Vol. 111, No.

980 The American Naturalist July-August 1977

COMPETITION ON MARINE HARD SUBSTRATA: THE ADAPTIVE

SIGNIFICANCE OF SOLITARY AND COLONIAL STRATEGIES

J. B. C. JACKSON

Department of Earth and Planetary Sciences,

Johns Hopkins University, Baltimore, Maryland 21218;
and Discovery Bay Marine Laboratory, Box 35, Discovery Bay, Jamaica

This paper will examine the comparative adaptive significanceof solitary and
colonial existence on marine hard substrata with an emphasis on features
important to interferencecompetition for space. Solitary animals are distinct
individuals which usually are capable of performingall individual functions.
Colonial animals are those in which "members of the colony must be physically
connected and ... have common ancestry through asexual reproduction"
(Boardrnan et al. 1973, pp. vi-vii). The major groups of nonvagile marine
animals which live attached to hard substrata are listed in table 1. Phyla are
subdivided so far as is necessary to include only sessile attached formsand to
separate solitary and colonial groups.
Space on which to live is oftenthe most importantlimitingresourcein marine
hard substratum environments (Connell 1961a; Dayton 1971; Paine 1974).
Solitary and colonial animals differfundamentallyin their growth patterns and
other life-historyattributes and thus in their ability to use space. I will attempt
to demonstrate the functional significanceof competitive strategies of solitary
and colonial animals for space. The results provide an ecological basis for
classification of animals as solitary or colonial, help to explain differencesin
diversity of the two functional groups, and lead to testable hypotheses about
recruitmentrates, geographic range, and palatability to predators of space-
limited organisms. I will firstdocument the general distributionof solitary and
colonial animals in Jamaican reef environments,then argue that the observed
patterns are of general occurrence, and finally analyze the attributes of these
organismswhich are responsiblefortheirdistributions.The adaptive significance
of varyingmorphological strategiesof colonial animals are considered elsewhere
(Jackson 1978).

DISTRIBUTION AND ABUNDANCE OF SOLITARY AND COLONIAL ANIMALS

ON JAMAICAN CORAL REEFS

For the past 9 yr I have been investigatingthe faunas of Jamaican coral reef
environments.The clearly space-limited systems here are (1) cryptic environ-

Aiiier.Na-tur.1977. Vol. 111, pp. 743-767.

? 1977 by The Universityof Chicago.All rightsreserved.

743

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744 THE AMERICAN NATURALIST

TABLE 1
MAJOR GROUPS OF MARINE EPIFAUNAL METAZOA
THAT ATTACH PERMANENTLY TO HARD SUBSTRATA

SKELETAL CHARACTERISTICS

+ Complete
Enclosure by
Mineralized
TAXON SOLITARY COLONIAL Type Material* Skeleton
Porifera ............. ... + Internalt CC &/or S ...
Cnidaria:
C. Hydrozoa:
0. Hydroida ...... + + External CH +
0. Milleporina .... ... + External CC
0. Stylasterina .... ... + External CC +
C. Anthozoa:
S. C. Alcyonaria..... ... + Internal CC ...
S. C. Zoantharia .... ... ... ... ... ...
0. Actiniarial .... + ? None ... ...
0. Scleractinia .... + + External CC
0. Zoanthidea .... + + None 1 ... ...
0. Antipatharia ... ... + Internal CC ...
Mollusca:
C. Gastropoda:
0. Mesogastropocla:
S. F. Cerithiacea. + ... External CC +
C. Bivalvia:
0. Filibranchia#... + ... External CC +
Annelida:
C. Polychaeta:
F. Sabellidae .... + ... External MS
F. Serpulidae ..... + ... External CC +
F. Sabellariidae ... + ... External MS
Arthropoda:
C. Crustacea:
S. C. Cirripedia:
0. Thoracia .... + ... External CC. +
Ectoprocta ........... ... + External CC or CH +
Brachiopoda:
C. Inarticulata:
0. Neotremata .... + ... External CC +
C. Articulata ....... + ... External CC +
Echinodermata:
C. Holothuroidea** . + ... Internal CC ...
C. Crinoidea:
S. 0. Isocrinida ... + ... Internal CCn..
Chordata:
S. P. Tunicata
(Urochordata):
C. Ascidiacea ..... + + Internal CC ...
* CC = calcium carbonate; S = silica: MS = mucus and sand; CH = chitin.
t Sclerospongia possess external calcareous skeletons which contain siliceous spicules.
The skeleton does not completelyenclose the sponge tissues.
I Most Actiniaria are vagile.
? Clonal species like Anthopleuraelegantis8imaare not morphologicallyconnected.
Palythoa incorporatesand grains in the cuticle.
# Attached epifaunal groups include the superfamiliesArcacea, Mytilacea, Pectinacea,
Anomiacea, and Ostreacea.
** Some suspension-feeding holothuriansdo not move but none are permanentlyattached.

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 COMPETITION ON MARINE HARD SUBSTRATA 745

TABLE 2
RELATIVE ABUNDANCE OF SOLITARY ANIMALS, COLONIAL ANIMALS, PLANTS,
AND BARE SPACE IN FOUR JAMAICAN REEF ENVIRONMENTS

COVER (0)

Solitary Colonial Bare

ENVIRONMENT DEPTH (mn) Animals Animals Plants Space

Foliaceous corals (Rio Bueno) .... 20 0.0 86.5 11.2 2.3

Reef buttresses (Rio Bueno) ..... 10 0.0 80.0 20.0 0.0
Vertical wall (Rio Bueno) ....... 15-20 0.6 70.9 26.2 2.3
Pinnacle reef (Discovery Bay) . . . 20-30 0.0 72.5 23.1 4.4

NOTE.-Data from two transects per environment of 50 points per transect and from 13
foliacious coral undersurfaces (25 random points per coral) ranging in size from 8 to 32 cm
maximum dimension.

ments, (2) vertical rock walls, and (3) open (noncryptic) surfaces in zones of
active reef constructionsuch as buttresses and pinnacle reefs. The distribution
and abundance of solitary and colonial animals in these reef environmentsare
summarized below.

CrypticEnvironments
Cryptic environmentsof coral reefs consist of the undersurfacesof foliaceous
corals, overhangs, and the walls of crevices and caves (Jackson et al. 1971). In
Jamaica, substrata in these environments are normally entirely covered by
organisms(table 2). Free space is almost nonexistent,and competitionforspace,
evidenced by overgrowths, is intense (Jackson 1977). Predators or signs of
predation and physical disturbances are rare. Algae, except corallines, are of
minorimportance.Colonial animals, especially sponges, ectoprocts,and ascidians
usually cover more than 9500 of the substratum. Solitary animals may be
numerous but occupy little space. The most common forms in these environ-
nents are serpulids, brachiopods, bivalves, and ahermatypic corals.
In 1975 I completed an experimental study of recruitmentand development
of encrusting communities onto Transite (asbestos-cement) panels placed in
artificialcrypticenvironmentsat -40 m on the Discovery Bay reef.Results are
only brieflysummarized here; a more detailed report is in preparation. Panels
were submergedforvarying periods, collected, preserved,and censured under a
microscope. Data for 12 panels collected in August 1975 are summarized in
figure1. Percentage of cover (space occupied) of solitary animals doubled be-
tween 7 and 14 mo submergencebut then decreased by 60% between 14 and 26
mo. Percentage of cover of colonial animals increased throughoutthe experiment.
Incidence of overgrowths of species by one another increased greatly over
time as freespace (bare substratum) became less and less available. Dissection
of zones of overgrowthcommonlyrevealed dead skeletal structures(e.g., worm
tubes, bivalve shells) of overgrownspecies beneath the tissues of superiorforms.
Colonial animals (especially sponges and ectoprocts) frequently overgrew
solitary animals (mostly serpulids and bivalves), but examples of the reverse

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746 THE AMERICAN NATURALIST

100 * SOLITARYANIMALS
90 o COLONIALANIMALS
80 A FREE SPACE /o
70 \.
U 60 \
0 4 26
40 _
(30 -//\
Z20 XA

7 14 26
MONTHS OF SUBMERGENCE
FIG. 1.-Relative abundance (% cover) of solitary animals, colonial animals,
and freespace (bare substratum)on panels placed in artificialcrypticenvironments
(boxes) at Discovery Bay, Jamaica. Depth -40 m; collectionAugust 1975. Data
are averaged from 250 random points per panel for four panels per period of
submergence.

interactionwere exceedingly rare. The nature of overgrowthsstronglysuggests

that the decrease in solitary animal cover between 14 and 26 mo was due to
their loss in spatial competition with encroaching colonial animals. This con-
clusiontis supported by more recent experiments in the same environment
(Jackson 1977).

Vertical Walls
Vertical rock walls are common all along the Jamaican north coast in depths
greater than -50 to -70 im and may extend upward to -10 m (Lang 1974).
The fauna of these walls is similar to that of cryptic environments.Except in
areas of sediment downpour, organisms cover nearly 100% of the substratum
(table 2), and interference competition, again evident from overgrowths,is
intense. Colonial animals and some plants occupy more than 95% of the space
on the walls. Sponges, scleractinian corals, and other cnidarians are the most
abundant colonial animals, bivalves and tube wormsthe most importantsolitary
forms.

Open Surfaces in Zones of ActiveReef Construction

On gentler slopes more typical coral reef development occurs (Goreau 1959;
Goreau and Goreau 1973; Kinzie 1973). Cover is usually extensive and com-
monly approaches 100% of the available hard substratum in zones of active
reef constructionsuch as buttresses and deep fore reef sills (table 2). Colonial

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 COMPETITION ON MARINE HARD SUBSTRATA 747

animals are the major space occupiers (Goreau 1959; Kinzie 1973; Lang 1974;
Reiswig 1973). Scleractinian corals dominate to depths of -25 to -50 in, and
sponges dominate below. Other important space occupiers include imilleporid
corals and gorgonians.
Solitary attached animals on such open reef substrata are usually incon-
spicuous. Obvious exceptions are large bivalves (Spondylus, Ostrea, Pinctada)
which may be locally abundant. Many of these epifaunal bivalves live well
above the basement substratum, on living or dead parts of corals, sponges, or
gorgonians. They reach their greatest abundance in bays and lagoons where
coral populations are reduced compared with open-coast environments.In the
moderatelyturbid waters of Discovery Bay, extensive populations of Spondylus
arnericanusand sponges cover the substratum along with corals. Spondylus may
be so abundant that on approach by a diver the bottom appears to move as
these bivalves close their heavily encrusted upper valves.
In summary, colonial animals tend to exclude solitary animals in Jamaican
reef environments where space is at a premium. This suggests that colonial
animals mightbe superiorto space competitorsin other marine hard-substratum
environments.

DISTRIBUTIONS OF SOLITARY AND COLONIAL ANIMALS

IN OTHER MARINE ENVIRONMENTS

CrypticEnvironments
Subtidal cryptic substrata throughout the world tend to be completely
overgrown by animals with colonial forms similar to those of the Jamaican
fauna predominating (Morgans 1959; Peres 1967; Sara and Vacelet 1973;
Vasseur 1964). Photographs show abundant overgrowth interactions, mostly
between colonial species as these are the most common organisms. Authors
report numerous examples of overgrowthsof solitary animals by colonial forms
but give no indication as to whetherthe colonial animals kill the solitary forms
or grow over their skeletons after they are dead. Lower intertidal cryptic
substrata also are usually covered by colonial animals, but these are of lesser
abundance higher on the shore (Lewis 1964; Morton and Miller 1968; Ricketts
and Calvin 1968; Stephenson and Stephenson 1972).

Vertical Walls
Photographs of rock walls from Palau in the Indo-Pacific show nearly com-
plete substratum coverage by colonial animals and extensive competitive
overgrowthssimilar to the Jamaican wall and cryptofaunas (Faulkner 1974).
Wall environmentsin temperate seas also tend to be completely overgrownby
organisms,with colonial animals usually the most-abundant forms(Peres 1967;
Sara and Vacelet 1973). Solitary animals, especially large bivalves, anemones,
and brachiopods, are apparently more abundant than in tropical waters, but
quantitative data are not available. Even when bivalves are present in dense

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748 THE AMERICAN NATURALIST

aggregations, however, their upper valves are heavily encrusted by a thick

carpet of colonial animals (Pequegnat 1964) just as Sp)ondy1usare covered in
Jamaica.

Open Surfaces
More nearly horizontal surfacesin the tropics are commonly covered by coral
reef associations of primarilycolonial animals except in areas of high sedimen-
tation and/or very turbid conditions (Cameron et al. 1974; Jones and Endean
1973; Stoddart and Yonge 1971). As in Jamaica, buttresses and other sites of
active reefconstructionexhibit high coral cover and intense spatial competition.
Except in very shallow depths (reef crest, algal ridge, back reef lagoons, etc.),
free-livingplants are minor space occupiers in most tropical subtidal hard-
substratum environments. In contrast, comparable temperate and boreal
substrata are commonlyovergrownby dense populations of benthic algae which
appear to displace colonial animals in these environments (Foster 1975a,
1975b; McLean 1962; Morgans 1959; Peres 1967). No quantitative data are
available, but solitary animals, especially anemones, bivalves, and barnacles
apparently occupy more space than in comparable tropical environments.
Study of such temperate-zone environmentshas lagged behind that of coral
reefs, and consequently there are not adequate data to determine whether
competition for space or disturbance is the primary process structuringthese
communities. The study of Dayton et al. (1974) on the structureand dynamics
of an Antarctic community makes clear the need for adequate informationon
this point. Colonial animals, especially sponges, are clearly the major space
occupiers. Competitive interactions do occur, but the system is structured
primarilyby disturbance.

Intertidal Substrata
In space-limited,hard-substratumsystemsforwhich there are adequate data,
the major exception to the general pattern of competitive exclusion of solitary
animals by colonial formsis found in the littoral zone of rocky intertidal shores.
Throughout the world the littoral zone of rocky shores, especially the upper
littoral, is populated primarily by solitary animals (Lewis 1964; Morton and
Miller 1968; Ricketts and Calvin 1968; Stephenson and Stephenson 1972). On
temperate and boreal coasts fleshyalgae may be the most abundant organisms
in the lower reaches of the littoral, but comparable plant populations are
uncommon in the tropics. Solitary animals may formbeds or mats (e.g., mussels,
barnacles, serpulids, and sabellarids of temperate seas, and oysters, serpulids,
and vermetids in the tropics) or they may comprise scattered populations
with abundant available empty space, as on many tropical shores sheltered
fromwave action (Foster 1974). In areas of dense populations, spatial competi-
tion may be intense (Connell 1961a; Dayton 1971; Paine 1974). Colonial
animals are almost completely restrictedto cryptic environments.

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 COMPETITION ON MARINE HARD SUBSTRATA 749

Infralittoralhard substrata in the tropics may be overgrownby dense popula-

tions of either solitary or colonial animals (Stephenson and Stephenson 1972).
On many tropical continental coasts colonial animals are uncommon, but
around islands and on the Great Barrier Reef corals, zoanthids, and alcyonaceans
are the major space occupiers, often covering nearly 100% of the substratum.
Infralittoralsubstrata on the outer ridges and back-reefflats of the same areas
are primarily overgrown by coralline algae and Sargassum. On wave-swept
temperate and boreal infralittoralshores, laminarians, other fleshyalgae, and
coralline algae cover almost all available space (Lewis 1964; Ricketts and Calvin
1968; Stephenson and Stephenson 1972). Animals are usually uncommon except
in areas where plants are less abundant. Comparable substrata on more pro-
tected coasts support a variety of generally smaller plants and a greater abun-
dance of both solitary and colonial animals. Serpulids and solitary ascidians
may formdense mats under these conditions.
In summary, space-limited hard substrata for which we have adequate data
are almost completely overgrown by colonial animals. Two major exceptions
include most rocky intertidalsubstrata, where solitary animals or plants are the
superior space competitors,and subtidal hard substrata (mostly temporal and
boreal) overgrownby dense plant populations.

WHY COLONIAL ANIMALS WIN SPACE

The ability of colonial animals to outcompete solitary animals in most

space-limited systems appears clearly related to differencesbetween basic
morphological and life-historyattributes of the two groups, in particular (1)
reproductiveand growthpatterns,and (2) the nature oftheirskeletons,suscepti-
bilityto fouling,and overgrowth.Vertical growth(escape in size) and aggregation
favor survival of certain solitary animals. Data for the following discussion,
much of which is available in Beklemishev's treatise (1969) and standard text-
books of invertebrate zoology, are summarized in tables 1 and 3. Some basic
information is lacking, but the pattern of differencesbetween solitary and
colonial groups is clear.

Reproductionand Growth
All groups reproduce sexually, and most produce planktonic larvae. Within
species, fecundityis often proportional to body or colony volume and is also a
linear function of colony area (space occupied) among colonial groups (e.g.,
Davis 1971; Hayward 1973; Sugimoto and Nakauchi 1974). Solitary animals
generallylack asexual reproduction. Colonial animals grow by asexual budding
and also asexually produce new colonies (fission,partial disintegration),free-
swimming(sexual) larvae, and restingstages (gemmules).
Solitary animals exhibit simple growth (simple increase in body size), whereas
colonial animals exhibit both simple growth of fundamental units (polyps,
zooids, stolons, etc.) and varyinglycomplex budding patterns of these units, all

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 TABLE 3

ECOLOGICAL AND LIFE HISTORY CHARACTERISTICSOF SOLITARY AND COLONIAL ATT

Method of Asexual Sexual

Invertebrate Morphology Growth Pattern Growth Reproduction Reproduction

Solitary:
Serpulidae and
Sabellariidae. Encrusting; erect; Determinate; Simple Usually absent May rapidly
or both when exponentially (transverse attain sexual
"solitary," decreases with fission of maturity (3-6 wk);
massive age Filograna) many brood eggs;
"colonies" erect also produce
and/or larvae; occasional
intertwined self-fertilization
individuals
Bivalvia ...... Encrusting; Determinate; Simple Absent Maturity at
erect usually various ages
exponentially (more often years
decreases with than months);
age most produce
larvae; fecundity
proportional to
body size
Vermetidae .... Encrusting; (? apparently Simple Absent Direct develop-
erect; or both determinate but ment or
when "solitary"; no reliable planktonic larvae
erect and/or data)
intertwined in
massive
"colonies"

Cirripedia ..... Encrusting Determinate; Simple Absent Maturity at

(cemented); exponentially various ages (1
erect (stalked) decreases with mo to >1 yr);
age produce larvae;
occasional self-
fertilization
Ascidiacea .... Encrusting; Determinate; Simple Absent Mature at various
erect exponentially ages (3 wk to
decreases with > 1 yr); produce
age larvae

Colonial:
Demospongiae . Encrusting; Determinate for Edge extension Buds and Absent in many
massive- erect massive and erect by cell prolifer- branches new intertidal indi-
forms: indeter- ation, immigration sponges; break viduals; produce
iilnate for and displacement up of encrusters larvae; fecundity
encrusters with followed by into two or more proportional to
exponential division into sponges; gem- sponge volume
increase in functional units; mules - free and area
colony area not true budding larvae or attached occupied
sponges

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 TABLE 3 (Continued)

Method of Asexual Sexual Competition

Invertebrate Morphology Growth Pattern Growth Reproduction Reproduction Mechanisms

Hydroidea .... Encrusting; Usually Linear growth Colony budding; Rapid maturity; Toxins and/or
erect; indeterminate; of stolons; regeneration fecundity pro- growth inhibito
polymorphism of exponential or budding of from small portional to overgrowth;
polyps linear growth of hydranths pieces of stolon colony area tissue invasion;
individual or coenosarc and/or no. nematocysts;
stolons; hydranths; stolons survive
exponential produce larvae or overgrowth if
growth of total medusae hydranths
stolon length and exposed
hydranths
Scleractinia Encrusting; Usually Division Colony budding Slow maturity Extracoelenteri
massive; erect indeterminate; (budding) of of new polyps; (yr); produce feeding respons
most rapid in polyps increase in no. larvae; fecundity nematocysts an
small colonies; colonies by may be toxins;
exponential death of proportional to overgrowth
increase in no. intermediate no. polyps and
polyps and colony areas colony area
area; growth
slower than most
cnidarians due to
calcification
processes
Bryozoa ...... Encrusting; Usually- Budding of zooids Budding of Very rapid Simple
erect; massive; indeterminate; zooids; brown maturity; no. overgrowth;
polymorphism of exponential bodies - regen- ovisacs and stolonal over-
zooids increase in eration of zooids fecundity growth (fronta
colony area proportional to and terminal
colony area; kenozoids);
produce larvae frontal budding
spines and rais
calcareous
margins to pre
vent overgrowt
stolons can
survive over-
growth if have
connection to
surface
Ascidiacea .... Encrusting; Complex; usually Budding (often Budding of May mature very Overgrowth;
massive; zooid determinate; or complex patterns zooids; colony rapidly (3 wk); toxins
polymorphism cyclical expan- of differentzooid fission; extrusion may alternate
sion and types) of buds - new with periods of
contraction of colonies asexual reproduc-
colony tion; no. mature
zooids and fecund-
ity proportional
to colony area;
produce larvae

SOURCES.-Bakus and Green 1974, H. Barnes 1956, 1958; Barnes and Powell 1953; R. D. Barnes 1974; Bergquist et al. 1970; Braverman 19
and Candelas 1963; Chiba and Kato 1966; Connell 1961a, 1961b, 1973; Davis 1971; Forbes 1971 Fulton 1962; Galtsoff 1964; Goodbody
Hadfield et al. 1972; Halstead 1965; Hartman and Reiswig 1973; Hayward 1973; Hayward and Harvey 1974; Hill 1967; ten Hove 1978;
1967; Lang 1973; deLaubenfels 1933, 1947, 1950, 1952; Lewis 1974; Meadows 1969: Millar 1952, 1971; Moore 1973; Multer and Milliman
1968; Reiswig 1973; Rltzler 1965a, 1956b, 1970; lRyland 1970; Safriel 1966; Sara 1970; Sarh and Vacelet 1973; Scheer 1945; Simpson
1973b; Sugihoto and Nakaucbi 1974; Wells et al. 1964; Werner 1967; Wilbur and Owen 1964; Weiss 1948; Wilson 1968, 1971.

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752 THE AMERICAN NATURALIST

of which contribute to size increase. Sponges grow by edge extension, cell

proliferation,and immigrationfollowed only later by division into semidistinct
functional units (Simpson 1968). Solitary animals display approximately
determinate growth with size increases falling off more or less exponentially
with age (e.g., Barnes 1956, 1958; Grave 1933; Millar 1952; Wilbur and Owen
1964). Some massive colonial animals (sponges, perhaps some corals) also display
approximately determinate growth (Connell 1973; Reiswig 1973), but most
encrustingforms are apparently indeterminate (e.g., Braverman 1963; Connell
1973; Davis 1971; Hayward 1973). Thus colony area tends to increase expo-
nentially with time.
Indeterminate growth by colonial animals allows them continuous lateral
substratum expansion (potentially an exponential increase in surface area
occupied) without requiring intervening stages of sexual reproduction and
recruitment.This is especially important when bare spaces (patches [Levin and
Paine 1974]) occur in an environmentdue to predation, physical disturbance, or
the sloughing off of large, heavy organisms (Dayton 1971; Goodbody 1963;
McDougall 1943). Patches provide bare substratum for colonization by other
organisms regardless of their ability to compete directly for space. However,
patches formed within areas overgrown by colonial animals often have a very
differenthistoryfrompatches within areas overgrownby solitary animals. This
is because colonial animals with indeterminate growth can immediately begin
to spread out over previously occupied territory.The closing rate of a patch
depends on the growth rate of the surroundingcolonial animals. For example,
in a shallow-water sponge communityin Jamaica, bared areas less than about
200 cm2 were rapidly overgrownby adjacent sponges (Goodbody 1965). Larger
bare areas were rare in this community.This rapid closing of patches along with
possible secretion of toxic substances by the sponges (Goodbody 1961) pre-
vented colonization of the sponge communityby other organisms. In contrast,
larger patches, or those formedamong slower-growingcolonial animals such as
seleractinian corals, provide space for sufficientperiods for settlement and
growth to maturity by competitively inferior species (Porter 1972, 1974).
Eventually, these patches are also closed by surrounding colonial animals.
Relative abundance and temporal occurrence of inferiorcompetitors, solitary
or colonial, is thereforedetermined by the frequency distribution of different-
sized patches and the growth rates of the surrounding organisms (Levin and
Paine 1974).
Patch formation may be particularly destructive to associations overgrown
by solitary animals because these cannot normally replace their losses without
sexual reproduction and recruitment. Thus, patches cleared among subtidal
populations of solitary ascidians, bivalves, or barnacles may be overgrown by
previously existing or newly recruited colonial animals before the solitary
animals are able to rerecruit.One exception actually supports the generalization
of the superiorityof colonial animals in closing over patches. Patches formed
among intertidalbeds of Mytilus californianusmay be closed offby immigration
into the patches by adult mussels which smother newly settled organisms
(Robert Paine, personal communication). Intertidal barnacles cannot close
patches in this manner. Thus the ability of Mytilus to close patches without

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 COMPETITION ON MARINE HARD SUBSTRATA 753

interveningrecruitmentgives them a competitive advantage over barnacles

similar to that of colonial over solitary animals in subtidal environments.

and Susceptibilityto "Fouling"

Skeletons,Overgrowth,
Colonial animals (except ectoprocts) generally lack completely enclosing
exoskeletons,whereas most permanentlyattached solitaryanimals possess hard,
mineralized exoskeletons which make them particularlysusceptible to epifaunal
colonization ("fouling") by all other hard-substrate organisms (table 1). In
Dayton's (1971) terminology their shells provide secondary free space. Thus
colonial animals are able to settle on solitary animals, grow over their shells,
and in the process frequentlyocclude their apertures. For example, in cryptic
reefenvironments,encrustingsponges and cheilostomous ectoprocts commonly
overgrow,and may even preferentiallysettle upon, the tubes of serpulids and
bivalves. Serpulids near the thinnerperipheryof sponges are usually still alive,
but worms near the thickercentersof colonies are usually completelyovergrown
(Jackson, unpublished data). Even if the solitary animals survive, their
susceptibilityto overgrowthincreases the substratumsurfacearea, and thus the
potential biomass and reproductive output of colonial animals is enhanced. Of
course, solitary animals commonly settle on preexisting solitary animals, but
the latter are still liable to overgrowthby colonial species.
Colonial animals are much less fouled. Colonial animal defenses against
epizoic settlementby larvae upon themselves include tentacles and nematocysts
of cnidarians (Barnes 1974); avicularia of ectoprocts (Ryland 1970); and wide-
spread toxicity of sponges, cnidarians, and ascidians (Bakus and Green 1974;
Burkholder 1973; Chiba and Kato 1966; Goodbody 1961; Halstead 1965;
deLaubenfels 1933; Sara and Vacelet 1973). These defenses are not totally
effective.Solitary animals can settle on and overgrowmany hydroids,ectoprocts,
and (less commonly) sponges (Gordon 1972; Meadows 1969; Stebbing 1971a)
and on dead spots (exposed skeletons) of corals and gorgonians (Forbes 1971)
but usually cannot overgrow their hosts. Among hydroids and ectoprocts,
settlementis largely on exoskeletal surfaces between polyps or zooids.

Defense Mechanisms of Solitary Animals

Some solitary animals survive spatial competition with colonial animals by
escape in size or by aggregative settlement. Colonial animals may exhibit
similar generalized defenses, or may possess highly specificcompetitive mech-
anisms (e.g., allelochemicals [Jackson and Buss 1975], aggressive behaviors
[Lang 1973]) which allow them to capture space from other, usually colonial,
animals. The importance of these differentcolonial strategies is considered
elsewhere (Jackson, in press).
Escape in size. Solitary animals with calcareous exoskeletons or tunics are
not harmfullyaffectedby overgrowthunless theirfeedingapertures are blocked
off(Gordon 1972; Jackson, unpublished data; Stebbing 1973a; Wilson 1968).
The large size and initiallyrapid growthof many bivalves and solitary ascidians
raise their feedingapertures well above the substratum and lessen the chances

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754 THE AMERICAN NATURALIST

of complete overgrowthby encrustingcolonial forms.Although usually smaller,

some serpulid, sabellariid, and vermetid species living in environments over-
grown by encrusting colonial animals are able to survive by changing their
pattern of growthfromadherence to the substratum to an erect habit (Hadfield
et al. 1972; Jackson, unpublished data; Stebbing 1973a; Wilson 1968). Over-
growth of basal parts of the shell, tube, or tunic does not harm these solitary
animals, just as many stolonate hydroids, ectoprocts, and hemichordates
survive stolonal overgrowthso long as theirzooids or polyps are elevated above
the substrate (Stebbing 1973a).
These examples demonstrate that escape in size can be of direct advantage in
spatial competition as well as providing refuge from predation (Dayton 1971;
Paine 1965). In examination of such processes, however, the scale of the en-
vironmentand the attached organisms must be clearly defined. This is readily
apparent for the three space-limited Jamaican reef systems previously de-
scribed. In cryptic environments, large foliaceous corals very rarely exceed
2 m in maximum dimension and commonly range from a few to 50 cm. The
colonial animals which cover most of these coral undersurfacesare usually less
than 1 cm thick, and many competitive dominants are less than 1 or 2 mm in
thickness. Thus solitary animals can often escape complete overgrowth by
raising their apertures only a few millimetersaway fromthe plane of the coral
substratum. The system is essentially two-dimensional. Continuous hard
substratum on rock walls suitable for habitation by attached animals may
extend for 10 m or more. Colonial animals covering such walls are often 10 cm
or more thick,and solitary animals must grow correspondinglygreaterdistances
fromthe substrate to avoid overgrowth.Finally, on gentlerslopes with typical
coral-reefdevelopment, corals, sponges, and gorgonians form extensive three-
dimensional structures which often rise 1 m or more above the substratum.
Except forspecialized epizoans, only very large solitary animals like Spondylus
and Tridacna can survive encroachment by colonial animals.
Aggregation. Dense aggregations of tube-dwelling polychaetes are less
susceptible to overgrowththan isolated individuals of the same species. Asexual
reproduction (ten Hove 1977) and/or synchronous aggregated settlement of
larvae may produce dense monospecific stands (Wilson 1968). Preferential
settlementon live or dead adults ofthe same species perpetuates the aggregations
(Wilson 1968). The tightlypacked tubes of sabellariids, serpulids, and vermetids
grow so as to present an outer "colony" surface consisting almost entirely of
feedingapertures (Hadfied et al. 1972; Multer and Milliman 1967; Safriel 1966;
Wilson 1968, 1971). Feeding activities of such dense populations reduce the
probability of successful settlement by larvae of other species and inhibit
overgrowthby adjacent plants and animals. Expanding "colonies" may over-
grow previously established populations of other organisms (Wilson 1971).

THE ROLE OF DISTURBANCE

Physical disturbance and biological disturbance (predation) often prevent

monopolization of substrata by colonial animals.

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 COMPETITION ON MARINE HARD SUBSTRATA 755

Physical Factors

Physiological stress.-The absence of most groups of colonial animals from

exposed, rocky intertidal substrata (scleractinian corals, milleporids, and
zoanthids in the lower intertidal of many reef flats are exceptions [Milliman
1973]) is probably a result of intolerance to high temperature and desiccation.
Colonial animals usually lack completely enclosing exoskeletons and/or water-
trapping mechanisms (table 1) which provide protection from desiccation for
solitary animals and algae. Luxuriant growthsof littoral algae may be protected
by collapse and consequent trapping of water duringlow tides. Such growthsare
common on exposed outer coasts, but are often absent in more wave-protected
areas where desiccation stress is more severe (Dayton 1971). Water trapping is
apparently sufficientto prevent desiccation of infralittoralalgae under a wider
range ofwave-exposure conditions (Lewis 1964). Solitary animals with calcareous
exoskeletons (bivalves, barnacles, tubicolous polychaetes, and vermetids) show
wider distribution patterns across desiccation gradients (Dayton 1971) and
dominate exposed littoral substrata throughout the world. Solitary animals
lacking such protection (solitary ascidians) are generally limited to the lower-
most intertidal and deeper substrata. The occurrence of actinians in littoral
environmentsis not contradictoryas these anemones may exhibit considerable
vagility and behavior to protect themselves from desiccation (Ottaway 1973).
Sediments.-Excessive sedimentation may inhibit the activities of colonial
animals (Fulton 1962; Goreau and Goreau 1973; Lang 1974; Reiswig 1973;
Round et al. 1961) but may also limit solitary suspension feeders (Jorgensen
1966). Moving sands commonly cover and kill large areas of zoanthids and
corals in shallow back-reef environmentsat Discovery Bay. Sediment scour at
the borders of rocks with sediments may limit colonization by all kinds of
organisms but seems physically most destructive to colonial animals (Forster
1954, 1955, 1958; Kinzie 1973; Morgans 1959). For example, low intertidal
gulley walls and the undersurfaces of overhanging ledges in New Zealand are
dominated by colonial animals except in regions of excessive sand scour where
mussels and serpulids predominate (Morton and Miller 1968). The calcareous
exoskeletons of these animals presumably help to protect them fromsediment
abrasion.
Substratumstabilityand energyconditions.-Ustable substrata do not support
most colonial animals except for occasional small encrusting forms (Riitzler
1965a; Morton and Miller 1968). The stability of small, hard substrata (shells,
stones) depends on environmental energy conditions (waves, currents) which
may shift,overturn,or bury the substrata under sediments. Such substrata are
primarilycolonized by solitary animals, which may in turnprovide the necessary
stabilization for survival by colonial animals. For example, along North
Carolina small stones and shells in quiet coastal waters are usually dominated
by sponges (Wells et al. 1964). In contrast,shells lyingon continentalshelfsands
(more exposed to waves and currents) are dominated by solitary animals,
especially barnacles (Wells and Wells 1964). Shells of living snails or those
occupied by hermitcrabs are dominated by colonial animals (sponges,bryozoans,

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756 THE AMERICAN NATURALIST

hydroids) throughout a wide range of energy conditions (Gordon 1972; Rees

1967). Presumably the activities of the hosts decrease physical disturbance to
the shell surfaces.
Why have not most colonial animal groups become adapted to live in inter-
tidal and many other physically high-stress environments? Survival under
such extreme conditions would require evolution of well-developed external
skeletons or other protective mechanisms. Zoanthids in the tropics are the only
colonial group which occupies extensive space on exposed intertidal substrata
but does not possess an external skeleton. Even among zoanthids, the genus
Pal ythoa,which is most tolerant to exposure, incorporates sand grains into the
cuticle (Judith Lang, personal communication). Many colonial groups (most
classes of sponges, many cnidarians, ascidians, etc.) apparently cannot produce
completely enclosing external skeletons without fundamental morphological
reorganization. Even for groups which do produce such structures, their
development must require significantenergyexpenditure. Thus it is no accident
that colonial animals possessing massive skeletons (scleractinian corals) possess
zooxanthellae which aid in calcification (Goreau and Goreau 1959; Muscatine
1973) or that colonial animals with completely enclosing exoskeletons, such as
hydroids and ectoprocts, are small. For any species, the energy drain for
skeletal production must decrease its growth rate and thus its ability to occupy
space. Among corals, for example, branchingformssuch as Acropora cervicornis
extend faster than more massive forms of Diploria and Montastrea (Glynn
1973).
The intertidal zone is a peripheral environmentwhich contains a very small
percentage of the world's marine hard substrata. Presumably there is a trade-off
between the advantage to a species in occupying peripheral, more stressful
environments and maintenance of superior competitive ability for space in
physically less stressfulsubtidal environments.For many solitary animals, in-
tertidal substrata provide an important refugefrom competition with superior
space competitors.In contrast,most colonial animals possess competitivemech-
anisms favoringtheir survival in physically low-stressenvironments,and there
can be little selective basis for evolution of costly mechanisms favoringsurvival
in physically more disturbed areas.

Predation
Predation may act to make space available on substrata which might other-
wise be covered by competitively dominant organisms (e.g., Paine 1974).
Starfishand crabs may prevent coverage of some intertidalsubstrata by mussels
(Ebling et al. 1964; Kitching et al. 1959; Paine 1966, 1971, 1974), barnacles
(Dayton 1971), or algae (Safriel 1966). It has been hypothesized that the
starfishAcanthastercan prevent dominance of Indo-Pacific and Eastern Pacific
coral reefsby faster-growingand/ormore aggressive coral species (Goreau et al.
1972; Porter 1972, 1974). Grazing sea urchins and fish apparently prevent
coverage of intertidal and subtidal substrata by competitivelydominant plants

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 COMPETITION ON MARINE HARD SUBSTRATA 757

(Earle 1972; Mann and Breen 1972; Ogden et al. 1973; Paine and Vadas 19,69;
Randall 1965; Stephenson and Searles 1960; Vine 1974) or encrustinganimals
(Karlson 1975).
The calcareous exoskeletons of most solitary animals appear to provide their
greatest protection from predation. Lacking such skeletal protection, many
solitary ascidians and colonial animals are toxic to potential predators
(Burkholder 1973; Bakus and Green 1974; Russell 1966). Nematocysts, spicules,
touch fibers, and other skeletal elements also provide protection. Predation
events are fatal to most solitary animals but are often limited to portions of
colonial animals and may not be fatal to the entire colony (Dayton et al. 1974;
Glynn et al. 1972; Randall and Hartman 1968; Reiswig 1973; Ryland 1970;
Wyer and King 1973). Survival of portions of colonies capable of regeneration
and furtherasexual proliferationprovides the potential for rapid recovery of
colonial animal populations after episodes of intense predation.

THE ROLE OF PLANTS

Many benthic plants and colonial animals share a variety of characteristics

important in spatial competition, in particular, asexual reproduction, in-
determinate growth, and the employment of allelochemicals. In environments
with adequate light, plants have the furtheradvantage of photosynthetically
derived energy for growth and reproduction, although many animals, such as
corals and the giant clam Tridacna, also derive energy fromphotosynthesisvia
their symbiotic zooxanthellae.
Where conditions are favorable, dense growths of benthic macrophytes such
as kelps cover large areas fromwhich they may exclude many colonial animals
(Foster 1975b). There dense growths of colonial animals are usually limited to
crevices and other cryptic (dark) environments. Contacts between colonial
animals and plants are often abrupt, and macrophytes might penetrate deeper
on open substrates or fartherinto caves were it not for competition by faster-
growing (for those light conditions) colonial animals. Abundance of solitary
animals among kelps suggests that dense growths of these plants may diminish
the competitive superiorityof colonial over solitary animals. This may be due to
direct plant-mediated physical disturbance (whipping action of blades), over-
growth, or increased heterogeneityof the environment (Candelas and Candelas
1963; Lewis 1964; Paine 1971; Rutzler 1965b).
The development of extensive coral growths in many shallow tropical en-
vironmentsmay be dependent on the near elimination of macrophytic algae by
sea urchin and fish grazing (Walter Adey, Jane Menge, and Paul Sammarco,
personal communications). Experiments by Sammarco (1975) have shown that
in the absence of grazing algae overgrow and kill most coral species. In the
absence of such predation macrophytes might exclude or greatly diminish coral
populations just as they apparently reduce colonial animal populations in
temperate seas.

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758 THE AMERICAN NATURALIST

DISCUSSION

I have argued that solitary and colonial animals differfundamentallyin their

growth patterns and other life-historyparameters and thus in their ability to
use space. Here I suggest that understanding of the ecological significance of
solitary and colonial strategies (1) obviates the need for classificationof certain
"problem" groups such as sponges as solitary or colonial, (2) provides an ex-
planation forthe greater diversityof colonial animals, and (3) allows a number
of predictions of general ecological interest.

Conceptsof Coloniality
In treatmentsof the evolution of coloniality there has been much discussion
regarding the definitionof coloniality and the categorization of certain groups
as either solitary or colonial (e.g., Beklemishev 1969; Boardman et al. 1973).
Problems arise with the concept of what are "members" of a colony, especially
withthe sponges (Hartman and Reiswig 1973; Simpson 1973). The morphological
basis of this confusion is evident in the absence of readily identifiable "in-
dividuals" within sponge "colonies" and the organized pumping behavior of
many sponges, especially large erect forms with single large atrial chambers
such as many Verongia (Reiswig 1971). Sponges like Verongia behave ecolog-
ically much like solitary animals, exhibiting approximately determinategrowth
(Reiswig 1973) which limits their ability to occupy bare substratum without
sexual reproduction and recruitment.Most sponges, however, lack well-defined
organization around one or even a few atrial chambers. Especially among
encrustingformsand massive branching sponges such as Agelas, their ability to
expand over available substratum without sexual reproduction and the ability
of differentmasses of tissue of an "individual" sponge to survive and function
separate from one another after death of intermediate tissues (as with sclerac-
tinian coral and ectoproct colonies) makes these sponges ecologically equivalent
to typically colonial groups.

Diversity
Because they are physiologically excluded from exposed intertidal habitats,
the variety of physical environments potentially available to most colonial
animals is less than that available to many solitary forms. In spite of this
environmental limitation, hard-substratum colonial animals exhibit greater
diversity than do attached solitary animals. For example, from the Bay of
Fundy to Cape Hatteras colonial animal species which live permanentlyattached
to benthic hard substrata outnumber similarly attached species of solitary
animals by a ratio of about 3:1 (Gosner 1971). Comparable data are unavailable
fortropical regions,but survey of a variety of environmentsin Jamaica suggests
that ratios are even higher.
The greaterdiversityof colonial animals appears clearlyrelated to adaptations
for spatial competition. Specific competition mechanisms (e.g., allelopathy)
provide for the existence of competitive networks (A beats B beats C but C

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 COMPETITION ON MARINE HARD SUBSTRATA 759

beats A) rather than simple competitive hierarchies (A beats B beats C

and A beats C) (Gilpin 1975; Jackson and Buss 1975). For example, the cryptic
coral reef community in Jamaica contains some 300-500 encrusting animal
species, of which the vast majority are colonial. This system is characterized by
an abundance of highly complex competitive networks (Buss and Jackson,
in press). Species which form networks (break hierarchical sequences) are
colonial animals or plants (coralline algae), many of which exhibit specific
allelochemical effects(Buss 1976; Jackson and Buss 1975). To date we have not
observed networkformationby solitary animals. Position effects(which species
settles or grows next to which other species), preferential settlement, and
finely-tunedsubdivision of environments(zonation) also contributeto increase
in diversityof colonial animals exhibiting competition strategies.
In contrast, most solitary animals are poor space competitors, generally
lacking specificcompetitionmechanisms,and are more dependent on disturbance
processes to provide suitable environmentsfor settlement and growth. Small
size, rapid growth, and short generation times of most solitary animals favor
such a generalist (fugitiveor opportunistic) strategy. Numerous small colonial
animals, including many hydroids, ectoprocts, and ascidians, exhibit similar
strategies (Jackson 1978). Generalists must use whatever substrata are avail-
able, and there can be little basis for selection favoring subdivision of en-
vironments. Studies in progress of Jamaican cryptic environments support
this conclusion. Many solitary species (especially bivalves and serpulids) occur
throughouta wide range of crypticenvironments,whereas most colonial species,
especially the best space competitors,are more limited in the range of depths
and substrates occupied (Jackson, unpublished data).

Predictions
Recognition of the generalist-specialistand early-late "successional" roles of
most solitary and colonial animals in potentially space-limited systems allows a
number of predictions relevant to current ecological theory. For example, (1)
recruitmentrates should be higherforsolitary than colonial animals (MacArthur
1972; MacArthur and Wilson 1967; but see Wilbur et al. 1974); (2) high recruit-
ment rates and broad environmental distributions of most solitary animals
should provide the basis for wider geographic distributions of these animals
compared with competitively superior colonial animals just as habitat dis-
tributioninfluencesgeographic distributionof marine infaunal bivalves (Jackson
1974); and (3) within any "successional" framework,early colonizers (solitary
animals) should be more palatable to predators than later arrivals (colonial
animals) (Margalef 1958; Cates and Orians 1975). Taxonomic problems preclude
analysis of geographic distributionsat this time.
Recruitmentrates-.Dependence on disturbance processes to provide suitable
environmentsshould require production of large numbers of potential recruits.
In contrast, superior space competitors presumably enjoy a higher survival of
recruitsbut must devote a largerpercentage of their energytoward maintenance
of the specific mechanisms which favor their competitive position than to

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760 THE AMERICAN NATURALIST

reproduction.Preliminary analyses of experimental data fromartificialcryptic

environmentsin Jamaica (same panels as forfig. 1) demonstrate such a pattern
(Jackson, unpublished data). Serpulids are the most abundant (both numbers of
individuals and space occupied) early colonizers but the worst space competitors,
whereas sponges dominate the older substrates and are the best space com-
petitors After 7 mo of submergence, serpulid recruitment exceeds sponge
recruitmentby a ratio of 12:1. Live serpulids (total tube area) also occupy more
space than live sponges, but the ratio is only 3:1. The lower ratio results from
the larger area occupied by individual sponge colonies compared with serpulids.
After 14 mo of submergence,serpulid recruitmentstill exceeds sponge recruit-
ment by a ratio of 8:1, but live serpulids then occupy slightly less space than
live sponges (ratio approximately 1:1). Clearly, sponges gain more space by
lateral expansion of the few colonies that recruit rather than by increased
settlement later in the successional sequence. Such lower reproductive output
of superior space competitors is apparently related to the energy required for
continuous growth and specialized competition mechanisms such as production
of allelochemicals.
Palatability to predators.-As noted above, signs of predation (scrape marks,
drill holes, bare zooids, etc.) are rare in natural cryptic environments,and the
same is true on panels in artificial cryptic environmentswhich are also pre-
dominantly covered by colonial animals. Panels submerged for only 7-14 mo,
however, reveal numerous bivalves (mostly Echinochama, Dimya, and Spondy-
lus) killed by drilling gastropods. On many panels more than 500% of the
bivalves had been drilled. Serpulids are not drilled, but often a similarlylarge
percentage of tubes, not overgrown at the aperture, lacks living worms. These
patterns were repeated in more recent experiments (Jackson 1977). As in many
plant communities(Cates and Orians 1975), predation appears most devastating
to early successional components of cryptic reef communities. For such orga-
nisms fated to be soon overgrown by superior space competitors there can be
little selective basis for evolution of specificantipredatorymechanisms.

SUMMARY

Most solitary and colonial animals inhabiting marine hard substrata differ
fundamentallyin their ability to use space. Colonial animals are superior space
competitors because (1) indeterminate growth allows continuous lateral sub-
stratum occupation without requiringinterveningstages of sexual reproduction
and recruitment,and (2) they are less susceptible to "fouling" and overgrowth.
Solitary animals survive in the seas because (1) various morphological and
behavioral attributes (escape in size, aggregative behavior) protect them in
spatial competition with colonial animals or because (2) predation, physical
disturbance, or competition with plants prevents monopolization of substrata
by colonial animals. Focus on ecological strategies circumvents arguments
regarding the solitary or colonial identity of problematical groups such as
sponges. The evolution of specificcompetition mechanisms by colonial animals
has provided the basis forcompetitivenetworkswhich have furtherfavored the

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 COMPETITION ON MARINE HARD SUBSTRATA 761

evolution of higher diversity within colonial rather than solitary groups.

Recognition of the generalist-specialist and early-late "successional" roles of
most solitary versus colonial animals leads to predictionsthat solitary animals
should recruit more heavily and be more palatable to predators than are
colonial animals. Preliminary evidence supports these predictions.
NOTE ADDED IN PROOF.-Results of Osman's (1977) excellent experimental
study of fouling organisms near Woods Hole, Massachusetts, unfortunately
appeared too late for inclusion here. His observations on competitive inter-
actions among solitary and colonial animals are in substantial agreement with
the conclusions of this paper.

ACKNOWLEDGMENTS

B. D. Keller has dived with me almost fromthe beginningof my crypticreef

studies; his support has been essential to development of this research. L. W.
Buss helped gather data for table 2. He and B. A. Menge generously gave
detailed criticismsof most stages of the manuscript. R. Karlson, R. A. Kinzie,
N. Knowlton, J. Lang, J. L. Menge, K. Rylaarsdam, S. M. Stanley, G. J.
Vermeij, S. A. Woodin, and four reviewers provided many useful suggestions.
Much of this work was supported by NSF grants GA-35443 and DES 72-01559.
To all I am grateful.

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