Download the paleoecological significance of opportunistic

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
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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.
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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.
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