. Key mating behaviours such as dominant male courtship and nest defence did not differ between sites with ambient versus elevated CO2 concentrations. Dominant males did, however, experience significantly lower rates of pair spawning at elevated CO2 levels. Despite the higher risk of sperm competition found at elevated CO2, we also found a trend of lower satellite and sneaker male paternity at elevated CO2 Given the importance of fish for food security and ecosystem stability, this study highlights the need for targeted research into the effects of rising CO2 levels on patterns of reproduction in wild fish.

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.

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.