Climate, Energy and Diversity Author(s): Andrew Clarke and Kevin J.

Gaston Reviewed work(s): Source: Proceedings: Biological Sciences, Vol. 273, No. 1599 (Sep. 22, 2006), pp. 2257-2266 Published by: The Royal Society Stable URL: http://www.jstor.org/stable/25223597 . Accessed: 02/10/2012 19:14
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PROCEEDINGS
-OF-TQ) THE ROYAL Proc. R. Soc. B (2006) 273, 2257-2266 H?\ doi:10.1098/rspb.2006.3545

SOCIETY JLLJs

3May 2006 Published online

Review

Climate,
Andrew

energy
Clarke1*

and diversity
and Kevin J. Gaston2

1 Biological Sciences, British Antarctic Survey, NERC, High Cross, Madingley Road, Cambridge CB3 OET, UK and ofAnimal and Plant Sciences, University of Sheffield, Macroecology Group, Department 2Biodiversity Sheffield S10 2TN, UK
In recent years, a number of species-energy hypotheses have been developed to explain global patterns in

plant and animal diversity. These hypotheses frequently fail to distinguish between fundamentally different forms of energy which influence diversity in dissimilar ways. Photosynthetically active radiation (PAR) can be utilized only by plants, though their abundance and growth rate is also greatly influenced by water. The Gibbs free energy (chemical energy) retained in the reduced organic compounds of tissue can be utilized by
all heterotrophic influence dynamic ecologists organisms. temperatures mechanism; diversity to plant biomass organisms. and/or Neither abundance; processes. for energy; influence niche different If we PAR nor diversity Temperature it does, diversity however, by chemical may is not energy then influences increase of the as diversity a result though directly. of Both, however, population used loosely energy at warmer by by secondary

or evolutionary as a proxy It may (the

a form

energy, rate

it is often of

influence allowing We link

of utilization of there energetic is no

chemical lifestyles

also

a greater conclude energy to

range that

metabolic

hypothesis). processes are to make

single and

species/energy animals, and it is important

fundamentally is affected secondarily.

abundance these

in plants mechanisms,

progress

in elucidating

to distinguish
and

climatic effects on species' distribution

animal Keywords: diversity. abundance; energy; species

and abundance

from processes

linking energy supply

photosynthetically richness; temperature

active

radiation;

speciation;

1. INTRODUCTION
It is clear that, as a broad generalization, species diversity

on land and in the sea attains

tropics typically gradients of the and is lowest intermediate. in the sea, driven and of at the poles, There by

its highest
with are the high also

values

in the
regions

this by modifying classic island biogeography theory, area with energy. Specifically, Wright replacing argued that the diversity of one trophic level was determined by
the amount of energy available from the level below, and

temperate

longitudinal species regions, richness and on

tested this with data for plants and birds living on islands. these are distinct ideas about the role of Although
climate became energy systems, and energy in under Originally have been the regulation the umbrella formulated extended of subsumed hypotheses'. these ideas diversity, they term 'species/ for to the terrestrial sea (see, for

Indo-West across

Pacific

Caribbean

land

a number

continents

(Rosenzweig

1995;

Clarke St Crame 1997; Brown & Lomolino 1998; Gaston 2000; Gaston St Blackburn 2000). Here, we examine two
broad those The promoting classes based idea of around that tropical explanation climate favourableness diversity for and these energy of goes patterns, namely availability. is a key climate back to the

example,
et al. 2005; increasingly climate

Fraser
Rex

St Currie
et al that

1996; Roy
Recently, regulation

et al
of

1998; Hunt
become by diversity mechanisms

2005).

it has

factor earliest

recognized by productivity sea and

and

are quite

separate

naturalists
recognized

(von Humboldt
that climate exerts

1808),
an

and it is now widely

important influence on

(Ricklefs 2004; Turner

measure used ture as and in the a proxy measure,

2004).

Productivity
has

is difficult
frequently been tempera

to

so temperature

plant and animal distribution

Currie increased 1991). attention These through

(Turner
the use of

et al
have

1987,

1988;

relationships

received models

productivity

thereby confounding on diversity. effects

statistical

The of
under

different
the general

hypotheses
title of

that are frequently

hypotheses'

grouped
thus

(bioenvelopes)
organisms to

to predict
climate change

the potential
(Parmesan

response
et al

'species/energy and

differ
mechanism

1999;

significantly

in the extent
in what

to which
is meant

a physical
by energy.

Walther Dawson
structure

et al 2002; Parmesan St Yohe 2003; Pearson St of the effect of energy flow on 2003). Discussion has roots in its the of the trophic diversity development
of ecosystems by Odum and Lindemann, but

is described,

2. WHAT ISMEANTBY ENERGY?

The
sity different

especially Hutchinson
* Author

(1959). Wright

(1983)

formalized

literature discussing
and energy meanings availability of'energy'.

the relationship
encompasses These may

between
a number be

diver
of

summarized

for correspondence

(accl@bas.ac.uk).

as follows. ? 2006 The

2257

Royal

Society

2258

A. Clarke St K. J. Gaston
energy, or more

Climate,

energy and diversity

photo ourselves most data to terrestrial primarily are available. habitats, for this is where

(i) Radiation

specifically

synthetically active radiation (PAR), which is the fraction of the visible spectrum between 400 and
700 nm.

If photon flux were all that was involved in determining the abundance or diversity of higher plants, then we might
expect globe a more than even is actually distribution observed. ofthat There diversity is strong across latitudinal the

(ii) Thermal
temperature combination climate,

energy,
sensu with

frequently
stricto, other

expressed
or more that

as either
loosely determine in

factors

variation in the seasonality and intensity of light input, the latter being caused by the shallow angle of incidence and
greater towards the year, scattering higher the in the longer However, between atmosphere when received path-length averaged energy at over the latitudes. difference

(iii) Gibbs
the when

free energy
bonds are these

(chemical
of reduced oxidized

energy) released from

organic during compounds intermediary

covalent

metabolism. are

These

three

quite

different

forms

of

energy,

and

the

tropics and poles is only about fourfold (?pik St Rolfe the variation in plant diversity is very 2005), whereas much greater (Barthlott et al 1996; Davies et al. 2005).
The reason that plant use well by and distribution and diversity are not

lack of consensus
caused in part by

or clarity
confusion

in the ecological
them. This

debate
confusion

is
for

between

linked directly

to patterns
of as

of received
the light which providing

light energy
it receives, the electrons is the

is that
it also and solvent in

is not helped by our inability to define energy other than as clear the ability to do work (Haynie 2001). Nevertheless,
distinction energy, needs thermal to be maintained and chemical between energy radiation when energy

a plant to make water. As needs protons needed

photosynthesis, is involved

water as reactant

for biochemistry,

or product

discussing
way they Recent

patterns
influence discussions

of diversity, because
diversity. of species-energy

they differ in the

relationships have

all of the major

important, allows It is however, the plant therefore

classes
to absorb perhaps

of physiological
movement and surprising nutrients not

reactions. Most
of water to move that is what materials. the most

is that

between solar or ambient (thermal) energy distinguished and productive energy (Evans et ah 2004; (chemical) et ah (in press) recognize all et Allen ah 2005). Rodriguez three forms of energy identified above, but by analogy with to describe the physics of the terminology developed
moving potential includes bodies, energy. both they classify this and them as either kinetic energy, kinetic energy whereas or Under radiation scheme thermal

of the energy-related diversity hypotheses has that much of the been the demonstration undoubtedly successful
large-scale terrestrial biogeographical vascular plants can variation be explained in the by diversity variations of in

water availability 1993, 1998; (Currie 1991; O'Brien et al. 2005). Because water Francis St Currie 2003; Moser
is involved, by light or plant abundance alone: and hot diversity deserts are not have dictated low plant temperature

potential energy equates to Gibbs free energy (Haynie 2001). The combination of radiation and thermal energy
into between quite In a single two class forms ways. review, we seek to distinguish the various obscures of energy an that important influence distinction organisms in

diversity. Water
potential at which

availability

is frequently
(PET), loses water

determined
of the atmosphere.

as
rate

evapo-transpiration a saturated surface

a measure to the

different this short

O'Brien
relationship

(1993,

1998) has argued

and

that the PET-richness

that a combination of

is hump-shaped

forms of energy and identify the different ways in which influence biological diversity. Our aim is to they might
clarify the mechanistic links between the various forms of

PET
richness.

and precipitation
The importance

is the best
of water

predictor
to plant

of plant
and

biomass

energy
rigorously energy

and
on

diversity,
the First,

and
effects we

specifically
of climate the discuss

to distinguish
and links chemical between

plant richness have also been shown recently by Bjorholm et al (2005) and Sankaran et al (2005).
Although light is the primary energy source for plants,

between diversity.

solar radiation (PAR) and plant diversity, for it is at this lowest level of the food web that the important distinction
between diversity the the are effects clearest. energy of energy then supply discuss by those on biomass the links plants and between in their on We

they use only a small fraction of the incident PAR, typically less than 1% (?pik & Rolfe 2005). We have an excellent
understanding plants pounds There utilize for new of PAR tissue, the to molecular synthesize but variations mechanisms reduced in PAR by carbon alone which com explain

chemical

retained

very little of the global patterns

is thus no direct relationship

of higher plant diversity.

between plant diversity

tissues and the diversity of herbivores and higher levels in the food web. Finally, we explore the role of thermal
energy in these mechanisms, and linking introduce temperature unrecognized mechanism a previously to diversity.

and

a fairly strong energy (PAR); there is, however, relationship with a combination of water availability and temperature. While it iswidely observed that habitats with
freely support available a greater water biomass and a warmer of plants mean and/or temperature a larger number

(a) Radiation
For plants,

(photon flux)
a fundamental resource is light. In this sense,

of individuals, it is not immediately clear why this greater be distributed should necessarily abundance among a
of species. larger number we need to examine the diversity, is and the diversity Before links of returning plant to this point, and them. between biomass that eat

the photons
biodiversity, used systems in the where

in sunlight
for they are biosphere. the energy The

are the primary

the source major synthesis of almost exceptions

driver
all are

of all
energy those

the herbivores

for

of organic

tissue

obtained
between organisms, discussion

chemically. Most
PAR and to and

discussions

of the relationship
non-microbial we will We limit also our limit

concerned have diversity for the rest of this review plants and animals.

energy (b) Chemical The energy in photons

tissue of the biomass. reduced The carbon

trapped by plants
retained in the synthesized compounds

is used
covalent by

to build
bonds plants is

energy

higher (2006)

Proc. R. Soc. B

Climate, and other heterotrophic then utilized by herbivores in the food web. The Gibbs free energy in the
is released by retained such new also the catabolic within as ATP tissue store or a processes small and of number NADPH, intermediary of and energy then

energy and diversity

A. Clarke St K. J. Gaston on
rather numbers once for (see,

2259 plant
enable for species

1996). However,
species being present There covariation of has specialization. geographic and numbers

this depends
in sufficient is actually between animal species,

the different
abundance little to evidence

organisms
food metabolism, carrier used work. form

of plant

molecules either to build

environmental for example,

to perform in the short

Organisms of chemical, but energy

energy or

physiological term in the

covariation

been

accounted

Hawkins
Where into tural

St Porter
the greater

2003a;
species

Hawkins

& Pausas
also greater of this

2004).
translates struc

osmotic these flow are

electrical and

membranes, terms of

transient

across gradients not in important For energetic

richness complexity, a greater

of plants

enhanced diversity

structural may allow

between

organisms.

diversity

organisms

relationships within
chemical body To tissue a first energy and

food webs,
within at

the important factor is the

fraction organic the next level. trophic the of the

retained consumed

approximation,

therefore, is simply

what the

is important amount

1959; Pielou 1975; utilizing these habitats (Hutchinson Lee & Rotenberry 2005), although caution is needed to distinguish between species diversity and habitat diversity the MIH, 1995). These three mechanisms, (Rosenzweig
prey greater higher secondary specialization diversity diversity processes at and at one habitat level in the levels. build on complexity, food They the web are, enhanced allow to promote however, biomass for

of food organism are dynamic, it is the (and because relationships trophic rate of production than that rather crop biomass standing are subtle is critical). there compli Clearly, physiological cations, such as the need for vitamins, essential amino

to a heterotrophic

higher which

or abundance
energy. For a

driven
recent

by

the higher
of these

levels of available
mechanisms, see

acids (Mevi-Sch?tz
(Sargent et ah

St Erhardt
1999), or

2005),

specific fatty acids

relationships

review

stoichiometric

(Sterner St Elser 2002). Overall, however,

and nature of and food not resources the range that of are heterotroph, species

it is the amount
important which to comprise a

Evans et al (2004). The existence of mechanisms linking plant diversity to herbivore and higher trophic level diversity means that
these may also Thus be correlated studies with factors have shown that drive that plant animal diversity. diversity many

that food. This might

chemical predictor energy of animal available

imply that some measure

as biomass but this should does not be seem

of the
the best to be

richness,

et ah the case (e.g. Kaspari et ah 2000, 2004; Rodriguez to extent The here is the which traditional 2005). difficulty
ecological energy presence herbivores Although obviously consumers, necessarily to measures available of of food to the next cellulose only a biomass reflect the chemical the level; for example, trophic means in plants that many fraction food of of their food. would resources

is frequently correlated with actual PET, ?vapo or measures sensed of transpiration remotely plant as the normalized such difference production vegetation

et al 2003; Bailey index (NDVI; Currie 1991; Hawkins et al 2004; Seto et al. 2004; Bellocq & G?mez-Insausti 2005; Pautasso & Gaston 2005). Although the availability
of water food may affect these the ability correlations of animals are to generally exploit their resources, indirect,

and lignin can utilize the support it is not equate

a small of greater

existence

mediated
temperature We thus

through
on have plant

the effects
diversity. two quite

of water
different

availability
forms of

and

larger a

biomass how

heterotrophic this should

at all obvious to higher

or why

energy

heterotrophic

diversity

(Blackburn St Gaston
problem why does that posed a higher of

1996). This
in the

is clearly an analogous
for plants: not in greater and

influencing diversity at different levels of the food web, namely light energy in plants and chemical energy in
heterotrophs (herbivores and carnivores). In both cases,

abundance utilizing

section previous of resources result that resource,

however,

the link to diversity

processes these two

is indirect, and ismediated

linked to abundance. are influenced We by

diversity

organisms

simply a higher biomass? (c) Abundance

We have understood to the

through population now how explore to what temperature. extent

relationships

a third form of energy, namely and diversity

above link that the of fairly simple of and well availability resources and by thermal established mechanisms

thermal energy (enthalpy),

is validly approximated

energy

abundance In the

or biomass case of plants, nutrients); plant mechanism carnivore

resources. water the other plant, (and resource

organisms the resources in the and

inorganic is their One or

those utilizing are light and case of herbivores, carnivores the leads increase to higher it is in

3. TEMPERATURE AND DIVERSITY

Temperature of a body the them; times (Haynie interval same this is not to gain is the or energy; lose heat. if there definition as the of zeroth can it is a measure Two is no bodies net heat of are the said flow and tendency to be between is some at

food,

for

animals. herbivore

by which abundance

temperature

temperature law be of

diversity
extinction,

is that larger populations

the risk of which is an

buffer
inverse

species
and

against overall
popu

formalized 2001). scale

thermodynamics as an such

nonlinear

function
abundance

of population
enables more

size (Lande
species

1993). Greater
to attain viable

such

Temperature as degrees

Celsius,

either expressed or a ratio scale

as Kelvin
Neither content;

(Stevens
is two bodies

1946).
a same direct measure can of heat at the temperature contain

lation sizes. This

used to explain

is the more-individuals
why areas with greater

hypothesis (MIH)
resources support

temperature

higher diversities (Wright 1998; Evans et ah 2005).

A food second plants allows important for factor the which parasites

1983;
is that evolution in and

Srivastava

& Lawton
of of

very

a greater diversity of a wider range allows for (e.g. a wider Gaston

different of heat energy, this being quantities expressed as thermal capacity (specific heat capacity in the older literature). The very different thermal capacities
air and very the water much mean more of that heat air a given volume of water of roughly (by a factor X4) at the same temperature,

of

specialist range

herbivores, of predators, (2006)

turn

contains than

pathogens

same

mass

Proc. R. Soc. B

2260

A. Clarke St K. J. Gaston which

to thermal temperature

Climate,

energy and diversity climate

as essay, some Hutchinson species places, is centred being of himself a group why on in some the counter posed question: can evolve of organisms to live cannot This others? perceptive subjective tougher view of some habitats While if in

a difference
system and Because

is fundamental
ecology. is not energy,

to the global
it cannot

be used

tougher question or regions

such by organisms
discussions temperature literature of used (for of with is replete the

(Huston
energy with

2003).
supply,

Despite
hypothesis and the as here

this, many
equate ecological a function is being energy sometimes of energy

the

species-energy

way

for organisms.

this might
envisage regulate Although arisen by

seem
a mechanism

intuitively

reasonable
temperature

it is not
alone

easy to
could

graphs often, some

of diversity temperature

by which is not are

temperature. as a surrogate example,

Most for

diversity. temperature grouping what energy, essentially confusion hypotheses has of

measure production), as

of

chemical but

net

primary

temperature

is viewed

(incorrectly)

a source

regulation
class of undoubtedly

by an abiotic
'species/energy the affects

factor
activity

(temperature)
and distribution

within

the

in itself. Despite
to discern

hypotheses'.

Temperature of many

this lack of clarity in the literature, it is possible

two separate themes in the profusion of

links between diversity and temperature: proposed (i) temperature affects diversity directly and (ii) temperature rates of speciation and affects diversity by determining
extinction. We will discuss these in turn.

organisms (Turner et al 1987, on energetics influence powerful

theless, a cow, lizard but we are or fish can food the that temperatures, therefore, without left with feeling and hence

1988) and also has a (Clarke 2003); never

bask it will forever die. (but warmer more as it At in warm present,

intuitive somehow

dangerously places species, to how are but this that in polar and thereby temperature a source where of

(a) Direct
A direct is no in there change

effects
effect of

of temperature
temperature link leads on between

on diversity
diversity the occurs two, and when a to a whereby

anthropocentric) more amenable, with might no viable

can

support

mechanistic In might the case limit its and This, control of

explanation plants,

intermediate temperature

work.

is possible

inevitably

directly

temperature regions

overall of

abundance nutrient availability

change
controls prediction are tures intuitive make earliest

in diversity.
diversity that higher. feeling a living than diversity This that

Any
will

hypothesis
has be the greater has

that
where its

temperature
consequential tempera in the

through

directly

simple

transpiration, limit as an diversity. abiotic and the

through of course,

the MIH

mechanism by as

is limitation factor, of ectothermic rate of physiological mechanism, not

explanation warmer habitats ones, which a view has

origin

environmental same is true the

are that been

easier goes

colder and

to places to the back

energy,

animals,

temperature In the absence

influences

processes. it is difficult to

naturalists

summarized

of a convincing

succinctly
more

by Currie

(1991)

as 'benign conditions
of guises,

permit
including

move

the debate
diversity

beyond
with

the current
temperature.

phase

of simply not by
the

species'.

It appears

in a number

correlating mean Although

the 'physiological tolerance hypothesis' (Currie et ah the 'range limitation hypothesis' (Evans et ah 2004), and the 'thermoregulatory loads' hypothesis 2005) (Lennon et al. 2000). Turner (2004) calls it the 'ambient energy hypothesis' to distinguish it from the productivity based hypothesis of Wright (1983). These are all slightly
different warmer hypotheses, places are but seen have a common amenable, theme in either that by as more

A second possibility
temperature, a number but

is that diversity
by variability have of authors

is controlled
in considered

temperature.

possibility
variability,

of
the

link between
debate

diversity
was opened

and
by

climate
Stevens

modern

(1989).
latitudes ecology and thus

Stevens
required because

suggested
a more of the strong

that organisms
generalist seasonal more low variation

living at high
and in climate, In

physiology

allowing greater activity, more

not clear quite the how), physiological energy physical or in reducing thereby Although

species to exist (though it is

the costs case in of endotherms warm by and keeping larger

contrast, resulted

were able species at low latitudes in more localized

to become the

widespread. climatic variability and hence

species

ranges,

releasing the precise

to

allow mechanisms

populations. are not always

higher richness. What

is thus not the low seasonal mechanism effect could of mean of course differences is thus

keeps diversity
mean between quite temperature, summer independent on diversity; or

low at high latitudes

but and of the even the large This winter. any two

specified, these ideas are given strength by the widely observed correlation between latitude (which is frequently
taken ture) involve as and a proxy diversity. plants, for climate or environmental are widespread, endotherms tempera and (Gaston These ectotherms correlations and

postulated processes

temperature act

in parallel

synergistically.

2000).
The ging diversity One can problem a mechanism (or at with this hypothesis comes with could Currie could envisa regulate 1991). set temperature by which set a maximum value: least that particular

Gaston critical
and occurring much of

St Chown (1999) have recently shown that the factor is the relationship between the variability
value, intermediate tropics. which suggests latitudes can that also many occur at the species across

the mean

recognize

habitats

As

is often

specific physiological
of organisms with the shallow could meet.

challenges
Examples

that only certain groups

might be polar regions

hypothesis continent
examples extend the

tested his the case, Stevens (1989) one and one from with data hemisphere only case Most of the North this America). (in
were terrestrial, to the sea. argument The although marine Stevens taxa did used

below and winter temperatures permafrost with of fluids, temperate regions body point freezing areas with or tropical low winter humidity. frosts, regular

used

(fishes and molluscs)

tropics matched seas, marine which to poles, by the at

do show a strong diversity cline from

least in shallow of water, but this is not in the temperature from typically that much variability on land. less

In a classic
suggested become isms being

contribution
that as one moves tougher, to tolerate

to ecology, Hutchinson
from with the tropics fewer to poles and But fewer in the

(1959)
habitats organ same

pattern

somehow able

is very

different are

Polar variable

conditions.

environments

Proc. R. Soc. B

(2006)

Climate, Pacific Ocean (170?W)

energy and diversity 'MM?M?&u?a

A. Clarke & K. J. Gaston South Americas

2261

(a) 35

40

h 30

h 20

10

90 75 60 45 30

15 0-15-30-45-60-75-90 latitude

90 75 60 45 30 15 0-15-30-45-60-75-90 latitude
in the Pacific 170? W Ocean. Note along 1983-2003. for the period The AVHRR at Active Archive Centre (PO.DAAC) and annual (b) Mean (black) (grey) at data 1961-1990 (?C) for the period to an equal-area a Behrmann grid using are for Data (provided by R. G. Davies). and plotted after pooling into bins of Io of in each bin.

1. (a) Mean and annual range of sea-surface Figure (black) temperature (grey) (SST) are in the temperate are averages how the largest seasonal variations latitudes. Data v. 5.0 SST Pathfinder data were from obtained the Physical Distributed Oceanography the NASA California Jet Propulsion Pasadena, Laboratory, (http://podaac.jpl.nasa.gov). air temperature of synoptic for terrestrial habitats. Mean annual range temperature et ah 2002), 10 min resolution from station means and resampled interpolated (New at a resolution m at the standard of 96486.2 of 30? N and 30? S projection parallels North latitude, seasonally and South the than America range cold with at http://www.cru.uea.ac.uk/cru/data/tmc.htm), (available calculated from seasonal and minimum average maximum or warm temperate latitudes, with

there has been

become saturated;

sufficient
the

time for the new habitats

patterns were thus

to
the

tropical regions also being relatively stable (figure 1). These differences allow for a simple test of the role of climate variability in governing broad patterns of diversity.
If temperature we variability would expect were marine the key determinant to peak of in diversity, diversity This However,

observed

result of limits set by climate and not slow and incomplete

recolonization. historical There recolonization is, however, signal in North some evidence for species a American

polar and tropical

highly observed some seasonal (Clarke indications

latitudes, with
St Crame that strong

reduced diversity
is not there seasonality

in the
what is are is

richness Hawkins
Another and

(Hawkins 2004).
class of are

et ah 2003; Hawkins
explanation determined is that by

St Porter 20036;
rates of speciation as and

temperature

latitudes. 1997).

extinction

temperature,

climate

result tropical areas have achieved higher diversities

temperate non-equilibrium tion in colder or polar regions. This could operate both mechanism regions (if the is simply process and of diversifica has not

than
as a

associated with reduced marine diversity, both in benthos and plankton. The first is that the diversity of benthic on both the Atlantic molluscs and Pacific continental
shelves marine tropics of North America drops switch from steeply the at the point relatively zones where temperatures to the seasonal aseasonal (Roy et al

slower

yet

proceeded
mechanism steady The state, most

so far as in the tropics) and as an equilibrium

(if but rates differ of speciation and extinction are regions). is that of at between contribution and polar tropical to this debate

temperature

1998). The
marine

second
is

is that
lower

the diversity
in more seasonal

of epipelagic
provinces

recent

copepods

(Woodd-Walker
correlations and

et al 2002). These
it is not at all clear

are, however,
what

simply

et ah (2002), who Allen linked the widely observed correlation between diversity (both plant and animal)
and temperature to the metabolic theory of ecology

the mechanism

a reduction in diversity in climatically underpinning one possibility seasonal habitats might be (although might be if an obligately eurythermal physiology were
necessarily to a narrow more range energetically of expensive than one adapted temperatures).

(Brown et ah 2004), (Damuth equivalence

linked through higher did directly 'the and generally

and to the principle of energetic 1987). They argue that diversity is

mechanistically faster (Brown through could to temperature at rates observed biological et ah 2003). If temperature its effect not on speciation the

temperatures' govern this diversity mechanism

rate

(b) Temperature,
The previous two concern temperature

speciation
classes an of

and extinction
explanation world: involving temperature

then

explain

observed

diversity
temperatures

patterns

in birds

and mammals,
at a relatively

whose
high

body

equilibrium

are maintained

and more

sets
absolute

limits
value

to maximum
or its seasonal

diversity
variability,

either
and

through
organisms

its

or less constant
mammals show

level (Storch 2003).

strong diversity

In fact, both birds and

so this mech

gradients,

have diversified until those limits are reached and the habitats saturated. Currie (1991) recognized that inNorth
America recovered many from higher the last latitude glacial areas have only but recently felt that maximum,

anism
provide

linking diversity
a convincing

directly

to temperature

fails to

general

explanation.

Allen et ah (in press) have subsequently idea further, the link to abandoning

developed the the energetic

Proc. R. Soc. B

(2006)

2262

A. Clarke

St K. J. Gaston teleostfish resting metabolism

Climate,

energy and diversity

ectotherm

(a)

scope

250

for activity (model)

(c)
1.4 1.2

endotherm

field metabolism

-10
Figure Note

10 20

30

40

50

5 10 15 20 25 30 35
temperature (?C)

-20

-10

10

20

30

40

temperature (?C)

temperature (?C)

2. Temperature and metabolic niches, in resting metabolic rate in teleost fish St Johnston (a) Variation (Clarke 1999). at higher the wider of values how absolute aerobic also increases with range temperatures, (b) Diagram scope showing rate increases This arises because with and relative aerobic temperature. temperature scope resting metabolic positively (the to resting metabolism) ratio of active was based on data is temperature invariant. the model for teleost it also fish, Although to other ectotherms are for field metabolic niches in mammals and birds applies (Clarke 2003). (c) Energetic (black) (grey). Data rate, and have been of values corrected at higher for body mass assuming a mass exponent of 0.75 (redrawn from Anderson & Jetz 2005). Note the range temperatures. diversity circumstances mutation rates implies would limit that not adaptation rates. to new ecological and is rather that little

wider

equivalence of populations (which is itself controversial: Gaston St Blackburn 2000) but combining the metabolic theory of ecology and the neutral model of biodiversity (Hubbell 2001). They propose that temperature dictates
the evolutionary of free two rate rate of energy processes and thus a population, governs in standing the concert whereas number dictate Turner the of the availability populations; overall speciation

be mutation-limited, There

speciation rate is a strong

evidence
The implicitly

for this (Evans St Gaston

evolutionary that there

2005).
also between assumes current

hypothesis correlation

these

diversity.

(2004)
diversity temperature

has
can

also proposed
be and explained processes

that
by formalized

large-scale
an interaction in Hubbell's

patterns
between neutral

in

and historic energy levels; this is probably reasonable. it is now recognized that variations in the Earth's Although orbit will result in changes in the amount and distribution
of solar energy are of received too that small, solar on and energy, the surface plants that of utilize they on with are do the planet, such not a these small changes fraction

theory of biodiversity.
A affects central the tenet of these evolutionary is that proposals rate of populations. temperature This evol

influence

diversity
however, and factors, timing

directly. These Milankovitch

have of these a profound the seasons, climate influence together cycles

climate
the other

cycles do,
distribution climate driver

utionary rates hypothesis (Rohde 1992) makes several key (Evans StGaston 2005). Most importantly, it assumptions
assumes that higher temperatures promote mutation. This

and

in turn

a major

can be either through direct pathways,

pathways time, such as an rate between the of effect or of temperature metabolic population two

or through
on size. and Analysing speciation

indirect
the rates the on

of speciation and extinction (Clarke St Crame 1997, 2003; St Jansson 2000; Jansson St Dynesius Dynesius 2002).
Finally, changes sufficiently speciation unlikely. Speciation is, however, is in also extinction important. with only one aspect of diversity; studies temperature of are the in evolutionary species' weaken in an area ranges the rates hypothesis assumes speciation between richness. the This do rate seems that not of following

generation

relationship thus involves

temperature of on first

correlation and species

disentangling

separate rate,

effects: and mutations

influence generation

temperature The

mutation generates

time.

process

(although
determines

these can be corrected),

whether these mutations

but
are

it is meiosis
transmitted

that
to the

extinction variation almost

Unfortunately, or latitude

next
tackled that

generation.
this mutation

Recently,
manner, rate is driven

Gillooly
starting directly over a decade

et al
with by

(2005)

have
rate,

non-existent.

in a formal

the premise

metabolic species earlier and

through radicals

the production (an idea proposed

of reactive

oxygen

free

4. TEMPERATURE AND METABOLIC NICHES

Recent relationship studies have revealed a previously unrecognized and the between environmental temperature

by Martin

(1995)).
predict rate and

Using
the temperature,

the metabolic
to be after

theory
expected

of ecology,
between mutation mass.

they
Data

relationship

correction

for body

niches, which is that the absolute diversity of metabolic and scope for activity (the difference between maximal
resting metabolic rates) temperature. scope resting 2a), ratio more follows because rate in ectotherms This of increases relative increases increased two factors; with with absolute the first environmental metabolic is that (figure (the remains

for four different

encompassed the

sections
predicted

of the mitochondrial
value, whereas data

genome
for the

nuclear

genome were equivocal (Gillooly et al 2005). In contrast, Held (2001) could detect no decrease in the rate
substitutions from for a warmer direct those crustaceans in polar compared waters. rates Any evolutionary link between temperature and

metabolic and the second

temperature scope rate)

of molecular with

is that

metabolic metabolic the

between or

hypothesis

and resting constant less

maximal across

physiological

Proc. R. Soc. B

(2006)

Climate, temperature
are more temperatures

energy and diversity

A. Clarke St K. J. Gaston

2263

range (Clarke 2003). This

energetic than ways at cold of making temperatures, a

implies that there

living and at warm hence a

ft?*
temperature----1--**

water

for higher diversity (Clarke 1993, potential opportunity under 2003; Clarke St. Johnston 1999). The mechanisms
pinning undoubtedly maintenance these relationships involve processes a are not balance and of yet a clear, between particular the they though costs of ecological

temperature

plant diversity

lifestyle
Data there for

(Clarke
resting

1993,
metabolism

2004;
range

Clarke
in teleost

& Fraser
fish

2004). herbivore diversity

is indeed

a wider

of metabolic

that suggest rates in warmer

than in colder fish (figure 2b), and this is coupled with a in particular, wider range of lifestyles; highly active
predatory lifestyles are found only in warmer water fish carnivore

(Clarke & Johnston 1996). Recently, Anderson St Jetz (2005) have shown a related the pattern for birds and mammals (figure 2c), whereby case rates field metabolic this of metabolic range rates) (in
is wider temperature, at lower and latitudes. their They link is thus this explanation pattern a version of to the

diversity
Figure processes arrows 3. A conceptual diagram that link energy supply of illustrate the transfer of the complexity showing to organism Solid diversity. with energy, photosyntheti as an open arrow and shown arrows. complex; and rate The influence of the it influences

benign
has

environment
that resting

radiation active (PAR) cally as shown chemical energy temperature and also the is all-pervasive

hypothesis.
metabolic

Lovegrove
rate tends

(2000,
to be

2003)
lower in

grey and

shown

rate of utilization
population hand side there processes animal is no

of energy (left-hand side of the diagram)

of water, This of mutation and abundance diagram hypothesis, of plant to diversity (right that emphasizes that different and diversity a complex

mammals
lower between related

from tropical habitats,

costs. and the The ectotherms directly to and strong

and this may be linked to

mechanism though rate. environmental thus differs are both

availability

thermoregulatory

endotherms, between

processes linking of the diagram). single underpin

correlation metabolic in that

environmental Nevertheless, tempera

temperature there are

resting parallels

species/energy the evolution and that

diversity,

temperature

has

ture
metabolic can

is affecting
rate and be supported. and

diversity
the We term that

through
range this the

its
of

influence
lifestyles

on
that niche by one

influence.

consequent

metabolic a mechanism

a source of energy in itself. This

figure There 3. is thus no single

is shown schematically
hypothesis,

in
but

hypothesis,

propose

this

affords

which

diversity may be linked positively

We and for and that emphasize we not do the widely that suggest observed temperature; of further it

to environmental
this is is the only complete between do, however,

species-energy is a fundamental in the nature

rather there is a suite of mechanisms

energy. between they further those affecting use, In particular, plants and progress, processes animal and the we that diversity. there animals role

linking diversity
distinction of the To energy make

to

temperature. mechanism, explanation diversity suggest

correlation we

environmental it is worthy

temperature. by played to distinguish need clearly influence We now plant have

between

exploration.

those and diversity an outline working

5. SUMMARY
The range of species-energy three different hypotheses meanings of in the energy, literature namely encompasses

PAR, Gibbs
compounds thermal and energy.

free energy
that comprise Temperature can energy their affect

retained
tissue is not be utilized and at which

in the reduced
(chemical energy, by biomass; organisms energy), and only

carbon
and PAR

of the control of plant diversity by a understanding combination of energy supply (PAR) and water dynamics, sufficient to be codified in an empirical model (O'Brien 1998; Field et ah 2005). The influence of plant diversity on
herbivore, there are and also thereby statistical factors on carnivore associations and animal diversity between diversity. means the that same

environmental and

chemical affect however,

Together

organisms temperature make

thereby does,

abundance the rate

use

of PAR and chemical

of molecular evolution.

energy, and itmay

influence

the rate

these provide the structure for the productivity advanced originally by Wright (1983), with individuals hypothesis providing the mechanistic
abundance carnivore are thus to diversity. diversity best viewed or the for using and as Associations abiotic between environmental and not We

hypothesis the more link from

or variations separate should as a in of

herbivore

of
with

Only plants can utilize PAR and this step is the source almost all fixed biological energy on the planet.
the diversity with of land plants of is correlated energy and not water energy, but a combination

epiphenomena, in environmental or chemical measures themselves.

However,

hypotheses abandon

mechanisms use of

temperature energy, of especially the form

availability. The
used to reduce C02

energy extracted
to the organic

from PAR by plants

compounds comprising nor

is

surrogate the sea,

radiation instead

direct

tissue, and this chemical

food web. In neither case

energy fuels all other levels of the

does the amount of energy,

energy that is hypothesized

not be easy, always in a position

to influence diversity. This

in the sea, but only then we the will true in understanding

is

the rate of its utilization,

increases increase dynamics ture plays biomass as and a key a and/or second-order speciation role in

affect diversity directly. Rather

abundance, effect processes. influencing and diversity may through population In all cases, tempera rates, though it is not

it

especially to make progress

relationship(s)
The ideas in

between
this the paper Santa

species diversity
were Fe first Institute October outlined and 2004.

and energy.
at the We a workshop for Centre thank Drew

organized Theoretical

by Studies

in Prague,

Proc. R. Soc. B

(2006)

2264
Allen paper tive

A. Clarke & K. J. Gaston

and on colleagues a related which for allowing

Climate,

energy and diversity

A. Clarke, radiation & Johnston, of Antarctic I. A. 1996 Evolution Trends Ecol. and adaptive Evol. 11, rate Ecol.

NER/O/S/2001/01257. comments

us sight of their unpublished and from NERC theme, support two referees We thank for construc improved the paper.

fishes.

212-218.
Clarke, with 68, A. &

(doi:10.1016/0169-5347(96)10029-X)

significantly

1999 Scaling N. M. of metabolic Johnston, mass and in teleost fish. temperature body J. Anim. 893-905. (doi:10.1046/j.l365-2656.1999.00337.x) D. plant D. J. 1991 species and large-scale Energy Am. Nat. richness. 137, patterns 27-49. of

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