The increasing CO2 concentration is a major cause of the climate change phenomenon. Concurrently, the same increase is leading to ocean acidification (OA), which is projected to decrease seawater pH by 0.4 units by 2100. Here we investigated the potential impacts of OA on the canopy-forming brown macroalga Gongolaria barbata from the Venice Lagoon. One-year-old individuals were maintained in mesocosms under two pH levels: 8.1 (current ambient value) and 7.7 (the end-of-the-century value predicted under the current scenario of anthropogenic CO2 emissions). The physiological responses of the algae were assessed during the experiment in terms of oxygen production and consumption, and maximal PSII photochemical efficiency. At the end of the experiment, we analyzed the percentage of mature receptacles, algal growth rate and the total polyphenolic content and antioxidant capacity as indicators of the stress response. The significant decrease in polyphenolic content indicates the impairment of the defence mechanisms, which could make the algae more vulnerable to grazing under acidified conditions. Yet, conversely, our results suggest that changes in pH levels do not significantly affect the physiological processes, growth or fertility of the algae. These findings suggest that while OA may weaken defence mechanisms, the preservation of physiological and reproductive functions would still support the potential of G. barbata populations from the Venice Lagoon to act as donor sources for restoration efforts, highlighting their resistance to the acidified conditions expected in the future.
Aquatic species living in productive coastal habitats with abundant primary producers have evolved in highly dynamic diel and seasonally fluctuating environments in terms of, for example, water temperature and dissolved oxygen. However, how environmental fluctuations shape the thermal tolerance of marine species is still poorly understood. Here we hypothesize that the degree of predictability of the diel environmental fluctuations in the coastal area can explain the thermal response of marine species. To test this hypothesis, we measured the thermal tolerance of 17 species of marine ectotherm from tropical, warm temperate and cold temperate latitudes under two levels of oxygen (around saturation and at supersaturation), and relate the results to their site-specific temperature and oxygen fluctuation and their environmental predictability. We demonstrate that oxygen and temperature fluctuations at tropical latitudes have a higher predictability than those at warm and cold temperate latitudes. Further, we show that marine species that are adapted to high predictability have the potential to tune their thermal performance when exposed to oxygen supersaturation, despite being constrained within a narrow safety margin. We advocate that the predictability of the environmental fluctuation needs to be considered when measuring and forecasting the response of marine animals to global warming.
The decline of dissolved oxygen in the oceans could be detrimental to marine life and biogeochemical cycles. However, predicting future oxygen availability with models that mainly focus on temporal and spatial large-scale mean values could lead to incorrect predictions. Marine ecosystems are strongly influenced by short temporal- and small spatial-scale oxygen fluctuations. Large-scale modelling neglects fluctuations, which include the pervasive occurrence of high oxygen supersaturation on a daily time scale in productive ecosystems such as coral reefs, seagrass meadows and mangrove forests and the spatial heterogeneity in oxygen availability at microclimatic scales. In these temporal and spatial micro-environments, oxygen fluctuations control biogeochemical cycles and alter community responses to, for example, heat stress and hypoxia. Robust projections on the impact of predicted ocean and coastal deoxygenation require a better understanding of the dynamics of the dissolved oxygen coupled with scaled-down projections of oxygen fluctuations at small relevant scales for marine biogeochemical processes and communities. Overall, the study of the true oxygen dynamics in marine productive habitats can provide crucial insights into the feedback mechanisms between climate change and marine ecosystems and can help to develop effective management and conservation strategies.
Environmental fluctuation forms a framework of variability within which species have evolved. Environmental fluctuation includes predictability, such as diel cycles of aquatic oxygen fluctuation driven by primary producers. Oxygen availability and fluctuation shape the physiological responses of aquatic animals to warming, so that, in theory, oxygen fluctuation could influence their thermal ecology. We describe annual oxygen variability in agricultural drainage channels and show that disruption of oxygen fluctuation through dredging of plants reduces the thermal tolerance of freshwater animals. We compared the temperature responses of snails, amphipods, leeches and mussels exposed to either natural oxygen fluctuation or constant oxygen in situ under different acclimation periods. Oxygen saturation in channel water ranged from c. 0 % saturation at night to >300 % during the day. Temperature showed normal seasonal variation and was almost synchronous with daily oxygen fluctuation. A dredging event in 2020 dramatically reduced dissolved oxygen variability and the correlation between oxygen and temperature was lost. The tolerance of invertebrates to thermal stress was significantly lower when natural fluctuation in oxygen availability was reduced and decoupled from temperature. This highlights the importance of natural cycles of variability and the need to include finer scale effects, including indirect biological effects, in modelling the ecosystem-level consequences of climate change. Furthermore, restoration and management of primary producers in aquatic habitats could be important to improve the thermal protection of aquatic invertebrates and their resistance to environmental variation imposed by climate change.
EDITORIAL article Front. Physiol., 27 October 2023Sec. Environmental, Aviation and Space Physiology Volume 14 - 2023 | https://doi.org/10.3389/fphys.2023.1305645
Oxygen availability is a pivotal factor for ecosystem functioning and the resistance of organisms to the effect of climate change in aquatic habitats. Although extensive work has been done to assess the effect of oxygen on marine and freshwater biota, many studies have not captured the ecological importance of oxygen variations. Overlooking the fluctuating nature of oxygen may cause potential biases in the design and implementation of management policies for aquatic habitats. Conceptual perspectives on the dynamic nature of oxygen fluctuations have been raised in the scientific community in order to enhance the understanding of the effect of oxygen on the physiology and the ecology of aquatic species as well as the biogeochemical functioning of their ecosystems. A growing number of empirical work has been outlining a novel conceptual framework that considers the magnitude of oxygen fluctuation as a key variable that explains adaptation to stress conditions. Oxygen in productive aquatic habitats shows large fluctuations at the diel scale, exposing aquatic species to conditions ranging from extreme supersaturation to anoxia. Recent research has indicated that such a fluctuation tunes the physiological plasticity of the animal in response to thermal stresses. In this paper, we provide compelling evidence based on current research that the fluctuating oxygen landscape, here defined as “oxyscape”, has an important role in aquatic animal physiology and adaptation as well as the ecosystem biogeochemistry. We propose that the oxyscape should be considered in the modelling and managing policies of aquatic ecosystems.
Downscaling the study of the endangered relict snail, Melanopsis etrusca, at the level of populations, inhabiting geographically separated thermal springs in central Italy, we identified intraspecific mechanisms of local specialization. We advocate that the fit of physiological and behavioural traits to different microclimatic niches should be included to design effective conservation actions.
Oxygen availability, together with water temperature, greatly varies in coastal habitats, especially in those characterized by elevated primary production. In this study, we investigate the combined role of dissolved oxygen and temperature on the thermal physiological response of the mud crab Thalamita crenata living in an equatorial system of coastal habitats. We sampled temperature, oxygen and salinity in T. crenata habitats, mangrove creeks and fringes and seagrass meadows, at Gazi Bay (Kenya). We found that seagrass meadows exhibited higher temperature and oxygen saturation than the mangrove habitats during the day, creating conditions of oxygen supersaturation. By investigating the effect of different levels of oxygen saturation on the thermal response of T. crenata, we demonstrated that the respiratory physiology of this ectotherm has a pronounced resistance to heat, directly influenced by the amount of dissolved oxygen in the water. Under low oxygen saturation levels, the mud crab significantly reduced its metabolism, becoming temperature-independent. This result shows that aquatic species can modulate their thermal response in a stringent dependency with water oxygen saturation, corroborating previous findings on the thermal response of T. crenata under supersaturation. This contribution provides further support for the need to adopt an ecologically-relevant approach to forecast the effect of climate change on marine ectothermal species.
Coastal marine systems are characterized by high levels of primary production that result in diel oxygen fluctuations from undersaturation to supersaturation. Constant normoxia, or 100% oxygen saturation, is therefore rare. Since the thermal sensitivity of invertebrates is directly linked to oxygen availability, we hypothesized that (i) the metabolic response of coastal marine invertebrates would be more sensitive to thermal stress when exposed to oxygen supersaturation rather than 100% oxygen saturation and (ii) natural diel fluctuation in oxygen availability rather than constant 100% oxygen saturation is a main driver of the thermal response. We tested the effects of oxygen regime on the metabolic rate, and haemocyanin and lactate levels, of velvet crabs (Necora puber) and blue mussels (Mytilus edulis), under rising temperatures (up to 24°C) in the laboratory. Oxygen supersaturation and photosynthetically induced diel oxygen fluctuation amplified animal metabolic thermal response significantly in both species, demonstrating that the natural variability of oxygen in coastal environments can provide considerable physiological benefits under ocean warming. Our study highlights the significance of integrating ecologically relevant oxygen variability into experimental assessments of animal physiology and thermal response, and predictions of metabolic performance under climate warming. Given the escalating intensity and frequency of climate anomalies, oxygen variation caused by coastal vegetation will likely become increasingly important in mitigating the effects of higher temperatures on coastal fauna.
Grapevine is a well-known host plant of the invasive pest Drosophila suzukii, but its susceptibility to pest oviposition and development greatly depends on the cultivar. To address environmental sustainability during viticultural zoning planning, new vineyard plantation and Integrated Pest Management programmes, it is essential to take pest pressure and cultivar susceptibility into account. To determine the different grapevine cultivars susceptibility to D. suzukii, we tested twelve widely spread cultivars during the ripening period. We also tested three cultivars during the drying period for raisin wine production. The infestation and emergence rates were consequently related to chemical and texture features of the berries to explain the role of skin and pulp characteristics in determining the nature of the susceptibility. Our results showed that susceptibility to D. suzukii infestation varies across cultivars. On ripening grapes, infestation is primarily influenced by skin and pulp firmness, elasticity and consistency. Suitability for egg development resulted mainly related to skin and pulp deformation. In a drying loft, infestation may also occur in relation to skin and pulp consistency. Lastly, we discuss the practical implication of the underestimated role of berry texture in D. suzukii oviposition and emergence success, in both ripening and drying grapes.
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.
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.
Prolonged diapause occurs in a number of insects and is interpreted as a way to evade adverse conditions.The winter pine processionary moths (Thaumetopoea pityocampa and Th.wilkinsoni) are important pest of pines and cedars in the Mediterranean region.They are typically univoltine, with larvae feeding across the winter, pupating in spring in the soil and emerging as adults in summer.Pupae may, however, enter a prolonged diapause with adults emerging one or more years later.We tested the effect of spatial variation in winter temperature on the incidence of prolonged diapause, using a total of 64 individual datasets related to insect cohorts over the period 1964-2015 for 36 sites in 7 countries, covering most of the geographic range of the species.We found high variation in prolonged diapause incidence over the species' range.Insect cohorts exposed to average winter temperatures lower than 0°C were associated with higher prolonged diapause incidence than cohorts exposed to intermediate temperatures.Prolonged diapause may represent a risk-spreading strategy although it is associated with high mortality because of a longer exposure to mortality factors, desiccation, and energy depletion.Climate change, and in particular the increase of winter temperature, may reduce the incidence of prolonged diapause at the colder sites whereas it may increase it at the warmer ones, with consequences on the population dynamics.
Diapause development is a complex process involving several eco-physiological phases. Understanding these phases, especially diapause termination, is vital for interpreting the life history of many insect species and for developing suitable predictive models of population dynamics. The pine processionary moth is a major defoliator of pine and a vertebrate health hazard in the Mediterranean region. This species can display either univoltine or semivoltine development, with a pupal diapause extending from a few months to several years, respectively. Although the ecological and applied importance of diapause is acknowledged, its physiological regulation in either case remains obscure. In the present study, we characterize pre-termination, termination and post-termination phases of pupae developing as univoltine or remaining in prolonged diapause. Changes in metabolic activity are monitored continuously using thermocouples, comprising a novel method based on direct calorimetry, and periodically by use of O-2 respirometry. The two methods clearly detect diapause termination in both types of pupae before any visible morphological or behavioural changes can be observed. Univoltine individuals are characterized by an increase in metabolic activity from pre-termination through to termination and post-termination, ultimately resulting in emergence. Remarkably, a synchronous termination is observed in individuals that enter prolonged diapause instead of emerging; however, in these pupae, the increased metabolic activity is only transient. The present study represents a starting point toward understanding the eco-physiology of diapause development processes in the pupae of the pine processionary moth.
Expected temperature rise and seawater pH decrease may affect marine organism fitness. By a transplant experiment involving air-temperature manipulation along a natural CO2 gradient, we investigated the effects of high pCO2 (~1100 μatm) and elevated temperature (up to +2 °C than ambient conditions) on the reproductive success, recruitment, growth, shell chemical composition and oxygen consumption of the early life stages of the intertidal reef-building vermetid Dendropoma cristatum. Reproductive success was predominantly affected by temperature increase, with encapsulated embryos exhibiting higher survival in control than elevated temperature conditions, which were in turn unaffected by altered seawater pH levels. Decreasing pH (alone or in combination with temperature) significantly affected the shell growth and shell chemical composition of both embryos and recruits. Elevated temperatures along with lower pH led to decreases of ~30% oxygen consumption and ~60% recruitment. Our results suggest that the early life stages of the reef-builder D. cristatum are highly sensitive to expected environmental change, with major consequences on the intertidal vermetid reefs they build and indirectly on the high biodiversity levels they support.
Drosophila suzukii (Matsumura, 1931) is a highly successful invasive dipteran which represents a serious threat for global fruit industry. Among other adaptive traits, D. suzukii owes its success to the derived morphological features of its ovipositor, which allows the insect to exploit the exclusive ecological niche of fresh fruit, thus avoiding competition with other closely related species. With the aim of investigating temperature-induced phenotypic plasticity of D. suzukii ovipositor, we reared this insect in four different laboratory conditions, represented by the combination of two developmental temperatures and two diet regimes for the larvae. We recorded the effects of these two factors on ovipositor size and shape and overall body size through a combination of distance-based and geometric morphometric analyses. Results showed that insects attain the largest body sizes at lower temperature, whereas the diet does not determine significant difference in size. However, the effect on size of the two factors is less pronounced in the ovipositor, which shows a negative allometry with respect to body size in all treatments. At higher temperature, ovipositor shape tends also to co-vary with its own size. Neither temperature nor diet have significant effect on ovipositor bilateral fluctuating asymmetry. These results confirm the hypothesis that in D. suzukii the toughened valve of the ovipositor are subjected to effective morpho-functional constraints, while probably being under strong selection by reason of their mechanical role.
Prolonged diapause occurs in a number of insects and is interpreted as a way to evade adverse conditions. The winter pine processionary moths (Thaumetopoea pityocampa and Th. wilkinsoni) are important pest of pines and cedars in the Mediterranean region. They are typically univoltine, with larvae feeding across the winter, pupating in spring in the soil and emerging as adults in summer. Pupae may, however, enter a prolonged diapause with adults emerging one or more years later. We tested the effect of spatial variation in winter temperature on the incidence of prolonged diapause, using a total of 64 individual datasets related to insect cohorts over the period 1964-2015 for 36 sites in 7 countries, covering most of the geographic range of the species. We found high variation in prolonged diapause incidence over the species’ range. Insect cohorts exposed to average winter temperatures lower than 0°C were associated with higher prolonged diapause incidence than cohorts exposed to intermediate temperatures. Prolonged diapause may represent a risk-spreading strategy although it is associated with high mortality because of a longer exposure to mortality factors, desiccation, and energy depletion. Climate change, and in particular the increase of winter temperature, may reduce the incidence of prolonged diapause at the colder sites whereas it may increase it at the warmer ones, with consequences on the population dynamics.
1 Insects with short-lived adults must synchronize their emergence to maximize fitness. 2 However, pre-imaginal development time often varies among individuals as a result of exposure to varied abiotic and biotic factors; therefore, mechanisms adjusting pre-imaginal development time are expected. 3 Larvae of the pine processionary moth feed throughout the winter and conclude their development with characteristic processions in spring, leaving the trees to pupate in soil. 4 The procession period can be as long as 2 months in some regions because of prior desynchronization of larval colonies, whereas the emergence period of the adults in summer remains short (less than 1 month). 5 Through weekly sampling of larvae leaving trees to pupate in soil and subsequent rearing under field and laboratory conditions, it was observed that early prepupae waited longer than late prepupae before moulting into pupa. 6 The differential duration of the prepupal stage was independent of temperature conditions and allowed resynchronization of colonies and overlapping emergences. 7 The prepupal phase therefore appears to be critical for understanding the regulation of adult emergence of this important pest insect.
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.