1 ’

TREE vol. 6, no. 1, January 7991

ANeedforNiches?
Peter Chesson dividuals of different species. For
example, with two habitats and two
The idea that different species must population growth. Moreover, coexist- species, the species that at any time
have distinct ecologies if they are to ence in this setting can be expected has a higher fraction of its individuals
coexist has been challenged recently to be robust, for small quantitative in the better habitat would have the
by the claim that some models involv- changes in the model will not change higher recruitment rate. This mech-
ing stochastic factors or clumped a low-density advantage to a disad- anism would lead to fluctuations in
spatial distributions permit stable co- vantage. Here, I discuss two particu- relative recruitment rates, but would
existence of species that are identical lar models that have been suggested it confer an advantage on a species at
or differ only in competitive ability. as showing this sort of coexistence. low density?
However, these models have been The first is the lottery model for sess- Under the assumption that individ-
misinterpreted; except in rather lim- ile or territorial organisms with fluc- uals of different species are indis-
ited circumstances, they provide tuating recruitment rates, in a new tinguishable, the competition that an
further support for the notion that formulation due to Fagerstrom (see individual experiences within a habi-
species must be sufficiently ecologi- Ref. IO). The second is a model of tat depends on the total density of
cally distinct to coexist stably. The aggregated oviposition by compet- individuals in the habitat, regardless
possible, limited, exceptions to this ing insect speciesg. of species. An individual of the rarer
rule involve social factors by which Coexistence satisfying the invas- species experiences no less compe-
individuals of a species discriminate ibility criterion has important impli- tition than an individual of the more
between heterospecifics and con- cations for individual organisms: abundant species. Since habitat qual-
specifics without there being any there is an average advantage to ity is also the same for both species,
true ecological differences between membership of a species at low den- there can be no species distinction in
species. sity, as such species show stronger reproduction within a habitat. Be-
per capita growth over time. If indi- cause dispersal of offspring is also
viduals of one species are indis- identical for both species, individuals
The idea that similar species can- tinguishable from individuals of of either species in a habitat have
not coexist has been both potent and another, can this criterion possibly be identical chances of having offspring
controversial in ecology’-6. Skeptics satisfied? The answer seems to be no, that are successfully recruited into
argue that there is a variety of mech- for if there is no difference between the system. Thus, within a given habi-
anisms of coexistence that do not rely individuals of different species there tat, an individual gains no advantage
on ecological differences between can be no advantage to membership by belonging to one species or the
species7. Mathematical models have in one species over another. As other, either in the short run or in the
been used to support this case8-lo, shown below, models purportedly long run (i.e. how its offspring and
which in its most extreme form is the demonstrating long-term stable co- their offspring fare). In particular,
hypothesis that identical species can existence of species with identical viewed within either habitat, and
coexistlo. No one seriously argues niches in fact implicitly assume eco- regardless of species composition
that any two species in nature are logical distinctions between individ- within a habitat, there is no expec-
identical, but if models say that ident- uals of different species that can be tation of more vigorous lines of de-
ical species can coexist, we should considered to be niche differences. scent from individuals of the rarer
not expect to find a limit to the species compared with individuals of
similarity of coexisting species*. Lottery models for ecologically identical the more abundant species.
Models purporting to show coexist- species An individual in the better habitat
ence without niche differences have The lottery model assumes that of course has an advantage over an
been of two sorts. In the first sort, space is allocated to juvenile organ- individual in the poorer habitat. It fol-
exemplified by Hubbell’s model of isms by chance processes, possibly lows that an advantage to individuals
tropical forests (see Ref. 81, species with some bias to one species or of the rarer species would occur if a
are assumed to be identical and coex- another. In unbiased forms of the given individual of the rarer species
istence is not indefinite: extinctions model, the probabilitythat any juven- had a greater probability of being
occur, but they take a long time. Such ile is successful in gaining the space present in the better habitat than a
models do not confer long-term stab- needed for maturity and repro- given individual of the other species.
ility, which is defined here as the duction is inversely proportional to. Is this likely to occur? With identical
tendency for species to recover in the the density of competing juveniles. dispersal modes for the two species,
long run after falling to low density. The total number of individuals re- the theory of Markov chains14 shows
Moreover, a slight variation in the cruiting to the mature stage is limited that any difference between species
assumption of equality of species, by the available space, but relative in the probability that a given individ-
such as differences in average demo- recruitment from different species ual memberwill be found in a particu-
graphic parameters, can upset the fluctuates over time due to stochastic lar habitat must disappear with time.
conclusions of these models”. fluctuations in relative birth rates and We conclude, therefore, that the
In the second sort of modelg~‘O, juvenile survival rates. These relative scheme for generating birth-rate fluc-
there is a stable long-term coexist- fluctuations in the rates of recruit- tuations envisaged by Fagerstrom
ence: species recover from fluctu- ment are essential for coexistence in gives no advantage to a species at
ations that take them to low density. the lottery model13. low density. It follows that the invas
This involves showing that the invas- Originally, these fluctuations were ibility criterion is not satisfied, and
ibility criterion12 is satisfied, i.e. that a assumed to reflect species-specific there is no long-term stable coexist-
species at low density has an average responses to environmental factors, ence of identical species in the lot-
long-term advantage in per capita but Fagerstrom’O argued that random tery model.
dispersal between habitats of dif- The argument above is a general
Peter Chesson is in the Ecosystem Dynamics ferent quality could generate the one, and applies to models other than
Group, Research School of Biological Sciences, necessary asynchronous fluctuations the lottery model. It depends primar-
The Australian National University, GPO Box in recruitment rates, without any ily on the assumption that individuals
475, Canberra, ACT 2601, Australia. ecological differences between in- of one species are identical in rel-

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TREE vol. 6, no. 1, January 1991

evant ecological respects to individ- better when all environments are ual’s fitness is unaffected by the ratio
uals of other species. It does not de- considered16. However, this is per- of conspecifics to heterospecifics
pend on just two habitats or two fectly consistent with the coexist- among competing individuals. In-
species, random dispersal, or even ence requirement that each species deed, this is critical to the arguments
the nature of population dynamics be favored by some specific environ- (above) that rule out long-term stable
within a habitat. The important as- mental conditions underwhich it per- coexistence of identical species. Yet
pect of dispersal is that it is identical forms better than other species. individuals might easily distinguish
for all individuals regardless of Indeed, this is likely to occur if adap- between heterospecifics and con-
species, and satisfies the usual tation to certain environmental con- specifics without there being ecologi-
Markov chain model with the mild ditions trades off against adaptation cal properties that are unique to a
conditions necessary for conver- to other environmental conditions. species. Such discrimination by indi-
gence to a unique stationary distri- The idea that average similarity viduals opens up the possibility of
bution14. Indeed, dispersal can have favors coexistence is not unique to long-term stable coexistence without
the usual leptokurtic distribution the lottery model. Indeed, it also ap- different niches for different species.
often found for plant species15, so plies to the deterministic Lotka- For example, potentially easier rec-
long as all habitats can eventually be Volterra model on which classical ognition of conspecifics as com-
reached by descendants of an ideas of limiting similarity are based. petitors might lead to greater
individual. For this model, May’* showed that intraspecific interference than inter-
Species satisfying these conditions species can coexist if they differ only specific interference. The species
and living in a finite universe will ex- a little in resource use, provided they need not exploit different resources
perience the sort of random walk to have similar demographic parameters or be affected differently by environ-
extinction suggested by Hubbell and and can harvest similar average mental factors for this interference
Foster*. It is possible that this may amounts of resource. difference to exist, and for it to pro-
take a considerable time; neverthe- mote long-term stable coexistence.
less, it is not the sort of stable coexist- Coexistencefrom clumped egg distributions Sexual compatibility generally dis-
ence that implies recovery from fluc- Atkinson and Shorrocksg presented tinguishes heterospecifics and con-
tuations to low density. a model showing long-term stable specifics. The most likely effect of this
coexistence relying on spatially sort of distinction, however, is a low-
Lottery models with ecologically distinct patchy oviposition by the individuals density disadvantage. At low density,
species of two competing insect species. individuals might experience prob-
In a recent article’?, Chesson and While this is not a model of species lems such as failure of insemination,
Huntly discussed how the rare- identical in all respects, it was pre- inbreeding, or insufficient choice
species advantage occurs in lottery sumed that appropriately patchy egg among potential sperm donors. This
models and the related broad class of distributions do not require any dif- low-density disadvantage would
models of communities in fluctuating ferences in the oviposition behavior cause a departure from the slow ran-
environments. Such an advantage of individuals of different species, dom walk to extinction mentioned
depends critically on individuals ex- so long as individuals oviposit in above for cases where individuals of
periencing their most favorable en- batches. Hence, it has been cited as different species cannot be dis-
vironmental conditions when most an example of coexistence without tinguished, hastening competitive
other individuals with whom they niche differences7*1g. Using an argu- exclusion.
compete find the environment less ment similar to that above for the For a more promising situation,
favorable. This is only consistently lottery model, Green*O showed that consider the insect oviposition
likely when response to the environ- long-term stable coexistence could example above. Atkinson and Shor-
ment is a species-specific trait. not occur while individuals of differ- rocks9 and Ives2’ suggest that suit-
Species-specific responses to the ent species had identical oviposition able clumping might result if
environment can be said to define behavior. In essence, this situation individuals preferentially oviposit in
different niches for different species. does not lead to individual females places that have been visited pre-
Indeed, specific dependence of repro- ovipositing in less crowded sites viously by conspecifics. This could
duction and juvenile survival on the when the species is rare relative to indeed lead to a low-density advan-
temporally variable environment fits the other species. No advantage of tage, and long-term stable species
well with Grubb’s concept of the rarity relative to the other species coexistence, under the assumption
regeneration niche16,17. However, accrues. that intraspecific clump size is lower
separate niches defined in this way Atkinson and Shorrocksg recog- at lower density. We do not have to
may not be enough for coexistence. nized that ‘habitat preferences’, argue that species have ecological
Population growth rates must satisfy or species-specific oviposition re- differences for this to be true. In par-
additional requirements before co- sponses to spatially varying environ- ticular, long-term stable coexistence
existence is possible”. mental stimuli, could also lead to could occur without separate niches.
While the lottery model does not clumped distributions of eggs. As dis- However, this argument depends on
show that identical species can co- cussed by Iver?‘, this mechanism of there being a fitness disadvantage to
exist, it does imply that some simi- clumping does indeed promote long- clumping of eggs intraspecifically,
larities between species favor term stable coexistence. Such clump- making it doubtful that it could persist
coexistence. Species obeying the lot- ing, however, depends on differences as a behavior in a population. It
tery model are more Iikelyto coexist if between species that might be called seems more likely when such intra-
they have similar properties when ‘oviposition niches’, and does not specificaggregationoccursthatthere
averaged over all environmental con- represent a fundamentally new is a fitness advantage, and a conse-
ditions. Thus, having similar average mechanism of coexistence. quent individual disadvantage at low
birth rates, similar average death density as aggregating becomes
rates, and similar birth-rate variances Coexistence independent of ecological more difficult.
(which are also averages), favors co- differences? Social factors such as those dis-
existencelo. Such similarity pre- When discussing identical species, cussed here seem to hold the key to
cludes any species being significantly it was assumed above that an individ- species coexistence without separate

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 TREE vol. 6, no. 7, January 1991

niches, but in any case conditions for 2 Abrams, P.A. (1986) Trends Ecoi. Evoi. 12 Chesson, P.L. and Ellner, S. (1989)
it are probably restricted. Plausible 1,131-132 J. Math. Bioi. 27, 117-138
examples may require consideration 3 Roughgarden, J. (1986) Trends Ecoi. 13 Chesson, P.L. and Warner, R.R. (1981)
Evoi. 1, 132 Am. Nat. 117,923-943
of ecological and evolutionary pro-
4 Giller, P. (1986) Trends Ecoi. Evoi. 1, 14 Karlin, S. and Taylor, S.J. (1975) A
cesses on different temporal or
132 First Course in Stochastic Processes,
spatial scales, so that a trait confer- Academic Press
5 den Boer, P.J. (1986) Trends Ecoi. Evoi.
ring a fitness disadvantage under 1,132-133 15 Harper, J.L. (1977) Population Biology
some ecological conditions can 6 Pimm, S.L. and Gittleman, J.L. (1990) of Plants, Academic Press
persist. Trends Ecol. Evol. 5,70-73 16 Grubb, P.J. (1977) Biol. Rev. 52,
107-145
7 Silvertown, J. and Law, R. 11987)
Acknowledgements 17 Grubb, P.J. (1986) in Community
Trends Ecol. Evol. 2, 24-26
I am grateful for discussions with Nancy Ecoioav (Diamond, J. and Case, T.. eds),
8 Hubbell, S.P. and Foster, R.B. (1986) in
Huntly, Bryan Shorrocks and D.S. Wilson. pp. 207-225, Harp& & Row
Community Ecology (Diamond, J. and
Comments on the manuscript by Maridell 18 May, R.M. (1974) Theor. Popui. &ok 5,
Case, T., eds), pp. 314-329, Harper &
Bender, Susan House, Richard Law and 297-332
Row
anonymous reviewers have also been 19 Shorrocks, B., Rosewell, J., Edwards,
very helpful. This work was supported by 9 Atkinson, W.D. and Shorrocks, B. K. and Atkinson, W. (1984) Nature 310,
NSF grant BSR 8615028. (1981) J. Anim. Ecol. 50,461-471 310-312
10 Fagerstrom, T. (1988) Trends Ecol. 20 Green, R.F. (1986) Am. Nat. 128,
References Evoi. 3,303-306 301-304
1 den Boer, P.J. (1986) Trends Ecoi. Evol. 11 Chesson, P. and Huntly, N. (1989) 21 Ives, A.R. (1988) J. Theor. Biol. 133,
1,25-28 Trends Ecoi. Evoi. 4,293-298 345-361

PolarDinosaurs
andAncient
Climates
teeth of a tyrannosaur and a
Michael J. Benton troodont1-3. (See Box 1 for a glossary
of taxa.)
The southern polar dinosaurs were
Dinosaur skeletons have recently imagine dinosaurs as thermally in- first recorded in 1906, when Wood-
been found well within the contem- sulated warm-blooded animals that ward15 reported a lungfish specimen
porary Arctic and Antarctic Circles. ploughed through snowdrifts and and a dinosaurian claw from the Early
These discoveries have surprised scraped the ice off the ground to find Cretaceous (130-105 million years
palaeontologists who regarded the food? ago) of Victoria, southeastern Aus-
dinosaurs as warm-adapted animals. The first polar dinosaur remains to tralia. Further isolated fossils were
New geological evidence suggests be reported were some ornithopod found sporadically after 1906, but
that these polar areas were also footprints from Spitsbergen13, which recent systematic collecting has
rather colder than had been thought, lay at about 60”N in the Early Cre- yielded an extensive fauna4,5. The
and this raises further problems in taceous. Further footprints, skin im- area lay as far south as 70-85”s in the
interpreting dinosaurian palaeobi- pressions and bones have been Early Cretaceous, and it must have
ology: were the dinosaurs fully en- reported over the past 30 years from experienced up to three months of
dothermic and able to survive the the mid and Late Cretaceous (114-66 effective darkness in the austral win-
darkness and cold of the polar re- million years ago) of the North Slope ter. The fossil plants and invert-
gions, or could they undertake vast of Alaska, as well as from the North- ebrates, and the geochemistry, indi-
annual migrations of 30004000 km? west Territories and Yukon Terri- cate a cool humid climate.
tories of Canada. Much of this ma- So far, the Victorian flora and fauna
terial was collected by prospecting consists of more than 150 species:
Dinosaurs are usually pictured parties from coal and oil companies, deciduous and evergreen trees,
against a background of damp trop- and the specimens have only recently bushes and low ground cover,
ical jungle-like foliage or sandy been described1-3. aquatic and terrestrial invertebrates
deserts. Most fossil skeletons of The North Slope of Alaska today (ostracods, cladocerans, other crus-
dinosaurs have been found associ- lies at latitude 69”N, but geologists taceans, spiders, insects, earth-
ated with tropical or subtropical estimate that this area was further worms, bryozoans, bivalves), fishes
floras, and often with various sedi- north in the Late Cretaceous, at 75- (bony fishes, lungfishes), turtles,
mentological indicators of humid or 85”N. The climate appears to have lizards, pterosaurs, freshwater(?)
arid conditions. Further, their postu- been cool temperate in the Late Cre- plesiosaurs, birds and dinosaurs. A
lated thermal physiology and naked taceous, based on studies of the fossil jaw bone of a temnospondyl amphib-
skin was taken to indicate a prefer- plants. The flora consisted of decidu- ian has also been found: the last sur-
ence for the environments favoured ous plants which shed their leaves vivor of a group that had died out
by living reptiles. New findings, how- and died back or lay dormant in win- elsewhere long before the Early Cre-
ever, show that dinosaurs lived ter. Cross-sections of the fossil wood taceous. The dominant dinosaurs are
within the ancient Arctic and Antarc- also show that growth ceased in win- three or four genera of small- to
tic Circles1-8 (Fig. I), and that these ter2*‘*,14. The Alaskan fossils include medium-sized hypsilophodontid or-
zones may have been covered exten- a freshwater dermatemyid turtle, a nithopods, and other less-complete
sively with iceg, although this idea is freshwater clam bearing tooth marks remains indicate the presence of two
controversial’&‘*. Should we now of a crocodilian or dinosaur, an or- or three theropods.
nithopod dinosaur footprint, isolated A single vertebra of a theropod(?)
bones of ceratopsian dinosaurs (an dinosaur has also been recorded
Michael Benton is at the Dept of Geology, occipital condyle, a horn core, and a from the latest Cretaceous of North
University of Bristol, Bristol ES8 lRJ, UK. partial femur) and hadrosaurs, and Island, New Zealand6, in an area that

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