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AM. ZOOLOGIST, 10:9-15 (1970).
Evolution and the Ecosystem
REZNEAT M. DARNELL
Departments of Oceanography and Biology, Texas AirM University,
College Station, Texas 77843
SYNOPSIS. Long-range stability in natural communities is mediated through avenues of
communication. One of the most important pathways of communication involves nutrient
exchange, although other types of communication are suspected as being of considerable
importance. The potential role of special "regulator species" in community stabilization is
discussed and illustrated with two original examples, one dealing with brackish-water communities of the North Carolina coast, and the other dealing with communities of the piedmont
streams of eastern Mexico. The significance of multi-species groups in evolution is also
considered in the second example. It is suggested that the functional ecosystem is the
fundamental seleclional unit of evolution and that evolution proceeds by mutual adjustment of
ecological entities into harmonious systems with some degree ot permanence.
A logical framework has been developed
for understanding the nature of species
and the processes of speciation. Embracing
the fields of genetics (Dobzhansky, 1941)
and systematics (Mayr, 1942), this framework is essentially two-dimensional. It has
long been recognized that the environment
plays a prominent role in speciation and
long-term evolution, and indeed, much information from natural history has been
incorporated into the genetic-systematic
framework. It is a recognizable fact, however, that the formal field of ecology is
developing with little reference to evolution and that the workers in the field of
evolution are not party to the new developments in ecology. The dichotomy is
dramatically illustrated by the virtual absence of reference to either speciation or
evolution in most of the recent undergraduate textbooks of ecology. By implication a
major dimension is missing from formal
evolutionary theory, and it is my purpose
to explore this problem, first examining
certain directions of current ecological investigation, then analyzing relevant phenomena observable in natural communities,
and finally relating these observations to
evolutionary theory.
Research reported herein was supported in part
by NSF grants G-10865, GB-4712, and GB-5255. A
portion of the work was carried out at the Duke
University Marine Laboratory.
THE ECOSYSTEM
Much attention is now focused upon the
ecosystem as the basic functional unit of
ecology, and this attention is directed
largely into three channels of investigation: capture and turnover of energy (production and productivity), biogeochemical
cycling (especially of mineral nutrients),
and modeling of ecosystems (systems analysis and simulation). These studies have
been made generally feasible through the
use of microbomb calorimeters, radioisotopic tracers, and computers. Together
these three approaches should eventually
lead to a clearer understanding of the actual working dynamics of natural ecosystems. In point of fact, serious studies of
ecosystems are just beginning, and methodology is still a matter of major discussion.
Furthermore, whereas considerable information is being accumulated on the
matter of primary production, studies of
secondary production are still, by and
large, in their infancy. It is unlikely that
the mathematical models and computersimulations will hold great relevance to
actual field situations until the ramifications of secondary production are fairly
well understood, especially since these investigators who are closest to the situation
in the field have little facility with mathematics and computers, while the experts in
simulation have seldom had wet feet.
10
REZNEAT M. DARNELL
"conversations." At present we have only
inklings
of this communication, but
Of critical importance in understanding
enough
to
assume that natural prairie
long-term community function and ecosysplant
populations
are not controlled by
tem cycling is the matter of "balance of
browsing
alone.
To
understand stability in
nature" or, as it is now called, "community
animal
communities
we must tune in on
stability." The combined experience of
their
exchanges
of
information
with plants
field ecologists points to the general fact
and
with
each
other.
The
fact
that
animal
that, whereas natural ecosystems do undersenses
are
often
so
much
more
acute
than
go certain changes in composition and proour
own
suggests
that
we
are
missing
a
cess, in the long run they maintain a defingreat
deal
of
the
information
which
is
ite integrity. As yet the homeostatic
mechanisms are not well understood. It is passed within and between species in
fairly obvious that stability in population nature, and these signals may be of considsizes, species composition, and biomass are erable importance in regulating sizes of
somehow associated with stability in nutri- populations, rates of nutrient flow, and
ent cycling, but it is not clear which, if any eventually, system stability. These facts
of these, is the primary agent of stability. lead the field naturalist to suspect that laStable populations may lead to a stable boratory populational studies and equasystem, or a stable system may induce sta- tions derived therefrom may be synthetic
bility upon otherwise variable populations. oversimplifications of the drama of nature.
The search for homeostatic mechanisms is If such equations work in the long run
now uppermost in the minds of many they may work for the wrong reasons, but
ecosystem ecologists, and contributions to in any event, they seem inadequate to exstability theory are eagerly awaited. In this press the day-to-day happenings in the
vital area the field ecologist should have field. It may not be necessary, for example,
as much to contribute as the mathemati- for a predator to consume a prey animal
in order to affect the prey's reproduction.
cian.
After a narrow escape, the persistent odor,
At the outset it may be assumed that sight, or sound of nearby predators may
whether stability arises from the total constitute sufficient stress to suppress
functioning system or from the individual reproduction in prey individuals. In fact,
species, it is mediated through some means reproductive suppression by environmental
of communication, i.e., through the trans- cues is likely incorporated into the genetic
fer of information between individuals of constitution of many wild species. It is
the same or different species. Nutrient cy- reasonable to suppose that when several
cling itself is only one aspect (albeit, a species evolve together a given species may
very important aspect) of the communica- evolutionarily "tune in" on the intraspetion network in nature. Communication cific recognitory cues or other stimuli
leading to stability may result from nutri- provided by a co-evolving species. Nor is it
ent transfer (as the predator receives in- necessarily true that populations of potenformation from the prey, and vice versa), tial prey species are unstable in the abor as any individual in the community sence of controlling predators. Interaction
produces signals which may be received by of individuals within a species or between
any other individual in the community individuals of different "prey" species is
(through chemical, visual, auditory, tac- known to influence reproductive success
tile, and other receptors). Stability in and survival of the young (Chiang and
grassland communities, for example, may Hodson, 1950; Christian, 1956).
result in large part, from stimulatory and
inhibitory communication between roots in
REGULATORY SPECIES
the subsoil rhizosphere where terrestrial
plants may carry on their most relevant
On theoretical grounds it is possible that
COMMUNICATION WITHIN THE ECOSYSTEM
11
EVOLUTION AND THE ECOSYSTEM
community stability may be brought
about largely by special "regulator"
species. A good candidate for this role
would be a lazy carnivore with little patience and broad prey tolerance. Such a
predator would cease to feed upon a given
prey species when it became scarce and
turn its attention to other prey species
more easily obtainable, even if less generally desirable. A more effective regulator
would be the multivore (no species is an
omnivore) which could exploit almost any
nutritional opportunity that came along.
This regulator could, during off-seasons,
subsist upon vegetation or organic detritus
and be available in high local abundance
to exploit prey species which became seasonally abundant.
Careful analysis of the food habits of
fresh- and brackish-water fishes demonstrates that most are opportunistic to some
extent and that true regulators do, in fact,
exist in the sense that they will quickly
dampen major outbreaks of prey species.
Among the brackish-water fishes of the
south Atlantic and Gulf coasts the Atlantic
croaker (Micropogon undulatus), spot
(Leiostomus xanthurus), blue catfish (7ctalurns furcntus), and sea catfish (Galeichthys felis) have exceptionally broad food
tolerances, but the prime candidate for a
regulator species, at least in the shallow
grassy flats, is the pinfish (Lagodon rhomboides) (Darnell, 1958, 1961, 1964). In the
laboratory this fish will consume almost
anything offered, but it has a decided preference for small invertebrates. In the field
it will concentrate upon a particular type
of invertebrate food until this becomes
scarce and then turn its attention elsewhere. Being a multivore, it is able to exist
at very high populational densities, and,
with an exceptionally high rate of foodintake, its effect upon the prey species
must be considerable, if not actually controlling. Following the food of the young
pinfish week-by-week throughout the summer months in a North Carolina estuary
(Fig. 1), one notes that in early June during an outbreak of caprellid amphipods
these formed about 95% of the food of the
FOOD
CATEGORIES
WEEK
NO.
I 2 3 4 5 6 7 8 9 10 II 12
Macro - mobile
Animals
Micro - bottom
An im ols
Micro crustaceans
Fila m entous
8
Algae
I"
D i a torn s
Vascular
Plant
Material
Organic
Detritus
8
Undeter mined
Org anic
Material
FIG. 1. Food of young pinfish (Lagodon rhomboides) taken from Zostera beds near Beaufort,
N.C., at weekly intervals throughout the summer
of 1961. The first collection was made June 8, and
the last was taken August 25, 1961.
young pinfish. The caprellids quickly
dwindled in abundance, and the fish shifted to a mixture of amphipods and other
invertebrates, supplemented with algae
and detritus. During late June, bottom invertebrates constituted the main food.
During July a general mixture of food
types was taken in, and with depletion of
the invertebrate food supply, organic detritus became the predominant food during
the late summer. The fact the the pinfish
could maintain high populational densities
on a diet of detritus suggests that members of this species would still be present to
exploit prey species which might become
available during the fall.
Another method of achieving system stability would involve a small group of species which had evolved together as a stable
system so that they had become adjusted
to the environmental resources and to each
other. This regulated base might act as a
stabilizing influence upon other species
which enter the community so long as the
latter's influence upon the primary species
was not controlling. An apparent example
of this type of situation prevails in the
small piedmont streams of eastern Mexico
from the Rio Papaloapan, on the south,
to the Rio Tamesi, on the north, and pos-
12
REZNEAT M. DARNELL
e
N. O.L./S.L.
^v
3.0
N. 2.0
Food
^^
Categories \ I . Q
Macro-mobile
Animals
Macro-bottom
Animals
variatus"
oexicana*
variatus
regani*
"
X
a. x
a
I
S a o
«
u a
3
«
c
w
B
•-.
L.
>
u
H
•
n
a
.n
n
•
n
1II. III.. Illllll....
•
1
•i
1
—
l
l
l
-
Zooplankton
Benthic
Diatoms
Algae
---1-
1 -••-
Vascular
Plant
Material
and Undetermined
Organic Material
1II III- Ilii""—
FIG. 2. Food and relative lengths o£ digestive tracts
of fishes taken in a downstream series in the
Arroyo Encino, a tributary in the Rio Tamesi
drainage of eastern Mexico. Locations of stations
and the ratio of gut length/standard length are
explained in the text. Asterisks denote species
which first enter the series at a given station.
N'ames of species, in order of entry, include the
following: Xipliopliorus variatus; Poecilia mexicana, Gambusia regani; Cichlasoma cyanogultaturn, Aslyanax fasciatus; Dionda rasconis, Ictalurus
australis, Cichlasoma steindachneri, Notropis lutrensis, Flexipenis vittala, and Gobiomorus dormitor.
sibly farther north and south. The basic
pattern involves five species of fishes belonging to the genera Poecilia, ~X.iphoph.orus,
Cichlasoma, Astyanax, and Gambusia.
Regardless of where one pulls a seine in
these streams, the catch consists predominantly of fishes of these five genera.
Through a distance of some 500 airline
miles and through at least half a dozen
drainage systems the basic pattern prevails.
These five genera are of southern origin
(i.e., they originated south of the area under discussion) (Miller, 1966; Rosen and
Bailey, 1963), and have gradually moved
northward, presumably by coastwise mi-
gration (Darnell, 1962; Darnell and
Abramoff, 1968). Taxonomically the names
of the species may change from one
drainage to another, but ecologically the
roles seem to vary little. In the southern
part of the range they may be accompanied by a few species of other southern genera (esp. Rhamdia, Poeciliopsis, Meterandria, and Belonesox), while in the north
they may be joined by species of northern
genera (Ictalurus, Dionda, and Notropis).
A more detailed analysis of the ecological roles of these five species is informative. Figure 2 is based upon four collecting
locations in the Arroyo Encino, a tribu-
EVOLUTION AND THE ECOSYSTEM
tary of the Rio Sabinas (Rio Tamesi
drainage). The collecting sites represent a
series from the headwater spring down to
the confluence with the river. At the uppermost collecting site a single species was
obtained, the platyfish (X. variatus), predominantly a detritus feeder. Downstream
at the first broad shallow pool, the platyfish was joined by two other species, the
Mexican molly (P. mexicana), another detritus feeder, and the mosquito fish (G.
regani), a carnivore which feeds primarily
upon insect larvae dwelling in the bottom
detritus. It has been found that the two
detritus feeders occupy slightly different
habitats, the platyfish preferring shallow
peripheral backwaters and the molly tending to live in slightly deeper water, where
it is often associated with rocks and stones
in midstream and where it may be exposed to slight current. Both detritus feeders ingest a small amount of algae and
other material that has been difficult to
quantify.
Proceeding downstream to the first deep
pool, one encounters two additional species, a cichlid (C. cyanogutlatum) and a
characin {A. fasciatus). Both are broadly
omnivorous, consuming plant, animal, and
decomposing material, but the cichlid
consumes more detritus, whereas the characin depends more upon living plants and
animals. Downstream near the river, six
additional species eventually enter the
community, all of which live primarily in
the river itself and enter only the lower
portions of the Arroyo. Three of these are
of southern origin and may have undergone a large share of their evolution in
company with the Arroyo fishes. The three
remaining species (/. mexicana, D. rasconis, and N. lutrensis) are of northern
origin which, having more recently encountered the southern forms, might be
expected to be less well-adjusted to the
functioning system of southern species.
In the upper boxes of Figure 2 the relative length of the digestive tract (ratio of
gut length/standard body length) has
been plotted for each species. It is well
known that this ratio closely reflects the
13
FIG. 3. Relationship between maximum body
length and food habits (as expressed by the
G.L./S.L. ratio) for fishes o£ Arroyo Encino. The
species which enters at station I is indicated by the
solid circle, those which enter at station II by
solid squares, those entering at station III by solid
triangles. Species which enter at station IV are
indicated by open symbols; open squares denote
species of southern origin, and open circles species
of northern origin. The five southern creek species
which are considered to form a co-evolving ecological group are enclosed within the dashed line.
average food habits of fishes, detritus feeders having relatively long guts and carnivores having relatively short ones. The
ratio reflects the apparatus necessary to
handle and process the ingested food, and
from the figure it is clear that the correlation with food habits in the present case is
exceedingly good. In Figure 3 the maximum standard body length of each species
(as encountered in the Arroyo) has been
plotted against the corresponding G.L.
/S.L. ratio. In effect, body size is being
plotted against average food habits to
provide some insight into whether or not
the various species are likely to be in close
competition for food. From this plot it becomes immediately apparent that the five
basic southern creek species are clearly separated in food type and body size. Furthermore, addition of the three southern river
species does not greatly increase the possibility of competition. On the other hand,
two of the northern species seem to be
14
REZNEAT M. DARNELL
potential competitors of two of the south- trolling factor. Throughout the range of
this ecological group, regulation appears to
ern river species.
We conclude that one of the factors per- be an internal matter. Non-predatory regmitting the southern creek species to coex- ulation within this group is considered to
ist is the absence of any significant overlap be a distinct possibility, but clear-cut eviin basic food resources. From data dence is lacking so far. The elaborate
presented here, as well as other informa- chemo-sensory and vision-based reproduction on hand, it is obvious that minor but tive behavioral patterns exhibited by the
significant differences in habitat are also of poeciliids and cichlids suggest an area
importance in reducing competition. where interspecific interference might opThese forms have effectively divided erate.
up the limited environmental resources.
Among the five primary creek species, the
CO-EVOLUTION
two omnivores (C. cyanognttatum and A.
Tn the above discussion emphasis has
fasciatus) were the only ones which gave
evidence of feeding upon the eggs and been placed upon the functioning multiyoung of other fishes. It is suspected that species system because species evolution
these two species act in the capacity of does not proceed in an ecological vacuum.
regulators by removing a portion of the Indeed, it would be ecologically absurd to
young of other species in proportion to discuss the evolution of Astyanax jasciatus
their abundance. The more carnivorous G. in eastern Mexico without simultaneously
regani gave no evidence of feeding upon considering its ecological partner, Cicheggs or young of other species, and this lasoma cyanoguttatum, and the most
may, in part, reflect a mechanism which meaningful discussion would involve the
prevents this fish from feeding upon its evolution of the entire group of southern
own young. In this connection it is worth species within its environmental context.
noting that the three specialists (G. re- We are, thus, led to the conclusion that just
gnni, X. variatus, and P. mexicana) are all as the ecosystem is the basic functional
live-bearers. The two omnivores must unit of ecology, so it is also the basic seleccontend with swimming young rather than tional unit of evolution. The missing diwith more exploitable egg deposits. The mension referred to in the beginning of
live-bearing habit may, thus, represent a this paper is the dimension of the ecosyspartial escape from predation which per- tem.
mits a flexible multivore-prey interaction
In discussing some of the factors which
leading to relative stability.
lead to stability in nature one is, at the
Other factors, of course, enter the pic- same time, considering the selective forces
ture. The lazy creek may be changed to a which mold species into functional units
raging torent overnight by run-off from within functional systems. Grass-roots seheavy seasonal rains. The creek residents lection is the determining factor of surmeet this challenge by following the shal- vival, and this, in turn, leads to evolutionlows as the water rises and waiting out the ary adaptation. Communication is viewed
torrent in the protection of the flood plain as the general integrative mechanism of
vegetation where the current is still fairly natural ecosystems, and nutrient transfer,
slow. Where steep walls prevent such es- upon which so much effort is currently
cape, the fishes become badly battered, and being placed, is one of several potential
undoubtedly many are lost during the an- avenues through which community stabilinual floods. Predation by kingfishers, ty may be achieved. The possible interspegrebes, egrets, and other birds also accounts cific role of intraspecific recognitory cues
for some loss from the populations in shal- has been pointed out. The classical Gauslow water, but neither floods nor predation sian predator-prey interaction has been
by birds is considered to be a major con- modified to the ecologically more reason-
EVOLUTION AND THE ECOSYSTEM
able multivore-prey interaction which permits a flexible relationship between coexisting species.
By examining the parade of species
which enter a stream community in the
downstream series we are witness to the
development of community complexity,
and we have gained some insight into the
factors which permit coexistence and
which determine stability in a community
consisting of two detritus feeders, two multivores, and one carnivore. This analysis
suggests that within any given ecological
situation there are certain ecological jobs
and certain opportunities. Gene mutation
and recombination provide sufficient variability so that the ecological pieces can mutually adjust into a harmonious and semipermanent system. Elucidating the functional and developmental aspects of this
system should provide the third dimension
of evolutionary theory.
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