Download The relationship between local and regional species richness in

Journal of Animal
Ecology 2000,
69, 1111±1116
FORUM
The relationship between local and regional species
richness in birds of the Caribbean Basin
ROBERT E. RICKLEFS
Department of Biology, University of Missouri-St. Louis, 8001 Natural Bridge Road, St. Louis, Missouri
63121±4499, USA
Srivastava (1999) recently evaluated the relationship
between local and regional species richness as a tool
for determining whether local assemblages of organisms are ecologically saturated or open to invasion.
Srivastava also pointed out several pitfalls of sampling and interpretation in such studies. One problem arises when regional species pools are
estimated by summing species richness over habitats
(Method 1). In this case, the regional pool includes
species that may not be capable of living in a particular local community and the species pool is thus
overestimated. Terborgh & Faaborg (1980), Ricklefs
(1987), and Wiens (1989) used this approach to analyse local and regional richness in the avifauna of
the West Indies, where each island was considered a
separate region. The local±regional tests in those
studies correspond to Srivastava's Method 3, which
relates diversity in `identical habitats in geographically di€erent regions' to the regional species pools.
One may nonetheless object to these analyses
because regional species richness was estimated by
summing over habitats within islands and because
individual islands within an archipelago are not statistically independent, i.e. `regional', samples. The
problem is largely one of scale.
Loreau (2000) has pointed out that the relationship between local and regional species richness
depends on the scale at which each is measured.
Thus, when the concepts of `local' and `regional' are
similar, for example in terms of habitat breadth, a
large proportion of the regional heterogeneity is
sampled within each locality and local diversity
tends to vary in proportion to regional diversity.
This gives the appearance of non-saturation (Cornell
& Lawton 1992; Caley & Schluter 1997). When a
narrower concept of `local' is applied, local diversity
is relatively independent of regional diversity and
the appearance of saturation is a more likely outcome. In Pearson's (1977) study of birds in tropical
forests in six regions, concepts of `local' and `regional' did not di€er greatly with respect to habitat
breadth. Consequently, local communities contained
# 2000 British
Ecological Society
Correspondence: Dr R.E. Ricklefs, Department of
Biology, University of Missouri-St. Louis, 8001 Natural
Bridge Road, St. Louis, Missouri 63121±4499, USA.
60±80% of the regional species richness and local
species richness increased roughly in proportion to
regional species richness. The West Indian analyses
mentioned above adopted a relatively broader concept of `region', and local communities contained
only 20±60% of the regional species richness, as
reported in detail below.
Here I would like to address the problems of estimating regional species pools and establishing the
independence of these pools, and to comment more
generally on the practice of regarding local±regional
diversity relationships as either showing saturation
or not.
Data
The data reported by Ricklefs (1987) and subsequently analysed by Schluter & Ricklefs (1993) were
obtained by George Cox (Cox & Ricklefs 1977) and
Joseph Wunderle (Wunderle 1985) on several islands
(Jamaica, St. Kitts, St. Lucia, Grenada [JW], and
Tobago [JW]) and within two continental areas
(Trinidad and central Panama) in the Caribbean
Basin. (Trinidad was connected to the mainland of
South America during Pleistocene sea level lows and
has a continental avifauna.) The data are similar to,
but independent of, observations used by Terborg &
Faaborg (1980) in their seminal appraisal of the
local±regional species richness relationship. Cox and
Wunderle censused birds during ten 20-minute point
counts in each of nine matched habitats in each of
the islands or continental areas. Local species richness (L) is the average of the number of species
observed in each of the nine habitats in a single
island or area. Regional species richness (R) is the
number of species observed in all habitats together
(Robs) or the number of species known to occur in
the region (island or continental area) whether
observed during point-count sampling or not
(Rtotal). Ricklefs (1987) portrayed species richness
for several habitats as a function of the observed
regional species richness for the seven regions. As
Srivastava pointed out, the regional pool for any
given habitat may be overestimated because each
species in the regional pool may not be capable of
living in each of the habitats. Furthermore, if overestimation of the regional pool were to vary in a sys-
1112
Local and
regional species
richness
tematic way with respect to regional species richness,
this would lead to a bias in the relationship between
local and regional richness. It is generally true that
more diverse regions have a higher proportion of
habitat specialists. Therefore, the regional richness
that is relevant to a particular habitat is exaggerated
compared to less diverse regions. This tends to
stretch out the scale of regional diversity towards its
higher end and bias the local±regional diversity analysis in favour of ®nding a curvilinear relationship,
which Srivastava (1999), taking the `majority view',
would accept as evidence for saturation (also see
Griths 1999).
The local±regional regression
# 2000 British
Ecological Society
Journal of Animal
Ecology, 69,
1111±1116
Because regional richness estimated by summing
over habitats is likely to err in favour of supporting
saturation, it provides a conservative evaluation of
regional e€ects on local diversity. More importantly,
because both local and regional factors can in¯uence
local diversity, the degree of curvilinearity in the
local±regional relationship can reveal their relative
contributions. Saturation is not an either/or phenomenon. Rather, local community interactions balance the tendency of regional richness to contribute
to local richness through dispersal and habitat
expansion, with increasing resistance as local diversity increases.
Schluter & Ricklefs (1993) reported that the slope
of the logarithmic relationship between local and
regional diversity based on the Cox/Wunderle data
was 05 (see their Fig. 14). That is, both alpha
(local) diversity and beta diversity (turnover between
habitats) increased as the square root of regional
species richness. In that analysis, local species richness (L) was the average species richness in each of
the nine habitats on a particular island or within a
particular mainland region. Regional richness was
the observed number of species (Robs, or simply R).
Rtotal includes birds not seen in the point counts but
known to occur in the region and therefore overestimates the species pool for poorly sampled local
areas when local diversity is estimated from point
counts. This bias increases with increasing regional
diversity because average species abundance declines
and many species are missed locally. To minimize
this bias, all the regressions reported here are based
on Robs.
The linear regression, L ˆ a ‡ bR, was signi®cant
(F1,5 ˆ 765, P ˆ 00003, r2 ˆ 0939); however, adding
a quadratic term to obtain L ˆ a ‡ bR ‡ cR2 signi®cantly increased the goodness-of-®t (F2,4 ˆ 4444, P
ˆ 00001, r2 ˆ 0996). This suggests a curvilinear
relationship between local and regional species richness. The quadratic regression statistics (a ˆ 505 ‹
091, b ˆ 0372 ‹ 0031, c ˆ ÿ 000138 ‹ 000019)
indicate a peak local richness at R ˆ 1348 species,
that is, at the highest regional richness observed in
the study (Panama, R ˆ 135 species). Thus, local
richness increases monotonically through the range
of regional richness observed in the study. Accordingly, a power function, L ˆ aRb, should provide an
appropriate description of the relationship. The linear form of this regression, logL ˆ loga ‡ blogR,
was signi®cant (F1,5 ˆ 2572, P ˆ 00001, r2 ˆ 0981)
and the slope of the regression (b ˆ 0497 ‹ 0031)
suggests that local diversity increases as the square
root of regional diversity in this sample. The power
function also can be ®t by non-linear regression to
untransformed data, in which case the resulting
coecients were a ˆ 312 ‹ 042 and b ˆ 0470 ‹
0031 (r2 ˆ 0985).
The relationship between L and R was also
described well by several asymptotic equations. For
the logistic equation, L ˆ a/{1 ‡ exp[± b(R ± c)]}, the
regression coecients were a ˆ 3076 ‹ 060, b ˆ
00367 ‹ 00031, and c ˆ 3198 ‹ 140 (r2 ˆ 0994).
For the exponential equation, L ˆ a[1 ÿ bexp(± cR)],
the regression coecients were a ˆ 3360 ‹ 147, b ˆ
0911 ‹ 0044, and c ˆ 00167 ‹ 00025 (r2 ˆ 0994).
Both equations suggest an asymptotic local species
richness of 31±34 species, which is approached only
in the regions with the highest regional diversity:
Panama and Trinidad (Fig. 1).
Two points are evident.
1. The rate of increase in local species richness
decreases as regional species richness increases. This
could result in part from overestimation of the
regional species pool in regions with higher species
richness. If this were not an important problem, the
regressions would be consistent with the hypothesis
that more diverse assemblages of species are more
dicult to invade than are less diverse assemblages.
It would also be consistent with the hypothesis that
more diverse species pools contain more habitat specialists with limited capacity to live in other habitats. Whether local species richness actually levels
o€ at a `saturation' level is dicult to determine.
The non-asymptotic power function ®ts the data
almost as well as asymptotic logistic and exponential
functions. If the relationship did level o€, however,
this would occur only at the highest diversities
observed in the study.
2. Through most of the range of regional species
richness in this data set, increase in regional richness
is accompanied by an increase in local species richness. Thus, local assemblages evidently are open to
invasion by additional species at least up to the
maximum diversity observed in this study, even
though there is also evidence of increasing resistance
to invasion.
Independence of samples and the problem of
pseudoreplication.
A potential problem with statistical appraisal of patterns within a single large area, such as the Carib-
1113
R.E. Ricklefs
Fig. 1. (a) Relationship between average local within-habitat species richness and the regional species pool ®t by linear,
quadratic, logistic, and exponential functions. The last three are asymptotic or reach a maximum and ®t the data equally
well. (b) Logarithmic relationship ®t to the same data with slope 050.
bean Basin, is lack of independence of the data (Srivastava 1999). For example, the avifauna of St.
Kitts is largely a subset of the birds of St. Lucia,
and Grenada shares many of its species with
Tobago and Trinidad. Two considerations suggest
that the distributions of birds among habitats within
each of the regions are, for the most part, independent. First, many geographically separated populations of the same species within the Caribbean Basin
exhibit strong genetic divergence, indicating long
periods of evolutionary independence (Seutin et al.
1993; Klein & Brown 1994; Seutin et al. 1994; Lovette et al. 1998; Lovette, Bermingham & Ricklefs
1999; Ricklefs & Bermingham 1999). Secondly,
increase in habitat breadth (ecological release) of
colonists to the Lesser Antilles from Trinidad and
northern South America appears to occur rapidly
(Wunderle 1985) and is apparent even in island
populations lacking genetic di€erentiation in
mtDNA sequences from mainland source populations (Ricklefs & Bermingham 1999). Therefore,
habitat distribution and local species richness could
achieve independent local equilibria within each of
the regions.
Estimating regional diversity by summing over
habitats
# 2000 British
Ecological Society
Journal of Animal
Ecology, 69,
1111±1116
Within a region, species replacement occurs with
respect to habitat and to distance within habitat
(Cody 1993). Replacement within habitat presumably re¯ects subtle changes in environment, competitive exclusion by closely related taxa, and limits to
dispersal over long distances. To what extent should
variation between and within habitats be incorporated into the estimate of regional diversity against
which a particular sample of local diversity is measured? Srivastava (1999) suggests that because many
specialists cannot live in alternative habitats, summing across habitats provide an inappropriate estimate of regional diversity. Members of a regional
species pool can be absent from a particular local
community for many reasons. These include adaptation barriers imposed by habitat specialization, but
also similar barriers raised by environmental variation within habitats (which, after all, are subjective
distinctions) and barriers to dispersal over distance
within habitats. Two points argue for including variation across habitats in the concept of `region.'
First, habitat specialization is ¯exible and responds
to the intensity of competitive interactions among
species. This is particularly evident on islands in the
West Indies where species on depauperate islands
exhibit substantial ecological release by increasing
the number of occupied habitats (see Table 1). Secondly, adjustments of species within a regional pool
include evolutionary responses that potentially
would permit most species access to most habitats.
Comparative analyses show that most of the variation in range size (Gaston 1998) and habitat distribution (Ricklefs, unpublished) within large
taxonomic groups occurs at the level of species
within genera, that is, over relatively short evolutionary time frames. Thus, to the extent that the
sorting of local communities out of a regional pool
includes an evolutionary component, summing over
habitats is appropriate.
Area of regions
Srivastava (1999, p.10) points out that `the ability of
each species in the region to invade a given local
1114
Local and
regional species
richness
Table 1. Species abundance, habitat distributions, local species richness, and the `regional' pools of birds of the Caribbean
basin
`Region'
(2)
Total
regional
pool (Rtotal)
(3)
Observed
regional
pool (Robs)
(4)
Species
per habitat
(L)
(5)
Local
abundance
per species
(6)
Total
abundance
per habitat
(7)
Habitats
per
species
(8)
Regional
abundance
per species
(9)
Regional
abundance
of avifauna
St. Kitts
Grenada
St. Lucia
Tobago
Jamaica
Trinidad
Panama
21
34
40
64
68
186
296
20
30
34
53
55
108
135
119
155
153
214
213
288
302
59
54
57
48
49
32
29
699
842
879
1018
1038
934
887
54
47
41
36
35
24
20
315
253
233
173
170
78
59
629
758
791
916
934
841
798
(1)
Note: Columns (2) (3) (4) and (5) observed directly; (6) ˆ (4)x(5); (7) ˆ 9x(4)/(3); (8) ˆ (5)x(7); (9) ˆ (3)x(8).
community will be a decreasing function of the distance it must disperse.' Accordingly, summing species over area may overestimate the regional pool.
This raises important issues concerning how we
de®ne `region' and the temporal and spatial scales
we apply to our de®nition of region. For birds on
islands in the West Indies, however, distance is
probably not a problem. Distances within islands
are on the scale of kilometres or tens of kilometres,
which are less than the distances that individuals
crossed to colonize the islands.
Source±sink relationships
# 2000 British
Ecological Society
Journal of Animal
Ecology, 69,
1111±1116
A potential bias in the local±regional relationship
not mentioned by Srivastava (1999) could arise from
diversity-dependent di€erences in source±sink relationships. Under the saturation hypothesis, according to which local diversity is regulated by
interactions among species, the number of species in
a habitat may be further augmented by movement
of individuals from adjacent habitats, thereby establishing source±sink relationships (Pulliam 1988; Stevens 1989). If this were true, diversity within
habitats could be closer to the local saturation point
on islands than at mainland sites where diversity
could be maintained locally above saturation by
movement of individuals between source and sink
populations. This would shift the local±regional
regression to resemble proportional sampling more
closely than it would saturation. This bias seems
unlikely, however, inasmuch as species in continental regions have narrower rather than wider habitat
distributions. Individual species also exhibit lower
population densities on continents (Fig. 2), and perhaps less intimate juxtaposition of varied habitat
types, which weighs further against a role for source
populations maintaining diversity in sink areas.
Indeed, it is equally plausible that movement of
individuals between habitats augments local diversity on small islands given the higher average popu-
Fig. 2. Decrease in habitat breadth and local abundance
of speccies with increasing species richness of the regional
pool.
lation densities and frequent proximity of many
habitats within small areas.
Discussion
Rather than asking whether local communities are
ecologically saturated or not, it may be more useful
to ask how di€erences in the regional pool of species
are expressed in (i) the pattern of local diversity
within habitats, and (ii) turnover of species between
habitats within the region. Birds of the West Indies
show that these measures respond to change in size
of the regional pool approximately equally. Ecological release suggests that ecological interactions
within local communities make invasion of additional species more dicult. Presumably, reduced
1115
R.E. Ricklefs
# 2000 British
Ecological Society
Journal of Animal
Ecology, 69,
1111±1116
habitat breadth within regions having large species
pools results from the lower productivity of populations within their most productive habitats and
stronger interspeci®c competition in habitats that
are marginal for them. However, in spite of local
ecological pressure, there is no apparent upper
saturation point for species richness within avifaunas of the Caribbean Basin. As species are added to
the regional pool, species richness within local
assemblages continues to increase, although not at a
proportional rate.
Di€erences in `regional' diversity in this data set
are established by barriers to dispersal from continental sources of colonists and by higher rates of
extinction on small islands (Ricklefs & Lovette
1999). Thus, di€erences in regional diversity are
caused in part by factors external to the regions
themselves (colonization) and in part by factors
characteristic of the region but external to local
habitats (extinction of island populations). As Srivastava (1999) suggests, di€erences in `regional' species pools caused by barriers to dispersal and by
extinction may not be comparable to di€erences
accumulated over long periods of independent evolutionary history, as would occur between the southern continents in the case of birds. However,
comparison with Pearson's (1977) studies on tropical forest birds from six regions on three continents
suggest that these relationships may be general. The
logarithmic slope of the local±regional relationship
in Pearson's data is 065 (Srivastava 1999), which is
similar to slopes calculated from the Cox/Wunderle
data for comparable habitats in the Caribbean
Basin using Robs as the estimate of regional diversity
(young secondary forest, b ˆ 0714 ‹ 0065; old secondary forest, b ˆ 0476 ‹ 0176; mature lowland
forest, b ˆ 0616 ‹ 0103).
Srivastava (1999) makes the important point that
local±regional richness plots should be used in conjunction with other evidence pertaining to the e€ects
of local ecological interactions within assemblages.
Such evidence would include density compensation
and ecological release, which are well documented in
the data of Cox & Ricklefs (1977) and Wunderle
(1985). Furthermore, densities of bird populations
within the Caribbean Basin may be limited by local
resources, as indicated by the similar total abundance of birds in all regions regardless of the species
pool or number of species per habitat (Table 1, column 9).
Local diversity does not re¯ect only ecological
saturation or only proportional sampling of a regional species pool. Interactions between species constrain membership in local assemblages but do not
place an upper limit on their size. Local and regional diversity are connected through the pressure of
intraspeci®c competition, which compels individuals
to disperse from crowded to less crowded habitats
and populations to evolve adaptations that promote
broader habitat occupancy. Ecologists should be
less concerned about whether populations interact
within local assemblages than with the mechanisms
responsible for (i) generating the regional pool of
species, (ii) the distribution of those species over
habitats within the region, and (iii) evolutionary
adjustments that accompany invasion of a local
assemblage.
Acknowledgements
I am grateful to D. S. Srivastava and a referee for
helpful comments.
References
Caley, M.J. & Schluter, D. (1997) The relationship between
local and regional diversity. Ecology, 78, 70±80.
Cody, M.L. (1993) Bird diversity components within and
between habitats in Australia. Species Diversity in Ecological Communities. Historical and Geographical Perspectives (eds R.E. Ricklefs & D. Schluter,), pp. 147±
158. University of Chicago Press, Chicago.
Cornell, H.V. & Lawton, J.H. (1992) Species interactions,
local and regional processes, and limits to the richness
of ecological communities: a theoretical perspective.
Journal of Animal Ecology, 61, 1±12.
Cox, G.W. & Ricklefs, R.E. (1977) Species diversity, ecological release, and community structuring in Caribbean
land bird faunas. Oikos, 29, 60±66.
Gaston, K.J. (1998) Species±range size distributions: products of speciation, extinction and transformation.
Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences, 353, 219±230.
Griths, D. (1999) On investigating local±regional species
richness relationships. Journal of Animal Ecology, 68,
1051±1055.
Klein, N.K. & Brown, W.M. (1994) Intraspeci®c molecular
phylogeny in the yellow warbler (Dendroica petechia),
and implications for avian biogeography in the West
Indies. Evolution, 48, 1914±1932.
Loreau, M. (2000) Are communities saturated? On the
relationship between a, b, and g diversity. Ecology Letters, 3, 73±76.
Lovette, I.J., Bermingham, E. & Ricklefs, R.E. (1999)
Mitochondrial DNA phylogeography and the conservation of endangered Lesser Antillean Icterus orioles.
Conservation Biology, 13, 1088±1096.
Lovette, I.J., Bermingham, E., Seutin, G. & Ricklefs, R.E.
(1998) Evolutionary di€erentiation in three endemic
West Indian warblers. Auk, 115, 890±903.
Pearson, D.L. (1977) A pantropical comparison of bird
community structure on six lowland forest sites. Condor, 79, 232±244.
Pulliam, H.R. (1988) Sources, sinks, and population regulation. American Naturalist, 132, 652±661.
Ricklefs, R.E. (1987) Community diversity: relative roles of
local and regional processes. Science, 235, 167±171.
Ricklefs, R.E. & Bermingham, E. (1999) Taxon cycles in
the lesser Antillean avifauna. Ostrich, 70, 49±59.
Ricklefs, R.E. & Lovette, I.J. (1999) The roles of island
area per se and habitat diversity in the species±area
relationships of four Lesser Antillean faunal groups.
Journal of Animal Ecology, 68, 1142±1160.
Schluter, D. & Ricklefs, R.E. (1993) Species diversity. An
introduction to the problem. Species Diversity in Ecolo-
1116
Local and
regional species
richness
# 2000 British
Ecological Society
Journal of Animal
Ecology, 69,
1111±1116
gical Communities. Historical and Geographical Perspectives (eds R.E. Ricklefs & D. Schluter), pp. 1±12.
University of Chicago Press, Chicago.
Seutin, G., Brawn, J., Ricklefs, R.E. & Bermingham, E.
(1993) Genetic divergence among populations of a tropical passerine, the streaked saltator (Saltator albicollis). Auk, 110, 117±126.
Seutin, G., Klein, N.K., Ricklefs, R.E. & Bermingham, E.
(1994) Historical biogeography of the bananaquit
(Coereba ¯aveola) in the Caribbean region: a mitochondrial DNA assessment. Evolution, 48, 1041±1061.
Srivastava, D.S. (1999) Using local±regional richness plots
to test for species saturation: pitfalls and potentials.
Journal of Animal Ecology, 68, 1±16.
Stevens, G.C. (1989) The latitudinal gradient in geographical range: how so many species coexist in the tropics.
American Naturalist, 133, 240±256.
Terborgh, J.W. & Faaborg, J. (1980) Saturation of bird
communities in the West Indies. American Naturalist,
116, 178±195.
Wiens, J.A. (1989). The Ecology of Bird Communities, Vol.
1. Cambridge University Press, Cambridge.
Wunderle, J.M. (1985) An ecological comparison of the
avifaunas of Grenada and Tobago, West Indies. Wilson Bulletin, 97, 356±365.
Received 30 August 1999; revision received 16 June 2000