Thermal optima in the hypoxia tolerance of marine ectotherms: Physiological causes and biogeographic consequences.

The minimum O2 needed to fuel the demand of aquatic animals is commonly observed to increase with temperature, driven by accelerating metabolism. However, recent measurements of critical O2 thresholds ("Pcrit") reveal more complex patterns, including those with a minimum at an intermediate thermal "optimum". To discern the prevalence, physiological drivers, and biogeographic manifestations of such curves, we analyze new experimental and biogeographic data using a general dynamic model of aquatic water breathers. The model simulates the transfer of oxygen from ambient water through a boundary layer and into animal tissues driven by temperature-dependent rates of metabolism, diffusive gas exchange, and ventilatory and circulatory systems with O2-protein binding. We find that a thermal optimum in Pcrit can arise even when all physiological rates increase steadily with temperature. This occurs when O2 supply at low temperatures is limited by a process that is more temperature sensitive than metabolism, but becomes limited by a less sensitive process at warmer temperatures. Analysis of published species respiratory traits suggests that this scenario is not uncommon in marine biota, with ventilation and circulation limiting supply under cold conditions and diffusion limiting supply at high temperatures. Using occurrence data, we show that species with these physiological traits inhabit lowest O2 waters near the optimal temperature for hypoxia tolerance and are restricted to higher O2 at temperatures above and below this optimum. Our results imply that hypoxia tolerance can decline under both cold and warm conditions and thus may influence both poleward and equatorward species range limits.

Metabolic trait diversity shapes marine biogeography.

Climate and physiology shape biogeography, yet the range limits of species can rarely be ascribed to the quantitative traits of organisms1-3. Here we evaluate whether the geographical range boundaries of species coincide with ecophysiological limits to acquisition of aerobic energy4 for a global cross-section of the biodiversity of marine animals. We observe a tight correlation between the metabolic rate and the efficacy of oxygen supply, and between the temperature sensitivities of these traits, which suggests that marine animals are under strong selection for the tolerance of low O2 (hypoxia)5. The breadth of the resulting physiological tolerances of marine animals predicts a variety of geographical niches-from the tropics to high latitudes and from shallow to deep water-which better align with species distributions than do models based on either temperature or oxygen alone. For all studied species, thermal and hypoxic limits are substantially reduced by the energetic demands of ecological activity, a trait that varies similarly among marine and terrestrial taxa. Active temperature-dependent hypoxia thus links the biogeography of diverse marine species to fundamental energetic requirements that are shared across the animal kingdom.

Impact of warming on aquatic body sizes explained by metabolic scaling from microbes to macrofauna.

Rising temperatures are associated with reduced body size in many marine species, but the biological cause and generality of the phenomenon is debated. We derive a predictive model for body size responses to temperature and oxygen (O2) changes based on thermal and geometric constraints on organismal O2 supply and demand across the size spectrum. The model reproduces three key aspects of the observed patterns of intergenerational size reductions measured in laboratory warming experiments of diverse aquatic ectotherms (i.e., the "temperature-size rule" [TSR]). First, the interspecific mean and variability of the TSR is predicted from species' temperature sensitivities of hypoxia tolerance, whose nonlinearity with temperature also explains the second TSR pattern-its amplification as temperatures rise. Third, as body size increases across the tree of life, the impact of growth on O2 demand declines while its benefit to O2 supply rises, decreasing the size dependence of hypoxia tolerance and requiring larger animals to contract by a larger fraction to compensate for a thermally driven rise in metabolism. Together our results support O2 limitation as the mechanism underlying the TSR, and they provide a physiological basis for projecting ectotherm body size responses to climate change from microbes to macrofauna. For small species unable to rapidly migrate or evolve greater hypoxia tolerance, ocean warming and O2 loss in this century are projected to induce >20% reductions in body mass. Size reductions at higher trophic levels could be even stronger and more variable, compounding the direct impact of human harvesting on size-structured ocean food webs.

The origin of carbonate mud and implications for global climate.

Carbonate mud represents one of the most important geochemical archives for reconstructing ancient climatic, environmental, and evolutionary change from the rock record. Mud also represents a major sink in the global carbon cycle. Yet, there remains no consensus about how and where carbonate mud is formed. Here, we present stable isotope and trace-element data from carbonate constituents in the Bahamas, including ooids, corals, foraminifera, and algae. We use geochemical fingerprinting to demonstrate that carbonate mud cannot be sourced from the abrasion and mixture of any combination of these macroscopic grains. Instead, an inverse Bayesian mixing model requires the presence of an additional aragonite source. We posit that this source represents a direct seawater precipitate. We use geological and geochemical data to show that "whitings" are unlikely to be the dominant source of this precipitate and, instead, present a model for mud precipitation on the bank margins that can explain the geographical distribution, clumped-isotope thermometry, and stable isotope signature of carbonate mud. Next, we address the enigma of why mud and ooids are so abundant in the Bahamas, yet so rare in the rest of the world: Mediterranean outflow feeds the Bahamas with the most alkaline waters in the modern ocean (>99.7th-percentile). Such high alkalinity appears to be a prerequisite for the nonskeletal carbonate factory because, when Mediterranean outflow was reduced in the Miocene, Bahamian carbonate export ceased for 3-million-years. Finally, we show how shutting off and turning on the shallow carbonate factory can send ripples through the global climate system.

Facial dysmorphology in children exposed in pregnancy to anticonvulsant medications correlates with deficits in IQ.

Some children exposed at conception to the antiepileptic drugs (AEDs) phenytoin (PHT), phenobarbital (PB), and carbamazepine (CBZ) have changes in their midface and fingers. It has been suggested that the anticonvulsant-exposed child with these subtle changes in facial features (the "anticonvulsant face") has a greater likelihood of having deficits in IQ in comparison with children exposed to the same anticonvulsants who do not have these features. 115 AED-exposed children (40, PHT; 34, PB; and 41, CBZ) between 6.5 and 16 years of age and 111 unexposed children matched by sex, race, and year in school were evaluated. The evaluations were (WISC-III), physical examination with measurements of facial features and digits and photographs. The AED-exposed children had cephalometric radiographs, but not the unexposed. Each parent had a similar examination of face and hands plus tests of intelligence. These AED-exposed children showed an increased frequency of a short nose and anteverted nares, features of the "anticonvulsant face." Lateral skull radiographs showed a decrease in the angle between the anterior cranial base and nasal bone, which produces anteverted nares. Mean IQs were significantly lower on one or more IQ measures for the children with these facial features. Shortening of the distal phalanges and small fingernails correlated with the presence of a short nose in that child. The findings in 115 children exposed at conception to either phenytoin, phenobarbital, or carbamazepine, as monotherapy, confirmed the hypothesis that those with a short nose and anteverted nares had a lower IQ than exposed children without those features.

Coastal eutrophication drives acidification, oxygen loss, and ecosystem change in a major oceanic upwelling system.

Global change is leading to warming, acidification, and oxygen loss in the ocean. In the Southern California Bight, an eastern boundary upwelling system, these stressors are exacerbated by the localized discharge of anthropogenically enhanced nutrients from a coastal population of 23 million people. Here, we use simulations with a high-resolution, physical-biogeochemical model to quantify the link between terrestrial and atmospheric nutrients, organic matter, and carbon inputs and biogeochemical change in the coastal waters of the Southern California Bight. The model is forced by large-scale climatic drivers and a reconstruction of local inputs via rivers, wastewater outfalls, and atmospheric deposition; it captures the fine scales of ocean circulation along the shelf; and it is validated against a large collection of physical and biogeochemical observations. Local land-based and atmospheric inputs, enhanced by anthropogenic sources, drive a 79% increase in phytoplankton biomass, a 23% increase in primary production, and a nearly 44% increase in subsurface respiration rates along the coast in summer, reshaping the biogeochemistry of the Southern California Bight. Seasonal reductions in subsurface oxygen, pH, and aragonite saturation state, by up to 50 mmol m-3, 0.09, and 0.47, respectively, rival or exceed the global open-ocean oxygen loss and acidification since the preindustrial period. The biological effects of these changes on local fisheries, proliferation of harmful algal blooms, water clarity, and submerged aquatic vegetation have yet to be fully explored.

Biological sensitivities to high-resolution climate change projections in the California current marine ecosystem.

The California Current Marine Ecosystem is a highly productive system that exhibits strong natural variability and vulnerability to anthropogenic climate trends. Relating projections of ocean change to biological sensitivities requires detailed synthesis of experimental results. Here, we combine measured biological sensitivities with high-resolution climate projections of key variables (temperature, oxygen, and pCO2 ) to identify the direction, magnitude, and spatial distribution of organism-scale vulnerabilities to multiple axes of projected ocean change. Among 12 selected species of cultural and economic importance, we find that all are sensitive to projected changes in ocean conditions through responses that affect individual performance or population processes. Response indices were largest in the northern region and inner shelf. While performance traits generally increased with projected changes, fitness traits generally decreased, indicating that concurrent stresses can lead to fitness loss. For two species, combining sensitivities to temperature and oxygen changes through the Metabolic Index shows how aerobic habitat availability could be compressed under future conditions. Our results suggest substantial and specific ecological susceptibility in the next 80 years, including potential regional loss of canopy-forming kelp, changes in nearshore food webs caused by declining rates of survival among red urchins, Dungeness crab, and razor clams, and loss of aerobic habitat for anchovy and pink shrimp. We also highlight fillable gaps in knowledge, including specific physiological responses to stressors, variation in responses across life stages, and responses to multistressor combinations. These findings strengthen the case for filling information gaps with experiments focused on fitness-related responses and those that can be used to parameterize integrative physiological models, and suggest that the CCME is susceptible to substantial changes to ecosystem structure and function within this century.

Microbial ecosystem dynamics drive fluctuating nitrogen loss in marine anoxic zones.

The dynamics of nitrogen (N) loss in the ocean's oxygen-deficient zones (ODZs) are thought to be driven by climate impacts on ocean circulation and biological productivity. Here we analyze a data-constrained model of the microbial ecosystem in an ODZ and find that species interactions drive fluctuations in local- and regional-scale rates of N loss, even in the absence of climate variability. By consuming O2 to nanomolar levels, aerobic nitrifying microbes cede their competitive advantage for scarce forms of N to anaerobic denitrifying bacteria. Because anaerobes cannot sustain their own low-O2 niche, the physical O2 supply restores competitive advantage to aerobic populations, resetting the cycle. The resulting ecosystem oscillations induce a unique geochemical signature within the ODZ-short-lived spikes of ammonium that are found in measured profiles. The microbial ecosystem dynamics also give rise to variable ratios of anammox to heterotrophic denitrification, providing a mechanism for the unexplained variability of these pathways observed in the ocean.

Oxygen supply capacity in animals evolves to meet maximum demand at the current oxygen partial pressure regardless of size or temperature.

The capacity to extract oxygen from the environment and transport it to respiring tissues in support of metabolic demand reportedly has implications for species' thermal tolerance, body size, diversity and biogeography. Here, we derived a quantifiable linkage between maximum and basal metabolic rate and their oxygen, temperature and size dependencies. We show that, regardless of size or temperature, the physiological capacity for oxygen supply precisely matches the maximum evolved demand at the highest persistently available oxygen pressure and this is the critical PO2  for the maximum metabolic rate, Pcrit-max For most terrestrial and shallow-living marine species, Pcrit-max is the current atmospheric pressure, 21 kPa. Any reduction in oxygen partial pressure from current values will result in a calculable decrement in maximum metabolic performance. However, oxygen supply capacity has evolved to match demand across temperatures and body sizes and so does not constrain thermal tolerance or cause the well-known reduction in mass-specific metabolic rate with increasing body mass. The critical oxygen pressure for resting metabolic rate, typically viewed as an indicator of hypoxia tolerance, is, instead, simply a rate-specific reflection of the oxygen supply capacity. A compensatory reduction in maintenance metabolic costs in warm-adapted species constrains factorial aerobic scope and the critical PO2  to a similar range, between ∼2 and 6, across each species' natural temperature range. The simple new relationship described here redefines many important physiological concepts and alters their ecological interpretation.

Deep ocean nutrients imply large latitudinal variation in particle transfer efficiency.

The "transfer efficiency" of sinking organic particles through the mesopelagic zone and into the deep ocean is a critical determinant of the atmosphere-ocean partition of carbon dioxide (CO2). Our ability to detect large-scale spatial variations in transfer efficiency is limited by the scarcity and uncertainties of particle flux data. Here we reconstruct deep ocean particle fluxes by diagnosing the rate of nutrient accumulation along transport pathways in a data-constrained ocean circulation model. Combined with estimates of organic matter export from the surface, these diagnosed fluxes reveal a global pattern of transfer efficiency to 1,000 m that is high (∼25%) at high latitudes and low (∼5%) in subtropical gyres, with intermediate values in the tropics. This pattern is well correlated with spatial variations in phytoplankton community structure and the export of ballast minerals, which control the size and density of sinking particles. These findings accentuate the importance of high-latitude oceans in sequestering carbon over long timescales, and highlight potential impacts on remineralization depth as phytoplankton communities respond to a warming climate.

Oceanic nitrogen reservoir regulated by plankton diversity and ocean circulation.

The average nitrogen-to-phosphorus ratio of marine phytoplankton (16N:1P) is closely matched to the nutrient content of mean ocean waters (14.3N:1P). This condition is thought to arise from biological control over the ocean's nitrogen budget, in which removal of bioavailable nitrogen by denitrifying bacteria ensures widespread selection for diazotrophic phytoplankton that replenish this essential nutrient when it limits the growth of other species. Here we show that in the context of a realistic ocean circulation model, and a uniform N:P ratio of plankton biomass, this feedback mechanism yields an oceanic nitrate deficit more than double its observed value. The critical missing phenomenon is diversity in the metabolic N:P requirement of phytoplankton, which has recently been shown to exhibit large-scale patterns associated with species composition. When we model these variations, such that diazotrophs compete with high N:P communities in subtropical regions, the ocean nitrogen inventory rises and may even exceed the average N:P ratio of plankton. The latter condition, previously considered impossible, is prevented in the modern ocean by shallow circulations that communicate stoichiometric signals from remote biomes dominated by diatoms with low N:P ratios. Large-scale patterns of plankton diversity and the circulation pathways connecting them are thus key factors determining the availability of fixed nitrogen in the ocean.

Projections of climate-driven changes in tuna vertical habitat based on species-specific differences in blood oxygen affinity.

Oxygen concentrations are hypothesized to decrease in many areas of the ocean as a result of anthropogenically driven climate change, resulting in habitat compression for pelagic animals. The oxygen partial pressure, pO2 , at which blood is 50% saturated (P50 ) is a measure of blood oxygen affinity and a gauge of the tolerance of animals for low ambient oxygen. Tuna species display a wide range of blood oxygen affinities (i.e., P50 values) and therefore may be differentially impacted by habitat compression as they make extensive vertical movements to forage on subdaily time scales. To project the effects of end-of-the-century climate change on tuna habitat, we calculate tuna P50 depths (i.e., the vertical position in the water column at which ambient pO2 is equal to species-specific blood P50 values) from 21st century Earth System Model (ESM) projections included in the fifth phase of the Climate Model Intercomparison Project (CMIP5). Overall, we project P50 depths to shoal, indicating likely habitat compression for tuna species due to climate change. Tunas that will be most impacted by shoaling are Pacific and southern bluefin tunas-habitat compression is projected for the entire geographic range of Pacific bluefin tuna and for the spawning region of southern bluefin tuna. Vertical shifts in P50 depths will potentially influence resource partitioning among Pacific bluefin, bigeye, yellowfin, and skipjack tunas in the northern subtropical and eastern tropical Pacific Ocean, the Arabian Sea, and the Bay of Bengal. By establishing linkages between tuna physiology and environmental conditions, we provide a mechanistic basis to project the effects of anthropogenic climate change on tuna habitats.

Local versus basin-scale limitation of marine nitrogen fixation.

Nitrogen (N) fixation by diazotrophic plankton is the primary source of this crucial nutrient to the ocean, but the factors limiting its rate and distribution are controversial. According to one view, the ecological niche of diazotrophs is primarily controlled by the ocean through internally generated N deficits that suppress the growth of their competitors. A second view posits an overriding limit from the atmosphere, which restricts diazotrophs to regions where dust deposition satisfies their high iron (Fe) requirement, thus separating N sources from sinks at a global scale. Here we use multiple geochemical signatures of N2 fixation to show that the Fe limitation of diazotrophs is strong enough to modulate the regional distribution of N2 fixation within ocean basins--particularly the Fe-poor Pacific--but not strong enough to influence its partition between basins, which is instead governed by rates of N loss. This scale-dependent limitation of N2 fixation reconciles local observations of Fe stress in diazotroph communities with an inferred spatial coupling of N sources and sinks. Within this regime of intermediate Fe control, the oceanic N reservoir would respond only weakly to enhanced dust fluxes during glacial climates, but strongly to the reduced fluxes hypothesized under anthropogenic climate warming.

Three-Dimensional Analysis of Nasal Symmetry Following Primary Correction of Unilateral Cleft Lip Nasal Deformity.

OBJECTIVE: To evaluate nasal symmetry using three-dimensional photogrammetry following primary tip rhinoplasty with or without an internal splint in patients with unilateral complete cleft lip/palate. DESIGN: We captured three-dimensional images of patients with unilateral complete cleft lip/palate who underwent nasolabial repair by rotation-advancement of the lip and primary tip rhinoplasty, either with or without an internal resorbable splint, and normal control subjects. We assessed nasal symmetry by identifying the plane of maximum symmetry and the root-mean-square deviation between native and reflected surfaces. PATIENTS/PARTICIPANTS: We imaged 38 controls and 38 subjects with repaired unilateral complete cleft lip/palate (20 with, 18 without an internal splint). RESULTS: Nasal asymmetry root-mean-square deviation clustered between 0.19 and 0.50 mm (median = 0.24 ± 0.08 mm) for controls; whereas, those with repaired unilateral complete cleft lip/palate ranged from 0.4 to 1.5 mm (median = 0.75 ± 0.40 mm). Although root-mean-square deviation ranges overlapped, patients with repaired unilateral complete cleft lip/palate had significantly greater asymmetry than controls (P < .001). We found no difference in asymmetry between patients with or without an internal splint (P = .5). CONCLUSIONS: Three-dimensional photogrammetry was used to successfully compare symmetry among different patient and control groups. Although "normal" nasal symmetry was attained in some patients following cleft lip/nasal repair, most had persistent asymmetry compared with normal controls. Placement of a resorbable internal splint did not improve symmetry in patients with unilateral complete cleft lip/palate.

Ocean nutrient ratios governed by plankton biogeography.

The major nutrients nitrate and phosphate have one of the strongest correlations in the sea, with a slope similar to the average nitrogen (N) to phosphorus (P) content of plankton biomass (N/P = 16:1). The processes through which this global relationship emerges despite the wide range of N/P ratios at the organism level are not known. Here we use an ocean circulation model and observed nutrient distributions to show that the N/P ratio of biological nutrient removal varies across latitude in Southern Ocean surface waters, from 12:1 in the polar ocean to 20:1 in the sub-Antarctic zone. These variations are governed by regional differences in the species composition of the plankton community. The covariation of dissolved nitrate and phosphate is maintained by ocean circulation, which mixes the shallow subsurface nutrients between distinct biogeographic provinces. Climate-driven shifts in these marine biomes may alter the mean N/P ratio and the associated carbon export by Southern Ocean ecosystems.

From global change to a butterfly flapping: biophysics and behaviour affect tropical climate change impacts.

Difficulty in characterizing the relationship between climatic variability and climate change vulnerability arises when we consider the multiple scales at which this variation occurs, be it temporal (from minute to annual) or spatial (from centimetres to kilometres). We studied populations of a single widely distributed butterfly species, Chlosyne lacinia, to examine the physiological, morphological, thermoregulatory and biophysical underpinnings of adaptation to tropical and temperate climates. Microclimatic and morphological data along with a biophysical model documented the importance of solar radiation in predicting butterfly body temperature. We also integrated the biophysics with a physiologically based insect fitness model to quantify the influence of solar radiation, morphology and behaviour on warming impact projections. While warming is projected to have some detrimental impacts on tropical ectotherms, fitness impacts in this study are not as negative as models that assume body and air temperature equivalence would suggest. We additionally show that behavioural thermoregulation can diminish direct warming impacts, though indirect thermoregulatory consequences could further complicate predictions. With these results, at multiple spatial and temporal scales, we show the importance of biophysics and behaviour for studying biodiversity consequences of global climate change, and stress that tropical climate change impacts are likely to be context-dependent.

Laser light scan analysis of the "anticonvulsant face".

BACKGROUND: The "anticonvulsant face," with a short nose, broad nasal bridge, epicanthal folds, and wide mouth, was described in the 1970s in children who had been exposed during pregnancy to the anticonvulsant drugs phenytoin and phenobarbital. The laser light scan makes it possible to establish three-dimensional positions of physical features and to determine more objectively the changes in the size and shape of the affected soft tissues of the faces of children exposed to these anticonvulsant drugs during pregnancy. METHODS: Thirteen individuals, exposed throughout pregnancy to phenytoin as either monotherapy or polytherapy, were identified in a previous analysis as having significant changes in their craniofacial features based on measurements of cephalometric radiographs. Those changes were associated with midface hypoplasia and a short nose, features of the "anticonvulsant face." The soft tissues of their faces have been evaluated with laser light scans. RESULTS: The notable changes in soft tissues identified by laser light scans were a wide philtrum (cph-cph), narrow mouth (ch-ch), short nasal bridge (n-prn), shortened nose height (n-sn), and flattened orbits (orbital protrusion index). CONCLUSION: This analysis of the facial features of phenytoin-exposed individuals, selected because of changes in their craniofacial bony structures, showed that there were several significant changes, two of which, widening of the philtrum and a small mouth, have not been described previously as part of this phenotype.

Stereophotogrammetry-based facial depth measurements: a novel method for quantifying facial projection.

BACKGROUND: Orthognathic surgery leads to alteration of the spatial relationship of the mandible and maxilla resulting changes in the degree of facial projection. Traditional 2-dimensional cephalometry and photographic techniques do not provide data on facial depth. Though stereophotogrammetry can be used as a noninvasive method for evaluating facial depth, the unavailability of ethnicity-specific norms hinder its routine use in clinical practice. The objectives of this study were to (a) generate an analytic scheme suitable for evaluating facial depth using stereophotogrammetry and (b) create normative data for the facial depth measurements for young Hong Kong Chinese adults. METHODS: Stereophotographic images from 41 male and 45 female ethnic Chinese young adults without facial deformities were analyzed. Facial depth measurements were performed based on standard anthropometric landmarks, with the aid of 3dMDVultus software. RESULTS: All facial depth measurements were found in absolute terms to be significantly higher in males. In contrast, the upper face, maxillary, and sublabial depth indices were significantly higher in females, whereas no significant gender differences emerged for lower facial and maxillomandibular indices. CONCLUSIONS: A novel method of using stereophotographic images for quantifying facial depth was evaluated. Normative facial depth measurements for young Hong Kong Chinese adults were established. This gender-specific database can be used as a reference in the diagnosis, treatment planning, or evaluation of outcomes after surgical correction of facial deformities.

Geographical and taxonomic patterns in aerobic traits of marine ectotherms.

The metabolism and hypoxia tolerance of marine ectotherms play key roles in limiting species geographical ranges, but underlying traits have only been directly measured for a small fraction of biodiversity. Here we diagnose and analyse spatial and phylogenetic patterns in hypoxia tolerance and its temperature sensitivity at ecologically active metabolic rates, by combining a model of organismal oxygen (O2) balance with global climate and biogeographic data for approximately 25 000 animal species from 13 phyla. Large-scale spatial trait patterns reveal that active hypoxia tolerance is greater and less temperature sensitive among tropical species compared to polar ones, consistent with sparse experimental data. Species energetic demands for activity vary less with temperature than resting costs, an inference confirmed by available rate measurements. Across the tree of life, closely related species share similar hypoxia traits, indicating that evolutionary history shapes physiological tolerances to O2 and temperature. Trait frequencies are highly conserved across phyla, suggesting the breadth of global aerobic conditions selects for convergent trait diversity. Our results support aerobic limitation as a constraint on marine habitat distributions and their responses to climate change and highlight the under-sampling of aerobic traits among species living in the ocean's tropical and polar oxythermal extremes. This article is part of the theme issue 'The evolutionary significance of variation in metabolic rates'.