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Underwood and Chapman, 1996. Thus, small-scale studies are often at the appropriate scales, and the mechanics and logistics are usually manageable. Animals and plants may
live for extraordinarily long periods, but typically turn over in relatively few years. They therefore complete their life-cycles in the sort of time-scale that is matched by cycles of
grant-funding and scholarships for Ph.D.s. This has the serious down-side that studies have focussed on the conspicuous, abundant, slow-moving and shorter-lived components
of assemblages. This has ignored many of the long-lived plants Slocum, 1980 and the more active, small consumers e.g. Brawley, 1992, although there have been exceptions
e.g. Johnson and Mann, 1988; Duffy and Hay, 1991. It is also the case that the vast majority of studies have been focussed on species characterized by relative immobility.
The immobility has been emphasized by ignoring the potentially great distances travelled Scheltema, 1971 by the dispersive larval phases of life-history, although there
have been exceptions such as Shanks and Wright 1987, Shanks 1995, Eckman 1996 and Shkedy and Roughgarden 1997. Despite such biases, animals and plants on
rocky shores are quite suited by visibility, size, diversity, longevity, abundance and lack of emotional appeal to be subjects of experimental tests of hypotheses about ecological
patterns and processes. So, where are we now and what are we discovering from such experimentation?
2. Some conceptual issues
2.1. Trans-phyletic analyses of use of resources One area that has been extensively exploited in experimental analyses of processes
causing and maintaining ecological patterns in intertidal habitats has been the role of competition for resources of food and space reviews by Branch, 1984; Underwood,
1986a, 1992a. Two-dimensional space is a resource required by almost all intertidal species, either directly as an absolute need Andrewartha and Birch, 1954 for space on
which to settle and grow or as a relative need for space over which to feed.
As a result of the fixed because of geographical dimensions availability of the total amount of two-dimensional space available at any location and the varying and often
unpredictable nature of abundances and mixtures of species occupying the space, competition is often intense and sustained. So, as examples, competition among and
within species of limpets for food is a widespread and normal aspect of the ecology of limpets on South African shores Branch, 1981, 1984, competition for barnacles is a
well-described feature of ecology of shores in Britain Connell, 1961 and elsewhere Wethey, 1984a.
An interesting phenomenon of ecology of rocky intertidal habitats is the great and intriguing complexity of interactions among similar sorts of organisms. For example,
Kastendiek 1982 described an interesting situation where the turfing red alga, Halidrys dioica, outcompetes the alga, Pterocladia capillacea, by growing over and denying it
access to light. In the presence of the canopy-forming species, Eisenia arborea, however, the inferior competitor survives well under the canopy and is able to ‘resist’
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competition from H . dioica. Thus, competition between E. arborea and H. dioica
prevents overgrowth of P . capillacea by H. dioica.
Equally interesting and well-documented from many experimental studies is the widespread occurrence of competitive interactions between very different sorts of
organisms. Without entering the labyrinthine maze of numerous types and complex taxonomy of competitive interactions Schoener, 1983, competition on rocky shores is
of three general types. Pre-emptive competition occurs wherever occupation of space by one species prevents another species from settling from the plankton which may allow
the later arrival to find space elsewhere; Underwood and Denley, 1984. Interference competition is that involving a ‘contest’ e.g. Pielou, 1974, so that one user of space
directly harms or kills another. Examples are a faster-growing barnacle that undercuts or smothers a slower-growing species Connell, 1961 or mussels smothering other species
by growing over them Paine, 1974; Menge, 1976. Finally, there is exploitative or ‘scramble’ competition Pielou, 1974 where several species need the same space to
feed, but there is insufficient food to support all the animals needing it e.g. Underwood, 1984. Of these types, pre-emption and interference are often across phyla or between
animals and plants.
Pre-emption prevents barnacles from settling where algal fronds sweep the surfaces of the rock Dayton, 1971 and where the cover of plants prevents settlement or attachment
of larvae. Direct interference occurs where, for example, mussels encroach on the feeding territories of limpets Stimson, 1970, 1973 or overgrow and kill barnacles e.g.
Menge, 1976; Jernakoff, 1985.
Pre-emptive competition is fundamentally different from the other two types in that the outcome may not actually be any increased damage or increased risk of mortality to
the ‘loser’ members of the species arriving later. The larvae may simply go elsewhere, although it is possible that delaying settlement may lead to increased risk of predation or
accidental calamity. The hypothesis that larvae prevented from settling in one spot are more likely to die before settlement than are those not so prevented has not been tested
and will be very difficult to test in the field.
Competitive interactions between different sorts of species demonstrate the need for careful identification of the make-up of ‘guilds’ of species using similar resources Root,
1967. Taxocoenes groups of similar types of species are often considered a ‘unit’ of study in assemblages see discussion in Underwood, 1986b, but are not a relevant
grouping where resources are used by many organisms that are not taxonomically related.
2.2. Intermediate disturbance and competitive interactions One consequence of widespread, complex competitive interactions is that any other
process disturbance, disease, predation leading to reductions in densities or cover of competitors can have indirect effects on species not directly involved. For example, the
model of intermediate disturbance was proposed, historically, by Tansley and Adamson 1925; see Jackson, 1981 and, in a more recent context, by Paine and Vadas 1969 and
Connell 1978 to explain the often observed downwards concave curve of number of species across a gradient of disturbance. The model states that where disturbance is large
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or frequent or recent, only those species capable of withstanding it or colonizing and growing since the last disturbance can survive. This is only a subset of the species that
would otherwise be found in the habitat. At the other end of the gradient, where disturbances are small or rare or long ago,
superior competitors have time to build up sizes or numbers and to dominate resources. Consequently, the number of species is, again, reduced. Hypotheses derived from this
model must be tested by manipulations of the regime of disturbance. No amount of describing patterns of species richness across gradients of disturbance will help.
Two very convincing series of experiments have been done in rocky intertidal habitats to test predictions about changes and the processes causing changes in numbers of
species when disturbances are manipulated. Sousa 1979a,b, 1980 increased disturbance in a boulder-field by turning boulders over more frequently than occurred naturally. This
did lead to reductions in abundance of some species. Reducing disturbance by experimentally preventing boulders from being turned over did increase elimination of
green species by red algal species. The major conclusions were, however, that features of life-history rate of colonization, nature of cycle of breeding and responses to
disturbance were important reasons why the model of intermediate disturbance did not apply very well to explain the observed patterns of numbers of species. Responses of
long-lived red algae to being disturbed included ‘grab-and-hold’ strategies whereby vegetative growth from surviving remnants retained occupation of space by those
species. In the end, in areas that were not much disturbed or not disturbed often, the perennial red species became dominant by occupying space vacated by other species
when it became available, rather than by overgrowing and eliminating other species competitively.
McGuinness 1987a,b examined the consequences of experimentally increasing or decreasing disturbance in several boulder-fields at two heights on each of two shores.
His results found support for the model of intermediate disturbance for only some combinations of components of the fauna, under only some conditions. Intermediate
disturbance did not seem a widespread explanation for patterns of difference in numbers of species across gradients.
2.3. Keystone predation and other indirect interactions Other indirect effects have, however, been more widely demonstrated Dayton, 1971;
Lubchenco, 1978. The most widely cited is ‘keystone predation’ Paine, 1966, 1974, the situation where a predator can cause a large change in local diversity or relative
abundances of species because it consumes superior competitors in an assemblage. The best-known example is the starfish, Pisaster ochraceus, which eats mussels as a major
component of its food. The mussels are capable of smothering many, if not all, of the other users of primary space on the shore. So, the predators, by removing mussels, make
space continuously available for other species and thereby increase diversity. There have been critical evaluations of this example in terms of the evidence Fairweather and
Underwood, 1983; Underwood and Denley, 1984 and the extent to which the process is widespread e.g. Foster, 1990. It is also clear that areas with mussels generally support
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more rather than fewer species than are found where mussels are removed Lohse, 1993, because more species find habitat on and amongst mussels than on the rock itself.
Concepts of keystone predation have spread in marine ecological studies Mann and Breen, 1972; Mann, 1982; Estes and Duggins, 1995, with continuing criticism of their
validity and the lack of attention to other explanatory models for observed patterns of numbers of species Foster and Schiel, 1988; Elner and Vadas, 1990. There has also
been some uncritical adoption of the concept in areas far removed from its empirical
´ origins, such as in discussions of issues for biological conservation Soule and
Simberloff, 1986; Terborgh, 1986. Here, again, the validity of the concept, or the untested applicability of the concept to new situations has been seriously questioned
Mills et al., 1993.
Whatever the validity or applicability of keystone predation in any particular situation, there has been a renewed interest in and understanding of indirect interactions and their
importance in the ecology of complex assemblages reviewed by Menge, 1997. This was, of course, an older tradition dating back to Darwin’s ‘‘web of complex ‘interac-
tions’ ’’ Darwin, 1859. It generated some attempt at a novel theoretical synthesis of components of an organism’s environment Andrewartha and Birch, 1984. Certain
elements mates, food, predators were defined by Andrewartha and Birch 1984 to be in the core or ‘centrum’ of an animal’s environment. Other ecological components e.g.
competitors were considered to be in the ‘web’ of indirect influences on the abundance of an animal.
The most recent synthesis has been by Wootton 1993, 1994a who has demonstrated that indirect interactions fall into two main types, i.e., ‘interaction chains’ and
‘interaction modifications’. In the first case, a species A has direct effects on a second species B, which, in turn, has direct influences on a third species C. For example, a
predatory whelk A consumes barnacles B that occupy space, making it unsuitable for grazing limpets C see Dayton, 1971; Underwood et al., 1983, for examples. As a
result, consumption of barnacles by the whelks can lead to local increases in numbers of limpets because of the reduction in competition for space. Predation directly negatively
influences numbers of barnacles, but indirectly positively affects numbers of limpets.
In the second case an interaction modification, an indirectly acting species influences the direct interaction between two species. So, a predatory whelk A consumes
barnacles C, but is itself eaten by predatory crabs B see examples in Hughes and Elner, 1979; Hughes and Seed, 1995. Thus, the direct reduction of numbers of whelks
due to the activities of crabs may indirectly cause an increase in the number of barnacles.
Analyses of these interactions can require very carefully formulated hypotheses and the appropriate manipulative experiments to test them. Methods used include path
analysis Wootton, 1994b, but such approaches are saddled with all the problems of any derivative of techniques of multiple regression Petraitis et al., 1996.
Also, there can be problems with attempting to fit particular cases into a theoretical dichotomous framework. For example, Underwood 1999a demonstrated experimentally
that whelks Morula marginalba shelter under the canopy of an alga Hormosira banksii , creating reductions in densities of a prey species, the barnacle Chamaesipho
tasmanica see also related studies by Fairweather et al., 1984; Moran, 1985; Fair- weather, 1988.
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So, the alga directly increases the abundance of the whelk; the whelk directly decreases the numbers of the barnacle. Removal of the algal canopy causes local
increases in abundances of the barnacle, an indirect effect of the first type identified as an interaction chain by Wootton 1993. At the same time, however, the rate and
intensity of the direct predatory actions of the whelks i.e. reducing the numbers of barnacles are influenced by the size of the canopy, so the canopy has an indirect effect
of the second type identified by Wootton 1993. Despite potential problems with analyses and interpretations, complex chains of indirect interactions are an important
area for study, particularly because they will prove crucial for effective understanding of functional aspects of biodiversity in marine habitats.
2.4. ‘Top-down bottom-up’ regulation of assemblages A well-developed framework for understanding assemblages in some habitats is the
idea that structure of assemblages can be regulated by ‘bottom-up’ processes. In such processes, there may be quantitative or qualitative differences in the structure of
assemblages with different levels of nutrients in the system. This has been a feature of some interpretations of factors controlling structure and composition of assemblages in
freshwater habitats e.g. Hall et al., 1970; Power, 1990. The argument is that, where primary production is greater, there can be greater abundances and or greater diversity
of grazers exploiting the large primary production.
This idea contrasts with well-established notions in intertidal ecology that are interpreted as ‘top-down’ control. So, for example, predatory animals may consume
sufficient grazers in any area, thereby preventing excessive numbers in or, sometimes, eliminating species from patches of habitat. Alternatively, competitive interactions may
directly limit the numbers of all species that compete for a particular resource.
The degree to which either is the major influence on structure of an assemblage is emerging as an important issue in the analysis of complex ecological systems Fretwell,
1987; Menge, 1997; reviewed by Menge, 2000. Determining how important either type of process may be under different circumstances can be advanced by the experimental
opportunities offered by experiments on rocky shores.
There are potential managerial or conservatory issues associated with this concept. For example, where top-down processes matter, reductions in density or removal of
predators or large, competitively dominant grazers or users of space can have profound impacts on other components of the assemblage Paine and Vadas, 1969; Moreno et al.,
1984; Castilla and Duran, 1985; Castilla and Bustamante, 1989. Species that have abundances regulated by predators can explode in numbers with concomitant alterations
in density-dependent processes influencing other species. So, management for conserva- tion needs to be concerned with harvesting, fishing and any disruptive processes that
may alter relative abundances of the top-down, regulating species.
Where bottom-up processes are more important, the managerial issues must revolve around preventing alterations to productivity, in particular, to aspects of eutrophication
and other manifestations of overabundant nutrients. Menge 1992, 2000 perceptively pointed out that no ecological system is likely to be
controlled solely in one or other direction. There is also the well-known problem that primary production may, itself, regulate the number of trophic levels in an assemblage
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Hall et al., 1970; Fretwell, 1987. In such a case, the increased trophic complexity may allow for increased types of predators and increased variety, interactions and strengths of
predatory or other top-down controlling processes. Were this to be the case, it becomes philosophically unclear how top-down processes could control an assemblage, given that
the diversity of higher trophic levels, where many of the top-down controlling species are found, is itself controlled by bottom-up processes.
Nevertheless, more study is needed of the relationships between and synthesis of regulatory processes operating in opposite directions in assemblages.
2.5. Supply-side ecology Another area of intertidal investigation that has been of some influence in the
development of conceptual methods is the notion that supply of recruits into any patch of habitat is an important influence. This is, in no way, a new idea, but it was
unfashionable for a while and had to wait its turn to be ‘rediscovered’ Young, 1987; Underwood and Fairweather, 1989. The term ‘supply-side ecology’ was coined by
Lewin 1986 to summarize, in a pun, the fact that various important processes can only occur or can only take place at relevant magnitudes and rates if the species involved in
them are present in sufficient numbers.
As an example, predatory starfish or whelks cannot be involved in top-down control of the structure of an assemblage if they have not arrived in the assemblage as larvae or,
having arrived, fail to survive to sizes large enough to become dominant predators. Where there is great variation in the numbers of larvae arriving from time to time and or
place to place, there will be great variation in the duration, timing or frequency of any particular process.
Sometimes, as explained for a variety of examples by Underwood 1979 and Underwood and Denley 1984, prevailing explanations of observed patterns in intertidal
assemblages fail to include the possibility that larval supply or recruitment of juveniles could be important. So, for one example, Connell 1975 described a conceptual model
for recolonization of a disturbed patch of habitat. In relatively benign parts of the environment, predators were presumed to be able to eliminate most, if not all, of prey
species under most prevailing patterns of weather. Occasionally, however, the predators are absent e.g. whelks are missing because they were killed by an unusual period of
harsh weather; Dayton, 1971. Consequently, in those periods, prey arrive as larvae, settle and survive. If they then survive long enough to become sufficiently large, they
will escape being consumed by predators when the predators finally re-appear. This model can explain why there are intermittent ‘pulses’ of appearance of species of prey in
some intertidal habitats.
The alternative, supply-side explanation Underwood and Denley, 1984 is that predators fluctuate in abundance because of variations in their own recruitment and not
because of occasional periods of harsh weather. Regardless of the causes or amounts of such variation, numbers of prey fluctuate a lot because of the vagaries of larval
production, dispersal and survival. Occasionally, they will arrive in large numbers when numbers of predators recruiting at some earlier time happen to be small. Alternatively,
they may arrive in very large numbers, so that they ‘swamp’ their predators. Despite
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intense predation, sufficient prey survive long enough to reach sizes at which predators can no longer harm them. Under this explanatory model, it is not unusual weather events
that reduce numbers of predators. Instead, larger-than-normal recruitment of prey dictates temporal variation in the presence or in the numbers of a prey species present,
from time to time in an area.
The concept that larval variation drives abundances of adults of marine species has been widely understood in fisheries science. In fact apart from being understood with
respect to agriculture in biblical times; King James Bible, the earliest reference on the topic known to me was Hjort 1914 discussing fisheries. There have been many
observations of major variations in abundances of intertidal or shallow coastal species Coe, 1956; Loosanoff, 1964, 1966 and, more than 50 years ago, there were reviews of
the consequences e.g. Orton, 1937.
Thorson 1946, 1950 was the first marine ecologist to try to use variation in recruitment as a mechanism in models explaining temporal and spatial variations in
abundances of animals. He noted that three species of bivalves with long larval periods of planktonic development had abundances of adults that fluctuated much more than was
the case for three species living in the same habitats, but which had a short period or no pelagic development. He also commented on the consequences of the timing of
recruitment. When the larvae of a bivalve arrived before the larvae of one of their predators a starfish, they were able to survive for long enough to be too large to be
consumed by the predators when these eventually arrived. In contrast, if the bivalves recruited after the starfish, many more were consumed. So, timing of recruitment could
also influence the sizes of populations of adults.
The notion of supply-side ecology has become more important in recent developments of meta-models of patchy populations of marine invertebrates Underwood and
Fairweather, 1989. The best developments have been the models developed by Roughgarden e.g. Roughgarden et al., 1985. She developed a model for space-limited
habitats that linked the numbers of barnacles settling on the shore to the amount of free space available for settlement on that shore and to the probability of recruits surviving
from one time to another. The model was highly successful in some situations. For example, where competitors for space occupy areas that have generally poor recruitment,
the competitors will have abundances of adults regulated by processes post-recruitment. In contrast, where recruitment is generally great, sizes of populations tend to be
regulated by densities and fluctuations of recruits. These results conform well to some empirical observations see particularly Connell, 1985; Hughes, 1990; Sutherland, 1990.
The models are less successful at providing useful insights or predictive capacity for species that have variable rates of recruitment from time to time e.g. barnacles in New
South Wales discussed in Underwood and Denley, 1984; Underwood, 1999b.
Nevertheless, more recent advances have begun to demystify the vagaries of what Spight 1974 called the planktonic mystery stage see review by Eckman, 1996. As a
particular example, the consequences of variations in Roughgarden et al.’s 1985 ‘recruitment parameter’ the number of cyprids settling within a period of time per unit
area of free space that survive to the end of that period can be predicted for some species of barnacles on the coast of California. The numbers likely to be available for
settlement can be very satisfactorily predicted from a polynomial regression of numbers
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th
of recruits on sea-surface temperature to the 11 power; Shkedy and Roughgarden,
1997. The regression was associated with 59 of the variation in numbers of recruits, which is a remarkably good fit for field-derived empirical data.
So, in those systems that conform persistently to one or other end of the gradient of magnitude of recruitment, supply-side models and coupling with upwelling and other
coastal oceanographic processes can provide considerable understanding of and capacity to predict numbers of adults in intertidal populations.
3. Some methodological issues in experimental design
