The relationship between cave biodiversity

and available habitat

Mary C. Christman
1
and David C. Culver
2 1
Department of Animal and Avian Sciences,
University of Maryland, MD, USA and
2
Department of Biology, American University, NW,
Washington DC, USA
Abstract
Aim The goal of this study was to determine the role habitat availability plays in the
distribution of obligate subterranean cave fauna in eastern North America.
Location The numbers of stygobites, troglobites and caves in the counties of the south-
eastern USA were analysed.
Methods The data were characterized by large numbers of zeroes and by spatial
clustering of non-zeroes in ve regions. Regression and conditional autoregressive (CAR)
models were used to elucidate the patterns and relationships between numbers of species
and numbers of caves both locally and regionally.
Results Local effects (regions and numbers of caves in counties) accounted for 45% of
the variation in troglobite counts (P = < 0.001) and 24% of the variation in stygobite
counts (P = < 0.001). Signicant spatial autocorrelation among both stygobites and
troglobites (P = < 0.0001) was found as well.
Conclusion Overall, habitat availability as measured by cave numbers inuenced
species richness. Spatial and regional effects also played an important role in determining
the observed distributions of the subterranean fauna. Terrestrial and aquatic commu-
nities showed very different patterns in their relationship to habitat and within the
different regions.
Keywords
Analysis of covariance, caves, diversity, habitat, spatial autocorrelation, stygobites,
troglobites.
I NTRODUCTI ON
In the 48 coterminous United States nearly 1000 described
species and subspecies are known only from caves and
associated subterranean habitats (Culver et al., 2000). These
species (termed troglobites for terrestrial species and stygo-
bites for aquatic species) have a broad taxonomic represen-
tation, comprising 210 genera, 96 families and 38 orders of
Turbellaria, Oligochaeta, Mollusca, Arachnida, Crustacea,
Chilopoda, Diplopoda, Insecta, Osteichthyes and Amphibia.
This taxonomically diverse fauna are worth analysing as a
group because all of these species have successfully invaded
one of the harshest environments on earth caves aphotic
habitats with very little food. The fauna are also worth
analysing as a group because they are isolated both phys-
ically and genetically from non-cave dwellers.
Nearly all of these species are the result of independent
invasions of and subsequent isolation in the subterranean
realm. Most subterranean species have very restricted
ranges. Of the 973 species and subspecies known from
caves in the 48 contiguous United States, 594 (61%) are
restricted to a single county and an additional 23% are
restricted to a single state (Culver et al., 2000). Furthermore,
those species with ranges of more than a handful of caves
often comprise a group of sibling species (Kane et al., 1992;
Sket & Arntzen, 1994; Culver et al., 1995).
Caves are, contrary to general perception, quite common.
Over 45,000 caves have been reported from the USA (Culver
et al., 1999), and many more are known from Europe. The
vast majority of caves occur either in lava or in soluble
carbonates (limestone, dolomites and marble) as a result of
dissolution of the bedrock. Regions where carbonates
Correspondence: Mary C. Christman, Department of Animal and Avian
Sciences, University of Maryland, MD, USA. 2
Journal of Biogeography, 28, 367380
2001 Blackwell Science Ltd
predominate and solution rather than erosion is the major
geomorphic agent are termed karst regions. Such regions
represent about 15% of the earth's surface and about 20%
of the land area east of the Mississippi River (White et al.,
1995).
Most previous studies of subterranean biodiversity pat-
terns have emphasized the role of historical events
Pleistocene glaciations and Eocene Sea embayments in
particular (Peck, 1980; Boutin, 1994). What is implicit in
most of these studies is that the habitat itself is not limiting.
Differences in diversity, according to these studies, resulted
from the location of the area in time and space, rather than
habitat quality or quantity. The goal of this study is to take a
careful look at the role that habitat availability plays in the
distribution of troglobites and stygobites in eastern North
America.
In particular, we explore the relationship between the
number of stygobites and troglobites and the number of
caves, both locally (within a county) and regionally (adjoin-
ing counties). We focus on two hypotheses: (1) species
richness is dependent on local habitat availability, which
allows invasion and isolation, and (2) species richness is also
controlled by regional habitat availability because of migra-
tion. The local number of caves provides a measure of
subterranean habitat availability. For regional modelling,
biodiversity in neighbouring counties was explored as the
number of species in adjacent counties should be a measure
of the opportunity for subterranean dispersal. That is, if
considerable subsurface dispersal occurs, then species num-
bers in adjoining areas will inuence diversity locally, as Barr
(1967, 1968) suggested.
MATERI ALS AND METHODS
A data set containing the numbers of species per county for
the entire 48 coterminous United States was compiled by
Culver et al. (2000) and is available on the world wide web
at http://www.karstwaters.org. All formally described spe-
cies and subspecies limited to caves and other large cavities
were included; interstitial species (fauna of small subsurface
cavities) were excluded because they are poorly described in
the United States. Operationally, species and subspecies for
which over 95% of occurrence records were in subterranean
habitats are included. We refer the reader to Culver et al.
(2000) for more details and for discussion of sampling
completeness and data quality.
The data set containing the numbers of caves per county
for the lower 48 states was similarly compiled (Culver
et al., 1999) using published records. Reports from state
cave surveys and caving societies provided additional
information. Every reported cave was located to county-
level only.
The total amount of subterranean habitat available in a
county would include not only the known caves but also
entranceless caves (Curl, 1966) and caves too small for
human entry. A measure of total availablilty would require,
in addition to a complete enumeration of cave lengths and
volumes, an estimate of the fractal dimension of karst (Curl,
1986). But this information is not available. What is
available for the study region is the number of known caves
per county. If the fractal dimension is more or less constant,
then estimation of total habitat with number of caves may be
relatively robust.
We chose to study the cave fauna of the eastern United
States, south of the 40th parallel and east of the 100th
meridian in detail. This region, south of the southern border
of Pennsylvania and east of the western side of Texas
approximately corresponds to the non-glaciated United
States southeast of the Great Plains, and encompasses most
of the known obligate subterranean species. We looked at
this fauna at the scale of counties cells with average area
of roughly 2500 km
2
. The centroid (latitude and longitude
of the geographical centre) of every county in this region was
added to the data set.
Counties vary in size and consequently might inuence the
counts of the species or caves. To mitigate any possible
effects, we rst identied those counties under 100 km
2
.
There were c. 32 such counties (1.9% of the total number of
counties). None of these counties contained any subterra-
nean fauna, so we merged them with their nearest neighbour
to create a single larger county. Its centroid was deemed to
be the centroid of the bigger county.
In addition to truncating the sizes of the smallest counties,
we also determined whether the county size was related to
either the number of caves or the number of species. The
natural logarithm of cave number and the size of the county
for counties with at least one cave were found to be
uncorrelated (Spearman's r = 0.0507, P > 0.20). Species
number and county size for counties with at least one species
were also found to be uncorrelated (Spearman's r =
0.0105, P > 0.20). These results lend support to the
argument that county size does not inuence the results
and interpretations.
For statistical analyses, we employed two approaches. The
rst was usual general linear modelling. Here, the counties
are assumed to be independent observations. We did both
regression analyses of the relationship between species and
cave numbers and analyses of covariance in order to allow
for different slopes among different regions of the south-
eastern United States (Neter et al., 1990).
For some analyses, there was evidence of variance of the
response variable increasing with the independent variable.
Hence, we performed weighted regression with the weights
being the inverses of the standard deviations of Y stratied at
unit intervals of the independent variable.
In cases where a quadratic equation t best, we used a
centred independent variable, X
c
= (X
"
X), in place of X.
Centring of the explanatory variable reduces multicollinear-
ity between X and X
2
and hence allows the model coef-
cients to be interpretable.
The second approach does not assume independence
among the observations. In fact, it is the non-independence
that is of interest. Conditional autoregressive (CAR) models
allow the observations to be spatially autocorrelated by
assuming a conditional model in which an observation in
one county depends on the observed values in the neigh-
Blackwell Science Ltd 2001, Journal of Biogeography, 28, 367380
368 M. C. Christman and D. C. Culver
bouring counties (Cliff & Ord, 1973; Cressie, 1993). The
CAR model (Cressie, 1993) is given by
Y
i
= l g

j
W
ij
(Y
j
l) e
i
(1)
where Y is the response variable of interest (number of caves,
number of troglobites or number of stygobites suitably
transformed), l is the grand average of Y, g is the spatial
parameter, e
i
is the random error, and the {w
ij
}, i, j = 1,,n,
are spatial weights relating Y at location i pairwise with the
Y-values at other locations (the Y
j
). The random error terms
are assumed to be normally distributed and independent
with a mean of zero and a constant conditional variance, s
2
.
The spatial weight relating the Y-values at two locations
we used is
W
ij
=
max(d
rt
)
d
ij
I[d
ij
_ 30 minutes[ (2)
where d
ij
= [[S
j
S
i
[[ is the Euclidean distance between the
centroids for county i and county j, max(d
rt
) is the maximum
distance between any two county centroids and I is an
indicator function taking the value of 1 if d
ij
30 and equals
0 otherwise. These weights restrict the spatial relationship, if
it exists, to be between counties whose centroids are within
30 min (56 km) of one another and, in addition, restricts the
value of g to the range of [1, +1]. Hence, g in equation 1 is
interpretable as an autocorrelation coefcient.
For analysing the spatial relationship of the numbers of
caves, we estimated the model parameters using data only
for those counties in which the number of caves was greater
than 0. As a result, counties with zero caves appear in the
model only on the right hand side as conditional explanatory
variables for the number of caves in counties with at least
one cave and only when they are neighbouring counties in
close proximity to counties with at least one reported cave.
This approach ts a model in which non-zero predicted
values were estimated for counties having at least one cave
and a value of 0 is assigned to counties with zero observed
caves. We chose this approach because of the clustered
nature of the distribution of caves in the study region
(Fig. 2). Ignoring the clustering and including all of the
counties with zeroes in the model would be the equivalent to
assuming that the entire study region is a realization of a
single random spatial eld. This is clearly not the case as
some areas cannot support caves because of their geology.
Including the counties with zeroes also would provide a
tted surface that is too smooth, i.e. would estimate a non-
zero number of caves in regions which have no caves and
would seriously underestimate the numbers of caves in
regions in which caves tend to cluster.
As the subterranean fauna are dependent of the existence of
caves, we made similar adjustments for handling zero counts
in the spatial analyses of troglobites and stygobites as well.
We employed various measures of spatial clustering
(Moran's I and colleagues) as well as the CAR model. All
descriptive and statistical analyses were made on natural
logarithm transformed data because the variables are counts
and highly positively skewed. Data were analysed using
either JMP (SAS Institute, Inc., Cary, NC, USA 3,4 ) or
S-PLUS (MathSoft, Inc., Seattle, WA, USA 3,4 ) software.
RESULTS
Distribution of caves
A total of 27,280 caves have been reported in the study area.
Out of a total of 1622 counties, 622 (37.3%) had one or
more caves. One county Jackson County, Alabama had
more than twice as many caves (1526) than the county with
the next largest number of caves, White County, Tennessee
(711 caves). As Jackson County is so unusual compared with
the other counties in the south-eastern United States, we
chose to exclude it from the analysis because of its
potentially strong inuence on any t to the data and
because of its outlying value in terms of the explanatory
variable, number of caves per county.
The descriptive statistics and box plot of the distribution
of the remaining 621 counties are shown in Fig. 1 and
Table 1. The mean number of caves for these counties is
52 and the median is 13. As the number of caves is a
count, it is not surprising that the distribution is highly
skewed (skew = 3.32). Even the logged values are slightly
skewed (skew = 0.09), although much less so (Fig. 1,
Table 1).
The geographical distribution of caves, by county, is
shown in Fig. 2. The distribution of caves is patchy and
highly clumped. All three measures of clumping (Moran's I,
Geary's C, and the proportion of black-white joins; Cliff
& Ord, 1973) show signicant clustering of the caves
(Table 2).
One might expect, given the geographical pattern of
cave-bearing regions (especially karst areas), that the
number of caves within counties would be positively
spatially autocorrelated. By positively autocorrelated we
mean that neighbouring or contiguous counties should have
similar numbers of caves. Using maximum likelihood
estimation, the resulting parameter estimates for the auto-
regressive model in equation 1 are l = 2X244, g = 0.561
and s
2
= 2X550 (619 d.f. with a log-likelihood of
)2299.334). A likelihood ratio test indicates that the
autocorrelation coefcient is statistically signicantly dif-
ferent than zero (X
2
= 134.4, d.f. = 1, P = < 0.0001). The
reasonably large value of the autocorrelation coefcient, g,
provides additional evidence that the number of caves in
neighbouring counties are positively related.
Five major cave regions, all located in areas of extensive
limestone outcrops, have been recognized (Culver, 1999).
These are (Fig. 2): (1) Florida Lime Sinks (part of Florida);
(2) Appalachians (parts of West Virginia, Virginia, Ala-
bama, Tennessee and Georgia); (3) Interior Low Plateau
(parts of Alabama, Tennessee, Kentucky, Indiana and
Illinois); (4) Ozarks (parts of Missouri, Arkansas and
Oklahoma) and (5) Balcones Escarpment and Edwards
Plateau (part of Texas). We applied equation 1 to each
region separately to determine if the autocorrelation varied
by region. The results are given in Table 3. The autocor-
Blackwell Science Ltd 2001, Journal of Biogeography, 28, 367380
Relationship between cave biodiversity and available habitat I 369
relation coefcients tend to sort into two groups. Regions 1
and 5 have relatively lower autocorrelation coefcients
than the other three regions but this could be an artefact of
the smaller sample sizes.
Distribution of stygobites and troglobites
Not all counties with caves have stygobites or troglobites.
This can be for several reasons, including having habitat that
is too scarce to sustain populations or sampling error or lack
of sampling. We were not able to disentangle entirely these
different possibilities, so we have limited our analysis to
counties with at least one troglobite for modelling the
number of troglobites, and similarly for stygobites. If zeroes
were included, this would result in forcing any regression
line toward the origin. This would be inappropriate for
many reasons including (1) the relationship might not be
linear near the origin, or (2) the intercept might be negative,
i.e. more than one cave could be required for a species to be
known from a county.
A total of 263 stygobites and 576 troglobites occur in
the study area (Table 4). This represents more than 85%
of the known stygobitic and troglobitic fauna from the 48
contiguous United States (Culver et al., 2000). The broad
taxonomic basis of the obligate subterranean fauna in our
study area is obvious 34 families of stygobites and
44 families of troglobites are represented. Crustaceans
dominate the aquatic fauna, accounting for nearly 70% of
the species and subspecies. Arachnids and insects (nearly
exclusively beetles) dominate the terrestrial fauna,
accounting for over 75% of the species and subspecies.
While many genera have only a few subterranean species,
six genera contain over 25 the pseudoscorpion genera
Kleptochthonius (30 species) and Tyrannochthonius (35
species), the spider genus Cicurina (39 species), the isopod
genus Caecidotea (42 species and subspecies), the amphi-
pod genus Stygobromus (54 species and subspecies) and
the beetle genus Pseudanophthalmus (157 species and
subspecies).
Most species have very restricted ranges 115 stygobites
(44%) and 359 troglobites (62%) are restricted to a single
county. In fact, only nine species (six troglobites and three
stygobites) are known from more than 30 counties. Of these,
seven were described before 1900 (Table 5), suggesting that
modern taxonomic treatment would likely result in splitting
of these species. Christiansen & Culver (1968) came to the
same conclusion about one of the species Pseudosinella
hirsute (Delamare DeBoutteville) but did not formally
describe any new species.
Figure 1 Box plots and frequency distributions of the number of caves per county and the natural logarithm of the number of caves per
county for the south-eastern region of the United States. The box in the box plot indicates the middle 50% of the data. The whiskers show the
range of the data, except for outliers (values which are further away from the box by more than 1.5 times the length of the box) which are
shown as points. The line within the box indicates the value of the median; the diamond indicates the 95% condence interval for the mean.
Table 1 Descriptive statistics of the number of caves per county and
the natural logarithm of the number of caves per county for the
south-eastern region of the United States
Statistics Caves Ln caves
Y 52.346 2.579
SE 3.778 0.072
S 94.159 1.810
Skew 3.321 0.087
CV 179.878 70.198
Min 1 0
Median 13 2.565
Max 711 6.567
n 621 621
Blackwell Science Ltd 2001, Journal of Biogeography, 28, 367380
370 M. C. Christman and D. C. Culver
The distributions of stygobites and troglobites are patchy
and highly clumped. Moran's I and Geary's C statistics
indicate signicant clustering of the counts (Table 2). Con-
versely, the blackwhite (BW) join statistics indicates
higher than expected proportions of BW joins. This is
largely the result of a small number of stygobites and
troglobites found in isolated counties not associated with
one of the ve major regions. We also applied equation 1 for
the stygobites and troglobites separately to determine if
spatial autocorrelation varied by region. The results are
given in Table 3. It appears that the autocorrelation coef-
cients sort differently for stygobites and troglobites.
Local models of distribution
A total of 262 (excluding Jackson County) counties had one
or more troglobites, and the distribution of number and the
natural log of both the number of troglobites and the
number caves is shown in Fig. 3 and Table 6. A weighted
quadratic regression of Y (Ln troglobites) on X (Ln caves) t
the data best; higher order terms were not statistically
different than zero. The resulting model is shown in Fig. 4
and Table 7. Using the centred independent variable,
X
c
= (X = X) = (X 3X9334), the tted equation is
Y = 0X99 0X409 X
c
0X073X
2
c
Y (3)
(adjusted R
2
= 0.39). The minimum of the tted line
(equation 3) occurs at X = 1.140 which is equal to 3.127
caves per county. When this model is used to extrapolate to
the expected number of troglobite species in Jackson
County, Alabama, we obtain an estimate of 29.8 species,
much lower than the observed number of 52.
Stygobites are found in a total of 304 (excluding Jackson
County) counties. The distributions of the numbers and the
natural logs of the numbers of stygobites and caves are
shown in Fig. 5 and Table 8. In contrast to the case with
troglobites, the quadratic terms were not statistically signi-
cantly different from zero (Table 9), yielding a linear
equation (Fig. 6). The estimated regression line was
Figure 2 Geographical distribution of the number of caves per county in the south-eastern portion of the United States. One dot equals
one cave. The ve regions used in the study are labelled on the map.
Table 2 Weighted spatial clustering statistics for caves and obligate
cave species in the south-eastern United States. `BW Joins' is the
proportion of pairs of neighbouring counties in which one county
has reported species and the other has no known species.
Expected proportion under the null hypothesis of random spatial
distribution is in ( ) under the estimated proportion. All statistics
are calculated using weights based on distance to neighbours within
56 kilometers. See equation 2 in the text for more information
Variable
Statistics Caves Stygobites Troglobites
Moran's I 0.5109*** 0.3758*** 0.4349***
Geary's C 0.6033*** 0.5617*** 0.4963***
BW Joins 0.2091*** 0.1707*** 0.1505***
(0.2364) (0.1524) (0.1354)
*** P < 0.001.
Blackwell Science Ltd 2001, Journal of Biogeography, 28, 367380
Relationship between cave biodiversity and available habitat I 371

Y = 0X023 0X259 XY (4)

with an R
2
of 0.35. The intercept has a standard error of
0.077 and hence is not statistically signicantly different
than zero (Table 9) implying that a county with one cave
also has, on average, one stygobitic species. In terms of the
original units, the model is S = 1.023C
0.259
, where S is the
number of stygobites in a county and C in the number of
caves in a county. When extrapolating the expected number
of stygobites in Jackson County, Alabama, we get 6.53
species, an underestimate of the observed number of 14.
Local models with regional effects
Box and whiskers plots of the residuals from the quadratic
regression of Ln troglobites on Ln caves are shown, by
region in Fig. 7. Residuals for those counties not in one of
the ve regions were excluded from the analysis. The Florida
Lime Sinks were also excluded because only one troglobite is
known from this region. An analysis of variance (ANOVA ANOVA) of
the residuals showed signicant overall differences
(F
3,215
= 22.40, P < 0.0001). Three groups are apparent:
(1) the Ozarks (region 4) with reduced species richness, (2)
Edwards Plateau/Balcones Escarpment (region 5) with
increased species richness, and (3) the Appalachians (region
2) and Interior Low Plateau (region 3) with intermediate
species richness. However, a full analysis should include Ln
cave numbers as well as possible interaction terms so we
performed an analysis of covariance that includes the
regression relationship between numbers of caves and the
numbers of species.
An analysis of covariance model of the form
Y
ij
= l a
i
b
1
X
cYij
b
2
a
i
X
cYij
b
3
X
2
cYij
b
4
a
i
X
2
cYij
e
ij
(5)
was tted to the data set where Y is Ln troglobites in the jth
county within the ith region, l is the overall mean, a
i
is the
regional effect, X
c,ij
is the centred Ln Caves in the jth county
in the ith region, a
i
X
c,ij
and a
i
X
c,ij
2
are the interaction effects
and e
ij
is the random error term. The interaction of the
regional effect and the quadratic term was not statistically
signicant in the presence of all other terms (F = 1.04,
P = 0.3766) and hence was dropped from further consid-
eration. The reduced model with the remaining terms had
Table 3 Estimated spatial autocorrelation coefcients for cave,
stygobite and troglobite abundances in regions of karst in the
South-eastern United States. g is the estimate of the spatial
autocorrelation coefcient for the conditional model of the
autoregression of the log(Y) variable on its neighbours. The range of
each g is constrained to be within ()1, +1) by using the max
(distance) within each region in the spatial weights matrix. Sample
sizes are shown within ( )
Variable
Region Ln caves Ln stygobites Ln troglobites
1 0.031 (14) 0.162 (12) Na
2 0.409 (92) 0.485 (68) 0.535 (68)
3 0.274 (122) 0.330 (76) 0.288 (91)
4 0.308 (104) 0.304 (70) 0.256 (44)
5 0.104 (19) 0.242 (15) 0.528 (16)
Table 4 Obligate subterranean species, genera, families and
orders for the 11 classes and phyla represented in caves
Phylum
or class Orders Families Genera Species
Sub-
species Total
a. Aquatic species (stygobites)
Turbellaria 2 4 5 22 0 22
Oligochaeta 3 3 6 12 0 12
Mollusca 1 1 11 21 1 22
Arachnida 1 1 2 3 0 3
Crustacea 9 20 38 178 6 184
Insecta 1 2 2 2 0 2
Osteichthyes 2 2 5 6 0 6
Amphibia 1 1 5 10 2 12
Total 20 34 74 254 9 263
b. Terrestrial species (troglobites)
Mollusca 1 3 3 4 0 4
Arachnida 4 18 41 204 0 204
Crustacea 1 2 4 13 4 17
Chilopoda 2 2 2 2 0 2
Diplopoda 5 8 11 41 1 42
Hexapoda 3 7 11 64 2 66
Insecta 2 4 17 212 29 241
Total 18 44 89 540 36 576
Table 5 Species known from 30 or more counties in the study area, together with the year they were described
Order Family Species No. of counties Year described
Araneae Linyphiidae Porhomma cavernicola (Keyserling) 39 1886
Araneae Linyphiidae Phanetta subterranean (Emerton) 79 1875
Pseudoscorpiones Chernetidae Hesperochernes mirabilis (Banks) 48 1895
Collembola Entomobryidae Pseudosinella hirsute (Delamare DeBoutteville) 47 1949
Collembola Entomobryidae Sinella cavernarum (Packard) 36 1881
Diptera Sphaeroceridae Spelobia tenebrarum (Aldrich) 37 1897
Isopoda Asellidae Caecidotea antricola (Creaser) 32 1931
Amphipoda Crangonyctidae Crangonyx packardi Smith 31 1888
Amphipoda Crangonyctidae Crangonyx antennatus Packard 35 1881
Blackwell Science Ltd 2001, Journal of Biogeography, 28, 367380
372 M. C. Christman and D. C. Culver
statistically signicant effects which were thus retained
(Table 10). Not all regions or the interactions of those
regions with Ln caves were statistically different (Table 11)
so the regions were collapsed into three groups: region 2
(Appalachians), region 4 (Ozarks), and regions 3 and 5
combined (Interior Lowlands and the Edwards Plateau/
Balcones Escarpment).
The final estimated regression equation is

Y
ij
=
1X097 0X564X
cYij
0X046X
2
cYij
if i = 2
0X585 0X158X
cYij
0X046X
2
cYij
if i = 4
0X990 0X371X
cYij
0X046X
2
cYij
if i = 3Y 5
V
b
b
`
b
b
X
(6)
(see Fig. 8 for the regression lines on the original scale of the
variables). This equation provides an estimate of 26.46
troglobitic species in the caves in Jackson County, Alabama,
which is approximately half the observed number of 52,
implying that the number of caves is not sufcient to explain
theunusuallylargenumberof species foundinJacksonCounty.
Box and whiskers plots of the residuals of the linear
regression of Ln stygobites on Ln caves are shown, by region,
Figure 3 Box plots and frequency distributions of the number of caves per county, natural logarithm of the number of caves per county,
the number of troglobites per county, and natural logarithm of the number of troglobites for counties with at least one troglobite in the
south-eastern region of the United States.
Table 6 Descriptive statistics for counties with at least one
troglobite
Variable
Statistics Caves Ln caves Troglobites Ln troglobites
Y 104.122 3.933 5.069 1.213
SE 7.606 0.085 0.338 0.054
S 123.109 1.369 5.476 0.881
Skew 2.208 )0.643 2.787 0.366
CV 118.235 34.817 108.037 72.636
Min 1 0 1 0
Median 63 4.143 3 1.099
Max 711 6.567 35 3.555
N 262 262 262 262
Blackwell Science Ltd 2001, Journal of Biogeography, 28, 367380
Relationship between cave biodiversity and available habitat I 373
in Fig. 9. Residuals for Ln stygobites in counties not in one of
the ve regions were excluded from the analysis. ANOVA ANOVA of
the residuals showed signicant differences (F
4,230
= 5.50,
P < 0.003). Two groups were apparent: (1) the Florida Lime
Sinks (region 1) and Edwards Aquifer/Balcones Escarpment
(region 5) with increased species richness, and (2) the other
regions with reduced species richness.
Like the troglobites, an analysis of covariance was per-
formed in which the both X (Ln caves) and a regional effect
were included, as well as possible interactions terms that allow
the slope of the relationship between Ln stygobites and Ln
caves to vary by region. We found (Table 12) that there were
no interaction effects and that there were two regression lines
relating Ln stygobites to Ln caves: one for the Appalachians,
Ozarks and Interior Lowlands combined, and the other for the
Florida Lime Sinks and Texas Escarpment. The estimated
regression equation (see Fig. 10) is:

Y
ij
=
0X281 0X305X
ij
if i = 1Y 5
0X281 0X305X
ij
otherwise
&
(7)
This equation provides an estimate of 7.08 stygobitic
species in the caves in Jackson County, Alabama, which is
well below the observed number of 14 species. Interestingly,
had Jackson County been located in either region 1 (Florida)
or 5 (Texas), the estimate would have been 12.405 species,
very similar to the observed number.
Regional models of distribution
We investigated the predictive power of data from neigh-
bouring counties for the number of stygobites or troglobites,
using a CAR model (see equations 1 and 2). This is of
particular importance if there is subsurface migration. For
troglobites, an autoregressive model predicting number of
troglobites from number of troglobites in adjoining counties
yields a spatial autocorrelation, g, of 0.632 (Table 13). For
stygobites, an autoregressive model predicting number of
stygobites from number of stygobites in adjoining counties
yields a spatial autocorrelation, g, of 0.771 (Table 14). Both
of these spatial autocorrelations are consistent with the
proposition that subsurface dispersal is an important factor
in determining species richness.
As caves themselves are strongly spatially autocorrelated
(g = 0.561), one might conjecture that spatial autocorrela-
tions based on species richness may just reect spatial
autocorrelations of cave number. If this were true, then the
residuals from the regression of Ln troglobites and Ln
stygobites on Ln caves (equations 3 and 4) should display
little autocorrelation. In fact, the estimated spatial auto-
correlations of the residuals are very similar to those
obtained for the species counts themselves (Tables 13 &
14). Given that the number of caves does not appear to
explain the spatial autocorrelation of the species richness,
we examined the autocorrelations for each of the ve
distinct regions.
Regional models with regional effects
As was the case with local models, regional differences in
spatial autocorrelation are apparent (Table 3). The spatial
autocorrelation of caves in the Florida Lime Sinks (region
1) and in the Edwards Plateau/Balcones Escarpment
(region 5) is low relative to the other regions. This same
pattern is reected in the spatial autocorrelations of
stygobites in regions 1 and 5. This overall pattern echoes
the differences between these two regions and the other
regions for local models with regional effects (Fig. 1 and
Table 12). On the other hand, spatial autocorrelations
among troglobites fell into two groups correlations of
< 0.3 for the Interior Low Plateau (region 2) and the
Ozarks (region 3) and correlations of > 0.5 for the
Appalachians (region 2) and the Edwards Plateau/Balcones
Escarpment (region 5). This pattern is different than those
suggested by the local models with regional effects (Figs 7
& 8), which groups the Appalachians and the Interior
Low Plateau together and the Ozarks and the Edwards
Aquifer/Balcones Escarpment separately.
DI SCUSSI ON
The problem of zeroes
The distribution of stygobites, troglobites and caves are all
clumped in their distribution. Most counties in the study
area have no reported stygobites, no reported troglobites and
no reported caves. As we have shown, those counties with
Figure 4 Quadratic weighted regression of Ln troglobites on Ln
caves (centred around its mean). Middle line is the tted regression;
surrounding lines are the 95% condence limits for the t.
Table 7 Results of weighted regression analysis of Ln troglobites
on Ln cave numbers. Adjusted R
2
= 0.39, F = 84.95, P < 0.001
Term Estimate SE t-Ratio Prob > |t|
Intercept 0.994 0.054 18.44 < 0.0001
(X ) X) 0.409 0.032 12.90 < 0.0001
(X ) X)
2
0.073 0.016 4.70 < 0.0001
Blackwell Science Ltd 2001, Journal of Biogeography, 28, 367380
374 M. C. Christman and D. C. Culver
many caves, many stygobites, and many troglobites tend to
be surrounded by counties with many caves, many stygobites
and many troglobites. In addition, the recorded zeroes may
be true zeroes (no caves, stygobites or troglobites), or they
may be the result of inadequate sampling and collecting, or
the stygobites and troglobites have been collected but not yet
described. For example, in one of the most intensively
studied states, West Virginia, only one-third of the caves
Figure 5 Box plots and frequency distributions of the number of caves per county, natural logarithm of the number of caves per county,
the number of stygobites per county, and natural logarithm of the number of stygobites for counties with at least one stygobite in the
south-eastern region of the United States.
Table 8 Descriptive statistics for counties with at least one
stygobite
Variable
Statistics Caves Ln caves Stygobites Ln stygobites
Y 95.648 3.752 3.418 0.943
SE 6.803 0.085 0.171 0.043
S 118.616 1.486 2.981 0.742
Skew 2.315 )0.625 2.740 0.292
CV 124.013 39.607 87.211 78.662
Min 1 0 1 0
Median 55.5 4.016 3 1.099
Max 711 6.566 26 3.258
n 304 304 304 304
Table 9 Results of weighted regression analyses of Ln stygobites
on Ln cave numbers. (a) Linear model ) adjusted R
2
= 0.34,
F = 159.25, P < 0.0001; (b) Quadratic model ) adjusted R
2
= 0.35,
F = 81.56, P < 0.0001
Term Estimate SE t Ratio Prob > |t|
(a)
Intercept )0.023 0.077 )0.31 0.7605
X 0.259 0.021 12.62 < 0.0001
(b)
Intercept )0.097 0.105 0.09 0.3538
(X ) X) 0.141 0.073 1.94 0.0530
(X ) X)
2
0.020 0.012 1.70 0.0911
Blackwell Science Ltd 2001, Journal of Biogeography, 28, 367380
Relationship between cave biodiversity and available habitat I 375
have been investigated biologically (J. Holsinger, personal
communication).
This pattern of clumped organisms and clumped habitat
with zeroes of uncertain provenance is a very common
biogeographic occurrence. In a sense, biodiversity hotspots
themselves t within this framework, and the problem of
zeroes of unknown provenance is reected in the two kinds
of zeroes used in the conservation status ranks of The Nature
Conservancy GX for presumed extinct (not located despite
extensive searches) and GH for possibly extinct (missing but
still some hope of rediscovery) (Master, 1991). In this
context, our decision to treat the zeroes as xed for most
analyses holds considerable promise as a useful approach to
data of this kind.
Comparison of terrestrial and aquatic patterns
The plots of species richness for both terrestrial and aquatic
species against number of caves are shown in Fig. 11. While
there may be a temptation to look at these graphs as though
they were species area curves, especially as the plot of Ln
stygobites against Ln caves has a slope typical of species area
curves (z = 0.26), they are not. The number of caves is not a
particularly good surrogate for area, as caves vary greatly in
area, particularly in the dimension of length. What the
number of caves probably measures is a combination of
habitat diversity, the number of available habitat patches or
`islands' (Culver, 1970), sampling intensity, and time avail-
able for colonization.
The relationship between caves and stygobites appears
relatively simple a straightforward exponential relation-
ship that accounts for approximately one-third of the
variance in number of stygobites. The fact that the curve
climbs slowly (Fig. 11) may reect one or both of the
following factors. First, as the number of caves in a county
increase, connectivity of caves is probably also increasing,
especially in the aquatic habitat. Caves form at or below the
surface of the water table (White, 1988), and consequently
connectivity will be greater for the aquatic habitat than for
the terrestrial habitat. This results in less opportunity for
isolation within the county. Secondly, the slow climb of the
curve may be the result of constraints on the pool of species
available for colonization. For example, relative to the
extensive cave region along the coast of the Adriatic Sea, the
aquatic fauna of eastern North America is depauperate
(Culver and Sket, 2000). This difference is at least in part
because of the greater opportunity for cave colonization
afforded by the proximity of the Adriatic Sea and the
Mediterranean salinity crises that resulted in colonization of
caves by marine ancestors (Sket, 1999).
The terrestrial curve is more complex. The descending
part of the quadratic curve (and limb of the piecewise linear
model) implies that more troglobites are found on average in
counties with one cave than in counties with two caves. We
believe this to be an artefact of the small number of
observations at cave densities less than four per county.
There are 10 counties with two or fewer caves and
containing between one and three troglobitic species. In
fact, the counties with one cave have two or three species
whereas the counties with two caves have one, two or three
species. A change in any of these values toward a more even
distribution would probably make the relationship insignif-
icantly different from a zero slope. Seven of the 24 troglobite
records are for the wide-ranging troglobites (Table 4), whose
Figure 6 Linear weighted regression of Ln stygobites on Ln caves.
Middle line is the tted regression; surrounding lines are the 95%
condence limits for the t.
Figure 7 Distribution by ecoregion of the residuals from the
weighted quadratic regression of Ln troglobites on Ln caves.
Table 10 Analysis of covariance table for Ln troglobites as a
function of region and Ln caves
Source d.f. SS F-Ratio Prob > F
(X ) X) 1 20.918 54.00 < 0.0001
Region 3 15.941 13.72 < 0.0001
(X ) X)
2
1 2.352 6.07 0.0145
Region (X ) X) 3 4.761 4.10 0.0075
Blackwell Science Ltd 2001, Journal of Biogeography, 28, 367380
376 M. C. Christman and D. C. Culver
validity is in question. Nonetheless, there does appear to be a
threshold number of caves per county for more than one
troglobite to be present.
As expected, the curve rises more steeply than that of the
stygobitic fauna, and this reects the more fragmented
nature of the terrestrial habitat and the greater pool of
species available for colonization. In eastern North America
and many other temperate zone cave areas, terrestrial species
probably invaded caves as a result of the vicissitudes of
Pleistocene climate (Culver, 1982).
Regional differences among the stygobitic fauna
Both the local model with regional effects (equation 7) and the
spatial models (equations 1 and 2) indicated that there were
signicant differences among regions. In addition, it appears
that regions 1 and 5 have higher diversity than the other
regions (t = 4.41, P = < 0.0001, Table 12). For the local
model with regional effects, the differences resulted from
differences in the intercept of the loglog regression. This
makes biological sense as both the Florida Lime Sinks and
the Edwards Plateau/Balcones Escarpment, unlike the other
regions, have a rich fauna in permanent groundwater. The
most famous example of this is the remarkable fauna collected
at the artesianspring at SanMarcos, Texas (Longley, 1981 5 ). In
the other regions, the fauna is mostly a stream fauna.
Table 11 Results of analysis of covariance
models of Ln troglobites as a function of
region and Ln caves. Interactions of region
and (X X)
2
are not statistically signicant
and hence are not shown. (a) All regions
treated separately (adjusted R
2
= 0.48,
F = 26.46, P < 0.0001); (b) regions collapsed
into three regions where regions 3 and 5 are a
single grouping (adjusted R
2
= 0.45,
F = 30.96, P < 0.0001)
Term Estimate SE t Ratio Prob > |t|
(a) Four separate regions
Intercept 1.158 0.064 18.12 < 0.0001
(X X) 0.389 0.053 7.35 < 0.0001
Region [2 vs. 5] )0.067 0.083 )0.82 0.4150
Region [3 vs. 5] 0.021 0.078 0.27 0.7860
Region [4 vs. 5] )0.583 0.094 )6.20 < 0.0001
Region [5]
(X X)
2
0.054 0.022 2.46 0.0145
Region [2 vs. 5] (X X) 0.174 0.075 2.30 0.0222
Region [3 vs. 5] (X X) )0.007 0.063 )0.11 0.9133
Region [4 vs. 5] (X X) )0.233 0.081 )2.88 0.0043
Region [5] (X X)
(b) Regions collapsed into three groups
Intercept 0.990 0.059 16.81 < 0.0001
(X X) 0.371 0.044 8.47 < 0.0001
(X X) 0.046 0.022 2.07 0.0397
Region [2 vs. 3,5] 0.107 0.071 1.53 0.1265
Region [4 vs. 3,5] )0.405 0.081 )5.06 < 0.0001
Region [3, 5]
Region [2 vs. 3,5] (X X) 0.193 0.063 3.06 0.0025
Region [4 vs. 3,5] (X X) )0.213 0.068 )3.13 0.0020
Region [3,5] (X X)
Figure 8 Analysis of covariance model of Ln troglobites on region
and centred Ln caves. Data are plotted in the original units.
Quadratic regression line for region 2 is solid (associated data are
open circles); quadratic regression line for regions 3 and 5 are a
dashed line (data are open triangles); and, quadratic regression line
for region 4 is shown as a dotted line (data are +signs).
Figure 9 Distribution by ecoregion of the residuals from the
weighted linear regression of Ln stygobites on Ln caves.
Blackwell Science Ltd 2001, Journal of Biogeography, 28, 367380
Relationship between cave biodiversity and available habitat I 377
The spatial model indicated lowered autocorrelation
coefcients for both caves and stygobites in regions 1 and 5,
relative to the other regions (Table 3) which could be an
indication of the smaller numbers of counties with subter-
ranean species in these regions. In these regions, the counties
with non-zero counts are more likely to be adjacent to
counties with zero counts. As a result, the autocorrelation
will be lower. This in turn suggests that neighbourhood
effects at the scale of county may not be particularly
important in these two areas. How this may be connected to
species richness is problematic as it is difcult to determine if
there are any dispersal capabilities.
Finally, we note that there is no obvious connection
between regional differences in the stygobitic fauna and
regional differences in cave length and depth. Table 15
summarizes what we know about these regional differences.
Regions 1, 2 and 3 have a high frequency of long caves and
regions 2 and 3 have a high frequency of deep caves, and this
does not correspond to faunal differences.
Regional differences among the troglobitic fauna
Regional differences among the troglobitic fauna are more
complex. The local model with regional effects produced
three groups (equation 4): (1) the Ozarks with both a small
intercept and small slope, a generally depauperate fauna, (2)
the Appalachians with a small intercept but large slope, and
(3) the Edwards Plateau/Balcones Escarpment and Interior
Low Plateau with a larger intercept and smaller slope
relative to the Appalachians. The larger intercept in regions
3 and 5 may indicate a greater connectivity of caves and
greater regional effects. This is in accord with Barr's
hypothesis that the local diversity was higher in the Interior
Low Plateau and b-diversity was higher in the Appalachians
as a result of the greater connectivity of caves in the Interior
Low Plateau (Barr, 1967).
In terms of the caves themselves, there seems little, if any,
difference between region 2 and 3 in terms of lengths and
depths, but region 5, which is grouped with the Interior Low
Plateau has few long or deep caves (Table 15). This suggests
that individual cave characteristics are not important, as was
the case for the stygobitic fauna. However, when we turn to
spatial models, the distinction between the regions does not
match with the differences noted in the local model with
regional effects. In particular, spatial autocorrelations of
troglobites are high for the Appalachians and the Edwards
Plateau/Balcones Escarpment, and low for the Interior Low
Plateau and Ozarks. These differences in spatial autocorre-
lation do not accord with differences in species richness, no
matter how species richness is considered. Whether they
should be is problematic and difcult to interpret. In
particular, the pairing of the Ozarks, a low diversity area
with the Interior Low Plateau, a high diversity area, because
of similar spatial autocorrelation coefcients is unclear.
These results imply that other factors such as habitat quality
or climatic features or vegetative cover are important in
Table 12 Results of analysis of covariance of Ln stygobites as a
function of region and Ln caves. The intercept term and interactions
of region and X are not statistically signicant and hence are not
given in the nal model listed in the text (equation 7). (a) All
regions treated separately (adjusted R
2
= 0.25, F = 16.13,
P < 0.0001); (b) regions collapsed into two groupings regions 2, 3
and 4 together and regions 1 and 5 together (adjusted R
2
= 0.24,
F = 16.11, P < 0.0001)
Term Estimate SE t-Ratio Prob > |t|
(a) Four separate regions
Intercept )0.008 0.165 )0.05 0.9595
X 0.297 0.038 7.92 < 0.0001
Region [1 vs. 4] 0.293 0.156 1.88 0.0622
Region [2 vs. 4] )0.244 0.083 )2.95 0.0035
Region [3 vs. 4] )0.320 0.082 )3.88 0.0001
Region [5 vs. 4] 0.400 0.141 2.83 0.0051
Region [4]
(b) Regions collapsed into two groups
Intercept 0.103 0.164 0.63 0.5297
X 0.284 0.036 7.83 < 0.0001
Region [2,3,4 vs. 1,5] )0.291 0.066 )4.41 < 0.0001
Region [1,5]
Figure 10 Analysis of covariance model of Ln stygobites
regressed on region and Ln caves. Data are shown in original units.
Regression line for regions 2, 3 and 4 (combined) is shown as
dashed line (data are open circles) and the linear regression line
for regions 1 and 5 (combined) is solid (data are +signs).
Table 13 Results of CAR models for Ln troglobites
Explanatory variables g Log-likelihood d.f.
Ln troglobites in adjacent counties 0.632 )680.575 260
Ln caves within the county + Ln
troglobites in adjacent counties
0.625 )623.600 259
Table 14 Results of CAR models for Ln stygobites
Explanatory variables g Log-likelihood d.f.
Ln stygobites in adjacent counties 0.771 )762.365 302
Ln caves within the county + Ln
stygobites in adjacent counties
0.795 )705.282 301
Blackwell Science Ltd 2001, Journal of Biogeography, 28, 367380
378 M. C. Christman and D. C. Culver
determining species richness in areas with otherwise similar
features (latitude, cave densities, etc.).
Is subsurface migration important?
The local models attempted to explain the number of species
of stygobites and troglobites on the basis of local habitats,
i.e. the number of caves within the county. These regression
models, especially in the case where regional differences
were allowed for, explained some but not all of the variation
in the number of stygobites and troglobites, both in a
quantitative and qualitative sense. Approximately 45% of
the variance in troglobite numbers was accounted for by the
local model (Table 11) and about 25% of the variance in
stygobite numbers were accounted for by the local model
(Table 12). Hence, there is unexplained variation that needs
to be explored.
Furthermore, the differences between stygobites and
troglobites (Fig. 11), and some of the regional differences,
as well, make intuitive sense. This is not to say however, that
species numbers were only the result of local conditions. In
particular, there exists strong spatial autocorrelation of both
stygobite and troglobite numbers, an autocorrelation that
cannot entirely be accounted for by the strong spatial
autocorrelation of caves themselves (Tables 13 & 14),
although this is obviously a contributing factor. Two factors
then make the analysis of spatial relationships difcult. First,
the habitat itself is clumped and spatially autocorrelated.
Thus, species richness may be autocorrelated because of
some spatial process involving the species (migration), or be
the result of the spatial autocorrelation of some other
unmeasured environmental parameter such as food availab-
ility. Secondly, the tools of spatial statistics themselves do
not easily lend themselves to inferences about the causes of
the observed patterns. We examined spatial correlations
among the species counts but for determining explanatory
variables we used local regressions. A model combining the
two (autocorrelation model of the residuals from the
regression of troglobites on cave numbers; see Tables 13 &
14) includes both aspects but does not provide more
information about the probable causative effects. We believe
that further progress on this problem and related problems
will come from an analysis of different scales. Preliminary
analysis at both ner and coarser spatial scales indicates that
the statistical link between number of caves and number of
troglobites and stygobites disappears both at a scale of
100 km
2
and at the larger scale of eco-regions (cf. Master
et al., 1998; Ricketts et al., 1999).
An alternative approach would be to determine the spatial
relationships among endemic species, either aquatic or
terrestrial. Unfortunately, this data cannot be analysed using
the current spatial methodology because of the rarity of
endemics (values ranging from 0 to a maximum of 6 species
in a county with many counties having zero endemics).
Figure 11 Regression functions for Ln sty-
gobites and Ln troglobites on Ln caves
(equations 2 and 3 in text) shown in original
units with condence limits for each equa-
tion.
Table 15 Comparison of long (> 1 mile) and deep (> 400 feet)
caves based on information compiled by Robert Gulden on behalf of
the National Speleological Society. The continually updated list is
available at www.pipeline.com/~caverbob/
No. of caves
Region
> 1 mile
long
> 400 feet
deep
Total no.
of caves
%
Long
%
Deep
1 21 0 769 2.70 0.00
2 187 16 7063 2.60 0.23
3 418 67 15061 2.80 0.24
4 88 0 6984 1.30 0.00
5 20 1 1924 0.10 0.05
Blackwell Science Ltd 2001, Journal of Biogeography, 28, 367380
Relationship between cave biodiversity and available habitat I 379
ACKNOWLEDGMENTS
The research was partially supported by a grant from the
National Science Foundation, No. DMS 9806051, to
Christman. Development of species lists was supported by
contracts from The Nature Conservancy to Culver. Both
authors wish to thank Chris Belson and Jolie Paterson for
data management and computer support. Some of the work
was performed while the rst author was visiting the
Department of Statistics at Iowa State University, Ames,
IA, USA. The authors also wish to thank an anonymous
reviewer for thoughtful comments that resulted in a much
improved manuscript.
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BI OSKETCHES
Mary C. Christman is an Assistant Professor in the
Biometrics Program at the Department of Animal and
Avian Sciences, University of Maryland, College Park,
MD, USA. She is active in developing sampling designs
and statistical models for environmental studies and
biological research. Her interests include modelling
zoogeography and biodiversity, and estimating the
abundance of rare, geographically clustered populations.
David Culver is a professor in the Biology Department of
American University, Washington, DC. He is the Presi-
dent of the Karst Waters Institute and an honorary Life
Member of the National Speleological Society. His
current research interests focus on biogeography of cave
faunas, conservation biology and groundwater ecosystem
services.
Blackwell Science Ltd 2001, Journal of Biogeography, 28, 367380
380 M. C. Christman and D. C. Culver