Sea level change and the area of shallow-marine habitat: implications for marine

biodiversity
Author(s): Steven M. Holland
Source: Paleobiology , Spring, 2012, Vol. 38, No. 2 (Spring, 2012), pp. 205-217
Published by: Cambridge University Press

Stable URL: https://www.jstor.org/stable/41432803

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Paleobiology, 38(2), 2012, pp. 205-217

Sea level change and the area of shallow-marine habitat:

implications for marine biodiversity

Steven M. Holland

Abstract. - Analysis of a global elevation database to measure changes in shallow-marine habitat area
as a function of sea level reveals an unexpectedly complicated relationship. In contrast to prevailing
views, sea level rise does not consistently generate an increase in shelf area, nor does sea level fall
consistently reduce shelf area. Different depth-defined habitats on the same margin will experience
different changes in area for the same sea level change, and different margins will likewise experience
different changes in area for the same sea level change. Simple forward models incorporating a
species-area relationship suggest that the diversity response to sea level change will be largely
idiosyncratic. The change in habitat area is highly dependent on the starting position of sea level, the
amount and direction of sea level change, and the habitat and region in question. Such an
idiosyncratic relationship between diversity and sea level reconciles the widespread evidence from
the fossil record for a link between diversity and sea level change with the lack of quantitative support
for such a relationship throughout the Phanerozoic.

Steven M. Holland. Department of Geology, The University of Georgia, Athens , Georgia 30602-2501. E-mail:
stratum@uga.edu

Accepted: 10 August 2011

Supplementary materials deposited at Dryad: doi:10.5061/dryad.4pt8h

Introduction long-term changes in shelf area of continents,

especially on how the average elevation of a
Since at least the early 1900s, paleontologists
have suspected that sea level changecontinent
has is controlled by its size (Harrison
et al. 1981, 1983; Wyatt 1984, 1987). As the
shaped the history of marine life (Chamberlin
number
1909; Moore 1954). The theory of island bio- and size of continents change during
the
geography (MacArthur and Wilson 1963, 1967) formation and breakup of superconti-
nents,
offered a promising mechanism for tying diver- continents are flooded to varying de-
grees, which drives changes in shelf area.
sity directly to changes in the area of shallow-
Previous
marine habitat driven by changes in sea level. approaches have also emphasized
This simple relationship explained the the use of normalized hypsometric curves,
com-
mon association of extinction with sea level which correct elevation for the average area
of
fall and of radiation with sea level rise (e.g.,continent (Wyatt 1987), and hypsometric
Newell 1967; Simberloff 1974; Flessa and slopes, which describe coastal hypsometry
Sepkoski 1978; Bayer and McGhee 1985; Dock- with a single value called the hypsometric
ery 1986; Jablonski 1986; Hallam 1987, 1992;slope, which describes a linear fit of coastal area
to elevation (Algeo and Wilkinson 1991). Both
Brett and Baird 1995; Brett 1998). Despite the
appeal of this argument, many more studiesapproaches have been criticized for masking
have found no quantitative evidence of a re-substantial variation, raising the question, How
does habitable area vary regionally, and in
lationship between diversity, sea level change,
and shallow-marine habitat (e.g., Raup 1976; detail, as a function of the position and change
of sea level?
Wise and Schopf 1981; Valentine and Jablonski
1991; McGhee 1991, 1992; McRoberts and This study reappraises the link between the
area of shallow-marine habitat and sea level.
Aberhan 1997; Roy et al. 1998; Peters and
Foote 2001; Smith 2001; Martin 2003; Cramp- It does so by directly measuring the change in
area on basin-scale regions based on a global
ton et al. 2006) than those that have (Sepkoski
1976). elevation data set, rather than using summary
Previous studies of the link between habit- measures such as normalized hypsometric
able area and sea level have concentrated on curves or hypsometric slopes. The approach

© 2012 The Paleontological Society. All rights reserved. 0094-8373/ 12/3802-0002/$!. 00

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206 STEVEN M. HOLLAND

used here, which is based on modern eleva- habitat was calculated over the region. Sea
tions, suggests that the relationship between level positions between -200 m and +200 m
sea level and habitable area is much more
relative to present sea level are considered, as
these
complicated than previously recognized. span the realistic range of possible po-
This
sitions
relationship becomes even more complicated based on Phanerozoic eustatic curves
when coupled with previous work (Miller
on how et al. 2005). Code for GMT and R is
included
plate tectonic evolution alters continental and in the supplementary materials.
global-scale hypsometry. Simple models of regions were analyzed to capture
Multiple
the species-area relationship are used atorange
show of coastline shapes and coastal
how the same sea level fluctuations will physiographies (Fig. 1). In particular, straight
change diversity to varying degrees in coasts, curved coasts (both embayments and
differ-
ent habitats and on different margins. peninsulas), and highly complex coasts with
numerous topographic highs and lows are
Methods
contrasted. Straight coasts studied include the
coast
In this study, habitable area - the area of of Georgia and of Oregon and Wash-
shallow-marine habitat - is measured for
ington in the United States, the west coast of
modern basin-scale regions, assuming India, and the southern coast of Brazil.
a vari-
Embayed coasts studied include the Persian
ety of positions of sea level. Shallow-marine
habitat is defined here as locations within a Gulf and Adriatic Sea. The coasts of the
given depth range (e.g., 0-25 m below Sunda
seaShelf, Bahamas Platform, and Florida
level), and the effect of different ways
wereof
studied for their complex shapes. Stud-
ied coasts range from mountainous (e.g.,
defining shallow-marine habitat is explored.
Nine locations were selected for study to to gently sloping coastal plains (e.g.,
Oregon)
Georgia).
examine a range of modern physiographies of The goal in this study is to illustrate
the substantial
regions spanning on the order of hundreds of variation in the relationship
of shelf area to sea level within basin-scale
kilometers. These locations typically repre-
sent basin-scale regions, that is, foreland
regions, rather than provide an exhaustive
basins, carbonate platforms, and portions of
coverage of all potential regions on earth.
passive margins. Larger regions that encom-
Results
pass substantial physiographic variation are
also examined. Shared Characteristics. - Shallow-marine ar-
Elevations within these regions wereeaob- varies considerably with the position of sea
tained from the ETOPOl data set available level, even within individual coasts (Fig. 2).
from NOAA's National GeophysicalAlthough Data there is also considerable variation
Center (http:/ /www.ngdc.noaa.gov/mgg/ among coasts (discussed below), most coasts
global/global.html). ETOPOl is a global sharedata
basic patterns.
First, every margin has at least one well-
set consisting of elevations at the intersections
of a one-arcminute mesh and is compiled defined maximum in shallow-marine area. As

from multiple regional and global data sets. a sea level rise that begins below this
a result,
Subsets of ETOPOl data were extracted with
maximum and that does not cross beyond it
Generic Mapping Tools (GMT; Wesselwillandincrease habitat area. A sea level rise that
begins above this maximum will decrease
Smith 1998; http://www.soest.hawaii.edu/
habitat
gmt/). Elevations for each region were ob- area. A sea level rise that crosses this
tained from ETOPOl and converted to an maximum might either increase or decrease
xyz-format text file containing longitude,
habitat area, depending on the starting and
ending
latitude, and elevation for every point lyingpositions of sea level. For example,
on a one-arcminute grid within that any region
sea level rise on the coast of India (Fig. 2,
(see Appendix). Calculations of area astop a func-
center) that starts below approximately
tion of sea level were performed in R -50(RmDe-
(the mode of the distribution) but does
velopment Core Team 2011). For any given not pass
seathis elevation will increase habitable
level position, the total area of shallow-marine
area, and any rise that starts above -50 m will

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 SHALLOW-MARINE HABITAT 207

1 к , i ' к i 1. Map of world showing approximate bounding boxes o

decrease habitable area. In short, sea level from -100 m to +200 m). Intervals character-
change cannot be used as a proxy for changeized by especially steep slopes on the area/
in habitat area: some rises will increase sea level plot represent thresholds in habit-
habitat area and other equally largeable rises
areacan
(e.g., Bahamas, from -10 m to 0 m,
decrease habitat area. The same is true for sea and from +20 m to +30 m). Any sea level
level fall. change that traverses one of these steep slopes
Second, the slope of the area /sea level will profoundly increase or decrease habit-
relationship varies with the position of seaable area, potentially severely affecting ma-
level. Steeply sloping curves indicate that rine biotas (Johnson 1974; Hallam 1989).
shallow-marine area is acutely sensitive to sea Differences among Margins. - The relation-
level change (e.g., Georgia, from -50 m toship of shallow-marine area to sea level differs
-20 m), whereas flat curves indicate that sea substantially among margins (Fig. 2), particu-
level change has little effect on shallow- larly in the number of local maxima and the
marine area (e.g., Brazil, from +50 m to position of the primary maximum. Combined,
+200 m). As a result, not only could a giventhese differences demonstrate the strongly
sea level change either increase or decreasevarying responses of habitat area to the same
the amount of habitable area, but also the sea level change on different margins.
amount of habitat change depends on the First, some margins have fairly simple rela-
starting position of sea level. In some inter-tionships between shallow-marine area and
sea level, such as a simple unimodal curve,
vals, the slope on the area /sea level plot is
gradual and constant, such that there will be whereas
a others have much more complicated
simple correlation between sea level changefunctions with multiple local maxima. For
and change in habitable area (e.g., Oregon,example, both the Bahamas platform and the
coast of India have a single peak in shallow-
from -200 m to -100 m), but the relationship
marine area, reflecting a simple relationship
of habitat area to sea level may be much more
complex over other intervals (e.g., Oregon,between sea level and habitable area. Georgia,

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208 STEVEN M. HOLLAND

Figure 2. Plots of shallow-marine area as a function o

area. "Shallow-marine" is defined in these plots as
habitat is expressed as a proportion of the maxim
positions from -200 m to +200 m relative to prese

Florida, and the Sunda shelf are similar, but Second, the position of the primary maxi-
have two or more subequal peaks in habitable mum on the shallow-marine area /sea level
area separated by minor lows over a small plot varies among margins by 200 m, even in
(-50 m) range of elevations. The overall this limited sampling of the world. Most
response of habitat area to sea level is simple margins have at least a local maximum in
on these coasts, but is more complicated over a shelf area when sea level is near its current
narrow range of sea level positions. Several position. In most cases, this local maximum is
margins (Oregon, Brazil, Persian Gulf, Adriatic not exactly at present sea level, but may be 20-
Sea) have complex relationships with wide 30 m higher or lower than present sea level.
and reversing patterns in habitable area over a The true maximum on these nine margins,
however, varies over a much larger range,
broad range of sea level positions. The effect of
sea level change on habitable area on these from nearly 100 m below present sea level
margins will be acutely sensitive to the starting (Oregon) to nearly 100 m above it (Adriatic).
position, direction, and amount of sea level Third, some margins possess steep slopes
change. on the habitable area /sea level plots, but

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 SHALLOW-MARINE HABITAT 209

Florida being carbonate

others do not, and the positions of these platforms and the
thresholds differ amongSunda Shelf being
margins thatlargely siliciclastic (but
have
with coral reefs
them. For example, the Bahamas along its margins).
platform has All three
regions are
two thresholds, one at present seacharacterized
level (0bym) a broad shallow-
and one at +20 m. Sea level change
water platform withon the
a steep shelf edge, which
Bahamas platform would be expected to have relationship.
results in a simple unimodal
Whereas
dramatic effects on habitable the Bahamas
area anywhereis an isolated platform,
Florida is connected
in this range, but minimal effects outside to a continent
of with a
this range. The Oregon and gentlyAdriatic
dipping coastal plain, and the Sunda
coasts
Shelfsimilar
have thresholds in positions is ringed by tomountains.
those As a result, the
Bahamas could
in the Bahamas, but the Oregon and be overtopped by a signifi-
Adriatic
cantly
thresholds are substantially large sea level
smaller. Even rise,on
whereas the same
coasts lacking thresholds, seathe
level slopes
rise would of flood
the uplands on the
Florida and Sunda
habitable area /sea level relationship coasts and
varies at preserve some
the same sea level position. shallow-marine
For habitat.
example,
habitable area changes little Differences
on the among Habitats. - Even on a
Georgia
coast from -200 m to -50 m, but increases single margin, the response of individual
substantially over this sea level range on thehabitat zones will differ for the same sea
Oregon coast. Habitable area increases mark- level change (Fig. 3). For example, two hab-
edly on the Georgia coast from -40 m toitats that span the same depth range (e.g., 0-
-20 m, but declines just as markedly over this25 m and 75-100 m) will have the same
range on the India coast. overall form of the area /sea level relation-
Much of the variation among coasts stems ship, but their curves will be shifted laterally
from differences in the shape of their coastline,by the differences in their depths (75 m in this
and it is useful to separate regions by coastline example). The optimum position of sea level
shape. Georgia, India, Oregon, and Brazil are for one habitat zone will not be the optimum
all characterized by straight coasts, with all but for another. For example, the habitat zone of
0-25 m on the Oregon coast will reach its
Oregon developed along passive margins.
Even controlling for coasts that are approxi-maximum extent when sea level is 100 m
mately linear, the positions of the maxima vary lower than today, but a deeper-water habitat
from -100 m (Oregon) to +30 m (Georgia). Thezone of comparable breadth (75-100 m) will
reach its maximum extent when sea level is
overall form of the relationships for these
margins varies as well, from simple and uni-only 25 m lower than today. As a result, sea
modal (India), to bimodal (Georgia) and mul- level changes will affect different habitats to
timodal (Oregon and Brazil). different extents, with some increasing in area
Both the Persian Gulf and Adriatic Sea are and others decreasing for the same sea level
enclosed seas developed in foreland basins. change. On margins with simple area/ sea level
Both display a similar bimodal relationship, relationships (e.g., India, Bahamas, Florida),
with one maximum just above present this sea change in area across shelf habitats will
level (+10 m) and a higher maximum (+120 likewise
m be simple, but for margins with more
complex relationships (e.g., Brazil, Adriatic,
in the Persian Gulf, and +90 m in the Adriatic).
Persian Gulf), the changes in habitat area of
The two differ in substantially lower positions
of sea level, with the Persian Gulf showing
habitats across the shelf will be correspondingly
rapid flooding beginning near -80 m, and complicated.
with the Adriatic showing a more a gradual Habitats that differ in their extent will have
increase in habitable area at increasing sea
area /sea level relationships that differ in their
level positions. form (Fig. 4). In particular, habitats that
encompass a greater range of water depths
The Sunda Shelf, Bahamas, and Florida are
all broad nonlinear shelves, yet they (e.g.,
all 0-100 m in Fig. 4) will have simpler and
smoother area /sea level relationships than
display simple relationships between habit-
habitats that span a narrow range of water
able area and sea level, despite Bahamas and

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210 STEVEN M. HOLLAND

area as sea level changes, these responses sum

to form a global change in habitable area
(Fig. 5). For this plot, change in habitat area
was calculated for all latitudes between 60°N
and 60°S (Fig. 1). Polar regions were not
included, owing to the isostatic depression
of continental lithosphere under the Green-
land and Antarctic ice sheets, as well as the
ongoing and transient effects of glacial re-
bound in northern North America, Europe,
and Asia.

At this near-global scale, habitat area for 0-

25 m increases steadily from sea level positions
of -200 m to +10 m, declines rapidly to +50 m,
and is stable from +50 m to +200 m (Fig. 5, left).
This global pattern is much more similar to
coasts like Georgia, India, Sunda, and Florida,
although with substantially more elevations
above +100 m. The strongly bimodal or mul-
timodal patterns seen in some regions (e.g.,
Oregon, Brazil, Persian Gulf, Adriatic) are
absent at this near-global scale.
For habitats spanning a broader depth
range (e.g., 0-100 m), the pattern in the
area /sea level curve is smoothed and simpler
(Fig. 5, right). In particular, it lacks the rapid
drop in area above modern sea level. The
form of this curve is simpler, such that high
Figure 3. Plots of the extent of habitable area for the positions of sea level generally correspond to
Oregon and Washington coast of the United States, large habitable areas.
with
habitable area defined as 0-25 m (upper plot) and 75-
100 m (lower plot). Because habitable area covers a 25 m Discussion
depth range in both plots, the plots have the same form,
Most
but with the lower plot shifted 75 m to the right relative to previous thinking on the relationship
the upper plot. For two habitats with the same
ofdepth
shallow-marine habitat to sea level changes
range, the greatest extent in habitable area will occur at
different positions of sea level.
has focused on total continental shelf area,
which necessarily increases as sea level rises
depths (e.g., 0-25 m in Fig. 2). Habitatsand
thatdecreases as sea level falls (but see Wyatt
span a greater range of water depths have1995 and Jablonski 1985). Combined with a
less
species-area
fine-scale sensitivity to sea level changes and relationship (Rosenzweig 1995),
generally have a slower rate of change
thisin
has led to the simple and widespread
habitat area as a function of sea level position.
idea that transgressions foster diversification
For example, the fine-scale troughs thatand regressions promote extinction (e.g.,
appear
near the peak of the Georgia and Sunda Chamberlin
plots 1909; Newell 1952; Schopf 1974;
Boucot 1983; Benton and Emerson 2007; but
(Fig. 2) disappear for more broadly defined
see Crampton et al. 2011). Several factors
habitats (Fig. 4). Even larger-scale variations
(such as those on Oregon, Brazil, Persian Gulf,
complicate this view.
and Adriatic in Figure 2) are dampened to
Variability in Relationship of Habitable Area
eliminated for more broadly defined habitats
and Sea Level. - Even if topography is static,
(Fig. 4). the relationship between sea level and habit-
Global Effects. - Although regions have able area is complex, and this complexity is
strongly idiosyncratic responses in habitable revealed when habitable area is treated as

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 SI 1 Л I LOW-MA RI N1 HABITAT 211

Figure 4. Plots of shallow-marine area as a function of sea level for

shallow-marine habitat defined as spanning depths from 0 to 100 m.

specific depth ranges rather all othersthan

constant asmayall areas
change not only the
above the shelf-slope break, magnitude
that of increase or decrease in habitat
is, continen-
tal shelves. Whether a given area, but sea level
also the change
sign of that change. In short,
increases or decreases habitable transgressions do notdepends
area necessarily increase
not only on the amount habitat and area direction
and regressionsof sea
do not necessarily
level change, but also on decrease habitat area. Significantly,
the starting position a given sea
of sea level (Newell 1956; Johnson 1974; level change can increase the area of some
Hallam 1984; Valentine and Jablonski 1991; habitats in a region while decreasing the area
McRoberts and Aberhan 1997), the topograph- of other habitats in the same region, and the
ic configuration of a given region (Stanley effects of that sea level change may be dra-
1984a,b; Wyatt 1984; Jablonski 1985; Jablonski matically different in other regions.
and Flessa 1986; Aigeo and Wilkinson 1991; In addition, topography is not static. Topog-
Harries 2008), and the bathymétrie range that raphy evolves in part because of deposition:
is used to define habitable area (Newell 1971; the progradation of deltas and the growth of
Boucot 1983; Jablonski 1986; Paulay 1990; carbonate platforms are two obvious cases in
Valentine and Jablonski 1991; Schaaf 1996). which deposition changes the topographic
Varying any one of these factors while holding configuration of a region. Topography also

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212 STEVEN M. HOLLAND

Figure 5. Plots of habitable area (0-25 m on the left, 0-

60°S. This latitude range excludes the ice-covered lan
isostatically depressed by the weight of ice sheets.

evolves from plate one is tectonics and

marine. Even so, multiple studies have resultin
shown a species-area
vertical crustal motions. relationship within both
Rifting, cooling, fle
ural loading, epeirogenic
patchy (e.g., seagrass beds)
motions,
and linear (e.g., and dy
namic topography produced
intertidal) by
marine habitats (McKinney 1998;mantle u
welling (Allen and Neigel
Allen 2003; McLachlan
2005; and DorvloPetersen
2007). et a
Fossil marine support
2010) all generate vertical crustalfor a species-area
motions th
alter topography and physiography.
relationship is weak (Jablonski 2007), but this The as
sembly and breakup must beof
temperedsupercontinents
by the formidable difficulties also
control continental-scale in detecting such a relationship in the fossil with larg
topography,
er continents having record.aOnlyhigher
a few studies have average
attempted a elevati
than smaller continents correlation (Wyatt
of diversity with habitable
1984; area. Algeo and
Wilkinson 1991). Furthermore, Those at a global scale (Sepkoski 1976;supercontine
Peters
breakup increases the and Footelength2001; Martinof 2003) passive-marg
found that
coasts, which tend to have lower coastal habitable area explained no more than 5% of
gradients and therefore greater habitat areas the variance in diversity, suggesting that other
than steeper active-margin coasts (Algeo and factors such as provincial differentiation dom-
Wilkinson 1991). The collective result ofinate all diversity at this scale. Studies at regional
these processes is that the relationshipsscales be- (e.g., Hansen 1987; Roy et al. 1998;
tween habitable area and sea level seen at one Valentine and Jablonski 1991; Crampton et al.
moment in geologic time may differ substan- 2006) have found weak or no evidence of a
tially from those seen at another time (Wyatt species-area relationship. The greatest difficulty
1987). in all such direct correlations is obtaining a good
Species-Area Relationship. - Numerous stud- estimate of habitable area, because outcrop area
ies from modern terrestrial settings indicate a generally will not be a good proxy of habitat
positive relationship between species diversi- area (Flessa and Sepkoski 1978). Furthermore,
ty and habitat area (Rosenzweig 1995). Many the habitable area must be consistently sampled
fewer comparable studies from modern ma- through time, and fluctuations in sea level
rine settings have been conducted (Gray commonly change the habitats that can be
2001), and this is almost surely in part due sampled (Flessa and Sepkoski 1978; Holland
to the increased difficulty of sampling. For 2000; Peters and Foote 2001; Smith 2001).
example, of the 54 species-area correlations Owing to the difficulties of directly testing
reported by Flessa and Sepkoski (1978), only species-area relationships in the fossil record,

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 SHALLOW-MARINE HABITAT 213

two common alternative

a given seaapproaches include
level change, yet some component
testing for correlationshabitats might show either
of diversity with a rise or fall in
either
their
sea level (e.g., McGhee diversity,
1991, depending
1992; on the change in
McRoberts
and Aberhan 1997; Smith 2001)
area for that orhabitat.
particular rock area
and volume (e.g., RaupThe 1976;
presencePeters and Foote
of onshore-offshore diversity
2001; Crampton et al. 2003;
gradients McGowan
(e.g., Bambach 1977; Sepkoskiand
1988)
Smith 2008). Attempts addsto recognize
to the a correla-
variation in outcomes, depending
tion of diversity and on whether
sea level the habitats that experienced
are mixed, but
this is unsurprising given
the greatestthechangepoor relation-
in area were the most or
ship between sea level and For
least speciose. habitable area
example, if a large sea level
shown here. Correlations of diversity
change substantially with
decreased habitable area,
rock area and volumebut are commonly
particularly strong,
so in a species-poor habitat,
but this is generallythetaken to
net diversity indicate
change sam-
might be minimal. In
pling bias, althoughcontrast,
factors a minorthat promote
sea level change that had
widespread rock area and
little total high
effect on area diversity
but substantially
may share a common cause
affected (Miller
a particularly 1997a;
species-rich habitat
Peters and Foote 2002; Peters
might 2005).
considerably alter diversity.
A final approach to To fossil species-area
illustrate, the Arrhenius (1921) species-re-
area relationship can be used to simulate
lationships is to estimate the change in habit-
diversity as a function
able area during a particular sea level of sea level
change for two
(such as the Late Pleistocene), use the
modern passive margins, Georgiaspecies-
and south-
area relationship to ern estimate the
Brazil (same regions as inexpected
Fig. 1):
diversity change, and compare D = that
kAz with the
observed change. Two studies that used this
approach (Wise and Schopf 1981;
where D is diversity, Valentine
A is area, and z and к are
constants.less
and Jablonski 1991) found In thisdiversity
simulation, the same z of 0.2
change
(Valentine andthat
than expected, suggesting Jablonski 1991) is assumed for
species-area
three onshore-offshore
effects are not important, or that biotas habitats do
(shoreface,
not
transition
respond quickly to short zone [also known
eustatic as the offshore
fluctuations
such as those in the transition],
Pleistocene and offshore). (Simberloff
The parameter к is
1974; Wise and Schopf allowed1981; Valentine
to vary, with a midshelf maximum,and
Jablonski 1991; Harries 2008).
according to the onshore-offshore diversity
Implications for the Fossil
patterns Record
of Sepkoski (1988), withof Ma-
a value of 10
rine Diversity . - Evenfor the
if shoreface, 40 for the transition
few previous stud-zone,
and 20 for thehave
ies from the fossil record offshore. supported
The result, as could be a
species-area relationship,
expected, isthe
that the abundant evi-
habitats and the margins
dence for species-area display substantially different
relationships in responses
mod- to
ern terrestrial environments and the more the same sea level changes (Fig. 6). For both
limited evidence from modern marine envi- margins, the shoreface contributes little to
ronments suggest the need to exploreoverall how diversity, partly because it has the
species-area relationships might be manifest- lowest к value, but also because it spans the
ed in the fossil record. smallest depth range (0-15 m, versus 15-45
That different habitats on the same margin for transition zone and 45-105 for offshore).
can increase or decrease in area with the same Although diversity increases substantially on
sea level change, and that changes at smaller the Georgia margin from sea levels of -50 m
scales (e.g., the shoreface) might not mimic to +50 m, diversity changes are minimal on
the Brazil margin for the same interval.
those at larger scales (e.g., the entire shelf),
points to potentially complicated changesSimilarin results were obtained for other pairs
habitable area during any given sea level of geologically similar margins, such as the
change. For example, a given region might semi-enclosed foreland basins of the Persian
either increase or decrease in diversity duringGulf and Adriatic Sea. Diversity among

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214 STEVEN M. HOLLAND

Figure 6. Plot of diversity in three habitats as a fu

based on a species-area relationship, with z = 0.20 f
transition zone, and offshore. Shoreface habitat spans
from 45 to 105 m.

loss caused by a change in habitat area for this

habitats differs as well. For example, diversity
in the transition zone on the Georgia coast interval would require consistent sampling of
changes little from 0 to +60 m, but offshore shallow-water and deep-water habitats, some-
diversity rises steadily through that interval.thing that is not possible in this region. Simi-
In addition, the offshore on both margins larly, the failure to observe expected diversity
shows little variation in diversity comparedchanges during past sea level fluctuations (e.g.,
with the transition zone because the combi- Wise and Schopf 1981; Valentine and Jablonski
1991) may in part be due to inconsistent
nation of its lower к and its much greater
within-habitat sampling, which may be geo-
depth range makes it less sensitive to changes
in sea level. Simulations like this show how logically imposed rather than caused by poor
diversity might respond to sea level changes,sampling design.
but are not intended to portray any particular Sea Level and Diversity. - Abundant evi-
sea level change. Choosing other species-areadence from the fossil record suggests a
coefficients, and allowing the z-coefficient relationship
to between sea level and diversity
(Hallam 1989; Brett 1998), and sea level has
vary among environments can add more
variation to patterns of diversity duringstrong
sea support as an external mechanism for
level changes. mass extinctions (Jablonski 1986). Paleontolo-
gists have long noted a connection between
The nature of habitat preservation during
sea level changes (e.g., Jablonski 1980; Hol-
regressions and extinctions, as well as a link
between
land 2000; Smith et al. 2001) makes it likely transgressions and radiations.
that the habitats that can be sampled The will interpretation of these associations is
complicated by severe stratigraphie biases. As
change over geologic time, making it difficult
to isolate how changing habitat area justhas one typical example of many, Dockery
influenced diversity. For example, strata
(1986) noted five intervals bounded by the
abrupt appearance and disappearance of
recording the Cenomanian-Turonian extinc-
many mollusk species, with each bounding
tion in western Europe display a systematic
shift from the preservation of speciosehorizon
shal- corresponding to a combined se-
low-water habitats to depauperate deeper-
quence boundary and transgressive surface.
water habitats (Smith et al. 2001). Reading
These horizons are where abrupt first and last
the record at face value indicates a drop in
appearances would be expected even if rates
diversity, but this is largely an artifact of
of origination and extinction were constant
(Holland 2000), raising the question of how
habitat preservation. Recognizing a diversity

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 SHALLOW-MARINE HABITAT 215

The
much of this pattern is empirical connectionartifact
stratigraphie of faunal change
and sea level truly
and how much of it reflects has led to elevated
the proposal of
turnover driven by sea level changes. For
several mechanisms not involving habitable
example, Smith (2001) recognized that of
area, including the removal peaks
migration bar-
of extinction occur at predictable
riers (Chamberlin 1909; sequence
Bayer and McGhee
stratigraphie positions 1985; andGale suggested that
et al. 2000), changes this
in the number
association is largely stratigraphie of habitats (Paulay 1990;bias. Like-
Harries 2008), hy-
wise, Smith et al. (2001) regarded
poxia the 1989;
and anoxia (Hallam appar-Smith et al.
ent loss of shallow-water taxa at major 2001; Peters 2007), nutrients (Hallock and
flooding surfaces as reflecting the inconsistent Schlager 1986), changes in stress (Kauffman
preservation of shallow-water habitats. 1978), and temperature change associated
Disentangling stratigraphie artifact from with but not caused by sea level change
elevated turnover is difficult, but recent work (Valentine and Jablonski 1991), or a broad
suggests that some of this turnover is real. combination of mechanisms (McRoberts and
Peters (2005) found that there is a strong Aberhan 1997; Peters 2008). These mecha-
correlation of genus last occurrences and nisms may well operate during sea level
stratigraphie section last occurrences, but that changes, but the difficulty of directly recog-
this correlation is weaker than the corre-
nizing species-area effects in the marine fossil
sponding correlation of first occurrences. If the highly complex effects of sea
record and
stratigraphie architecture was the level primary
change on habitat area point to the need
cause of range truncations - of bothfor taxa and examination of the link between
renewed
stratigraphie sections - then these two corre-
sea level change and diversity in the marine
lations ought to be equal. That they differ
fossil record.
suggests that some of this turnover must have
Conclusions
an origin beyond stratigraphie architecture, in
other words, that turnover must truly be
1. Shallow-water habitable area is not a
elevated (Peters and Ausich 2008).
The connection between sea level and diver-simple function of sea level. In particular,
sity has been clouded by the lack of extinction level rise does not consistently increase
sea
habitable area and sea level fall does not
during several major sea level fluctuations.
consistently decrease habitable area.
For example, the Oligocene contains one of the
2. Different coasts display substantially dif-
largest known sea level falls, yet has no mass
ferent changes in area for the same sea
extinction (Stanley 1984a,b, 1986). Likewise,
the extreme and repeated Pleistocene sea levellevel fluctuations, and different habitats on
changes resulted in no appreciable extinction the same margin can also show marked
(Wise and Schopf 1981; Stanley 1984a, b; Val- differences in the change in area for the
same sea level fluctuations.
entine and Jablonski 1991; but see Paulay 1990
3. If shallow-marine area controls diversity
for a countering view). The results presented
here may reconcile the conflict between thethrough a species-area relationship, the
abundant anecdotal evidence for the impor- effect of sea level change on diversity will
not be simple and different regions would
tance of sea level change and the lack of broad
be expected to have different diversity
quantitative evidence of the link and the
presence of examples where sea level changetrajectories even if sea level were the only
control on marine diversity (e.g., Miller
did not result in substantial diversity change.
1997b). The diversity response to sea level
Strong variability in the response to sea level
change is to be expected, with idiosyncraticchange is likely idiosyncratic: the combi-
responses among habitats and margins. nation of the right sea level change at the
Expansions and contractions in area areright time on the right margin might
such a promising and intuitive mechanism produce a substantial diversity change,
that the failure to find convincing and whereas other sea level fluctuations of
comparable size might produce little or
consistent evidence has long been perplexing.

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216 STEVEN M. HOLLAND

Gale, A. S., A. B. Smith, N. E. A. Monks, J. A. Young, A. Howard,

no diversity change. These prediction
D. S. Wray, and J. M. Huggett. 2000. Marine biodiversity
agree with the widespread
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of
the Geological Society, London 157:745-757.
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Gray, J. S. 2001. Marine diversity: the paradigms in patterns of
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Marina 65:41-56.
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Hallam, A. as Annual
1984. Pre-Quaternary sea level changes. a who
Review of Earth and Planetary Sciences 12:205-243.

Acknowledgments
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in these analyses are deposited in the Transactions

Dryad of the Royal Society of Londo

repository: doi:10. 5061 /dryad. 4pt8h. This

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