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Exclusion Or Coexistence and the Taxonomic Or Ecological Relationship Between Species

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Exclusion Or Coexistence and the Taxonomic Or Ecological Relationship Between Species EXCLUSION OR COEXISTENCE AND THE TAXONOMIC OR ECOLOGICAL RELATIONSHIP BETWEEN SPECIES by P. J. DEN BOER (Biological Station of the Agricultural Universityof Wageningen,Wijster, The Netherlands) SUMMARY The history of the "principle of competitive exclusion" is briefly reviewed. Next, it is shown that taxonomically closely related (carabid) species, i.e. species in the same genus, can indeed be considered to be also ecologically closely related. This opened the possibility to test whether or not exclusion plays a demonstrable role in the distribution of species belonging to the same or to different genera over different habitats. The method used was proposed by SIMPSON(1949) and applied for the first time by WILLIAMS(1951). With the help of the pitfall-catches of 149 carabid species during nine years and in 73 different habitats, and by using three, different "values" it could thus be shown that congeneric species coexist more frequently in the same habitats than could be expected from a random distribution of the available species over habitats. This "coexistence principle" was further illustrated by two examples from habitats studied during a number of years. It could also be shown that interaction groups of coexisting congeneric (carabid) species do not die out more frequently than those of species belonging to different genera, not even in the course of a century. These findings are thus in agreement with the conclusion of BIRCH(1979) from a review of the field evidence, that "competitive exclusion" must be considered an only exceptional outcome of the possible interactions between species. The most parsimonious hypothesis for understanding the findings discussed in this paper therefore is: Taxonomically closely related (carabid) species are also ecologically closely related, and will thus more often than not be found coexisting in the same habitats. 1. INTRODUCTION During many years already I have been puzzled by the thoughts of ecologists who have apparently access to knowledge about "laws of nature" which seems not to be obtained from a comparative study of a large number of populations. To give an example, NICHOLSON ( 1954) deduced, that populations must be "regulated by density-governing factors", which will keep population density "in a state of tending towards a position of equilibrium" (i.e. "a state of balance"). This seems to be more than a hypothesis that can be tested and thus possibly (communication no. 214 of the Biological Station, Wijster) 279 rejected (see discussion following REDDINGIUS, 1971b), for NICHOLSON (1933, p. 133), also stated: "populations must exist in a state of balance for they are otherwise inexplicable" (see also: REDDINGIUS, 1971a, p. 12). Of course, with "for they are otherwise inexplicable", NICHOL- SON wants to say: "for otherwise they would not be in keeping with my presuppositions". A predominant one among these presuppositions seems to be the expectation that population density will persist between finite and positive bounds, or in the words of NICHOLSON ( 1958) : in the centre of distribution "density-governing reaction permits a species to persist indefinitely in all favourable places". REDDINGIUS ( 1971 a) con- vincingly showed that under not too unrealistic conditions (i.e. in a not completely constant and homogeneous environment) "density govern- ing reactions" cannot even theoretically be expected to accomplish this job. In addition to this DEN BOER (1979) showed that also in nature populations-taken as "interaction-groups" (see also BAKKER, 1971)- do not persist, but die out and are (re)founded more or less frequently. See also: DIAMOND ( 1979) . A "law of nature", arisen in a comparable way by deduction from a presupposition, is "the principle of competitive exclusion". Although for a considerable time already I have data at my disposal that indicate that under more or less natural conditions related carabid species as a rule do not exclude each other, either because they do not compete or because other "factors" are apparently more important than a possible interference, up to now I was not highly motivated to devote a paper to this subject, because "the principle" is gradually disappearing now from the ecological literature. After reading the review of the present field evidence on exclusion and coexistence by BIRCH (1979), however, I thought it useful to support his conclusions and considerations by presenting another type of data, at the same time recalling attention to some papers of WILLIAMS (1947, 1951) which appear to have been generally overlooked by field ecologists. 2. THE EXCLUSION PRINCIPLE 2.1. History In fact, the exclusion principle was already given the status of a "law of nature" by DARWIN (1859, 6th ed. 1888), who clearly was of the opinion, that species with similar needs cannot coexist; the competi- tively inferior species will be eliminated by the superior one (s) . GRINNELL (1904) for the first time connected this principle with the concept of "niche". He wrote: "Two species of approximately the same food habits are not likely to remain long evenly balanced in numbers in 280 the same region", and drew the conclusion: "It is, of course, axiomatic that no two species regularly established in a single fauna have precisely the same niche relationships". VOLTERRA and LOTKA gave the principle a mathematical base (see: ScuDO & ZIEGLER, 1978) by modelling exclusion as the outcome of competition for a resource in short supply under fairly severe, limiting conditions. GAUSE ( 1934) showed that exclusion may indeed occur in model experiments, in which the conditions underlying the Lotka- Volterra-equations are approximated as closely as possible. A sympo- sium of the British Ecological Society (ANONYMOUS, 1944), where the question was considered: "Can two species with similar ecology live together in the same place?", was the start of a considerable number of publications on this subject. Most of these papers dealt with compe- tition experiments carried out in the laboratory under constant con- ditions (for a review see e.g.: AYALA, 1970). By historically interpreting special cases of the geographical distribution of taxonomically related species (mainly birds) some other authors tried either to support the "principle of competitive exclusion" (e.g. LACK, 1946, 1971), or to question its generality (e.g. MAYR, 1942, 1963). Field experiments and field observations with the aim to actually test this principle were mainly started more recently (for a review see: BIRCH, 1979). Only a few ecologists severely critized the principle (e.g. ANDREWAR- THA & BIRCH, 1954; COLE, 1960). They think it to be either trivial or invalid, depending on how it is formulated. If it is formulated in the sense OfSLOBODKIN (1961, p. 122): "If two species persist in a particular region it can be taken as axiomatic that some ecological distinction must exist between them", the principle is true, but trivial. If it is re- versed in the sense, that two species with identical ecological require- ments cannot coexist, it is invalid, since two species, whether coexisting or not, will not have exactly the same requirements. The latter will not even be true for two individuals from a bisexual population (see further: AYALA, 1970). 2.2. Laboratory tests The explanatory value of a theory or hypothesis will directly depend, of course, on the number and admissibility of the underlying assump- tions, To study these assumptions we start from one of the more strin- gent formulations of the principle (see e.g. ELTON, 1927) in which it is said that two species cannot coexist if they share one or more resources essential for the survival of the species. Frequently, but not always ex- plicitly, the shared resource (s) is (are) also required to be in short supply for the greater part of time. In the mathematical formalizations of LOTKA & VOLTERRA (see ScuDO & ZIEGLER, 1978) this is indeed sup- 281 posed, whereas the biologically most unrealistic assumptions concern the environment common to the competing species: it should be homo- geneous and constant in all respects, and it must be "closed" (i.e. no immi- and emigration). In many relevant laboratory experiments in which these assump- tions were satisfied as good as possible these indeed appeared to be sufficient conditions to bring about the extermination of one of the species (e.g. GAUSE, 1934; CROMBIE, 1945; PARK, 1948, 1954; MER- RELL, 1951; BIRCH, 1953), though some of these exclusions took a remarkably high number of generations (e.g. PARK, BIRCH). However, many of these experiments also showed the above conditions to be necessary ones: a small change in pH (GAUSE), in temperature and/or moisture conditions (PARK, BIRCH) may be sufficient to transfer the advantage from one species to the other. A periodical fluctuation in the quality of the food may give two Drosophila-species the opportunity to coexist permanently (MERRELL). Coexistence can also result from a small difference in "life tactics" between the species concerned, i.e. Rhizopertha-Oryzaephilus (CROMBIE) ; Paramecium caudatum (or aurelia)- P. bursaria (GAUSE), and/or from the introduction of small hetero- geneities in the environment, e.g. small glass tubes in the culture medium of Tribolium-Oryzaephilus (CROMBIE). For more details, see: ANDREWARTHA & BIRCH (1954, p. 421-433). A more recent example of this kind was even presented as "experimental invalidation of the principle of competitive exclusion" (AYALA, 1969). A discussion in Nature led to the statement, that the (small) fluctuations in temperature permitted to occur in the incubators "will have exerted large selective pressures, by which a state of disequilibrium was maintained" (Bo- ROWSKY, 1971). This conclusion was refuted again by AYALA ( 1971 ), but the fact remains, that his Drosophila-species coexisted under experi- mental conditions that only slightly deviated from those necessarily dictated by the generally favoured (simple) competition model (or by a non-linear version of it: GILPIN & JUSTICE, 1972). 2.3. Exclusion in the field Hence, even under biologically fairly unrealistic conditions (in a closed and nearly constant and/or nearly homogeneous environment) the exclusion principle seems not to be a "law of nature".
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