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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.▪
RESEARCH
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.
ON OUR WEBSITE◥
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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
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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.
Grady et al., Science 363, eaat4220 (2019) 25 January 2019 2 of
7
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)
Grady et al., Science 363, eaat4220 (2019) 25 January 2019 3 of
7
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
Grady et al., Science 363, eaat4220 (2019) 25 January 2019 4 of
7
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
Grady et al., Science 363, eaat4220 (2019) 25 January 2019 5 of
7
0 10 20 30
102
103
104
39404142
Sea Surface Temperature (ºC)
1/kT
Con
sum
ptio
n (t
yr
1 )
Con
sum
ptio
n
Prim
ary
Pro
duct
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.
REFERENCES AND NOTES
1. N. P. Kelley, N. D. Pyenson, Evolutionary innovation
andecology in marine tetrapods from the Triassic to
theAnthropocene. Science 348, aaa3716 (2015). doi:
10.1126/science.aaa3716; pmid: 25883362
2. J. G. Speight, Lange’s Handbook of Chemistry
(McGraw-Hill,2005), vol. 1.
3. H. Hillebrand, On the generality of the latitudinal
diversitygradient. Am. Nat. 163, 192–211 (2004). doi:
10.1086/381004;pmid: 14970922
4. D. K. Cairns, A. J. Gaston, F. Huettmann,
Endothermy,ectothermy and the global structure of marine
vertebratecommunities. Mar. Ecol. Prog. Ser. 356, 239–250
(2008).doi: 10.3354/meps07286
5. A. I. Dell, S. Pawar, V. M. Savage, Temperature dependence
oftrophic interactions are driven by asymmetry of speciesresponses
and foraging strategy. J. Anim. Ecol. 83, 70–84(2014). doi:
10.1111/1365-2656.12081; pmid: 23692182
6. D. P. Tittensor et al., Global patterns and predictors of
marinebiodiversity across taxa. Nature 466, 1098–1101 (2010).doi:
10.1038/nature09329; pmid: 20668450
7. D. P. Faith, Conservation evaluation and phylogenetic
diversity.Biol. Conserv. 61, 1–10 (1992). doi:
10.1016/0006-3207(92)91201-3
8. J. M. Grady, B. J. Enquist, E. Dettweiler-Robinson, N. A.
Wright,F. A. Smith, Evidence for mesothermy in dinosaurs.
Science344, 1268–1272 (2014). doi: 10.1126/science.1253143;pmid:
24926017
9. D. Bernal, K. A. Dickson, R. E. Shadwick, J. B. Graham,
Review:Analysis of the evolutionary convergence for high
performanceswimming in lamnid sharks and tunas. Comp.
Biochem.Physiol. A 129, 695–726 (2001). doi:
10.1016/S1095-6433(01)00333-6; pmid: 11423338
10. A. Berta, J. L. Sumich, K. M. Kovacs, Marine
Mammals:Evolutionary Biology (Academic Press, 2015).
11. M. L. Brooke, The food consumption of the world’s
seabirds.Proc. R. Soc. London Ser. B 271, S246–S248 (2004).doi:
10.1098/rsbl.2003.0153
12. K. H. Mann, J. R. Lazier, Dynamics of Marine
Ecosystems:Biological-Physical Interactions in the Oceans (Wiley,
2013).
13. T. Westberry, M. Behrenfeld, D. Siegel, E. Boss,
Carbon-basedprimary productivity modeling with vertically
resolvedphotoacclimation. Global Biogeochem. Cycles 22,
GB2024(2008). doi: 10.1029/2007GB003078
14. C. A. Stock, J. P. Dunne, J. G. John, Global-scale carbonand
energy flows through the marine planktonic food web:An analysis
with a coupled physical-biological model.Prog. Oceanogr. 120, 1–28
(2014). doi: 10.1016/j.pocean.2013.07.001
15. A. P. Allen, J. H. Brown, J. F. Gillooly, Global
biodiversity,biochemical kinetics, and the energetic-equivalence
rule.Science 297, 1545–1548 (2002). doi: 10.1126/science.1072380;
pmid: 12202828
16. D. Tittensor, B. Worm, A neutral-metabolic theory of
latitudinalbiodiversity. Glob. Ecol. Biogeogr. 25, 630–641
(2016).doi: 10.1111/geb.12451
17. J. F. Gillooly, J. H. Brown, G. B. West, V. M. Savage,E. L.
Charnov, Effects of size and temperature on metabolicrate. Science
293, 2248–2251 (2001). doi: 10.1126/science.1061967; pmid:
11567137
18. A. I. Dell, S. Pawar, V. M. Savage, Systematic variation in
thetemperature dependence of physiological and ecological
traits.Proc. Natl. Acad. Sci. U.S.A. 108, 10591–10596 (2011).doi:
10.1073/pnas.1015178108; pmid: 21606358
19. See supplementary materials.20. S. Pawar, A. I. Dell, V. M.
Savage, Dimensionality of consumer
search space drives trophic interaction strengths. Nature
486,485–489 (2012). doi: 10.1038/nature11131; pmid: 22722834
21. P. Domenici, The scaling of locomotor performance
inpredator-prey encounters: From fish to killer whales.Comp.
Biochem. Physiol. A 131, 169–182 (2001). doi:
10.1016/S1095-6433(01)00465-2; pmid: 11733175
22. K. A. Christian, C. R. Tracy, The effect of the
thermalenvironment on the ability of hatchling Galapagos land
iguanasto avoid predation during dispersal. Oecologia 49,
218–223(1981). doi: 10.1007/BF00349191; pmid: 28309312
23. A. Rand, Inverse Relationship Between Temperature andShyness
in the Lizard Anolis Lineatopus. Ecology 45, 863–864(1964). doi:
10.2307/1934935
24. R. L. Vaughn, E. Muzi, J. L. Richardson, B. Würsig,
DolphinBait-Balling Behaviors in Relation to Prey Ball
EscapeBehaviors. Ethology 117, 859–871 (2011). doi:
10.1111/j.1439-0310.2011.01939.x
25. K. A. Fritsches, R. W. Brill, E. J. Warrant, Warm eyes
providesuperior vision in swordfishes. Curr. Biol. 15, 55–58
(2005).doi: 10.1016/j.cub.2004.12.064; pmid: 15649365
26. A. M. Magera, J. E. Mills Flemming, K. Kaschner,L. B.
Christensen, H. K. Lotze, Recovery trends in marinemammal
populations. PLOS ONE 8, e77908 (2013).doi:
10.1371/journal.pone.0077908; pmid: 24205025
27. K. Kaschner, R. Watson, A. Trites, D. Pauly, Mapping
world-widedistributions of marine mammal species using a
relativeenvironmental suitability (RES) model. Mar. Ecol. Prog.
Ser.316, 285–310 (2006). doi: 10.3354/meps316285
28. K. Kaschner, thesis, University of British Columbia
(2004).29. D. Pauly, A. Trites, E. Capuli, V. Christensen, Diet
composition
and trophic levels of marine mammals. ICES J. Mar. Sci.
55,467–481 (1998). doi: 10.1006/jmsc.1997.0280
30. D. Pauly, V. Christensen, Primary production required
tosustain global fisheries. Nature 374, 255–257 (1995).doi:
10.1038/374255a0
31. E. Chassot et al., Global marine primary production
constrainsfisheries catches. Ecol. Lett. 13, 495–505 (2010). doi:
10.1111/j.1461-0248.2010.01443.x; pmid: 20141525
32. P. D. van Denderen, M. Lindegren, B. R. MacKenzie,R. A.
Watson, K. H. Andersen, Global patterns in marinepredatory fish.
Nat. Ecol. Evol. 2, 65–70 (2018). doi:
10.1038/s41559-017-0388-z
33. T. Roslin et al., Higher predation risk for insect prey at
lowlatitudes and elevations. Science 356, 742–744 (2017).doi:
10.1126/science.aaj1631; pmid: 28522532
34. D. Wright, Species-Energy Theory: An Extension of
Species-Area Theory. Oikos 41, 496–506 (1983). doi:
10.2307/3544109
35. A. E. Moura et al., Phylogenomics of the killer whale
indicatesecotype divergence in sympatry. Heredity 114, 48–55
(2015).doi: 10.1038/hdy.2014.67; pmid: 25052415
36. K. J. Gaston, T. M. Blackburn, J. H. Lawton,
InterspecificAbundance-Range Size Relationships: An Appraisal
ofMechanisms. J. Anim. Ecol. 66, 579–601 (1997). doi:
10.2307/5951
37. M. P. Hare, F. Cipriano, S. R. Palumbi, Genetic evidence on
thedemography of speciation in allopatric dolphin species.Evolution
56, 804–816 (2002). doi: 10.1111/j.0014-3820.2002.tb01391.x; pmid:
12038538
38. K. Longenecker, Fishes in the Hawaiian monk seal diet,
basedon regurgitate samples collected in the Northwestern
HawaiianIslands. Mar. Mamm. Sci. 26, 420–429 (2010). doi:
10.1111/j.1748-7692.2009.00332.x
39. T. Sasaki et al., Balaenoptera omurai is a newly
discoveredbaleen whale that represents an ancient evolutionary
lineage.Mol. Phylogenet. Evol. 41, 40–52 (2006). doi:
10.1016/j.ympev.2006.03.032; pmid: 16843687
40. D. Lee, P. Reddish, Plummeting gannets: A paradigm
ofecological optics. Nature 293, 293–294 (1981).doi:
10.1038/293293a0
41. C. Duffy, G. Taylor, Bull. Auckland Mus. 20, 497–500
(2015).42. P. Bertilsson‐Friedman, Distribution and frequencies of
shark-
inflicted injuries to the endangered Hawaiian monk seal(Monachus
schauinslandi). J. Zool. 268, 361–368 (2006).doi:
10.1111/j.1469-7998.2006.00066.x
43. R. A. Martin, N. Hammerschlag, R. S. Collier, C.
Fallows,Predatory behaviour of white sharks (Carcharodon
carcharias)at Seal Island, South Africa. J. Mar. Biol. Assoc. U.K.
85,1121–1136 (2005). doi: 10.1017/S002531540501218X
44. C. Lydersen, A. T. Fisk, K. M. Kovacs, A review of
Greenlandshark (Somniosus microcephalus) studies in the
Kongsfjordenarea, Svalbard Norway. Polar Biol. 39, 2169–2178
(2016).doi: 10.1007/s00300-016-1949-3
45. B. A. Block et al., Migratory movements, depth preferences,
andthermal biology of Atlantic bluefin tuna. Science 293,
1310–1314(2001). doi: 10.1126/science.1061197; pmid: 11509729
46. D. W. Sims et al., Hunt warm, rest cool: Bioenergetic
strategyunderlying diel vertical migration of a benthic shark.J.
Anim. Ecol. 75, 176–190 (2006). doi:
10.1111/j.1365-2656.2005.01033.x; pmid: 16903055
47. T. Kitagawa, S. Kimura, H. Nakata, H. Yamada,
Thermaladaptation of Pacific bluefin tuna Thunnus orientalis
totemperate waters. Fish. Sci. 72, 149–156 (2006). doi:
10.1111/j.1444-2906.2006.01129.x
48. B. Bogstad, H. Gjøsæter, T. Haug, U. Lindstrøm, Front.
Ecol.Evol. 3, 29 (2015). doi: 10.3389/fevo.2015.00029
49. J. P. Croxall, P. N. Trathan, E. J. Murphy, Environmental
changeand Antarctic seabird populations. Science 297,
1510–1514(2002). doi: 10.1126/science.1071987; pmid: 12202819
Grady et al., Science 363, eaat4220 (2019) 25 January 2019 6 of
7
RESEARCH | RESEARCH ARTICLEon A
ugust 30, 2020
http://science.sciencemag.org/
Dow
nloaded from
http://dx.doi.org/10.1126/science.aaa3716http://dx.doi.org/10.1126/science.aaa3716http://www.ncbi.nlm.nih.gov/pubmed/25883362http://dx.doi.org/10.1086/381004http://www.ncbi.nlm.nih.gov/pubmed/14970922http://dx.doi.org/10.3354/meps07286http://dx.doi.org/10.1111/1365-2656.12081http://www.ncbi.nlm.nih.gov/pubmed/23692182http://dx.doi.org/10.1038/nature09329http://www.ncbi.nlm.nih.gov/pubmed/20668450http://dx.doi.org/10.1016/0006-3207(92)91201-3http://dx.doi.org/10.1016/0006-3207(92)91201-3http://dx.doi.org/10.1126/science.1253143http://www.ncbi.nlm.nih.gov/pubmed/24926017http://dx.doi.org/10.1016/S1095-6433(01)00333-6http://dx.doi.org/10.1016/S1095-6433(01)00333-6http://www.ncbi.nlm.nih.gov/pubmed/11423338http://dx.doi.org/10.1098/rsbl.2003.0153http://dx.doi.org/10.1029/2007GB003078http://dx.doi.org/10.1016/j.pocean.2013.07.001http://dx.doi.org/10.1016/j.pocean.2013.07.001http://dx.doi.org/10.1126/science.1072380http://dx.doi.org/10.1126/science.1072380http://www.ncbi.nlm.nih.gov/pubmed/12202828http://dx.doi.org/10.1111/geb.12451http://dx.doi.org/10.1126/science.1061967http://dx.doi.org/10.1126/science.1061967http://www.ncbi.nlm.nih.gov/pubmed/11567137http://dx.doi.org/10.1073/pnas.1015178108http://www.ncbi.nlm.nih.gov/pubmed/21606358http://dx.doi.org/10.1038/nature11131http://www.ncbi.nlm.nih.gov/pubmed/22722834http://dx.doi.org/10.1016/S1095-6433(01)00465-2http://dx.doi.org/10.1016/S1095-6433(01)00465-2http://www.ncbi.nlm.nih.gov/pubmed/11733175http://dx.doi.org/10.1007/BF00349191http://www.ncbi.nlm.nih.gov/pubmed/28309312http://dx.doi.org/10.2307/1934935http://dx.doi.org/10.1111/j.1439-0310.2011.01939.xhttp://dx.doi.org/10.1111/j.1439-0310.2011.01939.xhttp://dx.doi.org/10.1016/j.cub.2004.12.064http://www.ncbi.nlm.nih.gov/pubmed/15649365http://dx.doi.org/10.1371/journal.pone.0077908http://www.ncbi.nlm.nih.gov/pubmed/24205025http://dx.doi.org/10.3354/meps316285http://dx.doi.org/10.1006/jmsc.1997.0280http://dx.doi.org/10.1038/374255a0http://dx.doi.org/10.1111/j.1461-0248.2010.01443.xhttp://dx.doi.org/10.1111/j.1461-0248.2010.01443.xhttp://www.ncbi.nlm.nih.gov/pubmed/20141525http://dx.doi.org/10.1038/s41559-017-0388-zhttp://dx.doi.org/10.1038/s41559-017-0388-zhttp://dx.doi.org/10.1126/science.aaj1631http://www.ncbi.nlm.nih.gov/pubmed/28522532http://dx.doi.org/10.2307/3544109http://dx.doi.org/10.1038/hdy.2014.67http://www.ncbi.nlm.nih.gov/pubmed/25052415http://dx.doi.org/10.2307/5951http://dx.doi.org/10.1111/j.0014-3820.2002.tb01391.xhttp://dx.doi.org/10.1111/j.0014-3820.2002.tb01391.xhttp://www.ncbi.nlm.nih.gov/pubmed/12038538http://dx.doi.org/10.1111/j.1748-7692.2009.00332.xhttp://dx.doi.org/10.1111/j.1748-7692.2009.00332.xhttp://dx.doi.org/10.1016/j.ympev.2006.03.032http://dx.doi.org/10.1016/j.ympev.2006.03.032http://www.ncbi.nlm.nih.gov/pubmed/16843687http://dx.doi.org/10.1038/293293a0http://dx.doi.org/10.1111/j.1469-7998.2006.00066.xhttp://dx.doi.org/10.1017/S002531540501218Xhttp://dx.doi.org/10.1007/s00300-016-1949-3http://dx.doi.org/10.1126/science.1061197http://www.ncbi.nlm.nih.gov/pubmed/11509729http://dx.doi.org/10.1111/j.1365-2656.2005.01033.xhttp://dx.doi.org/10.1111/j.1365-2656.2005.01033.xhttp://www.ncbi.nlm.nih.gov/pubmed/16903055http://dx.doi.org/10.1111/j.1444-2906.2006.01129.xhttp://dx.doi.org/10.1111/j.1444-2906.2006.01129.xhttp://dx.doi.org/10.3389/fevo.2015.00029http://dx.doi.org/10.1126/science.1071987http://www.ncbi.nlm.nih.gov/pubmed/12202819http://science.sciencemag.org/
-
50. J. P. Gattuso et al., Contrasting futures for ocean and
societyfrom different anthropogenic CO2 emissions scenarios.Science
349, aac4722 (2015). doi: 10.1126/science.aac4722;pmid:
26138982
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
www.sciencemag.org/content/363/6425/eaat4220/suppl/DC1
Materials and Methods
Table S1
Figs. S1 to S10
Data S1References (51–110)
24 February 2018; accepted 13 December
201810.1126/science.aat4220
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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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