Transcript of H. A. GLEASON'S INDIVIDUALISTIC CONCEPT AND THEORY OF ...
H. A. GLEASON'S ‘INDIVIDUALISTIC CONCEPT’ AND THEORY OF ANIMAL
COMMUNITIES: A CONTINUING CONTROVERSYH. A. GLEASON’S
‘INDIVIDUALISTIC CONCEPT’ AND THEORY OF ANIMAL COMMUNITIES: A
CONTINUING
CONTROVERSY
BY ROBERT P. McINTOSH
Department of Biological Sciences, University of Notre Dame, Notre
Dame, I N , U S A
(Received I I February 1993 ; revised 16 May 1994; accepted 3 0
August)
CONTENTS
I. Traditions of community concept . . . . . . . . . . 11. Animal
community studies from the 1950s to the 1970s and recognition of
Gleason’s
concept . . . . . . . . . . . . . . . . . . . . . . . . .
( I ) Evolution and community theory . . . . . . . . . (2)
Individualistic concept revisited . . . . . . . . . (3) Definition
of community . . . . . . . . . . . (4) Key questions for community
ecology . . . . . . . . ( 5 ) Empirical studies of communities . .
. . . . . . .
IV. Community theory and questions for the 1990s . . . . . .
.
VI. Acknowledgments . . . . . . . . . . . . . VII. References . . .
. . . . . . . . . . .
V. Summary . . . . . . . . . . . . . .
I . TRADITIONS OF COMMUNITY CONCEPT
In the early decades of ecology in the twentieth century most
ecologists took for granted that communities existed as natural,
repeated, internally organized units with a considerable degree of
integration which governed their structure, function, development
or succession and even their evolution (McIntosh, 1985).
Communities were likened to an individual organism and commonly
called a superorganism (Clements, 1936) or quasi-organism (Tansley,
1935). Nicholson (1990) noted that not all ecologists accepted the
extreme views of Frederic Clements, whose ideas about community
dominated American ecology in its early decades, but only H. A.
Gleason (1917, 1926, 1939) in three elaborations of his
‘individualistic concept ’, openly attacked them and offered an
alternative concept predicated on the individualistic capabilities
of species, continuous variation of the environment and diverse
probabilities of arrival of propagules. Although several American
ecologists had expressed similar views, none publicly supported
Gleason’s heretical concept until 1947 (McIntosh, 1975, I 985).
Gleason’s concept provided an alternative paradigm and the
potential, at least, for revolution in the Kuhnian sense (Price,
1984b). Gleason’s (1926) version of the individualistic concept was
recently recognized as one of the ‘classic papers in the
foundations of ecology’ (Real & Brown, 1991).
Early marine animal ecologists such as Edward Forbes, Victor Hensen
and C. G. J. Petersen had independently developed concepts of
marine plankton and benthic communities largely in the traditional
paradigm of discrete communities. Terrestrial
R. P. MCINTOSH and freshwater animal ecologists, notably E. A.
Birge, S. A. Forbes, Victor Shelford, C. C. Adams and Charles
Elton, undertook surveys of terrestrial and freshwater animal
communities (McIntosh, 1985). Forbes (1880) described ‘the ideal
balance of nature’ and a ‘tendency towards a just equilibrium’ in
animal communities. Elton (1927) wrote, in his pioneer volume,
Animal Ecology, that animals were not ‘mere assemblages’ but formed
‘closely knit communities or societies’. However, he later attacked
the widely used clockwork simile for communities by noting that the
animal ‘wheels’ retain the right to move to another clock and each
clock has its own mainspring (Elton, 1930) ascribing to them
considerable independence. Shelford eventually subscribed to
Clements’s ideas and joined with him to produce a catalogue of
plant and animal communities or biomes (Clements & Shelford,
1939). In 1939 a symposium was held designed to bring together
plant and animal community ecologists that, however, had little
influence on the already established barriers between them (Just,
1939). The commentators at this symposium raised many questions
evident in recent discussions of community ecology. Both of these
volumes were criticized by reviewers for the absence of the
statistical and mathematical analyses which became the hallmark of
later studies of animal community ecology (McIntosh, I 985).
Animal ecologists in the early decades of ecology emphasized
studies of individual populations or population interactions with
notable exceptions (Elton, I 927, I 930, Cole, 1946; Renkonen,
1949). Elton (Elton & Miller, 1954), for example, noted his
diversion from community studies to studies of population
fluctuations for 20 years after 1923 with community on the back
burner. Wiens (1989) described David Lack as switching from
community to population studies in the 1940s and commented that
there were few studies of bird communities before the 1950s. Grant
& Schluter (1984), however, dated consideration of community
structure and the role of biotic interactions from Lack’s work with
Darwin’s finches in the 1940s. In 1944 the British Ecological
Society addressed ‘The ecology of closely allied species’ in a
symposium and Elton and Lack agreed that competition was an
important influence on community composition ; but others argued
that the absence of equilibrium conditions precluded competition
having a major influence on community composition (McIntosh, I
985). However, these inferences about competition and community
were not extensively developed until the I ~ ~ O S , when Robert
MacArthur introduced his ideas of community, and they only really
got going in the 1960s according to Brown & Bowers (1984).
Minshall (1988) identified an ‘ era of refinement and
experimentation ’ in stream communities also beginning in the
1960s. Heins & Matthews (1987) dated widespread interest in
stream community dynamics in North America from 1975. Esch et al.
(199ob) dated quantitative approaches to helminth communities from
the early 1960s along with the roots of ecological
parasitology.
Although Grinnell’s early ideas of niche were seen by Wiens (1989)
as paralleling Gleason’s individualistic concept, controversy about
the community as a Clementsian integrated or organismic entity as
against Gleason’s ( I 926) concept of community as ‘not an
organism, scarcely even a vegetational unit, but merely a
coincidence’ was, through the I ~ ~ O S , largely the province of
plant ecologists. Some marine ecologists, however, had addressed
many of the same issues and arrived at concepts similar to
Gleason’s (Stephen, 1933; MacGinitie, 1939; Mills, 1969). Jones
(1950) was more equivocal suggesting the fauna could be divided
into communities on ‘ more-or-less
Gleason’s ‘ individualistic concept ’ 3 I 9
definite limits to the physical conditions’. He denied, however,
that any assemblage of animals reacted as a unit or was structured
by biological factors such as competition. Wieser (1958) recognized
two approaches to marine communities - the ‘particulate’, or
classificatory and the ‘ comparative ’ which, like the
individualistic concept, held that a natural classification of
communities was not possible.
It is commonly recognized that Gleason’s individualistic concept
was a primary stimulus to the development, in the I ~ ~ O S , of
the ideas of continuum and gradient applied to community in the
vegetation studies of J. T. Curtis, Robert Whittaker and their
students and associates (Curtis & McIntosh, 1951 ; Curtis,
1959; McIntosh, 1958, 1967, 1983, 1985, 1993; Whittaker, 1967).
Their studies brought Gleason’s ideas out of limbo and added a new
dimension (literally multidimensions) to the discussion of
community. Gleason’s individualistic concept, and the issues it
addressed, were introduced into general textbooks of ecology in the
1950s; but they were not immediately widely incorporated into
animal community ecology (McIntosh, I 975, 1985). The midcentury
works of Allee et al. (1949) and Dice (1952) on animal ecology were
unusual in citing Gleason’s work but both accepted that communities
were natural aggregations of interdependent species. Dice wrote
:
The concept that most communities are composed of more or less
independent individual organisms which are interrelated and to some
extent coordinated so that the whole community forms a unit of
organization agrees well with what is known of ecology.
Elton and Miller (1954) traced the development of ideas of the
animal community and noted a change of philosophy, essentially to a
community view of ecology in the recognition that the importance of
biotic relations in influencing organisms required knowledge of
species associations to understand the population ecology of single
species. Most to the point of this discussion, they recognized
Gleason’s individualistic concept and the problems it posed for the
search for uniform habitats and comparison of communities. British
animal ecologists, they said, found that only very small ‘centres
of action’ or microhabitats, such as dung and logs, fitted their
concepts of uniformity and achieved ‘broadly repeated identity’.
However, the tradition in most animal ecology of the community as a
highly integrated entity was recognized by Bodenheimer (1957) who,
however, denied there was any evidence to support the organismic
concept of community.
11. ANIMAL COMMUNITY STUDIES FROM THE 1950s TO THE 1970s AND
RECOGNITION OF
Gleason’s concept, and the derivative ideas and methods of
continuum and gradient in plant ecology, reviewed by McIntosh
(1967,1993) and Whittaker (1967), filtered into the literature of
terrestrial animal ecology. Richardson (I 980) wrote, ‘ In America
the individualistic concept has been in the ascendancy for at least
30 years and there is now widespread acknowledgement that Clements
pressed his organismic analogy too far ’. Perhaps the earliest
specific support for it in an animal community was Whittaker’s ( I
952) study of insect communities in the Great Smoky
Mountains.
Among distributional patterns charted for IOO species no two were
alike; and it was not possible to fit the distributions into
associations, formations or zones. Gleason’s individualistic
hypothesis is asserted for animal communities.
GLEASON’S CONCEPT
3 20 R. P. MCINTOSH Some marine biologists adopted a continuum
concept. Sanders ( I 960), for example, described the benthic fauna
of Buzzard’s Bay as a ‘continuum’ changing with gradual change in
composition of sediment. Bond (1957) and Beals (1960) adapted
ordination methods, developed in plant ecology, to studies of bird
communities. Beals wrote, ‘ Because different bird species seldom
if ever coincide in their ecological distributions, no discrete
communities can be clearly defined except where there are sharp
changes of environment ’. Larimore and Smith ( I 963) asserted
species individuality in associations of stream fishes.
This lack of similarity or consistency in associations seems to
suggest little interdependence between species but rather
dependence of certain species on certain ecological factors.
Other animal ecologists, notably invertebrate ecologists,
independently pursued diverse interests in community organization
(Cole, 1946; Fager, 1957, 1968; Hairston et al., 1960; Macfadyen,
1963; Root, 1973). Cole commented that cryptozoan communities under
debris on the forest floor lacked the interspecific integration of
a biocoenose. Fager (1957) addressed the classical question of
community ecology - whether ‘recurrent’ groups of species occurred
that are a nearly constant part of each others environment? and
answered in the negative. Fager (1968), even in studies of
invertebrates in small decaying logs, failed to find the ‘centres
of action’ or the uniformity noted by Elton and Miller (1954).
Using his method of ‘recurring groups’ he found much variability of
invasion and re-establishment suggesting that each sample was ‘
individualistic in the sense of Gleason ( I 939) ’.
Macfadyen (1963), in an extended review of community definitions in
a current textbook of animal ecology, illustrated how varied were
ideas about animal community. Root (1973), in studies of the
arthropod fauna of collards, found no evidence that the guild
structure remained relatively constant and summarized :
The dynamic structure of the collard fauna illustrates that the
concept of communities as associations with a characteristic
composition, or trophic structure can be somewhat misleading.
Wilbur (1972), however, had urged that ‘classical models’ of a unit
organized community not be discarded, at least for amphibian
communities. He wrote,
My thesis is that these natural groupings of species are organized
by interspecific interactions that can be discovered and evaluated
by experimentally dissecting the community into smaller
components.
Some students of bird communities adopted methods similar to those
of plant community ecologists and recognized the relevance of
contemporary studies of plant communities influenced by Gleasonian
concepts but marched to a different drummer of a widely hailed new
theory of animal communities. Cody ( I 968) studied grassland bird
communities and showed a pattern of individualistic species
distribution (his Figs. 8 and 9) remarkably similar to that
illustrated by Bond (1957) in a study of forest birds. Cody
emphasized the then burgeoning theory of niche initiated by G. E.
Hutchinson and Robert MacArthur and interpreted the grassland bird
community on ideas of resource division, based on a community
structured by competition and climatic instability controlling
niche size in a saturated community. Kikkawa ( I 968) interpreted
his studies of bird communities of Australian forests as ‘unique
associations’ of bird species in different rain forest habitats of
North Queensland contrasted with a
Gleason’s ‘ individualistic concept ’ 321
distribution ‘hierarchically arranged along the mesic-xeric
gradient ’ in forests of New South Wales.
The increased interest in communities and their abstract
properties, diversity and stability, gave rise to a symposium in I
969 that addressed the problems of defining and measuring what all
agreed were critical attributes of community (Brookhaven Symposia
in Biology 1969). It was commonly assumed at that time that
increased diversity was associated with stability until later
theoretical and empirical studies demolished this tradition of
natural history, ecology and conservation (Goodman, I 9-75),
although diversity persists as a key concept.
James (1971) used ordination methods to study bird communities,
contrasting her approach to that of Cody (1968). James specifically
stated that her study was conceptually related to the
individualistic concept of Gleason and the derived continuum
concept of J. T. Curtis, citing the prior work of Bond (1957) and
Beals ( I 960). Terborgh ( I 97 I) also recognized current work of
plant ecologists and offered an approach to the study of avian
distributions similar to that pioneered by R. H. Whittaker (1952).
Terborgh worked on an elevational gradient of 3000 m in the Andes
Mountains with four physiognomically distinct vegetation types. He
examined the distribution of species relative to three models based
on distributional limits of species and the factors that determine
their limits. Criteria for judging the predictions of the models
were (a) shape of population curves, (b) shape of the curves of
faunal attenuation - ‘congruity’ or similarity of adjacent samples
along the gradient, (c) species distribution patterns at termini of
gradients, (d) frequency distribution of ecological amplitudes of
species. Faunal turnover rate was, he said, continuous with
elevation, even in the context of several distinctive vegetation
types, and ecotones accounted for < 20 % of distributional
limits. Circumstantial evidence of competitive replacement of
congeners based on narrow or abruptly terminated species amplitude
curves, was interpreted as accounting for ca. 33 % of species
limits. Terborgh attributed approximately 50 % of species limits to
gradually changing conditions along the gradient. Distribution and
shape of curves of species populations on diverse gradient are
still widely used as criteria of community.
Students of aquatic organisms of various taxa in marine and fresh
waters shared similar concerns about the nature of community. Mills
(I 969) and Stephenson et al. ( I 972) reviewed marine community
concepts with specific reference to Gleason’s ideas and subsequent
studies in plant community ecology. Mills noted then current marine
benthic studies that allowed ‘analysis as parts of continua of
distribution along gradients’. Stephenson, and other marine
biologists, joined with W. T. Williams, a statistician, to
reanalyze the data of a pioneer student of marine benthic
communities, C. G. J. Petersen. They expected to confirm the
communities that Petersen had recognized by subjective analysis of
dominant species. Their analyses revealed some ‘ Petersen-type ’
communities but these differed markedly from Peterson’s original
results. Their findings revealed no groups of species with similar
ecological requirements. Bourdouresque ( I 970) explicitly
addressed the concepts of biocoenose and continuum and found
continuity between organismic and continuum ideas in benthic taxa.
Levandowsky ( I 972) used ordination techniques on phytoplankton of
ponds varying in salinity and supported an individualistic
hypothesis of species distribution. Sale and Dybdahl(1975) asserted
that coral reef fish communities were the
322 R. P. MCINTOSH result of ‘purely chance colonization of species
which do not interact with each other sufficiently to shape the
community’. Briand (1976) cited the concepts of Clements and
Gleason in a study of marine phytoplankton and found, ambiguously,
that ‘three groups of species appear closely defined within the
yearly phytoplankton community ’ but there was relative continuity
among them because of linking species.
Makarewicz & Likens (1975) analysed niche relations of a
zooplankton community and concluded that their findings paralleled
those of Gleason and Ramensky :
The niche structure of the zooplankton community should be
conceived of as an intensive or intracommunity population continuum
corresponding to niche hyperspace.
Lane ( I 978) vigorously attacked them for ‘ forcing their data to
fit the individualistic concept that was originally developed for
terrestrial plants’. According to Lane, such reductionist
approaches are of limited use for animal communities. Levandowsky
and White (1977), perhaps prematurely, wrote ‘the battle between
the community school and the individualistic or continuum school
seems to have been fought and won by the latter in the 1950s’. In
an unusually extreme interpretation, Taylor (1979), in a study of
bactivorous ciliates in a pond, described independent, essentially
random, species distributions. Sousa ( I 979) also recognized the
Clements/Gleason division and, in studies of rocky intertidal
communities, supported a non-equilibrium, disturbance- based view
akin to Gleason’s ideas.
Animal community ecology in the 1960s and 1970s was, however,
largely dominated by proponents of an expanded theoretical
population ecology who, following Hutchinson (1957), centered their
ideas on competition as the major influence in community
organization (MacArthur, I 958, 1972; Lewontin, 1969 ; Schoener,
1974 ; Cody, 1974 & Diamond, 1975; Diamond, 1975, 1978; May
19764 b). Hutchinson’s (1957) ‘Concluding Remarks’, in which his
theory of the multidimensional species niche appeared, stimulated a
profusion of empirical and theoretical studies of communities under
the umbrella of niche theory with proliferation of collateral ideas
- resource partitioning, character displacement, species packing,
niche shifts, ‘ etc I. Schoener (1974) reported that in the 1960s
and early 1970s studies of resource partitioning ‘have grown
exponentially at a rate four times that of typical scientific
works’. Lewontin (1969) described this facet of ecology as
transforming Clements’s idea of succession by a union of
mathematics and evolution to produce ‘the bare beginning of an
exact theory of the evolution of communities of organisms’. The new
framework was, he said, ‘the concept of the vector field in
n-dimensional space’. According to Levin (1988), the mathematical
theory of animal ecologists emerged from the Clementsian approach
and ‘ emphasized equilibrium, constancy, homogeneity, and
predictability’. These are the key elements of the ‘New ecology’
that Colwell (1985) said dominated animal community ecology of the
I 960s and I 970s, with little reference to Gleason’s
concept.
The ‘bare beginnings’ of Lewontin (1969) grew into ‘new paradigms’.
According to Cody and Diamond ( I 975) :
Within two decades new paradigms had transformed large areas of
ecology into a structured, predictive science that combined
powerful quantitative theories with the recognition of widespread
patterns in nature.
Much of this theory was first justified, and later criticized,
based on studies of bird
Gleason’s ‘ individualistic concept ’ 323 communities. Stearns
(1982), in an essay on 25 years of progress in community biology,
asserted ‘it was birds that inspired the idea that communities are
static systems in competitive equilibrium in the work of MacArthur
(1958)’. This comment seems justified, in that the major volume on
animal community ecology published in the mid- I ~ ~ O S ,
celebrating two decades of the new theory associated with the work
of Robert MacArthur (Cody & Diamond, 1975), had birds cited on
216 pages, mammals on 35, lizards on 28, insects on 6 and fish not
at all. According to Grant (1986) this volume ‘marked the final
flourish of an era of unbridled enthusiasm for the notion that
interspecific competition is important in conferring structure upon
communities of organisms’. The proportions of citations were more
equal a decade later in the volume in which Grant’s article
appeared. Birds were cited on 89 pages, fish on 63, lizards on 62,
insects on 47 and mammals on 40 pages (Diamond & Case, 1986).
Wiens (1986) described animal community ecology from 1960 to 1975
as follows:
it seemed clear that many ecologists believed that natural systems
were at or close to equilibria determined by resource limitation,
that selection on resource-utilization traits was more or less
incessant, and that competition between species was the primary
component of this selection and therefore played the major role in
structuring communities.
The similarity between early plant ecology and the theoretical
animal community ecology of the 1960s and 70s was noted by Law
& Watkinson (I 988) :
From this blend of field study and theory there emerged a picture
of communities neatly ordered by competition into groups of
compatible species (Diamond, 1978), not altogether dissimilar to
that suggested by plant ecologists of earlier generations.
These ideas initially enjoyed widespread and enthusiastic
acceptance but soon provoked discussion that was later described in
a commentary in Science (Lewin, 1983) as, ‘a debate as acerbic and
acrimonious as any that has stirred the combative instincts of
academia’. The crux of the more heated discussions revolved around
the idea that species distributions, particularly of birds, were
determined by interspecific com- petition. This had culminated in
the assertion that bird communities were organized according to
‘assembly rules’ delineated by Diamond (1975). The concept of rule-
governed community organization was vigorously and, if one followed
the statistics, rigorously disputed by Connor & Simberloff
(1979). Caswell (1976) had introduced a null model of community
structure that examined distribution of species abundances assuming
no interspecific interactions among them. The core of the later
debate was the necessity of distinguishing apparent pattern in
community organization from random events. Connor & Simberloff
argued that the concept of a community organized by assembly rules
as a consequence of competition was false and Diamond’s assembly
rules were ‘tautological, trivial or a pattern expected were
species distributed at random ’. They urged the need of a null
hypothesis of random species assemblies to be tested by appropriate
statistics before a pattern of organized communities based on
competition could be sustained. Schoener (1982) noted an additional
pole of the dispute, that favoured predation as the structuring
force as suggested by the work of Paine (I 966) and Connell (1975)
in marine littoral communities.
May (1976) suggested, like others before and since, abandoning
consideration of species to focus on more general aspects of
community organization such as energy flow, trophic groups, body
size, species number or diversity which would, he said,
324 R. P. MCINTOSH reduce the ‘chaotic and vagarious’ level of
individual species to ‘constant and predictable ’ properties of
community organization. Transferring the long familiar object of
community research from the species and number of individuals to
such generalized categories recalls Robert Frost’s saying that
writing poetry in blank verse was like playing tennis without a
net. Certainly the evolutionary connection is lost.
The diverse interpretations of the results of animal community
studies during the I 960s and 1970s recalls Macan’s ( I 974)
question about community concept :
How far is a community an entity any alterations to a part of which
must affect the whole, and how far is it a collection of
independent species ? Results so far indicate that it is not an
entity to the extent that some have suggested.
The relatively spasmodic attention to animal communities evident in
the infrequent earlier symposia and texts gave way to a rush of
symposia and attendant volumes in the 1980s and 1990s (Barnes &
Minshall, 1983a; Strong et al., 1984b; Price et al., 1984; Kikkawa
& Anderson, 1986; Diamond & Case, 1986a, Gee & Giller,
1987; Gray et al., 1987; Matthews & Heins, 1987; Grubb &
Whittaker, 1988; Hastings, 1988; Morris, et al., 1989; Polis, 1991
; Ricklefs & Schluter, 1993). The thread of the traditional
dispute concerning the organized community and Gleason’s
individualistic concept is woven through this literature. I hope to
follow this thread and examine, if not untangle, some of the knots,
Gordian or otherwise. Some of the dispute was complicated by
frequent misstatements about Gleason’s concept and belaboring straw
men set up in place of Gleason’s ideas. Although Gleason emphasized
chance arrival of immigrants, he did not assert that a community
was a random assemblage of species selected solely by their
response to the physical environment of a site. Gleason recognized
patterns, each species responding individualistically to the
complex of biotic and abiotic forces. He asserted that early
arrival and control of a site by a species could inhibit the
success of later arrivals as competition did restrict a new species
once the ground was fully occupied (McIntosh, 1975).
111. ANIMAL COMMUNITIES IN THE 1980s
The controversy of the I 970s about animal communities precipitated
by theoretical population ecology and its attendant ideas of niche,
resource partitioning, competitive exclusion, coexistence,
character displacement, saturation and equilibrium continued in the
1980s amid pleas for tolerance and pluralism in ecology (Schoener,
1982, 1987; McIntosh, 1987). Animal community ecology in the 1980’s
was variously described as experiencing, ‘disappointment’ (Brown,
1981), a ‘ dream world’ (Price, 1984b), ‘growing disquietude’
(Wiens, 1986), ‘fierce counterattack’ (Schoener, 1986d), ‘morbid
self-evaluation’ (Cody, 1987), and being in ‘a state of flux’
(Kareiva & Anderson, 1988) or ‘ in disarray’ (Morin, 1989).
Nevertheless, extended empirical studies of communities and
symposia on communities proliferated, theoretical models were
constructed and deconstructed and speculation about the nature of
community continued. Richardson ( I 980) reviewed the familiar
dichotomy between Frederic Clements’s organismic community and H.
A. Gleason’s individualistic concept of community. According to
Richardson, the re-emergence in the I 970s of organismic ideas of
community, that were then waning among plant ecologists, was
attributable to animal ecologists who were emphasizing the
importance of biotic controls on the
Gleason’s ‘ individualistic concept’ 325 structure of the
community. Richardson said that animal communities were more
conducive to organismic notions than plants and both concepts were
acceptable since communities in stable environments are more
organismic because, ‘ species evolve toward accommodation with
others in the enduring species complex, ’ whereas successional
communities, in contrast, are ephemeral and individualistic.
Collins et al. ( I 982) expressed doubt about Richardson’s
statement that animals are more likely than plants to occur in
tightly co-evolved organismic communities. Any lagging confidence
in the much criticized superorganism was renewed by Moore ( I 983)
who described the ‘revival of the organismal heresy’. Wilson &
Sober (1988) gave added evidence of the resilience of the
superorganism writing :
Imposing consistency clearly shows that groups and communities can
be organisms in the same sense that individuals are. Furthermore,
superorganisms are more than just a theoretical possibility and
actually exist in nature.
A landmark in changing ideas of animal ecology was a symposium held
in I 98 I . The organizers of the symposium (Strong, et al . ,
19843) expected to find:
fairly commonly.. . the community with so few strong interactions
that organization arises primarily from mutually independent
autecological processes rather than from synecological ones.
Since some of the participants were among the major promulgators of
the idea of community as organized by interspecific interactions,
especially competition, significant differences of opinion
concerning the evidence, appropriate experiments, theory and
methods of data analysis were to be expected (Diamond & Gilpin,
1982). Various participants came down on either side of the
controversy. Gilpin & Diamond (1984), reiterated Diamond’s ‘
assembly rules ’ for bird communities and stoutly defended these
against the requirement that a null hypothesis of random
aggregations be tested before a pattern in a community could be
asserted. Their position was rebutted by Connor & Simberloff
(1984) followed by reciprocal ‘rejoinders’ (Gilpin et al., 1984).
Gilpin and Diamond’s arguments were criticized as ‘obfuscatory goo
” by Connor & Simberloff. Some may have judged the exchange of
goo a draw but Gilpin subsequently, if unilaterally, declared
victory, asserting that he and Diamond had shown that Connor and
Simberloff s ‘statistical observations were invalid and that a
proper statistical analysis confirmed the reality of permitted and
forbidden communities according to Diamond’s assembly rules (Gilpin
et al., 1986). T. Underwood (1986), however, reviewed this
controversy and found the arguments of Simberloff and co-workers
cogent and that the rebuttals of Diamond & Gilpin ‘make no
concrete progress’ on the underlying issue of competition.
( I ) Evolution and community theory The idea of evolution of
species producing an organized community was implicit in
ecological thought long before coevolution became a familiar term.
It became a matter of considerable debate in the 1970s and 1980s.
Oddly, the originators of the organismic- individualist community
dispute did not advance Darwinian evolutionary consider- ations.
Clements was essentially neo-Lamarkian, and Wilson ( I 983)
commented that Gleason never used the evolutionary argument which,
he said, is an obvious part of
3 26 R. P. MCINTOSH community ecology today. Commentators on
community theory and evolution, however, commonly alluded to its
Gleasonian interpretations and coevolution was held by some to be a
bulwark of the theory of the organized community. Advocates of
competition based theory argued that if competition could not be
demonstrated in the present it must have occurred in the
evolutionary past (Rosenzwieg, 1979), which Connell ( I 980) termed
‘the ghost of competition past ’. The ghost haunted some animal
community ecology and was joined by ghosts of predation past and
theory of community, sometimes touted as ahistorical, was reduced
to appealing to spooky historical events to explain its presumed
patterns. In spite of these difficulties, Rosenzweig held out hope
for theoretical ecologists writing that Einstein ‘might have
congratulated us for organizing a bewildering chaos into the rich
rococo tapestry that ecological science is becoming ’.
Connell (1980) contrasted the two schools of community thought.
One, he wrote, denied the likelihood of coevolution and competition
as a major force in structuring communities and was led by Gleason,
and his contemporary, the Russian botanist, Ramensky, who had
advanced the individualistic hypothesis independently (Mclntosh,
1983). In this corner Connell included the animal ecologists H. G.
Andrewartha, L. C. Birch 8z J. Wiens. In the opposite corner of
supporters of the organized community he located the classical
plant ecologists F. E. Clements, a similarly classical animal
ecologist, A. J. Nicholson, and the more recent participants, R. H.
MacArthur, M. L. Cody 8z J. Diamond, who supported a new theory of
an organized community, predicated on competition. Connell asserted
that until adequate evidence was produced, ‘ I will no longer be
persuaded by such invoking of the Ghost of Competition Past’.
Gilpin 8z Diamond ( I 984) later sounded a more moderate tone
asserting that the school of ecology they represented had not
claimed that competition was ‘unusually dominant’, which may have
surprised some of their critics.
Stearns ( I 982) asserted that theoretical predictions in
evolutionary ecology stood up to testing although theoretical
models propounded for community ecology were shown to be false. He
noted the increasing recognition among ecologists that ‘the world
is an unpredictable and contingent place’ and said that the
hoped-for order must be on a larger scale and a product of more
complex processes than previously thought. In Stearn’s vision,
field experimentation was the key to community ecology. Gilpin et
al. ( I 986) argued, conversely, that field studies of community
suffered ‘ crippling disadvantages ’ and that it was necessary to
understand laboratory communities before field communities could be
comprehended.
Walter et al. (1984) wrote that ‘The concept of an “organized”
community, particularly if it carries evolutionary connotations, is
unrealistic. ’ Schoener ( I 984b) argued, to the contrary, that
competition was a significant component of evolution and community
organization. Colwell ( I 985), considering ‘The Evolution of
Ecology’ itself, introduced conceptual and philosophical issues of
history and mechanism asserting that Jacques Monod’s ‘ Chance and
Necessity ’ ( I 97 I ) ‘ have taken an increasingly central role in
both ecological and evolutionary thinking ’. According to Colwell a
shift had occurred in ecology ‘toward a contemporary version of
Gleason’s (1939) idea that natural communities are composed of
‘individualistic species’. He concurred with the press by Connor
and Simberloff for null models in ecology by asserting that the
individualist concept ‘is currently regarded by many ecologists as
a
Gleason’s ‘ individualistic concept’ 3 27 kind of ‘ null model ’
for community organization - the case to be disproved with sound
evidence’ - specifically indicating that lack of such evidence had
been at the heart of heated debates in the 1970s and 1980s.
Futuyma ( I 986) considered evolution and coevolution in
communities and maintained that in situ evolution in a local
community accounts for little because species have not been
associated for very long. Community structure, he said, ‘is largely
a consequence of ecological sorting among species that evolved
their properties in a variety of other arenas’. Diamond (1986)
returned to the ‘ghost hypothesis’ and provided a test based on
what he has termed a ‘natural experiment’ in Montane birds of New
Guinea. He discredited Connell’s ( I 980) anti-ghost argument that
he said was a consequence of a logical fallacy. According to
Diamond, the ghost hypothesis, that competing sympatric species
evolved to reduce competition between them, was true for most
montane birds in New Guinea. Wilson & Sober (1989), contrary to
other evolutionists such as John Maynard Smith, asserted that the
properties of organism, including evolution, can be extended to
include superorganisms and predict where they do or do not exist.
Although evolutionary ecology flourished in the 1980s, the
significance of evolution to community organization remains
problematic.
( 2 ) Individualistic concept revisited Citations of Gleason’s
articles propounding the individualistic concept increased
five-fold from 1965 to 1990 and an increasing proportion of
citations was by animal ecologists who strongly supported it
(Price, I 984a; Schoener, 1 9 8 6 ~ ) . Strong (1983) posed
alternative forces in community structure to counter the then
prevalent theory of community with ‘a singular emphasis on
competition ’ as explained by Roughgarden ( I 983). Strong (1986)
cast the individualistic concept of Gleason as an alternative to
classical superorganism theory and ‘ to another extreme, to
excessive competitionism ’. He proposed a concept of ‘
density-vague ’ population dynamics with varying intensity of
interspecific competition as ‘ akin to the individualistic view of
species in communities ’. Brown ( I 984) examined the relationship
between abundance and distribution of species and argued that the
prevalence of relatively rare species ‘ appears to support
Gleason’s ( I 926) classical “ individualistic ” concept of species
distribution and community organization ’. Price ( I 984a) was most
explicit :
The most important factor in assembly of specialists appears to be
the individualistic response of species to the display of resources
in a habitat. This view mirrors that held by phytosociologists from
Ramensky (1924) and Gleason (1926) to Whittaker (1967).
Price was correct in asserting that Gleason’s concept referred to
more than response of species to abiotic conditions and included
the ‘display of resources’. It is incorrect to pose Gleason’s
concept as purely based on response of species to abiotic forces as
against an alternative theory based on response to biotic forces,
as some have done (Pound, 1988; Simberloff & Dyan, 1991).
Gleason is also sometimes interpreted as asserting that an
association or community is a purely random collection of the
available species, perhaps stemming from later association with
Connor and Simberloff s null model. Communities, Gleason said,
occurred as a consequence of environmental variation that was
continuous and fluctuating and the variable and fortuitous
immigration of plants. He wrote that the community ‘is merely one
minute part of a
3 28 R. P. MCINTOSH vast and ever-changing kaleidoscope of
vegetation, a part which is restricted in its size, limited in its
duration, never duplicated except in its present immediate vicinity
and there only as a coincidence, and rarely if ever repeated’
(Gleason, 1939). His successors in the continuum concept similarly
argued that not all things were possible, only some, and though
chance was important, communities were not random aggregations of
species (Curtis & McIntosh, 195 I). Schoener (19866), cited the
long-standing debate between proponents of Clementsian ideas and
Gleason’s concept, and, correctly, said that null models propounded
by Connor & Simberloff, ‘The Florida School’, had an
individualistic view more extreme than Gleason’s.
(3) Definition of community One of the difficulties of the ‘new’
community ecology’, as of the ‘old’, was
succinctly stated by Giller & Gee ( I 987) :
Community ecology may be unique amongst the branches of science in
lacking a consensus definition of the entity with which it is
principally concerned.
Many ecologists reverted to Elton’s ( I 927) usage and preferred to
speak of ‘ assemblage ’. Simberloff (1990) asserted that the switch
to assemblage was due to the notion that community had come to
denote integration and order almost as great as that depicted in
the holistic, superorganismic community of Clements and his
associates ’. The new animal community theory of the 1960s and
1970s had revived the notion of a highly organized community. A
common alternative was that an assemblage was a group of co-
occurring organisms without interspecific interactions, hence
lacking organization or structure (Connell, I 975). Assemblage was
particularly favoured by students of fishes and insects, although
many animal ecologists used it, not always consistently. Cody &
Diamond (1975) had ‘ species assembled non-randomly into
communities ’ and the ‘fine structure of such assemblages ’
determined by physical and biological environment. Dayton ( I 984)
referred to both ‘ very loosely organized assemblages ’ and ‘ well
organized, self-regulating assemblages ’. Grant & Schluter
(1984) similarly refer to ‘ structured ’ assemblages of finch
species. Gee & Giller ( I 987) edited a volume entitled
Organization of Communities with a subhead on Spatial and Temporal
Organization in Contemporary Communities under which were
categories of Terrestrial, Microbial, Decomposer and Aquatic ‘
assemblages ’ most of which included articles about ‘communities’.
O’Connor (1987) had alternatives of ‘communities are random
assemblages ’, or ‘ communities are highly self-organized
entities’. Assemblage by some definitions, avoids any intimation of
interaction among a group of organisms. It begs the question,
however, at what level of interaction have the ‘rules of
organization’, if any, transformed a ‘mere assemblage’ into a
‘closely knit’ or ‘structured ’ community ? The structured
assemblage ’ and ‘random community’ became oxymorons by some
usages.
There is little merit in providing separate terms for a new
dichotomy in ecology for groups of interactive and non-interactive
species. The distinction has already gone the route of other
dichotomies in ecology, such as r and K species, in being described
as a continuum from interactive species to non-interactive species
(Cornell & Lawton, 1992). Community has covered the gamut for
generations of ecologists. If one insists that interactions be
thoroughly understood before recognizing a community there
will
Gleason’s ‘ individualistic concept ’ 329 be very few communities.
Ecologists would be hard pressed to identify a site demonstrably
lacking in interspecific interactions to qualify as an assemblage,
sensu stricto.
Community has commonly served as a catchall for any group of
organisms with terms such as association, guild or biome applied to
sometimes murky ideas about aggregations of organisms. The influx
of animal ecologists into community ecology in the last several
decades added new nuances to the old meanings of community but
often they worked familiar ground. One thing the new community
ecology shares with the old is the lack of a ‘consensus
definition’, as Giller & Gee noted. This lack of consensus
disappointed Pimm (1984) who had hoped for better things following
MacFadyen’s (1963) extended review of definitions. All that came of
it was, he said, the addition of a qualifier e.g. ‘bird community ’
limiting community to ‘this newer definition ’ of organisms on the
same trophic level. Such communities were simply ‘horizontal ’,
whereas Pimm preferred to consider the ‘vertical’ property of
community that extended across two or more trophic levels
appropriate to analysis of food webs. Colwell (1984) described the
traditional definition of community as ‘ no more than a set of
interacting or potentially interacting populations that coexist in
a habitat’. Strong et al. (1984b) also offered a somewhat equivocal
definition : ‘ Ecological communities are groups of species living
closely enough together for the potential of interaction’. The
awkward words are ‘closely’ and ‘potential ’. Wiens (1984b) added
some complicating factors in asserting : ‘Aggregates of populations
and underlying resource systems occurring together in an area over
some period of time make up communities.’
Diamond & Case (19863) provided a ‘flexible’, some would say
‘vague’ definition of community: ‘the populations of some or all
species coexisting at a site or in a region’. Later in the same
volume, Roughgarden & Diamond (1986) considered communities and
recognized as a ‘unifying theme ’ ‘limited membership ’ thus
reverting back to earlier ideas of restricted composition. Schoener
(19863) described the ‘most general ’ definition of community as ‘a
set of species populations that occur in one place’ and said it is
commonly nearly equivalent to ‘guild’, a term with its own
ambiguities (Simberloff & Dyan, 1991).
The nature of community as including horizontal and vertical
interactions, within and between trophic levels, was reiterated by
Kitching (1986) who reasserted the view that a community is a
‘coevolved whole’ continuing the organismic tradition. Yodzis
(1986) ambitiously defined community ‘to mean the set of all living
things at some given location’. He noted the tradition of studying
smaller components of the total community and suggested that too
little has been done to show that such studies make sense; although
such studies have ‘certainly shaped the myths and metaphors in
terms of which we currently think about communities’. Yodzis’s
resolution is to lump the biospecies, with which community ecology
is usually concerned, into ‘ trophospecies ’ comprising several
species with similar food habits. Yodzis, however, reported that
even his simple models when perturbed ‘ are in significant measure
indeterminate when viewed on a relatively long temporal scale ’.
Terborgh & Robinson ( I 986) joined Yodzis and May ( I 976 b)
in anticipating that transtaxonomic recognition of guilds will
become ‘the standard currency of ecologists in their efforts to
understand community relationships ’. Holmes & Price (1986)
defined community as ‘a group of organisms in a particular place,
without any preconceptions on whether they interact or not’.
They
3 30 R. P. MCINTOSH also called on Root’s (1973) categorization of
communities as ‘component communities’ of specific
microenvironments and ‘ compound communities ’ as a ‘ complex
mixture of component communities that interact to varying degrees
’.
Schoener ( 1 9 8 6 ~ ) expressed reservations ‘about adding a new
term to an already jargon-laden biological vernacular ’, but saw no
alternative but to add ‘similia- community’ (from similiu = similar
things). Similia-communities are sets of species in different
places that ‘ are similar with respect to crucial organismic and
environmental traits’. Similarity and its measurement are a
long-term concern of ecology, the crucial question generally being
how similar must things be to be similar or similia- communities ?
Rosenzweig ( I 987) coined ‘ anomic ’ community for a group of
organisms in which the presumed ‘rules of organization’ have not
organized them into a proper community. Like Frederic Clements in
the early era of ecology, Rosenzweig preferred Greek sources and it
is probable that ‘anomic’ community will go the way of most of
Clements’s classic terminology. Giller & Gee ( I 987) provided
a hierarchy of levels of organization in community ecology
(community, subcommunity, guild, taxon guild) and a ‘plea for
consistent terminology’ echoing the sentiments of all too many
earlier ecologists with, perhaps, no more hope of success. Gee and
Giller optimistically noted, ‘ a pleasing parallel between
mathematical models and empirical analyses of the effect of spatial
scale on the perception of the equilibria1 status of the community’
- a parallel not equally apparent or pleasing to other
ecologists.
(4) Key questions for community ecology
Ecology has a long history of questions. Vas ist ein
Pflanzengemeinschaft ? or Why are there so many kinds of animals?
(Hutchinson, 1959), which Schoener (1974) described as a
‘celebrated riddle’: there have been many responses if not answers.
Animal community ecologists in the I 980s produced numerous
additional questions some new, some old, some clear, some abstruse.
A. J. Underwood (1986), Roughgarden & Diamond (1986) and
Southwood (1987) explicitly addressed the old and difficult
question - What is a community ? Underwood argued that study of
community properly deals with species and individuals and wrote ‘it
is probably more profitable for ecologists to pay more attention to
how often, and how consistently, various combinations of species
occur together ’. Study of interactions and interdependence, he
wrote, must be done at several scales ‘without reference to
organized communities or superorganisms ’. Roughgarden &
Diamond agreed with Underwood that community ecology is concerned
with the variety and abundance of organism, in their term ‘ limited
membership ’. The problem has always been what constitutes limited
membership - association, character species, constancy or fidelity
of species in a nearly forgotten lexicon. Limited membership,
according to Roughgarden & Diamond, has three causes all long
familiar to ecologists : physical environment, dispersal limits and
interactions among species. Roughgarden & Diamond posed a
subsidiary question, What is community structure? Structure takes a
bewildering range of meanings and is loosely synonymized with
organization or pattern, each of which has its own nuances
(Connell, 1975). Included in structure, beyond the classical
attributes of spatial and temporal abundance of species
(composition), are resource allocation, niche relations, species-
area, trophic levels or food webs, body size relations, foraging
techniques, age distribution, vertical and horizontal distribution
(literally in space or abstractly in
Gleason’s ‘ individualistic concept ’ 331 trophic levels) temporal
distribution and morphology. A perennial, and perhaps the oldest,
concern in assessment of community structure, or indeed any
attribute of community, was rediscovered by May (1984)’ ‘any
attempt to elucidate patterns of community structure must deal with
the question of how to delimit the community’. For ecologists who
wished to work with real communities rather than mere assemblages,
Hairston (1984) stated ‘The greatest need is for a legitimate means
of identification of interacting groups of species ’.
The major problem of quantification of a community is entitation,
which is often overlooked. Southwood’s ( I 987) answer to ‘What is
a community ? ’ first required that a community be recognized, then
went on to the nature, properties and function of communities
including horizontal links on the same trophic level and vertical
links between trophic levels. He joined Underwood and Roughgarden
& Diamond in asserting that the most fundamental description of
a community is the number of different species and the abundance of
individuals of each. Southwood concluded, noting two of Schoener’s
(1987) seven axes of controversy about community, ( I ) tightly
linked structured groups vs. individualistic groups, (2)
organism-driven (biotic) vs. environment driven (abiotic). His
‘forecast’ is that the poles of neither axis will be the answer
‘for ecology deals with a mixture of pattern and probabilism.
’
Strong et al. (19846) provided a series of ‘contemporary questions
in community ecology’ all turning on interactions of species but
they commented that ‘the most profound issue of contemporary
ecology.. . stochasticity makes deductive answers to these
questions doubly difficult to find’. Nevertheless they raised ‘one
of the ultimate community questions ’ - How do communities really
behave ?
Many questions were generated under the umbrella of the ruling
school of animal community theory of the 1960s and 1970s and
continued into the 1980s. Lewontin ( I 969) had asked, ‘ Can there
be more than one stable community composition in a given habitat?’
Chesson 8z Case (1986) asked ‘To what extent are the attributes of
natural communities predictable ? ’ noting the derivation from
community theory predicated on equilibrium and reviewing new
theoretical directions beginning with a new question ‘What is a
non-equilibrium explanation ? ’ Their answer is in substantial part
damage control for the traditional theories that constructed models
based on competition and stable equilibria. One response to the
evident difficulties posed by the proponents of Gleason’s concept
was to urge pluralism which is progress following an era of
monistic community ecology (McIntosh, 1987). T. Underwood (1986)
raised collateral questions about the worth of community
theory.
How well will the currently available studies stand up when
analyzed by less personally involved historians of ecology at some
point in the future when today’s hypothesis and theory might be as
interesting and relevant as Ptolemy’s? If in the search for new
theory today’s is found wanting, will future ecologists view
today’s experiments excitedly, as an abandoned gold-mine to be
reopened, or as the ideological equivalent of a used-car lot,
littered with the rusty remains of vehicles of self-advancement,
now abandoned by careless speedsters down the vanished highways of
former ecological theory ?
Sadly, Underwood’s ‘message for future historians of ecology is ‘do
not look - spare yourselves ’. Historians, however, find as much
interest in misguided or failed science as in successful
science.
Kitching ( I 986) posed a methodological problem for community
ecologists claiming
332 R. P. MCINTOSH that to answer community-level questions one
must carry out community level studies rather than make inferences
from lower level population studies. Carpenter (1989) applied this
rule to the study of lakes. Rosenzweig (1987), to the contrary,
asked ‘ Is it possible to learn anything useful about large systems
of interactions by focusing on one ? ’ He suggested a mathematical
theorem that ‘ proves that one can make accurate inferences about
the dynamics of entire systems just by studying (carefully) the
dynamics of any single species that belongs to it’. However, he
leaves the original question unanswered leaving the reader to
wonder why he brought it up at all.
Schoener ( 1 9 8 6 ~ ) addressed the question that is at the hub of
the traditional debate between Clements and Gleason and their many
successors. Is each community effectively unique, or is there a
modest number of ‘types ’ of communities ? Diamond & Case
(1986b) asked the same question and, foregoing the hope of devising
a model that would apply to all communities, expressed a more
modest hope that it might be possible to ‘devise a model for each
type’. Bush & Aho (1990), in an attempt to summarize a
symposium on parasite communities, generalized that there had been
no central conclusions offered but emerged with a unifying central
question - What happens to empty space? - the classical question of
succession.
Some questions raised by animal community ecologists are more pithy
if not more clear than those posed above. Rathke ( I 984), for
example, asked ‘ Quo Vadis ? ’ calling on the abilities of her
readers in Latin as well as in speculation about the future.
Rathke’s response to her rhetorical question was that random models
had led to rejection of a competition hypothesis about flowering
phenology. Colwell (1984) was similarly cryptic, but at least in
plain English, asking ‘What’s New ? ’ What was new was a move
toward a community ecology that rejected the basic assumptions on
which the mathematical theory of ecology of the 1960s and 1970s was
erected, leading to the ‘Death of the “old ecology”?’. The question
mark possibly implied that it wasn’t surely dead and, like Count
Dracula, might be around to haunt its opponents, as it has.
Schoener (1987) identified seven axes of controversy in community
ecology that provide a summary of the history of community ecology
and of the several recent articles asking the grand question -What
is a community?, or inquiring about the nature of community.
Schoener’s axes orient the empirical studies on axes different
from, or complementary to, the classical organismic-individualistic
community axis. Several of Schoener’s seven axes may be seen as
implicit in the classical axis but segregated out of it in the
context of more recent disputes and disputants in community
ecology. Others are not neatly seen as part of the classical
dichotomy. The poles of several of Schoener’s axes, e.g.
unpatterned, vs. patterned, random vs. nonrandom, physical vs.
biological, interactive vs. noninteractive, do not match the
classical axis. Both organismic and individualistic communities are
patterned but in quite different ways, organismic communities are
non-random but so are Gleason’s individualistic communities,
contrary to a common misrepresentation. Schoener suggested two
‘emollients’ for the scars of controversies that have developed in
community ecology over the several axes he outlines. First, a
pluralistic approach which is tolerant of variation among
communities and ‘many faceted theory’. The second is a mechanistic
approach for a theory of community ecology based on concepts from
lower levels, which is what ecologists usually mean by
reductionism.
Hengeveld ( I 988) considered deterministic vs individualistic
hypotheses of
Gleason’s ‘ individualistic concept ’ 333 biological invasions in
the context of community theories. Hengeveld argued that species
invasions can be viewed as individualistic species responses, a
position clearly kin to Gleason’s. Russell (1992) tried to bridge
the gap asking, ‘How does an assembled community fit into the
concept of spatial and/or temporal continua? ’ The questions about
trophic controls posed in the famous HSS (Hairston et al., 1960)
article continued to exercise ecologists and a new set of
terminology was introduced to ecology in its wake. Keystone species
gave rise to trophic cascades and discussions of top-down versus
bottom-up control of community, usually in aquatic communities.
Strong (1902) asked, ‘Are trophic cascades all wet ? ’ but
described finding forces extending through as many as four trophic
levels as ‘one of the most important in all of ecology of the last
decade ’.
The ‘enduring debate in American ecology about the nature of the
biological community’ (Richardson, I 980), ‘temporal schizophrenia’
(A. J. Underwood, I 986), ‘current uncertainties and controversy in
community ecology ’ (Southwood, 1987) and seven ‘axes of
controversy’ (Schoener, 1987) persisted through the 1980s and on
into the 1990s. Many studies of diverse taxa or habitats addressed
the grand questions of community just described. Some commentators
on ecology deplored the tendency of ecologists to ask such large
questions. Price ( 1 9 8 6 ~ ) offered a ‘critical review of
questions and approaches and attributed the controversy to ‘
miscommunication fueled by failure to focus on well-defined
questions’. Slobodkin (1986) suggested the possibility that ‘the “
big questions’’ of ecology are simply too big to be answered’. He
advocated ‘ minimalism ’ or choosing the smallest questions
recognizable in a professional field. Peters (1991), in a
universally negative critique of ecology, stated that ecologists
must shun unanswerable or intractable grand questions. Among his
bad examples was ‘What is a community? ’ Community ecologists,
nevertheless, addressed questions large and small and, as Slobodkin
noted, this may add to the ‘volume and vituperative quality ’ of
current ecological publications. Slobodkin ( I 992) wrote, ‘Ecology
may be the most intractable, legitimate science that has ever
developed’, an unpromising prospect for community ecologists who
engage in the most complex aspects of ecology. Menge (1992)
deplored the tendency of ecologists to pose questions like ‘ Do
top-down (e.g. trophic interactions) or bottom-up (e.g. nutrients)
effects control communities ? ’ He allowed that both could affect
community structure and more modest questions should ask how, or
when, they interact and what mechanisms operate in each.
( 5 ) Empirical studies of communities
Numerous empirical studies of animal communities of diverse taxa
and habitats provided a spectrum of evidence and interpretations
concerning community in the 1980s. These ranged from explicit
support of either pole of the traditionai axis to various positions
that ranged from intermediate to indeterminate. The number of
studies in each of the three groups was roughly the same, no
position enjoying a plurality. Proponents of either extreme, or the
intermediate positions, appeared in studies of all major taxa and
many different habitats. Examples of these are considered below in
sequence : ( I ) those at or near the individualistic, Gleasonian,
or continuum pole; (2) those at or near the organismic,
Clementsian, deterministic pole; and (3) those intermediate or
variable.
334 R. P. MCINTOSH Wiens & Rotenberry (1981) concluded that few
significant correlations were evident
among breeding birds of shrubsteppe, ‘suggesting that bird
populations in this system vary largely independently of one
another ’. James et al. (I 984), noted that the niche of the wood
thrush was more aligned with the individualistic approach of
Gleason. Bock (I 987) wrote of Arizona land birds :
It is apparent that these assemblages usually are dominated
numerically by widespread species whose past histories and present
dynamics cannot have anything to do with communities as we have
delimited them. This leads me to advocate an individualistic
approach to avian ecology.
Wiens (1989) assembled two volumes on ecology of bird communities.
He noted the dominance of the competition - based ‘ MacArthurian
paradigm’ in the 1960s followed by increasing studies of species
characteristics. According to Wens :
This pattern may be a manifestation of the resurgence of an
individualistic Gleasonian view of communities among ecologists at
that time, a movement that apparently did not influence those
publishing in ornithological journals.
Marine biologists had long participated in discussion of the nature
of community (McIntosh, 1967, 1985). Dean & Hurd (1980)
continued the tradition applying the continuum concept to the
marine fouling community. Williams et al. (1981) were more extreme
finding distributions of marine planktonic diatoms were ‘ entirely
probabilistic’. They looked enviously at terrestrial ecology where
they said ‘the meaning of the term “community” can largely be rid
of ambiguity’, a situation not apparent to terrestrial ecologists.
Gray (198 I) asserted that the continuum viewpoint agrees with most
marine benthic studies. Jones (1984) asserted that absence of
classificatory groups in coral-reef sediments showed that community
composition varies continuously along a sedimentary gradient.
According to Sale (I 984) presumed orderly patterns of animal
communities in coral reef fish were not true. There was, he wrote,
little evidence of biotic interactions influencing distributions
and ‘ assembly rules, if they exist, must be very subtle’. Dean
& Connell(1987) stated that patterns of a marine invertebrate
community did not meet predictions based on expectations of a
highly organized community. The community was unorganized, with
only predation possibly important but it was weak. Ebeling &
Lauer (I 986) offered an individualistic explanation of resource
partitioning in surf perches.
Freshwater biologists commonly described various communities as in
accord with the individualistic hypothesis. Reice (1980) wrote that
benthic fauna supported ‘the individualistic hypothesis of
community structure, common in plant ecology, dating back to
Gleason (1926)’. Matthews & Hill (1980) wrote that stream fish
‘species associations were transitory ’ with ‘ a few stable
interspecific interactions ’. Grossman et al. (I 982) deplored the
‘ overburdened ecological vernacular ’ and attempted to clarify it
in finding that stream fish assemblages were regulated by
stochastic factors. Yant et al. (I 984) argued that Grossman et al.
had biased their results by using an atypical site. Rahel et al.
(1984) and Herbold (1984) asserted that Grossman et al. had used a
faulty definition of the fish assemblage and studied it at the
wrong scale, an increasingly frequent accusation in the 1980s.
Grossman et al. (1985) rebutted each criticism saying their
conclusions had only been strengthened by the exchange. Matthews (I
982) found no more structure of fish communities than random
aggregation with little interspecific interaction. Heins &
Matthews (I 987) provided an historical perspective on studies
of
Gleason’s ‘ individualistic concept ’ 335 ‘North American stream
fish communities’ noting that by the late 1970s ecologists were
being cautioned against an uncritical acceptance of competition as
structuring fish communities. Norton (1991) said that patterns of
distribution and abundance of cottid fishes are more consistent
with Gleason’s individualistic concept than with a ‘ synecological
mechanism ’.
Mammal communities were frequently exploited in examining community
questions in the 1980s (Morris et al., 1989). Dueser & Brown
(1980) thought that competition was insufficient to structure a
community of rodents by assembly rules. Dueser & Porter ( I
986) found competition in a small mammal community, although
ubiquitous, was relatively weak. Brown & Kurzius (1987) noted
that recent discussions of animal communities continued the
traditional Clements vs. Gleason debate. They put animal ecologists
R. MacArthur, J. Diamond and P. Grant in the Clements camp and a
largely botanical group, R. Whittaker, L. Cole, B. Huntly and H. J.
B. Birks, in the Gleason camp. By 1987 numerous animal ecologists
might have been added to the Gleason camp. Brown & Kurzius,
themselves, noted that desert rodents were distributed
individualistically making co-evolution unlikely and efforts to
study ‘assemblages of many species in terms of pair-wise
interactions ’ ineffectual or even ‘ misleading’. Owen (1990)
described mammals in Texas as fortuitous assemblages and wrote
:
This supports the concept of an open community of mammals analogous
to that espoused by phytosociologists. Spatial structure of
mammalian distributions is thus concordant with the continuum
concept of community.
Studies of amphibian and reptile communities proliferated in the
1970s and early 1980s (Toft, 1985). Scheibe (1987) studied
temperate lizard communities comparing field data with randomly
generated null communities and found ‘no evidence to support the
limiting similarity hypothesis ’ associated with communities
structured by competition. Haefner (1988) compared a range of
random and competition models with data of Anolis lizards.
Competition models were no better than some random models Gascon
(1991) assessed distribution of rain forest tadpoles and produced
an interesting concatenation of Gleasonian ideas.
Insects of diverse taxa and habitats were studied to address
community questions. Vepsalainen & Pisarski (1982) found that
ant communities did not fit into ideas of assembly processes and
that early arrival was an important consideration. Boecklen &
Price (1989) studied sawfly ‘assemblages’ on willow clones and
found that every clone had a unique arrangement of sawflies with
independent species responses. Gilbert & Owen (1990) denied a
Clementsian ‘holistic vision’ of community and provided a
remarkable parallel to Gleason’s ideas :
We believe that any ‘structure’ is a biological epiphenomenon, a
statistical abstraction, a descriptive convention without true
emergent properties but only collective ones, wholly referable in
its properties to those of the constituent species, populations,
and individuals. Thus we believe that animal ecology is learning
what plant ecologists learned many years ago.. . , and lean to the
view that at least some communities of syrphids are merely
coincidences of species in space and time.
Perhaps the major contribution of paleontology to ecology stems
from consideration of micro- and macro-fossil communities. Birks
(1981), Davis (1986), and others, found that putatively stable or
climax communities of Clements segregated into species that
336 R. P. MCINTOSH migrated separately to different refugia in the
Pleistocene. Springer & Bambach (1985) began a study of marine
invertebrate fossils with a review of Gleasonian and post-
Gleasonian concepts. They found ideas of discrete communities less
informative than gradient analysis and no evidence that species
interdependence was important in community structure. Janssens et
al. (1986) found fossil mosses, that had once coexisted, occurred
in very different phytogeographic contexts. They wrote :
Such fossil records support Gleason’s ( I 926) individualistic
concept of vegetation, the uniqueness of past communities (Birks
1981) and the short term nature of vegetation units.
Graham (1986) found individualistic responses of mammalian species
during the late Quaternary, the species having been ‘massively and
repeatedly reshuffled ’ . Coope ( I 987) interpreted insects in the
late Quaternary as forming individualistic species associations
:
It is clear that the insect community did not react en bloc as an
integrated whole, but each of its component species responded by
moving at its own rate as the climate underwent rapid and intense
changes.
In contrast to the foregoing, many ecologists supported concepts of
organized and integrated communities often in the same taxa and
habitats used to demonstrate individualistic communities. Haefner (
I 98 I ) found well defined community structure in birds, the
species being clustered according to rules. Noon (1981) inferred
that competition was important in a community of thrushes. Moulton
& Pimm (1986) found evidence of extensive competition in avian
communities and recalled the ‘ intellectual blood spilled’ in
earlier debates about the need for a null hypothesis.
Marine biologists also discerned kinds of community concepts. Mook
(1981) interpreted marine fouling organisms converging to the same
community. Perks (1982) preferred organismic ideas to continuum
concepts in marine communities. Dayton et al. ( I 984) expressed
hope for a Clementsian deterministic stability of kelp communities
that offered some hope, perhaps, to animal ecologists. Pearson
& Rosenberg (1987) emphasized the importance of food in marine
benthic communities and claimed that succession of these
communities was predictable and produced characteristic
communities.
Freshwater communities of diverse types were sometimes interpreted
as organized, integrated, distinct entities. Naiman et al. (1988)
found:
Compelling reasons for examining the stream-river profile as a
series of discrete patches or communities with reasonably distinct
boundaries rather than a gradual gradient or continuum.
Tonn & Magnuson (1982) found fish ‘assemblages’ in northern
Wisconsin lakes resulted from deterministic mechanisms. Power 8z
Matthews (1983) gave evidence of vertical structure or ‘trophic
cascade’ in a sequence of effects of piscivorous bass on
herbivorous minnows affecting attached algae. Moyle & Vondracek
(1985) found a fish ‘assemblage’ with the characteristics of a
‘highly structured community’. Matthews et al. (1988)’ contrary to
some of Matthews earlier studies, found persistent and stable
faunas and many individual locations had relatively stable fish ‘
assemblages ’. Wikramanayake ( I 990) argued a co-evolutionary
adjustment in a tropical stream ‘assemblage’ to reduce
interspecific competition. According to Meffe & Sheldon (1990)
fish ‘ assemblages ’ recovered following defaunation. They wrote
:
Gleason’s ‘ individualistic concept’ 337 These assemblages were not
randomly structured units but were largely deterministic systems
highly predictable from local habitat structure.
Kodric-Brown & Brown (1993) examined relative importance of
deterministic and stochastic factors in assembly of fish
communities of desert springs in Australia. They concluded that ‘
ecological relationships that determine community structure may be
highly deterministic with the proviso, ‘When the influence of
historical and environmental factors can be assessed ’. Gilliam et
al. ( I 993) reported that interspecific interactions structured a
stream fish community in tropical Trinidad.
Amphibian and reptile communities also illustrated the extremes of
interpretations. Woodward (1983) found anurans of desert ponds were
segregated into species characteristic of temporary and permanent
ponds which he attributed to predation ‘operating in the past ’.
Wilbur ( I 984) suggested that contemporary predation determined
frog survival in long-lived ponds, whereas competition was more
important in short-lived ponds. Roughgarden (1986) asserted:
Now there is no doubt that interspecific competition occurs between
anoles and that its strength depends on the similarity in body size
of the species.
Southerland ( I 986) noted the controversy about equilibrium
(competition based) and non-equilibrium (non-interactive)
communities and claimed that salamanders of streamside habitats
occurred as discrete ‘ assemblages ’ representing the former.
Insect communities were seen as organized less frequently than
those of other taxa. Joern & Lawlor (1980) asserted that
resource use patterns of grasshoppers were not ‘ merely the result
of fortuitous occurrences among the individual species but reflect
biotic interactions among these species’. Lawton (1984) suggested
that the insect community on bracken fern was predictable and
controlled by density dependent events operating independently of
other species, at least those on the same trophic level.
Fossils were also interpreted as organized communities in some
instances. Van Devender (1986) called on the ghost of competition
past to explain niche separation in Pleistocene packrat middens.
Webb ( I 987) applied rules of assembly and disassembly to Cenozoic
mammals and reported faunal equilibrium that ‘ implies the
probability of higher-structured (interactive) tetrapod
communities.
Many ecologists got mixed or equivocal signals from their data, and
some warned against undue expectations of either extreme of
individualistic or organized community. Schemske & Brokaw
(1981) compared bird distributions in treefall gaps and closed
forest and found some species in either but ‘the majority of
species overlap broadly along the gap-mature continuum’. Grant
(1986) wrote ‘we are far from being able to generalize confidently
about the frequency and intensity of competition for food among
these birds, or indeed among any animals’. Homes et al. (1986)
struck a plural view of community structure between competition
models and non-equilibrium models, although they found little
evidence of a tightly organized community of birds at any one
spatial scale.
In marine communities less explicit positions were also
encountered. Venrick (1982) attributed individualistic
distributions to the ghost of competition past but identified two
distinct recurring associations of species. Grossman ( I 982)
expressed surprise that fish in a rocky intertidal habitat fitted a
deterministic model but algal and invertebrate ‘ assemblages ’ were
stochastically regulated. Fenchel ( I 987) described a community
of
338 R. P. MCINTOSH microorganisms as species populations that
interact or are confined in space or time but indicated that scale
of size and interaction time restricts the likelihood of strong
interaction. Wilson ( I 99 I ) argued that soft-sediment
communities required a distinct paradigm but that at present a
unifying theory of such communities is not attainable.
Freshwater communities produced similarly equivocal or variable
results. Hockin ( I 982) interpreted the copepod community as
switching from a non-interactive community in spring to an
interactive community in a time of less disturbance. Beckett &
Miller (1982) described two endpoints of an invertebrate community
with composites of individualistic species responses in between.
Minshall et al. (1985) described the stone dwelling fauna of
streams as changing from equilibrium status in summer to non-
equilibrium in autumn. Hildrew & Townsend (1987) said that
neither deterministic or stochastic factors in structure of
freshwater benthic communities was primary. Wevers and Warren ( I
986) explored the unlikely possibility of ‘ integrating organismic
and individualistic views ’ of stream communities. They considered
the stream community as organized hierarchically as a group of
subsystems on five levels which, they said, are indistinct.
Freshwater fish communities produced similarly variable
interpretations. Peckarsky & Dodson (1980) suggested that
stream community structure differed in ‘harsh ’ (physically
controlled) streams from ‘benign ’ (biotically controlled) streams.
In the latter, competition is mitigated by predation that reduces
populations of prey. Schlosser (1985) allowed that both
deterministic and stochastic factors regulate stream fish ‘
assemblages ’. Tonn ( I 985) conjectured that factors determining
fish community structure differ from ‘assemblage’ to ‘assemblage’,
season to season and year to year. Grossman ( I 990) reviewed the
thorny question of ‘ assemblage ’ stability in stream fishes noting
a lack of concensus which remains as a spur to further
investigation.
Ross ( I 986) reviewed resource partitioning in fish ‘ assemblages
’ from seven global habitats, including freshwater streams, lakes
and the oceans, based on the literature from 194-1983. The pace of
events is evident in Ross’s bibliography, which includes 5 articles
from 1940-50, 7 from 1951-60, 23 from 1961-70, I I I from 1971-80
and 63 from 1981-83. Ross stated that differential resource use is
widely documented but underlying mechanisms are ‘obfuscated ’ which
showed ‘the difficulty of formulating broad generalizations of
community control ’.
Students of parasite communities introduced the terms ‘ interactive
’ and ‘ isolationist ’ to the community lexicon (Price, I 984b).
Isolationist communities are dominated by individualistic responses
with weak interspecific interactions. Interactive communities are
dominated by interspecific interactions and are closed (saturated).
Bush & Holmes (1986) said that helminth communities of lesser
scale formed a continuum between interactive and isolationist
extremes. Kennedy et al. (1986) found helminth com- munities in
fish were isolationist, whereas those of birds were interactive.
Holmes ( I 990) considered the poles of isolationist and
interactive communities and asked : ‘Where along this continuum do
communities of gastrointestinal parasites lie ? ’ Not surprisingly,
the answer was, ‘The evidence is contradictory’. Aho ( I 990)
reported that helminth communities of amphibians are
characteristically non-interactive or iso- lationist, but the
infracommunity helminth community in birds could be determined by
either biotic or stochastic processes.
Efforts to clarify the controversy concerning community
organization were
Gleason’s ‘ individualistic concept ’ 339 complicated in some sense
by Schoener’s ( I 987) multiplying the axes from one to seven.
Hubbs’s (1987) summary of the symposium in which Schoener’s paper
appeared responds to a question posed by one of Schoener’s
axes.
Are stream fishes regulated by stochastic or deterministic factors?
The proper answer is yes. Depending on circumstances stochastic or
deterministic factors are the most important. The interesting
questions now revolve about when and where do the controls
differ.
Strong et al. ( I 984a) recognized a spectrum of theoretically
ideal communities from essentially random assemblages with little
density dependence to highly deterministic systems, ‘structured by
strong interspecific competition’. They found only 38-39 yo of
herbivorous insect populations were not density dependent but
populations fluctuated markedly between generations and ‘
communities of phytophagous insects are only moderately constant in
their structure’. Wilbur (1987) joined other ecologists in writing:
‘A general answer to the classic question in community ecology of
what regulates the distribution and abundance of species remains
elusive ’. Wilbur’s results, he said, suggested ‘the futility of
arguments between proponents of predation and competition as the
single unifying force structuring communities ; and he asserted the
importance of chance events in structuring communities.
The above review of animal community studies, although incomplete,
makes evident the lack of concensus lamented by Giller & Gee
(1987). Interpretations of community pattern, structure or
organization, and the reasons therefore, ranged from firmly
deterministic, integrated communities based on biotic interactions,
or the ghosts thereof, to explicitly individualistic communities
predicated on interactions of species with their abiotic and biotic
environment coupled with stochastic events. Rarely, a group of
species was seen as approaching the null model of a random
aggregation; more frequently it was somewhere between the
integrated-individualistic poles.
IV. COMMUNITY THEORY AND QUESTIONS FOR T H E 1990s In the mid 1980s
an anonymous editor posed the rhetorical question. ‘Community
ecology: back on its feet again? If volume of research activity and
publication addressing the myriad questions posed about community
were the basis for answering the editor’s question, the answer
would have been a resounding -Yes! If achieving consensus on
defining community and its terminology, agreement about the
existence of community structure and about processes or ‘ rules ’
that structured communities were the criteria, the answer would
have to be - No! Questions concerning communities persisted.
Williamson ( I 987) asked, almost plaintively, ‘Are communities
ever stable ? ’ Crawley ( I 987) asked ‘ What makes a community
invasible ? ’ J. H. Lawton ( I 987) asked ‘Are there assembly rules
for successional communities ? ’
Perhaps the most cogent, if least tractable, question was the
oldest - What is the community ? The many definitions reviewed
ranged from simple groups of closely related taxa to grandiose
representations about all species in a specified site. Many of the
characteristics ascribed to community (richness, diversity,
stability, etc.) depended in the first instance on the entity
chosen for study. Not a few criticisms of studies reporting
community attributes were based on claims that the original study
was dependent on a biased or non-representative choice of study
area and the now frequent
340 R. P. MCINTOSH problem of scale. A corollary of the above
question is whether the community studied at a particular site (the
concrete community of an older if not wiser literature) is a
replicate of a larger community repeated at different sites (the
abstract community of the earlier lexicon, now sometimes designated
as meta-community). Depending on the response to these questions is
whether the functions of any species as a member of the community
are to be described specifically as in Charles Elton’s famous
analogy, ‘There goes the vicar’. That is, do species have
functional attributes that mandate certain combinations of species
and numbers of individuals in repeated instances of a
community.
The questions that are engaging the attention of animal community
ecologists in the 1990s were posed in the late 1980s and commonly
involve a search for ‘rules’. ‘Are there assembly rules for
successional communities ? ’ (Lawton, 1987). In a broad sense this
is in the tradition emanating from Frederic Clements who posited
‘laws’ of community formation in the early decades of the twentieth
century and perpetuated by animal ecologists, notably Eugene Odum (
I 969)’ who anticipated an orderly, predictable process of
succession, community development or community assembly. Lawton’s
response to his question is that there are some broad rules but the
details are ‘fuzzy’.
Distinguishing between the effects of chance and determinism on
community assembly undoubtedly constitutes one of the most
important and difficult problems in contemporary ecology.
Although ‘assembly rules’ as described by Diamond (1975), and the
theory and empirical studies of community on which they rested, had
been severely criticized throughout the I 980s, the search for
assembly rules and many of the assumptions about community on which
they rest persisted unabated. Brown (1987) suggested that the
functional organization of communities could be characterized by
two classes of rules. ‘ Capacity rules ’ include all extrinsic
processes, both physical and biotic, that affect the capacity of
the environment to support the community in question. ‘Allocation
rules’ are biotic interactions, such as competition, intrinsic to
the community. Brown stated that extrinsic rules ‘ultimately
determine the outcome of the interactions within the assembl