AMER. ZOOL., 39:104-112 (1999)
Integration of Local and Regional Perspectives on the Species Richness of
Coral Assemblages'
RONALD H. KARLSON 2 AND HOWARD V. CORNELL
Department of Biological Sciences, University of Delaware, Newark, Delaware 19716
SYNOPSIS. We have evaluated the relationship between regional species richness
and the number of species occurring within local, quantitatively sampled assemblages of scleractinian corals. Our data have been extracted from the published
literature describing richness patterns from over 100 locations around the world.
In general, we find a positive relationship between local and regional richness.
Local richness is not independent of regional richness as posited by conventional
theory and there is no hard upper limit indicating saturation. Instead, local coral
assemblages are regionally enriched. This result suggests that these assemblages
are open to regional sources of species. The degree of regional enrichment is geographically variable. In the Indo-Pacific, assemblages in speciose regions appear
to be less open and much more sensitive to local depth and habitat gradients than
those in more depauperate regions. Other large-scale geographical and historical
effects on local richness in the Indo-Pacific include the degree of isolation from
high-diversity regions and distance from the equator. In contrast, local richness in
the relatively homogeneous and depauperate western Atlantic is insensitive to the
large-scale variables we examined. As in most ecological communities, membership
in local assemblages of corals is not absolutely limited (by biotic interactions or
local environmental factors) nor is it totally open to regional pools of species.
Understanding the dynamics of coral communities will require integrating the local
ecological perspective with large-scale phenomena {i.e., physical TECO processes
[Myers, 1994] and evolutionary history [Hugueny et al. 1997]). Such an integration
will necessarily encompass multiple spatial and temporal scales.
INTRODUCTION
in recent years, community ecologists
have begun to recognize the influence of
large-scale phenomena on the structure of
local communities {e.g., Ricklefs and
Schluter, 1993; Giller et al., 1994). These
comprise a wide variety of historical and
geographical factors including such things
as regional climate, geological disturbances,
unique speciation and extinction events,
oceanographic transport processes, atmospheric-oceanographic coupling, and even
orbital forcing of global climate. Traditional
notions regarding the structure of ecological
communities invoked local resource competition and niche diversification as central
paradigms. We are now faced with the chal-
1
From the Symposium Coral Reefs and Environ-
lenge of integrating the effects of these local factors with much larger scale processes
in order to
understand community structure
a n d
dynamics.
Expectations based on conventional theor
y i n c l u d e t h e Prediction from MacArthur
< 1 9 6 5 > t h a t t h e h i g h diversity exhibited by
man
y t a x a i n t h e t r o P l c s 1S d u e t o h a b l t a t
specialization (i.e., there are relatively large
differences in species composition among
habitats). Within habitats, species membershi
P w a s t h o u g h t t o b e restricted primarily
because of strong biological interactions,
habitat
stratification, and partitioning of
food
resources. Consequently, MacArthur
< 1 9 6 5 > predicted that tropical habitats are
saturated with species.
The notion that habitats are saturated
dates back at least to Elton (1933). Based
o n animal
s u r v e y s in similar habitats
in
mental Changes—Adaptation. Acclimation, or Extinc- q u j t e different places, he noted that the
(ton presented at the annual Meeting of the Society for n u m b e r o f
in one
ecies
co . O ccurring
Comparative and Integrative Biology, 3-7 January
i
.
r
1998, at Boston, Massachusetts.
place was far below the number occurring
2
E-mail: [email protected]
in the general area. Thus he suggested that
104
SPECIES RICHNESS OF CORAL ASSEMBLAGES
the species composition (i.e., membership)
within local assemblages is limited to relatively few species rather than being open to
all. Conventional theory predicts that limited membership is a consequence of biological interactions (competition and predation) and physical environmental factors
characteristic of the local habitat. This theory also predicts the following: 1) "local
diversity should be correlated with features
of the environment, especially the diversity
of resources," 2) "independently assembled communities in similar habitats on different continents (or in different oceans)
should contain similar numbers of species"
(i.e., convergence), and 3) local "diversity
within any habitat should reach a ceiling
that is independent of the number of species
in the regional pool" (Schluter and Ricklefs, 1993a). This last prediction describes
the quantitative relationship between local
and regional species richness and provides
the focus for our work on coral species
richness.
Species richness is the component of species diversity referring only to the number
of species. At very large spatiotemporal
scales, species richness describes biogeographical assemblages and is indicative of
the influence of evolutionary phenomena
and large-scale variation in the physical environment. We define regional richness for
corals as the number of species measured
over large geographical scales (102-104
km). At much smaller spatiotemporal
scales, species richness describes ecological
assemblages and is indicative of the effects
of biological interactions and the local
physical environment. We define local richness for corals at small spatial scales (10°—
103 m). At these scales, samples provide estimates of the within-habitat component of
species diversity. Although local richness is
sampled at one point in time, the recent history of the assemblage over the life span of
the resident organisms is reflected in such
samples. As recognized by Done (1999)
and many others, local richness in ecological assemblages is highly dynamic. By examining the relationship between local and
regional richness, we explore potential
cross-scale linkages between ecological and
biogeographical phenomena.
105
boundary
o
Type I
ic
"5
o
o
Type II
Regional Richness
FIG. 1. Two theoretical models for the relationship
between local and regional richness in ecological assemblages. In the Type I model (proportional sampling), local richness is independent of biotic interactions. The Type II model depicts saturation as local
richness reaches an upper limit and becomes independent of regional richness (from Cornell and Lawton,
1992).
The theoretical relationship between local and regional richness for a saturated local assemblage is depicted as a curve in
which local richness reaches an upper limit
and becomes independent of regional richness (Fig. 1; Cornell and Lawton, 1992).
This saturation or Type II model is contrasted with a Type I model in which local richness is independent of biotic interactions as
it increases proportionately with regional
richness. This pattern has been called "proportional sampling" by Cornell and Lawton
(1992). It is equivalent to earlier "pool enrichment" (Cornell, 1985) and "regional
enrichment" (Ricklefs, 1987) models. Real
assemblages are thought to fall between
these two theoretical extremes.
To date, empirical evidence supports the
conclusion that "unsaturated patterns are
common and widespread in natural communities" (Cornell and Karlson, 1997). The
majority of studies are consistent with the
proportional sampling model or provide evidence for a curvilinear relationship between local and regional richness, but not
saturation (Table 1). Early reports suggesting saturation among Caribbean birds (Terborgh and Faaborg, 1980; but see Wiens,
1989) and freshwater fishes (Tonn et ah.
106
R. H. KARLSON AND H. V. CORNELL
TABLE 1. Studies reporting sufficient local and regional richness values for regression analyses. A significant linear relationship is consistent with the Type
I model in Figure 1. Significant quadratic relationships indicate curvilinearity and possible saturation
when local richness levels off (after Cornell and Karlson, 1997).
three sources published between 1918 and
1993 reported the data as individual samples or as means of replicate samples collected in the same vicinity. These provided
1329 estimates of local richness from over
100 sites located throughout the Indo-Pacific and Atlantic Oceans (they are cited in
Linear relationship (Type I model)
Karlson and Cornell, 1998).
Cynipid wasps (Cornell, 1985); Bracken insects
These estimates were collected primarily
(Lawton, 1990); Parasitoid wasps (Dawah et al.,
1995; Gaston and Gauld, 1993); Freshwater fishes
using quadrat, line-transect, and point-inter(Griffiths, 1997; Hugueny and Paugy, 1995); Paracept techniques and sample sizes for each
sitic worms (Kennedy and Guegan, 1994); Mixed
were highly variable. We factored out vartaxa including vertebrates, insects, corals, and trees
iation
among methods and that due to sam(Caley and Schluter, 1997)
pling effort by first regressing the logarithm
Curvilinear relationship but not saturation
of local richness against the logarithm of
Caribbean birds (Ricklefs, 1987), Fig wasps (Hawsample size for each method separately
kins and Compton, 1992), Deep-sea gastropods
(these relationships are typically linear). We
(Stuart and Rex, 1994)
then
pooled the unexplained residuals from
Curvilinear relationship and saturation (Type II model)
these
regressions for further analysis. They
Fig wasp parasitoids (Hawkins and Compton, 1992);
were used as the dependent variable in a set
Banksia (Richardson et al., 1995); Parasitic worms
of simple and stepwise regressions exam(Aho, 1990; Aho and Bush, 1993; Kennedy and
Guegan, 1994)
ining the sensitivity of local richness to several independent variables (see below).
Our analysis of the quantitative relation1990) provided limited data unsuitable for ship between local and regional richness usregression analyses. More extensive data ing data pooled across methods indicates
from studies on fig wasps, Australian bank- that coral assemblages are not saturated
sias, and parasitic worms (see Table 1) in- (Cornell and Karlson, 1996; Karlson and
dicate saturation as local richness levels off Cornell, 1998, Table 2). Furthermore, we
with increasing regional richness (Cornell found no evidence for saturation when we
and Karlson, 1997). Among the quantitative analyzed quadrat, line-transect, and pointstudies to date, there are few which have intercept data separately (Cornell and Karlbeen conducted in marine environments and son, 1996). Local richness was most sennone of these provide evidence for satura- sitive to regional richness using data coltion. These include studies of deep-sea gas- lected from line transects and least sensitive
tropods (Stuart and Rex, 1994), several taxa using point-intercept data (Cornell and
of encrusting marine invertebrates (personal Karlson, 1996).
As an example of regional variation in
communication, J. D. Witman), fishes (Caley, 1997), and corals (Cornell and Karlson, local richness, we contrast the mean num1996, Caley and Schluter, 1997, Karlson ber of coral species observed along 10-m
line transects. In the Philippines and Indoand Cornell, 1998).
nesia, where regional richness has been esREGIONAL ENRICHMENT OF
timated to be at least 350 species (Best et
CORAL ASSEMBLAGES
al, 1989; Veron, 1993) or even higher
We conducted a survey of the published (over 450 species, Veron, 1995), the publiterature in search of quantitative estimates lished literature supports an estimate of
of the number of species occurring within 16.7 species per transect (from Sy et al,
local coral assemblages. Prior to 1970, such 1982; Moll, 1986). A comparable value for
quantitative studies were not common the relatively depauperate eastern Pacific
(Stoddart, 1969). We found over eighty (with only 19 species in the region) is 2.5
publications reporting local richness data, species per transect (from Porter, 1972;
but sampling methods were so variable that Glynn, 1976; Guzman and Cortds, 1989).
not all of these were useful to us. Sixty The mean across all regions in the Indo-
107
SPECIES RICHNESS OF CORAL ASSEMBLAGES
TABLE 2. Selected results for the slope of the relationship between log-transformed local richness against logtransformed regional richness (from Karlson and Cornell [1998f and unpublished analyses). Residuals (R)
were used as the dependent variable to account for variation due to multiple sampling methods (Q = quadrats,
L = line transects, P = points) and effort. IP indicates the Indo-Pacific.
Slope
(mean ± ISE)
Spatial scale
Global
Global
Global
Global
Global
Global
Global
IP
Atlantic
Depauperate IP
Speciose IP
Great Barrier Reef
Q, L2 and P', R
1-m quadrats
all small quadrats, R
all large quadrats, R
all quadrats, R
10-m line transects
all line transects, R
Q, L and P', R
Q, L and P1, R
Q, L and P', R
Q, L and P1, R
Q. L and P1, R
0.21
0.15
0.14
0.30
0.18
0.81
0.32
0.27
0.06
0.60
0.24
0.27
±
±
±
±
±
±
±
±
±
±
±
±
0.03***
0.09 n.s
0.04 n.s
0.04***
0.03***
0.04***
0.03***
0.04***
0.07 n.s
0.06***
0.05**
0.07*
r-tests: *** P < 0.00001, ** P < 0.00005, * P < 0.0005, n.s. = not significant.
Pacific and Atlantic Oceans is 8.5 species
per transect (Karlson and Cornell, unpublished data); the maximum is 33 species per
transect (from Moll, 1986).
This pattern of regional enrichment is
much less evident when local richness is
sampled at smaller local scales. Although
the coefficients of variation for local richness are similar at commonly used 10-m
and 1-m2 scales (80% and 73%, respectively), the slope of the simple regression between local and regional richness in the latter is not significantly different from zero
(Table 2). At this scale, the mean local richness globally is 3.2 species per quadrat
(Karlson and Cornell, unpublished data);
the maximum is 13 species per quadrat
(Connell, 1973; Grassle, 1973). Regional
enrichment was also not detected using
pooled data from all small quadrats (<6.7
m2), whereas it was quite significant when
local richness was estimated using larger
quadrats or line transects (Table 2). Thus
we speculate that local processes operating
at these larger spatial scales contribute to
regional enrichment and species coexistence by offsetting factors typically thought
to generate saturation (i.e., competitive exclusion and niche partitioning). Such processes may also operate at smaller spatial
scales, but are likely to be much more difficult to detect. After evaluating the putative
explanations for the generation of spatial
heterogeneity in local assemblages (re-
viewed in Cornell and Lawton, 1992), we
suggest that some combination of three processes may operate in coral assemblages.
These include small-scale disturbances and
predation (Connell etal, 1997; Sale, 1977),
neighborhood competition (Tilman, 1994;
Pacala, 1986a, b), and intraspecific aggregation (Shorrocks, 1990). We suggest that
these local phenomena operate in concert
with much larger scale processes to control
the magnitude of regional enrichment.
LOCAL AND REGIONAL INFLUENCES ON
LOCAL RICHNESS
Unlike the majority of studies examining
the relationship between local and regional
richness (see Table 1), our studies have explored the simultaneous influences of local
and regional variables on local species richness (see Schluter [1986] and Schluter and
Ricklefs [19936] for a comparable approach). We used depth (measured relative
to mean low water) and habitat categories
(ranked by relative distance from shore
through habitats in reef flat, crest, and slope
environments) as proxies for local environmental variation. Using stepwise regression
procedures, we found that regional species
richness and these two local variables each
accounted for approximately one third of
the explained variation in the regression
model (Table 3); the total explained variation (R2) was 37% (Cornell and Karlson,
1996). Therefore, the processes contribut-
108
R. H. KARLSON AND H. V. CORNELL
TABLE 3. Selected ANOVA results from stepwise regression analyses of local richness residuals vs. multiple
independent variables (from Cornell and Karlson [1996]' and Karlson and Cornell [1998]2). Only results from
the global scale of analysis are reported here. Q = Quadratic term.
Source of variation
Model I1
Depth
Regional species
Habitat, Q
Regional species, Q
Error
Total
Model IP
Depth
Regional species
Habitat, Q
Distance to nearest high-diversity region
Distance to equator
Regional genera
Regional species, Q
Error
Total
ss
df
4
336.55
905
7
556.60
903.15
362.95
898
905
540.20
903.15
90
MS
84.14**
125.38**
102.22**
100.92**
8.04*
0.63
51.85**
125.38**
98.92**
95.82**
24.91**
9.54*
7.79*
0.60 n.s.
0.60
F-tests: ** P < 0.0005, * P < 0.0001, n.s. = not significant.
ing to the regional enrichment of coral assemblages would appear to be at least as
important as those generating zonation patterns along depth or habitat gradients (e.g.,
see Huston, 1985). Nevertheless, two thirds
of the observed variation in local richness
was attributed to the local environment.
This argues for continued emphasis on local
processes as determinants of community
structure, but also indicates the need to integrate local and regional perspectives. The
regional species pool influencing local assemblages is directly controlled by speciation, extinction events, transport processes
influencing species dispersal, and the fragmentation of biogeographical assemblages
(Myers and Giller, 1989).
To explore the possible influence of multiple large-scale variables on the local richness of coral assemblages, we again used
stepwise regression analysis to screen
depth, habitat, regional species richness,
and five additional variables (the distance
to the nearest high-diversity region, distance to the equator, the number of genera
in a region, the average age of genera in a
region, and a simple contrast between the
Indo-Pacific and Atlantic provinces). In
spite of being highly intercorrelated, four
large-scale variables entered the multiple
regression model along with depth and hab-
itat (Karlson and Cornell, 1998). These included the two geographical variables for
the distances to the nearest high-diversity
region and to the equator as well as regional
richness in terms of numbers of species and
genera (Table 3). Although it is premature
to designate causal relationships between
local richness and the influences of regional
richness, location, regional climate, degree
of isolation, sea surface temperatures, etc.
(see Fraser and Currie, 1996), it is clear that
local community structure is sensitive to the
regional setting in which coral assemblages
occur. Thus we urge that comparative studies of local communities across regional
scales be conducted in order to explore the
cross-scale linkage between local and regional phenomena.
We also found that the sensitivity of local
richness to regional richness varied with the
geographical scale of our analysis (see
Done, [1999] for a comparable argument
stressing the need to understand the regional dynamics of coral communities). The inference that coral assemblages are regionally enriched (based on a "global" analysis
of data collected in both the Indo-Pacific
and Atlantic provinces) did not apply to all
coral assemblages (Karlson and Cornell,
1998). Significant enrichment was detected
throughout the Indo-Pacific province at
SPECIES RICHNESS OF CORAL ASSEMBLAGES
three different spatial scales (the entire
province, speciose vs. depauperate regions,
and the Great Barrier Reef), but was totally
absent in the Atlantic province (Table 2).
Enrichment was stronger in depauperate regions of the Indo-Pacific where local variables explained little of the variation in local richness (e.g., the eastern Pacific), and
weaker in the speciose, central Indo-Pacific
where assemblages appear to approach saturation. Most of the coral assemblages
which have been studied in the Atlantic
province occur in the relatively homogeneous Caribbean Sea where strong regional
gradients in species richness are not known
to occur. Thus detection of significant regional enrichment in the Atlantic was precluded. In addition, Atlantic assemblages
are probably not saturated. The mean local
richness in the Atlantic is nearly identical
with that in the Indo-Pacific (Karlson and
Cornell, 1998) and approximately half of
that described for more diverse sites in Indonesia and the Philippines (see above).
Along 10-m line transects, there were 9.5
± 0.4 and 8.2 ± 0.6 species (means ± 1SE,
t = 1.286, P > 0.05) in the Atlantic and
Indo-Pacific provinces, respectively. Furthermore, the regional richness in the Caribbean Sea was severely depleted following the closure of the Isthmus of Panama.
The present 50 species represents approximately 62% of the regional species richness
in the Caribbean 4 MYA and more than half
of the extant species originated 1-4 MYA
(see Budd et al., 1996).
INTEGRATION
The extreme perspectives of coral assemblages being completely closed or totally
open to all potential colonists have been
supported by recent arguments based on paleontological evidence, colonization studies, and modelling efforts. Here we briefly
summarize some of this evidence as we begin the integration of these divergent perspectives. On the one hand, niche-based explanations for community structure are emphasized as a consequence of Pleistocene
evidence for limited membership (Pandolfi,
1996, 1999). On the other hand, dispersalbased explanations for community structure
are supported by colonization studies sug-
109
gesting unlimited membership (Tomascik et
al., 1996) and a metacommunity theory
unifying island biogeography with local
community dynamics (Hubbell, 1997). Our
own analyses indicate the importance of
finding the "middle ground" (as suggested
by Roughgarden, 1989) where both dispersal and niche attributes of corals are integrated.
Pandolfi (1996, 1999) examined sequences of fossil corals on the Huon Peninsula of Papua New Guinea. Because of
tectonic uplifting and sea level changes,
nine distinct reef-building episodes spanning a 95-ky Pleistocene interval were represented by 122 coral species on a set of
raised terraces. While finding significant
differences in species composition and relative abundances of corals both within and
among reefs, there were no significant temporal differences. The same assemblages reformed at each site during repeated reefbuilding episodes. Using a theoretical colonization model, Pandolfi (1996) concluded
that the high temporal similarity exhibited
by these assemblages could not be explained by random colonization processes.
Membership in local assemblages appeared
to be restricted rather than totally open to
all. Furthermore, he invoked niche differences among species as an explanation for
this apparent limited membership.
Elsewhere in the speciose central IndoPacific, Tomascik et al. (1996) examined
the colonization by corals of a 5-year old
lava flow in the Banda Islands of Indonesia.
A total of 124 coral species colonized this
substrate including a diverse set of 45 Acropora spp. Over half of the Acropora spp.
were judged to be relatively uncommon in
Indonesian waters. Their presence in the
Banda Islands was attributed to transport
processes and immigration from the regional pool of available species. Thus at this
short temporal scale, the coral assemblage
appears to have had much less restricted
membership with respect to this genus compared to the fossil assemblages described
by Pandolfi (1996). Although Acropora is
the most speciose genus of scleractinian
corals with at least 150 species (Veron,
1995), many species are not well represented in the fossil record. Pandolfi (1996)
110
R. H. KARLSON AND H. V. CORNELL
reported only four. Given that limited membership results from niche differences (influencing colonization or post-colonization
responses to the local environment), perhaps many of the successful acroporid colonists in the Banda Islands will be excluded
at some time in the future. Alternatively,
the notion of limited membership may not
apply to this highly successful coral taxon.
Acropora spp. may be adapted primarily for
successful colonization under nonequilibrial
environmental conditions rather than to
more stable local environments. Veron
(1995) attributed their success to morphological attributes favoring rapid growth, a
diverse range of integrated architectures,
and fragmentation. "These characteristics
would be particularly advantageous during
times of climatic change, when sea levels,
wave turbulence, surface circulations and
inorganic nutrients are all in states of flux."
At the extreme, niche differences among
species may have little influence on local
community structure. Hubbell (1997) recently illustrated how species richness and
relative abundance patterns can be generated in ecological communities in a "perfectly homogeneous environment inhabited
by perfectly identical species . . .." Using
a theoretical model, realistic patterns of
community structure emerged in the complete absence of niche differentiation. Local
assemblages were linked together into "metacommunities" and dispersal across this
landscape determined the membership of
species at the local scale. Only "moderate
rates of dispersal" were sufficient to "ensure that these species are nearly everywhere nearly all the time." Thus dispersalbased explanations of community structure
may be just as valid as niche-based explanations, yet they can be extremely difficult
to falsify (Hubbell, 1997).
Again we emphasize the importance of
both niche-based attributes and dispersal
processes. "Real species are not identical,
and they have niches" (Hubbell, 1997).
Furthermore, dispersal is an extremely important aspect of the dynamics of populations and communities. In the marine realm,
we are only just beginning to examine dispersal models at regional scales {e.g., Roberts, 1997; Benzie, 1999). We suspect that
a full understanding of how both niche differences and dispersal control community
structure will require continued efforts to
integrate community ecology with systematics, biogeography, and paleontology (as
suggested by Ricklefs, 1987). The relative
influence of local and regional phenomena
on coral species richness and other community attributes are likely to vary among
regions in response to their unique histories,
regional landscapes, and transport mechanisms.
ACKNOWLEDGMENTS
We thank the organizers of this symposium, R. W. Buddemeier and H. R. Lasker,
and the SCOR Working Group 104 for this
opportunity to present our work on coral
richness patterns. In addition, we acknowledge the sponsorship and support of
LOICZ, the SICB, and financial support
from the Coastal Ocean Program of NOAA
and the University of Delaware. R. W. Buddemeier, M. J. Caley, and two anonymous
reviewers made helpful suggestions for improving the manuscript. During final revisions, the authors were funded by NSF
Grant No. INT-9724759 and ARC Grant
No. A19801508 with T. P. Hughes, M. J.
Caley, and C. C. Wallace.
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Corresponding Editor: Kirk Miller