Brad A. Seibel

Synergistic effects of climate-related variables suggest future physiological impairment in a top oceanic predator

By the end of this century, anthropogenic carbon dioxide (CO2) emissions are expected to decrease the surface ocean pH by as much as 0.3 unit. At the same time, the ocean is expected to warm with an associated expansion of the oxygen minimum layer (OML). Thus, there is a growing demand to understand the response of the marine biota to these global changes. We show that ocean acidification will substantially depress metabolic rates (31%) and activity levels (45%) in the jumbo squid, Dosidicus gigas, a top predator in the Eastern Pacific. This effect is exacerbated by high temperature. Reduced aerobic and locomotory scope in warm, high-CO2 surface waters will presumably impair predator–prey interactions with cascading consequences for growth, reproduction, and survival. Moreover, as the OML shoals, squids will have to retreat to these shallower, less hospitable, waters at night to feed and repay any oxygen debt that accumulates during their diel vertical migration into the OML. Thus, we demonstrate that, in the absence of adaptation or horizontal migration, the synergism between ocean acidification, global warming, and expanding hypoxia will compress the habitable depth range of the species. These interactions may ultimately define the long-term fate of this commercially and ecologically important predator.

The rate of metabolism in marine animals: environmental constraints, ecological demands and energetic opportunities

The rates of metabolism in animals vary tremendously throughout the biosphere. The origins of this variation are a matter of active debate with some scientists highlighting the importance of anatomical or environmental constraints, while others emphasize the diversity of ecological roles that organisms play and the associated energy demands. Here, we analyse metabolic rates in diverse marine taxa, with special emphasis on patterns of metabolic rate across a depth gradient, in an effort to understand the extent and underlying causes of variation. The conclusion from this analysis is that low rates of metabolism, in the deep sea and elsewhere, do not result from resource (e.g. food or oxygen) limitation or from temperature or pressure constraint. While metabolic rates do decline strongly with depth in several important animal groups, for others metabolism in abyssal species proceeds as fast as in ecologically similar shallow-water species at equivalent temperatures. Rather, high metabolic demand follows strong selection for locomotory capacity among visual predators inhabiting well-lit oceanic waters. Relaxation of this selection where visual predation is limited provides an opportunity for reduced energy expenditure. Large-scale metabolic variation in the ocean results from interspecific differences in ecological energy demand.

Critical oxygen levels and metabolic suppression in oceanic oxygen minimum zones.

Summary The survival of oceanic organisms in oxygen minimum zones (OMZs) depends on their total oxygen demand and the capacities for oxygen extraction and transport, anaerobic ATP production and metabolic suppression. Anaerobic metabolism and metabolic suppression are required for daytime forays into the most extreme OMZs. Critical oxygen partial pressures are, within a range, evolved to match the minimum oxygen level to which a species is exposed. This fact demands that low oxygen habitats be defined by the biological response to low oxygen rather than by some arbitrary oxygen concentration. A broad comparative analysis of oxygen tolerance facilitates the identification of two oxygen thresholds that may prove useful for policy makers as OMZs expand due to climate change. Between these thresholds, specific physiological adaptations to low oxygen are required of virtually all species. The lower threshold represents a limit to evolved oxygen extraction capacity. Climate change that pushes oxygen concentrations below the lower threshold (∼0.8 kPa) will certainly result in a transition from an ecosystem dominated by a diverse midwater fauna to one dominated by diel migrant biota that must return to surface waters at night. Animal physiology and, in particular, the response of animals to expanding hypoxia, is a critical, but understudied, component of biogeochemical cycles and oceanic ecology. Here, I discuss the definition of hypoxia and critical oxygen levels, review adaptations of animals to OMZs and discuss the capacity for, and prevalence of, metabolic suppression as a response to temporary residence in OMZs and the possible consequences of climate change on OMZ ecology.

Climate change tightens a metabolic constraint on marine habitats

Double trouble It is well known that climate change will warm ocean waters, but dissolved oxygen levels also decrease as water warms. Deutsch et al. combined data on metabolism, temperature, and demographics to determine the impact of marine deoxygenation on a variety of fish and crustacean species (see the Perspective by Kleypas). Predicted climate and oxygen conditions can be expected to contract the distribution of marine fish poleward, as equatorward waters become too low in oxygen to support their energy needs. Furthermore, even the more-poleward waters will have reduced oxygen levels. Science, this issue p. 1132; see also p. 1086 Warming waters and reduced O2 will contract fish distributions poleward. [Also see Perspective by Kleypas] Warming of the oceans and consequent loss of dissolved oxygen (O2) will alter marine ecosystems, but a mechanistic framework to predict the impact of multiple stressors on viable habitat is lacking. Here, we integrate physiological, climatic, and biogeographic data to calibrate and then map a key metabolic index—the ratio of O2 supply to resting metabolic O2 demand—across geographic ranges of several marine ectotherms. These species differ in thermal and hypoxic tolerances, but their contemporary distributions are all bounded at the equatorward edge by a minimum metabolic index of ~2 to 5, indicative of a critical energetic requirement for organismal activity. The combined effects of warming and O2 loss this century are projected to reduce the upper ocean’s metabolic index by ~20% globally and by ~50% in northern high-latitude regions, forcing poleward and vertical contraction of metabolically viable habitats and species ranges.

Biological impacts of deep-sea carbon dioxide injection inferred from indices of physiological performance.

SUMMARY A recent proposal to store anthropogenic carbon dioxide in the deep ocean is assessed here with regard to the impacts on deep-living fauna. The stability of the deep-sea has allowed the evolution of species ill-equipped to withstand rapid environmental changes. Low metabolic rates of most deep-sea species are correlated with low capacities for pH buffering and low concentrations of ion-transport proteins. Changes in seawater carbon dioxide partial pressure (PCO2) may thus lead to large cellular PCO2 and pH changes. Oxygen transport proteins of deep-sea animals are also highly sensitive to changes in pH. Acidosis leads to metabolic suppression, reduced protein synthesis, respiratory stress, reduced metabolic scope and, ultimately, death. Deep-sea CO2 injection as a means of controlling atmospheric CO2 levels should be assessed with careful consideration of potential biological impacts. In order to properly evaluate the risks within a relevant timeframe, a much more aggressive approach to research is warranted.

Decline in Pelagic Cephalopod Metabolism With Habitat Depth Reflects Differences in Locomotory Efficiency

The metabolic rates of 33 species of pelagic cephalopods from California and Hawaii were measured and correlated with minimum depth of occurrence. Mean metabolic rates ranged from 0.07 {mu}mol O2g-1 h-1 for the deep-living vampire squid, Vampyroteuthis infernalis, to 8.79 {mu}mol O2 g-1 h-1 for Gonatus onyx, a vertically migrating squid. An individual of V. infernalis, which lives within the oxygen minimum layer off California, had the lowest mass-specific metabolic rate ever measured for a cephalopod (0.02 {mu}mol O2g-1 h-1, 1050 g wet weight). For species collected in sufficient quantity and size range, metabolism was related to body size. Critical partial pressures of oxygen (Pc) were determined for Hawaiian and Californian cephalopods. Pc values for Hawaiian animals were considerably higher than for those taken off California, a trend that corresponds to the higher levels of environmental oxygen in the Hawaiian waters. Buffering capacity ({beta}) of mantle muscle, assayed in eight cephalopod species, was used to estimate the capacity for glycolytic energy production. Mean {beta} ranged from 1.43 slykes for a bathypelagic octopod, Japetella heathi, to 77.08 slykes for an epipelagic squid. Sthenoteuthis oualaniensis. Significant declines with increasing depth of occurrence were observed for both metabolism and {beta}. The decline in metabolic parameters with depth is interpreted as a decreased reliance on locomotory abilities for predator/prey interactions in the light-limited deep sea. The decline in metabolism with depth observed for pelagic cephalopods was significantly steeper than that previously observed for either pelagic fishes or crustaceans. We suggest that since strong locomotory abilities are not a priority in the deep sea, deeper-living cephalopods may rely more heavily on means of locomotion that are more efficient than jet propulsion via mantle contractions--means such as fin swimming or medusoid swimming utilizing the arms and extensive webbing present in many deep-living species. The greater efficiency of deeper-living cephalopods may be responsible for the observation that the decline in metabolic rates with depth is more pronounced for pelagic cephalopods than for fishes or crustaceans.

On the depth and scale of metabolic rate variation: scaling of oxygen consumption rates and enzymatic activity in the Class Cephalopoda (Mollusca)

SUMMARY Recent ecological theory depends, for predictive power, on the apparent similarity of metabolic rates within broad taxonomic or functional groups of organisms (e.g. invertebrates or ectotherms). Such metabolic commonality is challenged here, as I demonstrate more than 200-fold variation in metabolic rates independent of body mass and temperature in a single class of animals, the Cephalopoda, over seven orders of magnitude size range. I further demonstrate wide variation in the slopes of metabolic scaling curves. The observed variation in metabolism reflects differential selection among species for locomotory capacity rather than mass or temperature constraints. Such selection is highest among epipelagic squids (Lolignidae and Ommastrephidae) that, as adults, have temperature-corrected metabolic rates higher than mammals of similar size.

Natural egg mass deposition by the Humboldt squid ( Dosidicus gigas ) in the Gulf of California and characteristics of hatchlings and paralarvae

The jumbo or Humboldt squid, Dosidicus gigas, is an important fisheries resource and a significant participant in regional ecologies as both predator and prey. It is the largest species in the oceanic squid family Ommastrephidae and has the largest known potential fecundity of any cephalopod, yet little is understood about its reproductive biology. We report the first discovery of a naturally deposited egg mass of Dosidicus gigas, as well as the first spawning of eggs in captivity. The egg mass was found in warm water (25‐278C) at a depth of 16 m and was far larger than the egg masses of any squid species previously reported. Eggs were embedded in a watery, gelatinous matrix and were individually surrounded by a unique envelope external to the chorion. This envelope was present in both wild and captive-spawned egg masses, but it was not present in artificially fertilized eggs. The wild egg mass appeared to be resistant to microbial infection, unlike the incomplete and damaged egg masses spawned in captivity, suggesting that the intact egg mass protects the eggs within. Chorion expansion was also more extensive in the wild egg mass. Hatchling behaviours included proboscis extension, chromatophore activity, and a range of swimming speeds that may allow them to exercise some control over their distribution in the wild.

Cascading Trophic Impacts of Reduced Biomass in the Ross Sea, Antarctica: Just the Tip of the Iceberg?

BRAD A. SEIBEL* AND HEIDI M. DIERSSEN†Monterey Bay Aquarium Research Institute, Moss Landing, California 95039A significant reduction in phytoplankton biomass in theRoss Sea was reported in the austral summer of 2000–2001,a possible consequence of a disruption in sea-ice retreatdue to the presence of an immense iceberg, B15 (1) (Fig. 1).Our observations in McMurdo Sound suggest temporallyand trophically cascading impacts of that depression inproductivity. Reduced phytoplankton stocks clearly affectedthe pteropod Limacina helicina (Phipps, 1774) (Gastro-poda: Mollusca), an abundant primary consumer in theregion (2, 3), as indicated by depressed metabolic rates in2000–2001. The following season, for the first time onrecord, L. helicina was absent from McMurdo Sound. Manyimportant predators, including whales and fishes, relyheavily on L. helicina for food (3, 4). However, most obvi-ously impacted by its absence was Clione antarctica (Smith,1902), an abundant pteropod mollusc (Gastropoda) thatfeeds exclusively on L. helicina (5). Metabolic rates of C.antarctica were depressed by 50% in 2001–2002. BothL.helicina and C. antarctica are important components ofpolar ecosystems and may be good indicators of overallecosystem “health” in McMurdo Sound and perhaps in theRoss Sea. In this last austral summer, 2002–2003, sea-iceextent was much higher and phytoplankton stocks weredramatically lower than any reported previously, effectspossibly associated with El Nin˜o conditions, and we hypoth-esize that pteropods and their consumers may be furtherimpacted.In the Southern Ocean, phytoplankton production islinked strongly to the seasonal oscillations in the extent ofthe sea ice (6, 7) and survival of higher trophic levels isdependent on reproductive cycles that are synchronous withphytoplankton blooms. This is especially true of the directfood link between L. helicina and C. antarctica. L. helicinalives and feeds in the water column by extending a web ofmucus that traps phytoplankton and, to a lesser extent, smallzooplankton (3). L. helicina is the exclusive food source ofC. antarctica throughout the life cycle, and the two specieshave parallel life histories. They grow in concert, with thepreferred prey size increasing with predator size (3). Suchspecificity within the context of a highly seasonal environ-ment requires precise timing to ensure that predator andprey coexist. The coevolved predator-prey relationship be-tween L. helicina and C. antarctica provides a uniqueopportunity to study the ecological and trophic conse-quences of a depression in primary productivity in the RossSea.A 50% to 75% reduction in phytoplankton biomass, es-timated as chlorophyll a (Chl) concentrations, and highsea-ice cover was observed in December 2000–2001 rela-tive to previous years (Table 1; Fig. 2; 8). A limited bloomdid form by February, but annual primary production wasstill only 60% of the previous year (1). We believe that thereduced phytoplankton stocks in 2000–2001 had pro-nounced impacts on the condition of primary consumers inthe region, causing cascading effects through higher trophiclevels in the following year. This assertion is supported hereby a series of metabolic measurements made on L. helicinaand C. antarctica between 1999 and 2002.Nutritional state is known to be among the primary de-terminants of metabolism in all organisms, including ptero-pods (3), and is especially important in the highly seasonalAntarctic environment (9, 10). Food availability will influ-ence, among other things, the rates of protein synthesis,oxygen consumption, growth, and reproduction (9–11). Wecollected L. helicina and C. antarctica at four samplingstations along Ross Island (Fig. 1) and measured the oxygen

Energetic plasticity underlies a variable response to ocean acidification in the pteropod, Limacina helicina antarctica.

Ocean acidification, caused by elevated seawater carbon dioxide levels, may have a deleterious impact on energetic processes in animals. Here we show that high PCO2 can suppress metabolism, measured as oxygen consumption, in the pteropod, L. helicina forma antarctica, by ∼20%. The rates measured at 180–380 µatm (MO2  = 1.25 M−0.25, p = 0.007) were significantly higher (ANCOVA, p  =  0.004) than those measured at elevated target CO2 levels in 2007 (789–1000 µatm,  =  0.78 M−0.32, p  =  0.0008; Fig. 1). However, we further demonstrate metabolic plasticity in response to regional phytoplankton concentration and that the response to CO2 is dependent on the baseline level of metabolism. We hypothesize that reduced regional Chl a levels in 2008 suppressed metabolism and masked the effect of ocean acidification. This effect of food limitation was not, we postulate, merely a result of gut clearance and specific dynamic action, but rather represents a sustained metabolic response to regional conditions. Thus, pteropod populations may be compromised by climate change, both directly via CO2-induced metabolic suppression, and indirectly via quantitative and qualitative changes to the phytoplankton community. Without the context provided by long-term observations (four seasons) and a multi-faceted laboratory analysis of the parameters affecting energetics, the complex response of polar pteropods to ocean acidification may be masked or misinterpreted.