AMER. ZOOL., 34:23-32 (1994)
Biodiversity in Geological Time1
PHILIP W. SIGNOR
Department of Geology and Center for Population Biology,
University of California, Davis, California 95616
SYNOPSIS. The numbers of animal and plant species extant on Earth
have fluctuated dramatically through geological time. Animals and vascular plants were absent from the first three billion years of Earth history,
although there is ample evidence of prokaryotic life in rocks as old as 3.5
billion years and fossil eukaryotic organisms in rocks as old as 2.0 billion
years. The Cambrian Metazoan Radiation, during a geologically brief
interval about 540 million years ago (Ma), saw the appearance of most
classes and orders of skeletogenous marine invertebrates. Vascular plants
appeared in a subsequent radiation in the mid-Paleozoic (~400 Ma),
followed closely by terrestrial vertebrates.
Over the past 400 million years, the trajectories of taxonomic diversity
among marine invertebrates, vascular plants, and terrestrial vertebrates
were roughly congruent; there were relatively few taxa in each group in
the late Paleozoic followed by a striking increase from the late Mesozoic
to the levels observed today. The reasons for these increases remain
unclear, but both physical and biological processes are likely to have
played important roles. Occasional mass extinctions severely reduced
taxonomic diversity over geologically brief intervals of time. However,
recovery from mass extinctions was invariably a prolonged process. The
lesson that diversity, once lost, is regained only slowly over geologic time
must not be forgotten as plans are developed to mitigate the coming
biodiversity crisis.
INTRODUCTION
The Earth's rich abundance and profuse
diversity of plant and animal life has long
provoked interest and inspiration for poets,
philosophers, naturalists and biologists. The
variety of species present in virtually every
habitat known to humans, from alpine tundras to oceanic abyssal depths, is unfailingly
impressive and is sometimes truly staggering. We are almost invariably overwhelmed
in our efforts to list or tabulate the numbers
of species present within single habitats, let
alone whole provinces or realms. Likewise,
estimates of the numbers of species within
the major clades have been speculative at
best. For example, attempts to estimate the
total number of arthropod species on Earth
• From, the symposium Science as a Way of Know-
ing—Biodiversity presented at the Annual Meeting of
the American Society of Zoologists, 27-30 December
1992, at Vancouver, Canada.
have produced results that vary by as much
as an order of magnitude {e.g., Erwin, 1982;
May, 1988; Thomas, 1990). Consequently,
the number of species extant on Earth today
is not well constrained (Wilson, 1985, 1988,
1992; May, 1988).
Not surprisingly, it has been even more
difficult to chronicle the history of diversity
in geological time. The difficulties inherent
in estimating the number of extant species
at any one time in the history of life {e.g.,
the Recent) are compounded by the notorious shortcomings of the fossil record,
These difficulties were in large measure
responsible for extended debates over patterns of taxonomic diversity through geological time (see Signor [1990] for summary). Attempts to reconstruct the history
of marine metazoan species richness through
geological time were based on different
m
f inferring
,
°
the species
present in
K
,
< _.•
ages past, and produced Strongly divergent
results. Debate between proponents of
23
24
PHILIP W. SIGNOR
steady-state, "equilibrium" diversity (e.g.,
Raup, 1972; Gould et al., 1977; Sepkoski,
1978) and their opponents (Valentine, 1970;
Valentine et al, 1978; Signor, 1978, 1982)
continued for more than a decade before
reaching apparent resolution (Sepkoski et
al, 1981). This decade of conflict mirrored
earlier debates between the progressionists
and the uniformitarians of the 19th century.
The subsequent decade has seen the continued development of a consensus on general
qualitative patterns of marine metazoan
diversity through time (Sepkoski, 1988,
1991; Signor, 1990).
Our knowledge of the evolutionary history of the terrestrial realm is weak in comparison to the fossil record of marine organisms. Terrestrial arthropods (especially
insects) dominate tabulations of metazoan
species richness in the modern world but
terrestrial environments are poorly represented in the stratigraphic record (e.g., Ager,
1981). As a direct consequence, terrestrial
floras and faunas constitute a disproportionately small fraction of the fossil record.
Nevertheless, there is sufficient evidence
available in the fossil record to reconstruct
the broad outlines of evolutionary history
within the terrestrial realm.
PATTERNS OF BIODIVERSITY IN
GEOLOGICAL TIME
The number of species on Earth has been
a dynamic variable through geological time,
fluctuating between dramatic lows following mass extinctions and intervening peaks
of diversification. The first fossil evidence
of Metazoa is found in rocks believed to
date from approximately 600 Ma, although
there is some evidence to suggest the history
of metazoans predates those fossils (e.g.,
Runnegar, 1982; but see Erwin, 1989). The
radiation of skeletogenous Metazoa began
in the Cambrian, at approximately 540 Ma.
The first convincing fossils of vascular plants
are found in rocks of Silurian age (~420
Ma), although older evidence has been
reported (e.g., Gray et al., 1982). Commencing during the Cretaceous period, at
about 144 Ma, there was an extended interval of parallel diversifications in the marine
and terrestrial realms that reached a unique
peak within the past few million years. While
human activities have apparently resulted
in a fair number of extinctions over the past
thirty thousand years, the number of species
extant today is far greater than was characteristic of most of life's history.
The central problem in reconstructing
patterns of diversity in the geological past
is to reach beyond the problems inherent in
analysis of the fossil record. As in the modern world, species are the fundamental unit
of biodiversity in geological time (e.g., Wilson, 1992). But tabulations of the numbers
of species extant in each age of the geologic
past require extensive surveys of the literature. Such surveys are extraordinarily time
consuming and have not been attempted,
although Raup (1976a) compiled an extensive survey based on the Zoological Record.
More importantly, surveys of the numbers
of described species are notoriously vulnerable to biases reflecting patterns of preservation and sampling effort (e.g., Raup, 1972,
1976a, b). The closely similar trends in sediment volume, sediment area, and numbers
of described species (Raup, 1976a, b) is a
classic example of the relationship between
sampling and diversity in geologic time (Fig.
1). On the other hand, complete censuses
of higher taxa (e.g., orders, families, or genera) are more easily obtained. For example,
one of the earliest published tallies of global
metazoan taxonomic diversity was Sepkoski's (1978; also see Newell, 1967) tabulation of marine orders through time. Sepkoski (1978) constructed an explicit defense
of the use of higher taxa (e.g., families or
orders) as a surrogate for species diversity,
and employed ordinal diversity to infer that
the numbers of extant marine species had
been constant since the late Ordovician
(~440 Ma). Subsequently, this methodology has been implicitly rejected in favor of
estimates based upon families or other data
(Sepkoski et al., 1981; Sepkoski, 1991).
Any attempt to employ higher taxa as surrogates for species begs the question of the
relationship between orders, families, or
genera and the numbers of species they
include. Higher taxonomic units, even if
cladistically defined, are conceptually distant from the phenomena of species. There
is little reason to suggest that numbers of
higher taxa should closely track species rich-
25
BIODIVERSITY IN GEOLOGICAL TIME
ness. In fact, subsequent work suggests the
opposite: higher taxonomic levels are
increasingly unlikely to reflect species-level
events (Signor, 1985, 1990; but see Sepkoski, 1991;SepkoskiandKendrick, 1993).
For the present, it seems most reasonable
to work as close to the species level as possible, and employ genus or, if necessary,
family level data when estimating species
diversity.
Tert
Apparent Species Diversity
h600
^
400 2
Crct
Dev
Ord
Sil
Carbon
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j
u r
-200
Camb
600
|
O-
500
400
300
200
100
0
Tert
The marine realm
•0.3
Geologic Map Area
The most complete history of metazoan
Cret
life is to be found in the fossil record of
skeletogenous marine invertebrates. Valentine (1989) demonstrated that the potenTri
tial taxonomic completeness of the marine
Sil Dev
Perm,
?rmi 1
record is quite good; 77 percent of CaliforCarbon
Camb Ord
—I
Jur
nia's modern fauna is represented in the
Pleistocene fossil record. The missing spe- 600
500
400
300
200
100
cies are mostly small, fragile, or rare, or they
inhabit deep-water environments. How- Estimated Volume
Tert
ever, this potential is rarely achieved; by
Dev
r-i-5 g
any absolute criterion the record must be
Tri
Perm,—, j u r
hl.0 £
judged woefully incomplete. Almost cerCrel
Camb Ord
tainly fewer than 10 percent, and possibly
-0.5
fewer than 1 percent, of the marine skeletogenous species that existed in the past have 600
500
400
300
200
100
0
been recovered from the fossil record
(Signor, 1985). The major loss of species FIG. 1. Numbers of described marine species, areas
exposure, and volumes of rock from each period of
from the record is probably during times of of
the Phanerozoic. Modified from Raup (1977a, b).
low sea stands, when no sediments are Reproduced, with permission, from the Annual Review
deposited on the continental shelves (see of Ecology and Systematics, vol 21, © 1990 by Annual
Sadler, 1981), and by the loss of sediments Reviews, Inc.
through erosion or metamorphism (Gregor,
1970, 1985; Blatt and Jones, 1975).
Within marine habitats, only a third of higher taxa, especially those lacking durable
the macroscopic benthic species typically skeletons, are found in Lagerstdtten such as
possess durable skeletons, and can reason- the Burgess Shale. Such faunas permit verably be expected to occur in the fossil record ification that ancient faunas were far more
(Johnson, 1964; Lawrence, 1968; Schopf, diverse and complex than is evident from
1978). This suggests that even when the fos- the "normal" fossil record. But Lagerstdtten
sil record is relatively complete, which it are too rare to have significant effect on direct
usually is not, it will only include about one- counts of species.
third of the marine benthic species.
The most thoroughly documented reconUnusual fossil occurrences (Lagerstdt- struction of diversity in geologic time is Septen), such as the famous Middle Cambrian koski's (1979, 1984, 1991) tabulation of
Burgess Shale Fauna (Whittington, 1985; marine metazoan families (Fig. 2). That hisConway Morris, 1989) or the Jurassic Soln- tory is complex, but there is a relatively
hofen Limestone (Barthel, 1990), allow us simple pattern underlying the apparent
access to the soft-bodied animals that are complexity. It opens with the most specusually absent from the fossil record. Con- tacular diversification in the history of anisequently, the first occurrence of many mal life (Sepkoski, 1979, 1991; Glaessner,
s.
26
PHILIP W. SIGNOR
200-
Orders
Birds
0
€
800-
O S D ' C ' P '•» J ' K
T
N
o
u
I
Families
6004002000
°'sf~D
100-
| L.K- | U.K. | Pg N ;
FIG. 3. Taxonomic diversity of terrestrial animals
through time. Vertebrate data is from Benton (1985a,
b) and Padian and Clemens (1985). Insect data is from
Niklas(1986).
Genera
50-
0
|MIS5|PEN|
€ ' O 'S D ' C ' P '•»' J ' K ' T
€
100-
O S D
C ' PV
J
K
T
Species
€
O 'S' D
C ' P 'Ti' J
K
T
FIG. 2. Numbers of marine orders, families, genera,
and species through the Phanerozoic. Data on orders
and families are from Sepkoski (1978, 1984). Estimated numbers of genera and species, expressed as a
percent of modern diversity, are from Signor (1985).
1984; Erwin et al., 1987; Valentine et al.,
1991). Many of the orders and classes of
marine invertebrates first appeared at this
time. The rapid increase in the numbers of
higher taxa continued until the Ordovician,
when diversity leveled off. The Ordovician
level of diversity was maintained until the
great Permian Mass Extinction (~245 Ma),
when more than 50 percent of the marine
families became extinct (Raup, 1979; Sepkoski, 1979, 1984; Erwin, 1990). Subsequently, the number of families increased
more or less steadily to the present day (Sepkoski, 1984, 1991). There are now nearly
twice as many easily preserved marine families than at the highest point of the Paleozoic. This increase presumably reflects a
similar increase in the numbers of skeletogenous marine species.
The terrestrial realm
Recent compilations of the diversities of
vascular plants (Niklas et al., 1980, 1983,
1985; Niklas, 1986) and terrestrial vertebrates (Benton, 1985a, b; Padian and Clemens, 1985) reveal patterns that are strikingly
similar to the history of marine diversity
(Fig. 3). The numbers of terrestrial vertebrate orders increased rapidly following the
origination of amphibians, reaching a high
in the Permian. Following the Permian mass
extinction (~245 Ma), the number of orders
rebounded and increased to a level approximately 50 percent higher than the Permian
peak. Following the Cretaceous (K-T) mass
extinction, the number of orders increased
rapidly by a factor of five to the levels
observed today. The pattern of change at
the generic level is similar, although more
exaggerated (Padian and Clemens, 1985).
Compilations of the number of families
of vascular plants recorded from the Northern Hemisphere show relatively low numbers in the Paleozoic and through most of
the Mesozoic, followed by a dramatic
increase in the late Cretaceous and Cenozoic
(Fig. 4) (Niklas et al., 1980, 1983, 1985;
Niklas, 1986). This increase reflects the
origination and diversification of the angio-
BIODIVERSITY IN GEOLOGICAL TIME
27
421 408 360
286 248 213
144
65
2
sperms; the number of non-angiosperm
700
vascular plant families remained essentially
unchanged. At the species level, the general
pattern is one of nearly continuous increase
driven by the sequential radiations of pteridophytes, gymnosperms, and angiosperms (Fig. 4).
The fossil record of insects traditionally
has been regarded as a poor reflection of
insect evolution, although recent research
indicates the record of insects is much better
than generally appreciated (Labandeira and
Sepkoski, 1993). The record suggests that
the diversification of insects roughly mirrors the diversification of vascular plants
(Strong et ai, 1984; Carpenter and Burnham, 1985; Niklas, 1986). Insects first
appear in the Devonian (~400 Ma) and
diversify more or less continuously thereafter (Strong et ai, 1984; Carpenter and
Burnham, 1985, Labandeira and Sepkoski,
FIG. 4. Taxonomic diversity of vascular plants
1993). The apparent revolutionary rela- (Northern
Hemisphere only) through geologic time.
tionship between the insects and vascular Data is from Niklas et al. (1980, 1983, 1985) and Nikplants, especially angiosperms, is a striking las (1986).
aspect of the history of terrestrial life (Strong
et ai, 1984; Niklas, 1986; but see Labandeira and Sepkoski, 1993, for a contrasting
view).
diversification observed in the fossil record.
However, attempts to identify any single
CONTROLS ON BIODIVERSITY
critical factor are probably naive; the probThe trends in global biodiversity over lem is more likely to involve many factors
geologic time summarized above suggest acting at different intensities and in different
that the modern world is not representative combinations through geological time. In
of other, earlier times in the history of life. order to understand fluctuations in diversity
Consequently, analyses of diversification in the geologic past it is necessary to deterthat depend upon the modern world as a mine the relative contribution of each promodel for events of the past might be mis- cess to global diversity through geologic
leading. Furthermore, excessive concentra- time. This effort remains to be undertaken
tion on modern biotas might lead one to and may well prove to be unmanageably
overlook important, rare but intense {e.g., complex, although work by Bambach (1977,
mass extinctions) or slow {e.g., plate tecton- 1983) and Sepkoski (1988, 1991) represent
ics) biological and physical processes that significant contributions toward underexert a profound influence on diversity. For standing the components of global marine
these reasons, analyses of biodiversity in diversity.
geologic time yield important insights into
the nature of processes controlling biodi- Biological controls
versity.
The numbers of species within marine
The processes that control diversity over habitats seem to have increased through time
geological time have been the subject of in an apparently stepwise pattern (Bamconsiderable speculation (see Signor, 1990). bach, 1977). Nearshore, physically stressed
Over the past two decades, authors have environments show no increase in species
identified a number of processes that were richness through geologic time (Fig. 5). But
believed to contribute to the patterns of there were strong increases in diversity
28
PHILIP W. SIGNOR
Variable
High Stress
Nearshore
Environments Environments
Cenozoic
5 -| •
5 -|
Open Marine
Environments
5
25
50
75
100
125
150
175
200
KEY
Middle
Paleozoic
25
50
Number of Species
in Samples
(in groups of
5 species)
Lower
Paleozoic
25
25
50
25
50
FIG. 5. Species richness in marine benthic environments through geologic time. Data is from Bambach (1977).
within variable nearshore environments and
open marine environments beginning in the
Cretaceous (Fig. 5) (Bambach, 1977). Interestingly, Bambach (1983, 1986) found no
increase in resource partitioning through
geologic time. Instead, the increasing numbers of species were accommodated through
the creation of new "guilds," or ecological
roles within a community.
A further increase in species richness
derives from a reduced similarity in the
composition of coeval marine benthic communities through geologic time (Sepkoski,
1988, 1991). Sepkoski examined patterns of
faunal similarity among contemporaneous
communities in the Paleozoic, and found a
significant decrease after the Cambrian
period. Sepkoski (1991) speculated that the
increases in within-habitat richness documented by Bambach (1977) and the
decreasing faunal similarity between coeval
communities were sufficient to account for
the changing global diversity during the
Paleozoic and, perhaps, throughout the
entire Phanerozoic.
Ausich and Bottjer (1982) postulated that
marine benthic diversity has increased
through time as a function of space utilization above and below the sediment-water
interface. Their data demonstrate that space
utilization has increased since the early
Paleozoic, but it is unclear what processes
control space usage. Ausich and Bottjer
(1985) contend that changes in tiering influ-
BIODIVERSITY IN GEOLOGICAL TIME
29
enced diversity through geological time, and has been substantiated by multiple lines of
had a particularly strong influence in the physical evidence. The newly discovered
Chicxulub crater in Yucatan, dated at 65
Paleozoic.
Ma (Swisher et al., 1992), is only the most
Physical controls
recent evidence supporting the K-T asterThe extended Mesozoic to Recent diver- oid-impact hypothesis. There is now limsification of marine species might have been ited evidence that impacts could be assodriven, at least in part, by plate tectonics ciated with other extinction events {e.g., the
(Valentine and Moores, 1972; Valentine et late Devonian extinction: Claeys et al.,
al, 1978; Schopf, 1979; Cracraft, 1985; 1992). Another hypothesis proposed to
Signor, 1990). The breakup of the Mesozoic account for mass extinctions is global coolsupercontinent into many dispersed land ing (Stanley, 1984). The cooling hypothesis
masses provided for the independent evo- is actually consistent with the asteroidlution of marine communities associated impact hypothesis, since the proximal cause
with each land mass. Interestingly, analyses of the impact-generated extinction would be
of terrestrial vertebrate diversity through cooling caused by dust high in the atmotime do not suggest such a strong influence sphere.
by plate tectonics (Benton, 1990, 1991),
THE INEVITABILITY OF EXTINCTION
although the importance of continental drift
in vertebrate evolution is unquestioned {e.g.,
Extinction is the inevitable fate of all speSimpson, 1980). Similarly, the role of bio- cies {e.g., Raup, 1978, 1982, 1986). For
geography in plant diversity in the Northern example, not a single species of the CretaHemisphere appears to be less important ceous period, which ended only 65 million
than total land area and the area of uplands years ago, remains extant. That interval of
(Tiffney and Niklas, 1990).
time represents only about 10 percent of the
Occasional mass extinctions, interspersed history of animal life. The median duration
through the history of life, are recognized of species within clades varies from less than
by a massive reduction in the numbers of one million years (for mammals and trilospecies extant and the loss of large numbers bites) to as much as 20 million years (for
of higher taxa (Raup and Sepkoski, 1982). corals and foraminifera) (Stanley, 1979).
The extinction at the end of the Permian Careful planning and mitigation measures
period (~245 Ma), the Permo-Triassic mass can prolong the survival of an endangered
extinction, is generally recognized as the species, but they only delay the inevitable.
most severe in the history of life (Raup,
This is not to imply that such efforts are
1979; Erwin, 1990). Other major mass without value. Significant durations of geoextinctions occurred at the end of the Ordo- logic time are apparently necessary to
vician (~438 Ma), during the late Devonian replenish diversity. Mass extinctions may
(-367 Ma), at the end of the Triassic (-208 have occurred in geologically brief, perhaps
Ma), and at the end of the Cretaceous period instantaneous, intervals, but the regenera(65 Ma). Another, previously unrecognized tion of marine diversity following mass
mass extinction occurred near the end of extinctions required millions of years (Septhe Early Cambrian (~515 Ma: Signor, koski, 1984, Hansen, 1988). Terrestrial ver1992).
tebrate diversity recovered more quickly
While the causation of mass extinctions following the Cretaceous-Tertiary mass
is still very much the subject of debate, and extinction, more than tripling the number
there is no substantial body of evidence to of orders by the end of the Paleocene (Lilsuggest that mass extinctions share a com- legraven, 1972). The relatively rapid,
mon cause, it is becoming increasingly clear although not sudden by any human stanthat at least one mass extinction is linked dards, radiation of mammals probably
to a physical event. The asteriod-impact reflects the generally more rapid evolutionhypothesis (Alvarez et al., 1980) for the ter- ary rates of mammals (Stanley, 1979). Stanminal Cretaceous (or K-T) mass extinction ley (1979) estimated the time required to
30
PHILIP W. SIGNOR
double the number of species within a clade
of marine metazoa during an adaptive radiation; his doubling times ranged from millions to tens of millions of years. Similarly,
the diversification of marine metazoan species beginning in the mid-Mesozoic continued at a modest pace, requiring over 140
m.y., with only occasional interruptions such
as the Cretaceous-Tertiary mass extinction.
The long times, even on geologic time scales,
necessary to reconstitute diversity are not
available for human enterprises. The most
enduring human civilization has lasted only
a small fraction of that time. Maintenance
of biodiversity is thus a crucial component
of efforts to manage biological systems.
What is frequently overlooked, however,
is the other parameter of the biodiversity
problem; the origination of new species
(Vermeij, 1986). We must make provision
for the origination of new species if the
Earth's biodiversity is to be maintained
indefinitely at some level near that of the
recent past. Providing for new species
requires commitment to the long term preservation of diversity. Of course, this proposition requires knowledge of the conditions favorable for the origination of species.
Despite many years of study, the process(es)
of speciation remains a murky proposition.
CONCLUSION
The Earth's biota includes far more species today than it has in the past. Parallel
diversifications in the marine and terrestrial
realms have more than doubled the numbers of species that were present 100 million
years ago. The proximal and ultimate causation of these diversifications are unknown,
but biological and extrinsic physical controls undoubtedly play important roles.
Mass extinctions were a powerful counteraction to the diversifications within the
marine and terrestrial realms. The tempo of
the marine and terrestrial faunas' recovery
following mass extinctions suggests that
diversity, once lost, is not quickly regained.
Therefore, it is imperative that biodiversity
be conserved to the maximum extent feasible.
ACKNOWLEDGMENTS
This research was supported by the
National Science Foundation (EAR 91-
117569). Thanks to J. J. Sepkoski, Jr., and
Geerat Vermeij for discussions of the material presented herein. J. H. Cooper and J. J.
Sepkoski, Jr., read the manuscript and suggested many improvements. J. J. Sepkoski,
Jr., kindly provided me with the unpublished manuscript by Labandeira and Sepkoski on the fossil record of insects.
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