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Basic and Applied Ecology 5 (2004) 435—448
www.elsevier.de/baae
Explaining the global biodiversity gradient: energy,
area, history and natural selection
John R.G. Turner
School of Biology, University of Leeds, Leeds LS2 9JT, England, UK
KEYWORDS
Climate change;
Neutral theory;
Species-energy
theory;
Speciation rate;
Metacommunity;
Topography;
Ecological niche;
Competition;
Extinction;
Latitude
Summary
Hubbell’s neutral theory of biodiversity is used to investigate the decline in species
richness from the tropics to the poles. On this basis, biodiversity should correlate with
productivity or climate (there is strong statistical evidence for this), with the
latitudinal width of the continents (insufficiently investigated as yet), and with the
speciation rate (which may not vary in such a way as to produce a planetary gradient).
According to the neutral, model biodiversity will vary with the area of the
‘‘metacommunity’’: it is suggested that at higher latitudes species disperse most
readily east–west, within their climatic belt, but that the relatively uniform
temperature across the intertropical belt allows isotropic dispersal there. Metacommunities within the tropics may therefore be an order of magnitude larger than those
at other latitudes. This could explain the extra bulge in the gradient in the tropics. It
is further possible that long-term and cyclical climate change generates a tropic-pole
gradient. Niche assembly models will also explain tropical biodiversity, but the
enhanced division of habitat may be the result, not the cause, of the species richness.
The neutrality–competition debate in ecology closely parallels the neutrality–natural
selection debate in evolution and may be equally hard to resolve.
& 2004 Elsevier GmbH. All rights reserved.
Zusammenfassung
Hubbells neutrale Theorie der Biodiversität wird genutzt um den Rückgang des
Artenreichtums von den Tropen zu den Polen zu untersuchen. Auf dieser Basis sollte
die Biodiversität mit der Produktivität oder dem Klima (es gibt überzeugende
statistische Beweise dafür) korrelieren, mit der Ausdehnung der Kontinente in
geografischer Breite (bisher unzureichend untersucht) und mit der Artbildungsrate
(welche möglicherweise nicht in der Weise variiert, als dass sie einen planetarischen
Gradienten erzeugen kann).
Dem neutralen Model entsprechend wird die Biodiversität mit dem Areal der
‘‘Metagemeinschaft’’ variieren. Es wird behauptet, dass sich Arten in höheren Breiten
Tel.: +44-113-343-2828; fax: +44-113-343-2835.
E-mail address: [email protected] (J.R.G. Turner).
1439-1791/$ - see front matter & 2004 Elsevier GmbH. All rights reserved.
doi:10.1016/j.baae.2004.08.004
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J.R.G. Turner
am leichtesten innerhalb ihres klimatischen Gürtels in Ost–West-Richtung ausbreiten,
dass aber die relativ gleichmäXige Temperatur des innertropischen Gürtels dort eine
isotrope Ausbreitung erlaubt.
Metagemeinschaften in den Tropen können daher um eine GröXenordnung gröXer
sein als in anderen Breiten. Dies könnte die zusätzliche Ausdehnung des Gradienten in
den Tropen erklären. Es ist darüber hinaus möglich, dass langfristige und zyklische
Klimaveränderungen einen Gradienten von den Tropen zu den Polen generieren.
Modelle der Nischenanordnung erklären ebenfalls tropische Biodiversität. Die
verstärkte Habitataufteilung könnte jedoch das Ergebnis und nicht der Grund des
Artenreichtums sein. Die Neutralitäts–Konkurrenz-Debatte in der Ökologie ähnelt sehr
der Neutralitäts–Selektions-Debatte in der Evolution und mag ähnlich schwer zu lösen
sein.
& 2004 Elsevier GmbH. All rights reserved.
Introduction
The observation that the tropics hold more species
than higher latitudes (Fig. 1), stemming from
Forster and Humboldt in the late eighteenth
century, is probably the oldest observed ecological
pattern (Forster, 1778; Hawkins, 2001; Gould,
2002a; Hillebrand, 2004). Talking to colleagues
over the last 20 years, I have found widespread
agreement that we understand the cause of this
planetary biodiversity gradient. The vigorous disagreement is over which of the many postulated
causes are actually responsible (for reviews, see
Pianka, 1966; Rohde, 1992; Huston, 1994; Rosenzweig, 1995; Turner, Lennon, & Greenwood, 1996;
Willig, Kaufman, & Stevens, 2003; Whittaker,
Willis, & Field, 2003). What follows is a critical
analysis of some of them. It is based on the premise
that to be a potentially valid explanation a theory
must be ‘‘dynamically sufficient’’: it should show
how the factor(s) thought to control the gradient
influence species richness through the fundamental
processes of species birth (speciation), species
death (global extinction), and species migration
Figure 1. The biodiversity gradient, exemplified by the
species richness of birds, in a random sample of 206
quadrats of 48,400 km2 on five continents. The dashed
lines are the two Tropics. From Turner and Hawkins
(2004), data from Hawkins et al. (2003a).
(expansion of range and local extinction). Thus the
popular theory that higher latitudes are species
poor because species that were displaced to lower
latitudes by glaciation have not all yet returned to
their original latitude is dynamically sufficient;
statements that there are more species at low
latitudes because it is warmer, or because ecological niches are narrower, are not in themselves
dynamically sufficient. I will argue that a dynamic
theory working ‘‘bottom up’’ from Hubbell’s neutral theory (Hubbell, 2001) provides a very satisfying way of considering the various candidate
mechanisms and suggests novel ways of testing
some of them. I will also suggest an explanation for
the marked and rather surprising ‘‘shoulders’’ of
the gradient (Fig. 1), a pattern seen also in other
groups (e.g. Clarke & Crame, 2003).
Striping the planet
We commence with a suggestion of Terborgh (1973)
and Rosenzweig (1992, 1995) that we should
consider the area of the whole planet, or more
particularly the area of a latitudinal zone. They
pointed out that tropical diversity could at least in
part be explained by the greater area of the
tropical belt, compared with other latitude belts
of analogous depth, first because the north and
south tropical belts are joined at the equator
whereas other analogous belts are separated by the
tropics, and second because the planet is wider at
the equator than at the poles (Fig. 2a). There is
however a lightly concealed further assumption in
this argument, that there is something non-arbitrary about latitude. It is easy enough to see this by
drawing the belts in another way, based on the
Greenwich meridian (or any other great circle) and
predicting a zone of greatly enhanced biodiversity
from Cape Town to Reykjavik, with species-poor
areas in Java and Ecuador (Fig. 2b).
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437
Figure 2. Planetary area and biodiversity. (a) High latitudes have smaller areas than the tropics, a smaller overall
regional diversity, and a smaller local diversity (circles represent species). (b) If the difference in local diversity is
purely the result of area, then we can also predict that meridians, and other great circles, should produce bands of high
diversity, and that their ‘‘poles’’ should have low diversity.
Instinctively, one knows that this reductio ad
absurdum contains a fallacy, involving latitude,
climate, and the distribution of biomes (Blackburn
& Gaston, 1997; Ruggiero, 1999; Hawkins & Porter,
2001). The trouble is that biomes are defined by
morphology: the fact that a tropical forest has
much the same physiognomy in Indonesia as in
Amazonia cannot be fed into a dynamically sufficient model that depends on the birth and death
rates of species. The privileging of latitude has to
arise from the way species, not organism morphologies, are distributed. Turner and Hawkins (2004)
suggest that the diffusion of species is more rapid
east–west than north–south. It is a commonplace of
horticulture and agriculture that plants can be
successfully moved across the planet within their
climatic belt (between for instance temperate
China, North America, Chile and Europe) but only
with great difficulty and under artificial climate
control between different belts (arctic alpines and
tropical species have to be grown under glass in
temperate climates). This fact was well known to
mediaeval herbalists and is even used as a
metaphor in the Paradiso (canto viii) in the fourteenth century (translation by Sinclair, 1939).
Other environmental factors change, on average,
isotropically; thus they resist range expansion
equally to all points of the compass, while climatic
temperature — and less clearly rainfall — will stripe
the planet because alone of all factors it has a
strong north–south gradient. Further, it is plausible
that the major factor limiting the distribution of
individual species is indeed the climate, as shown
by the success of climatic envelopes in describing
the limits of distribution (Woodward & Kelly, 2003),
or the fact that the environmental factors with the
strongest influence on the presence or absence of
individual species of British birds are climatic, with
both winter rainfall and summer temperature being
strongly directional (Lennon, Greenwood, & Turner,
2000).
The neutral theory of biodiversity
The Unified Neutral Theory of Biodiversity (Hubbell, 2001) makes an elementary (in the mathematical sense) statement of the problem, how does
diversity relate to birth, death and migration? The
null assumptions are that although individuals
compete, species are all identical in competitive
ability and in individual life expectancy. If they are
plants, they completely cover the ground, so that
gaps appear only with the death of individuals.
These gaps are then colonised by propagules chosen
randomly from all the species in the ‘‘community’’
(defined as the population within the dispersal
distance of individual propagules). There is thus a
continual random replacement of individuals,
resulting in steady ‘‘ecological drift’’ toward the
eventual random extinction of all but one of the
species. Species diversity will be maintained at a
dynamic equilibrium between this loss of species by
drift and the birth of new species (in the simplest
form of the theory, by chromosomal or genetic
mutation) (see Maurer & McGill, 2004, for a further
exposition).
A group of communities which can exchange
individual migrants in the long term is now defined
as a ‘‘metacommunity’’. The simplest case is an
archipelago with each island being a constituent
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J.R.G. Turner
community. A species that has originated in one
community may thus enter a different community,
and a locally extinct species may eventually
reappear. The equilibrium between the loss of
species by ecological drift and their creation by
speciation, is then described by
y ¼ 2JN n;
(1)
y ¼ 2rAn;
(2)
where y is the ‘‘fundamental biodiversity number’’,
JN is the total number of individuals (irrespective of
species) in the metacommunity, n is the rate of
speciation, r is the population density (the number
of individuals per unit area of all species combined), and A is the area occupied by the
metacommunity.
The fundamental biodiversity number is a dimensionless variable incapable of direct physical
representation. It can be used to predict such
things as the species-abundance curve and, to our
purpose, the species richness. This last calculation,
which is algorithmic, depends on three further
factors: the time of search or observation, the area
sampled, and the rate of migration between
communities, which governs the form of the
species–area curve (Hubbell, 2001). The first two
are purely matters of sampling, but the third is
clearly a relevant biological parameter. As a first
approximation, we can think of y as highly
correlated with species richness, and note that
Hubbell’s theorem predicts that species richness
will therefore be proportional to overall population
density, the area of the metacommunity, and the
speciation rate, with a further modulation arising
from the rate of long-term species migration
between communities. In turn, the overall density
of organisms is likely to be dependent on productivity, along with various modifying influences. All
these factors may change over the very large scales
that are needed to produce planetary gradients in
biodiversity.
Productivity and climate
The idea that climate, in particular its energetic
elements, influences biodiversity, first proposed by
Forster and Humboldt, surfaced again in the late
twentieth century (Hutchinson, 1959; Brown, 1981;
Wright, 1983; Turner, 1986; Turner, Gatehouse, &
Corey, 1987; Currie & Paquin, 1987). Slightly
misleadingly this is known as the ‘‘species-energy’’
theory. The proposal is simple: productivity and
temperature are likely to be major influences on
the number of organisms and hence on the
equilibrium number of species (Eqs. (1) and (2)).
In a meta-analysis of terrestrial biodiversity
gradients extending over a minimum 800 km linear
distance (small-scale studies were excluded), Hawkins et al. (2003b) found that in 82 of 85 studies the
leading explanatory variable was some measure of
productivity, water availability, or energy. This
accounted for an average of over 60% of the
variance in diversity. Similar results are found in
marine environments (Turner & Hawkins, 2004).
Naturally, a variety of other factors also explain
significant parts of the variance. Both these metaanalyses are deliberately biased, in that studies
which had not entered climatic factors into the
initial variable set were excluded: the point is that
when these factors are included, they overwhelmingly remain among the significant factors, and
then overwhelmingly explain the lion’s share of the
variance. This is consistent with the predictions of
the neutral theory.
Further detailed correlations lend support to the
belief that the relationship between climate and
species richness may be relatively direct. Thus the
species-energy hypothesis comes in two forms, only
recently recognised as distinct. The better-known
productivity hypothesis (Wright, 1983) claims that
the rate of energy fixation by photosynthesis
governs the growth, performance and hence
diversity of plants, then of herbivores, and so of
all the further links in the food chain. Biodiversity
can then be predicted by a combined water-energy
model (O’Brien, 1998), supported by the empirical
correlation of species richness with AET (Whittaker
et al., 2003). The ambient energy hypothesis
(Turner, 1986; Turner et al., 1987) suggests that
diversity is controlled directly by the effect of
climate on the individual organism. The reproduction and feeding of ectotherms is more efficient
when it is warm and sunny, and much the same is
true of endotherms: when it is cold they have to
burn energy to maintain their body temperature; in
warm weather more of this energy is put to other
uses such as reproduction (Turner, Lennon, &
Lawrenson, 1988; Currie, 1991). Both hypotheses
seem to be correct, depending on the latitude:
productivity, water availability, or such combined
measures of water and energy as AET give the best
predictions of biodiversity at low latitudes,
whereas direct measures of energy, such as
temperature or PET are the best at high latitudes;
the changeover, which can be mapped for butterflies and for birds in the northern hemisphere, is
around 501 (Hawkins et al., 2003b). This is
consistent with what we know of ecophysiology:
at low latitudes biological activity is limited by the
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Explaining the global biodiversity gradient
water supply, in the midst of plentiful energy. At
high latitudes temperature, especially in the
winter, limits activity, and in general there is no
critical shortage of water.
Further, among endotherms at high latitudes the
lightest species should be most sensitive to temperature (on account of surface-volume ratios),
and if the ambient energy theory is correct
migrating birds should show correlations only
with the appropriate seasons. In Britain, there is
some evidence that indeed the species richness of
winter visitors depends directly on winter temperature, of summer visitors less certainly on
summer (but not on winter) temperature, and of
year round residents on both seasons, but this
effect is detectable only among the lightest birds
(Turner et al., 1988); it cannot be found clearly
among heavier birds, or in the set of all weights
combined (Turner et al., 1996; Lennon et al.,
2000). Further, birds in winter are able to withstand
night temperatures well below freezing, provided
they can build up enough fat during the day to
maintain their body temperature during their
night-long fast (Newton, 1969). They are therefore
dependent on a food supply which is mostly the
result of summer productivity, banked in winter as
seeds or diapausing invertebrates. There is indeed
a correlation between the diversity of birds in
winter and the summer temperature; even winter
visitors, which never experience a British summer,
show this relationship (Turner et al., 1996; Lennon
et al., 2000).
Such direct physiological explanations are
strongly suggestive of a direct casual link between
climate and biodiversity, but indirect links are
also possible. It is strictly shown only that
species are adapted to the climate at their
native latitude and that there is some mechanism
which ensures that the number of species
adapted to a particular climatic regime is strongly
related to its energy (Turner, 1986). The mechanism
which generates such a correlation may or may
not be the link postulated in the neutral theory.
There is indeed a curious anomaly in this part
of the theory. Biodiversity is predicted to increase
with the number of individuals, or, factoring
out area, with population density. But it is an
axiom of the theory itself that the habitat is
permanently saturated with individuals, and that
therefore their overall density cannot change. If
we avoid this by assuming that there are at all
times unoccupied gaps in the environment, then
the rate of species replacement through ecological
drift is reduced (Huston, 1979). This is a problem
that requires resolution within the neutral model
itself.
439
Area
Area has a venerable history as an explicator of
biodiversity, commencing with Forster (1778), then
Arrhenius (1921), MacArthur and Wilson (1967),
Terborgh (1973), and Rosenzweig (1995). The
neutral theory explains explicitly how it exercises
this influence: species richness should be proportional to the area of the metacommunity (Eq. (2)).
This is defined as the distance over which a species
can spread from its point of origin before it
becomes extinct or speciates. If we accept that
dispersal is predominantly east–west, this could be
the full width of a band across the continental
landmass or the watermass, taken at the latitude of
the sample point. As we have no idea how deep to
make this transect, the best mathematical approximation will be simply the infinitesimal area
represented by the width (Turner & Hawkins,
2004). Clearly for any group in which the metacommunity is actually narrower than the landmass,
there should be no diversity–width correlation, but
otherwise neutral theory predicts a direct correlation between landmass width and the species
richness. Because a centrally placed community
receives species both from the east and the west,
its metacommunity size is greater than that of a
community located on the coast: it should therefore be possible to detect a form of mid-domain
effect (Colwell & Lees, 2000), with diversity
dropping somewhat near the east and west coasts.
Several studies have examined area alongside
climate. Wright’s classic study of world islands did
find a joint correlation of richness with climate and
land area (Wright, 1983), but as the richness was
measured from the whole island, not from a sample
quadrat, the sample area is confounded with the
metapopulation area, which may itself be smaller
or greater than the island, according to its size and
isolation. The same problem occurs in the studies of
Wylie and Currie (1993) on islands, and of Oberdorff, Hugueny, and Guégan (1995, 1997) on river
basins. To confirm the relationship predicted by the
neutral theory, it is necessary to keep the sample
area constant, and then to put an estimate of the
continental area into the multivariate analysis
(Rosenzweig, 2003). In the only study of this type,
the peninsular width of Great Britain, clearly far
too small a scale of measurement, was not a
significant predictor for birds (Turner et al., 1988).
There is one tantalisingly suggestive near-miss: it is
known that the latitude gradient of mammal
diversity in North America is strongly related to
productivity (Badgley & Fox, 2000), and the same is
likely to be true of South America. When the
gradients of North and South America are corrected
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440
for the latitudinal width of these continents, the
gradients become the same (Kaufman, 1995).
Otherwise, simultaneous analysis of area along
with climate has been singularly rare, with climate
studies omitting area (e.g. Lennon et al., 2000),
and area studies omitting climate (e.g. Blackburn &
Gaston, 1997).
In the few studies that have investigated diversity world wide, for the very well-known groups
such as birds, flowering plants and freshwater fish,
it is found that the continents tend to have their
own characteristic levels of diversity, independently of productivity (Adams & Woodward, 1989;
Oberdorff et al., 1995; Hawkins, Diniz-Filho, &
Porter 2003a). One telling study allows us to relate
this, in an elementary way, to area: among related
groups of vascular plants in North America and the
adjacent parts of eastern Eurasia, the Asian plants
are shown to have a higher species richness than
their North American counterparts (Qian & Ricklefs,
1999). This could well be the result of the much
greater latitudinal width of Eurasia compared with
North America. But area by itself cannot explain
the planetary gradient, at least for terrestrial
species, as the continental masses (except for
Africa and America in the southern hemisphere) do
not taper in the requisite way, and in the northern
hemisphere there is a dramatic increase in area
north of the Aleutian islands, where Eurasia and
North America become effectively a single land
mass (Rohde, 1998; Turner & Hawkins, 2004).
It is a fair proposition that the climatic gradient
produces the planetary diversity gradient, and that
the characteristic gradient and overall diversity of
each continent is produced by an effect of its area
and shape (Rosenzweig, 2003).
J.R.G. Turner
see this by considering the angle of the incident
radiation at the equinox). At this level, climate and
area are strictly colinear, raising the prospect that
the species-energy correlation is the secondary
outcome of a species–area relationship. The colinearity is however reduced (as well as by the
irregular shapes of the land masses) by the
transport of heat toward the poles by the oceans
and atmosphere, greatly raising the arctic temperature and converting the cosine curve to an
effectively linear gradient from the Tropics of
Capricorn or Cancer toward the polar regions. This
gradient has a rather flat top between the two
Tropics, produced at least for non-arid areas by the
increased cloudiness around the equator (Fig. 3)
(Terborgh, 1973; Rosenzweig, 2003). Much the
same flat topped gradient is shown by ocean
surface temperature. The shape of this graph,
whether a cosine curve or flat, has a profound
effect on our estimate of the area of the
metacommunity at tropical latitudes.
It is easiest to see this if we rescale temperature
so that, on average, between Tropic and Pole the
temperature reduces by 11 for every degree of
latitude (Fahrenheit approximates this). A temperate species which through physiological, behavioural and genetic adaptation can occupy a range
of say 101 above and below the temperature at its
latitude of origin, is confined to a belt 201 deep in
one or other hemisphere. The latitudinal range of
Interaction of climate and area
It is possible, given a long enough time span, that
the whole latitudinal width of the planet could
appear as a factor in the dynamics of biodiversity:
for mammals, birds and flowering plants on land
bridge islands, world-wide, after the energy and
the area of the local island are taken into account,
there remains a small residual correlation of
diversity with latitude itself (Wylie & Currie,
1993). The appropriate test would be a regression
not on latitude but on the cosine of the degrees of
latitude, which is an elementary function for
latitudinal circumference. But by the same elementary trigonometry, the flux of energy reaching
the earth, per unit area of surface, also declines
directly with the cosine of latitude (it is easiest to
Figure 3. An explanation of higher tropical diversity. The
graph shows the general shape of the planetary temperature gradient: flat within the tropics (dashed lines)
and linear at higher latitudes (based on Terborgh, 1973;
Rosenzweig, 2003). The shaded areas represent two
species with an equal range of temperature tolerance:
the tropical species has a much greater latitudinal range
than the temperate species. This greatly increases the
relative area of metacommunities in the tropics.
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Explaining the global biodiversity gradient
widespread bird species in Eurasia appears to be
around 201 (Harrison, 1982). Because of the
flattened gradient of temperature within the
tropics, an analogous tropical species potentially
occupies the whole of the tropical zone, plus
subtropical belts 101 to the north and the south, a
distribution of a startling 661 of latitude (Fig. 3).
The butterfly Heliconius erato spans nearly 601
between Buenos Aeres and Sinaloa (Turner, 1971).
The neutral theory thus throws into sharp relief
Terborgh’s (1973) suggestion that the effective area
of the tropics is greater by an order of magnitude
than that of other latitude belts of comparable
depth. Thus with recolonisation occurring predominately east–west, the metacommunity at high
latitudes has an area largely dependent on the
width of the land or oceanic mass; recolonisation
within the tropics is isotropic, meaning that the
whole intertropical area of land or water has prima
facie to be accounted as the area of the metacommunity. In this great effective area of the
tropics we have a good explanation for the peculiar
shape of the diversity gradient in Fig. 1: that it is
linear at the higher latitudes, but with a pronounced hump between the two Tropics.
How to fit this consideration into a multivariate
investigation is a puzzle. What we need to know is
roughly the depth of a metacommunity, and hence
the potential temperature-range tolerance, of
species at higher latitudes, and then their potential
latitude range in the intertropical region. These
factors could then be used to estimate land or
ocean area in the tropics and in other latitude
belts. It would also be valuable to split studies of
diversity in relation to area and climate into
separate analyses of the relationship inside and
outside the intertropical zone. The barriers to
distribution created by the subtropical arid zones
are likely to confuse the analysis.
441
far from clear whether it might produce the
latitudinal gradient.
Speciation might be higher in the tropics because
in warmer climates generation times are shorter,
leading to faster evolution of all sorts, including
speciation (Rohde, 1992). It is also likely that sister
species originating in allopatry, become sympatric
only after their niches have become somewhat
different, usually by becoming narrower: shorter
generation times and more rapid evolution will
result simultaneously in both greater per area
diversity and narrower ecological niches. However
the neutral equilibrium depends on a balance
between speciation and extinction measured on
the same time scale, and as extinction by
drift depends on the death of individuals, it follows
that its rate is governed by the generation time,
not by absolute time. As speciation must also be
reckoned per generation, the effect of shortening
generations at higher temperatures will be cancelled out, and warmer climates will not be more
species-rich.
There is therefore a need for theories which
suggest how speciation and extinction might
operate on different time-bases. Dynesius and
Jansson (2000) modelled a difference in the rate
of allopatric speciation: at high latitudes, species
are selected not only to be ecological generalists,
but to have high individual vagility, so restricting
the possibilities for isolation. Alternatively, if
environmental fluctuation is responsible for extinction, then this will cause the extinction rate to be
measured in absolute time, so that other things
being equal shorter generation times would alter
the equilibrium between extinction and speciation
in favour of greater diversity in the tropics.
Topographic relief
Speciation rate
There is little doubt that speciation rate influences
species richness, a prediction made, if not uniquely, by the neutral theory. If speciation is not by
point mutation but by allopatric fission or the
budding of peripheral populations, the mathematical solution (Eqs. (1 and 2)) becomes more
complex and algorithmic, but the principle remains
(Hubbell & Lake, 2003). But while variation in
speciation rate must surely influence the diversity
of different taxa and possibly of different continents (different topography and history giving
different rates of allopatry — McGlone, 1996), it is
An apparent effect of allopatric speciation rate on
large-scale species richness patterns is the repeatedly found correlation between richness and
‘‘relief’’, usually measured as the range of elevation: it has long been known that crinkly areas of
the planet have more species (Humboldt in Gould,
2002a; Simpson, 1964; Richerson & Lum, 1980;
Badgley & Fox, 2000; O’Brien, Field, & Whittaker,
2000; Hawkins & Porter, 2003a; Hawkins et al.,
2003a). This is readily explained as a consequence
of the argument so far.
During climatic fluctuations, montane species
must be repeatedly forced up and down the
mountain ranges, splitting into allopatric populations on separate peaks, and then becoming
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442
sympatric again in warm periods (Hewitt, 1996).
Additionally, mountainous areas contain many
climatic zones, thus compressing what are in effect
different latitudinal biota into one quadrat; north
and south facing slopes, because of differences in
direct solar heating on the microclimate, have
biota that on a planar surface would be several
hundred kilometres to the north and south (thus
again compressing several zones into one quadrat);
mountains allow shorter distance migration when
climate changes; and a crinkly quadrat has a
greater real area than a planar one (a 451 average
slope increases the area by 40%), producing an
apparently greater richness as an artefact of
drawing quadrats with a constant map area
(O’Brien et al., 2000; Whittaker et al., 2003;
Turner & Hawkins, 2004). However, in the reverse
direction, mountain ranges are also sinks for
species extinction during periods of warming. The
finding (Rahbek & Graves, 2001; Turner & Hawkins,
2004) that the correlation between richness and
relief is strong at low latitudes and is not
detectable at high latitudes, supports both of the
first two suggestions. First, allopatric speciation
will tend to be ineffective at high latitudes because
the biota are not so much moved up and down by
glaciations, as removed altogether. Second, the
compression of climatic belts will be less at high
latitudes: tropical mountains embrace rain forest
to permanent snow, Alaskan mountains embrace
tundra to permanent snow, and Antarctic mountains are just permanent snow. Conversely, as the
north–south slope effect cannot occur at the
equator, this explanation would lead to topography
having an increased effect on diversity at higher
latitudes, which is the reverse of what is observed.
If this factor operates, it must be weaker than the
others. Because the effect of relief is to increase
diversity at low latitudes by introducing highlatitude species, it is vital to factor out relief in
multivariate analyses.
Migration within the metacommunity
While y is expected to correlate strongly with the
three factors of Eq. (2), the species richness will
further depend on the area and time-duration
sampled, and on the rate of migration within the
metacommunity (via the form of the species–area
relationship and the rate of sympatry) (Hubbell,
2001). It is too early to say whether variation in this
last factor does or might contribute to the
planetary gradient in species richness. The latitudinal pattern of diversity does change with quadrat
J.R.G. Turner
size in British birds (Lennon, Koleff, Greenwood, &
Gaston, 2001; Koleff & Gaston, 2002), but the
fundamental power parameter of the species–area
curve explains very little of the variation in the
diversity of neotropical owls (Diniz-Filho, Rangel, &
Hawkins, 2004).
Migration between zones
Migration between zones happens in two different,
but readily confused ways: first a species may
spread into a new climatic zone, and hence into a
new latitude belt; second, the climate zones may
change their positions, taking all or some of the
species with them into new latitudes.
Even if dispersal is mainly east–west, there must
over time be some leakage or ‘‘bleeding’’ from one
climatic belt to another as species adapt and spread
to new regimes (Rosenzweig, 2003). If the direction
of this leakage is biased, it will produce a latitudinal
diversity gradient, in one direction or the other.
There seems to be no conclusive information on this
point. Sax (2001) showed that successful aliens tend
to expand their ranges more toward the poles than
to the tropics compared with their native range, but
any recent data on species spread is necessarily
confounded by the effects of global warming:
species are currently spreading north but not south
(Parmesan et al., 1999). It has reasonably been
suggested that tolerance to frost or to supercooling
requires abnormal levels of adaptational change
(perhaps in many genes simultaneously), so that
spread poleward is inhibited in the long term
(Latham & Ricklefs, 1993); in that case we might
expect the ‘‘shoulders’’ of the gradient to be
further away from the tropics than is observed
(Fig. 1). Further, we do not know how few gene
changes may be required to produce antifreeze, and
it is possible that it is just as hard for a high-latitude
species to spread to warmer climates, for instance
by abandoning diapause. We do not therefore know
whether bias in leakage is expected to produce a
gradient toward or away from the tropics.
Equal migration in both directions clearly will not
produce a gradient, but will tend to reduce the
angle of any gradient produced by other factors.
There are two interesting consequences. If the
tropics have, for any reason whatsoever, a greater
diversity, then the majority of species and of clades
on the planet, at all latitudes, will be found to have
originated in the tropics, as indeed is widely
believed by evolutionary biologists (Jablonski,
1993). Proving that the tropics are the powerhouse
of evolution thus tells us nothing of the mechanism
ARTICLE IN PRESS
Explaining the global biodiversity gradient
behind the diversity gradient. However, suppose
that area alone generates the latitudinal gradient
(‘‘interaction of climate and area’’ above) with no
further input from climate. In northern hemisphere
America we could expect to see a shouldered
gradient with a huge bulge of species in the tropics,
like that in Fig. 1, but then with a roughly constant
level of diversity, irrespective of latitude, right up
to the arctic. The effect of leakage will then be to
smooth the gradient by a net pouring of species out
of the tropics, and if such species become randomly
extinct on the way, this will give the gently sloping
gradient we observe from the Tropic of Cancer
toward the pole — the ‘‘tropical overspill’’ effect of
Rosenzweig (1992). As a result, there will be a
diffusion gradient of species closely paralleling the
diffusion gradient of heat energy, and in temperate
latitudes there will be a clear correlation between
diversity and climate produced simply by the
coincidence of the two gradients. Prima facie the
whole pattern can be explained by climate, area,
and overspill.
These results are considerably modified if there
are long-term changes in the climatic gradients. It
is widely believed that the northern latitudes of
Europe are still below equilibrium because species
displaced by the most recent glaciation have not
yet returned. This must mean, if they are not
extinct or prevented from occupying their climatic
envelope, that they still occupy climatic refuges at
low latitudes. This could indeed apply to those
alpine species which are absent in the arctic, and
could be tested by comparing their numbers with
those of arctic species which are not present in the
low-latitude mountains. If mutualism increases
species richness (below), then previously glaciated
areas will be poorer because whereas an independent species may readily colonise an empty
habitat, species bound together by mutualism can
only arrive when they migrate together (the
‘‘maturation’’ of ecosystems — McGlone, 1996;
Rohde, 1998). If the narrowing of niches (below)
and the evolution of mutualism are by slow
evolution, then perhaps the relatively young biota
of high latitudes simply have not had enough time
to reach equilibrium. However, multivariate analyses usually reject ‘‘glaciated versus non-glaciated’’ or even ‘‘time ice-free’’ as a significant
influence on species richness (Currie & Paquin,
1987; Turner et al., 1988; Adams & Woodward,
1989; Latham & Ricklefs, 1993; Oberdorff et al.,
1997; Francis & Currie, 1998; Ricklefs, Latham, &
Qian, 1999). Exceptionally, in North America time
ice-free does account for a significant minority of
the variance of mammal and bird diversity (Hawkins & Porter, 2003c).
443
More generally, it seems likely that during
periods of rapid climatic change, such as have
accompanied both the advance and the retreat of
the ice caps, many species become globally extinct
because they fail to change their range to match
the moving climate, an effect now predicted during
the present climatic warm-up (Thomas et al.,
2004). Provided that the climatic change is of
lower effective amplitude at lower latitudes, this
will have the effect of reducing biodiversity at high
latitudes. In the longer term, the planet has cooled
fairly steadily since the beginning of the Eocene
(Clarke & Crame, 2003). Particularly if there is an
evolutionary stalling point in developing resistance
to frost, it may be that the steepening of the
climate gradient which probably accompanied the
cooling has selectively exterminated species and
clades at higher latitudes, and that adaptation and
then speciation have not yet brought the biodiversity of these latitudes back to equilibrium (Latham
& Ricklefs, 1993). Effectively the high latitudes are
new habitats, and their age is colinear with their
temperature.
Habitats
Habitat diversity correlates with species richness,
as shown for both birds and butterflies by using
landcover classes derived from satellite scans
(Lennon et al., 2000; Kerr, Southwood, & Cihlar,
2001). This may be a tautology (Turner & Hawkins,
2004). If a ‘‘habitat’’ is the subvolume of ecological
space occupied by a species, then the number of
habitats, correctly observed, would exactly equal
the number of species. The empirical correlation of
less than 100% tells us only the relative lack of
success our satellites have had in identifying the
components of the real habitats. The empirical
correlation tells us nothing about the maintenance
of species richness.
Commencing with the neutral theory suggests a
more interesting conclusion. If we assume that the
ground is occupied by two separate but equal
communities of species, each with completely
different ecological requirements, then the members of community A can never colonise a gap in
community B, and vice versa (it is easiest to
imagine an area occupied by a mixture of land
and water). If the total number of individuals per
unit area is the same as in the simple case, the rate
of loss of species by ecological drift will be
reduced. However, this does not lead to any change
in biodiversity. If the whole environment is divided
into the two equal exclusive metacommunities,
then the number of individuals in each is half of
ARTICLE IN PRESS
444
what it would be in a unified metacommunity, so
that from Eq. (1) the value of y for each is halved.
However, the total value of y for the area sampled
is the sum of the individual community values,
which is exactly what one would get in an undivided
habitat (say ytotal=ya+yb=2Jan+2Jbn=2n(Ja+Jb)=2JNn,
where a and b denote the separate communities).
Thus under neutral theory, division of the environment into exclusive (or of course partly exclusive)
habitats will not increase the sampled biodiversity.
I will qualify this conclusion later.
It is a common assertion that some types of
habitat are richer in species. This clearly does
account for small- to medium-scale patterns in
species richness: Lennon et al. (2000) confirmed
that bird species richness in summer was higher in
woodland, and lower in urban areas and ploughed
land, which is not surprising as agricultural land in
Britain is a partial wildlife desert. In winter, the
effect of urban areas was reversed: town gardens
are a substantial source of food for birds (Toms,
2003). How far particular natural habitat types, as
ordinated by us, may be richer or poorer in species
is an interesting question in itself, and may explain
finer-scale patterns of richness. The differences
between structurally complex and structurally
simple habitats could be subsumed into a question
of area: at most body sizes, the relevant fractal
area of the surface of a woodland is considerably
greater than the surface area of a grassland.
Niche assembly
The old version of the dynamic theory, the
equilibrium theory of island biogeography, which
underlay the original species-energy theory (Turner
et al., 1996), had no means of incorporating
competition. One of the outstanding advances of
the neutral theory is that competition — equal
between all species — is directly incorporated
(Hubbell & Lake, 2003). Hence the above finding
that diversity is invariant with subdivision into
exclusive habitats changes completely if competition is unequal between species. Take the limiting
case that in any one community there is one
particular species which invariably out-competes
all others. In an undivided environment there is
eventually only that one species. In an environment
divided into exclusive habitats, in which species
cannot be out-competed by species from the other
habitats, there will be as many species as there are
habitats (or fewer if exclusion is only partial). This
is an important result in showing that unequal
competition causes habitat division to increase
species richness.
J.R.G. Turner
This theorem produces immediately a dynamic
basis for the common belief that if ecological
niches are narrower, more species can be packed
into the resource hyperspace. In general, reduced
competition (provided it is unequal), either by
increased specialisation or by intermediate levels
of disturbance (Huston, 1979), as well as by
increased mutualism, will increase species richness
above the neutral expectation. Although hard to
quantify, it does indeed seem to be the case that
species in the tropics show more ecological
specialisation and more mutualism. What the
theorem does not explain is how it comes about
that tropical organisms divide their environment in
this way more than species at higher latitudes. It
could be that the division is the consequence, not
the cause, of the increased richness (Turner et al.,
1996). As the ratio of species to individuals
increases, there is a hyperbolic increase in the
proportion of interactions that are interspecific —
in neutral theory this proportion is 1(y+1)1 (see
e.g. Maynard Smith, 1989, p. 146) — and therefore
in the strength of natural selection in favour of
avoiding interspecific competition.
Extinction risk is affected not merely by mean
population size but, more, by minimum population
size. If the coefficient of variation in population
size over time is lower in the tropics, or if the
relevant environmental fluctuations are less frequent, then species with the same mean population
size are at higher risk of extinction at high than at
low latitudes. Thus a high-ranking species in the
tropics has a larger population size — and lower
extinction risk — than a species of the same rank at
high latitude, and the distribution of species
abundances becomes fatter in the tail in the
tropics. This accords with the observation that
tropical biomes tend to be less dominated by their
commonest species than are high-latitude biomes,
thus deviating significantly from the distribution
predicted by the neutral theory (Hubbell & Lake,
2003). This model therefore generates not only
higher species richness in the tropics and the
reduction in single species dominance, but the
narrowing of ecological niches. Thus suppose that
there are five host plant species, whose population
fluctuations over time are relatively uncorrelated.
One polyphagous and five monophagous species
depend on the five hosts. Clearly, in a fluctuating
environment the monophagous species are at a
higher risk of extinction than the generalist. If, as is
widely believed, the high latitudes have environmental fluctuations of greater amplitude, this gives
them not only a lower species richness but a lower
percentage of specialist species. Thus the species
richness and the greater specialism of the tropics
ARTICLE IN PRESS
Explaining the global biodiversity gradient
are not causes one of the other, but stem from a
third cause, the amplitude or frequency of environmental change (Connell & Orias, 1964). Empirical
testing will encounter the question of what is the
appropriate time base, and how one weighs
variance in rainfall against variance in temperature: in theory one needs the intergeneration
variance, which is on a different base for different
organisms. The measure used in analyses is currently the intra-annual variation, or in more
general discussions the very long-term variation
associated with Milankovitch glacial cycles. Intraannual variability in temperature has been shown
to predict species richness (Andrews & O’Brien,
2000), but not often, perhaps because it is not
often entered into analyses.
It has long been postulated that herbivore, if not
overall animal, diversity would be affected by plant
diversity, this being a clear prediction if individual
plant species constitute the niches of animal
species. Surprisingly the most thorough test of this,
for phytophagous insects, showed no correlation
between plant and butterfly richness, neither for
polyphagous nor more surprisingly for monophagous
species (Hawkins & Porter, 2003b).
Discussion
It seems that every time a mechanism for the
regulation of species richness has been found or
proposed, an argument is produced to show how it
could make the tropics more species rich. However,
some mechanisms are clearly likely to lead only to
local variations in richness, with no systematic
global distribution (Whittaker et al., 2003). If one
can argue convincingly that, say, intermediate
disturbance leads to higher diversity (Huston,
1979) one does not have to suppose that the theory
succeeds only if it can then be shown that tropical
environments are more disturbed. The factor may
simply not be involved in generating the large-scale
gradient. Some mechanisms, like the north–south
slope effect noted above, might even lead to a
reverse gradient. There is a suspicious shortage in
the literature of theories predicting lower tropical
diversity.
The development of the neutral theory of
biodiversity has made very plain the close similarities in structure between evolutionary and ecological theory (see e.g. Turner, 1992). The
mathematical theorems are almost identical —
the term 2Nem in evolutionary theory (Maynard
Smith, 1989) is the exact analogue of y and could
be called ‘‘the fundamental heterozygosity num-
445
ber’’ — but the processes act at different levels of
organisation: the organism and the ecosystem.
Thus one theory deals with genes, the other with
species, but both invoke the same three processes:
random drift, mutation (known in ecology as
speciation), and competition (known in evolutionary theory as natural selection). In both theories
there are phenomena — respectively, individual
adaptation and the self-regulating biosphere (Lovelock, 1979) — which can be explained only by the
selective process (natural selection or competition). In evolutionary theory, there is a long running
and vigorous dispute over the role of selection
relative to the other two processes (Provine, 1986;
Gould, 2002b): the ‘‘universal Darwinist’’ view is
that selection is a process of such strength as to
obliterate any patterns that might be created by
mutation and drift (e.g. Clarke, 2004). The analogous view in ecology is that unequal competition
obliterates all patterns that random drift and
speciation create in ecological communities.
But the neutral theory is not open to rejection
merely because there are patterns in biodiversity
which it does not predict or explain. Such a
simplistic rejection would be the equivalent of
rejecting Newton’s first law of motion on the very
sound empirical grounds that satellites and planets
do not travel in straight lines and that objects
accelerate when dropped and decelerate when
rolled across the floor. The real task is the much
harder one of finding how much of the pattern is
selective and how much is random. Among the
major gradient-generating mechanisms, it is extremely difficult to disentangle primary causes and
direct casual connections from secondary causes
and indirect causal links. The massive correlation of
diversity with climate argues for a strong causal
link, but we have still to deal with the problems of
the colinearity of climate with area (particularly
with the uniqueness of the tropics shown in Fig. 3)
and with evolutionary time. The theory of niche
assembly is even more complex and therefore much
harder to test.
It is likely that we now possess the correct
explanation for the global biodiversity gradient.
The only problem is to work out which of the
proposed mechanisms this actually is. If the
example of evolutionary theory can be relied on,
we can still expect a prolonged debate.
Acknowledgements
My gratitude and thanks to Brad Hawkins, Richard
Field, Doug Futuyma, Chris Thomas, Jeremy
ARTICLE IN PRESS
446
Greenwood, Jean-Franc-ois Guégan, Fiona Proffitt
and a (sadly anonymous) referee.
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