BIODIVERSITY PATTERNS Metabolic asymmetryand the global … · predators. After demonstrating a systematic co-variation of global diversity with thermoregu-latory strategy, our analysis

RESEARCH ARTICLE SUMMARY◥

BIODIVERSITY PATTERNS

Metabolic asymmetry and the globaldiversity of marine predatorsJohn M. Grady*, Brian S. Maitner, Ara S. Winter, Kristin Kaschner, Derek P. Tittensor,Sydne Record, Felisa A. Smith, Adam M. Wilson, Anthony I. Dell, Phoebe L. Zarnetske,Helen J. Wearing, Brian Alfaro, James H. Brown

INTRODUCTION: One of the most generalpatterns in ecology is that diversity increasestoward the equator. In the ocean, however,mammal and bird richness generally peakin colder, temperate waters. This patternis especially puzzling given the thermalstress that cold water imposes on warm-bodied endotherms, which must maintainconstant, elevated body temperatures throughmetabolic activity. In contrast, ectothermicfish and reptiles that rely on ambient heatto regulate their body temperature show thehighest diversity in tropical and subtropicalhabitats.

RATIONALE: Large, predatory vertebratesregulate food webs across marine systems.Their distribution varies strongly with ther-moregulatory strategy, but the underlyingmechanisms are unclear. Using theory anddata, we sought to clarify the physiological andecological processes that lead to opposing pat-terns of diversity in marine predators.

RESULTS: To identify spatial patterns of di-versity, we synthesized range maps from 998species of marine sharks, teleost fish, mammals,birds, and sea snakes. We found that most

families of endothermic mammals and birdsshow elevated richness in temperate latitudes,whereas ectothermic sharks and fish peak intropical or subtropical seas. These findingsare reinforced by our analysis of phyloge-netic diversity, which weights diversity byspecies’ evolutionary relatedness.The strong latitudinal signal is suggestive

of thermal controls on diversity, but otherenvironmental features may be relevant. Inparticular, large, productive, or coastal hab-itats tend to support more species regard-less of thermoregulatory strategy. Endothermphylogenetic diversity and richness gen-erally peak between 45° and 60° latitude,but when we take the ratio of endothermto ectotherm richness—correcting for sharedspatial drivers—endotherm richness increasessystematically toward the coldest polaroceans.We then determined quantitatively and the-

oretically how these differences are linked tothermal physiology. We found that the meta-bolic response to ambient temperature is asym-metric between endotherms and ectotherms:Endothermic metabolism is generally constant,but in ectothermic fish, burst speed, routineswimming speed, neural firing rates, saccadic

eye movement, and visual flicker fusion fre-quencies fall exponentially in colder water.This has trophic and competitive implicationsfor marine species. Ectothermic prey are slug-gish in the cold and easier for mammals andbirds to capture, whereas slow-moving, pred-atory sharks are easier to avoid. As a result,marine endotherms are competitively favoredover ectothermic predators as water temper-atures decline.

We tested our theoryagainst a global datasetof pinniped and cetaceanabundance and foragingrates. As predicted, wefound that mammal con-sumption and density in-

crease log-linearly with water temperatureafter correcting for productivity. From theequator to the poles, marine mammal con-sumption of available food increases by afactor of ~80.

CONCLUSION: Our results and theory high-light the importance of energetics in speciesinteractions and the ecological and evolutionaryconsequences of endothermy at global scales.Although elevated metabolism is costly, it pro-vides foraging and competitive benefits thatunderpin the distribution and abundance ofmarine endotherms. Our findings also haveimplications for conservation. Rising oceantemperatures are predicted to exert substan-tial additional constraints on mammal andbird populations independent of food produc-tion or habitat conditions, and may alter thebalance of marine endotherms and ectothermsacross the globe.▪

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Grady et al., Science 363, 366 (2019) 25 January 2019 1 of 1

The list of author affiliations is available in the full article online.*Corresponding author. Email: [email protected] this article as J. M. Grady et al., Science 363, eaat4220(2019). DOI: 10.1126/science.aat4220

Water temperature drivesdifferences in metabolismand diversity betweenmarine endotherms andectotherms. Marine endo-thermic predators showcontrasting patterns ofphylogenetic diversitywith ectotherms, wherephylogenetic diversity isthe sum of evolutionarydistances between co-occurring species anddarker colors representhigher diversity. Unlike mostother taxa, mammal and bird phylogenetic diversity peaks in cold,temperate latitudes. Theory and data suggest that this reflects differ-ences in thermoregulation. In particular, thermal gradients acrosslatitude generate an asymmetric response in metabolic, sensory, and

locomotory rates between endotherms (which maintain constant rates)and ectotherms (which respond exponentially). As a result, colderwater is more favorable to endothermic predators pursuing sluggishectothermic prey or avoiding slower ectothermic sharks.

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RESEARCH ARTICLE◥

BIODIVERSITY PATTERNS

Metabolic asymmetry and the globaldiversity of marine predatorsJohn M. Grady1,2*, Brian S. Maitner3, Ara S. Winter4, Kristin Kaschner5,Derek P. Tittensor6,7, Sydne Record2, Felisa A. Smith8, Adam M. Wilson9,Anthony I. Dell10,11, Phoebe L. Zarnetske1, Helen J. Wearing8,12,Brian Alfaro8, James H. Brown8

Species richness of marine mammals and birds is highest in cold, temperate seas—aconspicuous exception to the general latitudinal gradient of decreasing diversity from thetropics to the poles. We compiled a comprehensive dataset for 998 species of sharks, fish,reptiles, mammals, and birds to identify and quantify inverse latitudinal gradients indiversity, and derived a theory to explain these patterns. We found that richness,phylogenetic diversity, and abundance of marine predators diverge systematically withthermoregulatory strategy and water temperature, reflecting metabolic differencesbetween endotherms and ectotherms that drive trophic and competitive interactions. Spatialpatterns of foraging support theoretical predictions, with total prey consumption bymammals increasing by a factor of 80 from the equator to the poles after controllingfor productivity.

Marine ecosystems are home to a varietyof large, active predators representingall major thermoregulatory strategies,including ectothermy (most sharks andbony fish), mesothermy (tuna, billfish,

lamnid sharks), and endothermy (mammals,birds). Of particular interest is the rich diversityof marine endotherms, which have repeatedlyinvaded the ocean despite numerous hurdles toentry, including high rates of heat loss fromwater (~23 times the rate of heat loss than air),obligate air-breathing, and, for many taxa, ener-getic and geographic restrictions imposed byterrestrial birth (1, 2). Despite the thermal stress,marine endotherm richness is generally highestin cold, temperate waters—a conspicuous excep-tion to the latitudinal pattern of increasing di-versity from poles to tropics observed in nearlyall other animal taxa (3). This unusual spatialpattern challenges general theories of diversity

and draws attention to the evolutionary impor-tance of thermoregulation in the abundance,distribution, and richness of species.To address this physiological, ecological, and

biogeographic puzzle, and to better understandthe evolutionary implications of endothermyand ectothermy, we synthesized a broad data-set of the distributions of large-bodied marinepredators. After demonstrating a systematic co-variation of global diversity with thermoregu-latory strategy, our analysis builds on existingtheory (4, 5) to derive underlying principles andquantitative predictions that link the metab-olism and foraging behavior of individual pred-ators to global patterns of energy flow andbiodiversity.

Empirical patterns of diversity

Ecologists have long noted that biodiversitytends to peak in the tropics, a pattern linkedto the greater stability, productivity, and area inlower latitudes (3). This holds for virtually allmajor multicellular taxa on land, including mam-mals, birds, reptiles, amphibians, plants, andinsects (3), and in the ocean for fish, mollusks,coral, seagrass, and mangroves (6). Most familiesof marine endotherms, however, have striking-ly different biogeographic patterns. Pinnipeds(walruses, seals, and sea lions) are virtually absentfrom tropical waters, and all major clades ofmarine birds that pursue prey via swimming(penguins, auks, grebes, loons, cormorants) arepredominantly temperate. Indeed, no species ofpenguin, auk, or pinniped inhabits the hyper-diverse central Indo-Pacific. Among cetaceans,only dolphins (Delphinidae) have truly diver-sified in the warm tropics. Nonetheless, the de-tails and causes of these patterns are obscured

by environmental variation across space, suchas variation in productivity or proximity toland, that affect both warm- and cold-bodiedtaxa. To clarify global patterns, we synthesizeddistributional data for 998 species of marinemammals, birds, sharks, large teleost fish, andsea snakes. We employed a measure of diversitythat controls for shared spatial drivers. Althoughendotherm diversity generally peaks between45° and 60° latitude (figs. S1 and S2) when wetake the ratio of endotherm to ectotherm rich-ness, we observed an inverse latitudinal gradientof diversity in which the endotherms becomesystematically more speciose than ectotherms incolder waters (Fig. 1).Another, perhaps more integrative, measure

than richness is phylogenetic diversity, whichweights diversity by the evolutionary distancebetween species (7) and may reveal patterns ob-scured by radiations of specialized taxa. Therecent availability of resolved phylogenies andcomprehensive species distributions now permitsglobal comparisons. Endothermic mammals andbirds show clear phylogenetic diversity peaksin temperate systems, in marked contrast toectotherms (Fig. 2 and figs. S1 and S2). Meso-therms such as great white sharks and tuna,which use metabolic heat to elevate body tem-peratures but do not maintain a thermal setpoint (8, 9), show intermediate and largely cos-mopolitan patterns of phylogenetic diversity. Forhigh-powered mesotherms and endotherms, it isalso apparent that diversity is less closely tied tocoastal habitats relative to ectotherms (Figs. 1 and2 and fig. S2).This covariation of spatial diversity with ther-

moregulatory strategy is striking and largelyunexplained by existing theory. Prior analyseshave typically focused on narrower taxonomicgroups or the origins of elevated tropical di-versity, or have suggested that endotherms, withtheir higher energy demands, are restricted totemperate seas because they are more produc-tive (10, 11). However, areas of high biologicalproductivity occur throughout the world’s oceans,including upwelling zones near the equator andalong tropical coastlines (12). Indeed, a number ofrecent models of net primary production (NPP)indicate a modest but significant increase in NPPin warm, tropical waters, where phytoplanktongrowth and turnover rates are higher (13, 14).These general patterns also extend to largerzooplankton (14). It has been proposed thatthermal constraints on predation are responsiblefor the temperate distributions of marine endo-therms (4). However, there have been limiteddemographic data to test this hypothesis, andthe quantitative, theoretical mechanisms arelargely unresolved. More broadly, most modelsof spatial diversity, including temperature-basedtheories, have generally ignored inverse latitudi-nal gradients and the role of species interactions[e.g., (15, 16)]. Here, we derive a quantitativetheory of species interactions that shows (i) howambient temperature generates metabolic andforaging asymmetries between endotherms andectotherms, and (ii) how metabolic asymmetries

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Grady et al., Science 363, eaat4220 (2019) 25 January 2019 1 of 7

1Department of Fisheries and Wildlife and Department ofForestry, Michigan State University, East Lansing, MI, USA.2Department of Biology, Bryn Mawr College, Bryn Mawr, PA,USA. 3Department of Ecology and Evolutionary Biology,University of Arizona, Tucson, AZ, USA. 4Bosque EcosystemMonitoring Program, University of New Mexico, Albuquerque,NM, USA. 5Department of Biometry and EnvironmentalSystems Analysis, University of Freiburg, Freiburg imBreisgau, Germany. 6Department of Biology, DalhousieUniversity, Halifax, Nova Scotia, Canada. 7UN EnvironmentProgramme World Conservation Monitoring Centre,Cambridge, UK. 8Department of Biology, University of NewMexico, Albuquerque, NM, USA. 9Department of Geography,State University of New York, Buffalo, NY, USA. 10NationalGreat Rivers Research and Education Center, East Alton, IL,USA. 11Department of Biology, Washington University,St. Louis, MO, USA. 12Department of Mathematics andStatistics, University of New Mexico, Albuquerque,NM, USA.*Corresponding author. Email: [email protected]

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lead to competitive differences between endo-therm and ectotherm predators that drive op-posing latitudinal gradients in diversity. Wevalidate theoretical predictions using data onendotherm and ectotherm metabolism and globalpatterns of abundance and consumption rates bymarine mammals. Warm-bodied mammals andbirds are more successful hunters and thereforebetter competitors than their ectothermic counter-parts when their metabolism is comparativelyhigher, leading to a systematic increase in therelative abundance and richness of endothermstoward the poles.

Metabolic model of predationand competitionIndividual predation rates

Foraging and locomotion, like all activity, isfueled by metabolism. The rate of metabolismis strongly temperature-dependent (17), as arerates of locomotion and foraging (18). Endo-thermic mammals and birds maintain a con-stant body temperature in the ocean, but thebody temperature of ectothermic predators andprey varies closely and passively with ambienttemperature. Overall, the kinetics of metabolic

rates (R) for endotherms (REndo) and ectotherms(REcto) can be written as

REndo º T0

REcto º exp � E0kT

� �

REndoREcto

º expE0kT

� �ð1Þ

where E0 is a metabolic “activation energy”(~0.65 eV), k is Boltzmann’s constant, T is ab-solute ambient temperature (17), and REndo/REcto is the ratio of metabolic rates that quan-tifies their metabolic asymmetry with respect toT. Body size is also an important driver of meta-bolic rates, but here we contrast thermoregulatoryguilds that overlap in size; in effect, this is a cor-rection for size differences, although body sizecan be incorporated for individual species (19).Although rarely studied, metabolic asymme-

tries between endotherms and ectotherms haveimportant implications for foraging and compe-tition (Eq. 1 and Fig. 3). To illustrate, we de-compose the rate of prey capture (Ca) into two

basic components (fig. S3): the encounter rateof predators with their prey (En) and the pro-bability of capture per encounter (Ce). Encounterrates reflect detection distance, prey density, en-vironment dimensionality, and the combinedspeed of predator and prey (20). In marine eco-systems, food webs are structured with largerpredators consuming smaller prey, so combinedspeed is closely approximated as the larger andfaster predator’s speed SPred, where En º SPred(19). Thus, the speed of ectothermic predatorsand their encounter rates with prey will increasein warm water, consistent with the temperaturedependence in Eq. 1, whereEnEctoº exp(–E0 / kT ).In contrast, the speed and prey encounter ratesof marine mammals and birds are largely inde-pendent ofwater temperature, and soEnEndoº T

0.Taking the ratio EnEndo /EnEcto, the temperature-independent components cancel and the thermaldependence of relative encounter rates is

EnEndoEnEcto

º expE0kT

� �ð2Þ

Following an encounter, the probability or effi-ciency of capturing prey is Ce, where Ce ≡ Ca /En.


Fig. 1. Relative richness of marine predators across space. (A) Largeectothermic predators (sharks, teleosts, sea snakes) dominate predatorrichness in tropical and subtropical coastal waters (blue), while endothermicswimming birds and mammals dominate cold waters and open oceans(red) (19). Where ectothermic species are absent, the highest value is

shown. (B and C) Coastal and oceanic spatial cell values are distinguishedby color, where coastal areas are cells < 200 m depth or include land.Quadratic fits are shown in (B) (r2coastal = 0.80, r

2oceanic = 0.47); cells are 1° × 1°.

For (A) and (C), cells are 110 km × 110 km. All taxa are primarily shallow-waterpredators (< 200 m depth); P < 0.0001 for all analyses. See also table S1.

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Capture efficiency should increase as SPred /SPreyincreases, where the most ecologically relevantspeeds are typically maximum rates, such as burstspeed during attack and escape (21). For ectother-mic hunters of ectothermic prey, CeEcto are pre-dicted to be approximately invariant alongthermal gradients because the metabolic rates

of predator and prey have similar temperaturedependence: CeEcto º SPredEcto /SPreyEcto º T

0.In contrast, for endothermic hunters of ecto-thermic prey, asymmetry in their metabolicresponse to water temperature (Fig. 3A) shouldlead to a higher capture efficiency in colderwaters, where prey are comparatively sluggish:

CeEndo º SPredEndo /SPreyEcto º exp(E1/kT ). Over-all, the relative capture efficiencies of endo-thermic and ectothermic predators are predictedto vary with water temperature as

CeEndoCeEcto

º expE1kT

� �ð3Þ

Although temperature constrains locomotoryand other metabolic-dependent rates given byE0 (Eqs. 1 and 2), behavioral strategies by bothpredator and prey can modulate capture effi-ciency and the value of E1 in Eq. 3, where E1 =aE0 and a is a multiplier. For example, whenambient temperatures drop on land, ectother-mic lizards have been observed to increase thedistance they flee endothermic predators (22)


Fig. 2. Phylogenetic diversity of large marine predators. Phylogenetic diversity, expressed asthe sum of evolutionary times of divergence [in millions of years (Ma)] between co-occurringspecies (7), is largely tropical or subtropical for ectothermic sharks (A) and teleost fish(B), cosmopolitan for mesotherms (excluding poles) (C and D), and peaks in cold, temperatewaters for endothermic mammals (E) and birds (F). Spatial cells are 110 km × 110 km;cells lacking species are unshaded.

Fig. 3. Metabolic and performanceasymmetry between endotherms andectotherms. (A) Endotherm metabolic andperformance rates are predicted to beinsensitive to water temperature,whereas ectotherm rates respond in anapproximately exponential fashion, promotingendotherm foraging and escape from sharksin colder water. (B) Data from the literatureon fish and endotherm speed supportpredictions. Red lines and symbols representendotherms; blue, ectotherms. Solid circles,fish; open circles, dolphins; solid squares,penguins; open diamonds, pinnipeds.Endotherm lines are mean values (9.1 fordolphins, 4.3 for penguins, 3.9 for pinnipeds).For fish, five species were analyzed, withtemperature and species as predictor variables,yielding ln(y) = 0.068t, n = 43, r2 = 0.98(shown) or ln(y) = –0.48(1/kT), where t andT are temperature in °C and K, respectively;P < 0.001. See (19).


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or switch from flight to crypsis (23). Conversely,some marine endothermic predators, such asdolphins, use cooperative hunting techniquesto herd fish and increase capture efficiency inwarmer waters (24) (see below). In these in-stances, we expect behavioral strategies to gen-erally dampen the thermal sensitivity of captureefficiency relative to metabolism (i.e., E1 ≤ E0).The ratio of endothermic to ectothermic capturerate provides a general measure of relative for-aging performance:

CaEndoCaEcto

º expEfkT

� �ð4Þ

where the thermal foraging constant Ef = E0 +E1, and 0.65≤Ef≤ 1.30. Equations 2 to 4 define themajor individual foraging asymmetries betweenpredatory endotherms and ectotherms in the ocean.

Scaling individual toecosystem consumption

The total rate of prey consumption by predatorsin an ecosystem or geographic region is simplythe sum of the rates of all the individuals. Treat-ing capture rate as a type I functional response(i.e., ignoring handling and satiety) is useful forlinking individuals to ecosystem scales: Valuesof Ca that exceed metabolic requirements rep-resent excess foraging capacity that promotespopulation growth (Fig. 4). Recognizing thattotal endotherm consumption (CTotEndo) is lim-ited by total prey production (PPrey) and treatingCaEndo/CaEcto as a rate variable, individual cap-ture rate can be linked to total ecosystem con-sumption using a Hill function:

CTotEndo ¼ PPrey1þ b= CaEndoCaEcto

� � ð5Þ

where b is a normalization constant. The ratioCaEndo/CaEcto in Eq. 5 connects differences inindividual foraging rates to competition for re-

sources at ecosystem scales: The proportion ofavailable prey consumed by endotherms is pre-dicted to increase as CaEndo/CaEcto increases, andto decline as it falls. Thus, although productivewaters will benefit all consumers, water temper-ature shifts the share of resources toward endo-therms in cold systems and toward ectothermsin warm waters (Fig. 4). To isolate the effects ofwater temperature, we transform and substitutefrom Eq. 4 to generate the slope-intercept formof Eq. 5:

logitCTotEndoPPrey

� �¼ Ef 1

kT

� �� lnðb1Þ ð6Þ

where b1 is a normalization constant, 1/kT is thepredictor variable, and Ef is the fitted slope (19),predicted to be 0.65 to 1.30 (see Eq. 4).

Testing the modelIndividual performance

To test predictions of metabolic asymmetries(Eq. 1 and Fig. 3A), we compiled and analyzeddata on metabolism and thermal performancefrom the literature (19). We found that musclecontraction rates, acceleration, and burst androutine swimming speeds of ectothermic fishdecline in an approximately exponential fash-ion with falling water temperature (Fig. 3B andfig. S4, A to C), supporting theoretical predic-tions and consistent with prior findings (18). Incontrast, burst speeds of endotherms are gener-ally insensitive to temperature, generating anasymmetry in performance in which endo-thermic predators become increasingly fasterthan their ectothermic prey and predators aswater temperature decreases (Fig. 3B). Meta-bolic asymmetries not only underlie asymme-tries in locomotion, but also drive asymmetriesin sensory and information-processing rates,such as flicker fusion rates, saccadic eye move-ment, and cerebral neural firing, all of whichgenerally support the theoretical expectationsfrom Eq. 1 (fig. S4, D to F). The ecological im-

portance of elevated sensory rates is underscoredby the unique physiology of mesothermic billfish(swordfish and sailfish), which channel metabolicheat production to elevate temperatures in theeyes and brain, thereby increasing neurosensoryrates (25). Overall, warm-bodied predators arefavored where prey are slow, stupid, and cold.

Ecosystem consumption

To test predictions of total consumption inEq. 6, we considered two major taxa of pred-atory endotherms whose abundance and globalconsumption have been spatially mapped: pin-nipeds and toothed whales (fig. S5). These taxawere generally not among the marine mammalsmost targeted by hunting in past centuries, andthe taxonomic breadth of our data, robustnessof predictions to global abundance fluctuations,and substantial recovery of most species (26)permits inferences into underlying ecologicalprocesses (19). We used data from Kaschneret al. (27, 28) on the consumption rates for pin-nipeds and small odontocetes (toothed whales,excluding beaked and sperm whales) to esti-mate CTotEndo in Eq. 6. Pinnipeds and smallodontocetes generally feed at a similar trophiclevel and forage in shallow waters that can belinked to available sea surface data (29). Weused NPP from the Carbon-based ProductionModel (17) as a proxy for prey production, inline with several fishery analyses (30, 31), butalso considered other NPP models and morecomplex trophic approaches (19). We also as-sessed the effects of additional environmentalvariables, such as ocean depth and distancefrom land, and models that partition spatialautocorrelation (19). We focus on differencesbetween endothermic and ectothermic pred-ators, but the more complex temperature depen-dence of mesotherms can be modeled andincluded in our framework.Endotherm consumption reflected both pro-

duction and temperature, but only sea surface


Fig. 4. A metabolic model of predation and competition.Watertemperature T drives ectothermic prey and predator metabolism andspeed S, generating shifts in trophic interactions between endothermsand ectotherms. In particular, per capita encounter rates (En), captureefficiency (Ce), and maximum capture rate (Ca) diverge over thermal

gradients for predators of different thermoregulatory guilds. As watertemperatures fall and CaEndo increases relative to CaEcto, endothermsare expected to collectively consume a proportionally larger shareof the available prey production (PPrey) and ectothermic predators alesser share. See also fig. S3.


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temperature showed a strong latitudinal gra-dient (fig. S7). Equation 6 predicts increasingtotal energy consumption, higher overall abun-dance and biomass, and, by extension, higherspecies richness of endotherms in colder watersafter controlling for production. We observedabsolute prey consumption by mammals to in-crease markedly in cooler waters, reflecting aconcurrent shift in their abundance (Fig. 5, fig.S5, and table S1). Consistent with predictions,annual total consumption by pinnipeds andsmall odontocetes increased by a factor of ~80from the tropics to the poles after controllingfor production (29° to –1°C; Fig. 5B and figs.S5 and S6), where Ef = 1.05 [95% confidenceinterval (CI), 1.04 to 1.05; r2 = 0.80]. Althoughtemperature was a strong predictor of total preyconsumption by mammals (r2 = 0.71; table S1),the relationship with NPP was poor. Only oneNPP model showed a positive association withmammal consumption but had almost no ex-planatory power (r2 = 0.038; table S1). Inclu-sion of additional predictor variables (chlorophylldensity, distance to land, ocean depth), parti-tioning of spatial autocorrelation, use of alter-nate NPP models, and incorporation of morecomplex trophic assumptions had little qual-itative effect on our results (table S1 and figs. S7and S8).Differences in speed and foraging strategy

within endotherms will modulate thermal sen-

sitivities of consumption. Pinnipeds are slowerthan dolphins (Fig. 3B) and do not cooperatewhile foraging (see below); thus, we expecta comparatively higher thermal sensitivityof consumption rates in pinnipeds. Indeed, Effor pinnipeds is 1.7, near the upper bound ofpredictions, and significantly higher than observedfor toothed whales (fig. S9 and table S1).The increase in relative prey consumption by

mammals observed in Fig. 5B implies a concur-rent decrease in relative consumption by ecto-thermic competitors in colder waters. Recentanalyses of fish stocks lend support to this pre-diction. Pelagic fish dominate fishery landingsof predatory fish in the tropics, but large demersalfish—which should experience less competitionand predation from air-breathing endotherms—constitute approximately an order of magni-tude higher proportion of landings in colder,temperate regions (32). Analysis of seabirdconsumption rates, which peak in cold latitudes,also reinforces the spatial-thermoregulatory link-ages observed here (11). Further support fordeclines in ectothermic predation in cold tem-peratures comes from land, where insect pre-dation from ectotherms declines away from theequator and at high elevations, unlike predationfrom endotherms (33).We suggest that thermal shifts in endotherm

abundance and prey consumption underlie theirlatitudinal patterns of phylogenetic diversity.Higher abundances and foraging success reduceextinction rates and permit specialization, whichpromotes speciation (34). With higher relativeperformance in cold waters, endotherms canconsume a higher fraction of their preferredprey, expand their dietary breadth, or specializeon a subset of their potential prey base. Forinstance, incipient speciation of killer whales(Orcinus orca) is in progress in the NorthPacific, where “transient” mammal-eating pop-ulations overlap but do not interbreed with fish-eating “residents” or “offshore” populationsspecializing on sharks and pelagic teleosts (35).In addition, species with high abundancestend to have large ranges (36) and subsequentfragmentation may promote allopatric specia-tion, particularly across ocean basins or hemi-spheres (37). The shift in intercept observed inFig. 1, B and C, and the strong coastal signal ofectotherm richness (fig. S2) indicate that endo-therm diversity is comparatively less respon-sive to the presence of coastal habitat. This mayreflect the advantages of speed and staminain the exposed, open ocean. In addition, highmetabolism may increase range size and reduceallopatric speciation, and respiratory constraintsmay limit utilization of benthic resources nearcoastlines.

Exceptions that support the rule

Temperature modulates metabolic asymmetriesbetween endotherms and ectotherms that arerelevant to active-capture interactions. Becausesea surface temperature shows a latitudinal gra-dient, our theory predicts a general latitudinalgradient in competitive success and relative

abundance for active, shallow-water foragers.However, not all tropical habitats are warmand shallow, and not all endothermic pred-ators pursue fast prey. In these instances, weexpect departure from general patterns. In par-ticular, we expect tropical species to show ahigher frequency of foraging in cool habitats(strategy 1), pursuit of comparatively slow prey(strategy 2), possession of exceptional foragingspeeds (strategy 3), or behavioral strategies thatlimit prey escape (strategy 4). These strategiesare evident in the limited diversity of tropicalendotherms (Fig. 1 and figs. S1 and S10). Forexample, sperm and beaked whales forage incold depths across the globe, while the penguinsand pinnipeds of tropical South America arerestricted to cool upwelling currents (strategy 1),but at lower abundances than southern, cold-water relatives (figs. S5 and S7); rare monkseals specialize on slower benthic fish andinvertebrates in warm seas (38), and tropicalpetrels and other “dippers” frequently alighton the water surface to feed on plankton (strat-egy 2); some baleen whales species pursue entirefish schools in the tropics by lunge feeding(39), mitigating caloric and maneuverabilitychallenges of hunting small prey while exploit-ing speed differences associated with larger bodysize and rapid gape expansion (21) (strategies 2and 4); plunge-diving birds, such as gannets, canreach exceptionally high speeds upon waterentry [~24 m/s (40) versus ~4 m/s for swim-ming birds in Fig. 3B] to feed on pelagic fishin tropical surface waters (strategy 3); cosmopol-itan dolphins (Delphinidae), in addition to beingfast (Fig. 3B), are large-brained foragers thatcooperate to herd fish into balls for easier cap-ture, among other techniques (24) (strategies 3and 4). Among swimming endotherms, onlydolphins have truly diversified in the warm,shallow tropics (fig. S2), perhaps reflecting theimportance of intelligence for mastering complexstrategies to tackle fast-moving prey. The ele-vated tropical diversity in dolphins is also con-sistent with their spatial patterns of consumption,which show a weaker response to water temper-ature relative to slower, solitary-foraging pinni-peds (fig. S9).

Biogeography of ectothermsand mesotherms

The importance of metabolic asymmetry is notrestricted to endothermic predation of ecto-therms. Many species of ectothermic sharksand even fish (41) are capable of preying onmarine mammals and birds. Our theory sug-gests that predation pressure by ectothermicpredators on endothermic prey should declineas water temperatures fall (Fig. 3A). To dealwith these constraints, we expect the followingbehavioral or thermoregulatory shifts in sharksforaging on endotherms: from pursuit in thewarm tropics to ambush or scavenging in coldtemperate seas, and/or an increase in meso-thermic shark predators in cooler waters. Indeed,high predation pressure from tropical Galapagosand tiger sharks is recognized as an important


0 10 20 30

102

103

104

39404142

Sea Surface Temperature (ºC)

1/kT

Con

sum

ptio

n (t

yr

1 )

Con

sum

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n

Prim

ary

Pro

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ion

10 6

10 4

10 2

39404142

slope = 1.05r2 = 0.80

1/kT

A

B

Fig. 5. Consumption across thermal gradi-ents in marine mammals. (A) As sea surfacetemperatures decline, pinniped and smallodontocete predators generally increase theirtotal consumption in a nonlinear fashion,as indicated by the loess regression fit.(B) Normalizing for primary production reducesnonlinearity and generates a dimensionlessratio of relative consumption. The fitted slopeprovides a measure of Ef (P < 0.0001); they axis is logit transformed. In (A) and (C), allvalues are per 110 km × 110 km spatial cell;temperature (°C) is shown for visualization.


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factor in the slow recovery of endangered trop-ical monk seals, which have failed to reboundfrom human persecution, unlike many over-hunted temperate species (42). At mid-latitudes,mesothermic great white sharks are commonhunters of pinnipeds, relying on ambush andelevated metabolism to seize their endothermicprey (43). In the coldest polar oceans, largeGreenland and sleeper sharks are generally tooslow to capture alert pinnipeds, but opportun-istically scavenge or hunt seals when they aresleeping (44). Instead, warm-bodied orcas andleopard seals dominate the apex predator niche.The high diversity of mesotherms in tropical

and warm temperate waters is also consistentwith foraging theory. Elevated body temper-atures in mesothermic tuna, billfish, and sharks(9) offer locomotory and sensory advantages forforaging and a degree of metabolic parity withendothermic competitors. In the warm tropics,species of tuna, swordfish, and other meso-therms will dive to cooler depths to feed (45),exploiting the favorable asymmetries shown inFig. 3. Indeed, even large ectotherms can exploitmetabolic advantages offered by thermal inertiawhen descending to forage (46). The appear-ance of many active mesothermic tuna andbillfish species in the clear waters of the openocean, in the company of fast-swimming dolphins(Fig. 1 and fig. S2), suggests that elevatedmetabolism is especially favored where prey isconspicuous and cannot hide. In cold temper-ate and polar seas, however, mesotherm bodytemperatures decline along with their perform-ance relative to endotherms. It is probably noaccident that the tuna species occupying thecoldest waters is also the largest, with thermalinertia buffering the bluefin tuna from fallingwater temperatures (47).

Conservation implications

Our results have implications for vulnerablemarine mammal and avian populations. Boththeory and data indicate that the ongoing in-crease in global ocean temperatures will impairendotherm populations independent of thermaltolerance, habitat preference, or prey availabil-ity. In the North Atlantic Barents Sea, research-ers have documented an increase in capelin andother small fish stocks over the past severaldecades, with a corresponding shift in thefortunes of two capelin predators: harp sealand cod (48). Harp seal populations have fallenwhile cod populations have surged, coincidingwith a period of unprecedented regional warm-ing. Rising sea temperatures near Antarctica arealso associated with widespread declines inseabird populations that cannot be consistentlylinked to changes in productivity or habitat(49). Indeed, after controlling for production,we find that each 1°C increase in sea surfacetemperature corresponds to a 12% decline inmarine mammal abundance, and a 24% declinefor pinnipeds (Fig. 5B, table S1, and fig. S9).Recent IPCC projections indicate that a 2° to 3°Cincrease by 2100 is likely (50), underscoring thisissue. For solitary foragers in particular, such

as seals and penguins, warming waters are pre-dicted to exert substantial foraging and demo-graphic repercussions.

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ACKNOWLEDGMENTS

We thank V. Christensen and R. Sibly for helpful discussions, andC. Stock for generously sharing data. Funding: Supported by afellowship from the Program in Interdisciplinary Biological andBiomedical Sciences at the University of New Mexico, NationalInstitute of Biomedical Imaging and Bioengineering grant

T32EB009414 to F.A.S. and J.H.B. Additional funding to J.M.G. andA.I.D. was provided by the NSF Rules of Life award DEB-1838346,P.L.Z. by NSF EF-1550765, and S.R. by NSF EF-1050770. Authorcontributions: J.M.G. and J.H.B. contributed to the study design;J.M.G, J.H.B., and H.J.W. contributed to the theoretical analysis;K.K., B.S.M., J.M.G., A.S.W., and S.R. contributed to the datacollection; J.M.G., B.S.M., A.S.W., S.R., A.M.W., and B.A.contributed to the data analysis; and all authors discussed theresults and contributed to the writing. Competing interests: Theauthors declare no competing interests. Data and materialsavailability: Data are available in the supplementary materials.

SUPPLEMENTARY MATERIALS

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Materials and Methods

Table S1

Figs. S1 to S10

Data S1References (51–110)

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Metabolic asymmetry and the global diversity of marine predators

Wilson, Anthony I. Dell, Phoebe L. Zarnetske, Helen J. Wearing, Brian Alfaro and James H. BrownJohn M. Grady, Brian S. Maitner, Ara S. Winter, Kristin Kaschner, Derek P. Tittensor, Sydne Record, Felisa A. Smith, Adam M.

DOI: 10.1126/science.aat4220 (6425), eaat4220.363Science

, this issue p. eaat4220; see also p. 338Sciencebase for large endothermic (''warm-blooded'') predators in polar regions.predation on ectothermic (''cold-blooded'') prey is easier where waters are colder, which generates a larger resourceanalyzed a comprehensive dataset of nearly 1000 species of shark, fish, reptiles, mammals, and birds. They found that

asked why this is (see the Perspective by Pyenson). Theyet al.occurring at the poles than at the equator. Grady plants and insects. Marine mammals and birds buck this trend, however, with more species and more individuals

Generally, biodiversity is higher in the tropics than at the poles. This pattern is present across taxa as diverse asCold is better for polar predators

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BIODIVERSITY PATTERNS Metabolic asymmetryand the global … · predators. After demonstrating a systematic co-variation of global diversity with thermoregu-latory strategy, our analysis