Beschreibung: The impact of a realistic warming scenario on the metabolic physiology of early cephalopod (squid Loligo vulgaris and cuttlefish Sepia officinalis) life stages was investigated. During exposure to the warming conditions (19 °C for the western coast of Portugal in 2100), the increase in oxygen consumption rates throughout embryogenesis was much steeper in squid (28-fold increase) than in cuttlefish (11-fold increase). The elevated catabolic activity–accelerated oxygen depletion within egg capsules, which exacerbated metabolic suppression toward the end of embryogenesis. Squid late-stage embryos appear to be more impacted by warming via metabolic suppression than cuttlefish embryos. At all temperature scenarios, the transition from encapsulated embryos to planktonic paralarvae implied metabolic increments higher than 100 %. Contrary to the nektobenthic strategy of cuttlefish newborns, the planktonic squid paralarvae rely predominantly on pulsed jet locomotion that dramatically increases their energy requirements. In the future, hatchlings will require more food per unit body size and, thus, feeding intake success will be crucial, especially for squid with high metabolic rates and low levels of metabolic reserves.

Beschreibung: Cephalopods are well known for their cognitive capabilities and unique behavioural repertoires. Yet, certain life strategies and behaviours are still not fully understood. For instance, coastal octopuses have been documented (mainly through citizen science and TV documentaries) to occasionally leave the water and crawl in intertidal areas. Yet, there is a complete lack of knowledge on this behaviour's physiological and biochemical basis. Within this context, this study aimed to investigate, for the first time, physiological (routine and maximum metabolic rates and aerobic scope) and biochemical (i.e., antioxidant enzymes activities, heat shock protein and ubiquitin levels, DNA damage, lipid peroxidation) responses of the common octopus, Octopus vulgaris, to emersion. The octopuses’ physiological performance was determined by measuring metabolic rates in different emersion treatments and biochemical markers. The size-adjusted maximum metabolic rates (MMRadj) of octopuses exposed to 2:30 min of air exposure followed by re-immersion did not differ significantly from the MMRadj of the chased individuals (control group). Yet, most biochemical markers revealed no significant differences among the different emersion treatments. Our findings showed that O. vulgaris could tolerate exposure to short-term emersion periods due to an efficient antioxidant machinery and cellular repair mechanisms. Alongside, we argue that the use of atmospheric air through the mucus-covered gills and/or cutaneous respiration may also help octopus withstand emersion and crawling on land.

Beschreibung: Ocean acidification is one of the many consequences of climate change. Various studies suggest that marine organisms' behaviour will be impaired under high CO2. Here, we show that the cognitive performance of the cleaner wrasse, Labroides dimidiatus, has not suffered from the increase of CO2 from pre-industrial levels to today, and that the standing variation in CO2 tolerance offers potential for adaptation to at least 750 µatm. We acclimated cleaners over 30 days to five levels of pCO2, from pre-industrial to high future CO2 scenarios, before testing them in an ecologically relevant task—the ability to learn to prioritize an ephemeral food source over a permanent one. Fish learning abilities remained stable from pre-industrial to present-day pCO2. While performance was reduced under mid (750 µatm) and high CO2 (980 µatm) scenarios, under the former 36% of cleaners still solved the task. The presence of tolerant individuals reveals potential for adaptation, as long as selection pressure on cognitive performance is strong. However, the apparent absence of high CO2 tolerant fish, and potentially synergistic effects between various climate change stressors, renders the probability of further adaptation unlikely.

Beschreibung: Cleaning interactions are textbook examples of mutualisms. On coral reefs, most fishes engage in cooperative interactions with cleaners fishes, where they benefit from ectoparasite reduction and ultimately stress relief. Furthermore, such interactions elicit beneficial effects on clients' ecophysiology. However, the potential effects of future ocean warming (OW) and acidification (OA) on these charismatic associations are unknown. Here we show that a 45-day acclimation period to OW (+3 °C) and OA (980 μatm pCO2) decreased interactions between cleaner wrasses (Labroides dimidiatus) and clients (Naso elegans). Cleaners also invested more in the interactions by providing tactile stimulation under OA. Although this form of investment is typically used by cleaners to prolong interactions and reconcile after cheating, interaction time and client jolt rate (a correlate of dishonesty) were not affected by any stressor. In both partners, the dopaminergic (in all brain regions) and serotoninergic (forebrain) systems were significantly altered by these stressors. On the other hand, in cleaners, the interaction with warming ameliorated dopaminergic and serotonergic responses to OA. Dopamine and serotonin correlated positively with motivation to interact and cleaners interaction investment (tactile stimulation). We advocate that such neurobiological changes associated with cleaning behaviour may affect the maintenance of community structures on coral reefs.

Beschreibung: Seagrasses play an essential ecological role within coastal habitats and their worldwide population decline has been linked to different types of anthropogenic forces. We investigated, for the first time, the combined effects of future ocean warming and acidification on fundamental biological processes of Zostera noltii, including shoot density, leaf coloration, photophysiology (electron transport rate, ETR; maximum PSII quantum yield, Fv/Fm) and photosynthetic pigments. Shoot density was severely affected under warming conditions, with a concomitant increase in the frequency of brownish colored leaves (seagrass die-off). Warming was responsible for a significant decrease in ETR and Fv/Fm (particularly under control pH conditions), while promoting the highest ETR variability (among experimental treatments). Warming also elicited a significant increase in pheophytin and carotenoid levels, alongside an increase in carotenoid/chlorophyll ratio and De-Epoxidation State (DES). Acidification significantly affected photosynthetic pigments content (antheraxanthin, beta-carotene, violaxanthin and zeaxanthin), with a significant decrease being recorded under the warming scenario. No significant interaction between ocean acidification and warming was observed. Our findings suggest that future ocean warming will be a foremost determinant stressor influencing Z. noltii survival and physiological performance. Additionally, acidification conditions to occur in the future will be unable to counteract deleterious effects posed by ocean warming.

Beschreibung: Carbon dioxide concentration in the atmosphere is expected to continue rising by 2100, leading to a decrease in ocean pH in a process known as ocean acidification (OA). OA can have a direct impact on calcifying organisms, including on the cuttlebone of the common cuttlefish Sepia officinalis. Moreover, nutritional status has also been shown to affect the cuttlebone structure and potentially affect buoyancy. Here, we aimed to understand the combined effects of OA (980 μatm CO2) and food availability (fed vs. non-fed) on the buoyancy of cuttlefish newborns and respective cuttlebone weight/area ratio (as a proxy for calcification). Our results indicate that while OA elicited negative effects on hatching success, it did not negatively affect the cuttlebone weight/area ratio of the hatchlings-OA led to an increase in cuttlebone weight/area ratio of fed newborns (but not in unfed individuals). The proportion of “floating” (linked to buoyancy control loss) newborns was greatest under starvation, regardless of the CO2 treatment, and was associated with a drop in cuttlebone weight/area ratio. Besides showing that cuttlefish buoyancy is unequivocally affected by starvation, here, we also highlight the importance of nutritional condition to assess calcifying organisms' responses to ocean acidification.

Beschreibung: Since the industrial revolution, [CO2]atm has increased from 280 µatm to levels now exceeding 380 µatm and is expected to rise to 730-1,020 µatm by the end of this century. The consequent changes in the ocean's chemistry (e.g., lower pH and availability of the carbonate ions) are expected to pose particular problems for marine organisms, especially in the more vulnerable early life stages. The aim of this study was to investigate how the future predictions of ocean acidification may compromise the metabolism and swimming capabilities of the recently hatched larvae of the tropical dolphinfish (Coryphaena hippurus). Here, we show that the future environmental hypercapnia (delta pH 0.5; 0.16 % CO2, ~1,600 µatm) significantly (p 〈 0.05) reduced oxygen consumption rate up to 17 %. Moreover, the swimming duration and orientation frequency also decreased with increasing pCO2 (50 and 62.5 %, respectively). We argue that these hypercapnia-driven metabolic and locomotory challenges may potentially influence recruitment, dispersal success, and the population dynamics of this circumtropical oceanic top predator.

Beschreibung: Increases in carbon dioxide (CO2) and other greenhouse gases emissions are changing ocean temperature and carbonate chemistry (warming and acidification, respectively). Moreover, the simultaneous occurrence of highly toxic and persistent contaminants, such as methylmercury, will play a key role in further shaping the ecophysiology of marine organisms. Despite recent studies reporting mostly additive interactions between contaminant and climate change effects, the consequences of multi-stressor exposure are still largely unknown. Here we disentangled how Argyrosomus regius physiology will be affected by future stressors, by analysing organ-dependent mercury (Hg) accumulation (gills, liver and muscle) within isolated/combined warming (delta T = 4 °C) and acidification (ΔpCO2 = 1100 μatm) scenarios, as well as direct deleterious effects and phenotypic stress response over multi-stressor contexts. After 30 days of exposure, although no mortalities were observed in any treatments, Hg concentration was enhanced under warming conditions, especially in the liver. On the other hand, elevated CO2 decreased Hg accumulation and consistently elicited a dampening effect on warming and contamination-elicited oxidative stress (catalase, superoxide dismutase and glutathione-S-transferase activities) and heat shock responses. Thus, potentially unpinned on CO2-promoted protein removal and ionic equilibrium between hydrogen and reactive oxygen species, we found that co-occurring acidification decreased heavy metal accumulation and contributed to physiological homeostasis. Although this indicates that fish can be physiologically capable of withstanding future ocean conditions, additional experiments are needed to fully understand the biochemical repercussions of interactive stressors (additive, synergistic or antagonistic).

Beschreibung: Cleaning symbioses are key mutualistic interactions where cleaners remove ectoparasites and tissues from client fishes. Such interactions elicit beneficial effects on clients' ecophysiology, with cascading effects on fish diversity and abundance. Ocean acidification (OA), resulting from increasing CO2 concentrations, can affect the behavior of cleaner fishes making them less motivated to inspect their clients. This is especially important as gnathiid fish ectoparasites are tolerant to ocean acidification. Here, we investigated how access to cleaning services, performed by the cleaner wrasse Labroides dimidiatus, affect individual client's (damselfish, Pomacentrus amboinensis) aerobic metabolism in response to both experimental parasite infection and OA. Access to cleaning services was modulated using a long-term removal experiment where cleaner wrasses were consistently removed from patch reefs around Lizard Island (Australia) for 17 years or left undisturbed. Only damselfish with access to cleaning stations had a negative metabolic response to parasite infection (maximum metabolic rate—ṀO2Max; and both factorial and absolute aerobic scope). Moreover, after an acclimation period of 10 days to high CO2 (∼1,000 µatm CO2), the fish showed a decrease in factorial aerobic scope, being the lowest in fish without the access to cleaners. We propose that stronger positive selection for parasite tolerance might be present in reef fishes without the access to cleaners, but this might come at a cost, as readiness to deal with parasites can impact their response to other stressors, such as OA.

Beschreibung: Little is known about the capacity of early life stages to undergo hypercapnic and thermal acclimation under the future scenarios of ocean acidification and warming. Here, we investigated a comprehensive set of biological responses to these climate change-related variables (2°C above winter and summer average spawning temperatures and ΔpH=0.5 units) during the early ontogeny of the squid Loligo vulgaris. Embryo survival rates ranged from 92% to 96% under present-day temperature (13–17°C) and pH (8.0) scenarios. Yet, ocean acidification (pH 7.5) and summer warming (19°C) led to a significant drop in the survival rates of summer embryos (47%, P〈0.05). The embryonic period was shortened by increasing temperature in both pH treatments (P〈0.05). Embryo growth rates increased significantly with temperature under present-day scenarios, but there was a significant trend reversal under future summer warming conditions (P〈0.05). Besides pronounced premature hatching, a higher percentage of abnormalities was found in summer embryos exposed to future warming and lower pH (P〈0.05). Under the hypercapnic scenario, oxygen consumption rates decreased significantly in late embryos and newly hatched paralarvae, especially in the summer period (P〈0.05). Concomitantly, there was a significant enhancement of the heat shock response (HSP70/HSC70) with warming in both pH treatments and developmental stages. Upper thermal tolerance limits were positively influenced by acclimation temperature, and such thresholds were significantly higher in late embryos than in hatchlings under present-day conditions (P〈0.05). In contrast, the upper thermal tolerance limits under hypercapnia were higher in hatchlings than in embryos. Thus, we show that the stressful abiotic conditions inside the embryo's capsules will be exacerbated under near-future ocean acidification and summer warming scenarios. The occurrence of prolonged embryogenesis along with lowered thermal tolerance limits under such conditions is expected to negatively affect the survival success of squid early life stages during the summer spawning period, but not winter spawning.