Coping with cyclic oxygen availability: evolutionary aspects

Both the gradual rise in atmospheric oxygen over the Proterozoic Eon as well as episodic fluctuations in oxygen over several million-year time spans during the Phanerozoic Era, have arguably exerted strong selective forces on cellular and organismic respiratory specialization and evolution. The rise in atmospheric oxygen, some 2 billion years after the origin of life, dramatically altered cell biology and set the stage for the appearance of multicelluar life forms in the Vendian (Ediacaran) Period of the Neoproterozoic Era. Over much of the Paleozoic, the level of oxygen in the atmosphere was near the present atmospheric level (21%). In the Late Paleozoic, however, there were extended times during which the level of atmospheric oxygen was either markedly lower or markedly higher than 21%. That these Paleozoic shifts in atmospheric oxygen affected the biota is suggested by the correlations between: (1) Reduced oxygen and the occurrences of extinctions, a lowered biodiversity and shifts in phyletic succession, and (2) During hyperoxia, the corresponding occurrence of phenomena such as arthropod gigantism, the origin of insect flight, and the evolution of vertebrate terrestriality. Basic similarities in features of adaptation to hyopoxia, manifest in living organisms at levels ranging from genetic and cellular to physiological and behavioral, suggest the common and early origin of a suite of adaptive mechanisms responsive to fluctuations in ambient oxygen. Comparative integrative approaches addressing the molecular bases of phenotypic adjustments to cyclic oxygen fluctuation provide broad insight into the incremental steps leading to the early evolution of homeostatic respiratory mechanisms and to the specialization of organismic respiratory functio

The trade-off between heat tolerance and metabolic cost drives the bimodal life strategy at the air-water interface

The principle of oxygen and capacity limitation of thermal tolerance in ectotherms suggests that the long-term upper limits of an organism's thermal niche are equivalent to the upper limits of the organism's functional capacity for oxygen provision to tissues. Air-breathing ectotherms show wider thermal tolerances, since they can take advantage of the higher availability of oxygen in air than in water. Bimodal species move from aquatic to aerial media and switch between habitats in response to environmental variations such as cyclical or anomalous temperature fluctuations. Here we tested the prediction that bimodal species cope better with thermal stress than truly aquatic species using the crab Pachygrapsus marmoratus as a model species. When in water, oxygen consumption rates of P. marmoratus acutely rise during warming. Beyond a temperature threshold of 23 °C the crab's aerobic metabolism in air remains lower than in water. In parallel, the haemolymph oxygen partial pressure of submerged animals progressive decreases during warming, while it remains low but constant during emersion. Our results demonstrate the ability of a bimodal breathing ectotherm to extend its thermal tolerance during air-breathing, suggesting that there are temperature-related physiological benefits during the evolution of the bimodal life style

Concurrent environmental stressors and jellyfish stings impair caged European sea bass (Dicentrarchus labrax) physiological performances

none8siThe increasing frequency of jellyfish outbreaks in coastal areas has led to multiple ecological and socio-economic issues, including mass mortalities of farmed fish. We investigated the sensitivity of the European sea bass (Dicentrarchus labrax), a widely cultured fish in the Mediterranean Sea, to the combined stressors of temperature, hypoxia and stings from the jellyfish Pelagia noctiluca, through measurement of oxygen consumption rates (MO2), critical oxygen levels (PO2crit), and histological analysis of tissue damage. Higher levels of MO2, PO2crit and gill damage in treated fish demonstrated that the synergy of environmental and biotic stressors dramatically impair farmed fish metabolic performances and increase their health vulnerability. As a corollary, in the current scenario of ocean warming, these findings suggest that the combined effects of recurrent hypoxic events and jellyfish blooms in coastal areas might also threaten wild fish populations.openBosch-Belmar, Mar; Giomi, Folco; Rinaldi, Alessandro; Mandich, Alberta; Fuentes, Verónica; Mirto, Simone; Sarà, Gianluca; Piraino, StefanoBosch Belmar, Mar; Giomi, Folco; Rinaldi, Alessandro; Mandich, Alberta; Fuentes, Verónica; Mirto, Simone; Sarà, Gianluca; Piraino, Stefan

Improved heat tolerance in air drives the recurrent evolution of air-breathing

The transition to air-breathing by formerly aquatic species has occurred repeat-edly and independently in fish, crabs and other animal phyla, but the proximatedrivers of this key innovation remain a long-standing puzzle in evolutio-nary biology. Most studies attribute the onset of air-breathing to the repeatedoccurrence of aquatic hypoxia; however, this hypothesis leaves the current geo-graphical distribution of the 300 genera of air-breathing crabs unexplained.Here, we show that their occurrence is mainly related to high environmentaltemperatures in the tropics. We also demonstrate in an amphibious crab thatthe reduced cost of oxygen supply in air extends aerobic performance tohigher temperatures and thus widensthe animal’sthermal niche. These findingssuggest that high water temperature as a driverconsistentlyexplainsthe numer-ous times air-breathing has evolved. The data also indicate a central role foroxygen- and capacity-limited thermal tolerance not only in shaping sensitivityto current climate change but also in underpinning the climate-dependentevolution of animals, in this case the evolution of air-breathing

Oxygen supersaturation protects coastal marine fauna from ocean warming

Ocean warming affects the life history and fitness of marine organisms by, among others, increasing animal metabolism and reducing oxygen availability. In coastal habitats, animals live in close association with photosynthetic organisms whose oxygen supply supports metabolic demands and may compensate for acute warming. Using a unique high-frequency monitoring dataset, we show that oxygen supersaturation resulting from photosynthesis closely parallels sea temperature rise during diel cycles in Red Sea coastal habitats. We experimentally demonstrate that oxygen supersaturation extends the survival to more extreme temperatures of six species from four phyla. We clarify the mechanistic basis of the extended thermal tolerance by showing that hyperoxia fulfills the increased metabolic demand at high temperatures. By modeling 1 year of water temperatures and oxygen concentrations, we predict that oxygen supersaturation from photosynthetic activity invariably fuels peak animal metabolic demand, representing an underestimated factor of resistance and resilience to ocean warming in ectotherms

Thermal sensitivity of the crab Neosarmatium africanum in tropical and temperate mangroves on the east coast of Africa

Mangrove forests are amongst the tropical marine ecosystems most severely affected by rapid environmental change, and the activities of key associated macrobenthic species contribute to their ecological resilience. Along the east coast of Africa, the amphibious sesarmid crab Neosarmatium africanum (=meinerti) plays a pivotal role in mangrove ecosystem functioning through carbon cycling and sediment bioturbation. In the face of rapid climate change, identifying the sensitivity and vulnerability to global warming of this species is of increasing importance. Based on a latitudinal comparison, we measured the thermal sensitivity of a tropical and a temperate population of N. africanum, testing specimens at the centre and southern limit of its distribution, respectively. We measured metabolic oxygen consumption and haemolymph dissolved oxygen content during air and water breathing within a temperature range that matched the natural environmental conditions. The results indicate different thermal sensitivities in the physiological responses of N. africanum from tropical and temperate populations, especially during air breathing. The differences observed in the thermal physiology between the two populations suggest that the effect of global warming on this important mangrove species may be different under different climate regimes

Sea urchin chronicles. The effect of oxygen super-saturation and marine polluted sediments from Bagnoli-Coroglio Bay on different life stages of the sea urchin Paracentrotus lividus

In marinas and harbours, the accumulation of pollutants in sediments, combined with poor exchange of water with the open sea, poses a major environmental threat. The presence of photosynthetic organisms and the related oxygen production, however, may alleviate the negative effects of environmental contamination on heterotrophic organisms, enhancing their physiological defences. Furthermore, possible transgenerational buffer effects may increase the ability of natural populations to face environmental stress. Here we tested the occurrence of transgenerational effects on larvae of the sea urchin Paracentrotus lividus, whose parents were exposed, during the gametogenesis, to contaminated sediments subject to two temporal patterns of water re-suspension events and normal- (90%) vs. super-saturated (200%) levels of O2. The study site was Bagnoli-Coroglio (Gulf of Naples, southern Tyrrhenian Sea), a historically polluted brownfield and Site of National Interest for which environmental restoration options are currently under exploration. Larvae from different adult populations were significantly, although not linearly, affected by the interaction of all factors to which parents were exposed, at both 24h and 48h post fertilization. Specifically, the exposure of larvae to elutriates from contaminated sediments determined a developmental delay, a reduction in size and an increased percentage of abnormalities in all larval populations independently of their parental exposure. On the contrary, larvae from parents exposed to contaminated sediments, when reared in clean filtered sea water, succeeded in developing until the echinopluteus stage after 48h, with size and abundance comparable to those of larvae from control parents. Pre-exposure of parents to contaminated sediments did not successfully buffer the negative effects of elutriates on their offspring, and no positive effects of ‘super-saturated’ levels of O2 in response to contaminants were observed, suggesting that the Bagnoli-Coroglio area is currently not suitable for the re-stocking or re-introduction of this species