Thermal bottlenecks in the life cycle define climate vulnerability of fish

Species’ vulnerability to climate change depends on the most temperature-sensitive life stages, but for major animal groups such as fish, life cycle bottlenecks are often not clearly defined. We used observational, experimental, and phylogenetic data to assess stage-specific thermal tolerance metrics for 694 marine and freshwater fish species from all climate zones. Our analysis shows that spawning adults and embryos consistently have narrower tolerance ranges than larvae and nonreproductive adults and are most vulnerable to climate warming. The sequence of stage-specific thermal tolerance corresponds with the oxygen-limitation hypothesis, suggesting a mechanistic link between ontogenetic changes in cardiorespiratory (aerobic) capacity and tolerance to temperature extremes. A logarithmic inverse correlation between the temperature dependence of physiological rates (development and oxygen consumption) and thermal tolerance range is proposed to reflect a fundamental, energetic trade-off in thermal adaptation. Scenario-based climate projections considering the most critical life stages (spawners and embryos) clearly identify the temperature requirements for reproduction as a critical bottleneck in the life cycle of fish. By 2100, depending on the Shared Socioeconomic Pathway (SSP) scenario followed, the percentages of species potentially affected by water temperatures exceeding their tolerance limit for reproduction range from ~10% (SSP 1–1.9) to ~60% (SSP 5–8.5). Efforts to meet ambitious climate targets (SSP 1–1.9) could therefore benefit many fish species and people who depend on healthy fish stocks

Broodstock exposure to warming and elevated pCO<inf>2</inf> impairs gamete quality and narrows the temperature window of fertilisation in Atlantic cod

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Early life stages of an arctic keystone species (Boreogadus saida) show high sensitivity to a water-soluble fraction of crude oil

Source: doi: 10.1016/j.envpol.2016.07.044Increasing anthropogenic activities in the Arctic represent an enhanced threat for oil pollution in a marine environment that is already at risk from climate warming. In particular, this applies to species with free-living pelagic larvae that aggregate in surface waters and under the sea ice where hydrocarbons are likely to remain for extended periods of time due to low temperatures. We exposed the positively buoyant eggs of polar cod (Boreogadus saida), an arctic keystone species, to realistic concentrations of a crude oil water-soluble fraction (WSF), mimicking exposure of eggs aggregating under the ice to oil WSF leaking from brine channels following encapsulation in ice. Total hydrocarbon and polycyclic aromatic hydrocarbon levels were in the ng/L range, with most exposure concentrations below the limits of detection throughout the experiment for all treatments. The proportion of viable, free-swimming larvae decreased significantly with dose and showed increases in the incidence and severity of spine curvature, yolk sac alterations and a reduction in spine length. These effects are expected to compromise the motility, feeding capacity, and predator avoidance during critical early life stages for this important species. Our results imply that the viability and fitness of polar cod early life stages is significantly reduced when exposed to extremely low and environmentally realistic levels of aqueous hydrocarbons, which may have important implications for arctic food web dynamics and ecosystem functioning

Northern cod species face spawning habitat losses if global warming exceeds 1.5°C

Source at: http://doi.org/10.1126/sciadv.aas8821 Rapid climate change in the Northeast Atlantic and Arctic poses a threat to some of the world’s largest fish populations. Impacts of warming and acidification may become accessible through mechanism-based risk assessments and projections of future habitat suitability. We show that ocean acidification causes a narrowing of embryonic thermal ranges, which identifies the suitability of spawning habitats as a critical life-history bottleneck for two abundant cod species. Embryonic tolerance ranges linked to climate simulations reveal that ever-increasing CO2 emissions [Representative Concentration Pathway (RCP) 8.5] will deteriorate suitability of present spawning habitat for both Atlantic cod (Gadus morhua) and Polar cod (Boreogadus saida) by 2100. Moderate warming (RCP4.5) may avert dangerous climate impacts on Atlantic cod but still leaves few spawning areas for the more vulnerable Polar cod, which also loses the benefits of an ice-covered ocean. Emissions following RCP2.6, however, support largely unchanged habitat suitability for both species, suggesting that risks are minimized if warming is held “below 2°C, if not 1.5°C,” as pledged by the Paris Agreement

Impact of Ocean Acidification and Warming on the bioenergetics of developing eggs of Atlantic herring Clupea harengus

Atlantic herring (Clupea harengus) is a benthic spawner, therefore its eggs are prone to encounter different water conditions during embryonic development, with bottom waters often depleted of oxygen and enriched in CO2. Some Atlantic herring spawning grounds are predicted to be highly affected by ongoing Ocean Acidification and Warming with water temperature increasing by up to +3°C and CO2 levels reaching ca. 1000 μatm (RCP 8.5). Although many studies investigated the effects of high levels of CO2 on the embryonic development of Atlantic herring, little is known about the combination of temperature and ecologically relevant levels of CO2. In this study, we investigated the effects of Ocean Acidification and Warming on embryonic metabolic and developmental performance such as mitochondrial function, respiration, hatching success (HS) and growth in Atlantic herring from the Oslo Fjord, one of the spawning grounds predicted to be greatly affected by climate change. Fertilized eggs were incubated under combinations of two PCO2 conditions (400 μatm and 1100 μatm) and three temperatures (6, 10 and 14°C), which correspond to current and end-of-the-century conditions. We analysed HS, oxygen consumption (MO2) and mitochondrial function of embryos as well as larval length at hatch. The capacity of the electron transport system (ETS) increased with temperature, reaching a plateau at 14°C, where the contribution of Complex I to the ETS declined in favour of Complex II. This relative shift was coupled with a dramatic increase in MO2 at 14°C. HS was high under ambient spawning conditions (6–10°C), but decreased at 14°C and hatched larvae at this temperature were smaller. Elevated PCO2 increased larval malformations, indicating sub-lethal effects. These results indicate that energetic limitations due to thermally affected mitochondria and higher energy demand for maintenance occur at the expense of embryonic development and growth

World ocean review: Mit den Meeren leben 5. Die Küsten - ein wertvoller Lebensraum unter Druck

Die fünfte Ausgabe des „World Ocean Review“ (WOR) beschäftigt sich mit dem Lebensraum Küste und den vielfältigen Erwartungen, die an diesen Lebensraum gestellt werden. Der WOR 5 gibt einen Einblik in die über Jahrmillionen zurückreichende Geschichte, erläutert die Theorie der Kontinentalveschiebung und erörtert wie sich das Gesicht der Küsten verändert hat. Er zeigt auf, wie die vielfältigen Ökosystemleistungen der Küsten immer mehr unter Druck geraten und stellt Maßnahmen vor, die in Zukunft notwendig sein werden, um den Bedrohungen durch Klimawandel und Naturkatastrophen Herr zu werden

World Ocean Review 2015 : living with the oceans 5. Coasts - a vital habitat under pressure

The fifth World Ocean Review (WOR) explores the coastal habitat and the diverse expectations upon this habitat. It provides a glimpse into millions of years of history, elucidates the theory of continental drift and discusses the many ways in which coasts have changed. It also illustrates how the diverse ecosystem services rendered by the coasts are being subjected to increasing pressure, and profiles measures that will be necessary in the future to respond effectively to the threats from both climate change and natural disasters

Influence of Ocean Acidification on a Natural Winter-to-Summer Plankton Succession : First Insights from a Long-Term Mesocosm Study Draw Attention to Periods of Low Nutrient Concentrations

Every year, the oceans absorb about 30% of anthropogenic carbon dioxide (CO2) leading to a re-equilibration of the marine carbonate system and decreasing seawater pH. Today, there is increasing awareness that these changes-summarized by the term ocean acidification (OA)-could differentially affect the competitive ability of marine organisms, thereby provoking a restructuring of marine ecosystems and biogeochemical element cycles. In winter 2013, we deployed ten pelagic mesocosms in the Gullmar Fjord at the Swedish west coast in order to study the effect of OA on plankton ecology and biogeochemistry under close to natural conditions. Five of the ten mesocosms were left unperturbed and served as controls (similar to 380 mu atm pCO(2)), whereas the others were enriched with CO2-saturated water to simulate realistic end-of-the-century carbonate chemistry conditions (mu 760 mu atm pCO(2)). We ran the experiment for 113 days which allowed us to study the influence of high CO2 on an entire winter-to-summer plankton succession and to investigate the potential of some plankton organisms for evolutionary adaptation to OA in their natural environment. This paper is the first in a PLOS collection and provides a detailed overview on the experimental design, important events, and the key complexities of such a "long-term mesocosm" approach. Furthermore, we analyzed whether simulated end-of-the-century carbonate chemistry conditions could lead to a significant restructuring of the plankton community in the course of the succession. At the level of detail analyzed in this overview paper we found that CO2-induced differences in plankton community composition were non-detectable during most of the succession except for a period where a phytoplankton bloom was fueled by remineralized nutrients. These results indicate: (1) Long-term studies with pelagic ecosystems are necessary to uncover OA-sensitive stages of succession. (2) Plankton communities fueled by regenerated nutrients may be more responsive to changing carbonate chemistry than those having access to high inorganic nutrient concentrations and may deserve particular attention in future studies.Peer reviewe

Identification of lifecycle bottlenecks to assess the vulnerability of fish species to climate change

Globally observed impacts of climate change on marine organisms and ecosystems highlight the need to assess the risks and benefits of international mitigation commitments, such as the goal of limiting global warming to 1.5°C above pre-industrial levels. This requires information on species-specific thermal tolerance thresholds, lifecycle bottlenecks and the sensitivity of critical life stages to additional climate factors such as ocean acidification (OA), the CO2-driven decrease in seawater pH. However, this information is not available for many important fish species, including Atlantic cod (Gadus morhua) and Polar cod (Boreogadus saida). A general assumption is that species adapted to variable climates (e.g., Atlantic cod) have larger tolerance windows than those adapted to relatively stable conditions (e.g., Polar cod), and that egg-stages (embryos) are more vulnerable to temperature changes and OA than adults with fully functional organ systems for oxygen supply and acid-base homeostasis. As adults become sexually mature, temperature windows may narrow due to additional metabolic loads associated with gonad development. Accordingly, there is a risk that future warming and OA will affect the suitability of spawning habitats by exceeding the tolerance thresholds of embryos and/or spawning adults. In this thesis, experimental and meta-analytical investigations on lifecycle bottlenecks were used to describe physiological principles and to identify mitigation pathways that minimize climatic risks regionally (for Atlantic cod and Polar cod) and globally (for marine and freshwater species). The objective of the experimental part (Publication I-III) was to investigate the effects of OA (−0.4 pH, 400 vs 1100 μatm CO2) on embryonic thermal tolerance in Atlantic cod and Polar cod, and to use those embryonic tolerance windows for projections of spawning habitat suitability under different climate change (emission) scenarios. The meta-analysis (Manuscript IV) encompassing data from several hundred species explicitly tested two hypotheses: (i) Thermal tolerance increases from spawning adults and embryos to larvae and non-reproductive adults; (ii) the temperature dependence of physiological rates (i.e., thermal responsiveness) is higher in organisms with narrow temperature windows (stenothermal species or life stages) than in organisms with wide temperature windows (eurythermal species or life stages). Finally, impact risks associated with different global warming scenarios were assessed based on stage-specific tolerance thresholds of species from various climate zones. Experimental results confirmed that embryonic temperature windows are wider in Atlantic cod than in Polar cod. Embryo mortality increased especially above the species-specific spawning temperature range (Atlantic cod: ≥9°C, Polar cod: ≥3°C), most likely due to constraints on aerobic energy (ATP) by mitochondria. The effects of OA intensified these thermal constraints, resulting in a narrowing of the temperature window for embryonic development and thus reproduction. Detailed experiments with Atlantic cod, including biochemical analyses, revealed that embryo vulnerability to additional effects of OA was highest during gastrulation, which is an early period characterized by high developmental complexity and low homeostatic capacity (i.e., low activity and expression of acid-base relevant ion transporters). Enhanced embryonic tolerance after this critical period was probably associated with a rapid (exponential) increase in capacity for ion transport and ATP production. The potential for acclimatization to warming and OA was evidenced through temperature- and OA-dependent changes in protein expression and enzyme activity, especially in larval stages. However, additional costs and developmental trade-offs associated with capacity adjustments during acclimatization (e.g., increased enzyme activity and ATP synthesis under OA) were reflected by increased embryonic oxygen consumption rates and reduced larval size at hatch in both species. Collectively, four experiments consistently showed that OA negatively affects embryonic thermal tolerance and energy efficiency in Atlantic cod and Polar cod. Spawning habitat projections based on embryonic tolerance windows suggest that under the high emission scenario (Representative Concentration Pathway 8.5), both species could lose many important spawning habitats in the northern Northeast Atlantic due to a decrease in embryo survival probability of more than 50%. Reduced emissions (RCP4.5) may avert dangerous climate impacts on Atlantic cod, but still leave few spawning areas for the more vulnerable Polar cod. However, strong emission cuts (RCP2.6), in line with the 1.5°C target, could minimize the risk of spawning habitat loss for both species. The meta-analysis revealed a globally consistent pattern of stage-specific thermal tolerance, indicating that spawners and embryos are less tolerant than larvae and non-reproductive adults. More specifically, it was shown that the tolerance windows of spawners and embryos are generally more than 10°C narrower than those of larvae and adults, possibly reflecting ontogenetic shifts in aerobic and homeostatic capacity. In addition, thermal responsiveness was found to be higher in stenothermal species and life stages with narrow temperature ranges than in eurythermal ones, indicating a mechanistic link between organismal thermal tolerance and the kinetic coordination of metabolic functions. These results clearly identify the temperature requirements for reproduction (gonad and embryo development) as a critical lifecycle bottleneck with respect to the climate change vulnerability of marine and freshwater fish. The global risk assessment revealed that if warming continues unabated (RCP8.5), approximately 50% of the investigated species (N = 107 out of 211) could be confronted with water temperatures exceeding the current tolerance limit of spawners and/or embryos. This means that many species would have to relocate their spawning activity into cooler seasons or regions, which may be particularly problematic for polar species and those dependent on specific habitats (e.g., reef fishes). A positive perspective is that limiting global warming to 1.5°C could reduce the number of species at risk to less than 10%. The results of this thesis clearly demonstrate the importance of integrating life cycle bottlenecks into physiology-based risk assessments for fish stocks. Habitat models and other modelling approaches thus become more effective tools not only to inform societies and policy makers about potential climate change impacts on fish populations and ecosystems, but also to develop effective mitigation strategies. For example, spawning habitat projections indicating potential refuge areas for Atlantic cod and Polar cod can help to establish marine conservation zones and other proactive measures against additional human perturbations such as overfishing and pollution