Curtis Deutsch

Impacts of climate warming on terrestrial ectotherms across latitude

The impact of anthropogenic climate change on terrestrial organisms is often predicted to increase with latitude, in parallel with the rate of warming. Yet the biological impact of rising temperatures also depends on the physiological sensitivity of organisms to temperature change. We integrate empirical fitness curves describing the thermal tolerance of terrestrial insects from around the world with the projected geographic distribution of climate change for the next century to estimate the direct impact of warming on insect fitness across latitude. The results show that warming in the tropics, although relatively small in magnitude, is likely to have the most deleterious consequences because tropical insects are relatively sensitive to temperature change and are currently living very close to their optimal temperature. In contrast, species at higher latitudes have broader thermal tolerance and are living in climates that are currently cooler than their physiological optima, so that warming may even enhance their fitness. Available thermal tolerance data for several vertebrate taxa exhibit similar patterns, suggesting that these results are general for terrestrial ectotherms. Our analyses imply that, in the absence of ameliorating factors such as migration and adaptation, the greatest extinction risks from global warming may be in the tropics, where biological diversity is also greatest.

Putting the Heat on Tropical Animals

I mpacts of climate warming in the tropics— the cradle of biodiversity—are often predicted to be small relative to those in temperate regions (1, 2), because the rate of climate warming in the tropics is lower than at higher latitudes (3). Yet, predictions based only on the magnitude of climate change may be misleading. Models that include organismal physiology suggest that impacts of climate warming may be more severe in the tropics than in temperate regions. The impacts of climate warming on organisms depend not only on the magnitude of the environmental temperature shift but also on the behavior, morphology, physiology, and ecology of the organisms in question (4–6). This added complexity is daunting, but some general principles are emerging from research focused mainly on ectothermal animals (such as insects, fish, reptiles, and amphibians), which cannot maintain a constant internal body temperature. Negative impacts should be greatest on animals that are physiologically specialized with respect to temperature (7) and have limited acclimation capacity (8). Further, species living in warm climates are likely to suffer disproportionately from small increases in temperature (9), and species that live in aseasonal environments may be particularly vulnerable to increases in temperature, because changes in behavior and physiology are less likely to provide relief from rising temperatures (10). Terrestrial ectotherms with these vulnerability traits are typically tropical (7, 11, 12). In the 1960s, Janzen (13) noted that tropical ectotherms should be thermal specialists (see the figure, top) and have limited acclimation capacities, relative to higher-latitude species, because they have evolved in relatively constant, aseasonal environments. These predictions have been largely validated for various terrestrial and aquatic ectotherms (7, 11, 12, 14–17), yet the implications of this pattern for species vulnerabilities to climate change have rarely been investigated (15, 17–19). Tropical ectotherms have other traits that increase vulnerability. Because tropical organisms experience far more warm weather throughout the year than do temperate organisms, tropical animals might be expected to have greater heat tolerance. Surprisingly, that is often not the case: Heat tolerance typically varies very little across latitude in terrestrial ectotherms (7, 12, 15). Thus, many tropical ectotherms live much of the year in environments where equilibrium body (“operative”) temperatures are near or above optimal temperatures for performance (15). Tropical forest species may be particularly vulnerable, because they live in constant shade, are not generally adapted to the high operative temperatures found in warmer open habitats, and have few behavioral options available to evade rising temperatures (10, 15). Any climateinduced increase in operative temperaturecould cause steep declines in thermal performance and Darwinian fitness (see the figure, top). To assess whether independent data support these assertions, longterm demographic data on tropical species are required. Such data are rare, but in the study of frogs and lizards in lowland Costa Rica, densities have declined by ~4% per year between 1970 and 2005 (20). These declines are explained by climatedriven declines in leaf litter on the forest floor over the study period. Theoretically, these patterns can cut both ways: The same factors that make tropical ectotherms vulnerable to changing climate may benefit some temperate ectotherms (15) (see the figure, bottom). Empirical data tell a more complex story. During the last rapid warming event, 50 million years ago, insect damage on temperate plants did increase sharply (21), but data on contemporary temperate-zone insects are mixed: Some species are expanding rapidly (22), occasionally causing large changes to ecosystems and economies (23), whereas others—often specialists relying on day-length cues and species living in disappearing high-elevation habitats—are predicted to decline (6). All these predictions are for terrestrial habitats, and patterns may differ elsewhere. In marine habitats, for example, thermal specialists occur both at low and high latitudes, and thermal generalists appear most common at mid-latitudes (9, 24). Yet this pattern tracks the seasonality of ocean surface temperatures—polar oceans are cold but show little temperature variation throughout the year, and the largest seasonality in ocean surface temperatures are seen at mid-latitudes. Therefore, both tropical and high-latitude species live at near-stressful temperatures and could be vulnerable to warming (24). In intertidal habitats, which Putting the Heat on Tropical Animals ECOLOGY

Spatial coupling of nitrogen inputs and losses in the ocean

Nitrogen fixation is crucial for maintaining biological productivity in the oceans, because it replaces the biologically available nitrogen that is lost through denitrification. But, owing to its temporal and spatial variability, the global distribution of marine nitrogen fixation is difficult to determine from direct shipboard measurements. This uncertainty limits our understanding of the factors that influence nitrogen fixation, which may include iron, nitrogen-to-phosphorus ratios, and physical conditions such as temperature. Here we determine nitrogen fixation rates in the world’s oceans through their impact on nitrate and phosphate concentrations in surface waters, using an ocean circulation model. Our results indicate that nitrogen fixation rates are highest in the Pacific Ocean, where water column denitrification rates are high but the rate of atmospheric iron deposition is low. We conclude that oceanic nitrogen fixation is closely tied to the generation of nitrogen-deficient waters in denitrification zones, supporting the view that nitrogen fixation stabilizes the oceanic inventory of fixed nitrogen over time.

Why tropical forest lizards are vulnerable to climate warming

Biological impacts of climate warming are predicted to increase with latitude, paralleling increases in warming. However, the magnitude of impacts depends not only on the degree of warming but also on the number of species at risk, their physiological sensitivity to warming and their options for behavioural and physiological compensation. Lizards are useful for evaluating risks of warming because their thermal biology is well studied. We conducted macrophysiological analyses of diurnal lizards from diverse latitudes plus focal species analyses of Puerto Rican Anolis and Sphaerodactyus. Although tropical lowland lizards live in environments that are warm all year, macrophysiological analyses indicate that some tropical lineages (thermoconformers that live in forests) are active at low body temperature and are intolerant of warm temperatures. Focal species analyses show that some tropical forest lizards were already experiencing stressful body temperatures in summer when studied several decades ago. Simulations suggest that warming will not only further depress their physiological performance in summer, but will also enable warm-adapted, open-habitat competitors and predators to invade forests. Forest lizards are key components of tropical ecosystems, but appear vulnerable to the cascading physiological and ecological effects of climate warming, even though rates of tropical warming may be relatively low.

Isotopic constraints on glacial/interglacial changes in the oceanic nitrogen budget

early deglacial maximum in nitrate 15 N/ 14 N in suboxic zones and no significant glacialto-late Holocene change in global ocean nitrate 15 N/ 14 N. Consistent with the work of Brandes and Devol [2002], we find that the steady state 15 N/ 14 N of oceanic nitrate is controlled primarily by the fraction of total denitrification that occurs in the water column. Therefore a deglacial peak in the ratio of water column-to-sediment denitrification, caused by either a strong feedback between water column denitrification and the N reservoir or by an increase in sediment denitrification due to sea level rise, can explain the observed deglacial 15 N/ 14 N maximum in sediments underlying water column denitrification zones. The total denitrification rate and the mean ocean nitrate concentration are also important determinants of steady state nitrate 15 N/ 14 N. For this reason, modeling a realistic deglacial 15 N/ 14 N maximum further requires that the combined negative feedbacks from N2 fixation and denitrification are relatively strong, and N losses are relatively small. Our results suggest that the glacial oceanic N inventory was at most 30% greater than today’s and probably less than 10% greater. INDEX TERMS: 4267 Oceanography: General: Paleoceanography; 4805 Oceanography: Biological and Chemical: Biogeochemical cycles (1615); 4845 Oceanography: Biological and Chemical: Nutrients and nutrient cycling; 4870 Oceanography: Biological and Chemical: Stable isotopes; KEYWORDS: feedback, nitrogen isotopes, paleoceanography

Climate-Forced Variability of Ocean Hypoxia

The spatial extent of ocean hypoxic zones, which are uninhabitable by many marine organisms, is very sensitive to dioxygen content. Oxygen (O2) is a critical constraint on marine ecosystems. As oceanic O2 falls to hypoxic concentrations, habitability for aerobic organisms decreases rapidly. We show that the spatial extent of hypoxia is highly sensitive to small changes in the ocean’s O2 content, with maximum responses at suboxic concentrations where anaerobic metabolisms predominate. In model-based reconstructions of historical oxygen changes, the world’s largest suboxic zone, in the Pacific Ocean, varies in size by a factor of 2. This is attributable to climate-driven changes in the depth of the tropical and subtropical thermocline that have multiplicative effects on respiration rates in low-O2 water. The same mechanism yields even larger fluctuations in the rate of nitrogen removal by denitrification, creating a link between decadal climate oscillations and the nutrient limitation of marine photosynthesis.

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.

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.

Centennial changes in North Pacific anoxia linked to tropical trade winds

Climate warming is expected to reduce oxygen (O2) supply to the ocean and expand its oxygen minimum zones (OMZs). We reconstructed variations in the extent of North Pacific anoxia since 1850 using a geochemical proxy for denitrification (δ15N) from multiple sediment cores. Increasing δ15N since ~1990 records an expansion of anoxia, consistent with observed O2 trends. However, this was preceded by a longer declining δ15N trend that implies that the anoxic zone was shrinking for most of the 20th century. Both periods can be explained by changes in winds over the tropical Pacific that drive upwelling, biological productivity, and O2 demand within the OMZ. If equatorial Pacific winds resume their predicted weakening trend, the ocean’s largest anoxic zone will contract despite a global O2 decline.

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.