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.

Combined effects of climate change stressors and predators with contrasting feeding-digestion strategies on a mussel species.

We investigated the combined effects of Ocean Warming (OW), Acidification (OA) and predator cues (Non-Consumptive Effects; NCEs) of two predators with contrasting feeding-digestion strategies on the mussel Perumytilus purpuratus. We considered starfish-NCEs (partially external digestion) and snail-NCEs (internal digestion). Mussels were exposed for 13 weeks to cross-factored OA (~500 and ~1400 µatm, pCO2) and OW (~15 and ~20 °C) conditions, in the presence/absence of NCEs from one or both predators. Mussels exposed to both NCEs exhibited smaller length and buoyant weight growth than those under control or snail-NCEs conditions. Mussels exposed to starfish-NCEs exhibited smaller wet mass than control mussels. OW and starfish-NCEs in isolation or combined with snail-NCEs increased mussel oxygen consumption. Byssal biogenesis was affected by the three-factors interaction. Clearance rates were affected by the OW × OA interaction. We suggest that mainly starfish-NCEs, in isolation or interacting with OA or/and OW, can threat mussel traits and the associated community.

Multiple-stressor effects of ocean acidification, warming and predation risk cues on the early ontogeny of a rocky-shore keystone gastropod.

To understand how climate change stressors might affect marine organisms and support adequate projections it is important to know how multiple stressors may be modulated by the presence of other species. We evaluated the direct effects of ocean warming (OW) and ocean acidification (OA) together with non-consumptive effects (NCEs) of the predatory crab Acanthocyclus hassleri on early ontogeny fitness-related traits of the commercially important rocky-shore keystone gastropod Concholepas concholepas. We measured the response of nine traits to these stressors at either the organismal level (survival, growth, feeding rates, tenacity, metabolic rate, calcification rate) or sub-organismal level (nutritional status, ATP-supplying capacity, stress condition). C. concholepas survival was not affected by any of the stressors. Feeding rates were not affected by OW or OA; however, they were reduced in the presence of crab NCEs compared with control conditions. Horizontal tenacity was affected by the OA × NCEs interaction; in the presence of NCEs, OA reduced tenacity. The routine metabolic rate, measured by oxygen consumption, increased significantly with OW. Nutritional status assessment determined that carbohydrate content was not affected by any of the stressors. However, protein content was affected by the OA × NCEs interaction; in the absence of NCEs, OA reduced protein levels. ATP-supplying capacity, measured by citrate synthase (CS) activity, and cellular stress condition (HSP70 expression) were reduced by OA, with reduction in CS activity found particularly at the high temperature. Our results indicate C. concholepas traits are affected by OA and OW and the effects are modulated by predator risk (NCEs). We conclude that some C. concholepas traits are resilient to climate stressors (survival, growth, horizontal tenacity and nutritional status) but others are affected by OW (metabolic rate), OA (ATP-supplying capacity, stress condition), and NCEs (feeding rate). The results suggest that these negative effects can adversely affect the associated community.

Exposure time modulates the effects of climate change-related stressors on fertile sporophytes and early-life stage performance of a habitat-forming kelp species.

Understanding the impact of increases in pCO2 (OA) and extreme changes in temperature on marine organisms is critical to predicting how they will cope with climate change. We evaluated the effects of OA as well as warming and cooling trend temperature on early reproductive traits of Lessonia trabeculata, a bio-engineer kelp species. Sori discs were maintained for an exposure time (ET) of 3 (T3) and 7 (T7) days to one of two contrasting pCO2 levels (450 and 1100 µatm). In addition, at each pCO2 level, they were subjected to three temperature treatments: 15 °C (control), 10 °C (cool) and 19 °C (warm). Subsequently, we compared sorus photosynthetic performance (Fv/Fm), the number of meiospores released (MR) and their germination rate (GR) after 48 h of settlement, with values obtained from sori discs not exposed (DNE) to the treatments. The Fv/Fm measured for DNE was lower than at T3 and T7 at 10 and 15 °C but not at 19 °C. Regardless of temperature, we found no significant differences between MR measured at T0 and T3. MR at T7 was significantly lower at 19 °C than at 10 and 15 °C. We found only a significant reduction in MR in response to elevated pCO2 at T3. The GR of meiospores released by DNE and then maintained for 48 h to 19 °C decreased significantly by ~33% when compared with those maintained for the same time at 10 and 15 °C. A similar, but more drastic reduction (~54%) in the GR was found in meiospores released by sori discs exposed for T3 and maintained for 48 h to 19 °C. We suggest that OA and warming trend will threaten the early establishment of this species with further consequences for the functioning of the associated ecosystem.

Effects of artificial light at night and predator cues on foraging and predator avoidance in the keystone inshore mollusc Concholepas concholepas.

The growth of Artificial Light At Night (ALAN) is potentially having widespread effects on terrestrial and coastal habitats. In this study we addressed both the individual effects of ALAN, as well as its combined effect with predation risk on the behaviour of Concholepas concholepas, a fishery resource and a keystone species in the southeastern Pacific coast. We measured the influence of ALAN and predation risk on this mollusc's feeding rate, use of refuge for light and crawling out of water behaviour. These behavioural responses were studied using light intensities that mimicked levels that had been recorded in coastal habitat exposed to ALAN. Cues were from two species known to prey on C. concholepas during its early ontogeny: the crab Acanthocyclus hassleri and the seastar Heliaster helianthus. The feeding rates of C. concholepas were 3-4 times higher in darkness and in the absence of predator cues. In contrast, ALAN-exposed C. concholepas showed lower feeding activity and were more likely to be in a refuge than those exposed to control conditions. In the presence of olfactory predator cues, and regardless of light treatment, C. concholepas tended to crawl-out of the waterline. We provide evidence to support the hypothesis that exposure to either ALAN or predation risk can alter the feeding behaviour of C. concholepas. However, predator cue recognition in C. concholepas was not affected by ALAN in situations where ALAN and predator cues were both present: C. concholepas continued to forage when predation risk was low, i.e., in darkness and away from predator cues. Whilst this response means that ALAN may not lead to increased predation mortality in C. concholepas, it will reduce feeding activity in this naturally nocturnal species in the absence of dark refugia. Such results may have implications for the long-term health, productivity and sustainability of this keystone species.

The combined effects of climate change stressors and predatory cues on a mussel species.

In order to make adequate projections on the consequences of climate change stressors on marine organisms, it is important to know how impacts of these stressors are affected by the presence of other species. Here we assessed the direct effects of ocean warming (OW) and acidification (OA) along with non-consumptive effects (NCEs) of a predatory crab and/or a predatory snail on the habitat-forming mussel Perumytilus purpuratus. Mussels were exposed for 10-14 weeks to contrasting pCO2 (500 and 1400 µatm) and temperature (15 and 20 °C) levels, in the presence/absence of cues from one or two predator species. We compared mussel traits at sub-organismal (nutritional status, metabolic capacity-ATP production-, cell stress condition via HSP70 expression) and organismal (survival, oxygen consumption, growth, byssus biogenesis, clearance rates, aggregation) levels. OA increased the mussels' oxygen consumption; and OA combined with OW increased ATP demand and the use of carbohydrate reserves. Mussels at present-day pCO2 levels had the highest protein content. Under OW the predatory snail cues induced the highest cell stress condition on the mussels. Temperature, predator cues and the interaction between them affected mussel growth. Mussels grew larger at the control temperature (15 °C) when crab and snail cues were present. Mussel wet mass and calcification were affected by predator cues; with highest values recorded in crab cue presence (isolated or combined with snail cues). In the absence of predator cues in the trails, byssus biogenesis was affected by OA, OW and the OA × OW and OA × predator cues interactions. At present-day pCO2 levels, more byssus was recorded with snail than with crab cues. Clearance rates were affected by temperature, pCO2 and the interaction between them. The investigated stressors had no effects on mussel aggregation. We conclude that OA, OW and the NCEs may lead to neutral, positive or negative consequences for mussels.

The combined effects of ocean acidification and warming on a habitat-forming shell-crushing predatory crab.

In mid rocky intertidal habitats the mussel Perumytilus purpurarus monopolizes the substratum to the detriment of many other species. However, the consumption of mussels by the shell-crushing crab Acanthocyclus hassleri creates within the mussel beds space and habitat for several other species. This crab uses its disproportionately large claw to crush its shelled prey and plays an important role in maintaining species biodiversity. This study evaluated the consequences of projected near-future ocean acidification (OA) and warming (OW) on traits of A. hassleri linked with their predatory performance. Individual A. hassleri were maintained for 10-16 weeks under contrasting pCO2 (~500 and 1400 µatm) and temperature (~15 and 20 °C) levels. We compared traits at the organismal (oxygen consumption rate, survival, calcification rate, feeding rates, crusher claw pinching strength, self-righting speed, sarcomere length of the crusher claw muscles) and cellular (nutritional status ATP provisioning capacity through citrate synthase activity, expression of HSP70) level. Survival, calcification rate and sarcomere length were not affected by OA and OW. However, OW increased significantly feeding and oxygen consumption. Pinching strength was reduced by OA; meanwhile self-righting was increased by OA and OW. At 20 °C, carbohydrate content was reduced significantly by OA. Regardless of temperature, a significant reduction in energy reserves in terms of protein content by OA was found. The ATP provisioning capacity was significantly affected by the interaction between temperature and pCO2 and was highest at 15 °C and present day pCO2 levels. The HSP70 levels of crabs exposed to OW were higher than in the control crabs. We conclude that OA and OW might affect the amount and size of prey consumed by this crab. Therefore, by reducing the crab feeding performance these stressors might pose limits on their role in generating microhabitat for other rocky intertidal species inhabiting within mussel beds.

Combined effect of pCO2 and temperature levels on the thermal niche in the early benthic ontogeny of a keystone species.

We evaluated the effects of projected, near future ocean acidification (OA) and extreme events of temperature (warming or cooling) on the thermal tolerance of Concholepas concholepas, a coastal benthic keystone species. Three separate trials of an experiment were conducted by exposing juvenile C. concholepas for 1 month to one of two contrasting pCO2 levels (~500 and ~1200 µatm). In addition, each pCO2 level was combined with one of four temperature treatments. The control was 15 °C, whilst the other temperatures were 10 °C (Trial 1), 20 °C (Trial 2) and 25 °C (Trial 3). At the end of each trial, we assessed Critical Thermal maximum (CTmax) and minimum (CTmin) via self-righting success, calculated partial thermal tolerance polygons, measured somatic growth, determined transcription of Heat Shock Proteins 70 (HSP70) and measured oxygen consumption rates. Regardless of pCO2 level, HSP70 transcript levels were significantly higher in juveniles after exposure to extreme temperatures (10 °C and 25 °C) indicating physiological stress. Oxygen consumption rates increased with increasing temperature from 10 °C to 20 °C though showed a decrease at 25 °C. This rate was not affected by pCO2 or the interaction between temperature and pCO2. Juveniles exposed to present-day and near future pCO2 levels at 20 °C showed similar thermal tolerance polygonal areas; whilst changes in both CTmin and CTmax at 25 °C and 10 °C caused narrower and broader areas, respectively. Temperature affected growth, oxygen consumption and HSP70 transcription in small juvenile C. concholepas. Exposure to elevated pCO2 did not affect thermal tolerance, growth or oxygen consumption at temperatures within the thermal range normally experienced by this species in northern Chile (15-20 °C). At elevated pCO2 conditions, however, exposure to warmer (25 °C) or colder (10 °C) temperatures reduced or increased the thermal area, respectively. This study demonstrates the importance of examining the thermal-tolerance edges to better understand how OA and temperature will combine to physiologically challenge inter-tidal organisms.

Ocean warming and acidification pose synergistic limits to the thermal niche of an economically important echinoderm.

To make robust projectios of the impacts of climate change, it is critical to understand how abiotic factors may interact to constrain the distribution and productivity of marine flora and fauna. We evaluated the effects of projected end of the century ocean acidification (OA) and warming (OW) on the thermal tolerance of an important living marine resource, the sea urchin Loxechinus albus, a benthic shallow water coastal herbivore inhabiting part of the Pacific coast of South America. After exposing young juveniles for a 1-month period to contrasting pCO2 (~500 and 1400 µatm) and temperature (~15 °C and 20 °C) levels, critical thermal maximum (CTmax) and minimum (CTmin) as well as thermal tolerance polygons were assessed based on self-righting success as an end point. Transcription of heat shock protein 70 (HSP70), a chaperone protecting cellular proteins from environmental stress, was also measured. Exposure to elevated pCO2 significantly reduced thermal tolerance by increasing CTmin at both experimental temperatures and decreasing CTmax at 20 °C. There was also a strong synergistic effect of OA × OW on HSP70 transcription levels which were 75 times higher than in control conditions. If this species is unable to adapt to elevated pCO2 in the future, the reduction in thermal tolerance and HSP response suggests that near-future warming and OA will disrupt their performance and reduce their distribution with ecological and economic consequences. Given the wider latitudinal range (6 to 56°S) and environmental tolerance of L. albus compared to other members of this region's benthic invertebrate community, OW and OA may cause substantial changes to the coastal fauna along this geographical range.

Increased temperature but not pCO2 levels affect early developmental and reproductive traits of the economically important habitat-forming kelp Lessonia trabeculata.

The effects of ocean warming and ocean acidification on developmental and reproductive traits of Lessonia trabeculata were evaluated. Meiospores were cultured for 35 days in an experimental mesocosm where temperature (~15 and 19 °C) and partial CO2 pressure (pCO2, ~400 and 1300 µatm) were controlled. The results indicate that germination was reduced at 19 °C, whereas the increase of pCO2 only had effects at 15 °C. Likewise, the increase in temperature significantly affected the vegetative growth of female gametophytes. Sex ratio was not affected significantly by any of the variables studied. Fertility and reproductive success decreased by about 50% at 19 °C. The pCO2 levels had no significant effects on most early developmental traits. The results suggest that ocean warming or periodic warming events (e.g. an El Niño event) might affect the recruiting capacity of this or other similar species by affecting their early developmental stages.