Download Character Displacement and Fish Behavior, Especially in Coral Reef

AMER. ZOOL.. 14:1099-1118 (1974).
Character Displacement and Fish Behavior,
Especially in Coral Reef Communities
J. R . NlJRSALL
Department of Zoology, University of Alberta, Edmonton, Alberta, Canada
SYNOPSIS. Character displacement is a phenomenon of the species border directed
towards niche specification. It is posi-speciational and prezygotic, and has a strong
behavioral component. It has not been described in studies of fish by many ichthyologists. Examples are sought, not always successfully, among Coregonidae, Cyprinidae,
Catostomidae, Gadidae, Gasterosteidae, Poeciliidae, Cichlidae, Cottidae, Periophthalminae, and Pomacentridae. Character displacement is not invariable in the sense of
Brown and Wilson (1956). Examples may be relatively clear cut under conditions of
"r" selection, or complicated, involving several species under "K" selection. It has some
significance as a descriptive tool in systematics.
When introducing the concept of character displacement Brown and Wilson
(1956) made it clear that the phenomenon
could be studied broadly. "The characters
involved can be morphological, ecological,
behavioral, or physiological; they are assumed to be genetically based" (p. 49). This
is important, because it is a tacit assumption that processes of evolutionary importance are nearly universal among organisms, and the Brown and Wilson statement
is a form of a statement of universality.
The concept of character displacement is
intuitively satisfying. One is always relieved to find mechanisms by means of
which close species remain distinct, even
though sympatric. In numerous instances,
exemplified best by the papers of this symposium and the references therein, character
displacement has been invoked to explain
differences perceived. However, one should
note that ichthyologists largely have ignored the phenomenon.
Character displacement has also received
some general commentary. Hutchinson
(1959) gives examples from birds and mammals, involving "metric characters related
to the trophic apparatus, the length of the
culmen in birds, and of the skull in mammals" (p. 152). This specification of parts is
interesting in the light of what we know of
allometric growth, and that, at least in
Some of the work reported here on Pomacentridae and Periophthalminae was supported by
National Research Council of Canada grants A2071
and T0046.
birds, there seems to be greater variability
in certain characters of the head than in
other parts of the body (Marler, 1961).
Hutchinson was interested in niche requirements, particularly with regard to food,
while Marler dealt with visual communication, but both were concerned with basic
heterotroph requirements. The strong implication is that niche-directed divergence
will develop first in obvious and basic structures.
Mayr (1963) looked for a more quantitative analysis of character displacement.
Wilson (1965) himself attempted to provide
a framework for it. He looked upon the
final act of speciation as being a race between hybridization and displacement.
Character displacement, a prezygotic barrier mechanism, should commonly occur
distinctly and rapidly although one is to
expect "technically refractory problems."
Contributing to these problems is the
requirement in the model that "the prezygotic barriers are based on polygenes that
contribute additively to the phenotype"
(Wilson, 1965, p. 18). Implicit in this as well
is that prezygotic mechanisms are in significant part ethological. Wahlert (1965)
gives us the phrase "ethological key characters" which signal adaptive changes followed by morphological key characters.
MacArthur and Wilson (1967) emphasize
the potential importance of (behavioral)
character displacement by pointing out that
evolution is apt to occur most rapidly in
the prezygotic side of mating. The subse-
1099
1100
J. R . NURSALL
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CHARACTER DISPLACEMENT AND FISH BEHAVIOR
1101
quent morphological adaptations may be we are working at the species border, where
slow (Christiansen and Culver, 1969). Roux the marginal population has the severe
(1971) gives evidence that sympatry in- handicap described by Mayr (1963) as
creases the efficacy of the mechanisms of "having to remain coadapted with the gene
ethological isolation. Caspari (1958) pro- pool of the species as a whole . . . and yet
vides examples of the pleiotropic effects of be adapted to local conditions" (p. 526-7).
genes on behavior and morphology.
The species epigenotype will exert a pov.'erMayr (1958) pointer] out that often a ful counterforce to character displacement.
study of behavior permits a finer taxonomic
Ayala (1972) has concluded that natural
discrimination than is possible (at least selection can work on species competing for
initially) with morphological criteria. This, limiting resources in two ways. One is posiI think, is now widely accepted. Liley (1966) tive competitive ability, wherein one species
suggested "that ethological isolating mech- will flourish at the expense of its competianisms are among those most likely to be tors. The second is character displacement,
selected for, as they normally operate at the which should promote stability in the sysfirst contact of two potential mates" (p. 6). tem.
Mayr (1963) said "Ethological barriers to
One more complication must be reported.
random mating constitute the largest and MacArthur and Wilson (1967) and Macmost important class of isolating mech- Arthur and Levins (1967) provide models
anisms in animals" (p. 95).
for character convergence as an alternative
Tacit recognition of displacement in the to character displacement under certain
ecological sense is seen in a paper by Whit- conditions of competition for resources.
taker and Woodwell (1972), though here it Such possibilities are explored and exbecomes difficult to disentangle distribution amples gives by Moynihan (1968), Schoener
along environmental gradients by niche (1969), and Rohwer (1973).
and habitat differentiation from the initial
Let us look at some examples of species
more clearly defined character displace- interactions amongfishes,to see if character
ment.
displacement can be recognized.
The distinctiveness of character displacement in the meaning of Brown and Wilson
CORECONIDAE
(1956) has been blurred by Mayr (1963) and
Simpson (1969) both of whom attempt to
The coregonid whitefishes of North
give Darwin priority for the concept. "Di- America and Eurasia are an economically
vergence of character" as outlined in The important but morphologically variable
Origin of Species is a careful exposition of and systematically puzzling group, which
the quality of evolutionary divergence in have been the subject of much study, withthe broadest sense. Brown and Wilson out a clear picture of phylogenetic relationspecify a local phenomenon, which, though ships yet emerging. I shall focus on three
certainly a part of evolutionary divergence, examples within this group.
may be segregated and treated separately.
Svardson (1970) summarizes aspects of
As such it has a significance of its own; it Scandinavian work. One of the "disoperais not recognizable in Darwin's treatise. tions" of MacArthur and Wilson (1967),
Bock (1972), in chasing the phantom of the namely hybridization, is taken to account
evolution of higher taxa, suggests character for much of the variation in Scandinavian
displacement as one of the first steps in coregonids, acting especially through intromacroevolution; I think it is no more than gression. Workers with coregonids have
part of evolutionary divergence, a previ- found that measurements of body proporously undefined first step.
tions and many meristic characters, their
In dealing with character displacement stock in trade, are of limited value for disFIG. 1. Gill raker numbers and growth curves of
three sympatric Coregonus spp. in Lake Ockesjon,
Sweden. Species C was introduced in 1870. The large
and dwarfed species were already present and distinct. (From Svardson, 1970, with permission of the
University of Manitoba Press.)
1102
J. R . NURSALL
tinguishing allopatric species. They have
had to depend on gill raker number and
length as being under genetical control and
relatively constant (see Lindsey, 1963, and
Svardson, 1970, for references). Thus, as in
Figure 1, three sympatric species diverge
regularly in mean gill raker number, but
differently in body form (the parameters
of growth rate). In this situation (Lake
Ockesjon) species A and B existed together
as large and dwarfed species with low numbers of gill rakers (low-raker). About 1870,
species C was introduced from upstream
and is distinguished now from species A
chiefly by having a high number of gill
rakers (high-raker). Allopatrically, species
C would be thought to be an introgressed
population of A or B, but in Lake Ockesjon
it behaves as a separate species. The species
are not named.
Lindsey (1963) described the sympatric
occurrence of two species of Coregonus in
Squanga Lake, Yukon Territory, Canada.
Again the distinction was made on the basis
of gill raker counts. The high-raker species
was mostly caught in floating nets over deep
water, with 65% of stomachs examined containing exclusively pelagic or surface food
and 20% being empty. The low-raker specimens were chiefly captured in bottom-set
nets, and 80% of the low-raker specimens
had eaten exclusively benthic organisms.
None of these had an empty stomach.
Body proportions of the fishes were measured and shown statistically to demonstrate
differences between the species. These measurements were combined in a character
index which differentiated the species on
other than gill raker counts. "Despite these
average differences it was not possible even
after handling hundreds of specimens to
assign a fish with certainty to low or high
count form before examining the gill
rakers" (Lindsey, 1963, p. 761).
Some hybrids are present in the lake;
some separation of spawning times is evident. Obviously there are behavioral differences in terms of feeding and preferred
location within the lake, i.e., pelagic or
benthic.
FIG. 2. Heads and body outlines of Prosopium
coulteri from Chignik Lake, Alaska. Low-raker
shallow water form on left; low-raker deep water
form center; high-raker form on right. (From McCart, 1970, with permission of the University of
Manitoba Press.)
CHARACTER DISPLACEMENT AND FISH BEHAVIOR
1103
no
LONGITUDE
W
FIG. 3. Distribution of Prosopium coulteri in northwestern North America. Circles show locations of
high-raker forms, triangles low-raker forms. Sym-
patric populations joined by a bar. (From McCart,
1970, with permission of the University of Manitoba
Press.)
Although Lindsey (1963) suggested specific appellations for the Squanga Lake
whitefish, he later (McPhail and Lindsey,
1970) referred these fish simply to the
Coregonus clupeaformis complex. Lindsey
et al. (1970) pursued the problem further
with blood and muscle protein analysis by
electrophoresis. The two species in Squanga
Lake have the same proteins! Pairs of
Coregonus species in Ontario and Maine,
phenotypically similar to the Squanga Lake
pair, are also each alike internally, i.e., the
sibling sympatric species are more similar
than either is to any other pair. So it appears that similar pairs have evolved convergently; each of the lakes investigated has
its own pair of sibling species, the origin
of which is not at all certain. All are included within the Coregonus clupeaformis
complex.
McCart (1970) illustrates much the same
phenomenon in the coregonid genus Prosopium. While two lakes examined have
pairs of siblings of low and high-raker form,
a third lake has three sibling species (Fig.
2). Some ecological and behavioral differ-
1104
J. R . NURSALL
TABLE 1. Ratios of means of displaced characters in coregonid fishes.
Mean (X) or Mode (Mo)
Author
Lake
High raker
Low raker
Svardson (1970)
Ockesjon
Squanga
Naknek
Aleknagik
Chignik
23 (Mo)
21 (Mo)
21 (Mo)
23 (Mq]_
1.09
L.10
.19
Lindsey (1963)
McCart (1970)
25 (Mo)
23 (Mo)
25 (Mo)
28 (Mo|
17.33 (X)
15.82 (X)
19.21 (X)
19.21 (K.)
14.54
13.46
14.16
14.50
.19
1.18
.36
1.33
ences are recognized (food preferences;
location in lake), and morphological differences can be used to distinguish the fish
without the need to resort to gill raker
counts. In this case geographic isolation in
Pleistocene glacial refugia and separate redistribution are invoked to account for the
present sympatric occurrences, although the
possibility of introgression is advanced to
account for the low-raker deep water form
in the lake with three species. Figure 3
shows the present distribution of the fish
Prosopium coulteri, the pygmy whitefish.
So, displacement of a genetically controlled character, gill raker number, occurs
widely among sibling coregonid species,
many of which are indistinguishable, or
distinguishable from each other only by
experts or experienced fishermen (Svardson,
1970). Further analysis shows behavioral
and ecological distinctions. What has been
measured is changes in trophic apparatus,
related to niche requirements. MacArthur
and Wilson (1967) suggest as an empirical
generalization that differences between the
means of displacing species will stabilize at
about 30 to 50% of the common mean.
This is not accomplished in the coregonid
examples, using data from the cited papers
(Table 1). This could mean that character
displacement has been caught in process of
development in some of these examples, or,
it could engender a healthy scepticism of so
neat a characterization of proportions.
The origin of the displacement is suggested by McCart (1970) as allopatric speciation, by Svardson (1970) as introgression,
while Lindsey et al. (1970) remain uncommitted. An example of artificial selection by
(X)
(X)
(X)
(X)
Ratio
.22
Svardson is of interest. Using as parents extreme variants of one species it was possible
to derive two groups of progeny of divergent mean number of gill rakers (38.3;
33.9; ratio 1.13) of an order of difference
similar to that described above for sympatric sibling species of whitefish. The possibility exists that such a difference, well
within the genetic combinations available
to a natural population, could provide a
morphological stimulus through modification of trophic apparatus, to ethological
changes in emphasis (e.g., modes of food
gathering), which in turn could lead to
ecological separation and the arisal of sibling species.
CYPRINIDAE; CATOSTOMIDAE
Members of these two families are commonly sympatric and widely reported as
hybridizing, often intergenerically. It was
Carl L. Hubbs and his co-workers who most
clearly denned the characteristics of hybrids
of freshwater fishes (e.g., Hubbs and Miller,
1943; Hubbs et al., 1943; Hubbs, 1955).
This takes the form chiefly of a pervasive
intermediacy of related and unrelated characters. Smith (1973) demonstrated how
principal components analysis elucidates
intermediacy even in characters not usually
considered discriminatory in cyprinids. Selected examples are cited below.
Among minnows (Cyprinidae) Hubbs and
Miller (1943) reported a probable response
to a disturbed environment by hybridization between two species, one of which was
forced into new habitat by the loss of its
own. Some evidence of heterosis and some
CHARACTER DISPLACEMENT AND FISH BEHAVIOR
introgression (though not by that term) was
reported between Gila orcutti and Siphateles mohavensis. Later reports (Hubbs,
1955) suggest replacement of the native S.
mohavensis by the introduced G. orcutti.
Greenfield and Greenfield (1972), examining morphometric, karyotypic, and electrophoretir data, and undertaking breeding
experiments suggested that extensive introgression was taking place between G. orcutti
and Hesperoleucus symmetricus. They also
recognized parental (i.e., non-intermediate
characters). in Fx hybrids.
When G. orcutti (still water) and H.
symmetricus (streams) are forced together
in streams in periods of low water, hybridization occurs. H. symmetricus and the
hybrids have an advantage in that situation,
through direct competition for food. G.
orcutti is at further disadvantage by being
preyed upon by centrarchid fishes in its
still water habitat. During an 8-month period the G. orcutti population declined, H.
symmetricus increased, and F1 hybrids remained constant in number (Greenfield and
Deckert, 1973).
Nelson (1966; 1973a), describing hybrids
between Couesius plumbeus and Rhinichthys cataractae, suggested that local
hybridization occurred in disturbed environments (e.g., with hydroelectric development). There was no evidence of
introgression; hybrids were essentially intermediate. Some examples of hybrid characters lying within one or the other parental
range of variability was attributed to allometric variation, it being not always possible to compare specimens of the same size,
age and locality.
Greenfield et al. (1973) examined hybridization between Chrosomus erythrogaster and Notropis cornutus in Illinois. In
this instance intermediacy of morphometric
characters was found, but gut length segregated to either one or the other parental
value. There was some evidence of environmental disturbance increasing the probability of hybridization. There was no
evidence for introgression.
Among suckers (Catostomidae) hybridization is probably less common than among
minnows. No signs of introgression are re-
1105
ported by Hubbs et al. (1943) or by Nelson
(1968, 1973b). Nelson (1968) further reports
that there are no morphological differences
(i.e., no character displacement) between
allopatric and sympatric specimens either
for Catostomus commersoni or C. macrocheilus, the hybridizing species which he
investigated. He also reported no differences in spawning time or habitat of the
sympatric sucker. He inferred from his data
that undefined ethological isolation kept
the species apart.
Thus, we see that commonly in these two
families of cypriniform fishes sympatry occurs with species that can and do hybridize.
Neither pre-zygotic nor post-zygotic mechanisms are fully effective, but hybridization
as observed seems not to be interfering with
the species boundaries in most instances.
GADIDAE
In Cambridge Bay, Victoria Island,
N.W.T., three populations of codfish have
been described (Boulva, 1972). These are
identified as Gadus ogac, Arctogadus glacialis, and A. borisovi. Walters (1955) considered the latter two to be one species,
although Danish and Russian workers recognized two (see Boulva, 1972, for references). G. ogac and A. glacialis are phenotypically stable and distinct, while A.
borisovi is phenotypically variable and superficially intermediate. The possibility of
hybridization between G. ogac and A. glacialis giving rise to a variable intermediate
was explored and dismissed. The strongest
evidence against this concept was in the
form of otoliths, which are distinctly different between Gadus on one hand and the
two species of Arctogadus on the other.
Convergent phenotypic similarities between
G. ogac and A. borisovi are not unexpected,
given their similarities in niche requirements and normal allopatry. The possibility
of A. glacialis and A. borisovi being two
types of a polymorphic species is considered
to be unlikely owing to their general allopatry and the number of morphometric
character differences between them. Fifteen
of 27 measured characters differed significantly between the two Arctogadus species.
J. R. NURSALL
1106
O
ARCTOGADUS
GLACIALIS
•
ARCTOGADUS
BORISOVI
O
A. GLACIALIS AND BORISOVI
A
GAOUS OOAC
'
FIG. 4. Distribution of Arctogadus glacialis, A.
borisovi, and Gadus ogac in Arctic waters. (From
Boulva, 1972, with permission of the Journal of the
Fisheries Research Board of Canada.)
Two out of eight meristic characters differed significantly. Figure 4 shows the distribution of these fishes.
The evidence for character displacement
in the two species of Arctogadus in Cambridge Bay is by no means clear, but the
distributional pattern, the confusion of systematics that has existed, and the possibility
of comparing measurements of allopatric
representatives of the species suggest this as
an example that would repay extensive
quantitative study.
species with different developments of
lateral bony plates: trachurus is used for
those specimens which are fully plated (ca.
29 to 35 plates in a row along the side);
leiurus is essentially naked (ca. 4 to 8
plates); semiarmatus is intermediate in
plate number (ca. 9 to 28). The plate is
controlled by simple Mendelian inheritance
(Miinzing, 1963) with maternal dominance
(Lindsey, 1962); semiarmatus, with two exceptions, is considered to be a hybrid form.
Some phenotypic variation, owing to conditions of temperature and salinity, has been
demonstrated (Lindsey, 1962). The trachurus form is mostly coastal and marine,
though by no means invariably so; leiurus
is freshwater and inland, though not necessarily isolated from the sea. Mixed populations, with all three forms in various
proportions are common. Heritability of
lateral plate and gill raker numbers has
been established by Hagen (1973), with no
apparent sexual differences. Predation is an
GASTEROSTEIDAE
Sticklebacks form a family of fishes of
very great biological interest, behaviorally,
ecologically, and phylogenetically, covered
by a vast literature. Miinzing (1963) outlined the European distribution and relationships of Gasterosteus aculeatus, the
three-spined stickleback, the species which
has received the most attention within the
family. Names are applied to forms of this
CHARACTER DISPLACEMENT AND FISH BEHAVIOR
important selective force in determining
lateral plate number (Moodie, 1972b;
Hagen and Gilbertson, 1973).
Hagen (1967) examined G. aculeatus of a
coastal stream in British Columbia, distinguishing marine trachurus (30 to 35
lateral plates), freshwater leiurus (3 to 7
lateral plates), allopatrically distributed,
and hybrids (8 to 29 lateral plates) from a
narrow intermediate zone. Studies were
made morphometrically, electrophoretically
(muscle protein), and by breeding. From
these Hagen concluded that trachurus and
leiurus forms fulfilled the biological definition of species. This was challenged by
Miller and Hubbs (1969), who gave examples of genetically mixed populations
and introgression, neither of which had
been observed by Hagen. Miller and Hubbs
also questioned the use of European terminology (trachurus, etc.) for North American
forms, and called for subspecific appellations distinct for North America. Hagen
and McPhail (1970) replied, defending the
distinctness of trachurus and leiurus as
defined by Hagen (1967), then extending
the Miller and Hubbs (1969) arguments of
great stickleback variability along the Pacific coast of North America. This, they
claimed was far greater than can be explained by mixing and variability; perhaps
new species must be denned.
That such distinct species exist is implicit
in the studies reported by Moodie (1972a,
b), in which a large black G. aculeatus is
described, living in the same lake but ecologically isolated from a leiurus form.
Selectively maintained polymorphism is reported by Hagen and Gilbertson (1972).
They further give evidence that mean
values for gill raker numbers, vertebral
number, and body depth diverge in streams
where leiurus and trachurus are sympatric,
and converge in lakes where they are allopatric.
Thus, it is apparent that in G. aculeatus
there is great environmental adaptability,
inherent variability, and responsiveness to
selective forces, and much opportunity in
sympatry for hybridization or character displacement, both of which have been reported.
1107
POECILIIDAE
The hybridization of Xiphophorus helleri
(swordtail) and X. maculatus (platyfish) is
common in aquaria but has never been
observed in nature, despite extensive and
intensive sampling. Yet these species are
sympaiiic in about 25% of their habitat
(Gordon and Rosen, 1951). Fertilization is
by copulation; the male gonopodia differ in
tip structure but this in itself seems not to
provide a mechanical barrier. The gonopodium acts as a holdfast; its tip must be
intact for insemination to occur (Clark et
al., 1954). These authors have detailed the
courting behavior repertory of the two species. No single difference between them is
sufficient to account for the failure of the
species to hybridize in nature. They conclude that "the isolating mechanism between the swordtail and the platyfish
appears to depend on an array of partially
isolating factors. Each alone is not sufficient to insure isolation, but acting
together these factors so reduce the probability of hybridization that under natural
conditions the isolation seems to be complete" (Clark et al., 1954, p. 218).
In this instance, therefore, it seems that
sympatric character displacement starts
with differences in summed behavioral responses. Under artificial conditions the
limits to freedom of action and choice are
sufficient to upset the balanced systems
which operate in nature. Gonopodial differences in form, not yet effective as barriers
(i.e., still insufficiently displaced) perhaps
are evolving to reinforce mechanically the
present behavioral isolation.
Liley (1966) considered ethological isolating mechanisms in four sympatric species
of Poecilia. Natural hybrids among these
species are unknown; artificial hybrids have
been obtained but rarely and seem not to
reproduce further. Once again gonopodial
differences are apparently not sufficient to
act along as barriers to hybridization,
though this has not been critically examined. Behavioral differences, particularly
in early courtship behavior of males, and
the selective responsiveness of females seem
to be paramount. The sums of the differ-
1108
J. R. NURSALL
ences (i.e., a series of small behavioral character displacements) are the most important
features. In the case of these Poecilia spp.
ethological isolation may be sufficiently
strong not to require the reinforcement of
mechanical (gonopodial) differences, which
in part are slight and less than the xiphophorine differences reported by Gordon and
Rosen (1951) and Rosen and Gordon (1953).
while the species flocks are subject to "K"
selection (MacArthur and Wilson, 1967).
COTT1DAE
Andreasson (1969a,fr, 1972) has examined
the consequences of sympatry between
Cottus poecilopus and C. gobio in Scandinavia. C. poecilopus is believed to have
arrived first, probably from the east and
the northeast post-glacially. C. gobio arCICHLIDAE
rived later, and now inhabits the lower
This family is exceptionally important reaches of streams, having displaced C.
because of its usefulness in ethological poecilopus to upper reaches (Fig. 5). There
studies and its remarkable evolutionary his- are areas of sympatry, but even in those one
tory in the great lakes of Africa. Both of finds ecological segregation. C. poecilopus
these aspects of the biology of cichlids have is widespread in the habitat where it is
a vast and growing literature; Fryer and found alone, but where the two species are
lies (1972) provide a large reference list. co-existent, C. gobio is found in stronger
In lakes where there are more than 170 currents, with C. poecilopus restricted to
endemic species in eight genera, four of weaker currents and reservoirs. Hydroelecwhich themselves are endemic (Victoria), tric regulation of streams is altering distrior more than 200 endemic species in 23 bution patterns, but there is a remarkable
genera, 20 of which are endemic (Malawi), distinction in the nature of the tributaries
or 126 species in 37 genera, of which 33 are which the species inhabit preferentially.
Where there is direct sympatry, some
endemic (Tanganyika) (Fryer and lies,
1972, p. 17, Table 2), one might expect to hybridization takes place, but this is found
find clear examples of character displace- only where one species is rare, i.e., lacks
ment. The usefulness of this family of fishes opportunity to mate conspecifically.
Behavioral and physiological studies
in this regard may be increased by the apparent speed with which some speciation (Andreasson, 1969a,b) show similar ecohas taken place, e.g., in Lake Nabugabo logical requirements, with C. gobio having
(Greenwood, 1965). In Lake Victoria par- a higher temperature tolerance and a lower
ticularly, the genus Haplochromis should oxygen requirement. Both species have acprovide examples. Furthermore, the great- tivity peaks after sunset, but C. poecilopus
est part of the diversity that has evolved begins its activity somewhat earlier, and at
has been trophic, and exceptionally spe- the Arctic Circle displays a phase-shift,
cialized niches have been utilized—one changing from dark-active in summer, to
light-active in winter.
could almost say "invented."
Here is an example of habitat displaceThe very exuberance of diversity in
African cichlids precludes analysis here, but ment, in which behavioral and physiocertainly intensive behavioral, ecological, logical variables are segregated and accentuand morphological studies in the field ated. It would be useful to compare activity
would clearly demonstrate the nature and cycles and physiological requirements of C.
reality of character displacement in fishes, poecilopus and C. gobio where they are allopatric, e.g., on the east slope of the Urals
if that is possible.
Fryer and lies (1969) make a useful anal- and in alpine Europe, respectively.
ysis of patterns of evolution of African
PERIOPHTHALMINAE
cichlid fishes, comparing those of Tilapia
spp. with those of species flocks (e.g., Haplochromis spp.), suggesting the Tilapia type
The mud-skipping gobies (Periophthalto be under the influence of "r" selection, mus spp. and Periophthalmodon spp.) are
CHARACTER DISPLACEMENT AND FISH BEHAVIOR
1109
FIG. 5. Distribution of Cottus gobio and C.
poecilopus in Scandinavia. (From Andreasson, 1972,
with permission of Zoologica Scripta.)
widespread through the Indo-Pacific, commonly inhabiting tidal mangrove areas.
Near Townsville, northern Queensland,
several species live sympatrically. In a small
area, not much more than one hectare of
which was examined, at least four species of
Periophthalmus as well as one Periophthalmodon co-exist. The species can be distinguished although initially, in the field,
they all look alike. My experience was that
behavioral differences in captured specimens in aquaria were the first distinctions
seen, which led to a search for morpho-
logical differences, which in turn could be
used for field recognition. Then ecological
differences became apparent. At the present
time I cannot name all the species; the
formal systematics simply are incomplete.
On the whole, mudskippers are aggressive, inter- and intraspecifically. In the
latter case, size is most important in the
resolution of agonistic encounters. A big
fish invariably dominates a lesser. Interspecifically, size is important, but other
factors also intrude. Table 2 shows the size
relationships of small samples measured
1110
J . R . NURSALL
paired encounters SBB and RF did not react antagonistically, although SBB generally
was more active, i.e., moved about more in
the aquarium.
A. Comparison of mean total lengths (X,)
An attempt was made to relate these
2
Species
.K, (mm)
Range
s
BB
4
32.2358 reactions to field behavior, but shortage of
85.98
79.5-91.5
time, a neaptide period, and relative scarcity
RS
4
:223.7500
72.25
55.0-91.5
RF
8
65.13
55.0-74.0
50.4821
of BB and RS made it impossible to outline
56.54
11
SBB
3.4346
52.0-58.5
the relationships completely. What was
seen
was as follows. The Three-Mile Creek
Significance of differences in X, (Student's t test)
mangrove area inhabited by the mudskipP
Pairs compared df
t
pers is flooded tidally twice a day, the creek
BB/RS
N.S.
6
1.7162
>1
overflowing
its banks and spreading several
BB/RF
5.0750
<.001
H.S.
10
tens of meters (on high spring tides). PeriBB/SBB
H.S.
76.8780
<.001
13
ophthalmodon sp., by far the largest of
RS/RF
N.S.
10
1.1486
>-2
RS/SBB
H.S.
<.01
13
3.6485
these mudskippers (to >250 mm) but not
RF/SBB
3.8709
H.S.
<.01
17
treated in these tests, appeared to stay always in or beside the creek channel. BB
when freshly killed. Measurements of pre- and SBB tended to stay at the margin of
served specimens corroborate these figures high water, i.e., with tidal overflow they
for the comparison of BB/RS where no migrated across the mangrove flats followmore specimens are available. In Table 2 ing the water's edge. At low tide they were
and Figure 6, the species are identified by found along the edge of the creek. RF (and,
abbreviations which reflect superficial spe- I think, RS) were inhabitants of the mancies recognition marks. Agonistic encoun- grove flats, appearing on the moist surface
ters involved, among other things, lateral even at low water, or disappearing into
display including the erection of the an- burrows when the surface dried. The result
terior or both dorsal fins. The dorsal fins of these spatial relationships is that when
are brightly colored with red, yellow, black, the tide rises and water moves across the
and white, the patterns differing from spe- mangrove flats, BB and SBB migrate into
cies to species. The dimensions of the fins
also vary from species to species. Dorsal fin
BB
RS
RF
SBB
differences were the first specific distincBB
SCORES
tions noted. Body colors also vary but these
\
BB • •
•
are labile, with various arrangements of
R
S
OO
O
black blotches, silvery guanine patterns,
RS
RF « O red and white spots, and darkening and
SBB • O "
lightening of the whole or part of the body
RF
under different conditions.
Figure 6 illustrates graphically the agonistic relationships of the four species of
SBB
Periophthalmus as tested in a large series
of encounters between pairs studied in the
laboratory. BB, the largest species (probably FIG. 6. Agonistic relationships of four species of
Periophthalmus vulgaris Eggert) displayed Periophthalmus from Townsville, Queensland. The
upper half of each square represents the species
before, and chased all other Periophthal- listed
along the top; the lower half of each square
mus species, or caused them to retreat. In represents the species listed to the side. A solid
aquaria, with mixed populations BB would circle means dominance in paired encounter; an
on occasion catch and eat smaller speci- open circle means retreat in that encounter. A dash
means no strong reaction. In encounters between
mens. RS, although second-ranked in size, conspecifics,
not plotted here, the larger of the pair
would retreat before all other species. RF invariably dominated. BB = black blotch; RS =
dominated RS whether larger or smaller. In red spot; RF = red fin; SBB = small black blotch.
TABLE 2. The total length size relationships of four
species of Periophthalmus from Townsville,
Qld., Australia.
X XX
X X XXX X XXX \
CHARACTER DISPLACEMENT AND FISH BEHAVIOR
TABLE 3. Comparison of mean total lengths and fin
proportions among four Periophthalmus spp.,
Townsville, Queensland.
Species compared
Ratio X,
BB/RS
BB/RF
1.19
1.32
1-52
1.11
1.28
1.15
BB/SSB
RS/RF
RS/SBB
RF/SBB
Ratio
RatI
Dl/Dl
° D,/D2
1.29
1.40
1.61
1.09
1.25
1.15
RF (? and RS) regions, which undoubtedly
accentuates interspecific reactions.
Stebbins and Kalk (1961) and Gordon
et al. (1968) have described aspects of the
behavior of Periophthalmus sobrinus, an
east African-Malagash form. Gordon et al.
(1968) described a number of behavioral
and physiological differences between
allopatric populations, and raised the possibility of these signalling incipient speciation. Published keys to Periophthalminae
ascribe many subspecies to the species (e.g.,
Eggert, 1935/36; Koumans, 1953). The
Townsville experience shows a complex
sympatry. These lines of evidence might all
be used circumstantially to suggest the
possibility of character displacement taking
place in this group of fishes, or at least to
suggest the utility of seeking specifically for
evidence of character displacement together
with systematic revision of the mudskippers.
I made an attempt to devise quantitative
measures of differences between the Townsville species, to see if one could support the
suggestions of MacArthur and Wilson
(1967) that the difference of the means of
two species would come to lie at about 30 to
50% of the common mean. Consistent differences were not found within the 30 to
50% range in the characters measured
(total length; area of first dorsal fin; second
dorsal fin; dorsal fins combined). These
characters were chosen because they seemed
to be most important in agonistic encounters. The ratios closest approximating the
range are shown in Table 3.
A tentative summary of behavior and
niche requirements for the four species of
Periophthalmus can be given as follows:
1111
BB : large, aggressive, active, tidal migrant.
SBB: small, aggressive, active, tidal migrant.
RF : medium, less-aggressive, less active, non-migrant.
RS : medium, unaggressive, quiescent,
non-migrani.
With such a distribution of size and activity patterns, it is obvious that each species
may utilize some portion of a common
habitat. A complex displacement is present.
It must be pointed out that extra-tidal
circadian differences were not examined,
and one would expect that they would be a
fundamental part of the distinctions noted,
e.g., RS may be crepuscular or noctural,
which would leave it free to utilize the
habitat in the absence of the other species.
FISHES OF CORAL REEF COMMUNITIES,
ESPECIALLY POMACENTRIDAE
The faunal complexity of a coral reef
community is practically indescribable. One
of its features is the obviousness of its components, i.e., that so many species are visible
and active together, sharing a habitat
volume. After this impression, however,
comes the realization that the invisible components are at least as abundant, and that
the shared habitat extends far beyond that
part of which the observer is immediately
aware. The student of reef communities
must start by concentrating on one species,
or population, or small co-active group,
hoping not to be too distracted by the
multifarious activities that constantly impinge on his senses.
Much work in coral reefs has been
centered on Pomacentridae. These are
colorful, active, aggressive fish, commonly
territorial during all or part of their postlarval life. It has been remarked that "there
is an underlying basic behavior pattern for
reproduction in the family from which the
characteristic patterns of each species have
been derived" (Reese, 1964, p. 459). This
is a statement of evolutionary divergence,
out of which one might expect to be able
to define instances of behavioral character
displacement, if they occur.
1112
J . R . NURSALL
TABLE 4. Feeding volumes of selected species to illustrate levels of substrate sharing.
LEVEL
1
Family
Species
Gobiidae
Lythrypnus elasson
L. nesiotes
Quisquilius hipoliti
Enneanectes altivelis
Clinidae
LEVEL
2
Clinidae
Pseudemblemaria signifera
Emblemariopsis
Starksia lepicoelia
LEVEL
3
Pomacentridae
Pomacentrus variabilis
Pomacentrus planifrons
But of potentially greater significance to
the coral reef community as a whole are
more generalized reactions of pomacentrids
and other fishes, especially the reactions
that guarantee living space. Space as space
is important. Smith and Tyler (1972) make
the important point that guarded, permanent home sites, even for a relatively small
proportion of species in a coral reef community could be an important mechanism
for stabilizing the community. They provide a basic substrate allocation against
which background all species move. Pomacentrids and members of several other
families provide this. In fact, there are
several levels of mostly non-competitive
species, assorted by size, that share the substrate, dividing it into territories that overlap from level to level, or into territory-like
areas. As an example of such I can report
a four-level group from Heron Island comprising (from smallest to largest): Ecsenius
spp. and others, mostly gobies; Cirripectes
spp. and others, mostly blennies; damselfish
(e.g., Pomacentrus spp. and others); and
surgeonfish (Acanthurus lineatus). Characteristically the inhabitants of each of these
levels pay little attention to the inhabitants
of the next level, though they share the
substrate. Of course there are exceptional
circumstances and individuals (e.g., Acanthurus lineatus confronting Pomacentrus
apicalis described by Nursall, 1974). One
may tabulate a similar relationship among
Caribbean fish from selected data from
Smith and Tyler (1972) (Table 4). In this
instance, feeding volume (reflecting territorial size) is used to distinguish levels.
Feeding
vol. m3
Density
ind/m 3
8.1
10.2
20.4
21.8
0.003
0.003
0.003
0.003
.03
.23
.04
.02
15.6
19.5
21.3
0.08
0.03
0.08
.05
.01
.04
S50.0
56.5
0.57
0.31
.09
.10
Mean
SL mm
This suggested superstructural arrangement
would well repay study.
The data of Low (1971) suggest defense
of a food supply as a proximate cause of
territoriality, at least in Pomacentrus flavicauda, and that such a single ecological
factor may have enough selective force to
be significant in evolution. Low suggests
that as a force in the evolution of territoriality; it might also be taken as a speciational force between teritorial siblings,
given behavioral differences in defence.
In a series of papers, Sale (1968, 1969a,fe,
1971a,6,) has explored the question of habitat selection in certain acanthurids and
pomacentrids, emphasizing changes made to
accommodate increased size.
I shall dwell briefly on two aspects of the
biology of coral reef fishes to illustrate possible approaches to identification and analysis of character displacement.
The first of these aspects is the lability of
color and color change within a species, for
which no better example than that of Eupomacenlrus variabilis can be invoked. Emery
(1968) gives extensive descriptions of pomacentrid color repertories. Myberg (1972)
discusses one species in detail. Under various stimuli, especially in breeding season,
a wide and variable repertory of changes
is available. Although the repertory is
species-wide, it is to be suspected that individuals have their own range within it. To
generalize, it might be said that animals
behave, not to form a group, but to distinguish themselves as individuals within it.
Yet their individualism must not be so great
that they divorce themselves from their
CHARACTER DISPLACEMENT AND FISH BEHAVIOR
group. In that way lies extinction. Nonetheless, somewhere between excessively deviant
self-expression and group homogeneity one
should find the kind of expression that will
distinguish related species and allow the
displacement of characteristics which will
establish new species borders and more precise utilization of habitat and niche. Perhaps that mysterious quality of niche width
or breadth (Van Valen, 1965; MacArthur
and Levins, 1967) and its associated problem of genetic load (Lewontin, 1967; Selander, 1970) represents the highly flexible
response of species to their habitats, with
the alternative possibilities of stabilization
(limitation) or differentiation (expansion).
In terms of character displacement, differentiation could work fore or aft; a variable
species could show displacement with a
sibling species already differentiated (an
example of speciation processes under directional selection), or it could have displacement of deviant members from the
modal mass (an example of speciation processes by disruptive selection).
The second aspect of the biology of coral
reef fishes is illustrated by Figure 7. This
represents mapped territories of five pomacentrid species in a small area of the edge
of the shallow coral reef platform off Heron
Island, Queensland. The map is synoptic,
representing in static fashion a sum of
results of 4 weeks' observation. The most
important species are Pomacenlrus tripunctatus, P. apicalis, and P. jenkinsi. P. flavicauda and Abudefduf dicki were represented by juveniles, which clearly avoided
contact with adults of the other species by
staying hidden most of the time within
coral interstices. They did, in fact, represent
what might be thought of as "colonizers,"
or emigrants from nearby areas where their
conspecifics were more concentrated; P.
flavicauda normally is closer to shore, on
the shallow flats; A. dicki typically is found
over the edge of the reef in deeper (1+ m)
water. However, each of these is also territorial in mixed communities, in its usual
habitat.
What such mixed communities seem to
illustrate is the establishment in close association of sibling species after they have
1113
diverged. This suggests that if character
displacement does take place, it occurs
quickly and is soon reinforced by other
differences, morphological and in compound behavior. In the example given, the
pomacentrid species are now widely divergent, but there are many less divergent
species in the same area (i.e., about Heron
Island) and less clear cut separations.
The pomacentrids defending territories
in a mixed community do so with no apparent differences to intra- or interspecific
transgressors (from among other territorial
pomacentrids). If there be an interspecific
hierarchy, it seems to be dominated by P.
apicalis, the largest of the competing species. P. jenkinsi ranks next in aggressiveness,
as judged by relative success in confronta-
KIG. 7. Inter- and intraspecific territorial relationships among pomacentrid fishes at reef edge at
Heron Island, Queensland. The territories are held
long-term, probably life-long, and represent activity
by both sexes. Further details in the text. T =
Pomacenlrus tripunctatus; A = Pomacentrus apicalis; J = Pomacentrus jenkinsi; F = Pomacentrus
flavicauda; D = Abudefduf dicki.
1114
J. R. NURSALL
tions, and P. tripunctatus the least. Evidence for this ranking include manipulation of territorial boundaries by erecting
new topographic features by shifting coral
rocks; in the cases where P. apicalis boundaries were affected, it was able to expand
its territory at the expense of others. Similarly P. jenkinsi dominated P. tripunctatus
at manipulated borders, and again during
an attempt by a member of each of the two
species to take over a vacated territory lying
between them, at which time P. tripunctatus was excluded entirely from expanding.
Behavioral reactions at confrontation are
usually brief—a threatening charge by the
inhabitant of a territory followed by the
retreat of the transgressor. However, the
display can be attenuated and examined in
its parts by providing a transgressor who
does not retreat, namely a mirror-image.
Such doughty opponent forces the defender
to present his full set of responses.
Experiments undertaken in this regard
at Heron Island were not complete, but
they did reveal some differences and similarities. The descriptions given here must
be taken only as an introduction to the
subject, which promises to be a most productive approach. In no instance here is
the complete repertory exposed.
P. apicalis appeared to have the most
complex reaction to a mirror-image, a compound lateral display. First it sits a few
centimeters from the mirror tilted slightly
away from it, exposing its belly and bright
blue-edged pelvic fins. After 1 or 2 sec
it becomes vertical, turns its head away
slightly, raises its dorsal fin and spreads its
caudal, these two fin actions exposing bright
golden-yellow dorsal fin edges. It then swims
away, and returns to display the other
side in the same way. It will return several
times, following a figure-eight pattern across
the mirror. No direct approach to the mirror was seen.
P. jenkinsi usually approached the mirror
directly, darkening dorsally and on the
head. The dorsal fin is raised. Sometimes it
nips head first at its image; sometimes it
accelerates rapidly by the mirror. The continued presence of a mirror image results in
a lateral display; this is chiefly a belly display, the fish tilting slightly to expose the
bright yellow pectoral and pelvic fins. The
dorsal fin is also raised, but there seems not
to be a special dorsal fin display. Rasa
(1969) details displays of P. jenkinsi induced
in laboratory studies.
P. tripunctatus was observed only to approach the mirror-image head first, with
dorsal fin raised, and nip. This might be
done repetitively. It should be noted that
P. tripunctatus does not possess brightly
colored fins like the two otb^r species.
There are obvious relationships in these
behaviors. Although it would be facile and
misleading to read too much into an apparent scale of differences, such a simpleminded comparison may serve to base an
initial hypothesis for subsequent study, such
as, e.g., that differences as described may
represent kinds of behavioral character displacement, reinforced by, and reinforcing
morphological changes, now established as
strong species differences. This kind of behavioral distinction might be sought among
the less clearly differentiated sibling species
of Pomacentrus, Chromis, and Abudefduf.
The differentiation of sibling species is
difficult, and calls for periodic systematic
revision. Among Caribbean fishes several
Eupomacentrus spp. cause difficulties. A
new revision by Greenfield and Woods
(1974) is a case in point, dealing as it does
with species of interest behaviorally to
ichthyologists. The new revision now distinguishes four species, separated on meristic and gill raker counts, as well as scale,
conformational, and color differences. E.
fuscus, a name heretofore widely applied
across the Caribbean, is now limited to
specimens from Brazil. E. variabilis, referred to above, extends from Brazil, Venezuela, and Belize to Puerto Rico and
Florida. E. dorsopunicans is found throughout the Antilles, along the Central American coast from Panama to the Campeche
Bank, to Florida and the Bahamas. E.
diencaeus is reported from Belize, the
Greater Antilles, Anguilla, and the Bahamas. This means that a group of species,
members of which have been studied under
various names, is now being distinguished
CHARACTER DISPLACEMENT AND FISH BEHAVIOR
throughout the Caribbean faunal province,
having a northernmost representative, diencaens, a southernmost representative, fuscus, and a couple of geographically intermediate species, with varying degrees of
overlap. Field identification of these is
difficult. Surely study of morphological, behavioral, and ecological displacement in
regions of sympatry would be of interest
and significance.
CHARACTER DISPLACEMENT: THE NATURE
AND APPLICATION OF THE PHENOMENON
Unequivocal evidence of character displacement in the sense of Brown and Wilson (1956) requires that two closely related
species be known allopatrically, under
which conditions they are similar in characters, and sympatrically, where they are
more distinctive, the characters under consideration having been displaced in relation
to each other. Therefore, zoogeographic or
broad systematic studies are best suited to
cover such evidence. None of the examples
I have given is unequivocal. In part this is
owing to the fact that ichthyologists seem
not to have been attracted to the concept
of character displacement, which means
that they have not extended the geographic
range of their studies. In other part it is
owing to the fact that field behavioral
studies are invariably local, and moreover,
to date, have stressed intraspecific reactions.
I must make it clear here that none of the
examples used by me in this review have
been published with character displacement
in mind as an aspect of the study; in each
case the interpretation has been mine, a
posteriori.
Character displacement is a post-speciational, pre-zygotic isolating mechanism,
which therefore serves to reinforce species
differences. Failure of isolating mechanisms
leads to hybridization, which Brown and
Wilson (1956) warn might be misinterpreted character displacement, in some instances. Among fish, the morphological
study of hybridization has been intensive,
following the early work of Hubbs (1955)
and his co-workers. Certainly among the
freshwater fishes, the distinction seems to
1115
be clear. For example, Bartnik (1970) is
able to distinguish clearly the ethological
mechanisms isolating sympatric species
within a family (Cyprinidae) wherein hybridization is demonstrated to occur commonly, i.e., either hybridization or mechanisms preventing hybridization can be
demonstrated under particular conditions.
As MacArthur and Wilson (1967) recognize the occurrence of displacement, it can
be taken as no more than a weak rule. It
has to be specified in any instance. It is
genetically based and may be treated by
the methods of population genetics (e.g.,
James, 1970) or quantitative ecology (e.g.,
"niche overlap," May, 1973).
The ideas of "r" and "K" selection (MacArthur and Wilson, 1967) also are pertinent
to character displacement. Of the examples
in this review those involving Coregonidae,
Gadidae, Gasterosteidae, and Cottidae seem
to be cases operating under "r" selection,
i.e., in relatively uncrowded environments
where productivity is favored. The examples given are relatively clear cut, with
two species involved and relatively restricted areas of sympatry. The examples
taken from Pomacentridae and Periophthalminae seem to be cases under "K" selection,
where crowded environments favor efficiency in conversion of food. Fryer and lies
(1969) suggest that both "r" and "K" modes
operate for Cichlidae. Where "K" selection
is working, the examples among fish become
complicated, several species being involved
in overlapping territories and multispecific
interactions.
Although not yet so used among fishes,
it is probable that the recognition and definition of character displacement could be
useful to distinguish more clearly the
boundaries of sibling species. Its fundamental use would be to rationalize systematic differences, and so it can take its place
as a descriptive tool.
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1116
J. R. NURSALL
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