Download Interphyletic Competition Among Marine Benthos

AMER. ZOOL., 19:1029-1043(1979).
Interphyletic Competition Among Marine Benthos
S. A. WOODIN AND J. B. C.JACKSON
Department of Earth and Planetary Sciences, The Johns Hopkins University,
Baltimore, Maryland 21218
SYNOPSIS. Marine benthic environments are of two basic types: hard substrata and sediments. Organisms living in these habitats are morphologically and taxonomically diverse.
Nevertheless, they can be subdivided into a limited number of functional groups according
to the different ways they use and alter the substratum. Each functional group is polyphyletic
and includes many trophic modes. Two groups, tube builders in sediments and sheet-like
animals on hard substrata, are examined in detail. Factors most important in competition
between members of different functional groups are often not the same as for competition
between members of the same functional group. In both situations there is more evidence
for competition between distantly related taxa than between closely related forms.
INTRODUCTION
One objective in this paper is to contrast
the importance of competition between distantly related taxa and between closely related taxa living on the sea bottom. There
are two basic types of benthic marine environments: hard substrata and sediments.
The physical structure of these habitats is
very different: hard substrata are inherently two-dimensional while sediments are
three-dimensional. The organisms dwelling in these two kinds of habitats are also
very different, both functionally and taxonomically. Nevertheless, competitive processes in these environments share many
important features. Most interesting here is
the occurrence of frequent and intense
competition between ecologically similar
organisms regardless of their phylogenetic
relationship to one another. We will first
outline some of the major features of the
two environments and their more important inhabitants. Second, we will define
functional groups of these organisms on
the basis of the different ways they use and
Order of authors was determined by the toss of a
coin.
We thank G. Brenchley and L. Buss for discussion
and M. Buzas, T. Hughes, C. Slocum, C. Wahle, D.
Wethey, and H. Wilson for critically reading the manuscript. Both authors were partially supported by
grants from the National Science Foundation.
alter their environments. Third, we will
point out some of the more important features of competition between organisms in
different functional groups and between
organisms in the same functional groups.
Results show that most of our information
regarding competition between benthic organisms is for competition among very distantly related taxa.
BENTHIC ENVIRONMENTS ANDTHEIR
INHABITANTS
Hard substrata are surfaces suitable for
encrustation and growth by macroorganisms (conventionally benthos, i.e., bottomdwelling organisms, larger than 1 mm).
The grain size of hard substrata is usually
much larger than the size of the organisms
present. Hard substrata are by definition
two-dimensional. Organisms can attach to
the substratum surface but cannot burrow
except by drilling and/or dissolving part of
the substratum material (e.g., excavating
algae or sponges). Hard substrata may take
on a three-dimensional aspect by convolution or fragmentation of the substratum
surface. Three-dimensionality may result
from physical processes as in the weathering of rocky intertidal shores. However, the
most extensive three-dimensionality of
hard substrata is biogenic as evidenced by
coral reefs, oyster bars, kelp forests, worm
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S. A. WOODIN ANDJ. B. C.JACKSON
reefs, etc. (e.g., McLean, 1962; Neushul,
1971; Goreau and Goreau, 1973).
Sediments are masses of paniculate substrata whose grain size is of the same order
of magnitude or smaller than most of the
macroorganisms present. An important
consequence of the relationship between
grain size and organism size is that the readily habitable space in sediments is threedimensional. This means that sediments
can commonly serve as refuges for their
inhabitants whereas unmodified hard substrata usually cannot (Woodin, 1978a). To
escape a predator or cope with extreme
physical conditions, inhabitants of hard
substrata must respond physiologically or
behaviorally. Organisms in sediments may
respond similarly, but they have the additional advantage of protection by the sediment which is a natural buffer of extreme
physical and chemical conditions in surface
waters as well as a visual and physical retardant to pursuit by epifaunal predators
(e.g., Johnson, 1965, 1967; Jackson, 1972;
Hall and Hyatt, 1974; Woodin, 1974,
1978a; Nielsen, 1975; Reise, 1977, 1978;
Virnstein, 1977). Cracks and crevices in
hard substrata may also serve as refuges to
their inhabitants (Lewis, 1964).
In this paper we consider interactions between sessile and sedentary benthos living
in or on the substratum. Excluded are vagile (mobile) organisms such as starfishes, sea
urchins, fishes, and crabs which frequently
prey upon more sedentary benthos but may
also compete with them.
Marine animals that live in sediments
are termed infauna while animals that live
on the upper surface of sediments or on
hard substrata are termed epifauna. Infaunal animals are solitary forms like clams,
worms, and small crustaceans. Animals inhabiting intertidal hard substrata are also
predominantly solitary forms like barnacles
and mussels, but the vast majority of subtidal hard substrata are dominated by colonial animals such as corals, sponges, ectoprocts, and ascidians (Jackson, 1977a).
Many marine plants are functionally
analogous to colonial animals in that they
can propagate clonally (vegetatively) across
the substratum (Jackson, 1977a, 1979a).
Many other plants appear more analogous
to solitary animals (e.g., the "shaving brush"
Penicillus in sedimentary environments and
many laminarians on hard substrata). In
this paper we will refer primarily to animals
because those are the organisms with which
we are most familiar and for which the most
data are available for our purposes. Nonetheless we recognize that plants are commonly abundant and diverse inhabitants of
shallow water benthic environments. For
example, marine angiosperms (e.g., the
"sea grasses" Zostera and Thalassia) may
overgrow vast areas of sediments while
corallines, other crustose algae, turfs, and
erect fleshy algae may entirely overgrow
many hard substrata.
FUNCTIONAL GROUPS OF MARINE BENTHOS
Marine benthos exhibit an enormous
array of forms, sizes, anatomical systems,
and growth processes. Nevertheless, these
organisms can be readily classified into a
limited number of functional groups each
of which includes representatives of a wide
range of benthic taxa. A functional group
includes all organisms which use and affect
their environment in approximately similar
ways. (This is rather different from the concept of a guild [Root, 1967] which is defined
solely on the basis of modes of exploitation
of resources.) We define functional groups
of benthos by the ways in which they exploit
their substratum environment and the nature of their effects on the substratum.
Criteria used to define functional groups in
sediments and on hard substrata differ according to apparent differences in the ways
such organisms compete.
Sediments
Sediment-dwelling organisms can be
subdivided into functional groups according to their varying effects on the properties
of the surrounding sediment and hence the
manner in which they make the environment more or less suitable for other organisms (Woodin, 1976). These are:
1. mobile burrowing organisms whose
movements cause the sediment to be
more easily resuspended and eroded.
The feeding activities as well as the
INTERPHYLETIC COMPETITION AMONC MARINE BENTHOS
1031
movements of these organisms may de- various Polychaeta, Bivalvia, Crustacea,
stabilize the sediment. This is particu- and Echinodermata. Feeding modes of
larly true of mobile deposit feeders (e.g., mobile burrowers are predation, herbivory,
Sanders, 1958, 1960; Rhoads and omnivory, suspension feeding, surface deYoung, 1970; Rhoads, 1974), but not all posit feeding, and below surface deposit
members of this category are deposit feeding. Photosynthesis is the only nutrifeeders (Brenchley, 1978).
tional mode characteristic of sediment2. sedentary organisms whose activities dwelling organisms not represented in this
(primarily feeding) cause the sediment group.
to be more easily resuspended and
eroded (e.g., the infaunal holothurian Hard substrata
Molpadia oolitica, Rhoads and Young,
Subdivision of inhabitants of hard sub1971).
3. sedentary organisms that project both strata into functional groups is more comabove and below the sediment surface plicated than for sediment-dwelling orthereby changing the local hydrody- ganisms. For animals, the primary division
namic regime and decreasing the rate of is one of basic body plan and functional
resuspension and erosion of sediments organization, i.e., whether the animal is soli(e.g., "seagrasses," Phillips, 1960; Orth, tary or colonial. Solitary animals are distinct
1977). Below-surface portions may ac- individuals which usually are capable of
tually bind the sediment (e.g., byssus performing all individual functions. Colothreads of semi-infaunal mussels, roots nial animals are those in which members of
and rhizomes of seagrasses) and may be the colony are physically connected and have
particularly dense in stands of the sea- common ancestry through asexual reprograsses Halodule, Thalassia, and Zostera duction. Both groups include numerous
phyla and feeding modes (Jackson, 1977a).
and in Spartina patens salt marshes.
4. sedentary animals that build tubes which However, the vast majority of hard subbind the sediment together. At high stratum animals are suspension feeders.
densities the tubes form mats that apSecondary subdivisions of hard subpear to stabilize the sediments, reducing stratum animals reflect the different ways
resuspension and erosion (e.g., am- they use available space. Functional groups
phipods, Mills, 1967; phoronids, Ronan, of solitary animals are subdivided on the
1975; polychaetes and tanaids, Bren- basis of mobility and life position into:
chley, 1978).
1. sessile forms which are permanently attached to the substratum after larval set5. sedentary organisms which do not aptlement and metamorphosis. These may
pear to have a significant effect on the
form extensive mats as well as reef-like
resuspension and erosion rates of the
structures or "bioherms" (e.g., sabelsurrounding sediments.
lariid, vermetid, and oyster reefs) (SafMostsediment-dwellingorganisms can be
riel, 1966; Multer and Milliman, 1967;
easily assigned to a single functional group
Wilson, 1968,1971; Hadfield etal., 1972).
but there are some intermediate forms.
Maldanid polychaetes, for example, are 2. sedentary forms which are not permasedentary below-surface deposit-feeders
nently attached and are capable of lim(Category 2) but also build tubes (Category
ited, slow movement along the sub3 or 4) (see Rhoads, 1974). Assignment of
stratum surface (e.g., anemones, mussuch organisms to any functional group resels). These do not form reef-like strucquires knowledge of the relative rates at
tures but may form extensive mats (e.g.,
which they stabilize and destabilize sedimussel beds and clonal populations of
ments.
anemones) (Francis, 1973; Paine, 1974).
Most of the above groups include 3. excavators which burrow into the subnumerous taxa and trophic modes
stratum (e.g., burrowing bivalves,
(Woodin, 1974, 1976; Brenchley, 1978).
polychaetes). These weaken the subFor example, mobile burrowers include
stratum (MacGeachy and Stearn, 1976).
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S. A. WOODIN ANDJ. B. C.JACKSON
Each of these solitary animal functional
projections with a restricted zone of subgroups includes numerous representatives
stratum attachment. Trees obtain maxof at least three major classes in as many
imal vertical relief and shade the subphyla (Anthozoa, Polychaeta, Bivalvia, Gasstratum.
tropoda, Crustacea, Brachiopoda, Crinoid- 7. excavators which burrow into and weakea, Holothuroidea, Ascideacea). The great
en the solid substratum.
majority of sessile and excavating forms are
Most sessile colonial animals can be easily
suspension feeders although some clams placed into one of the above categories.
like Tridacna and many solitary corals pos- Intermediates between two growth forms
sess endosymbiotic plants (see Barnes, 1974). are common for runners and sheets and
Sedentary solitary animals characteristic- for sheets and mounds, but are less comally exhibit a wider range of trophic modes mon between other forms. Runners and
including suspension feeding, predation, most vines are entirely committed to a fugiand photosynthesis by endosymbionts.
tive (refuge-oriented) strategy (Stebbing,
The vast majority of colonial animals on 1973a; Buss, 1979a; Jackson, 1979a). They
hard substrata are sessile. Unlike most ses- are, in effect, mobile organisms as comsile solitary animals, however, many colo- pared to other sessile animal growth forms.
nial animals are capable of continued Assuming comparable life spans, the removement along the substratum surface maining non-excavating colonial animal
through new growth (Jackson, 1977a, growth forms represent increasing com1979a; Buss, 1979a). Functional groups of mitments (trees > plates > mounds >
colonial animals on hard substrata are de- sheets) to survival within their immediate
fined on the basis of colony morphology areas of settlement and to maintenance and
(growth form) (Jackson, 1979a). These are: defense of the integrity of colony surfaces.
Each of the above colonial animal func1. runners which are linear or branching
encrustations. This growth form maxi- tional groups except excavators includes
mizes the substratum distance cov- numerous taxa and trophic modes
ered and the variety of environments (Jackson, 1979a). At least four major classes
encountered by the animal. Runners (Demospongiae, Hydrozoa, Anthozoa, and
have little effect on the substratum or Gymnolaemata) of three major phyla
(Porifera, Cnidaria, Ectoprocta) are comother encrusting organisms.
monly
represented in these six functional
2. sheets which are two-dimensional engroups.
These taxa include suspension
crustations. Sheets may continuously
cover and bind large areas thereby feeders, predators, and photosynthesizers
stabilizing the substratum and excluding (via endosymbionts).
larvae of other encrusting organisms.
Algae on hard substrata should be readily
3. mounds which are massive, three-di- divisible into functional groups comparable
mensional encrustations with vertical to the sessile animal groups above (Jackson,
as well as lateral growth. Like sheets, 1977a, 1979a).
mounds may continuously encrust large
areas. Mounds also increase vertical relief of the substratum and thus water COMPETITION BETWEEN MEMBERS OF DIFFERENT
FUNCTIONAL GROUPS
turbulence.
4. plates which are foliose projections from
Competition between benthic organisms
restricted zones of substratum attachment. Plates shade the underlying sub- may be direct or indirect (e.g., Connell,
1976). Direct interactions require actual
stratum and increase vertical relief.
5. vines which are linear or branching contact between the organisms involved or
semi-erect forms with restricted zones of direct interference in life functions. Examsubstratum attachment. Dense vine-like ples of direct interactions include overgrowths may shade and bind the sub- growth, undercutting, aggression, immune
responses, feeding interference, etc. (Constratum.
6. trees which are erect, usually branching nell, 1961; Lang, 1973; Stebbing, I973a,b:
INTERPHYLETIC COMPETITION AMONG MARINE BENTHOS
Jackson and Buss, 1975; Hildemann et al.,
1977; Buss, 19796). Some forms of direct
interactions involve behavioral recognition
as in aggression and immune reactions between corals (Lang, 1973; Hildemann et al.,
1977). Other direct interactions may occur
without specific behavioral recognition as a
result of such processes as lateral growth.
Indirect interactions do not involve contact
or direct interference between the organisms involved. Indirect interactions may
be mediated through the substratum or the
water column. The activities of one organism or group of organisms may make
the substratum somehow less suitable (e.g.,
too fluid or unstable) for other organisms
(Rhoads, 1974), or they may alter the hydrodynamic regime and/or food supply
(Bradley and Cook, 1959).
The outcome of competition on all these
levels can often be predicted on the basis of
the functional groups of the organisms involved regardless of their taxonomic composition. Here we discuss the outcome of
competition between members of different
functional groups. In the next section we
will discuss competition between members
of one functional group per habitat, sheets
on hard substrata and tube builders in sediments.
Sediments
Functional groups of sediment-dwelling
organisms are defined on the basis of how
their utilization of the habitat alters the resuspension and erosion rates of sediments.
This in turn affects the ability of other organisms to maintain burrows or to penetrate and move through the sediments
(Woodin, 1976; Brenchley, 1978). As a result of such sediment alterations, high density assemblages in sediments are usually
dominated by members of a single functional group (Woodin, 1974, 1976; Ronan,
1975; Brenchley, 1978). Several taxa and
feeding modes may be represented, however. For example, an intertidal assemblage
of more than 40,000 tube builders per
meter square was dominated by surface
deposit-feeding tanaids (isopod-like crustaceans), herbivorous nereid and lumbriner-
1033
id polychaetes, and below surface depositfeeding maldanid polychaetes (Woodin,
1974). All are members of Category four,
tube builders which bind sediments. When
densities of such tube builders are reduced
experimentally, the abundance of burrowing forms increases (Woodin, 1974; Brenchley, 1975, 1978; Ronan, 1975). Mortality
rates ofjuvenile tube builders are greater in
sediments dominated by organisms that destabilize sediments while growth rates of
burrowing forms are depressed in sediments dominated by organisms that stabilize sediments (Brenchley, 1978).
Dense assemblages of two functional
groups may occur when their effects on the
sediment are similar and their mobilities
comparable. Tube builders and seagrasses,
for example, often co-occur and their effects on the sediment appear to be additive
(Brenchley, 1978). In contrast, burrowing
and sedentary deposit-feeders do not usually co-occur in high densities, perhaps
because the activities of the former may
interfere with the normal respiratory and
feeding activities of the latter (Levinton,
1977). In addition, sedentary deposit-feeders may hinder the movement of burrowing deposit-feeders. Persistent dense assemblages of two functional groups which
affect sediments differently or have different mobilities seem to occur only when
individuals of the two groups are very different in size (e.g., the infaunal holothurian
Molpadia with tube-building polychaetes
[Rhoads and Young, 1971]).
The vast majority of sediment-dwelling
animals are solitary and cannot reproduce
asexually. Occupation of vacant space by
these animals is therefore dependent upon
larval recruitment or immigration of adults
from neighboring populations (e.g., Woodin, 1974, 19786; McCall, 1977). Plants also
enter unoccupied space as freely dispersed
propagules but many plants can also spread
laterally by clonal growth (e.g., Phillips,
1960; Tomlinson and Vargo, 1966; Eleuterius, 1975).
The lateral boundaries of dense assemblages of sediment-dwelling organisms are
frequently quite sharp, even when they do
not occur along physical discontinuities
(Woodin, 1976). Often one cannot predict
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S. A. WOODIN ANDJ. B. C.JACKSON
which way a boundary between functional
groups will move. Such boundaries appear
to change more as a result of predation or
disturbance than from competition between the different functional groups (e.g.,
Ronan, 1975). It would seem, therefore,
that an increase in the areal dimensions of a
dense assemblage in sediments can only
occur via lateral immigration of adults or by
larval recruitment into already vacant areas.
Preemption of vacant space by dense
populations of one functional group is
common in sedimentary environments
(Woodin, 1976, 19786). Dense multispecies
assemblages dominated by a single functional group may persist for many generations. Recall that most sediment-dwelling
animals cannot reproduce asexually. Persistence of such dense assemblages requires
continued larval recruitment, perhaps favored by habitat selection, as well as resistance to encroachment by larvae and adults
of other functional groups (Woodin, 1976,
19786). For example, the previously mentioned tube-building assemblage is dominated by species that live less than two years
(Woodin, 1974), yet this assemblage has
persisted for at least ten and quite possibly
fifty years. Large macrofauna and macrophytes may often live more than ten
years. Dense macrophyte assemblages (salt
marshes, sea grass beds) may persist for
hundreds of years, largely through clonal
growth (e.g., Harper, 1977 for other rhizomatous plants). Monospecific assemblages
of animals do not appear to be so persistent.
For example, dense monospecific mats of
amphipods are often made up of approximately similar-aged individuals because
young cannot recruit into the dense mats
(e.g., Mills, 1967). The adults all die at about
the same time and the mat disappears from
the local area. Preemption of space is, of
course, a density dependent phenomenon.
Thus at low densities, individuals of one
functional group cannot exclude individuals of another group by indirect means (i.e.,
sediment alteration). At low densities burrowers are probably competitively superior
to all sedentary forms of the same size.
Hard substrata
Unlike the situation in sediments, most
evidence for competition between representatives of different functional groups
on hard substrata involves direct interactions (see Jackson 1977a, I979a,b). As a
result of such direct interactions, high density (i.e., percent cover) assemblages are
often dominated by a single functional
group. The most striking pattern is that of
dominance of colonial animals over solitary
animals on subtidal hard substrata. The distinction between solitary and colonial animals is of profound significance in terms of
their ability to compete for and retain space
(Jackson, 1977a). Solitary animals have approximately determinate growth. Thus if
adjacent space becomes available they cannot grow to occupy the new space unless
they are capable of movement or asexual
reproduction to form clones (see Francis,
1973; Paine, 1974). Substratum colonization by solitary animals is therefore dependent on sexual reproduction and larval recruitment. In contrast, most colonial animals have indeterminate growth via asexual
reproduction. Thus they can occupy newly
available adjacent space without requiring
sexual reproduction and larval recruitment. Most colonial animals are also more
successful than most solitary animals in
maintaining space by inhibition of larval
recruitment and overgrowth (fouling) by
other organisms.
Solitary animals predominate on exposed intertidal hard substrata, apparently
because colonial animals cannot tolerate
such extreme physical environmental conditions. There sedentary solitary animals
commonly "climb" over and 'smother' sessile solitary animals like cemented barnacles
(Paine, 1974). Dense populations of sedentary forms can also close over disturbancegenerated patches (sensu Levin and Paine,
1974) simply by adult immigration into the
patches wheras sessile solitary animals must
rely on new larval recruitment (Jackson,
1977a). Both groups, however, may aggregate to form dense, commonly mono-specific mats which exclude all other comparable macrofauna (e.g., mussel beds, clonal
populations of anemones, or sabellariid
reefs) (Paine, 1974; Jackson, 1977a; Woodin, 19786).
The outcome of competition between
different functional groups of colonial
INTERPHYLETIC COMPETITION AMONG MARINE BENTHOS
1035
complexity should greatly increase the importance of indirect interactions for food
and/or light which may in turn preclude
the predictable "dominance of any single
functional group. Studies of these questions are badly needed.
Preemption of space by dense populations is at least as important on hard substrata as in sediments. In the rocky intertidal of Washington State, for example,
dense beds of solitary animals (mussels,
barnacles) may persist for decades, a time
considerably longer than the average lifespan of the organisms involved (Paine,
1974). In contrast, similar assemblages in
the New England rocky intertidal are often
replaced annually (Menge, 1976). There
the entire animal assemblage may be recruited anew almost every year, yet the
assemblage is remarkably constant. Maintenance of this pattern requires either differential recruitment or differential survivorship ofjuveniles belonging to the same
functional group as the established individuals (Woodin, 19786).
Numerous experiments demonstrate
that priority effects can be very important
to the short-term maintenance of dense assemblages of colonial animals (Sutherland,
1974, 1978; Standing, 1976; Jackson,
19776; Osman, 1977; Karlson, 1978). The
basis for this stability is the considerable
resistance of most colonial animals to larval
invasion of previously occupied substrata
(Jackson, 1977a and above references).
Data for the longer-term persistence of
dense colonial animal assemblages are
mostly circumstantial and anecdotal. For
In many other environments dense pop- example, dense assemblages of sheet-like
ulations of several functional groups co- colonial animals cover most of the underoccur. For example, large areas of shallow surfaces of all sizes of plate-like corals
fore reef environments in Jamaica are oc- in Jamaica, including corals estimated
cupied by mixtures of tree-like forms, from population studies to be more than
mounds, sheets, etc. (Goreau, 1959; Kinzie, 50 to 100 years old (T. P. Hughes and
1973). The same is true in some Antarctic J. B. C. Jackson, unpublished data). This
sponge communities (Dayton et al., 1974). suggests that dominance of these cryptic
Abundance of vertically growing forms in communities by a single functional group
these environments presumably adds a (sheets) often persists for the entire lifetime
strong biogenic complexity to the environ- of the coral substratum. Dense local asment; increasing turbulence and microen- semblages of plate-like or staghorn corals in
vironmental variation in sedimentation, Jamaica have persisted much the same for
food availability, etc. (Riedl, 1971; Reiswig, the nearly twenty years they have been
1974; Geiger, 1965), but microclimatic under observation. In Australia, undismeasurements have not been made. Such turbed reef flat assemblages dominated by
animals may also be highly predictable. For
example, sheets almost always overgrow
runners (Stebbing, 1973a; Osman, 1977;
Buss, 1979a; Jackson, 1979a). Dense assemblages of colonial animals are often
dominated by members of a single functional group. Many cryptic environments
(i.e., under foliaceous corals or boulders, in
crevices, etc.) are entirely overgrown by
sheet-like sponges, ectoprocts, ascidians,
crustose algae, etc. (Jackson et al., 1971;
Gordon, 1972; Jackson, 1977a,6; Osman,
1977). Obviously some cryptic environments may not provide sufficient space for
vertical growth forms such as trees, but this
is not the case under most corals or in caves.
Not all cryptic substrata are overgrown by
sheets. The probability of dominance is
size-dependent, with smaller substrata
more frequently covered by a single functional group than are larger substrata
(Jackson, 19776; Osman, 1977). Noncryptic assemblages of colonial animals may
also be dominated by a single functional
group. In Jamaica, for example, plate-like
corals often entirely overgrow considerable
areas of the deep fore reef and the sides of
reef buttresses (Goreau, 1959; Kinzie,
1973, Fig. 25). Similarly, the tree-like
staghorn coral Acropora cervicornis forms
vast, nearly monospecific assemblages (Kinzie, 1973, Figs. 14, 15). The presumed
basis for the development of such associations is rapid growth and overgrowth
coupled with shading of underlying forms
(e.g., Lang, 1973; Porter, 1974, 1976). The
importance of shading has not yet been
demonstrated however.
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S. A. WOODIN ANDJ. B. C.JACKSON
branching corals may persist for at least ten
years (limit of observations), although
many coral colonies come and go more frequently (Connell, 1973).
A big problem in studying persistence is
how to define the life span of colonial animals. Most colonies are subject to fragmentation and/or death of portions of the colony. The result is the production of clonal
offspring whose interrelationships are usually unresolvable unless one has a complete
history of past events. Many dense assemblages of corals and other reef organisms may consist of very few clonal
populations. For example, apparently distinct plate-like colonies of Montastrea annularis {e.g., Barnes, 1973, Fig. 3) can be
shown by time series observations to fuse
naturally upon contact resulting from
growth (T. P. Hughes and J. B. C.Jackson,
unpublished data). This strongly suggests
that they are clonal relations (e.g., Hildemann et al., 1977; Potts, 1976). On fore
reef pinnacles and on the walls of reef buttresses such "compound colonies" may
reach five meters or more in maximum dimension (Goreau, 1959; Porter, 1974,
cover photograph; Jackson, unpublished
data) at maximum long-term growth rates
of one cm per year (Dustan, 1975). Thus
such Montastrea assemblages may be more
than 1000 years old. Dense populations of
plate-like Agaricia spp. and Acropora cervicornis (Kinzie, 1973, Figs. 14,15,25) may
also be largely clonal populations (J. Lang,
personal communication) of comparable
long age. Like dense growths of the bracken
fern Pteridium aquilinum (see Harper, 1977,
pp. 728-733) and other rhizomatous plants,
such dense coral populations are apparently among the most persistent local assemblages of sexually reproducing organisms. Their local persistence, however,
is almost certainly more dependent upon
clonal growth (asexual reproduction) than
larval recruitment (sexual reproduction)
(see Williams, 1975, Chapter 3, Jackson,
1977a, 1979a).
COMPETITION BETWEEN MEMBERS OF THE SAME
FUNCTIONAL GROUP
In this section we discuss aspects of com-
petition between tube building animals in
sediments and between sheet-like inhabitants of hard substrata. More is known about
modes of competition of these organisms
than for most other functional groups of
benthos. Sessile and sedentary solitary animals are obvious exceptions. We chose not
to discuss these groups in detail because
dense assemblages of solitary animals are
uncommon on hard substrata except in intertidal environments (Jackson, 1977a).
Tube-builders and sheets are also the
groups with which we are most familiar. We
recognize that in utilizing tube builders as a
model for sedimentary environments the
importance of mobility may be underestimated because most tube builders are
sedentary. Similarly, in using sheets as a
model for colonial inhabitants of hard substrata we inevitably underplay the importance of biogenic three-dimensionality
since sheets are by definition two-dimensional. Obviously it would be more
desirable to draw on information for all
functional groups if more data were available.
Tube builders
a) Direct interactions. If space is limiting
then competitive exclusion or competitive
subdivision of the resource should be observed. Tube builders often show spatial
partitioning on the sediment surface as well
as below the sediment surface. Vertical partitioning appears to be more common
among sedentary deposit feeding and
sedentary suspension feeding bivalves (Levinton, 1977; Peterson, 1977) than among
tube builders. Vertical partitioning is
known to occur, however, between maldanid polychaetes, a tube-building family
of below surface deposit feeders (Mangum,
1964). The mechanism by which this subdivision is effected is unknown. Subdivision
of the sediment surface is common among
tube builders and often results from direct
encounters. For example, spionid polychaetes pull neighboring spionids out of
their tubes (Whitlatch, 1976), nereid polychaetes react aggressively to other nereids
and may cannibalize the loser (Reish and
Alosi, 1968; Evans, 1973; Woodin, 1974;
INTERPHYLETIC COMPETITION AMONG MARINE BENTHOS
Roe, 1976), tanaids shred the tubes and
often the bodies of encroaching tanaid
neighbors (R. Highsmith, personal communication), etc. These interactions are
characteristically intrafamilial and vary in
intensity as a function of the organisms'
taxonomic relationships so that intrageneric aggression is more severe than intergeneric aggression (Reish and Alosi, 1968;
Evans, 1973). This appears to be true even
when the members of other families are
present. For example, tube-building herbivorous nereid polychaetes interact aggressively with one another but ignore
tube-building herbivorous lumbrinerid
and onuphid polychaetes (Woodin, 1974,
unpublished data). They apparently do not
recognize the others as competitors. This is
probably true of many other organisms
such as birds {e.g., Lack, 1971) and mammals {e.g., Morse, 1974). Habitat heterogeneity, disturbance, and partial predation
may also play an important role in the
maintenance of diversity and the outcome
of competition in these systems {e.g., Mangum, 1964; Hall and Hyatt, 1974; Woodin,
1977, 1978a,6; Brenchley, 1978).
b) Indirect interactions. Activities of some
tube builders may alter local physical environmental conditions and so affect the
occurrence of other tube builders. Such interactions may be both inter- and intrafamilial. For example some worms attach
macroalgae to their tube surfaces or build
tubes on which macroalgae settle and grow.
Such accumulation of algae apparently
changes the properties of the underlying
sediments such that the abundance of below surface deposit feeders is locally reduced (Woodin, 1977).
Indirect interactions for food may also
occur among tube builders but have not yet
been investigated. Organisms can partition
food resources by feeding differentially or
by feeding in different regions of the habitat. Diverse assemblages of tube-builders
usually contain a wide range of feeding
types including herbivores, omnivores,
suspension feeders, surface deposit feeders, below-surface deposit feeders, and
carnivores (Woodin, 1974; Brenchley, 1975,
1978; Ronan, 1975). Dense patches of below-surface deposit feeders may be an ex-
1037
ception. The latter, however, are known
to consume different sized food particles
(Whitlach, 1976). Moreover, co-occurring
species of below-surface deposit-feeding
maldanids live at different depths in the
sediment (Mangum, 1964), possibly to
avoid competition for food. In no case has it
been demonstrated that foodperse is a limiting resource for sediment-dwelling organisms in nature although there are suggestive data (Raymont, 1949; Mangum,
1964; Newell, 1965; Levinton et al., 1977;
Tenore, 1977).
c) Life history. Pre-emption of vacant
patches by different species of tube builders
is dependent upon how fast they can colonize the area and how well they can prevent the subsequent invasion of other
species. Tube builders can invade patches
of sediment by larval recruitment or adult
migration. Species that can reproduce
asexually and/or produce "crawl-away"
larvae should have a head start over species
dependent upon planktotrophic larval recruitment during most of the year. Growth
rates are also important to successful exclusion of later arrivals. Rapid growth hastens
simple physical preemption of space and
increases an individual's chances in aggressive interactions with smaller tube
builders (e.g., Connell, 1963; Mills, 1967;
Evans, 1973; Roe, 1976). Preemptive competition for food may also be important
(Bradley and Cooke, 1959).
Sheets
a) Direct interactions. Dense assemblages
of sheet-like organisms occupy almost all of
the substratum surface area available to
them (Gordon, 1972; Jackson, 1977a; Osman, 1977). Thus growth and increase in
the substratum area occupied by one organism necessarily results in the overgrowth and usually the mortality of some
other adjacent organism(s). Such overgrowths occur frequently on all substrata
overgrown by sheet-like organisms (Gordon, 1972; Bryan, 1973; Stebbing,
1973a,*; Jackson, 1977a; Osman, 1977;
Karlson, 1978).
An enormous number of taxa may cooccur on the same substratum. For exam-
1038
S. A. WOODIN ANDJ. B. C.JACKSON
pie, more than fifty species of sheet-like organisms comprising seven or more phyla
may co-occur under a single plate-like coral
25 to 50 cm in diameter (Jackson, 19776).
Encounters between different species may
occur in proportion to their relative abundance on the substratum (Jackson, 19796).
Similarly, encounters between different
major groups (e.g., between algae and
sponges) occur in proportion to their relative abundance. For example, at —10 m at
Rio Bueno, Jamaica, crustose algae are the
most abundant organisms on coral undersurfaces immediately adjacent to the coral
growing edge. After algae come cheilostome ectoprocts and sponges, in roughly
equal abundance. Of 216 observed encounters that involved sheet-like cheilostomes,
48 percent were with sheet-like algae, 15
percent with sheet-like sponges, and 14
percent with other sheet-like cheilostomes
(J.B.C. Jackson, unpublished data). The
great majority of these encounters involved
overgrowth. Certainly in this case, the frequency of competition among distantly related taxa (here organisms in different
phyla) is more frequent than that among
closely related forms. However, the predictability of the outcome of such interactions
may have a strong taxonomic basis (Lang,
1973; Buss and Jackson, 1979).
The nature of competitive interactions
among sheet-like organisms is extraordinarily complex (Jackson, 1979a,6). For
example, the outcome of interactions
among cheilostome ectoprocts varies with
the growth directions and surface condition
(amount of "fouling") of the colonies involved. Numerous other aspects of colony
geometry and behavior may also affect the
outcome of competition among cheilostomes (Buss, 19796; Jackson, 19796). Other
colonial groups may employ aggression
(Lang, 1973), immune responses (Hildemann et al., 1977), and perhaps allelopathy
(Bryan, 1973; Jackson and Buss, 1975) as
well as simple overgrowth. One possible
explanation for the persistence of many
species in the face of such intense competition lies in the great diversity of interactive
mechanisms possessed by these organisms
which results in the formation of complex,
non-transitive patterns of competitive abil-
ity termed competitive networks (Gilpin,
1975; Jackson and Buss, 1975; Buss and
Jackson, 1979; Jackson, 19796). Differing
modes of competition, acting simultaneously, prevent any one species from dominating the system (Lang, 1973; Porter,
1974; Jackson and Buss, 1975; Buss and
Jackson, 1979). Thus is is extremely difficult to predict the outcome of direct encounters among sheet-like organisms. Of
course habitat heterogeneity and disturbance may also play an important role in the
maintenance of local diversity in these systems {e.g., Porter, 1974; Glynn, 1976). Partial predation may be particularly important (Jackson and Palumbi, 1979).
b) Indirect interactions. There is considerable behavioral and morphological evidence for subdivision of food by sheet-like
inhabitants of hard substrata, but no one
has as yet demonstrated food limitation in
situ. One obvious division is that between
photosynthetic plants and most animals
(animals with zooxanthellae may act as
plants nutritionally, Muscatine, 1974).
Among animals, there is clear morphological and behavioral evidence for partitioning
of food type and size by major taxonomic
groups. For example, sponges suspensionfeed primarily on very small particles and
bacteria (Reiswig, 1971) whereas ectoprocts
suspension-feed on larger plankton such as
naked flagellates (Winston, 1977). Further
evidence suggestive of food partitioning
comes from zonation of major taxa with
different feeding modes along apparent
water-movement and food-availability gradients under foliaceous corals (Buss and
Jackson, unpublished data) and the depth
zonation of sponges on coral reefs (Reiswig,
1973). There is also evidence for more
subtle food partitioning within groups as
Winston (1978) has shown for 56 species of
ectoprocts (also see Cook, 1977). These animals exhibit widely varying feeding modes
and their growth form may vary considerably as a function of the quality and quantity of available food (Winston, 1976). Variations in mouth size, tentacle length, and
ciliary current patterns are probably as significant for food partitioning among ectoprocts as variations in size and shpe of the
beaks of birds (Lack, 1971). As yet, how-
INTERPHYLETIC COMPETITION AMONG MARINE BENTHOS
ever, no one has done a reasonable experiment to test for food limitation or differential feeding abilities in the field.
Another potentially important mode of
indirect interaction involves the housing by
a sessile organism of mobile animals whose
behavior may harm the host's neighbor
more than it harms the host (like ants in
acacia trees [Janzen, 1966]). For example,
isopods living on sheet-like cheilostomes
and coralline algae mediate the frequency
of alternative outcomes of interactions between these organisms (L. W. Buss, unpublished data).
Life history. Variations in larval recruitment rates and colony growth rates strongly
influence the ability of different sheet-like
organisms to preempt space not yet occupied by other organisms. Examples include the colonization of bare patches on
large substrata (Levin and Paine, 1974) and
of small, bare, discrete substrata (Jackson,
19776). In both cases species with higher
recruitment and growth rates are more
likely, at least initially, to dominate the original bare surface. Once an area of substratum is occupied by a sheet-like colonial
animal it is normally unavailable for larval
recruitment by other organisms (Goreau
and Hartman, 1966; Sutherland, 1974,
1977, 1978; Jackson, 1977a). Such space
can only be lost if the animal is disturbed
physically, eaten, or overgrown by another
previously settled organism.
DISCUSSION
We have defined functional groups of
marine benthos by the ways they exploit
their substratum environment and the nature of their effects on the substratum. Support for this approach is evident in the frequent overwhelming dominance of dense
assemblages by members of a single functional group and the generally predictable
outcome of competitive interactions between members of different groups. Biogenic three-dimensionality complicates such
predictions, largely because we are so ignorant of the nature of indirect interactions between benthic organisms. Field experimental manipulations have taught us
1039
much about the relative importance of different general processes (e.g., competition
versus predation) (Connell, 1974; Paine,
1977) but almost nothing about the mechanisms of such interactions (see Harper,
1977, Chapter 11; Jackson, 19796).
The best documented interactions between sediment-dwelling organisms are
those which involve sediment alteration.
Sediment modification is a densitydependent process, i.e., the more inhabitants of a particular functional group there
are per unit area of bottom, the greater the
destabilization or stabilization of the bottom
(Rhoads, 1974; Brenchley, 1978). It should
be emphasized, however, that sediment
modification does not merely involve alteration of physical properties of the sediment
such as effective grain size or porosity.
Rather, modifications must also involve the
meiofaunal, meiofloral, microfaunal, and
microfloral components of the sediment
{e.g., Rhoads^a/., 1977). These organisms
comprise the diets of many macrofauna
(e.g., Levinton, 1977; Tenore, 1977) and
may also serve as cues for larval settlement
(Wilson, 1955; Scheltema, 1974). Changes
in their distributions may therefore be of
considerable importance in determining
macrofaunal distributions. All this strongly
suggests that sediment-mediated interactions among macroorganisms involve far
more than merely the inability of an organism to penetrate dense tube mats or to
tolerate a particular depositional regime.
Many kinds of direct interactions have
been observed between organisms inhabiting hard substrata. The best studied are
those involving simple physical overgrowth
(Stebbing, 1973a; Paine, 1974) or undercutting (Connell, 1961) and aggression
(Lang, 1973). Aggressive ability may have a
morphological, allelopathic, or immunological basis. Overgrowth or undercutting occur through differences in growth
rates in areas of contact between organisms which may in turn be dependent upon
direct or indirect competition for food
(Buss, 19796) and/or the recent experience and condition of the participants
(Jackson, 19796). The observation that
competition for space is occurring in no way
precludes the possibility of competition for
1040
S. A. WOODIN ANDJ. B. C.JACKSON
food (Buss, 19796). This problem has been
ignored by most benthic ecologists.
Buss's observations on the influence of
isopods on the outcome of competition between sheet-like organisms suggests that
such complex relationships may exist in
other benthic assemblages. For example,
we have no idea of how important the
myriad worms, small crustaceans, and
other infauna of the the byssus mats of
mussel beds, crevices among barnacles,
algal holdfasts, etc. may be in structuring
rocky intertidal communities. Many of
these organisms are predators and/or scavengers (e.g., gastropods, nereid polychaetes)
(Dayton, 1971; Roe, 1971; Branscomb,
1976; Emson, 1977) which may feed upon
the tissues of the dominant macrofauna or
macroflora. The densities and species richness of these mobile organisms are strongly
affected by the physical structures (shape,
size, packing) of the macroorganisms (e.g.,
Suchanek, 1978). Grazers living among the
byssus threads of mussels maintain bare
zones around mussel beds (e.g., Dayton,
1971) in the same way that small mammals
maintain clearings around chaparral plants
(Bartholomew, 1970).
Although they may compete, different
species of the same functional group may
also "help" each other in competition with
species in different functional groups. For
example, sheet-like organisms on the same
substratum frequently overgrow each other.
However, each sheet also commonly prevents larval recruitment by organisms
which, were they to settle, might overgrow
all of the sheet-like organisms present. The
same kinds of collective effects are apparent
in adult-larval interactions involving other
functional groups, the joint effects of different tube-building taxa in resisting invasion by burrowers, and numerous other intergroup phenomena. Such combinations
of unfavorable and favorable effects underline the enormous complexity of interactions between members of th,e same functional group.
Both in sediments and on hard substrata,
competition between members of different
functional groups shows no obvious taxonomic patterns. Overgrowth, for example,
occurs at least as often between plants and
animals, or between members of different
phyla, as between congeneric or confamilial
species. However, the importance of indirect interactions for food between different
functional groups may vary taxonomically.
Within functional groups some taxonomic
patterns are evident. Among tube builders,
aggression is more frequent and intense between congeneric or confamilial species
than among more distantly related organisms. No taxonomic patterns are evident, however, for indirect interactions involving sediment alteration. The frequency
of overgrowths between sheets shows no
taxonomic pattern although predictability
of the outcome of such interactions may
vary taxonomically. There is also strong circumstantial evidence for taxonomic patterns in partitioning of food resources by
different sheet-like organisms. For both
sheets and tube builders, the factors thought
to be most important in competition show
no taxonomic pattern. These results are in
striking contrast to many theoretical predictions (e.g., Mac Arthur, 1972).
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