Hydrobiologia 440: 3 7 4 4 , 2000.
M.B. Jones, J M.N. Azevedo, A.I. Nero, A.C. Costa & A.M. Frias Marti~ts(eds), Island, Ocean and Deep Sea Biology.
O 2000 Kluwer Academic Publislzers. Printed in the Netherlands.
Diversity, recruitment and competition on island shores at south-polar
localities compared with lower latitudes: encrusting community examples
David K. A. Barnes
Department of Zoology and Animal Ecology, University College Cork, Cork, Ireland
Key words: diversity, recruitment, spatial competition, intertidal, south-polar
Abstract
Comparisons of temperate and tropical shores have yielded considerable debate as to whether the former really are
less benign, diverse and structured by different ecological processes. Studies of comparable boulder communities have shown high within region variability. Equivalent polar assemblages, from island shores compared here,
show much reduced within region variability and considerably reduced numbers of phyla and species encrusting
boulders. The rate of colonisation (compared from settlement panel studies) was an order of magnitude higher in
warmer water, but did vary with isolation (near vs offshore islands). Comparison of the most ubiquitous taxon,
the bryozoans, between polar and non polar sites shows a decrease in the proportion of inter-specific competition,
indeterminate competitor (species) pairs and incidence of tied outcomes in competition. These three parameters all
increased with depth at the localities studied, whilst no obvious influence of isolation was found.
Introduction
In the last few decades, the investigation of latitudinal
trends into south-polar waters has changed from being largely theoretical to practical. Hypothesised lower
growth rates, greater longevity, reduced basal metabolic rates and lowered tempo of reproduction, with
respect to warm water (non-polar) ecological equivalents, have all been found to be generally true (Pearse
et al., 1991). Certain exceptions have been found.
Growth rates of a couple of south-polar sponges and
ascidians are as fast or faster than typical low-latitude
representatives of the same taxa (Dayton et al., 1974;
Rauschert, 1991). Thorson's rule (Mileikovsky, 197 I),
concerning the polar predominance of a suite of reproductive and larval characters, has proved true for
only few taxa (Stanwell-Smith et al., 1999 and refs
therein). The duration of phytoplankton abundance is
greater than previously believed, thus explaining the
findings of near year round activity of polar suspension feeders (Barnes & Clarke, 1995). Antarctic fauna
have long been considered very stenothermal and tests
on some organisms support this (e.g. Peck, 1989) but
others experience and tolerate regular fluctuations of
both temperature and salinity (Barnes et al., 1996).
There has been considerable debate as to the reason
for a general latitudinal cline in species diversity, most
recently whether it is explained by area (Rosenweig,
1995; Rhode, 1997). What appears certain is that the
pattern in the sea differs in the northern and southern
hemispheres as many Antarctic localities are highly
species rich (Clarke, 1992; Brey et al., 1994). Of
the sessile encrusting fauna, some can be relatively
species rich in south-polar waters (e.g. polychaetes
and bryozoans) whilst others are much more speciose in warmer waters (e.g. cnidarians, barnacles and
bivalves). A preliminary study by Barnes & Arnold
(1999) of encrusting boulder fauna on three polar island shores, suggested that south-polar assemEilage
diversity, growth, mortality and tempo of reproduction
may increase with latitude - all the converse of typical
patterns. '
Boulder communities have proved an important
testing ground for many ecological ideas, particularly those centred on the influences of disturbance.
Bolilders are characterised by being discrete (unlike
sediment samples), portable (unlike solid rock surfaces) and with a relative lack of variability. Of course,
as with any comparison of different sites, no two
boulder fields are identical, but problems of variance
in spatial heterogeneity can be minimised by selection
of substrata which are similar in size, wear (round-
ness) and smooothness. Of key significance to the
ecologist is that (within a region) disturbance is the
single most important factor determining faunal assemblage (Sousa, 1979; McGuiness, 1987). Typically,
disturbances create space by lethal or sublethal destruction of colonists, thus high frequencies reduce
diversity. At intermediate levels, however, disturbance
may prevent superior competitors from monopolising
resources (Connell, 1978; Huston, 1979).
Comparisons of temperate and tropical shores have
yielded considerable debate as to whether the former
really are less benign, diverse and structured by different ecological processes (Pianka, 1966; Moore, 1972;
Menge & Lubchenco, 1981; McGuiness, 1990). The
findings of high levels of variability within regions,
and differing results dependent on spatial scale examined, suggest that, overall, we do not have the data
to conclude that there are significant differences. The
wide geographical range of boulder community and
artificial simulation studies have, however, rarely includedpolar regions until recently (Barnes et al., 1996;
Barnes & Clarke, 1998; Barnes & Arnold, 1999).
The present study, using boulder substrata, conveys
advantages in comparing a similar habitat, over similar areas, using similar sampling design and over a
number of sites.
There have been few studies comparing foulinglencrusting taxa across latitudinal or isolation
gradients with similar sampling methodology and
more than one site at each latitude. Schoener et al.
(1978) and Barnes (1996) found that colonisation of
artificial panels was much faster at low latitudes, at
least in the early stages of community development. In
addition, species diversity was much higher at warm
water sites, although exceptions have been found
to both these trends - probably due to local conditions (Schoener & Schoener, 1981). Long & Rucker
(1970) and Hughes & Jackson (1992) compared near
and offshore sites, and Holmes et al. (1997) compared two sites at each of two latitudes. The present
study sought to examine how phyletic richness, species richness and the bryozoan (the most abundant
taxon) species richness at Antarctic and Subantarctic localities compared with other island study sites
around the world, with a consideration of isolation
and depth. In addition, this study investigated whether
rates of colonisation vary significantly: (1) between
broad latitudinal regions, and (2) with isolation by
comparing the data from four polar, nine temperate
and eight tropical studies. Finally, this study aimed-at
answering a number of questions concerning compet-
ition: are there relationships between latitude, depth
or isolation and the incidence of inter- vs intraspecific
competition of the outcomes of interspecific competition? If there are relationships, are they simple and do
they have an obvious biological interpretation? Quinn
(1982) considered that the differences he observed
between competiton in his temperate study and those
in tropical studies were due to differing taxa and more
specifically that a major taxon, the bryozoans, added
intransitivity to assemblage interactions. Here, interactions were studied and extracted from the literature
involving a single taxon, the bryozoans, common to
all studies.
Materials and methods
Study and literature sites
Intertidal and shallow subtidal zone encrusting species in boulder communities were compared between
sites on islands. Particular reference is made to bryozoans as the one taxon present (and abundant) at all
locations and studies. Boulder faunas examined during this study included southern hemisphere localities
of polar, subpolar, temperate and tropical latitudes
(Table 1). Various components of boulder fauna competition were investigated and calculated by drawing
up or interpreting existing contact matrices. A contact
matrix is a table in which various types of pair-wise interactions between different competitor identities can
be displayed. Such a matrix (Table 2) can represent
a subset or all competitors and is typically organised such that for each competitor pairing the number
of meetings, wins, losses and ties are apparent. A
matrix of meetings or interactions can thus be established for the suite of competitors at each site. From
each matrix (site), the proportions of inter- and intraspecific encounters, the proportions of tied outcomes,
indeterminate species pairs and competitive loops in
inter-specific encounters were calculated. Standoffs,
redirected growth on meeting or overgrowth by both
competitors, were recorded as tied outcomes (Russ,
1982; McKinney, 1992). Overall indeterminate species pairs refers to encounters by competitors such that
neither competitor won all encounters, so even if each
encounter produced a decided outcome one species
won some encounters, the second species, others. At
three locations, the above data were also recorded for
a variety of depths; 0 and 6 m (South Georgia), 0,
6, 12 and 25 m (Adelaide Is., Antarctica) and 0, 6,
Table 1. Islands investigated or previously studied in the Literature from which the data for this study were taken. The latitude,
longitude, ocean and near or offshore status are shown together with the reference material
Study islands
Antarctic
Subantarctic
Southern
temperate
Tropical
Latitude and
longitude
NearIOffshore & Reference
Ocean
Adelaide
Gellindez
Dobrowlski
Signy
Coronation
South Georgia
Bird
Falkland
Tierra del Fuego
Near, Southern
Near, Southern
Near, Southern
Off, Southern
Off, Southern
Off, South Atlantic
Off, South Atlantic
Off, South Atlantic
Near, South Atlantic
(Barnes & Arnold, 1999)
@This study
@This study
+Barnes & Rothery (1996)
@This study
*Barnes & Arnold
@This study
@This study
@This study
South
Inhaca
Long Reef
Lord Howe
Solitary
Heron
Green
Quirimba
Sencar
Bali
Galapagos
Off, South Pacific
Near, Indian
Near, South Pacific
Off, South Pacific
Near, South Pacific
Off, Pacific
Off, Pacific
Near, Indian
Near, Indian
Off, Indian
Off Pacific
@Gordon (1980)
@This study
#McGuinness & Underwood (1986)
OHolmes et al. (1997)
OHolmes et al. (1997)
ORyland (1974)
OHolrnes et al. (1997)
@This study
@This study
RWinston & Heimberg (1986)
THastings (1930)
12, 25, 32, 42 and 50 m (Signy Is., Antarctica). As
well as species richness, diversity of assemblages was
compared by counting the number of different species
pairs meeting in inter-specific competition for each
site.
Results and discussion
Species and interaction richness
The number of encrusting/sessile phyla present (occupying > 1% of space) on boulders decreased towards
the south-polar sites whilst there was little, if any,
difference between tropical and temperate sites (Figure la). Typically, in non-polar water, 3-6 phyla were
present on boulders while only two (polychaetes and
bryozoans) were present at the high latitude sites. The
total number of species at each site is shown in Figure l b and the total number of bryozoans in Figure lc.
Both plots show the number of species increased
with decreasing latitude (i.e. towards the tropics from
south-polar shores). The highest points were in the
mid-latitude temperate or subArctic localities. The
most striking difference with latitude was the comparative lack of variability (in numbers of phylafspecies
per site) in south-polar sites. There was considerable
variation between sites at comparable latitudes - indicating the importance of local conditions (Schoener
& Schoenern, 1981; McGuiness, 1990). At higher latitudes, ice scour (scraping of substratum by floating
ice) severely reduces shallow-water colonisation and
species richness (Barnes,'1999). Below the level of ice
scour, Antarctic benthic diversity may reach generally
high values (White, 1984; Arntz et al., 1997). Whilst
there are various agents of disturbance (e.g. storms,
floods and bioturbators) at non-polar localities causing
a wide range of impact levels (McGuiness, 1990), very
few rank alongside the magnitude of that caused by ice
(Gutt & Starmans, in press).
There was no obvious correlation between the
level of site isolation and species richness. Mainland, near- and off-shore island sites showed similar
patterns (Fig. la, b, c), although this is partly due
to a lack of studies of both island categories at certain latitudes. Whilst some workers (e.g. Long &
Table 2. Contact matrix of five competititor identities (at Dobrowlski Island, Antarctica). The
values in each cell are: number of tied outcomes between competitors A and B (top-left),
top-right (wins by B [= losses by A]) and bottom-left (wins by A [= losses by B]). Value
in bonom-right of each cell = total number of observed interactions for that competitor-pair.
The proportion of interspecific competition for this matrix is (9+3+11+2+5+6+3+6+1)/
(9+3+11+2+5+6+3+6+1+5+6+46) = 44.7%. The proportion of indeterminate species pairs is
217 = 28.6% (I. nutrix vs M. brevissima and F: rugula vs C. bougainvillei. The proportion of tied
outcomes is (1+1)/(9+3+11+2+5+6+3+6+1)= 4.3%. Three competitor pairs do not meet (M.
brevissima vs M. brevissima, Spirorbis sp. vs Spirorbis sp. and Spirorbis sp. vs C. bougainvillei
2
:
2
.-
r
.-
.g
w
.?3
t:
2
Li
A
Ci
1
1
9 3
3 11
1 0
Inversiula nutrix
5 5
4
Celleporella bougainvillei 2
0 0
5 6
4
1
0
Li
7
Micropora brevissima
.'1
'2
C
0
a
L:
%
2
%
0
2
6
1
3
46
Fenestrulina rugula 0
e
.-
0
11 2
0 0
6 3
2
6
0 0
1
46
Spirorbis sp.
Rucker, 1970; Holmes et al., 1997) have found reduced shallow marine benthic diversity on offshore
islands compared with comparable latitude near shore
islands, others (e.g. Dinesen, 1983; Hughes & Jackson, 1992) found the converse. Variations in many
factors, such as proximity of breeding adults (larval
supply), current conditions, water quality and smallscale parameters may mask or even reverse patterns
between near and offshore sites. There was also no
apparent relationship between island size and number
of taxa found (in samples) as might be predicted by
standard island biogeography models (MacArthur &
Wilson, 1967).
The number of different competitor (species) pairs
meeting in interspecific competition followed similar
patterns to those of species richness. The two highest
values (of number of different competitor pairings)
were the same siteslstudies exhibiting the peaks in species richness (plot not shown). The top values were
all from the Subantarctic or temperate regions, with
a decline to both tropical and polar regions. A large
number of different species interaction pairs at a site
not only demonstrates the presence of many species,
but a degree of evenness such that so many different
competitors meet. This could be further used as qQantifying evenness in competition by modifying diversity
8
I
2
0
3
0
1
I
indices to evaluate the spread of interactions between
competitors (compared to more usually measuring the
spread of different species present).
Colonisation and recruitrnenl
Experiments involving artificial panels (of similar
size and material) have been conducted at localities
spanning most latitudes. Although some studies have
shown initial rates (<6 months) of colonisation and
species diversity were higher at tropical than temperate sites, the majority have found little difference
after 10 months (Schoener et al., 1978). Recent panel
studies in Antarctic waters have shown that both colonisation rates and species richness may be nearly two
orders of magnitude lower than in warm water experiments (Dayton, 1989; Barnes, 1996; Stanwell-Smith
& Barnes, 1997). Variation in panel colonisation in excess of an order of magnitude is dependant on oceanic
conditions (Winston & Jackson, 1984), light conditions (Nandakumar, 1995), depth (Barnes, 1996),
isolation (Holmes et al., 1997) and sedimentation rates
(Maughan & Barnes, unpublished data). Annual or
even super-annual variability in recruitment onto artificial panels may be substantial both in non-polar
(Kendall et al., 1985) and polar environments (Dayton,
1989).
Table 3. Monthly colonisation, expressed as % cover,
of shallow-water panels in coastal or offshore studies. Data are calculated for mean cover after initial 6
months deployment, from the following literature; Sutherland & Karlson (1977), Schoener & Schoener (1981),
Jackson & Winston (1982), Dayton (1989), Rauschert
(1991), Barnes (1996) and references therein, Holmes
et al. (1997), Stanwell-Smith & Barnes (1997), Hextall (unpublished data). Values are presented as means f
Standard error with sample size
Region
Coastahear shore
Offshore
Antarctic
Temperate
Tropical
0.05 (0.05) n = 2
10.9 (1.7) n = 6
9.9 (2.1) n = 5
0.17 (0.05) n = 2
4.6 (1.9) n = 3
3.3 (1.6) n = 3
nual variability and physical environmental variables,
means such a finding must be treated with caution.
Competition
Latitude f' South)
Figure I . Number of sessile phyla (a), subtidal encrusting species
(b), and subtidal bryozoan species (c) with latitude south. The symbols are mainland (0).
near-shore islands (I))and off-shore islands
( 8 ) Data
.
are from the present study and taken from the literature
(see Table 1).
Monthly rates of panel colonisation (Table 3), calculated from the literature, show lower rates at polar
than warmer latitudes, despite the many complicating factors, but no significant difference was found
between temperate and tropical levels. Both temperate and tropical levels of recruitment halved from
coastal to isolated sites, whilst, curiously, polar levels
doubled. The small number of polar studies carried
out, and the potential confounding factors of an-
The data suggest that the itensity of interspecific interactions decreases towards the pole in the southern
hemisphere sites (Fig. 2A) and thus the level of intraspecific competition must proportionally increase.
This result is consistent with, and must be partly
caused by, the reduction in numbers of encrusting
species with latitude (Fig. lb). The proportion of
interspecific interactions increased with depth from
the intertidal zone to 50 m, although virtually all of
this increase occurred over the depth range 0-12 m
(Fig. 3A). There is a suggestion of a increase in the
proportion of determinate species pairings (in which
one competitor wins all encounters against another
competitor species). Typical proportions of determinate species pairings in warm waters were 70% compared to around 30% in polar waters (Fig. 2B). The
proportion of tied outcomes also decreased with latitude (Fig. 3C). As any tied outcomes between a pair of
species competing makes such a pairing indeterminate, any trend in tied outcomes must influence any pattern of determinate species pairings with latitude. The
trend of increased determinate species pairs (Fig. 3B)
and tied outcomes (Fig. 3C) with depth followed a
similar pattern to that of the increased prevalence of
interspecific competition (Fig. 3A). There appears to
be little or no influence of isolation, but this may need
more studies at comparable latitudes such as that of
Holmes et al. (1997).
Jackson (1979) suggested that increasing the number of taxa should increase the number of methods
Latitude ( 'south )
Figure 2. Proportion of inter-specific competition (c.f. intra-specific
competition), proportion of indeterminate species pairs and proportion of tied outcomes (in inter-specific competition) with latitude
South. The symbols are near-shore islands ( a ) and off-shore islands
(#). Data are calculated as shown in Table 2, and values are from
the present study and taken from the literature (see Table 1).
of interaction and, therefore, increase the probability
of varied outcomes (so indeterminate species pairs)
and competitive loops. However, virtually all studies
have found interphyletic interactions to be predictably
ranked in which ascidians > sponges > ctenostomatid
bryozoans > cheilostomatid bryozoans > cyclostomatid bryozoans > polychaetes, barnacles and hydroids (Russ, 1982; Quinn, 1982). Although only few
taxa were involved in competitive interactions on polar
boulders, the data analysed here suggest that, as with
warmer water assemblages, a ranking of sponges >
Figure 3. Proportion of inter-specific competition (c.f. intra-specific
competition), proportion of indeterminate species pairs and proportion of tied outcomes (in inter-specific competition) with depth (m).
The symbols are South Georgia ( O ) ,Signy Island (#) and Adelaide
Island ( a ) . Data calculated from contact matrices (e.g. Table 2)
from the present study and Barnes & Rothery (1996).
cheilostomatid bryozoans > cyclostomatid bryozoans
> polychaetes.
Conclusions
The polar data collected, and temperateltropical data
analysed here, suggest a number of trends in encrusting communities, more specifically the bryozoan
component, with latitude and depth but not obviously isolation. Species richness and colonisation
rates follow approximately parabolic relationships in
southern hemisphere assemblages, though possibly
with highest points at high temperatelsubpolar latitudes in the former. Also, in southern hemisphere
assemblages, intraspecific competition becomes more
prevalent with increasing latitude and less with depth.
There are suggestions of distinct changes in the ecological structure of competition with latitude in the
southern hemisphere, that is the outcomes of interactions between competitor pairs alters (the proportion
of tied interactions and indeterminate species pairs
both increase).
Potentially, the three factors have similar paths
of influence as, typically, the number of species increases towards the tropics and with depth (within the
context of the studies here), and decreases with isolation. Patterns of species richness have, in the case
of bryozoans, been shown to be questionable along
both latitudinal (Clarke, 1992) and isolation gradients
(Hughes & Jackson, 1992). Another potential common link for a modus operandi of latitude, isolation
and depth on the workings of encrusting communities is via disturbance. There was no evidence of the
high within region variability, characteristic of the
temperate and tropical regions (McGuiness, 1990), in
the south-polar sites studied. This is probably due to
the high variation in exposure of warm-water shores
whereas even the most sheltered south-polar shores
are highly disturbed by ice scour. Water-born disturbance, probably in terms of wave action (trans-global
fetch), but definitely in terms of ice scour, increases
with latitude and isolation but decreases with depth
(Barnes, 1999). So, increased levels andlor frequency
of disturbance may be important for generation and
maintenance of species diversity at high latitudes and
very shallow depths. An obvious question raised by
this study is whether patterns in the southern and
northern hemispheres are different? Whilst diversity
patterns are believed to be different (Clarke, 1992;
Rosenweig, 1995), colonisation and recruitment rates
may be very similar (Barnes, 1999). Many studies of
competition in boulder assemblages have been carried
out in the northern hemisphere, but there are few data
from the Arctic. Arctic patterns might be expected to
be different from the Antarctic findings for a number
of geographical, bathymetric and historical reasons.
Land surrounded by ocean would clearly be subject
to very different influences than ocean surrounded by
land (such as freshwater runoff). The proportion of
continental shelf is much greater in Antarctica, most
of the Arctic is deep and Antarctica is much older, so
patterns of invasion and speciation have had longer to
proceed
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