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Home , Balance of nature, Character displacement, Competition (biology), Predation, Species richness

TREE vol. 1, no. I, July 7986

could be expected to rise periodically some other nuclear power stations 6 Bumazyan, A./. f1975)At. Energi. 39, (particularly during the spring snow are beinq built much nearer to these 167-172 melting) for many years. than the Chernobyl station to 7 Mednik, LG., Tikhomirov, F.A., It is very likely that the Soviet Kiev. The Chernobvl disaster will Prokhorov, V.M. and Karaban, P.T. (1981) Ekologiya, no. 1,4C-45 Union, after some initial reluctance, affect future plans, and will certainly 8 Molchanova, I.V., and Karavaeva, E.N. will eventually adopt the same atti- make a serious impact on the nuclear (1981) Ekologiya, no. 5,86-88 tude towards nuclear power stations generating strategy in many other 9 Molchanova, I.V., Karavaeva, E.N., as was adopted by the United States countries as well. Chebotina. M.Ya., and Kulikov, N.V. after the long public enquiry into the (1982) Ekologiya, no. 2.4-g accident at Three Mile Island in 1979. 10 Buyanov, N.I. (1981) Ekologiya, no. 3, As well as ending the propaganda of Acknowledgements 66-70 the almost absolute safety of nuclear The author is grateful to Geoffrey R. 11 Nifontova, M.G., and Kulikov, N.V. Banks for reading the manuscript and for power and labelling them as (1981) Ekologiya, no. 6,94-96 comments and editorial assistance. 12 Kulikov, N.V. 11981) Ekologiya, no. 4, ‘potentially dangerous’, the US gov- 5-11 ernment also recommended that 13 Vennikov, V.A. (1975) In new nuclear power plants be located References Methodological Aspects of Study of in areas remote from concentrations 1 Medvedev, Z.A. (1979) Nuclear Disaster Biosphere(in Russian), pp. 55-71, of . The official Soviet in the Urals, W.W. Norton Moscow policy until the Chernobyl disaster 2 Trabalka, J.R.,Eyman, L.D.,and 14 Polushkin, K. (1980) Nauka iilhizn, no. did not take the Three Mile Island Auerbach, S.I. (1980) Science, 209,345 11.44-52 lesson into consideration. The long 353 15 Devel, L., Tovedal, H., Bergstrom, U., 3 Soran, D.M., and Stillman, D.B. (1982) Appelgren, A., Chyssler, J. and term planning continued to locate An Analysis of the Alleged Kyshtym Andersson, L. (1986) , 321, nuclear energy plants of different Disaster, Los Alamos National Laboratory 192-193 types (including the fast breeders) Report LA-9217-MS 16 Beardslev. T. 119861 Nafure. 321. 187 near large cities in order to heat 4 Die Presse, March 18,1959. Vienna 17 Aleksakhin, RIM., and Naryshkin, M.A. towns centrally with hot . 5 Gus’kova, A.K. (1967) Med. Rad. 7 7, (1977) Migration of Radionuclides in Voronezh, Gorky, Leningrad and 53-64 ForestBiocoenosis (in Russian), Nauka

Since Darwin accepted the Malthu- ThePresent Status of the Competitive Sian population theory to solve the demographic problems he thought to be logically connected with the ExclusionPrinciple universal operation of natural selec- tion, the numerical processes in both Pieter J. den Boer and were generally supposed to be governed stocked with inhabitants; and it each takes possession of certain by . For interspecific re- follows from this, that as the peculiar kinds of and modes of lations this found expression in the favoured forms increase in number, fife in which it has an advantage over ‘competitive exclusion principle‘. so, generally, will the less favoured its competitor”. The ‘niche’ of a After it was shown that coexistence decrease and become rare”. Darwin is thought to consist of the rather than exclusion of closely re- thought that this generally occurred essential resources of the species lated species is the rule, this prin- by competition, not only between inclusive of conditions of time and ciple gradually changed into the varieties of the same species, but space as well as the strategy of ‘competitive niche shift principle’. also between species: ‘We have which enable it sufficiently to make Recently the universality of competi- reason to believe that species in a use of these resources. Therefore, tion has been increasingly ques- state of nature are limited in their ‘competition’ is that kind of inter- tioned, so that other interspecific ranges by competition of other orga- action between individuals of two or relationships (especially ) nic beings quite as much as, or more more species, by which at least one are revaluated as possibly governing than, by to particular of the species is kept from sufficient many natural population and inter- climates”. Especially closely related ly using its essential resources. population processes. species would compete severely: ‘As In the 1920s the principle of com- species of the same genus have petition was formalized in the Lotka- By considering as usually, though by no means invari- Volterra equations. Given the highly the driving force of Darwin ably, some similarity in habits and restricting assumptions of these created a new problem: to be natur- constitution, and always in structure, models, which state that populations ally selected implies a better chance the struggle will generally be more of identical individuals of two spe- of leaving descendants, and if con- severe between species of the same cies are growing together in a closed ditions remain favourable numbers genus, when they come into com- and homogeneous environment are expected to increase. In his own petition with each other, than be- with constant physico-chemical words: ‘Owing to the high geometri- tween species of distinct genera”. properties, the principle is tautolo- cal rate of increase of all organic With this conclusion of Darwin the gical: the conclusions are implicit in beings, each area is already fully ‘competitive exclusion principle’ was the assumptions3. Laboratory ex- born, though it is generally referred oeriments in the 1930s and 194Os, to as Gause’s principle: ‘It is admit- usually with genetically homo- Pieter den Boer is at the Biological Station, Wijster (Agricultural University Wageningenb ted that as a result of competition geneous stocks of Tribolium or Dro- Kampsweg 27 9418 PD Wijster. The Nether- two similar species scarcely ever sophila species, aimed at satisfying lands. This article is Communication no. 309 of occupy similar niches, but displace as closely as possible the premises the Biological Station at Wijster. each other in such a manner that of the competition equations. They

25 TREE vol. 7, no. 1, July 1986

Fig. 1. Two species of Crateroscelis individual records relative warblers on Mt Karimui in New summit Guinea segregate in their niches by 4oOG altitude, replacing each other . abruptlv at 1543 m. Each circle rep- . resents one observation of C. rob&- ta ffilled circles) or C. murina Looen ing the species evolved separately, . circlesl. (Paucity of svmbols~ be- . and thus became adapted to dif- tween 650 and 1050 m is because ferent sets of conditions, or because little time wes spent there.) On the they coevolved under pressure of right, these observations are re- \ expressed es the percentage each competition, and thus diverged in warbler species contributes to the utilization’2,‘3. The latter total number of individuals of phenomenon, which was called all species at each altitude. (Based ‘character divergence’ by Darwin, on Ref. 9, with permission of the American Association for the but is better known as ‘character Advancement of Science.) displacement”4, and is also indi- cated as ‘niche shifVg or ‘niche seg- regation’, is at present one of the most controversial aspects of com- munity ecology15. After the war, ecologists had to 1 find their way between axiomatic theorizing and multi-interpretable field observations. As the gap be- tween these poles is wide, and hard-

_L III II I ly bridgeable, explorations could be 0 2 4 6 8 10 12 undertaken in many different direc- 91;of all bird individuals tions. Several authors tried to adapt their conviction of the universality of showed that the logic of the models generic species replace each other competition to the growing collec- is indeed irrefutable, but also that the abruptly over a short distance, e.g. tion of apparently conflicting field assumptions are so severe that even Fig. 1 (Ref. 9). But even observations observations, especially those con- small deviations from constant or of this kind (which cannot often be cerning coexistence of supposed homogeneous conditions might give made) are open for other explana- competitors: fundamental niche”j, unpredicted results4. Doubts grew tions, such as food preferences, competition theory17, and niche about the power of the principle to requirements for nesting, or highly theory’8-21. Others tried to tackle explain distributional patterns of specific physico-chemical toler- these questions more directly by closely related species living under ances. The same can be said when performing elegant field experi- natural conditions, ending in 1971- the invasion of some species into a ments22f23. Although the possibilities 72 in a discussion in Nature (cited in new area coincides with, or is fol- for such experiments are restricted, Ref. 5). The principle mainly survived lowed by, retraction of distribution it has at least been shown that the as the widespread conviction that or at least a striking decrease in num- coexistence of sessile natural selection should necessarily bers of related species’,‘. Such may be significantly favoured by pre- be ‘competitive selection’6,7. observations indeed suggest com- dation, including the feeding of herb- During most of this century it has petitive interactions, but other ex- ivores on plants22,24. It was con- been common to consider that the planations cannot be excluded’O,“. cluded that predation may prevent occupation of separate by Where congeneric species are found potential competitors from exceed- closely related species is due to com- to coexist it is generally supposed ing the of the en- petitive exclusions. Especially in- that their niches will differ signi- vironment, and thus will prevent ex- triguing are cases where two con- ficantly, either because before meet- clusion. The high of certain kinds of vegetation is some- times attributed to the effects of herbivores24. From the moment of the formula- tion of the competitive exclusion principle by Gause’ the danger of 32 mm Sitta tephronota\ circular reasoning has been recog- 31 nized. However ‘similar’ closely re- 30 lated species sometimes are, they are different by definition, and so will 29 be their niches. Therefore, to seek Fig. 2. in 28 - Asiatic . Bill length and ecological differences between coex- facial stripe in the two species are 27 isting congeneric species proves very different in areas where they 26 ._ nothing in itself, because we lack occur together but are quite similar reliable quantitative methods to com- where they occur alone. Populations 25 pare and evaluate the ecological dif- west of the zone of overlap (Sitta 24 neumayer): A, Dalmatia and Greece: ferences and similarities that will B. Asia Minor. In the zone of over- 23 -r naturally (that is, without competi- lap: C, Azerbaijan and Northern 22 tive ) coincide with the Iran; D, Kermanshah; E, Luristan and Bakhtiari; F, Fers; G, Kirman. HI JKLM morphological differences and simi- East of the zone of overlap (S. larities between species. We can tephronota): H. Persian Baluchistan; only show that it is reasonable to I, southern Afghanistan; J. Khor- suppose that taxonomically closely asan; K, north-central Afghanistan north of the Hindu Kush; L. north- related species will also be closely eastern Afghanistan (Pamin); M, related ecologically5, but this need Ferghana and western Tian Shan. not exclude coexistence. The few (Based on Ref. 30, with permission well-documented cases of direct ex- of McGraw-Hill Book Company.) clusion under field conditions show 26 TREE vol. 1, no. I, July 1986

Fig. 3. Eight species of fruit pigeons fruit Rilinopus and Ducula in New dnmeters Guinea lowland rain forest segre- c gate by size. The number below 7mm each pigeon is the average body weight of the species; each species weighs about 50% more than the than could be expected with a ran- preceding species. The sketch indi- dom distribution of the species’5,7. cates those pigeon species utilizing The advantages of coexistence of re- fruit of given sizes and the preferred lated species are apparently greater perch position of each species along a branch. Fruit is swallowed whole, than the drawbacks of possible d and larger pigeons can swallow lar- 20mm competitive interactions. Obviously, ger fruits. Smaller pigeons can no more is needed also to resolve perch on fine branches and can what is called ‘the paradox of the therefore reach some fruits inac- cessible to larger pigeons. But larger ”‘. pigeons aggressively displace smal- We are left with two hypotheses to ler species on branches thick explain the coexistence principle: (1) enough to support the heavier spe- in natural , adverse con- cies. The oiaeons are: 490. Ptilino- pus nanus: %g, P. p”lch&s; 1239, ditions (especially predation sensu P. superbus; 1639. P. ornatus; 2459. b lato, which is often proportionally 30mm P. perlatus; 4149, Ducula rufigaster; more severe at higher densities) are 5929, D. roe&s; 802g. D. pinon. so universal and significant that only (Based on Ref. 9, with permission of / the American Association for the / very occasionally will the numbers of Advancement of Science.) individuals of the coexisting popula- tions of species with similar resource utilization grow together such that carrying capacity is exceeded, and interspecific competition will rarely become so severe as to result even- 6 tually in exclusion of one or more of 40 mm the species”; (2) under favourable conditions the ecological differences that the excluding species rendered placed by the ‘coexistence principle’: between closely related species are essential resources unavailable for ‘As taxonomically closely related generally sufficient to allow coexist- the excluded speciesz5, either by species usually are also ecologically ence to begin, after which the grad- direct (), or by claim- closely related, related species will ually increasing pressure of com- ing the entire resource (), be found coexisting more frequently petition will shift the niches such or (within a closed environment) by more rapidly using up the resource (worms in intestines, larvae in fruits, droppings, carrion, etcJz6, or through interspecific territoriality (some pomacentrid fish), or (among sedentary ) by simply push- ing away the competitor (, limpets, anemones)25. However, such events will not only occur be- Fig. 4. During the six Years of tween related species; for instance, - observation populations of five spe- monkeys that remove fruits from a 1 2 3 4 5 cies of small ground of the tree will deprive the that lay genus Notiophilus were found to their eggs in those fruits. Hence, the year-catch occupy the same small birch wood (about 800 square meters), in Dren- laboratory experiments on exclusion 40 e-0 the, The Netherlands. Individuals of N. aquaticus (above) can be considered, at best, all species are of the same size (ab- as models for species living in closed 20 i \ .A%, ’ out 5 mm) and have the same feed- and comparatively small environ- . ing habits: adults as well as larvae 0’ are surface dwelling hunters of Col- ments, such as fruits, flower heads, 160 lemboles. Adults locate galls, or intestines?. by , the larvae by tactile stimuli. In spite of the above remarks, if 100 ?\,_.,e-?• 2 Year-catches resulted from con- / tinuous pitfall sampling in thecentre closely related species in the field 40 i ?? N. biguttatus of the wood, and were equivalent to have a higher chance of excluding 01 I , I I 1 0.1-l% of . Four of one another than less related spec- 2. ?yo\e_.,e? N.germiyi the five species reproduce in spring, and three also (or exclusively) in ies, it must be possible to test the i ‘. autumn. These data show that five hypothesis that ‘species belonging 01 I of the six Notiophilus species in the to different genera will more fre- area are able to coexist, though they quently coexist than congeneric occupy virtually the same niche: species’, against the appropriate null only N. sobstriatus was absent from hypothesis. This was first appreci- this simply structured wood, which consists of birches of about the ated and applied to flowering plants, same age. The species of this genus. insects and by Williams2’, fol- which are identified with the help of lowed by Simberloffz8 for vascular 1661 ’ ’ 19’65 small, but distinct, structural differ- plants, ants and birds on islands, and ences, such as elytral intervals, mic- rosculpture, form and punctuation Reproductive cycles by den Boer for carabid $. of the pronotum, frontal furrows These tests led to the conclusion that (see photoaraphs), are identical in congeneric species coexist more fre- ‘ - morphology’: man- quently than could be expected from dibles. size and field of vision of the . iong slender legs. (Data of the a random distribution of species Biological Station, Wijster, The over habitats (or islands), so that the Marc April Ma” .hna .I”,” ~“g”ej Sapt.[Oct. NO” 1 oat. Jan. Feb. Netherlands (Fiefs 5, 7); scanning ‘exclusion principle’ could be re- I I I I I I I I II I I II I I I I I I I I I I I photographs TFDL, Wageningen.) TREEvol. I,no. l,Ju/y 1986

that this early coexistence can be of past interspecific competition Communities, Belknap Press continuedg. The latter hypothesis (possibly maintained by intolerant 13 Connell, J.H. (1980) Oikos35,131-138 predicts that the ecological differ- behaviour) will have to stay unde- 14 Brown, W.L. and Wilson, E.O. (1956) ences between sympatric popula- cided. The message of Fig. 3 seems Sysr. Zoo/. 5,49-64 15 Strong, D.R., Simberloff, D.,Abele, L.G. tions of the supposed competitors to be: if they are to avoid severe and Thistle, A.B., eds (1984) Ecological will have become greater than be- interspecific competition, no more Communities. Conceptual issues and the tween primarily allopatric popula- than two coexisting species of these Evidence, Princeton University Press tions. fruit pigeons can have exactly the 16 Hutchinson, G.E. (1958) Co/d Spring Though the second hypothesis, same feeding habits, and in that case Harbor Symp. Quant. Biol. 22,41!5-427 which replaces the ‘competitive ex- they will differ appreciably in sizeg. 17 MacArthur, R.H. (1972) Geographical clusion principle’ by the ‘competitive But such specialization need not be , Harper&Row 18 Pianka, E.R. (1976) in Theoretfcal niche shift principle’, seems to be associated with competition, as is Ecology, (May, R.M., ed.), pp. 167-196, more favoured by ecologists than clearly illustrated by phytophagous insects36. Moreover, it is not difficult Blackwell the former’28’8, it now meets with a 19 Cody, M.L. (1975) in Ecologyand to find examples of coexisting con- growing resistance15. In the context Evolution of Communities (Cody, M.L. of competition theory it was un- generic species of the same size and and Diamond, J.M., eds), pp. 214-257. doubtedly a step forward to compare feeding habits (Fig. 4). We cannot, Belknap Press sympatric populations of two poten- however, make science by selecting 20 Diamond, J.M. (1975) in Ecologyand tial competitors with allopatric examples. We will have to judge the Evolution ofcommunities (Cody, M.L. ones14. The difficulty was, however, actual frequencies of these examples and Diamond, J.M., eds), pp. 342-444, that most ecological phenomena can in their natural context, and to test Belknap Press 21 Hutchinson, G.E. (1975) in Ecology and only be quantified by many years of against the correct null hypo- thesis7.37. A thorough frequency Evolution of Communities (Cody, M.L. intensive field work, so that for quick and Diamond, J.M., edsl, pp. 492-521, analysis of different kinds of coexist- inference one had to manage with Belknap Press measurable morphological charac- ence could indeed give valuable 22 Connell, J.H. (1975) In Ecologyand ters that could be supposed to be hints about probable and less prob- Evolution of Communities (Cody, M.L. directly related to the manner and able evolutionary processes’5. and Diamond, J.M., eds), pp. 46&490, degree of resource utilization, such As a future trend we can expect a Belknap Press as body sizes and bill dimensions in further depreciation of competition, 23 Wise, D.H. (1984) in Ecological birds. The example of bill lengths both intra- and interspecific, as Communities. Conceptual issues and the Evidence(Strong, D.R., Simberloff, D., in two Asiatic nuthatches (Sitta) being a major force in ecology and evolution. The manifold influences Abele, L.G. and Thistle, A.B., eds), pp. 42- seemed to be so convincing that it 53, Princeton University Press of weather, climate and other physi- was used in text books8,30 (Fig. 2). It 24 Huffaker, C.B. (1971) in Dynamicsof can be shown, however, that this cal factors38 will assume greater im- Popu/ations(Den Boer, P.J. and Gradwell, classical case of ‘character displace- portance, and the claim of universal- G.R., eds), pp. 327-343, PUDOC ment’ simply represents two parallel itv of comoetition will orobablv be 25 Birch, L.C. (1979) Fortschr. Zoo/. 25, character clines without indications replaced by a gradual r&aluatidn of 197-221 of niche shift between the sympatric the role of oredation’0.‘3C24S32.35. The 2i Zwalfer, H. (1979) Fortschr. Zoo/. 25, populations3’. Note that if the clines first hypothesis (above) to explain 331-353 27 Williams, C.B. (1964) Patterns ,n rhe M-C and G-A in Fig. 2 had not run the coexistence of related species will enter a period of extensive test- , Academic Press from right below to left above, but 28 Simberloff, D.S. (1970) Evolution 24, ing. from right above to left below, no- 22-47 body would ever have suggested, 29 Ghilarov, A.M. (1984) O/kos43,46-52 when comparing the situation at E 30 Ehrlich, P.R. and Holm, R.W. (1963) The with those at M and A, the occurr- Process of Evolution, McGraw-Hill ence of niche shift with connected References 31 Grant, P.R. (1975) in Evolutionary character displacement. Though not 1 Darwin, C. (1878) The Origin ofSpecies, (Dobzhansky, T., Hecht, M.K. and (6th ed.), John Murray all cases of character displacement’4 Steere, W.C., eds), Vol. 8, pp. 237-337, 2 Gause, G.F. (1934) The Struggle for Plenum Press can be invalidated as easily as this, it Existence, Williams&Wilkins- 32 Strong, D.R. (1983)Am. Nat. 122, is increasingly clear that character 3 Peters, R.H. (1976) Am. Nat 110, 1-12 636-660 displacement is not a promising field 4 Ayala, F.J. (1970) in Essays in Evolution 33 Hairston, N.G. (1984) in Ecological of research7,32-34. and Genetics in Honour of Theodosius Communities. Conceptual Issues and the If the niche segregation necessary Dobzhansky, (Hecht, M.K. and Steere, Evidence (Strong, D.R., Simberloff, D.. for permanent coexistence had W.C., eds), pp. 121-158, North Holland Abele, L.G. and Thistle, A.B., eds), occurred so long ago that the charac- 5 Den Boer, P.J. 11980) Neth. J. Zoo/. 30, pp. 19-27, Princeton University Press ter distance had become a general 278-306 34 Simberloff. D.S. (1984) in Ecological 6 Nicholson, A.J. (1960) in Evolubon after feature of the species concerned, we Communities. Conceptual issues and the Darwin (Tax, S., ed.), pp. 477-521, Evidence (Strong, D.R., Simberloff, D., can no longer observe any character Chicago University Press Abele, L.G. and Thistle, A.B., eds). displacement. It then becomes a 7 Den Boer, P.J. (1985) Z. Zoo/. Syst. pp. 234-253, Princeton University Press question of taste whether one Evolutionforsch. 23,259-274 35 Strong, D.R. (19841 in Ecological assumes that the ecological dif- 8 Mayr, E. (1963) Species and Communities. Conceptual Issues and rhe ferentiation of presently coexisting Evolution, Belknap Press, Harvard Evidence (Strong, D.R.. Simberloff, D., species originated from competitive University Abele, L.G. and Thistle, A.B., eds), coevolution in the past, or from 9 Diamond, J.M. (1978) Am. Sci. 66, 322- pp. 28-41, Princeton University Press separate evolution under different 331 36 Jermy, T. (1985) Z. Zoo/. Syst. 10 Andrewartha, H.G. and Birch, L.C. conditions’3. In fact, by referring to Evolutionforsch. 23,275-285 (1954) The Distribution andAbundance of 37 Strong, D.R. (1980) Synrhke43. 271.. competition past the problem has Animals, Chicago University Press 285 been manoeuvred outside the field 11 Lack, D. (1971) Ecological isolation in 38 Andrewartha, H.G. and Birch, L.C. of science. Whether examples of pre- Birds, Blackwell (1984) The Web of Ecology. More on the sent niche segregation by size, such 12 Cody, M.L. and Diamond, J.M., eds Distribution and Abundance ofAnimals, as pictured in Fig. 3, are the outcome (1975) Ecology and Evolution of Chicago University Press

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