The Structure and Replenishment of Rocky Shore Intertidal Communities and Biogeographic Comparisons

The structure and replenishment of rocky
shore intertidal communities and

biogeographic comparisons
David R. Schiel
*
Marine Ecology Research Group, School of Biological Sciences, University of Canterbury,
Private Bag 4800, Christchurch, New Zealand
Received 19 December 2003; received in revised form 29 December 2003; accepted 3 January 2004
Abstract
Marine scientists have made many recent advances in understanding the connections between the
structure of benthic communities, replenishment of populations through dispersal processes, and
interactions with the nearshore water mass. In this review, some of the themes and models relating to
these processes and interactions are discussed. Benthicpelagic coupling models are in the early
stages of development, but encompass oceanic processes such as upwelling and downwelling, the
transport of larvae and their arrival back to shore to settle. Most current knowledge of these processes
is based on a few taxa, especially barnacles and mussels. This is discussed with reference and
comparison to macroalgae, which dominate much of the intertidal zone on temperate rocky shores,
and have quite different life histories, transport and settlement processes. The role of key, habitat-
dominating species is discussed, particularly their early life histories, with reference to the
differences in community composition, nearshore dynamics and settlement processes in different
countries. Finally, some suggestions are made for future work to fill gaps in understanding about
rocky shore communities.
D 2004 Elsevier B.V. All rights reserved.
Keywords: Rocky intertidal; Benthic communities; Benthicpelagic coupling; Upwelling; Early life history
1. Preamble
Almost 18 years ago, two Australian ecologists asked in the title of a paper, do intertidal
communities have different ecologies or different ecologists? (Underwood and Fair-
0022-0981/$ - see front matter D 2004 Elsevier B.V. All rights reserved.
doi:10.1016/j.jembe.2004.01.001
* Tel.: +64-3-364-2031; fax: +64-3-364-2590.
E-mail address: [email protected] (D.R. Schiel).
www.elsevier.com/locate/jembe
Journal of Experimental Marine Biology and Ecology
300 (2004) 309342
weather, 1986). They referred specifically to studies on species that were common in
different countries but which had different trophic relationships. They also questioned how
advances in understanding of marine ecosystems could be made if different methodologies
and philosophies were applied in different places.
With increasing frequency in recent years, ecologists have explored the relationships
between localised and broader-scale processes within and among coastlines of different
countries in a search to understand not only local variation but also global processes (e.g.,
Jenkins et al., 2001; Menge and Branch, 2001). Inevitably, these studies involve a wide
range of differences in biological, chemical and physical variables, including community
composition, life histories of different taxa, trophic dynamics, coastal physics and nutrient
inputs. We know a great deal about each of these individually, but more so in some
ecosystems than in others. The interrelationship between these variables is less well
known. Furthermore, there may be biases in perception that are only slowly being
corrected, driven at least partially by the highly productive and influential literature from
US scientists which, at least until recently, has tended to cite mostly north American
studies (Wardle, 1995). As the realisation of global problems and an awareness of the need
for more scientific information and access to it to help solve them increase (Annan, 2003;
Lubchenco and Iwata, 2003), it is timely to re-visit the question posed by Underwood and
Fairweather (1986).
The history of marine ecological research is rich, extensive and varied, and there have
been numerous recent, thoughtful reviews of most topical issues. These include special
features in Ecology discussing the underlying philosophy of scientific progress in ecology
(Graham et al., 2002, et seq. [6 reviews]), long-range dispersal (Kinlan and Gaines, 2003),
issues relating to marine reserves (Lubchenco et al., 2003, et seq. [17 reviews]), a special
issue of the Journal of Experimental Marine Biology and Ecology (Gibson et al., 2000, et
seq. [12 reviews]), and a book covering most facets of marine ecology (Bertness et al.,
2001, 19 chapters). Our field has been well-served by excellent syntheses of the complex
issues facing marine ecologists as we grapple with natural ecosystems. Despite the wealth
of literature, however, we are also subject to bandwagon issues (Paine, 2003) and are
prone to drawing analogies from the ecosystems we are most familiar with, perhaps like
Miss Marple, Agatha Christies famous home-grown detective who found all facets of the
world within her own small village. This leads to several questions. How well do models
developed elsewhere apply to local ecosystems? How important are local variations in
community composition and dynamics to achieving a broad understanding of structure and
function? How do ecologists reconcile local issues relating to particular ecosystems with
broader issues when there are great differences in taxa, usage patterns and management
structures? And how can the predictive power of research and advice, which are both a
measure of the relevance of our science and its usefulness (cf., Peters, 1991a,b), be
increased?
Given the numerous recent reviews, it seems that no paradigm has been left unexplored.
Rather than plumbing the same waters, therefore, I address some of the above questions
not as a thorough review, but from a perspective of an ecologist who has worked
extensively on the rocky shores of New Zealand, where several models relating to benthic
community structure have been tested. This special edition of the Journal of Experimental
Marine Biology and Ecology provides an opportunity to put forth such a perspective and
D.R. Schiel / J. Exp. Mar. Biol. Ecol. 300 (2004) 309342 310
highlight both commonalities and divergences between widely separated rocky shore
ecosystems.
2. Introduction
One of the most important areas of research in ecology in recent times involves the
interactions of benthic communities with the nearshore and open ocean environments, so-
called benthicpelagic coupling (cf., Menge et al., 1997a,b). This topic encompasses
virtually every facet of marine biology involved in the physics of the coastal water mass,
the life histories of coastal species, larval supply, settlement, recruitment, and trophic
interactions. Conceptually, little of this is new (cf., Sinclair, 1988, Graham and Dayton,
2002 for review), but there are new methodologies and a greater focus on multidisciplinary
studies that have opened new possibilities of understanding complex processes and
interactions (Paine, 2002; Palumbi et al., 2003). Inevitably, this involves considerations
of spatial and temporal scales, and how to design and implement meaningful experiments
(Underwood, 2000). Seemingly simple questions like how connected are populations?
have absorbed fisheries ecologists and managers for over 100 years (Sinclair, 1988; Peters,
1991a,b) but have assumed increasing importance to coastal ecologists more recently.
Understanding connectivity is crucial for marine reserve designs (Palumbi, 2003; Shanks
et al., 2003), gene flow between populations (Palumbi, 2001), recovery from disturbances
(Sousa, 2001) and the potential impacts of invasive alien species (Ruiz et al., 1999).
Unfortunately, our knowledge of the interactions of the nearshore water mass with
benthic communities is currently based on relatively few species and even fewer types of
organisms. This has been highlighted in several recent reviews. For example, although
Granthamet al. (2003) compiled a list of >1000 species, documenting their larval life history
characteristics and potential distances of dispersal, most species were plankton feeders and
the great majority had an obligate period in the plankton. Kinlan and Gaines (2003) derived
dispersal distances of 95 species. Most of these were invertebrates with an obligate
developmental period and only 10 were larger macroalgae, the fucoids and laminarians
that dominate many habitats. Menge (2000a) reviewed top-down and bottom-up processes
and community regulation in marine rocky intertidal habitats. In his first table of examples of
top-down control, 17 of 20 examples involved barnacles and/or mussels. In prominent
examples of larval supply and benthic processes, all of the examples are barnacles and
mussels (Gaines and Roughgarden, 1985; Menge et al., 1999; Connolly and Roughgarden,
1998). Given the importance of these taxa to our current understanding of rocky intertidal
dynamics, it is worth asking to what degree they are representative of nearshore processes
and dynamics.
A recent (Bertness and Callaway, 1994; Bruno et al., 2003) and controversial (Menge,
2000b) issue has been a re-focus on facilitation and positive interactions within marine
communities. Are they an essential structuring force, under what circumstances, and how
strong is their effect relative to other processes such as trophic dynamics? Many of the
cited studies involved plants, particularly large brown algae.
Whether or not facilitation occurs, macroalgae, particularly those in the Order Fucales,
are dominant occupiers of primary space in the middle to low intertidal zone of temperate
shores throughout the world (Abbott and Hollenberg, 1976; Schonbeck and Norton, 1978;
Clayton and King, 1981; Kautsky et al., 1986; Adams, 1994; Chapman, 1995). Inter-
actions between macroalgae and other taxa in the communities in which they occur are
fundamental to local dynamics and are essential components of general models. One focus
of this review, therefore, is on macroalgae, which offer many contrasts to filter-feeding
invertebrates. Macroalgae do not have an obligate development period in the plankton and
tend to have shorter dispersal distances than most invertebrates (Santelices, 1990; Norton,
1992; Reed et al., 1992; Dethier et al., 2003; Kinlan and Gaines, 2003). Consequently,
their interaction with the nearshore water mass is far different from filter-feeding
invertebrates, and the degree of connectivity of localised populations could therefore be
quite different. As for invertebrates, however, the relationship between propagule supply,
settlement, recruitment and post-recruitment processes is not well-known for many
species. Obviously, relatively inert macroalgal propagules do not display the behaviours
of invertebrate larvae (cf., Morgan, 2001; Underwood and Keough, 2001) but nevertheless
their ability to settle and attach, particularly in turbulent conditions near rocky shores can
be critical to community structure (cf., Brawley and Johnson, 1991).
Finally, most elements of marine ecology come together in biogeographic comparisons.
There is a long history of descriptions across biogeographic regions in most countries,
usually describing floral and faunal components on the basis of latitude, temperature or
degree of wave exposure (e.g., Stephenson and Stephenson, 1949; Dakin, 1960; Morton and
Miller, 1968; Ricketts et al., 1985). The history of experimentally testing underlying
processes responsible for regional differences is more recent, especially within a framework
of top-down (trophic) and bottom-up (nutrients and larval supply) processes (reviewed in
Menge, 2000a,b). Environmental gradients of nutrients, productivity, physical harshness
and disturbance can have major effects on the types and strengths of community interactions
(Connell, 1975; Menge and Sutherland, 1976, 1987; Menge and Olson, 1990). Four distinct
regions of the world have been cited in support of the critical interaction of top-down and
bottom-up processes in community regulation: the Pacific Northwest of the United States,
South Africa, Chile, and New Zealand. A comparative-experimental method (McPeek,
1998; Menge et al., 2002) using experiments in widely separated regions has been used to
elucidate general principles in the structure of marine communities. Because such studies
have involved NewZealand (Paine, 1971; Menge et al., 1999, 2003), which has some shores
that are at least superficially similar to those in the northwestern USA, I discuss various
structuring processes, often by using specific comparisons to New Zealand to illustrate
strengths and deficiencies in nascent nearshore-benthic models.
3. The upwelling hypothesis and community structure
Connolly and Roughgarden (1998) pointed out many of the contradictions in the
literature relating to community structure and regulation. Although the roles of compe-
tition, predation and disturbance have been elucidated in many countries and regions, these
processes can vary considerably within regions and at different scales. They and others
(e.g., Underwood and Denley, 1984; Connell, 1985; Gaines and Roughgarden, 1985;
Gaines and Bertness, 1992) have argued that if recruitment rates largely determine adult
distribution and abundance patterns, then they may also determine the strength of
interactions among species. Furthermore, a primary determinant of recruitment rates is
the rate at which larvae arrive to shore through upwelling-related events.
Upwelling occurs when strong equatorward winds blow along a coastline causing the
surface layer of water to move offshore (Pickard and Emery, 1990). Colder water, usually
laden with nutrients moves up from below the thermocline to replace it, and then moves
offshore as winds persist. This not only circulates nutrients into the shallow nearshore zone
but also transports larvae in the surface waters offshore (Lalli and Parsons, 1997). A
variety of processes, such as relaxation events, can move larvae back towards coastal
habitats (Connolly and Roughgarden, 1998). Because of the coriolis effect, upwelling
tends to occur commonly along the eastern boundary currents and, hence, west coasts in
both hemispheres (Pickard and Emery, 1990; Bearman, 1998). Where upwelling is strong
and persistent, therefore, the arrival of larvae back to shore is poor but where it is
intermittent, with frequent relaxation events, larvae may be brought shorewards and
recruitment can be high (Menge et al., 1997a,b; Connolly and Roughgarden, 1998),
leading to different trophic effects.
3.1. South Africa, Chile
Although the broad correlations between species distributions and physical factors
such as temperature, wave exposure and upwelling have long been known (Hubbs, 1948;
Stephenson and Stephenson, 1949; Dawson, 1950; Lewis, 1964), most evidence for the
interaction of trophic and nutrient-derived influences in marine community structure is
more recent. The most cited example is for South African shores (review in Menge,
2000a,b) which, along with the west coast of the USA and PeruChile, has a major
upwelling system. Bustamante and Branch (1996) surveyed 2500 km of shoreline,
quantifying and extending earlier observations of the distinct biogeographic provinces
along the upwelled Benguela west coast, a southern and an eastern region. Although the
west coast had a higher biomass of species in the intertidal zone, it also had only about half
the number of species of the south and east coasts, which were influenced by the Indo-
Pacific radiation. Within each of these regions, however, were great localised differences
in intertidal communities that largely related to the degree of wave exposure (cf., McQuaid
and Branch, 1984, 1985). Filter-feeding invertebrates were an order of magnitude more
abundant on exposed than on sheltered shores around Cape Peninsula. Intertidal algae
were also far less abundant on sheltered shores than in exposed and semi-exposed places.
Bustamante et al. (1995) referred to the subsidy of intertidal grazer biomass by drift
kelp fronds that came ashore on the west coast and sustained much larger populations of
intertidal limpets than did in situ algal productivity alone. This had trophic consequences
because the abundant grazers controlled the standing crop of benthic intertidal algae. It
appeared, therefore, that it was not just the highly productive subtidal mass of kelp that
sustained intertidal invertebrate populations but the delivery of kelp fronds to shore in
more exposed conditions.
Other work from South Africa shows that kelp beds occur nearshore throughout the
provinces and yet this does not necessarily imply large herbivore and filter/suspension-
feeder populations were present (Field and Griffiths, 1991; Branch et al., 1994). Hence, the
question is begged, is it more the productivity per se that drives the subsidy (i.e., a
nutrient-derived, bottom-up process, leading to increased production) or the degree of
wave exposure (a delivery process) interacting with intertidal dynamics that drive these
intertidal invertebrate populations? The answer is not clear for many coastal ecosystems.
However, because of the great importance of wave exposure to community structure, the
explanation could be more physically based than nutrient-based. The relative contributions
of plankton and subtidal, macroalgal-derived energy to benthic community structure and
regulation are of some importance but are little understood.
The processes that tip the balance between dominance by filter-feeders and algae are
not always clear, yet they form a major focus in intertidal studies examining both broad
and localised scales of community organisation. For example, along the coast of Chile,
Broitman et al. (2001) did extensive surveys and noted a distinct discontinuity in
community structure at about 32jS latitude. Mussels were rare north of this latitude but
tended to increase in abundance to the south in the mid-intertidal zone. This was presumed
to coincide with an oceanographic feature. The low tidal zone was dominated by kelps,
which also became more abundant to the south, while ephemeral and crustose algae were
more abundant in warmer northern waters. They characterised some of their many study
sites as undergoing occasional upwelling, but they found no trend of increased abundances
of filter-feeders at these locations. While the abundances of major taxa showed clear trends
with latitude and its correlate sea-surface temperature, there was no clear trend that could
be ascribed to upwelling or productivity.
The western coast of the USA is probably the most studied nearshore region of the
world. There has been considerable analysis of biogeographic boundaries and within-
region variation in community structure relating to oceanographic features, particularly
upwelling. This involves a complex interaction of many variables and is still in the early
days of experimentation, which I discuss below.
3.2. Pacific coast of the USA
The mechanisms influencing upwelling, the transport of larvae, and effects on
community structure and processes in the Pacific northwest have been examined and
discussed in several papers (Ebert and Russell, 1988; Roughgarden et al., 1991; Wing et
al., 1995; Connolly and Roughgarden, 1998; Largier, 2003). In this region, upwelling is
more intense towards the south and is particularly intense around major headlands (Huyer,
1983; Ebert and Russell, 1988). Connolly and Roughgarden (1998) used transect data
from many exposed rocky intertidal benches in California and Oregon to determine the
relationship between sessile invertebrate cover and bare space and how they are related to
upwelling intensity. They found less free space in Oregon than in central and northern
California, less primary algal cover in Oregon, and a greater cover of the mussel Mytilus
californianus and acorn barnacles (Balanus glandula) in Oregon. They concluded that
there was less free space and greater cover of competitively dominant filter-feeders in the
area of weakest upwelling. They considered a predation gradient to be an unlikely cause
of these patterns because the areas surveyed were above the lower limit of mussel beds
where predation by sea stars mostly occurs. They further argued that the wide area of the
continental shelf in California and the persistence of upwelling led to fewer invertebrate
larvae reaching the shore to settle, compared to the narrower shelf and frequent relaxation
events in Oregon that allow more larvae to reach shore. Consequently, their model and the
work on which it was based (e.g., Roughgarden et al., 1988) provide an oceanographic
circulation-modulated driver of recruitment variation that leads to variations in the
intensity of trophic interactions.
Clearly, complex oceanography intersects with upwelling, larval transport and settle-
ment events. Based on SST and long-term trends in wind stress, there are distinct regions
along the US west coast, with transitions near Point Conception in the south and Cape
Mendocino in the north (Mendelssohn and Schwing, 2002). These headlands coincide
with the southern limits of many northern species and the northern limits of southern
species, respectively (Morris et al., 1980). These areas, therefore, have biogeographic as
well as structural importance for benthic communities. Within these regions, however,
there is great variability. For example, Connolly et al. (2001) argue that because
recruitment by competitively dominant filter-feeders is not saturating in central and
northern California, mesoscale processes within this region are more important than
larger-scale trends in upwelling as determinants of community structure.
These arguments for benthicpelagic coupling have considerable strength in linking
together most aspects of the nearshore environment, community structure and regulation.
Importantly, they also provide a predictive framework for testing critical processes. The
major strengths are in clarifying mechanisms for recruitment variability and its causes and
the trophic effects that result from recruitment variation, thereby coupling pre- and post-
recruitment processes and broad and local-scale events. Nevertheless, there are critical
processes in the supply and delivery process, and considerable variability in benthic
processes that include not only predation and grazing but also disturbance variability and
intensity, successional events, competitive hierarchies, and community composition that can
play a more dominant role than upwelling in determining community structure (e.g., Foster
et al., 2003; Chapman and Underwood, 1998). Clearly, there are problems in testing large-
scale processes related to upwelling, and much of the evidence is correlational. So, how
general are the predictions of upwelling events and effects on community structure and
organisation?
3.3. New Zealand and comparisons to other regions
Bruce Menge and his collaborators have been insightful and instrumental in realising
that a comparative-experimental approach can be used across continents and hemispheres
to evaluate the generality of processes in widely separated ecosystems. Their recent work
comparing Oregon and southern New Zealand is based on the similarity in latitude and
composition of exposed shores that are dominated by filter-feeders (Menge, 2000a). Major
findings are that there are significant differences in settlement and trophic interactions
between the east and west coast of NZ that are largely driven by oceanographic conditions,
particularly upwelling on the west coast and downwelling on the east coast (Menge,
2000a,b; Menge et al., 1999, 2003). They found that predation rates were higher,
recruitment of barnacles and mussels was greater, there were more large predators (sea
stars), and that grazing was more intense on west coast sites. Menge et al. (2003)
concluded that because the concentration of phytoplankton (as measured by chlorophyll-a)
and particulates was similar on both coasts, that larval transport and oceanic productivity
are decoupled in New Zealand, unlike results from Oregon (Menge et al., 1997a,b).
These are complex issues involving the interactions of nearshore processes with commu-
nity structure and ecological processes. Here, I discuss these issues within the broader
context of NZ shores.
3.3.1. New Zealand community structure
In many ways, New Zealand serves as a microcosm of processes affecting temperate
communities: it has a complex hydrography, large rivers affecting coastlines, prominent
headlands, a complex continental shelf, and a large suite of endemic species. New
Zealand has been described as an archipelago in space and time (Nelson, 1994). With
three main islands and around 600 islands and islets (Molley and Dingwall, 1990), NZ
spans 13j of latitude and is influenced by complex oceanography (Heath, 1985; Fig. 1).
Fig. 1. The currents and continental shelf around New Zealand. Note position of subantarctic waters to the south
(SAW); subtropical waters to the east; the Southland Front (SF), the Southland Current (SC), the warm-core eddy
(Wairarapa Eddy) on the east coast; the currents around East Cape (central right, North Island); the tropical front
and East Australian Current in the north; the Westland Current (top right, South Island). Depth contours of
continental shelf are shown. Further details in the work of Heath (1985). Redrawn from map by National Institute
of Water and Atmospheric Research.
The major land masses extend from the subtropical north (34.5jS) to the cool temperate
south (47.5jS), but territorial waters are extended considerably by the subtropical
Kermadec Islands, the Chatham Islands to the east, and the subantarctic islands in the
far south. Along the mainland of the North and South Islands, the annual average sea-
surface temperature (SST) varies from 17.5j in the far north to 11.5j at the tip of the
South Island, with surprisingly little variation at equal latitudes between the east and
west coasts (e.g., Uddstrom and Oien, 1999; Murphy et al., 2001). Biogeographic
provinces have long been recognised, although these varied depending on taxa (Moore,
1961; Pawson, 1961; Dell, 1962). The west coast has a mixed coastal flora and fauna,
with a historically recognised breakpoint just south and west of Cape Reinga (at the top
of the North Island) and in the south in the vicinity of Fiordland (southwest coast of the
South Island). Discontinuities have been noted on the east coast at East Cape for many
invertebrates and south of Cook Strait (between the North and South Islands) for many
algae (Moore, 1961). Nelsons (1994) analysis of large brown algal distributions found
distinct elements in the northern part of the North Island, but no clear separation from
the region of Cook Strait south. Very distinct elements of communities were noted at the
widely separated subantarctic islands and the Chatham Islands, and the Three Kings
Islands, 57 km north of the North Island, all of which have a high degree of endemism.
Nelson reiterated reservations (e.g., Lang, 1895) about the explanatory power of
dispersal as the prime influence shaping the composition of the NZ algal flora and
stressed geological, oceanographic, climatological and ecological influences that have
interacted over millions of years.
On intertidal rocky shores, two of the most striking features are that barnacles and
mussels dominate most west coast sites but are found primarily on headlands on the east
coast, whereas large brown algae dominate most east coast sites but few on the west coast
(Schiel, unpublished database). Of particular note is that smaller fucalean species (less
than about 1 m in length as adults), especially the endemics Carpophyllum maschalo-
carpum, C. angustifolium, Cystophora torulosa, and Hormosira banksii, are abundant
along much of the east coast but give way to the giant southern bull kelp (Order Fucales)
Durvillaea antarctica (Hariot) in the more exposed waters south of Cook Strait. Bull kelp
can reach >80 kg/m
2
, can have considerable whiplash effects that limit the taxa able to
survive in nearby areas (Santelices et al., 1980) and often occurs just below mussels,
especially on east coast headlands. This zone on the west coast is usually occupied by
tough red algae (corallines and Gigartina species) that can withstand the considerable sand
scour on low tidal benches.
Across sites of different wave exposures on both coasts in the South Island, mussels
(both Perna canaliculus (Gmelin) and Mytilus galloprovincialis) are found commonly
on sheltered shores (mostly within harbours and behind headlands), and on exposed
shores (i.e., average wave force 4060 Newtons), mostly in the mid intertidal zone.
Therefore, one of the most important associations between barnacles and mussels is that
on exposed shores they tend to co-occur with bull kelp on the east coast but not on the
west coast. It should be noted that the intertidal sea star Stichaster australis occurs
abundantly on the west coast, but is found only in small numbers on the east coast itself
but often on wharf pilings in harbours when mussels are abundant (cf., Morton and
Miller, 1968, p. 362).
3.3.2. New Zealand coastal environment and upwelling
The nearshore environment around New Zealand is complex, yet understanding its
nature is fundamental to determining how it affects onshore community structure and the
validity of comparisons to elsewhere. The currents, continental shelf, positions of
persistent eddies, productivity patterns, amount of sedimentation and geomorphology
form an intricate interwoven picture (Bradford-Grieve et al., in press). On average, the
entire west coast (other than within harbours and fiords) is considered very exposed with
almost continual pounding of oceanic swells. The east coast is mostly semi-protected north
of East Cape but more exposed on outer coasts sites from there southwards. Most east
coast sites are composed of softer sedimentary rocks, except for headlands such as Banks
Peninsula (cf., Menge et al., 1999) which are harder volcanic or metamorphic rock, while
west coast reefs are composed mostly of hard metamorphic rock. The broad relationship
between rock types and exposure may affect community structure; few mussels are found
on the softer sedimentary rocks, mostly because they do not attach well (although this has
not been tested). For example, mussels are uncommon on the Kaikoura peninsula
(composed mostly of mudstone and friable limestone), although they are common on
harder reefs to the south and north. Reefs composed of softer rocks rarely occur where
wave-exposure is great, and are usually dominated by fucalean seaweeds, such as H.
banksii, Cystophora spp. and Carpophyllum species.
Hydrographically, NZ is surrounded by several distinct water masses (the surface
Subtropical and Subantarctic waters, and from the surface down, Antarctic Intermediate
Water, Deep Water, and Antarctic Bottom Water; Fig. 1). Major currents are the
subtropical East Australian Current in the north, the Westland Current in the southwest,
and the Southland Current that flows from the south-western end of the South Island and
northwards up the east coast (Heath, 1985; Vincent et al., 1991; Chiswell and Schiel,
2001). Around the middle of the South Island, a mixture of water from the Southland
Current is deflected eastwards along the continental shelf, but some northward flow is
evident intermittently through a submarine saddle (Shaw and Vennell, 2000) (contrast with
Menge et al., 2003; Fig. 1). Upwelling occurs intermittently from at least the central west
coast of the South Island northwards to Cook Strait (Vincent et al., 1991; Stanton, 1971,
1976) and also along the northeast coast of the North Island.
There is some debate about how frequently upwelling occurs along the west coast and
whether sudden decreases in seawater temperatures as recorded by onshore sensors
(frequently used in intertidal studies; cf., Menge et al., 1999) are indications of upwelling
or of freshwater input. There is considerably higher rainfall on the west coast than the east
coast (e.g., average annual rainfall is around 2200 vs. 600 mm; NIWA meteorological
records) and there are two large rivers that may have caused the cold water plumes seen in
some studies. Vincent et al. (1991) found cold-water plumes extending offshore from the
coast in the vicinity of river mouths but argued they were unlikely to be a direct effect of
cold riverine input because of dilution and because differences between seawater and river
temperatures were not large at the time of their study. However, Stanton (1972) showed
there can be a salinity anomaly near rivers, and Vincent et al. (1991) also found that the
colder water had reduced salinity. In areas where river discharge significantly affects
surface salinity values, as along the west coast of South Island (Stanton, 1976; Bradford,
1983) and the west coast of the US, upwelling episodes may, in fact, result in higher
salinity waters being brought to the surface, which may not be nutrient-rich as they do not
represent below-thermocline waters (Pickard and Emery, 1990). Productivity along the
west coast of NZ, therefore, may not be due to upwelling alone but to freshwater input of
nutrient-rich water, a benthic-terrestrial rather than a benthicpelagic coupling (cf.,
Menge et al., 1999). These sorts of issues need considerably more work because they
entail far different mechanisms for benthic processes. Analyses of stable isotopes may help
resolve the sources of nutrient inputs.
Circulation around the east coast of the South Island is also complex. Murphy et al.
(2001) showed that the highest concentrations of chlorophyll-a around NZ occurred off the
southern region of the South Island and to the east along the continental shelf. Rather than
upwelling-driven productivity, it appears that this is due to mixing of the warmer coastal
waters, poor in macronutrients but iron-rich, with the macronutrient-rich but iron-poor
subantarctic waters (Abraham et al., 2000; Boyd et al., 2000). These waters are driven up
the east coast by the Southland Current, although this process is not well-understood
(Murphy et al., 2001). Whatever the combination of processes driving coastal productivity
and benthic community structure, it is undoubtedly more complicated than upwelling and
downwelling, and we are only in the early stages of understanding.
4. Alternative hypotheses for replenishment of populations
All studies on benthicpelagic coupling highlight the importance of phytoplankton
production, larval transport, the interface with the nearshore environment, and recruitment
limitation, which affects community processes. Where organisms with an obligate period
in the plankton are concerned, it is trivial to conclude that larval transport and recruitment
are linked to coastal oceanography (including circulation and nutrient concentrations). As
Menge et al. (2003) note, it is coupling between processes and their various strengths that
require understanding. Furthermore, larval behaviours and retention can be important
factors in larval transport (Morgan, 2001; Warner and Cowen, 2002). Here I discuss other
hypotheses relating to larval transport and early life histories.
4.1. Coastal circulation, larval pool and retention
As Largier (2003) points out, coastlines are not usually straight or smooth, and
consequently water flows can separate from the coast and form eddies. Furthermore,
cross-shore flow is an integral part of larval dispersal. Results from intensive, yet
temporally limited studies indicate relatively poor recruitment of mussels and barnacles
on the east coast compared to the west coast of the South Island of New Zealand (Menge et
al., 1999), but the influence of large-scale circulatory flows vs. localised influences is not
clear. For example, study sites on the north side of Banks Peninsula on the east coast have
unique localised influences which may be far different from other east coast sites. The
strong, permanent, northwards-flowing current that sweeps past the peninsula often creates
large eddies that meander into the bay on the north side of the peninsula (Shaw and
Vennell, 2000), probably transporting larvae away from shore. Although downwelling can
influence larval transport, there is little evidence that it is strong or even exists nearshore,
let alone is a dominant process affecting communities along the east coast. However, the
presence of eddies, the width of the continental shelf, and the great distances between large
mussel populations are likely to have a reduction effect on larval abundance. The nearest
large mussel patches to this peninsula (other than on the peninsula itself) are >50 km to the
north and south, where small headlands and reefs occur. Therefore, the regional pool of
larvae may be quite small and diffuse, compared to the west coast where mussel
populations occur on most reefs from the far north to the far south.
For any group of taxa, it seems unlikely that we can be sure of the influence of physical
factors affecting settlement unless we have a reasonable idea of what the local and regional
pool of larvae may be for those taxa (Meidel and Scheibling, 2001). Where mussel and
barnacle populations are ubiquitous along a coastline, such as the Pacific northwest, this
larval pool may be large, but this is less likely in areas with widely spaced, sparser
populations (Warner and Cowen, 2002).
The larval pool may be maintained by retention near adult populations. There is
considerable evidence that even long-lived larvae may not be dispersed great distances and
that local retention may be considerably more prevalent than previously thought (Warner
and Cowen, 2002). Larvae have numerous sensory capabilities and behaviours that detect
variations in the water column and help them find suitable settlement sites (Kingsford et
al., 2002). By moving vertically, larvae of many species are able to take advantage of
different characteristics of the water column. Sponaugle et al. (2002) concluded that
physical factors resulting in departure from unidirectional water flows that are uniform
with depth (characteristics of most heterogeneous coastlines) provide the opportunity for
larval retention, and therefore self-recruitment of populations.
4.2. Dispersal, habitat-forming seaweeds
There have been excellent recent reviews on dispersal in marine organisms, which
recognise the critical importance of this process to all facets of marine community
structure (Warner and Cowen, 2002; Kinlan and Gaines, 2003; Shanks et al., 2003; which
I will not review here). Overall, however, marine algae, especially habitat-forming large
brown algae are poorly represented. Because seaweeds are such a dominant component of
nearshore subtidal and intertidal communities, are associated with many other organisms
and processes and have been central to the often intense debate about the nature and extent
of community structure and dynamics (Foster, 1990, 1991; Paine, 1991; Underwood,
2000), it is crucial to understand their place in models involving dispersal.
Reviews of dispersal in seaweeds have highlighted both knowledge and shortcomings
in this critical process (Santelices, 1990; Norton, 1992; Johnson and Brawley, 1998).
Algae have small propagules that when released into a turbulent coastal environment are at
the mercy of the water mass. Laminarian spores are motile and may swim for many hours
(Reed et al., 1999), but they are only around 610 Am in length and actively travel only
very small distances. Successful colonization of kelps requires around 110 spores per
mm
2
to ensure fertilization (Reed, 1990a; Reed et al., 1991, 1997). Fucoid algae, the most
common intertidal large brown algae, produce non-motile eggs that are not of neutral
density (so they sink) but move largely with the water mass (Clayton, 1992; Chapman,
1995; Gaylord, 1999; Gaylord et al., 2002). To colonize habitats, therefore, large brown
algae must achieve several processes: fertilization, dispersal to appropriate substrata, initial
attachment and subsequent recruitment, often in high-energy, turbulent shores where water
velocities can reach several metres per second (Denny, 1995). These processes are, to
some extent, density-dependent and also different from most invertebrates, the larvae of
which can display complex behaviours and respond to settlement cues (e.g., Keough,
1989; Raimondi, 1990; Gaines and Bertness, 1992).
Most fucoid and some laminarian algae are capable, at least potentially, of dispersing
both as propagules and as adults, in contrast to attached invertebrates, which are confined
to dispersing in their early life stages only (Fig. 2). The relative importance of these two
dispersal stages can be surmised for a few algal species, but is probably species-specific.
For example, the notoriously invasive fucoid Sargassum muticum, when still attached to
the substratum, drops the vast majority of its propagules within 5 m of parent plants, yet
populations have spread widely and quickly once introduced to a new areas because of
detached, drifting adult plants (Deysher and Norton, 1982; Chapman, 1995 for review).
Although most detached seaweeds probably get cast ashore, some can survive for
extended periods as drift plants (Norton and Mathieson, 1983). Species such as S.
muticum, S. sinclairii (in New Zealand) and Cystoseira osmundacea (California) have a
form of parental care in that germlings, complete with sticky rhizoids, are attached to
receptacles of drifting plants and are capable of quick attachment after they drop from
parents, descend through the water column and contact a surface (Norton and Fetter, 1981;
Deysher and Norton, 1982; Schiel, 1985, 1988).
Drifting adult plants have the potential to disperse long distances. For most species,
however, the ability of drift plants to remain reproductively viable is simply assumed, but
unknown. For example, southern bull kelp (D. antarctica) and H. banksii make up a
significant portion of coastal drift and beach-case seaweed along the east coast of southern
Fig. 2. Stylised diagram comparing potential dispersal of laminarian and fucoid algae (shaded bars) with sessile
invertebrates (open bar) at different stages of development. Most fucoids and some laminarians float when
detached; drift represents detached, reproductive plants, which may be >10 years old. Furthermore,
reproductively active fronds can detach from perennial fucoids over many years. Although potential dispersal
distances can be high, it is largely unknown how important and effective long-range dispersal is to population
replenishment over generational time.
New Zealand, but whether these drifters are capable of effectively seeding onshore rocky
habitats has never been tested.
It was generally thought that the major form of longer-range dispersal for large subtidal
algae was through detached, drifting adult plants (e.g., Anderson and North, 1966; Dayton
et al., 1984) but recent work has shown that the early life stages are also capable of
dispersing at least several kilometres. Reed et al. (1992) showed that spores have the
capacity to survive for long periods and germinate in the water column, providing a
possible means of dispersal. Gaylord et al. (2002) showed that spores of giant kelp,
released near the bottom of plants, are capable of successful dispersal, fertilization,
settlement and development up to several kilometres away from adults. This depends on
the period of competence, flow conditions, turbulence, sinking speed of propagules and
their proximity to the substratum (McNair et al., 1997; Gaylord et al., 2002).
When spores and zygotes are released directly into the water column, the synchrony of
release and the presence of a spore cloud may significantly aid in providing the densities
required for fertilization and colonization (Norton, 1992; Reed et al., 1997), although these
processes are unknown for most seaweeds. Intertidal fucoids face special challenges by
releasing eggs into often turbulent onshore waters. Although egg release can occur during
low tide in some species (Brawley et al., 1999), the speed and strength of propagule
attachment are critical before the onslaught of tide and waves (Vadas et al., 1990; Taylor
and Schiel, 2003). Furthermore, because of the presence of a viscous sub-layer near the
benthos that varies with water motion (Schlichting, 1979; Gaylord et al., 2002), the ability
of propagules to penetrate this, attach and develop can vary. There is great diversity of
types of algal propagules and how they adhere (Fletcher and Callow, 1992) and also of
their constituent mucilage, reactions and rates of curing (Vreeland et al., 1998). Gaylord et
al. (2002) highlighted the need to understand the physics of algal propagule dispersal and
its relationship to water flow to achieve an understanding of algal dispersal in hydrody-
namically complex waters.
4.3. Propagule abundance, settlement, recruitment
4.3.1. Algae
The arrival of settlers in high numbers is crucial for fucoid algae, but for reasons other
than fertilization. Not only is post-settlement mortality of zygotes and embryos high due to
various stresses at low tide (e.g., Brawley and Johnson, 1991) but high densities of recruits
may be required for viable adult populations to form. Plant morphology can be related to
density (Schiel and Choat, 1980; Ang and DeWreede, 1992; Reed, 1990b). Dense adult
stands of fucoids can help lessen desiccation at low tide because of the layering of fronds
(e.g., Schonbeck and Norton, 1978, 1979), as well as reducing water flow, providing shade
and microhabitat to areas below that can affect community structure (Bruno et al., 2003).
For example, the most common intertidal fucoid in New Zealand (H. banksii) requires >1
recruit (ca. 2 mm in length) per cm
2
to produce a closed canopy in the absence of grazing,
and the number of settlers needed to produce these recruits is much greater (ca. 250750
per cm
2
; Schiel, unpublished data).
Dense algal populations are one of the commonest features of temperate intertidal reefs
worldwide and their critical dynamics seem, at this stage, to be only loosely connected to
larger scale processes such as upwelling and downwelling. Algae have complex ways of
extracting resources from the surrounding water mass across different hydrodynamic
environments (Hurd, 2000), they do not have obligate planktonic development, and most
of their mass of propagules do not seem generally to go far. Most intertidal fucoids and
laminarians are highly tuned to the disturbance regimes in which they form dense
populations. Understanding the interaction of their heteromorphic life histories, especially
their early life stages, with turbulence, water flow and substratum characteristics is at least
as essential as trophic dynamics to general models of community structure.
4.3.2. Invertebrates
Establishing the relationship between larval abundance, settlement and recruitment is
notoriously difficult, usually requiring pumping, netting or trapping of larvae, counting
microscopic settlers and recruits. Capturing settlers often involves artificial samplers, the
use of which has a long history in marine ecology (e.g., Coe, 1953; Foster and Sousa,
1985, for review). One such sampling device is the tuffy, a spun plastic pot scrubber on
which mussels readily settle (e.g., Connolly et al., 2001; Menge et al., 2003). This is
similar to the furry ropes used commercially in NZ to catch mussel spat (Meredyth-Young
and Jenkins, 1978). Tuffies are a standard size, so allow comparisons between sites and
times, and are therefore a useful experimental unit. Recently settled mussels on tuffies
have been used as a measure of recruitment in several important recent publications (e.g.,
Menge et al., 1999, 2003; Connolly et al., 2001). But is it recruitment? Although this
term can be loosely defined (Connell, 1985), whatever these artificial collectors catch is a
large step away from recruitment to a natural rock surface. Although tuffies can be a
valuable tool in providing a standard measure of mussel settlement among sites, it is not
clear how this relates either to larval abundance or to replenishment of populations. The
relationships between larval abundance and recruitment can be modified by settlement
patterns, larval behaviour, larval competence and condition, the nature of the substratum
and post-settlement mortality (Morgan, 2001, for review).
To determine the relationships between larval abundance, settlement (i.e., <1 week old)
and recruitment, Hayden (1995) did simultaneous sampling over 3 years in a mussel-
growing centre in central NZ. She found there was usually a significant correlation
between larval abundance and settlement (15 out of 20 sites, where weekly larval
abundance and settlement were measured; significant r-values ranging from 0.56 to
0.94; minimum n=12) but that the relationship failed altogether in one of the years. At
two sites, the correlations were negative. There was also usually a significant correlation
between settlement and 8-week-old recruits (13 out of 20 weekly samples; significant r-
values ranging from 0.41 to 0.75; minimum n=12), but the relationship between settlement
and 12-week-old recruits was much weaker (only 3 of 10 correlations were significant;
significant r-values ranging from 0.43 to 0.58). Some relatively poor settling sites had
good recruitment while other sites had high mortality of settlers. It is hardly surprising that
there is variability in these relationships but they highlight that it cannot be assumed that
the numbers that appear on collectors necessarily relate to the numbers at earlier or later
stages.
Estimating these relationships is not easy (cf., Gaines and Roughgarden, 1985), and is
made more complicated by the highly variable nature of the plankton, identification of
larval stages of invertebrates of particular interest in benthic communities, and capturing
settlers for species other than barnacles and mussels. Nevertheless, understanding these
linkages for more key taxa is essential for elucidating the mechanisms linking the pelagic
and onshore environments, and replenishment of benthic populations (cf., Roughgarden et
al., 1984).
4.4. Wave exposure
The degree of wave exposure is a crucial predictor of community structure and
processes (Menge and Sutherland, 1976, 1987) and has long been used as one of the
main categorizers of marine communities (e.g., Stephenson and Stephenson, 1949; Dakin,
1960; Morton and Miller, 1968; Ricketts et al., 1985). It also affects the activity of mobile
predators, and thus top-down interactions and community structure. However, separating
the effects of the various large-scale physical effects from smaller scale processes on
biological communities is challenging. For example, El Nino events are associated with
large-scale nutrient depletion that leads to reduced giant kelp populations, but they are also
associated with frequent and intense storm activity that removes kelp plants (Dayton and
Tegner, 1984; Dayton, 1985; Dayton et al., 1999). Populations of giant kelp in more
sheltered areas away from the open coast can survive El Nino events, presumably because
they are protected from severe wave action and because there may be localised variation in
nutrient depletion (Foster and Schiel, 1993). There is also a positive correlation between
the degree of wave exposure and other physical variables such as sedimentation, which
may affect community structure (Kendrick, 1991; Airoldi, 1998; Schiel et al., in review).
One of the most important effects of wave exposure is on the ability of organisms to
attach and stay attached. There are limits to the forms of benthic invertebrates on wave-
exposed shores (Denny et al., 1985) that allow them to stay attached in waves that can
travel at >10 m/s (Denny, 1995). Seaweeds such as Fucus gardnerii have smaller prostrate
forms in exposed conditions and poorer survival than in more protected sites (Blanchette,
1997). However, much less is known about effects on early life stages. The ability to attach
in sufficient numbers to form a viable population may be one of the more important
discriminators in community structure, especially for seaweeds, the propagules of which
have little or no ability to swim (Santelices, 1990; Norton, 1992).
Several studies have shown that the propagules of habitat-forming algae have a
differential ability to remain attached to substrata across different wave climates. For
example, Vadas et al. (1992) found that 99% of zygotes of Ascophyllum nodosum (L.)
LeJolis that had been settled for 15 min were removed by a single low-energy wave. In
New Zealand, Taylor and Schiel (2003) tested the ability of zygotes of an exposed-coast
species, D. antarctica, and a sheltered-coast species, H. banksii, to remain attached across
wave exposures. They found that in most wave exposures, 80100% of Durvillaea
zygotes survived a full tidal cycle, regardless of wave exposure or the post-settlement time
that zygotes were attached. However, Hormosira zygotes that had been settled for 1 and 6
h had no more than 8% survival, and then only in very sheltered conditions. Given 12 h of
post-settlement time before being exposed to field conditions, Hormosira survival was still
only 2040% in sheltered conditions and <5% in exposed sites after one tidal cycle. In
most conditions, only Durvillaea was able to attach firmly and quickly. They concluded
that at least some fucalean species may be precluded from forming populations on exposed
shores where conditions are mostly unsuitable for their attachment.
Settlement of large, habitat-forming seaweeds involves a series of complex physical,
biological, ecological and chemical processes at a micro-scale, from the release of
propagules by reproductive adults, arrival at suitable substrata, initial adhesion to a
surface, permanent attachment and development (Norton, 1983; Reed, 1990a; Brawley
and Johnson, 1992; Vreeland and Epstein, 1996). The timing of release of propagules can
also be critical to attachment. For example, propagules that are released from parent plants
during low tide may avoid the problems associated with turbulence, at least for the critical
period of initial attachment. Microsites are known to be important in the ability of
propagules of many species to survive (Eckman, 1990; Amsler et al., 1992; Crimaldi et al.,
2002) but their relationship to the physics of attachment and detachment of large brown
algae is unknown. The integration of these factors will advance our knowledge of how
these processes combine to produce windows of recruitment. We especially need a
greater knowledge about microscopic-scale processes to attain a more comprehensive
understanding of marine community development, and the feedbacks between resident
populations, dispersal and recruitment processes across wave climates (Caley et al., 1996),
which are so crucial to understanding the downstream effects of disturbances and potential
for recovery (Sousa, 1984, 2001).
4.5. Sedimentation
Sedimentation can have adverse effects on benthic organisms (Abelson and Denny,
1997), but is unlikely to be independent of other factors, especially wave exposure. Coarse
sediments such as sand and gravel can abrade tissue from organisms or remove them from
reefs, thereby affecting community structure. For example, some red algae are resistant to
sand abrasion and can survive where few other species can (DAntonio, 1986). Sediments
can interfere with settlement, cause a reduction in light penetration in the water column
and be associated with nutrient enrichment (Kautsky et al., 1986; Jonsson and Carmen,
1994; Heiskanen and Tallberg, 1999), affect the light environment of settled early stages
(Devinny and Volse, 1978), or create anoxic smothering conditions (DAntonio, 1986).
Most studies of sediments on rocky shores have noted the variable arrival and departure
of sediments, and consequently the variable effects on reef organisms (e.g., Littler et al.,
1983; Stewart, 1983; Airoldi et al., 1996). In heavily sedimented areas of the Mediter-
ranean Sea, the growth patterns and biomass of algal turf assemblages are affected by the
degree of sedimentation (Airoldi and Virgilio, 1998; Airoldi et al., 1996). In one study in
southern California, sand cover changed from 0 to 55% during winter, which affected the
relative abundances of an anemone, a sand tube worm and macroalgae (Taylor and Littler,
1982). One of the most frequent effects on larger algae, however, may be on settlement.
Kelp spores may fail to attach to primary substratum when a layer of sediment is present
and may not develop if covered by even a light dusting of fine sediment (Devinny and
Volse, 1978; Norton, 1978; Vadas et al., 1992; Chapman and Fletcher, 2002). For example,
Schiel et al. (in review) found that a light dusting of fine sediment reduced attachment of
Durvillaea and Hormosira zygotes by up to 70% compared to clear substratum, and that a
complete cover of sediment prevented attachment altogether.
There can also be interactive and indirect effects of sediments. For example, on
sheltered shores in Britain, the removal of an Ascophyllum canopy resulted in a loss of the
understory turf assemblage and a reduction in silt (Jenkins et al., 1999). This led to an
increase in the abundance of limpets and eventually to recruitment of Fucus species. In
New England, the removal of the snail Littorina littorea resulted in algal recruitment, the
accumulation of sediment and eventual recruitment of invertebrates characteristic of soft
sediments (Bertness, 1984). In each of these cases, the local character of the assemblage
and trophic interactions were changed at least partly by sedimentation.
The interaction of sediments and reef biota clearly may contribute to the renowned
patchiness of benthic communities, can operate on a fine scale at specific settlement sites
and concavities within reefs (Airoldi, 1998), and at greater scales where sediments
accumulate over large areas (Norton, 1978). Increases in sedimentation along the coastal
strip, particularly in less exposed areas, from changes in land use, urbanization, forestry,
farming, and coastal dredging are seen as major threats to benthic communities in many
places, including New Zealand (cf., Heiskanen and Tallberg, 1999; Lotze et al., 2000;
Madsen et al., 2001). Understanding how sedimentation may affect the early life stages, in
particular, of benthic organisms may prove to be crucial in elucidating influences on
community structure and the interaction of wave exposure gradients.
4.6. Predation
The intensity of predation is a key component of models on community organisation
(Paine, 1974; Connell, 1975; Menge and Sutherland, 1976, 1987; Menge et al., 1994) that
can be affected by high recruitment of filter-feeding benthic invertebrates (Connolly and
Roughgarden, 1999a,b). Where mussels are involved, predation by sea stars can set the
lower vertical limit of mussel populations on a shore as well as create or maintain patches
within mussel beds that allow a wide diversity of other species to persist without being
overgrown by competitively superior mussels (Paine, 1974; Paine and Levin, 1981; but
see Lohse, 1993). In studies in several countries, the abundance of predators is positively
correlated with the abundance of filter-feeders, and these tend to occur mostly on exposed
shores (Bustamante and Branch, 1996; Menge et al., 1999; Connolly and Roughgarden,
1998). Furthermore, it has been argued that predation intensity is one of the key trophic
interactions in benthicpelagic coupling, whereby the increased recruitment of filter-
feeders and increased productivity in areas affected by upwelling also have increased
intensity of predation (Menge et al., 1997a,b). Given the overall importance of this
process, it is worthwhile to assess its generality.
The size and types of predators and invertebrates that have been used to test for
predation clearly have an influence on its intensity and importance to community
organisation. For example, Menge et al. (2003) experimentally tested predation on mussels
that were 3040 mm in shell length and found that they were differentially affected
between coastlines of New Zealand. Predation rates were higher on the west coast, which
was due to the predacious sea star Stichaster australis. They suggested that predation
intensity was upwelling-related because of differences in larval supply of sea stars to the
different coasts. Mussels in this size range are at least 6 months old (i.e., post-settlement;
Fox, 2003), which leaves a considerable gap in time between the sizes caught on tuffies as
a measure of recruitment and those used to measure predation intensity. What about the
earlier life stages?
In New Zealand, one of the most important predators of recently settled mussels is the
labrid fish Notolabrus celidotus. Hayden (1995) showed experimentally that the dense
populations of this fish around the mussel-growing areas of central NZ were a major cause
of spat loss on commercial farms. N. celidotus could completely strip lines of mussels less
than ca. 1 cm in length. This fish and the related N. fucicola are the commonest fish
species along eastern NZ coastal sites (Hickford and Schiel, 1995; Schiel and Hickford,
2001), where they feed on a wide range of small invertebrates (Denny and Schiel, 2001).
Like lobsters in southern California that move up during high tide to feed in intertidal
mussel beds (Robles, 1987; Robles et al., 1995), these fish readily forage for invertebrates
at high tide. Furthermore, they tend to have relatively restricted territories on nearshore
reefs and do not move far from these areas to feed (Jones, 1984). They may well be the
cause of poor recruitment of mussels at reef-associated sites, which are particularly
common along the east coast (Rilov and Schiel, unpublished data). Therefore, it is not
necessarily the case that predation intensity is greater where recruitment is high.
In summary, there is often a significant gap in time between settlement, recruitment to
populations, and the stages on which predation experiments are done. If larger prey are
used for experiments, the actual strength of this process in community structure may be
underestimated, thereby altering our perception of how different oceanographic regimes
affect important top-down trophic interactions. The incorporation of the earlier post-
settlement stages into experiments and a greater understanding of the role of mobile
subtidal predators are crucial to the development of benthicpelagic models.
4.7. Key species and recovery from disturbance
Disturbance is a constant feature of nearshore rocky reefs and especially for intertidal
communities, which are subjected to waves, desiccation and, increasingly, human impacts
of various types. Following a disturbance, there is often a bloom of ephemeral algae, such
as Ulva, that may slow the development of longer-lived perennials (Sousa, 1979, 2001). In
some circumstances, facilitation may occur. For example, Farrell et al. (1991) found that
barnacles facilitated algal development in Oregon, but Foster et al. (2003) did not find this
to be the case at sites in central and northern California. Perceptions of crucial processes
may be both site and zone-dependent. For example, in the high intertidal zone, algal
abundance is a function of grazing and of the suitability for algal growth (Foster, 1982;
Cubit, 1984), but relatively little is known about variation in the latter for most places
(Foster et al., 2003).
Depending on resident communities and their location, there may be vastly different
responses to disturbance. For example, a recent study on the high shore at six sites along
the California coast used complete clearances in two seasons (spring and autumn) to
determine recovery relative to controls (Foster et al., 2003). The quick appearance of
ephemeral algae at two sites was associated with delayed recovery of perennial algae. At
two other sites, autumn clearances resulted in a different dominant alga (Mastocarpus
papillatus) than the spring clearings (Endocladia muricata). Slower recovery occurred in
the plots cleared in autumn but, nevertheless, five of the six plots recovered to control
conditions by the end of 6 years. Overall, the main differences between controls and
disturbed plots were in abundance and not composition of species. Foster et al. (2003) also
reported that the amount of bare space was high and concluded it was unlikely to be a
limiting resource for settlement. Although the number of grazers was high (>100 limpets
per 0.19 m
2
), peaking after 23 years, the importance of their role was lessened because
their abundance, combined with calculations of species-specific consumption rates, was
only weakly correlated with recovery. Recovery, therefore, varied among sites, between
seasons at some sites, and had no consistent relationship to latitude. They concluded that
their results were remarkably similar to those of Chapman and Underwood (1998) on
wave-exposed shores of New South Wales.
Recovery from episodic disturbances, however, can take many years, particularly if
they are large. When large-scale events such as El Nino affect widespread areas, there is a
relationship between the dispersal of propagules and spatial heterogeneity during the
recovery process. Reed et al. (2000) showed that in 27 sedentary marine species within
kelp forest communities, those with limited dispersal showed high variation among sites
but became more evenly spread over several years after severe disturbance whereas
species with long-range dispersal retained the same variability among years. These results
seem to reflect the proximity of disturbed areas to sources of propagules.
Underwood (1998, 1999) followed the recovery of a population of H. banksii after a
large disturbance from a severe storm and through a series of experiments. Virtually all
Hormosira plants were removed by a large storm in 1974, but the recovery process was
complex and the full original assemblage did not recover (Underwood, 1998). Recovery of
the Hormosira populations took up to 5 years, but this depended on the initial degree of
damage at each site. Underwood (1999) also showed experimentally that a series of direct
and indirect interactions affected recovery. Recovery was far quicker if only fronds and not
holdfasts were removed because plants could regenerate from fronds. Molluscan grazers
affected recovery, delaying it by around 9 months where holdfasts were left intact and for
up to several years where entire plants had been removed. Furthermore, there was a series
of indirect effects. The barnacle Chamaesipho tasmanica (Foster and Anderson) recruited
into areas where the Hormosira canopy was removed by the storm but there was also a
change in predator abundance and activity associated with this. Underwood (1999)
showed experimentally that whelks had little influence where the canopy of Hormosira
was sparse and furthermore that barnacles survived well under intact Hormosira canopies
when whelks were not present.
Several contrasts to other studies were noted by Underwood (1999). The whiplash
effects by dominant algae seen in many other studies (Dayton, 1971; Menge, 1976;
Santelices et al., 1980; Hawkins, 1983) did not occur. This may well be a consequence of
the unique buoyant, beaded form of H. banksii plants that tend to stay off the substratum
during submergence. Second, because the whelks rely on Hormosira for shelter, the
interaction of barnacles and whelks depended on the presence of the algal canopy, a form
of indirect interaction. Finally, there was also a modifying interaction (cf., Wootton, 1993,
1994) because the influence of whelks on barnacles was modified by the size and extent of
the algal canopy.
Experiments done on the same species in southern New Zealand showed similar slow
recovery of H. banksii after disturbance but through a quite different process (Schiel and
Taylor, 1999; Schiel, unpublished). No limpets or barnacles ever recruited into any of the
frond-removal or full clearances done quarterly at six sites over 2 years and followed for 5
years. The major grazing mollusc within the Hormosira beds, Turbo smaragdus Gmelin,
had an effect on reducing ephemeral algae such as Ulva and Adenocystis utricularis (Bory)
Skottsberg and the perennial articulated coralline Jania micrarthrodia Lamouroux, but
little or no effect on Hormosira (Walker, 1998), even though this grazer can affect
recruitment of fucoids in northern New Zealand (Creese, 1988). Recovery in cleared areas
was mediated almost entirely by recruitment processes of Hormosira, which occurred
more quickly in the lower portion of the Hormosira zone than in the upper portion.
On New Zealand shores, at least one of the major structuring factors for the mid-
intertidal assemblage is that H. banksii is the only perennial large brown algae capable of
forming large beds. Ultimately, therefore, patches cleared of this species are likely to be re-
occupied. This stands in contrast to studies such as Foster et al. (2003) that had several
species capable of dominance and where switches occurred after disturbance. In other
systems, such as the Pacific northwest, where space can be dominated by barnacles,
mussels and several species of algae, the structuring processes are bound to be more
complex.
These studies are only a few examples of many that illustrate complex pathways of
direct and indirect interactions intersecting with life histories. Even comparing the same
species (H. banksii) across nearby countries reveals different associated assemblages,
different interactive processes involving grazers and predators, considerable site-to-site
variation, and different pathways to recovery from disturbance, especially when they are
large or involve many species (Povey and Keough, 1991; Underwood, 1998, 1999; Schiel
and Taylor, 1999). As pointed out by others, predictability is not likely to be great unless
these complex pathways are clarified in detailed experimental analyses within particular
assemblages.
5. Conclusions
Searching for general principles that lead to predictive capacity in marine communities
is fraught with the difficulties of dealing with often unique assemblages, great site to site
variation in both composition and structuring processes, largely unknown life histories
(especially early life stages) of most species, inadequate knowledge of the interactions
with the nearshore water mass and the extent to which populations are open or closed (cf.,
Cowen et al., 2000). Nevertheless, progress towards understanding all facets of marine
benthic communities has never been so dramatic as in the past several years. Most aspects
of marine ecology have been reviewed recently and major, and often contentious, views
have been brought into sharp focus. I conclude here by offering a perspective on some of
these issues for future work.
5.1. The role of key species
On both conceptual and practical grounds, a better understanding is required of the
dynamics of key species, especially habitat-forming foundation species, and not just
keystone species. For many years, there has been an emphasis on trophic interactions and
the role of top predators (e.g., Paine, 1980) and the ways they may affect communities and
ecosystems (e.g., Paine, 2002) but in the absence of strong keystone interactions (c. f.,
Menge et al., 1994), the demographics and population dynamics of dominant space-
occupiers are of some importance. Bruno et al. (2003) highlighted the role of facilitation or
positive interactions in community structure. One of the most important distinctions they
made was between species that were primary and secondary holders of space. So, for
example, where algae or mussels are removed, the species that live on, under and among
them may disappear or be greatly reduced in abundance (e.g., Dayton, 1971, 1975;
Witman, 1985; Dean and Connell, 1987; Lohse, 1993). They provide modified models
relating to environmental stress and disturbance that incorporate the positive interactions
of species across gradients. Although the relative importance of positive interactions
compared to other processes in community structure has been questioned (Menge, 2000b;
Shouse, 2003), these interactions are undoubtedly important in many cases, particularly in
the more stressed habitats higher on the shore (Bertness et al., 1999; Bruno et al., 2003).
Marine algae in the low to mid-intertidal zone provide many examples of such key
foundation species (Bruno et al., 2003). Although not discussed in this context,
Underwood (1998, 1999) clearly showed that a fucoid alga (H. banksii) is such a species
in New South Wales. Its loss triggered a series of direct and indirect interactions in the
community. Also of interest was that even though there were strong interactions involving
barnacles, whelks and ephemeral algae, Hormosira returned to dominance within several
years. Presumably, despite all of the interactions, this species and others such as A.
nodosum (Jenkins et al., 1999) have a large pool of propagules, repeated reproduction, and
enough escapes from grazers to swamp areas and eventually to recover populations.
It seems likely that if such key species prove to be vulnerable to increased temperature
through climate change, there could be dramatic shifts in community structure. For
example, seaweeds have thermal limits for their survival, growth or reproduction (Van den
Hoek, 1982). Several studies have presented evidence of long-term changes in commu-
nities associated with seawater warming (Southward et al., 1995; Holbrook et al., 1997;
Sagarin et al., 1999). Schiel et al. (in press) showed that increased seawater temperature
from a thermal outfall in central California resulted in the virtual disappearance of
dominant red algae (Mazzaella spp.) and a replacement by low-lying turfs, ephemeral
algae and grazing gastropods. Understanding the structuring processes of these sorts of
species that in many cases do not seem to be restricted by strong trophic interactions will
be crucial.
These studies merely highlight the fact that while progress is dramatic, our knowledge
of important species in different parts of the marine ecosystem is quite narrow, that there
are important localised differences, and that interactions and their strengths will vary
among locations.
5.2. Algae vs. filter-feeders
What tips the balance between domination by filter-feeders and algae across shores? It
appears that one of the important dichotomies in perceptions about the importance of
various processes is in the roles and interactions of the two primary space occupiers, plants
and filter-feeding invertebrates. Within mussel beds, for example, mussels are competitive
dominants and predators play a key role in creating and maintaining primary space in
which other species can live (Paine, 1966, 1971; Dayton, 1971; Menge, 1976). Connolly
and Roughgarden (1998) suggest that higher algal abundances in northern California
compared to Oregon are because of competitive release from mussels, which do not recruit
well into these southern sites. In models derived from these and similar studies, therefore,
the major driver is whether or not competitively superior invertebrates recruit in sufficient
numbers. Foster et al. (2003), however, highlight the importance of understanding the
dynamics of the algal populations, especially their variation in demographic features of
dominant plants, their fecundity and reproduction and, presumably their ability to swamp
areas near adults with propagules. They point out that most of the intertidal zone
throughout much of the west coast of the USA is dominated by algae. Furthermore,
many species of algae are capable of living on and among filter-feeding invertebrates
(Lohse, 1993) and are therefore not excluded entirely. Foster et al. (2003) call biotic
variations that result from facilitative interactions and variations caused by consumers
small ripples on the large waves of variation caused by site-specific demographic
attributes of dominant marine plants.
Experiments within mussel beds show that patches within them are created and
maintained by physical disturbance and predation (e.g., Paine and Levin, 1981). Species
such as the sea palm Postelsia palmaeformis Ruprecht can establish within these patches
but are eventually excluded as mussels re-establish and outcompete them for primary
space (Paine, 1979, 1988). On many reefs dominated by algae, however, mussels do not
play a prominent role (Foster, 1990; but see Paine, 1991). Reciprocal transplant experi-
ments would help clarify the roles and capabilities of these dominant taxa in areas of their
abundance. If, for example, mussel domination is mediated by recruitment limitation (cf.,
Connolly and Roughgarden, 1998, 1999a,b), experimental placement of mussels within
algal beds should be able to test competitive interactions and establish under what
circumstances mussels or algae are competitively superior.
5.3. Early life history
The emphasis in marine ecology has clearly shifted to early life histories of coastal
species and the processes affecting dispersal, return to shore, settlement and recruitment.
There is considerable recognition of the importance of these processes and how they vary
among species (Dewreede and Klinger, 1988; Menge and Branch, 2001; Morgan, 2001;
Underwood and Keough, 2001) but many challenges lie ahead in understanding the
interactions with the nearshore water mass, the mechanisms of attachment in turbulent
coastal waters and survival to recruitment. Before models of dispersal and recruitment
mechanisms can be generalised, we will need a better understanding of a greater range of
species and habitats.
Experimental manipulations of different densities of the microscopic stages of habitat-
forming species have been a useful tool since the early days of experimental marine
ecology (Connell, 1961). Current hypotheses relating to facilitation (for example, by algal
canopies), the influence of gradients of environmental variables (for example, wave
exposure), disturbance and recovery in different habitats, and the role of density-
dependence in settlement are eminently testable using transplants of habitat-forming
species (e.g., Brawley and Johnson, 1993; Reed, 1990a) and should help complete the
loop from release of propagules to viable adult populations.
5.4. Effect of the nearshore water mass
Although processes such as upwelling and downwelling can affect larval transport to
shore (Connolly and Roughgarden, 1998), the relationships between oceanic conditions,
larval arrival and settlement processes are far from clear. Satellite images showing, for
example, warm water intrusions into the coast that coincide with settlement (e.g., Menge et
al., 1997a) are suggestive, but offer only a few points of a correlation of wide-ranging
processes. Questions arise: how often is high settlement of potentially long-range
dispersers such as barnacles and mussels associated with relaxation events in upwelling?
Conversely, how often are relaxation events associated with high settlement (i.e., how
good is the correlation between them)? How do the intensities of these different processes
relate to each other?
Achieving a greater understanding of oceanographic-onshore linkages is difficult and
will increasingly involve multi-disciplinary studies and more extensive use of remote
sensing. For example, improved algorithms and better satellite imagery will be a great aid in
achieving more accurate data on SSTand productivity. Murphy et al. (2001) point out some
of the problems of calibration that can arise in coastal waters, such as degraded signals,
validation of signals from (for example) chlorophyll vs. fine sediments in coastal waters,
and differences in signals in different water masses and different parts of the globe. It is also
clear that molecular techniques provide powerful tools to discern genetic structure,
dispersal and gene flow within and among populations (Grosberg and Cunningham,
2001). As pointed out by Palumbi et al. (2003), physical patterns do not always predict
biological connectivity and, because it is impractical to gather precise information for
thousands of species, it may be possible to test predictions from oceanographic models
using a range of species with different dispersal traits. Achieving this for a wider range of
taxa and oceanographic conditions will be a significant step in the process. Mapping results
from these sorts of studies onto oceanographic features, and the use of onshore experiments
at more replicate sites grouped within a greater range of factors (such as strong and weak
upwelling) will provide new insights into structuring processes of benthic communities.
5.5. Human impacts
Invasive alien species, pollution, urbanization, coastal development, and extraction of
species will be an increasing challenge to marine ecologists and managers (Ruiz et al.,
1999). Thompson et al. (2002) forecast for 25 years and discuss potential impacts and their
differences between industrialised and developing nations. They argue for strategic
research that integrates field experiments and monitoring programmes to verify manage-
ment regimes.
Not only is the problem of transporting species across borders, particularly through
shipping, of critical importance, but also our knowledge of how species take hold and
spread once they do arrive (Ruiz et al., 1999). Effects on native flora and fauna, human
impacts on benthic communities, and facilitative processes and trophic interactions are
all testable (e.g., Moreno et al., 1984; Castilla and Duran, 1985; Bruno and Bertness,
2001).
5.6. Cross country comparisons
Underwood (2000) called for (among other things) larger-scale analyses using careful
integration of the comparative-experimental approach at smaller scales nested within
larger scales, and to ensure that analyses at larger scales are commensurable with similar
studies in other places and habitats. Menge et al. (2002) have been at the forefront of such
experimental procedures . These sorts of experimental comparisons are fraught with
difficulties because of different species pools, variable oceanographic regimes, coastal
sedimentation, etc. (factors that operate at the local scale) but nevertheless are powerful
tools in working towards general principles of community dynamics. Given the great local
variation, site selection and replication within and between major sources of variation are
crucial.
The caveats for these sorts of studies are that we simply do not have enough knowledge
about more than a few species and their interactions with the complexities of the nearshore
water mass. Whether nutrients are actually limiting in nearshore waters, the degree of
availability of nutrients and phytoplankton because of thermal or freshwater stratification,
and the composition and abundance of the local species pool could all affect perceptions
about the importance of other mechanisms such as upwelling and downwelling (some of
these discussed in Menge and Branch, 2001; Menge et al., 2003).
Despite its problems and shortcomings, experimental marine ecology is not only
thriving but also playing a more prominent role than previously in ecological theory
and in addressing global problems. An awareness of increasing threats to the marine
environment presents a challenge to all of us: to grapple with the localised problems in
our own ecosystems (i.e., the back-yard issues that we all face); to do the broad-
ranging, underpinning science that leads to basic understanding of marine ecosystems;
and to help ensure that our science is useful and gets translated into management
policy.
Acknowledgements
Thanks to Tony Underwood for inviting me to write this review and for his many
insights, and to Sandra Shumway for her editorial work. I thank Mike Foster, Bruce
Menge and Steve Schroeter (not all of whom agreed with some sections of this review) for
stimulating discussion and detailed comments. Thanks also to numerous post-doctoral and
post-graduate students for their help and comments, especially Janelle Reynolds-Fleming,
Gil Rilov, Mike Hickford, Roly Russell, Spencer Wood and Dave Taylor. Preparation of
this paper was supported by grants from the New Zealand Foundation for Research,
Science and Technology and the Andrew W. Mellon Foundation of New York. I thank
them for their considerable support. Finally, my apologies to those whose excellent work I
did not cite. [SS]
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