Climate Action

Living Edition
| Editors: Walter Leal Filho, Anabela Marisa Azul, Luciana Brandli, Pinar Gökcin Özuyar, Tony Wall

Climate Change, Multiple Stressors, and Responses of Marine Biota

  • Eduardo SampaioEmail author
  • Rui Rosa
Living reference work entry
DOI: https://doi.org/10.1007/978-3-319-71063-1_90-1

Synonyms

Definition

Human-exacerbated emissions of greenhouse gases and nutrients are creating a multitude of chemical, physical, and biological stressors, disrupting the natural equilibrium within individual homeostasis, multi-species communities, and entire ecosystems.

Introduction

Climate change is ongoing and will be further aggravated if greenhouse gas emissions, and other anthropogenic pressures, remain unabated (IPCC 2013). Such scenario will imply a marked change on several abiotic parameters caused by said gases, with a special highlight for carbon dioxide (CO2), which constitutes the majority of anthropogenic emissions. These abiotic alterations occur in all physical realms on the planet, with the oceans and the life they sustain being threatened by multiple fronts. Coined as “the deadly trio,” climate change is expressed via three main stressors in the marine realm: increasing surface temperature (ocean warming), decreasing mean pH (ocean acidification), and decreasing mean oxygen content (ocean deoxygenation). These abiotic stressors impact biological responses and traits in a varied number of ways, displaying interactive effects on marine biota. In this entry, we will shortly explain the physicochemical changes associated with these stressors while providing an overview of their hampering effects on marine biota at different levels of biological organization – from molecules to ecosystems. Moreover, we will discuss HOW these stressors may potentially interact under realistic scenarios and the consequent impacts on marine life in the ocean of tomorrow.

Climate Change Stressors

Ocean Warming

During the last 30 years, sea surface temperature (SST) has averagely increased 0.18 ± 0.16 °C per decade, despite differential spatial and seasonal rates of change. Conversely, the global ocean (above 75 m) has suffered an increase of about 0.11 ± 0.02 per decade (Lima and Wethey 2012). Global mean temperatures are expected to continuously rise throughout the twenty-first century (IPCC 2013). Anthropogenic-related CO2 and methane accumulates in the atmosphere, retaining the infrared radiation reflected from Earth’s surface and warming the atmosphere. Concomitant to the increased temperature verified in the atmosphere, ocean temperature is also increasing, particularly at the surface level. According to IPCC (2013), model projections encompassing most plausible scenarios (e.g., decrease in emissions, “business-as-usual,” and emissions increase) predict a further temperature increase averaging 1–3.5 °C for 2081–2100. Global warming is preeminently a feature of surface and lower atmosphere and is manifested more on land compared to water masses, by a factor of 1.4–1.7. Moreover, temperature change will not be uniform throughout global regions – global warming is projected to be stronger in Arctic latitudes, a phenomenon termed polar amplification. The less pronounced magnitude of this phenomenon in the South Pole appears to be linked to strong oceanic heat uptake and the persistence of the thick Antarctic ice sheet, as well as significantly higher deep ocean mixing, which allows for a better heat dispersion (Meehl et al. 2007). The phenomenon of global warming has received the most significant attention of climate change researchers (Fig. 1), with the largest number of studies trying to predict how marine organisms will cope with such warming trend.
Fig. 1

Publication trends of scientific studies (all fields of research) per decade, from 1950 to 2018, addressing ocean warming, ocean acidification, and hypoxia. Literature search was conducted via Web of Science and carried out with the three stressors (warming, acidification, and hypoxia) together with the words “ocean,” “sea,” “coastal,” or “marine.” (Data source: Web of Science, Clavirate Analytics)

At biological level, temperature expresses far-reaching effects across several levels of organization, from biochemical and molecular reaction dynamics to organism fitness, species distribution, and global biogeography (Angilletta 2009). The thermodynamic properties of biochemical kinetics and protein stability determine the thermal sensitivity of reactions (Kingsolver 2009). Consequently, according to basic metabolic theory, all organisms possess a survival thermal window, where increasing temperature increases reaction rates until an optimal level is reached, beyond which physiological stress (e.g., protein denaturation) is imposed and a steep decline is seen in metabolic and biochemical processes, such as growth, development, and feeding activity (Angilletta 2009; Mertens et al. 2015; Pörtner and Farrell 2008; Pörtner and Knust 2007; Rosa et al. 2012). Allied to this, organisms presenting higher optimal temperatures typically present a higher metabolic fitness, but that comes with the associated cost of a smaller thermal window, both for optimal and for basal levels (Kingsolver 2009). As such, predicted temperature increases will provoke larger negative fitness impacts on tropical than temperate species (particularly in ectotherms), since the first have already relatively small thermal margins and are generally living near their thermal maximum limits (Stillman 2003; Tewksbury et al. 2008).

Moreover, due to differential acclimation potential by autotrophic and heterotrophic metabolisms, the metabolic theory of ecology (MTE) predicts that less temperature-associated effects will be provoked on producers in comparison to consumer (O’Connor 2009). Thus, gradual increases in temperature will maximize consumer metabolism and strengthen top-down control on marine communities. However, in plant- and algae-dominated ecosystems, pronounced increases in temperature may result in an overdrive of consumer metabolism, leading to bottom-up dominated communities and increased primary producer biomass growth (Sampaio et al. 2017). Nevertheless, the width of organismal thermal range, optimal temperature, and temperature response varies across populations, which may lead to heterogenic effects on the same species depending on geography and other physicochemical properties (Stillman 2003). Regarding primary producers, for instance, in the temperate water of Australia, warming can lead to permanent shifts in kelp-dominated systems in favor of otherwise ephemeral algal mats and turfs (Wernberg et al. 2011). At the same time, in tropical waters, increases in temperature have been shown to elicit coral species to expel their symbiotic microalgae (zooxanthellae), a process known as bleaching (Kwiatkowski et al. 2015; Van Hooidonk et al. 2013). In the case that abiotic conditions do not return to favorable conditions in a specific time frame, these corals lose their nutrient source and perish, leaving huge inhabitable white “patches” across the ocean floor. Conversely, while warming has been shown to produce negative impacts on kelp and coral physiology and weaken their ecological fitness, this stressor increases algal turf productivity and spread, leading to a pronounced change on habitat-forming structures and potential for harboring species pertaining to higher trophic levels (Connell and Russell 2010).

Another important issue linked to temperature changes, with vast consequences on organism and ecosystem health, is the increase in frequency and magnitude of marine heat waves (IPCC 2013). These events have recently provoked pronounced negative effects on marine ecosystems across a disparity of areas such as the Southeastern, Northern, and Western Australia, the Northwest Atlantic, and the Northeast Pacific (Oliver et al. 2018). It is widely known that organisms are generally more impacted by rapid changes in abiotic conditions, than by gradual changes in mean conditions. Consequently, the sudden temperature increase coupled with extreme weather phenomenon, e.g., El Niño, led to sharp metabolic overdrive resulting in massive die-offs of fish, mollusks, crustaceans, corals, and even calcifying algae and seagrasses (Arias-Ortiz et al. 2018). Ecologically, beyond the mass mortalities of vertebrates and invertebrates, these events have caused marked losses on kelp forest, coral reef habitats, reduced primary productivity, species range limitations, phenological changes, communities’ restructuring, and rupture of fishing stocks and respective quotas (Arias-Ortiz et al. 2018; Oliver et al. 2018).

Ocean Acidification

The ocean uptakes a third of the atmospheric CO2 emissions, which causes profound changes in seawater carbonate chemistry. Specifically, the added CO2 leads to the formation of bicarbonate and hydrogen ions, leading to an acidification of pH values and the sequestration of biological calcium (IPCC 2013). Since the Industrial Revolution, the initial CO2 atmospheric concentrations of 280 ppm have amounted to over 400 ppm nowadays, with an associated drop in pH from approximately 8.2–8.1. Further increases are expected to happen, and CO2 concentrations of 760–900 ppm (high confidence from several predictive models) will lead to a concomitant drop of 0.3–0.4 in pH, by the end of this century (IPCC 2013). As for ocean warming, ocean acidification will exhibit large regional and temporal variability, something that will be particularly true for coastal waters, in comparison to the open ocean. Such differential expression is explained by distinct upwelling intensities along the coasts, deposition of nitrogen and sulfur, freshwater input from rivers, as well as organic matter and nutrient runoffs (IPCC 2013; Melzner et al. 2013).

Ocean acidification is considered a major global threat for marine organisms and ecosystems alike (Kroeker et al. 2010, 2012; Rosa et al. 2017; Seibel et al. 2014). Many marine organisms across the trophic web are sensitive to alterations of carbon and hydrogen ion availability, and the ability to cope or not with the forecasted changes can lead to severe ecological shifts in the way ecosystems are organized (Kroeker et al. 2012; Sampaio et al. 2017). The UN and the scientific community have thus made ocean acidification a priority area for research, and the number of experimental projects contemplating its effects on marine life has increased exponentially (Fig. 1). A clearer understanding of what underpins differential biological responses to ocean acidification will allow policy makers and stakeholders to better deal with this problem and build more accurate models of future impacts, both organism and ecosystem wise.

In general, studies so far have shown a pronounced negative impact on marine organisms (Frommel et al. 2011; Kroeker et al. 2010; Rosa et al. 2017; Rosa and Seibel 2008); however, the strength of this effect varies with the vulnerability inherent to different sensitivity of specific taxonomical groups and ontogenetic life stages (Kroeker et al. 2010; Pimentel et al. 2015; Rosa et al. 2013; Wittmann and Pörtner 2013). In detail, ocean acidification is mostly known for the negative effects prompted on calcifying organisms. The augmented quantity of hydrogen ions in seawater leads to a concomitant decrease in available carbonates ions and to a potential dissolution of biological calcium carbonate, from a certain threshold on. The calcium carbonate of echinoderms and mollusks is chemically unprotected from the surrounding environment and thus particularly endangered by this chemical equilibrium imbalance (Kroeker et al. 2010). With comparatively higher repercussions on the ecosystem, the calcification rates of corals, calcifying algae, and coccolithophores are also severely affected, inducing profound changes to habitat structures and food web basis, respectively (Beaugrand et al. 2013; Kroeker et al. 2012). Moreover, impairments on calcification indirectly affect other metabolic and physiological processes, such as growth and reproduction, and can ultimately lead to organism death, especially if coupled with other sources of physiological stress. Nevertheless, some taxa, e.g., crustaceans and fish (particularly the latter), possess advanced mechanisms of acid-base regulation, actively removing excessive ions from the bloodstream (Frommel et al. 2011; Heuer and Grosell 2014). Moreover, both these taxonomical groups possess a biogenic protection over the calcium carbonate structures which likely infers further defense against acidic environments (Kroeker et al. 2010). However, even these taxa have shown ocean acidification-related impairments, particularly at the metabolic and behavioral levels (Munday et al. 2014; Pimentel et al. 2015; Rosa et al. 2017; Rosa and Seibel 2008). Metabolic depression or compensatory upregulation, in response to environmental acidification, is reported for several invertebrates (and even vertebrates,) and is thought to be at least partly caused by decreased extracellular pH, modulated by the inhibition of proton transport across the membrane (Rosa and Seibel 2008; Wittmann and Pörtner 2013). Most likely due to energy reallocation, multiple studies have concurrently suggested linked between lower or altered metabolic rates and upregulation of enzymatic and nonenzymatic CO2-excretory machinery (Rosa et al. 2016; Sampaio et al. 2018; Wittmann and Pörtner 2013). Moreover, special behavioral impairments in fish and crustaceans have been shown to arise derived from excessive concentrations of H+/HCO3 ions in the GABAergic neurotransmitter system (Nilsson et al. 2012). By increasing the ionic load on the synaptic cleft, the equilibrium necessary for the passage of electrical currents through ionic Cl and HCO3 concentrations is disrupted, and correct functioning of olfactive reception cues is impaired, increasing vulnerability to predation and difficulty to locate food (Munday et al. 2014).

Moving to an ecosystem perspective, the end result at ecosystem levels depends on the role that affected species play in said ecosystem, as small changes to structural species physiology (e.g., corals or macroalgae) will be more visible than changes in consumer physiology, for instance (Fabricius et al. 2011; Hepburn et al. 2011; Kroeker et al. 2012). Thus, several nonlethal physiological effects registered and detailed until now may lead to pronounced changes in community assemblages and trophic interactions (Kroeker et al. 2012; Sampaio et al. 2017). One of the most worrying cases is the competition that tropical and subtropical coral reefs are suffering from algal turfs, worsened by climate changes (Connell and Russell 2010). Coral reefs shelter over a quarter of total marine biodiversity and provide several ecosystem services that are vital for human populations worldwide, such as coastal protection, fisheries, materials and biochemical composites used by industries, as well as ecotourism (Bell et al. 2013). Ocean acidification promotes the dissolution of calcified structures from hard corals, which will weaken its presence in the environment, thus providing a further competitive edge for algal turfs, which harbor significantly less biodiversity and provide a lower range of ecosystem services.

Ocean Deoxygenation

Since consistent time series data started being collected circa 1950, overall oxygen (O2) concentrations, both in the open ocean and in coastal areas worldwide, has been decreasing at alarming rates, reaching 7 μmol kg−1 per decade in the North Pacific’s mid-water depths (Keeling et al. 2010). The mean oceanic O2 content is presently 162 μmol kg−1 (or roughly 5.05 mg L−1), but dissolved oxygen concentration, as for temperature and ocean pH, displays high regional and temporal variation (Breitburg et al. 2018; IPCC 2013). At around 500 m of depth, naturally occurring oxygen minimum zones (OMZs) exist in the Atlantic, Indian, and Pacific oceans, close to the tropics, where oxygen regularly reach below 60 μmol kg−1 (i.e., hypoxia), resulting from poor water renewal and the input of anoxic water (Levin and Bris 2015). However, given anthropogenic pressures, total OMZs area is nowadays expanding, both horizontally and vertically, for thousands of miles more compared to what was registered in the middle of the twentieth century (Levin and Breitburg 2015). This rate of deoxygenation is faster in coastal areas than in the open ocean, and the number of coastal “dead zones” has increased over tenfold since the 1950s (Breitburg et al. 2018).

Ocean deoxygenation (OD) is caused by diverse chemical and biological processes, which have been exacerbated in recent years. Increasing temperatures are accelerating the spread of hypoxic zones worldwide, by accentuating established depth thermoclines and reducing the vertical mixing of water masses (Breitburg et al. 2018; Diaz and Rosenberg 2008). Water stratification is even more strengthened by salinity differences prompted by freshwater inputs, relating to the melting of polar ice caps and increased precipitation. Concomitantly, other sources of coastal hypoxia are sewage discharges and general runoffs from estuaries where anthropogenic pressure is high (Keeling et al. 2010). The excessive input of nutrients leads to an exacerbation of eutrophication phenomena, and as the superficial layer of water is covered by green algae, the subjacent marine fauna and flora die off, leading to organic matter decomposition, formation of nitrous oxide, and intensive microbial respiration, which depletes coastal waters of O2 (Diaz and Rosenberg 2008). Not only that, the strengthening of wind-driven upwelling leads to the dispersion of these eutrophic waters into the open ocean. There, the sinking of senescent algae and phytoplankton (also known as “marine snow”) increases organic matter decomposition over the water column and the ocean bottom. The seawater masses at these different depths are subsequently driven to coastal areas by the upwelling related outward movement of surface water masses, closing a continuous self-feeding cycle.

Although OD and hypoxia impacts have been somehow neglected by the scientific community in the past decades (Fig. 1), it is known that most life in the oceans is based on aerobic metabolism to catabolize biochemical compounds and produce energy, being thus highly dependent of O2. Under low O2 conditions, despite the existence of several hypoxia-tolerant species among metazoan meiofauna, its diversity is extremely reduced, while the selected few species that are usually less motile, i.e., have minor metabolic requirements, such as nematodes, start dominating benthic communities in abundance (Levin et al. 2009). Given their inherently higher motility, phenotypic responses to hypoxia by macro- and megafauna usually start to be detected at the behavioral level (Breitburg et al. 2018). To increase their body surface and O2 sequestration, amphipods and polychaetes usually extend tubes or their bodies into the surrounding environment by shallowing, completely emerging from the sediment and forming stacks of individuals to move up in the water column (Levin et al. 2009). Continued exposition to hypoxic conditions leads to more pronounced physiological changes, particularly on body size and morphology. Under this scenario, reduced body sizes are particularly favored due to its higher ratio of surface area to body volume, as well as fast life cycles and mass spawning, such as polychaetes which are characterized by prolific respiratory morphological structures. Despite that meiofaunal organisms typically display high population turnover rates, the velocity and range of recolonization of sediments can vary greatly, and continuation of hypoxic events may hinder severely this recovery. Pelagic fish and invertebrates are also affected by these changes on the distribution and content of O2 concentrations, particularly the ones with higher oxygen physiological demand, such as tunas and sharks (Prince et al. 2010; Prince and Goodyear 2006; Queiroz et al. 2016; Stramma et al. 2012). By diminishing suitable O2 conditions, the habitat of these macropredators horizontally and vertically is compressed, which prompts shifts on their distribution, migratory potential (for diel movements), and routes, as well as in reallocation of their prey’s distribution, which may lead to closer proximities or a decoupling of predator and prey frequented areas, as well as increasing fishing vulnerability (Rosa and Seibel 2008; Stramma et al. 2012). Conversely, pelagic cephalopods, such as the colossal squid (Dosidicus gigas), have the capacity to suppress their metabolism to extreme thresholds, allowing for the use of these habitats to escape predators, and also to hunt on OMZ-adapted taxa (Prince et al. 2010; Rosa and Seibel 2008).

Physiological changes driven by oxygen limitation will lead to fragmentation of existing communities, with the possibility of reassembling other communities with similar features (with different participants), which will always change the patterns of competition and interaction strength between trophic levels. At ecosystem level, and as referred before, hypoxic events usually have catastrophic outcomes across the world (Breitburg et al. 2018; Chan et al. 2008; Diaz and Rosenberg 2008). For instance, in temperate marine habitats that should supposedly already be accustomed to hypoxic conditions, the rise of anoxic waters in the Northwestern coast of America caused near-complete die-offs in the totality of trophic web (Grantham et al. 2004). Similar occurrences are known to happen in other coastal areas beneath OMZs which are getting further depleted from O2. Also recently, Altieri et al. (2017) compiled 20 occasions where hypoxia was directly linked to massive mortalities of fish, mollusks, and corals in tropical waters, adding to the fact that, given the isolation of certain locations (e.g., some Pacific Islands) and rudimentary technology for monitoring, hypoxia events in these world regions are likely very underreported, perhaps by an order of magnitude.

Interactive Scenarios and Consequent Impacts on Marine Biota

Despite the scientific community’s (by now well-grounded) understanding of the responses of marine biota to isolated climate change-related stressor scenarios, in the future ocean, all three stressors will interactively affect (e.g., additively, synergistically, or even antagonistically) marine life. The fact that most experiments have been performed using single stressor or single species scenarios hampers our ability to predict the responses of marine communities and ecosystems and sometimes even that of single organisms. Thus, a more integrative and holistic framework is warranted for climate change experimentation and modeling, to accurately portray the biological responses of the marine biota to the future conditions (Fig. 2). Attesting to this, current literature shows that the interactive effects provoked by climate stressors and respective physiological response from organisms and communities are many times nonlinear, depending highly on the degree of increase and consistency of each stressor, genetic potential, and phenotypical plasticity of individuals, among other factors (e.g., Riebesell and Gattuso 2015).
Fig. 2

Framework for future climate change-related experimental and modeling studies. (Adapted from Nature Publishing Group©, Riebesell, U., Gattuso, J.-P., 2015. Lessons learned from ocean acidification research. Nat. Clim. Chang. 5, 12–14.  https://doi.org/10.1038/nclimate2456))

Starting with the most studied interaction, and taking the examples used above involving corals (predominantly from tropical areas), both ocean warming (through pushing thermal thresholds) and acidification (through biogenic calcium sequestration and ionic deregulation) will interactively affect marine species’ physiology (Kwiatkowski et al. 2015). However, negative or counteracting effects are many times species dependent. In specific coral species, warming (prior to bleaching levels) has been shown to counteract acidification-prompted negative effects (such as decalcification and energy expenditure), by increasing the productivity of the algal symbiont and providing the coral with more energy to regulate carbonate chemistry through acid-base balance, at the sites of calcification (Anthony et al. 2011). However, the general predicted scenario is that the degree to which temperature is increasing (especially through more and more frequent marine heat waves) will indeed lead to bleaching, which will be further worsened by acidification-related energy consumption and decalcification of corals (Anthony et al. 2011). Such is in line with what is being recorded in the present day, wherein two recent mass bleaching occurrences on 2016 and 2017, across the northern area of the Great Barrier Reef, 90% of the corals bleached, and were unable to recover, following extreme weather events (Hughes et al. 2018).

The difficulty in predicting mixed effects of warming and acidification is not exclusive to specific coral species. Other literature has shown that basal activity and metabolic rates are lowered in fish and invertebrates in response to acidification, to allow allocation of energy expenditure to acid-base regulation (Gobler and Baumann 2016; Kroeker et al. 2010; Pimentel et al. 2015; Rosa and Seibel 2008). However, when temperature is added into the equation, metabolic levels can be returned to normal and sometimes raised over what was reported under normal circumstances (Kroeker et al. 2013; Sampaio et al. 2018). Even isolated stressor-elicited physiological responses to oxidative stress have been shown to be normalized under combined stressor presence, in some fish and crustacean species (Pimentel et al. 2015; Sampaio et al. 2018). Nevertheless, such is possible due to a prioritization of underlying basic cellular functions and repairing mechanisms, in detriment of non-vital functions (e.g., reproduction), which may cause further negative impacts on organism and population-wise further down the time line (Kroeker et al. 2013). Thus, responses to combined ocean warming and acidification seem to predominantly depend on species and sometimes individual-specific capacity for physiological trade-offs and the ability of organisms to maintain a significant energy allocation to all functions (vital and non-vital), which determine physiological (i.e., individual) and ecological (i.e., population) fitness (Lopes et al. 2018; Pimentel et al. 2015; Repolho et al. 2017; Rosa et al. 2013, 2017; Sampaio et al. 2016, 2017, 2018)

Ecosystem wise, while in the tropics, these combined stressors generally provoke negative effects; responses in temperate or algae-dominated habitats are potentially self-counteracting (Connell and Russell 2010; Goldenberg et al. 2018). Non-calcifying primary producers can use CO2 as a nutrient which increases resources for the upper trophic levels. Thus, in these cases, warming-related increases in grazer metabolism are equilibrated by increases in algal biomass, which serves as support for predators, such as fish, to maintain healthy populational status. Conversely, predator-prey interactions and overall top-down pressure are strengthened by warming, which is met by higher resource availability prompted by acidification. However, it is important to highlight that several meta-analytical studies conducted, compiling a substantial amount of the available literature, have shown general negative (albeit differential) effects on both organism and ecosystem levels from the combined exposure to both warming and acidification (Kroeker et al. 2010, 2013). Moreover, the referred maintenance of trophic interactions will be supported by CO2- and thermal-resilient species which will come with an associated cost to species and possibly functional diversity, since important calcifying species, such as mollusks and echinoderms, will still suffer grave consequences (Gobler and Baumann 2016; Levin and Breitburg 2015). Biodiversity loss is an issue that the general population, particularly managers and stakeholders, are able to comprehend the inherent consequences than of the physiological responses of biota, which may allow for a more “readable” assessment of climate change impacts on socioeconomic context, focusing on ecosystem goods and services.

In complete contrast to what is observed for ocean warming and acidification, interactions with ocean deoxygenation appear to present a dreadful linear trend of additive or even synergistic negative effects on marine biota. Not only that, the physicochemical underpinnings prompting each stressor are themselves synergistic and will, in all likelihood, further stimulate the impacts registered for isolated stressors (Breitburg et al. 2018; Levin and Breitburg 2015). Increasing temperature reduces O2 solubility, increases water stratification (lowering mixing rates), and increases animal respiration and O2 consumption, among other effects which reduce mean oceanic O2 content. Accordingly, albeit taxonomical-specific differences must be considered; low O2 conditions and warming synergistically increase the vulnerability of marine biota, by impacting virtually all biological responses, including survival, metabolism, abundance, and reproductive outputs. The higher metabolic cost demanded by increasing temperature lowers oxygen threshold concentrations for marine fauna (Rosa et al. 2013), which taxonomically decrease from fishes to crustaceans, and mollusks, with meiofauna following, i.e., polychaetes, echinoderms, and cnidarians (Vaquer-Sunyer and Duarte 2008, 2011). The extent of these impacts will also depend on species-specific physiological strategies, life stages, and motility, as well as populational adaptations to the gradual abiotic changes (Vaquer-Sunyer and Duarte 2008). Nevertheless, it is consensual that these interactive effects will reduce both the quality and the range of suitable habitats for aerobic organisms to live, leading to constrictions on both organism development, population health status, and marine biodiversity.

Concomitantly, hypoxic and acidified areas are linked by the process of heterotrophic and autotrophic respiration, given the removal of O2 and adding CO2 to the surrounding environment (IPCC 2013; Levin and Bris 2015). Thus, it is not uncommon to have daily occurrences of this interaction on, e.g., eutrophic ecosystems, where nutrient inputs drive communities to grow and respirate more on nocturnal hours. Accordingly, OMZs are also low pH locations, and their shoaling is tightly associated with additional acidity, which can create corrosive conditions during upwelling events on coastal ecosystems (Levin et al. 2009). Furthermore, this increase in CO2 can decrease the oxygen affinity of respiratory proteins, while the required increased metabolic costs for maintaining acid-base balance are further worsened by lower capacity in meeting aerobic demands, stemming from lower O2 concentrations (Pörtner and Knust 2007). Despite the paucity of studies analyzing the interaction between ocean deoxygenation and acidification, the first is confirmed as the strongest detrimental impactor, being additively, or in some cases synergistically, worsened by the co-occurrence of the latter (Gobler and Baumann 2016). These effects are most prominent in early ontogenetic life stages and are logically dependent of the current conditions the organisms face nowadays, e.g., despite still exhibiting negative effects, mollusks with a strong anaerobic capacity residing in areas of diurnal acidification/hypoxia are more resilient compared to organisms from low productivity/oxygenated areas (Breitburg et al. 2018; Vaquer-Sunyer and Duarte 2008). Also, echinoderms and other calcifying taxa struggle to cope with hypoxic conditions, which has been linked to the increased energetic demand for acid-base balancing provoked by an acidified environment (Breitburg et al. 2018). Although it is still early to accurately predict the impacts of this interaction on communities and ecosystems, all evidence hints to a strong decline in several traits, which will have profound implications for fisheries and other ecosystem services, particularly in industrialized coastal ecosystems.

“The Deadly Trio” Scenario

As made clear by the previous sections, ocean deoxygenation is connected to both warming and acidification, and this triple interaction will shape much of ecosystems’ fitness in the future years to come (IPCC 2013) (Fig. 3). Given the virtual nonexistence of experimental evidence for this multi-stressor scenario (albeit the most realistic one), current bioenergetic frameworks can be useful in helping determine organism fitness in future oceans. Beyond the already weighted physicochemical and biological synergetic mechanistics, while temperature increases metabolic demands, deoxygenation cuts off O2 supply and lowers metabolic potential (Breitburg et al. 2018; Pörtner and Knust 2007; Vaquer-Sunyer and Duarte 2011). Simultaneously, lower pH can require further energetic costs on ventilation and acid-base balance and activation of antioxidant and protein repair mechanisms, which will require energy reallocation from an increased basal metabolism (Gobler and Baumann 2016; Levin and Bris 2015). Parallelly, both lower O2 and pH are expected to reduce organism thermal windows, by pressing on their respective physiological thresholds (Kroeker et al. 2013; Vaquer-Sunyer and Duarte 2011). These physiological constraints cascade into ecological pitfalls, with ecosystem and community level changes predicted to be drastic, given massive mortalities (at all trophic levels), registered on several naturally occurring phenomena, such as prolonged exposure to eutrophic conditions and upwelling of hypoxic/acidic seawater masses (Breitburg et al. 2018; Chan et al. 2008; Keeling et al. 2010). Even the few antagonistic effects between ocean warming and ocean acidification contributing to organism and community resilience will likely be unbalanced toward negative impacts, when coupled with ocean deoxygenation (Altieri et al. 2017; Breitburg et al. 2018).
Fig. 3

Underlying links, impacts, and consequences of the “deadly trio”

Thus, overall organisms, populations, communities, and entire ecosystems are predicted to have their physiological and ecological potential reduced across multiple abiotic (and consequently biotic) dimensions and traits, which will lead to pronounced impacts on both non-vital and vital functions, severely compromising organism, population, community, and ecosystem viability. It is important to retain that these alterations are ongoing and that field data already reveals significant alterations in community dynamics and species distribution (Breitburg et al. 2018; Queirós et al. 2015; Queiroz et al. 2016; Stramma et al. 2012). Ocean deoxygenation, warming, and acidification alter biogeochemical cycles, climate-regulating processes, heat distribution, wind regimes, and ecosystem services for the human population (Breitburg et al. 2018; IPCC 2013; Kroeker et al. 2012). Beyond the negative biological impacts on marine biota described along this entry, one should keep in mind the sharp repercussions at socioeconomic levels. Climate change will also imply severe losses of ecosystem’s goods and services, leading to strainings in human activities and even diplomatic relations between countries (Breitburg et al. 2018; Frazão-Santos et al. 2016). Ocean management should rely on holistic frameworks combining modeling, observations, and experiments under multi-stressor environments to raise awareness within stakeholders and governments. This should ideally lead to halting or slowing the currently in effect rates of climate change-related gas emissions, in the hopes of thwarting a somber future for both marine life and human populations.

Cross-References

Notes

Acknowledgments

The authors, and the work for producing this entry, were funded by PTDC/BIA-BMA/28317/2017, PTDC/AAG-GLO/1926/2014, and MAR-01.04.02-FEAMP-0007.

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Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.MARE – Marine Environmental Sciences Centre & Laboratório Marítimo da Guia, Faculdade de CiênciasUniversidade de LisboaCascaisPortugal

Section editors and affiliations

  • Ulisses Azeiteiro
    • 1
  1. 1.University of AveiroAveiroPortugal