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T H E PALEOECOLOGICAL SIGNIFICANCE O F O P P O R T U N I S T I C SPECIES JEFFREY S. LEVINTON Levinton, J . S. : The paleoecological significance of opportunistic species. Lethaia, VOl. 3, pp. 69-78. Oslo, January 15th, 1970. Opportunistic species are not resource-limited. With favorable events they can increase rapidly in numbers. Such species populations are typically very unstable and may become extinct very quickly. In contrast, equilibrium species populations are resource-limited and maintain stable population levels. The identification of explosive opportunists in the fossil record i s an important means of recognizing animal communities which were primarily controlled by the physical, and not the biotic, environment. In young environments of high physiological stress where animal communities are physically controlled, most species are opportunistic. In old and biologically accommodated communities opportunists are relatively rare. Explosive opportunists can be recognized by means of distributional, relative abundance and fossil occurrence data. J. S. Levinton, Department of Geology and Geophysics, Yale University, New Haven, Connecticut 06520, U.S.A., October ZOth, 1969 MacArthur (1960) made an important distinction between opportunistic and equilibrium species. Opportunistic species populations have their numerical abundances determined mainly by very high fecundity and short generation time, and have high intrinsic rates of population increase. Such species are physiological generalists and may rapidly increase in numbers when such environmental factors as salinity, space, temperature, predation, and food availability become favorable. Populations of opportunistic species experience long periods of time in which they are not resource-limited. That is, population size is below the carrying capacity of the associated habitat. T h e above characteristics of opportunistic species, with favorable events, may allow quick colonization of areas which have been previously sparse with organisms. T h e unusually dense spatfall of mussels (Mytilus edulis) during the spring of 1940 in the River Conway Estuary is a good example of such a phenomenon. As many as 700 young mussels settled on previously established individual adults, which were completely smothered over. ‘And so the immediate result of this wonderful abundance of spat was disaster to what had been a well-stocked fishery’ (Savage, 1956). The intertidal bivalve, Donax gouldi, has experienced many recorded population explosions on the beaches of southern California. I n 1937-1938 this clam reached such high densities that it was newly used extensively for commercially sold broth. However, the population disappeared suddenly a year later. I n the spring of 1949, a resurgence of quite unusual magnitude occurred, causing populations with densities of 20,000 individuals per square 70 JEFFREY s. LEVINTON meter to appear in 2-5 meter wide band over 5 miles of coast. Ocean currents were probably responsible for concentrating swarms of larvae in this area (Coe, 1953). Of current interest is the spectacular population increase undergone by the coral-eating ‘crown-of-thorns starfish’, Acanthaster planci, in the last few years. Perhaps in response to an opportunistic provision of larval settling sites (caused by the blasting activities of man) these starfish have exploded in numbers and are now decimating coral reefs in the Pacific Ocean. I n a two and a half year period, 90% of the coral were killed along 38 km of Guam’s shoreline (Chesher, 1969). T h e transient and explosive nature of such opportunistic species populations may produce instability in the community which they invade. Habitats formerly at equilibrium or sparsely populated may suddenly become severely space and nutrient-limited. I n environments of high environmental stress, such as the sandy beach, wave-swept intertidal zone, a community of exclusively opportunistic species may be present, as controls of population numbers are climatic. However, even in habitats of low physico-chemical stress and great stability, opportunists may participate in occasional invasions of an otherwise stable fauna. A stable fauna consists of equilibrium species, whose populations are at or near the carrying capacity of the environment (resource-limited). Equilibrium species numbers are due more to the size of the breeding population available, than to the intrinsic rate of increase (MacArthur, 1960). Stable faunas may be more difficult to invade because resources available to the community are being fully exploiteds. But invasions of stable faunas could take place because the factor allowing opportunistic species explosions may be unrelated to the resources which limit the resident faunas. For example, a food-limited marine benthic community may be invaded by an opportunist in years when predation on the opportunist’s pelagic larval stages is relaxed, thus causing unusually great larval survival. T h e opportunist will establish a large population and die out gradually or quickly, depending upon its ability to compete with resident species. This process might take several years if the environment is variable, or if the competitive ability of the resident species is only slightly greater than that of the opportunist. Disease, predation or other factors may also eliminate the opportunist. Viewing the fossil record from this perspective, we may indirectly see instances of opportunistic species (and faunas), and cases of faunas consisting of equilibrium species. This distinction is crucial, as it indicates the equibility of a habitat, the maturity of a community, and the nature of fluctuating physical and biological parameters. T h e analysis of opportunism allows us to impose a dynamic dimension to the birth, development and disappearance of fossil marine benthic faunal assemblages. As will be shown below, opportunistic species (in the sense of those species with explosive population characteristics - explosive opportunists) can be identified by use of distributional and facies relations, and relative abundance data. OPPORTUNISTIC SPECIES 71 Community perspectives and opportunistic species Opportunistic species populations may show only modest changes in numbers over time, especially in habitats with minor fluctuations in food, temperature, salinity, etc. (e.g. subtidal tropics). This is because resources are rarely underexploited enough to allow rapid infiltration of opportunists, and also due to the fact that sudden changes in the environment, which allow explosions, are rare. I n practice, the distinction of such opportunists, that maintain small, nonfluctuating populations, from equilibrium species would be quite difficult. This is especially true as it is generally not possible to regard relative fossil species abundances as being closely representative of actual living abundances. Yearly changes in population dynamics and dominance relationships, small shifts in physical parameters and features of preservation tend to mask minor changes in original living relative abundances (Johnson, 1965). It is possible, therefore, to recognize only those opportunistic species whose fecundity and ability to rapidly colonize bottoms are very high. T o gauge the probability of explosive opportunistic species occurring in a habitat, several extant marine benthic environmental types were evaluated (in a manner suggested by Levins, 1963), based upon the following three factors : (1) age of the habitat, (2) Tr-Te ; where T r is age of first reproduction, assuming animal usually dies soon after, and T e is period of most environmental fluctations (e.g. daily tides, yearly storms) - see Hutchinson 1961, for a similar approach and (3) the degree of environmental stress. T h e age of a habitat has been shown to be directly related to the diversity, stability and complexity of a community (see Pianka, 1967; Sanders, 1968). Parameter 2 is an index of the predictability of the habitat, and the probability that a population will evolve, through natural selection, to adapt to the fluctuations in the habitat. As the value of this predictability index approaches zero, the probability of successful adaption to fluctuations approaches zero (see Hutchinson, 1957; Levins, 1962; Green, 1969). If T, is much greater than T,, then the species will develop homeostatic mechanisms to deal with environmental variation within the lifespan. If Tr is much less than T,, then the species will change, through selection over succeeding generations, to adapt to environmental changes. T h e degree of environmental stress, finally, is well known as a determinant of diversity and population stability. These three parameters interact to determine a species’ population dynamics and niche breadth. T h e selected environments were evaluated (Table l), relative to each other, on the basis of these parameters. An index of opportunism was taken to be the sum of three scores for parameters 1-3, for the given environment. A low score indicates a high probability of explosive opportunists, while a high score indicates a low probability. This approach predicts that intertidal boreal biomes should have many explosive opportunists, whereas abyssal bottoms should have very few. I I 72 JEFFREY s. LEVINTON Table 1 . Probability of explosive opportunists in different habitats ITr-TeI ‘Predictability index’ Age of Habitat 1 2 1.5 1 1 2 3 3 4 5 3 4 5 N. Atlantic boreal intertidal Intertidal tropics Boreal estuary Tropical estuary N. Atlantic boreal subtidal Subtidal tropics Abyssal mud bottom 2 Degree of physiological stress (salinity, expoIndex of sure, low oxygen, Opportunism etc.) 1 1.5 1.5 3 3 4 5 3 4.5 5 8 9 12 15 Tr = period between spawning peaks; T, = period of environmental fluctuations. Scale for all parameters is relative, ranging from one to five. Estimates are highly speculative. N.B. A low index of opportunism indicates more explosive opportunists. Most investigators agree that the degree of organization, diversity and biotic stability of a community are directly proportional to the age and stability of the associated habitat, but inversely proportional to the degree of physiological stress. In the framework of time, communities can be seen as evolving from those which are highly unstable and subject to rapid change, to communities of high organization and great stability of population numbers, diversity and species content. I n a newly opened habitat, the rate of immigration of species is exponential and is limited by the availability of colonists. As time passes, common species become less common and rare species become less rare. Finally the habitat attains a maximum diversity pattern, with a steady-state condition being in effect (Goulden, 1969). I n shallow tropical waters, the average niche size of species has decreased over time, with increasing diversification (Valentine, 1969). This increase in diversification has probably resulted in more interspecific interactions (predation, commensalism, etc.) thus increasing the stability of the community (see MacArthur, 1955). As a result, the probability of opportunistic species invading or living in this stable biome has diminished continually. I n space, an analogous set of changes may be seen by going from young communities of high physiological stress to ancient communities of low stress. T he young, unstable communities (e.g. arctic intertidal) have their diversity, population dynamics and specific content controlled primarily by physical factors ; whereas ancient, stable communities (e.g. abyssal benthos) are primarily regulated by biological factors and are biologically accommodated (Sanders, 1968, Fig. 1). I n physically controlled communities, where pronounced catastrophes are common, there is often no mechanism of escape from death other than chance. This will have the effect of selection for the ‘ability to increase rapidly without regard to the specific source of the catastrophe that initially depleted the population’ (Slobodkin, 1968). OPPORTUNISTIC SPECIES Predominantly Biologically Accommodated Predominantly Physically Controlled 73 Abiotic . . . . ' , . stenqtopic species Gradient of Physiological Stress Species Numbers Diminish More Explosive Opportunists eurrfopit species stress conditions beyond adaptive means of animals d ___) __j Fig. 1 . Bar-graph representation of relations between physiological stress, community stability and organization, adaptability and the probability of explosive opportunists. Adapted from Sanders, 1968. T o summarize, young communities with high physiological stress are characterized by the presence of many explosive opportunists, whereas old communities with low stress have few. T h e presence of fossil faunas dominated by explosive opportunists is an excellent paleoecological indicator for physically controlled biological communities. Explosive population events and paleoecological consequences T h e presence of a non-transported fossil species in high densities may indicate that formerly it was in great living abundance (assuming sedimentation rates were not inordinately low). But our estimate of the nature of an ancient environment will be greatly enhanced if we know whether this great abundance was limited to short-lived invasions, or was continual over many years, with the population maintaining a stable equilibrium level. Such a dynamic problem arose in the analysis of Recent molluscan death assemblages from Long Island Sound and Buzzards Bay, Massachusetts subtidal muds (mud, in this discussion, includes sediments of high silt-clay content). Dredge, grab and core camples of bottom muds taken at depths of 0-20 m commonly reveal the presence of valves of the small mud-dwelling mactrid bivalve Mulinia lateralis (Say) in great densities(Levint0n & Bambach, 1970). However, this species is rarely found live in any of these same samples (Table 2). This same phenomenon has been observed in Naragansett Bay (Stickney & Stringer, 1956). M . lateralis formerly lived in high densities in the muds of Long Island Sound and certain areas in Buzzards Bay. Post mortenz transport of these shells does occur, as evidenced by intertidal beach deposits composed solely of Mulinia valves. But the wide distribution and abundance of this species as dead shells in all shallow water mud samples from Long Island Sound indicates its importance as former living in situ populations. 74 JEFFREY S. LEVINTON Sanders (1956) showed that Mulinia lateralis is an extremely transient opportunistic species, fluctuating strongly in numbers from year to year and from place to place, in Long Island Sound. T h e distribution of Muliniu in the East Mississippi Delta region supports the conclusion that it is a highly unpredictable species, showing strong within-habitat spatial variation (see Parker, 1956). Mulinia sets in extremely high densities, and usually disappears soon after (within a year or two). I n August, 1966, M . lateralis occurred in densities of thousands per meter square, but was absent as a living population two months later at a subtidal locality off Point Lookout, Milford, Connecticut (verbal communication, Anthony Calabrese). A station very dense with this species in 1952 (36 gm per meter square - Sanders, 1956) yielded no live specimens in October, 1968. Mulinia invasions, therefore, have not occurred simultaneously all over the Long Island Sound region, but have mainly been spatially and temporally sporadic. It is possible, however, that one large scale invasion did occur in addition to many smaller localized invasions. In both cases, the net result is the occurrence of Mulinia shells in great abundance throughout Long Island Sound. T he reproductive biology of this species conforms well to its population dynamics. Mulinia lateralis has a remarkably short generation time, averaging about sixty days from egg to egg (Calabrese, 1969). Gametogenic activity of adult Mulinia lateralis occurs throughout the year, the first ripe gametes appearing in April (Calabrese, 1970). These characteristics are adaptions for rapid population growth and availability of young in response to favorable environmental conditions. Levinton & Bambach (1969) showed that Mulinia has very high juvenile mortality, which is related to smaller individuals’ proneness to ciliary clogging by high bottom turbidity, and life position instability of small individuals in soupy muds. This mortality pattern, plus predation by starfish, fish and gastropods produces a high probability of frequent local extinction. It is curious in this respect that Mulinia lateralis lives only in muddy substrates. Its short generation time, high fecundity and ability to colonize bottoms rapidly allows its survival as a species in this tenuous ecological setting. T h e factors causing successful invasions are unknown. It is probable that population explosions are caused by some factor that greatly improves planktonic larval survival, such as a sudden relaxation of predation in the plankton. Sudden bursts of fecundity have probably little to do with population bursts, because the average fecundity (3-4 million eggs per female Calabrese, 1969) is more than enough to account for continually large populations, if larval mortality were slight. Great concentrations of larvae, near metamorphosis, by currents in localized areas may cause Mulinia invasions (Coe, 1953). Many of the muddy habitats experiencing periodic invasions by Mulinia OPPORTUNISTIC SPECIES Table 2. Comparisons of living and dead mollusks in a shallow (depth off West Haven, Connecticut Living (%) Yoldia limatula Nucula proxima Mulinia lateralis Other bivalves Gastropods 46 35 0" 0" 19 Total N 83 * found live in ' Dead (%) 2 6 89 2 0.6 1511 = 75 7 m) water silt, Dead, excluding Mulinia(%) 22 51 - 20 5.5 163 similar habitats along the Connecticut coast, in varying numbers support stable deposit feeding faunas which show evidence of maintaining equilibrium levels (see Sanders, 1956, 1960). T h e overwhelming dominance of Mulinia lateralis in the death assemblage, therefore, leads to incorrect conclusions concerning the taxonomic and biomass relations of the living benthic community. Given the dead relative abundances in Table 2 as a fossil assemblage, one might conclude that the assemblage represents a stable community which was continually strongly dominated by Mulinia. However, Mulinia was an erratic invader of an otherwise stable community. T h e rare species in the death assemblage were, at most times, dominant and affected community structure greatest. Current sorting of valves, re-suspension of bottom muds (concentrating heavier shells in layers), low sedimentation rates and high rates of biogenic reworking would tend to obscure microstratigraphic evidence for such invasions, unless they were quite pronounced. A fine example of faunal explosions and their paleoecological analysis was reported by Waage (1968). T h e assemblage zones of the type Fox Hills Formation (Maestrichtian) in South Dakota consist of geographically extensive contemporaneous horizons of concretions containing dense accumulations of fossils, being chiefly bivalve mollusks. These zones represent rapid and brief invasions, or settlements, of previously unoccupied or sparsely inhabited biomes. T h e Trail City member deposits represent a habitat mostly inhospitable to preservable marine benthos. During rare favorable times, rapid invasion occurred and very dense populations of mollusks developed in this biome. However, inhospitable conditions soon returned and mass mortality occurred (Waage, 1964). T h e Timber Lake member was more equitable, and supported a modest fauna. But periodic invasions of Pteria and Cucullaea (Bivalvia) occurred in response to changing physical parameters related to the breaking of a biogeographic barrier. Apparently, a persistent current system plus the stability of a sand bar determined the abundances of the species present. As predicted above the dominance of a habitat by explosive opportunists indicates that the community is controlled primarily by physical factors. 76 JEFFREY s. LEVINTON Recognition of opportunistic species explosions T he following criteria provide means of identifying explosive opportunists in the fossil record. Some are decidedly not unique to species explosions, and may be due to current transport, differential fossilization or low sedimentation rates. Consequently, all available evidence must be weighed carefully. (1) Random orientation and lack of size sorting of specimens in individual beds (concretions), but tendency for dominant species to occur in size-group aggregations (see Waage, 1968, p. 162). (2) Distribution over a limited area, the settlement, beyond which the horizon is unfossiliferous (Waage, 1968). (3) Aggregation of individual species in clusters, especially if the species is sessile, or stationary infaunal. (4) Presence of species in thin but widespread isochronous horizons, indicating brief invasions. T h e concretionary assemblage zones of the type Fox Hills Formation are of wide geographic extent, and represent brief invasions by different groups of species (Waage, 1968). (5) Species is found abundantly in several otherwise distinct faunal assemblages. This is due to the eurytopism typical of opportunists. Mulinia lateralis is found dead abundantly in many otherwise easily distinguishable benthic faunal assemblages. (6) Species appearing in great abundance in a facies with which it is no: usually associated. When striped bass were introduced into the waters off the U.S. west coast, a millionfold increase in numbers occurred over a period of twenty years. At the same time, striped bass on the east coast were slightly constant, or slightly declining in numbers (Merriman, 1941). (7) A species numerically dominates a fossil assemblage by 85-100% in numbers. Although marine benthic communities are often strongly dominated by one or two species, such overwhelming dominance by one species may indicate that an explosive opportunist continually invaded an unoccupied habitat or an otherwise stable community. Summary and conclusions Opportunistic species are not resource-limited, and, in environments of high physiological stress, can often rapidly increase in numbers in short spans of time. Such species populations are very unstable and may become extinct very quickly. In contrast, equilibrium species populations are resource-limited and maintain stable population levels. In young environments of high physiological stress where animal communities are physically controlled, many species are opportunistic. I n old and biologically accommodated communities, opportunists are rare. T h e identification of explosive opportunists in the fossil record is an important means 'of recognizing animal communities which were primarily OPPORTUNISTIC SPECIES 77 controlled by the physical, and not the biotic, environment. Such species that are ‘explosive’ can be recognized by means of distributional, relative abundance and fossil occurrence data. Often, in environments of high physiological stress, whole assemblages of species appear and die out in response to the same hospitable and unfavorable conditions. However, stable faunas may be invaded by a single explosive opportunist, whose brief appearance leaves very large numbers of specimens in the death assemblage. Mulinia lateralis, an extant mactrid mud-dwelling bivalve, is an explosive opportunist in Long Island Sound, and invades benthic communities in a temporally and spatially sporadic manner. Populations are short-lived, however, and great densities of shells are left in the death assemblage as a result. This species does not maintain stable long-lived populations in benthic communities of Long Island Sound. T h e recognition and distinction of opportunistic versus equilibrium species in the fossil record is an important way to evaluate the stability, maturity, and degree of environmental stress in fossil marine benthic communities. Acknowledgements. - Thanks are due to Anthony Hallam and J. W. Valentine for reading a preliminary version of these ideas and encouraging their development. The manuscript was read critically by D. C. Rhoads and H. L. Sanders. Both improved the manuscript substantially, but any errors are those of the author. Conversations with K. M. Waage on the Fox Hills Formation, and with Anthony Calabrese on Mulina lateralis were very helpful. REFERENCES Calabrese, A. 1969: Mulinia lateralis, molluscan fruit fly ? Proc. N u t . Shellfish. Assoc. 59, 65-6. 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