Download Contrast Between Solitary and Clonal Lifestyles in the Sea

AMER. ZOOL., 19:669-681 (1979).
Contrast Between Solitary and Clonal Lifestyles in the Sea Anemone
Anthopleura elegantissima
LISBETH FRANCIS
Biology Department, Bates College, Lewiston, Maine 04240
SYNOPSIS. The common intertidal sea anemone Anthopleura elegantissima (Brandt) occurs in
two forms, the clonal aggregating form and the solitary form. The obvious differences
between the two apparently result from the presence of asexual reproduction in the clonal
aggregating form and its absence in the solitary form; resulting differences in growth form
suit the two anemones to different lifestyles. The clonal form is well suited to life higher in
the mid-intertidal. Asexual reproduction, resulting in moderately small individual size and
close association with clonemates, improves its resistance to physical stress (drag and desiccation), and makes it a superior competitor in exposed habitats higher in the intertidal where
species diversity and predator pressure are low. The larger solitary animals live in more
protected microhabitats lower in the intertidal and subtidal, and are probably more resistant
to predation and less able to withstand physical stress or intense intraspecific competition.
The two forms also have different biogeographic ranges. While the clonal aggregations are
quite common at rocky sites at least as far north as Vancouver Island in British Columbia,
populations of solitaries have not been found north of Point Reyes, California. Apparently
the two forms are re productively isolated; phenotype frequencies are very different for
clonals and solitaries living at the same locations, while the between-sample variation within
each form is relatively small. These differences in phenotype frequencies, biogeographic
range and microhabitat suggest that the clonal anemones and the solitary anemones known
as Anthopleura elegantissima are actually a sibling species pair.
Some anemones that reproduce asexually live in clonal aggregations. Among the
The sea anemones are solitary polypoid most conspicuous of these are clonal agCnidarians in a phylum of colonial animals gregations of Anthopleura elegantissima
that often have complex life histories. The (Brandt), which cover substantial areas of
typical hydroid adult (class Hydrozoa) is intertidal rocky substratum from British
first an asexual colony of bottom-dwelling Columbia to Northern Mexico.
polyps, and finally a pelagic fleet of sexual
A. elegantissima and several other clonal
medusae. The typical jellyfish (class Scyph- anemones also occur as larger, solitary indiozoa) may or may not spend time as a polyp viduals. I consider here the relationship bebefore becoming free-floating and sexual. tween the clonal and the solitary forms of A.
Even within the entirely polypoid class An- elegantissima, and possible diversifying
thozoa (anemones, sea pens, hard and soft selection favoring each of the two forms.
corals, etc.), all but three of the eleven orders are colonial. The Actiniaria (true
CLONAL AND SOLITARY ANEMONES
anemones) are an order of solitary sexual
polyps that may also reproduce asexually
Several intertidal anemones that repro(Chia, 1976).
duce asexually show marked variation in
size correlated with microhabitat. In Central and Southern California, the common
actiniid
Anthopleura elegantissima is deI thank T. H. Bullock of Scripps Institution of
Oceanography, and A. O. D. Willows, Director of the scribed as occurring in two forms, the clonal
Friday Harbor Marine Laboratory for providing space
aggregating form and the solitary form
and equipment; V. B. Pearse, G. S. Lewbel and others (Hand, 1955a; Fig. 1). Individuals of the
for hospitality and assistance in the field; and A. E. clonal form are usually less than 3.5 cm
Balber and R. Strathmann for critically reading the
across the oral disc (Hand, 1955a); and they
manuscript. The work was supported in part by a
live in clusters segregated by genotype,
Bates College faculty grant to the author.
INTRODUCTION
669
670
LISBETH FRANCIS
FIG. 1. Clonal (A) and solitary (B) forms of the submerged (ripple marks on the water's surface,
anemone known as Anthopleura elegantissima in the lowupper left) clones separated by an anemone-free
mid-intertidal of the Scripps preserve, La Jolla, space. Eight submerged solitary individuals are visible
California. On the boulder (upper right) are two half- in the pools and crevices at the boulder bases.
the products of longitudinal binary fission They live out of contact with other indi(Francis, 1973a). Solitary animals are viduals, and are commonly found in more
larger, averaging 6.5 cm across the oral disc. sheltered situations, often living with 2/3 to
CLONAL AND SOLITARY ANEMONES
3/4 of the column buried in sand (Hand,
1955a). Individuals of both forms attack
and damage genetically different anemones of either form (Francis, 19736).
In Chile, small adults of the actiniid
anemone Phymactis clematis live in dense
clonal aggregations below the mussel beds,
while larger solitary specimens live slightly
lower in the intertidal (Stotz, 1979). Hand
(19556) and Purcell (1977) report a similar
situation for the acontiate anemone Metridium senile fimbriatum in California. Clus-
ters of small individuals are common inshore, while larger, less densely settled
individuals are restricted to deeper waters
offshore. Uchida (1936) reports the opposite pattern for the very small acontiate
anemone Haliplanella luciae in Japan.
Individuals higher in the intertidal are
larger and apparently are not reproducing
asexually.
It is not clear what the relationship is between large and small individuals of these
anemones. Differences in growth form, individual size, sociability and microhabitat
might be genetically determined, or they
might result from developmental responses to different environments.
RELATIONSHIP BETWEEN THE TWO FORMS
KNOWN AS ANTHOPLEURA ELEGANT1SSIMA
Occurrence of asexual reproduction
The solitary nature of the large anemones suggests that they are not reproducing asexually. If they were, one would
expect to see some large individuals in contact with each other in the field. Like individuals of the clonal form (Francis, 19736),
the solitary anemones respond aggressively
to contact only with genetically different
individuals; contact with one of their own
excised tentacles does not elicit aggression.
However, I always find very large individuals to be dispersed, even in high density
populations.
After dividing asexually by longitudinal binary fission, anemones of the aggregating form have a scarred area the length
of the column that is discernible for six
weeks or more. For the clonal form of Anthopleura elegantissima, individual size varies
both within and between clones (Francis,
671
1973a, 1976). Fission occurs seasonally
(Hand, 1955a; Sebens, 1977), and is influenced by light level (Pearse, 1974). Sebens
(1977) finds that starvation increases fission
rates, at least temporarily; and he develops a generalized model based on feeding and energy considerations to account
for differences in polyp size (Sebens,
1979).
Division scars were present on 17 of 42
individuals (45%) collected from the middle of several clonal aggregations in the
Scripps preserve area, La Jolla, California,
during June and July of 1976. None of the
52 solitaries of various sizes (0.34 to 104.7g
wet weight) collected nearby had fission
scars, and none underwent fission in the
laboratory where they were kept for up to
three years. The solitary anemones do not
appear to be reproducing asexually.
Size, microhabitat and relative success
Although the solitaries and the clonals
may be found living side-by-side, they occur
in somewhat different microhabitats. To
document these microhabitat differences
and to provide information concerning the
relative success of the two forms at different
tidal heights, I examined two systematic
samples in a mixed population of clonals
and solitaries at the Scripps preserve (Fig.
1). Each individual and each clone encountered was counted and measured until each
sample included 100 genotypes: 100 genotypes at greater than two feet above MLLW
(mean lower low water), and 100 at between MLLW and plus two feet. An assistant with SCUBA gear examined 74 solitary
individuals on a shallow subtidal rock in La
Jolla Cove.
For animals that reproduce asexually, it is
difficult to be certain that no genotypes are
sampled more than once. However, in the
San Diego area, tightly packed clonal
aggregations are isolated on ledges and
boulders that are surrounded by sand. The
boulders are convex and retain little water
at low tide; and in response to desiccation,
the clonal individuals reduce evaporation
by remaining in close contact with adjacent
clonemates (Roberts, 1941; Francis, 1976).
As a result of intraspecific aggression, adja-
672
LISBETH FRANCIS
cent clones remain separated by noticeable
anemone-free zones (Fig. 1). Although detachment and resettlement of adults is possible, successful resettlement must be quite
unusual in areas of sand, large rounded
boulders and fairly heavy surf. Therefore,
in this and all subsequent sampling procedures, each separate, contiguous group of
clonals is assumed to be a separate genotype. Since the solitaries apparently do not
reproduce asexually, each separate individual is assumed to possess a unique
genotype.
For each solitary individual, I measured
the maximum contracted column diameter.
Since the size of clonal individuals varies
both within and between aggregations
(Francis, 1976), I measured what seemed
average-sized specimens from each clone
and recorded either the number of individuals or the area covered by each aggregation.
Microhabitat information for the two intertidal samples is shown in Table 1. These
data demonstrate that where the two forms
co-occur, they occupy somewhat different
microhabitats. The solitary form is more
often found in the lower mid-intertidal in
protected areas at the bases of boulders or
in pockets and crevices, and it may extend
into the subtidal. The clonal form, which is
apparently more tolerant of wave buffeting, desiccation and temperature extremes,
is common in very exposed positions on
open rock surfaces higher in the mid-intertidal.
For organisms that reproduce asexually,
relative success is very hard to assess. Without deciding whether the individual anemone or the clone, as the genetic entity,
should be the basis for evaluation, I compare the individual size, number of genotypes, number of individuals, amount of
substratum occupied and biomass of each
form at each tidal height (Table 2). These
were roughly calculated using the field
data, and laboratory data on the relationship between column diameter in centimeters and wet weight in grams for the
solitary individuals: log wet weight = 3.27
(log column diameter) - 0 . 5 , (R = 0.92).
Solitary genotypes outnumber clonal
genotypes at all three tidal heights; but in
the higher intertidal sample, the clonal
population is more successful according to
any other measure used. In the lower intertidal sample, the solitary population is more
successful in terms of biomass.
Biogeographic distributions
During April, 1975, V. B. Pearse and I
conducted a survey of mid-intertidal Anthopleura species in exposed rocky areas between Punta Banda in Baja, Mexico, and
Point Conception, California. During June,
1978, I checked for the presence of these
anemones at exposed rocky sites along the
northern Pacific coast between San Juan
Island in Washington and Bodega Head in
California. I worked for extended periods
near Pacific Grove, Santa Barbara, and La
Jolla, California.
Figure 2 shows sample sites where observations were made and projected ranges for
the three forms of Anthopleura commonly
found. Sebens (1977) reports similar ranges
for these animals. The giant green anemone, Anthopleura xanthogrammica is common
on exposed outer coast north of Government Point, California (which lies on the
dividing line between northern and southern coastal waters). It is a large anemone
(average column diameter 12 cm; Hand,
1955a) that does not reproduce asexually
and is not known to attack conspecifics
(Francis, 19736). Like the solitary form of
A. elegantissima, it is found just below and
overlapping the zone dominated by beds of
the mussel Mytilus californianus and clonal
aggregations of A. elegantissima.
Aggregations of the clonal anemone Anthopleura elegantissima are common at rocky
locations all along the coast. Populations of
large solitary individuals are common as far
north as Santa Cruz, California, but are not
found at Bodgea Head or sites farther
north.
The ranges of Anthopleura xanthogrammica and the solitary form of A. elegantissima
are almost complementary, overlapping
only in the Monterey Bay area, a region
known for anomalous hydrographic conditions. Many warm water animals end their
ranges in the relatively isolated area of
warm water near Monterey Bay (cf., Mur-
673
CLONAL AND SOLITARY ANEMONES
TABLE 1. Microhabitat differences between clonal and solitary anemones (Anthopleura elegantissima)af too tidal heights.
Higher sample
(N=100)
Micro habitats
(mid-intertidal)
Open rock
surfaces
Pockets and
crevices
Base of
boulders
Lower sample
(N=100)
Clones
(N = 26)
Solitaries
(N = 74)
Clones
(N=12)
Solitaries
(N = 88)
42%
5%
67%
7%
42%
32%
33%
61%
15%
62%
0%
32%
phy, 1978). Populations of A. xanthogram- tissima belong to the same breeding populamica occur south of Point Conception at tions, I examined phenotype frequencies at
Point Dume and Bass Rock in Ventura seven sites in California during July and
County, and at Punta Banda, Mexico. August of 1978. Samples of 100 clonals and
These three exceptional areas are at the 100 solitaries were examined at each of five
heads of nearshore submarine canyons, sites along 30 miles of coast in the San Diego
probably in upwelling areas where some- area, at one site 200 miles north at Arroyo
what more northern organisms are com- Hondo, and at one site another 200 miles
mon.
north at Pacific Grove (Fig. 4).
Possible hybrids, with gross morphologiThe characters used are color markings
cal characteristics intermediate between on the tentacles, oral disc and columns of
those of Anthopleura xanthogrammica and the anemones. The following nine marking
those described for A. elegantissima, have patterns are assumed to be genetically debeen found where the two large anemones termined because their occurrence is conco-occur at Bass Rock (personal observa- sistent among individuals within a clonal
tion), and just north of their common range • group, and because they change only in
near Bodega (Michael Wang, personal intensity when the anemones are starved,
communication).
fed variable or unusual diets, or kept in the
The solitary form of Anthopleura elegantis- dark, causing them to lose their symbiotic
sima is probably prevented from extending algae: 1) tentacles with pink tips, 2) tentaits range northward because of increased cles with blue tips, 3) tentacles with opaque
predator pressure or competitive exclusion white or gold cross-bands, 4) pairs of tentacles with opaque, white or gold adoral surby A. xanthogrammica.
faces, 5) oral disc with radiating opaque,
white or gold sunburst pattern between the
Differences in phenotype frequencies
mesenterial insertions, 6) oral disc with
purple
color overlying the mesenterial inTo determine whether the clonal form
and the solitary form of Anthopleura elegan- sertions, 7) oral disc with reddish-brown
TABLE 2. Comparative success of clonal and solitary anemones (Anthopleura elegantissima) at three tidal heights.
Individual size
column diameters (cm)
Clonal
Solitary
(means ±sd)
Mid-intertidal
High sample
Low sample
Subtidal
1.7 ±0.2
1.6 ±0.1
-
3.4 ±1.2
3.6 ±1.4
3.4 ±1.5
Approximate ratios (clonals/solitaries)
Number of
genotypes
Number of
individuals
Surface
occupied
Bio mass
0.3/1
0.1/1
55/1
13/1
14/1
2.4/1
6/1
0.8/1
674
LISBETH FRANCIS
A.e.
(clonal)
Botanical Bay
Cape Flattery
San Juan Island
Yaquina Head
Trinidad Head
A.e.
(solitary)
Bodega Head
Santa Cruz
Pacific Grove
Government Pt.
Arroyo Hondo
Goleta Pt.
Point Dume
Corona
>—San Diego
Punta
Panda
FIG. 2. The Pacific coast of North America showing clonal aggregating anemone known as A. elegantissurvey sample sites and proposed ranges for the giant sima, and the solitary anemone, also called A. elegangreen anemone, Anthopleura xanthogrammica, the tissima.
color overlying the mesenterial insertions, in pools at low tide and were examined in
8) oral disc translucent, fluorescent green situ at night, when they tend to be exand 9) column blue or blue-green. General panded. Using a bright flashlight and bebackground color is not used, because it is ginning at an aribitrary spot, I examined all
not a consistent, stable character for these the anemones I encountered and recorded
anemones (Buchsbaum, 1968).
presence or absence of all nine color markSolitary individuals are often submerged ings for each. Clonal individuals, which are
CLONAL AND SOLITARY ANEMONES
usually exposed and contracted during low
tides, were similarly sampled, collected and
returned to the laboratory for inspection.
Care was taken to avoid multiple samples
from any single clone.
The bar graphs in Figure 3 show the percent frequencies of the color marking characters for clonals and solitaries at each of
the seven sample sites. Differences of approximately ten percent are significant at
the .05 level for samples of 100 using the
G-test with two-by-two contingency tables
(Sokal and Rohlf, 1969). Figure 4 shows
polygonal graphs of the same data. By
graphing each character on one of a set of
converging axes, one can examine and
compare an array of characters simultaneously.
The frequencies for seven of the nine
color markings are significantly different
for the two forms at all sample sites south of
Point Conception. North of Point Conception the otherwise consistent differences for
three of these patterns is reversed (pink,
tentacle tips, purple lines on the oral disc,
and cross-banded tentacles); however,
large differences between the forms are still
apparent.
Within each form, there are more significant frequency differences between
samples than would be expected by chance.
If the frequencies for all nine characters for
the five San Diego area samples are compared with San Diego averages, 11 out of 45
clonal frequencies are significantly different at the .05 level; and 10 of 45 are significantly different for the solitary form.
Choosing a significance level of .05 allows
an average of 2.25 chance differences in 45
comparisons. High phenotype frequency
variation among samples of clonals, and
among samples of solitaries in the San
Diego area may be artifact, perhaps the result of inaccurate scoring of the characters;
or it may reflect something real about the
populations, such as a tendency for infrequent reproductive success and patchy
settlement of larvae having common parentage.
Between-sample differences for a given
color pattern are not obviously clinal. However, there is obviously more total difference between San Diego, and Arroyo
675
Hondo or Pacific Grove populations than
between samples in the San Diego area (Fig.
4). Therefore, to measure such differences,
San Diego average frequencies for each
form are compared with the sample frequencies for that form at each sample site.
The difference between each character frequency is summed for all nine characters
and divided by nine to give, for each location, an average percent deviation of the
characters from the San Diego area mean.
The average character deviation for
clonals in the San Diego area ranges from
4.3 to 8.2 percent. The average deviation
for Arroyo Hondo clonals from the San
Diego norm is 13.5 percent, while that for
Pacific Grove clonals (north of Point Conception) is 23.3 percent.
For solitaries in the San Diego area, average deviations range from 4.0 to 8.3 percent. The average deviation for Arroyo
Hondo solitaries is 12.7 percent, and that
for the Pacific Grove population is 19.7
percent. For comparison, the mean difference between clonal and solitary averages in the San Diego area is 32.1 percent
per character.
There is apparently more genetic exchange between clonal populations living in
different water masses and separated by
500 miles of coastline than between clonal
and solitary populations living meters away
from each other in the same intertidal.
A sibling species pair
It is not obvious to what extent random
mating and panmixis can be expected
within a sessile intertidal species that has
epidemic spawning and long-lived planktonic larvae (Siebert, 1974). Increased differences in phenotype frequencies over
hundreds of miles, and some discontinuity
between populations in different major
current systems are patterns one might
predict. Color marking patterns on anemones are probably selectively neutral, if any
character is; and between-population differences are probably the result of genetic
drift. However, I cannot rule out the possibility that selection, acting either directly or
through linkage, accounts for some of the
observed variation.
676
LISBETH FRANCIS
1001
100.
Green oral di*c
Pink tentacle tip*
so
I
BR
50
AH
SIO
.£>
S
BR
SIO
C
E
AH
PG
PG
100
100-1
\l A
Purple lines on the o r a l dlac
Rad linea on the o r a l diac
50
soS
BR
BR
AH
SIO
SIO
C
E
AH
PG
AH
PG
H
PG
Blue tentacle tlpa
50
100-1
Blue column
S
BR
SIO
C
E
50
lOO-i
Croaa-banded tentacle*
03
UJ
_T7I
o
BR
111
Z>
SIO
AH
PG
50
fl
o
White tentacle palra
S
BR
SIO
C
E
AH
100
100-.
LU
Sunburn pattern on the oral disc
50
Q.
BR
SIO
SAMPLING
C
E
SITES
AH
BR
SIO
FIG. 3. Percent frequencies of nine color markings Rock (BR), Scripps preserve (SIO), Cardiff State
for samples of 100 clonal individuals (diagonally Beach (C), and Encinitas (E) are within 30 miles of San
hatched bars) and 100 solitary individuals (white bars) Diego. Arroyo Hondp (AH) is south of Point Concepof the anemone Anthopleura elegantissima at each of tion, near Santa Barbara; and Pacific Grove (PG) is
seven sample sites in California. Sunset Cliffs (S), Bird north of Point Conception, on Monterey Bay.
677
CLONAL AND SOLITARY ANEMONES
Sunaat Cliff*
San Dlago ar«a, ( Avaragaa)
100
GR
70
Bird Rock
RD
\
•
Scripps
Arroyo Hondo
90
FIG. 4. Polygonal graphs showing percent frequen- average frequencies for the San Diego area (lower left)
cies for nine color markings in samples of 100 clonal gives the arrangement of color characters on the nine
individuals (diagonally hatched polygons) and 100 sol- axes: pink tentacle tips (PK), purple lines on the oral
itary individuals (vertically hatched polygons) of the disc (PP), blue column (BC), white tentacle pairs (WT),
anemone Anthopleura elegantissima at seven sample sites green oral disc (GR), red lines on the oral disc (RD),
in California, (central map). Map symbols are keyed to blue tentacle tips (BT), crossbanded tentacles (XB),
the polygons, which are arranged south to north going and sunburst pattern on the oral disc (SB).
left to right from the upper left. The polygon showing
678
LISBETH FRANCIS
Phenotype frequency differences be- a suitable substratum, a conservative intween the two forms living at the same loca- vestment compared with the production of
tions seem too large and too consistent to be planktonic larvae by sexual reproduction.
explained except by lack of interbreeding Sebens (1977) points out that since division
between the forms. Since their intertidal tends to occur only once a year during the
distributions overlap, and since tidal height plankton-poor winter period, the increase
varies between samples, I do not believe in feeding surface area created by dividing
that these differences can be due to en- an animal two for one should make the
vironmental effects correlated with tidal clones more effective at catching plankton
height. Nor do I believe that gross differ- the following spring.
ences in food availability cause these differPurely in terms of sexual reproduction, a
ences in phenotype frequencies. Sebens successful, long-lived clonal genotype
(1977) finds that larger individuals of the should have the advantage over an equally
clonal form in Washington State feed on successful solitary individual that does not
mussels torn loose from upslope beds. multiply asexually. Assuming similar reHowever, between-sample variation should productive anatomy and physiology, a large
again eliminate consistent differences in clone of anemones with individuals numfood availability between the forms, since bering in the tens of thousands can certhe sample areas have extensive (Pacific tainly produce more gametes than can the
Grove), moderate (Arroyo Hondo, Encin- largest of the solitaries (column diameter
itas, Cardiff, and Scripps), poor (Sunset up to 20 cm).
Cliffs) or no (Bird Rock) mussel bed develGroup living may be advantageous in reopment near the sample sites.
ducing costs related to high surface to volTogether with the differences in growth ume ratios. The streamlined profile of a
by asexual reproduction, microhabitat and tight clonal group can reduce the air and
biogeography, the phenotype frequency water velocities to which the individuals are
data suggest that the clonal and solitary exposed thereby reducing air drying and
forms known as Anthopleura elegantissima hydrodynamic drag. At the same time, the
are different species, perhaps a sibling pair. individuals maintain many benefits of small
size such as large tentacle area for food
capture (Sebens, 1977) and large pedal disc
SELECTIVE FACTORS FAVORING CLONAL OR
area for attachment relative to their volSOLITARY LIFESTYLES
ume.
Advantages of asexual reproduction and clonal Individually these moderately small
clonal anemones prevent extreme drying
aggregation
during low tide exposure in several ways.
For a long-lived animal capable of regen- Like Phymactis clematis (Stotz, 1979), they
eration, like Anthopleura elegantissima, sim-can retract and enclose the tentacles and the
ple asexual reproduction by fragmentation oral surface by contracting the sphincter at
has some clear advantages. Growth by the top of the column, which also traps and
asexual multiplication allows the genotype holds water in the coelenteron. Shells and
(the clone) to increase in size indefinitely pebbles attached to the tubercles of the colwithout the mechanical problems inherent umn may serve as sun shades and also keep
in unlimited increase in individual size. the surface of the animal moist by capillary
Asexual reproduction may also be advanta- action. By living in groups, these anemones
geous in marginal situations where so few assure themselves a damp microhabitat,
clones are present that sexual reproduction one that can be extended as the clone exis impossible (Shick and Lamb, 1977). Fur- pands beyond the original crevice or edge
thermore, a genotype dispersed as a num- of a mussel clump onto formerly uninber of separate individuals is less likely to habitable, dry, open rock.
be exterminated.
The clonal form of Anthopleura elegantisDividing in half longitudinally produces sima is quite unusual in its ability to live in
large offspring that are already attached to exposed situations high in the mid-inter-
CLONAL AND SOLITARY ANEMONES
tidal over a wide latitudinal range. This
may be due in part to their ability to live in
tight aggregations while retaining at least
weak individual mobility. Pearse (1974) and
Fredericks (1976) find that individuals within clones move in response to differences
in internal and external oxygen levels, and
Roberts (1941) has shown that they move
in response to desiccation stress. This mobility could be important since the conditions to which they are exposed at low tide
vary seasonally.
The tendency to live in close contact with
members of the same species, while limiting
their mobility, allows these anemones to
blanket areas and exclude potential space
competitors such as barnacles, tube worms
and macroscopic algae. Association with
clonemates allows them to exclude intraspecific as well as interspecific competitors.
Asexual reproduction, which is the foundation of colonial sociality, may also provide a basis for true sociality (cooperative
association between physically separate
individuals). Since altruism toward a genetically identical individual is evolutionarily
equivalent to conventional selfishness,
cooperative associations between clonemates should be stabilized against disruption by "cheaters" (i.e., individuals that reap
the benefits of association without paying a
fair share of the costs). Even slight cooperative advantage should therefore lead to association between individuals produced
asexually. Within clones of Anthopleura
elegantissima there exists a very simple form
of social organization. These animals show
intraspecific aggression related to competition for space; individuals at the borders
between neighboring clones bear more of
the costs of clonal defense and are specialized as sterile warriors (Francis, 1976). The
ability to distinguish clone members from
all other individuals allows these anemones
to cooperate with clonemates while at the
same time interfering with all other competitors. The isolation of a possible alarm
pheromone (Howe and Sheikh, 1975) hints
at the possibility for communication between
neighboring individuals. This probably
represents the pinnacle of social organization for animals without direct connections
to each other and without brains.
679
The clonal form of Anthopleura elegantissima is clearly well suited to exposed situations in the upper mid-intertidal. Physical
factors there probably select against individuals on either end of an optimal size
range. Asexual reproduction allows continued growth for the genotype while individual size fluctuates both up and down,
presumably within an optimal range. Because of the physical rigor of the upper
mid-intertidal, there are fewer species in
competition for space and reduced predator pressure by comparison with the lower
intertidal and subtidal. This may favor
long-lived species with highly developed
competitive ability, such as the clonal
anemone.
Advantages of the solitary lifestyle
Some disadvantages of large individual
size and solitary living have been emphasized in the discussion above. Large individuals may be unable to live on exposed,
sloping surfaces because they cannot support their own weight and the weight of
contained fluids during low tides, or because they cannot endure the necessarily
increased hydrodynamic forces to which
they would be exposed in the surf (Koehl,
1976). Solitary individuals must deal individually with predators and competitors,
foregoing the advantages of clonal sociality.
What, then, are the advantages of the solitary lifestyle? For anemones living lower in
the intertidal or in the subtidal, the disadvantages of large size are reduced, and
large individuals may actually be at an advantage. By attaching to rock in lower, protected microhabitats (in cracks and pockets,
among dense stands of macroscopic algae,
or beneath several centimeters of sand),
large anemones can retract in times of stress
and extend under favorable conditions to
catch plankton and debris and to sun their
symbiotic algae (Muscatine, 1974). Larger
individuals may be able to reach over obstacles to feed, and may take food items too
large for smaller anemones to ingest (Sebens, 1977). Their solitary habit may allow
them to move away from encroaching competitors.
Large size may also offer protection from
680
LISBETH FRANCIS
predators such as the nudibranch Aeolidia (the two halves of the animal move in oppopapillosa (Rosin, 1970; Waters, 1973), the site directions and eventually tear apart),
snails Epitoneum indianorum and Opalia might well rule out this kind of asexual mulcrenimarginata or the seaspider Pycnogonum tiplication for large individuals as well.
stearnsi (Rickets et al., 1968). Sebens (1977)
finds that the predatory seastar Dermasterias Diversifying selection
imbricata prefers to feed on smaller specimens of the clonal form of Anthopleura
Jackson (1977) notes that aggregation
elegantissima; and I find that larger clonals may allow otherwise solitary forms to
can survive attacks by Aeolidia papillosa that exclude space competitors, just as colonial
are fatal to smaller specimens (unpublished forms monopolize space by asexual colony
data). Temporary reduction in size during extension. He also suggests that by virtue of
asexual division would be hazardous in the size, larger solitary animals may be at adpresence of such predators.
vantage in the face of competition or predaThe actual life history of the solitary tion. The sibling species presently known as
anemone is not yet known. However, for Anthopleura elegantissima probably diverged
the clonal form of A. elegantissima, individu- as each maximally exploited one of these
als below a certain critical size are sterile possibilities.
(Francis, 1976). Above that size, gonad volume is a function of body size (Sebens,
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