Content uploaded by Max Semenovich Barash
Author content
All content in this area was uploaded by Max Semenovich Barash
Content may be subject to copyright.
848
ISSN 0001-4370, Oceanology, 2006, Vol. 46, No. 6, pp. 848–858. © Pleiades Publishing, Inc., 2006.
Original Russian Text © M.S. Barash, 2006, published in Okeanologiya, 2006, Vol. 46, No.6, pp. 899–910.
INTRODUCTION
The paleontological record documents periods of
the biodiversity growth and reduction with the former
process being dominant (Fig. 1). In the initial part of the
19th century, the catastrophism hypothesis, according
to which geological history represented alternating
periods with stable and catastrophic biota development,
was prevalent among paleontologists. In the middle of
the 19th century, Darwin’s ideas stimulated the devel-
opment of evolutionism concepts implying that the
sharp faunal changes observed in the sections are
explained by lacunas in geological records, i.e., by
stratigraphic hiatuses. New geological information
accumulated by the middle of the 20th century, prima-
rily the data on the events that occurred in the terminal
Permian, again attracted attention to the phenomenon
of mass extinctions. Additional periods of catastrophic,
strong, and rapid changes in the composition of marine
organisms on the family level have been revealed in the
Phanerozoic: the terminal Ordovician, Late Devonian,
terminal Permian, Triassic, Cretaceous, and many other
less catastrophic changes. Greater or lesser biodiversity
reduction occurred in geographically different areas
from the regional to global scales. The general progres-
sive development of the biota was distorted only once,
when the extensive mass extinction in the terminal Per-
mian (Paleozoic–Mesozoic boundary period) resulted
in a reduction of the biodiversity down to the initial
Ordovician level, i.e., threw it back 250 My. There were
also other episodes of mass extinction. These episodes
are of greatest interest because their study offers an
opportunity to reveal the abiotic factors that influenced
or could influence the biota development.
Extinction is considered as a catastrophic event
when the geographic area where its relevant paleonto-
logical manifestations are evident is of a near-global
scale. Mass extinctions influenced different organisms
in different ways depending on their type: benthic or
planktonic, tropical or extratropical, of narrow or wide
distribution, and others. This implies different causes
MARINE
GEOLOGY
Development of Marine Biota in the Paleozoic in Response
to Abiotic Factors
M. S. Barash
Shirshov Institute of Oceanology, Russian Academy of Sciences, Moscow, Russia
e-mail: barashms@yandex.ru
Received March 7, 2006; in final form, March 23, 2006
Abstract
—An analysis of the biota development in response to the changing abiotic factors shows that long
relatively stable periods of transgression, high-energy hydrodynamics, and diverse ecological niches are favor-
able for a growth of biodiversity and the abundance of organisms. Biota reduction is determined by sharp envi-
ronmental changes, particularly by multiple alteration of opposite development trends (transgression–regres-
sion, warming–cooling, and others). In addition, events harmful for the development of organisms such as glo-
bal anoxia in the oceans, powerful eruptions of trap basalts and volcanism, and collision of the earth with
extraterrestrial bodies negatively influence the biota evolution. The impact of different factors is particularly
notable during biotic crises. The abiotic factors influencing the biota development are determined by three fun-
damental causes: terrestrial, orbital, and extraterrestrial. Frequently, these causes and relevant factors were syn-
chronous or almost synchronous in terms of geological time. Inasmuch as there is no cause–effect relationship
between them, we can assume that large-scale environmental changes are determined by general extraterrestrial
factors originating beyond the solar system.
DOI:
10.1134/S0001437006060105
Number of families
500
0
600 400 200 0
Geological time, My B.P.
Cm O S D C P Tr J K T
–12% –14%
–12%
–52%
–11%
Fig. 1.
Family diversity of marine organisms in the Phaner-
ozoic (modified after [36]).
OCEANOLOGY
Vol. 46
No. 6
2006
DEVELOPMENT OF MARINE BIOTA IN THE PALEOZOIC 849
responsible for these catastrophes or, more exactly,
environmental conditions that resulted in the catastro-
phes. This paper focuses attention on the most signifi-
cant changes in the marine biota development during
the Paleozoic and on the relevant abiotic events.
DEVELOPMENT OF ORGANISMS
IN THE PALEOZOIC AND ABIOTIC FACTORS
Before the Phanerozoic, immediately prior to the
biota outburst in the Early Cambrian (
≥
540
My B.P.),
mass extinction took place in the Vendian. The extinc-
tion affected acritarchs and Ediacaran fauna. It is
assumed that this extinction was caused by the trans-
gressive–regressive cycle of sea level fluctuations
accompanied by anoxia and reduction of shallow-water
habitats [26]. Stratigraphic hiatuses at the Vendian–
Cambrian boundary indicating the sea level fall are of a
global distribution. This regression resulted from tec-
tonic movements, which were accompanied by rift for-
mation and plate accretion.
The Cambrian
(542.0–483.3 My B.P.). During the
period of 570–510 My B.P. in the terminal Proterozoic–
Early Cambrian, marine organisms experienced a sig-
nificant evolutionary renewal against the background of
the changing environments [10]. This event is termed as
the “Cambrian outburst.” The period of 542–513 My B.P.
of the Early Cambrian (hereinafter, ages are given after
[24]) was marked by a very rapid biota diversification
that lasted less than 15 My. For example, reef-building
archaeocyathids and soft-bodied organisms were repre-
sented by 240 and 120 genera, respectively, at that time.
At least four groups of organisms with mineral shells
(arthropods, mollusks, hyolithids, and brachiopods)
and organisms with spiculae, teeth, and others appeared
in the Vendian–Cambrian boundary period. Calcium-
producing microorganisms [31], burrowing organisms
(mud eaters), and trilobites appeared at that time as
well. Development of all these organisms stimulated
accumulation of organogenic limestones and the
organic substrate provided conditions favorable for
accumulation of granular phosphorites. The appearance
of predators became an important biological evolution-
ary factor.
Biological changes occurred against the background
of global physical and chemical changes. The high
spreading rates and growth of mid-oceanic ridges dur-
ing the break-up of the Proterozoic supercontinent
resulted in an ocean expansion and transgression. Melt-
ing of Proterozoic glacial sheets was an additional fac-
tor responsible for flooding of continents. The appear-
ance of additional ecological niches stimulated origina-
tion of new species. Saturation of the World Ocean
waters with oxygen in response to the vegetation devel-
opment provided prerequisites for evolution and diver-
sification of Metazoa. This period is particularly nota-
ble for mass development of organisms with mineral
skeletal elements, which are preserved in the fossil
state. Thus, in the considered case, the biodiversity
growth was determined by both tectonic (transgression)
and biochemical (enrichment of the waters with dis-
solved oxygen up to some critical level) factors. By the
end of the Early Cambrian, the biodiversity had
decreased: archaeocyathids had almost entirely disap-
peared and the number of genera of trilobites,
hyolithids, and other organisms had reduced. This pro-
cess is correlated with the negative
δ
13
C shift [14]. The
δ
34
S values confirm the intense sulfate reduction at the
sea bottom. Geochemical indicators suggest intense
burial of organic carbon under stagnant conditions.
This period was characterized by a global regression
and reduction of biotopes provided by epicontinental
seas.
The Ordovician
(488.3–443.7 My B.P.). The termi-
nal Cambrian crisis was followed by a new faunal
bloom reflected in the further development of trilobites,
brachiopods, bryozoans, graptolites, conodonts, echin-
oderms, corals, and various mollusks (nautiloids,
bivalves, and gastropods). The Ordovician biodiversity
peak coincided with the sea level rise, which was the
highest one in the Phanerozoic. Continental blocks sep-
arated by the oceans were characterized by endemic
faunas.
Nevertheless, the terminal Ordovician was marked
by the first of the five greatest global Phanerozoic biotic
crises, when 57% of the genera and over 25% of the
families became extinct [12]. Simultaneously, most of
the conodonts disappeared. The extinction affected the
shelf taxa. At the same time, new species appeared orig-
inating from the deepwater or bathyal taxa [9]. Approx-
imately 80% of the nautiloids became extinct at the end
of the Ordovician. The biotic crisis also affected plank-
tonic organisms: Chitinozoa and acritarchs. Brachio-
pod communities lost 150 of their 180 genera. Two
extinction periods are defined separated by a renewal
stage, when cold-resistant brachiopods advanced up to
the equator. Trilobites also experienced two extinction
stages, when the number of genera decreased from 113
in the Late Ordovician to 45 at the beginning of the Sil-
urian. The extinction affected all the pelagic forms and
many outer-shelf taxa, while shallow-water taxa sur-
vived relatively unchanged. It is assumed that all the tri-
lobites with pelagic larvae or adult forms became
extinct [21]. The crisis in the terminal Ordovician also
involved bryozoans and bivalves, particularly in coastal
communities. Approximately 60–70% of the coral ge-
nera became extinct. Due to the mass extinction of reef-
forming organisms, the development of reef buildups
almost completely ceased for several million years.
Thus, the mass extinction in the terminal Ordovician
took place during two phases separated by an extremely
strong, although relatively short, glaciation. This
extinction was critical for benthic forms and even more
catastrophic for pelagic (phytoplankton, graptolites, tri-
lobites) taxa. What were the factors responsible for the
mass extinction in the Ordovician? The areas that rep-
resented constituents of Gondwana in the Late Ordovi-
850
OCEANOLOGY
Vol. 46
No. 6
2006
BARASH
cian (northern Africa, areas in southern Europe and
South America) provide geological evidence for glaci-
ation: diamictic sediments, “boulder pavements.” Cor-
responding parts of Gondwana were located in high
southern paleolatitudes at that time. According to dif-
ferent estimates, at the end of the Ordovician, the sea
level became lower by 40–100 m.
The ratios of stable oxygen and carbon isotopes
indicate sharp ecological changes at that time [15]:
development of anoxic conditions and removal of the
light oxygen isotope from seawater during the forma-
tion of the Gondwana ice sheet. The accompanying
regression should have resulted in a sharp reduction of
shallow-water ecological niches. As is assumed, the
two-phase Late Ordovician extinction was related to
the sudden glaciation of Gondwana and its rapid degla-
ciation.
The glaciation onset stimulated the formation of
cold oxygen-enriched seawater in the coastal areas of
the near-polar Gondwana, which subsided and spread
over the sea bottom like the present-day Antarctic Bot-
tom Water mass. The enrichment of the near-bottom
waters with oxygen should have negatively affected the
organisms that had adapted to the oxygen-poor,
although nutrient-enriched environments (graptolites
and others). The second phase of the Late Ordovician
extinction was more intense and strongly affected the
middle- and outer-shelf biota. The following succes-
sion of events is assumed [27]:
(1) The precrisis phase (Rawtheyan Age): anoxic
deep-water conditions and development of correspond-
ing benthic organisms, accumulation of black shales,
development of graptolites at the upper levels of the
anoxic zone, productive surface waters with pelagic tri-
lobites, and formation of carbonate platforms.
(2) The first phase of extinction (beginning of the
Hirnantian Age, 445.6 My B.P.): beginning of the
Gondwana glaciation, ventilation of the ocean by cold
oxygen-enriched near-bottom waters, disappearance of
almost all graptolites, cooling in the tropical areas,
regression, karst processes in carbonate platforms, and
reduction of shallow-water habitats.
(3) The second phase of extinction (Ashgill–termi-
nal Hirnantian, 443.7 My B.P. ago): warming, deglaci-
ation, restoration of anoxic deepwater conditions,
transgression, extension of areas with black shale accu-
mulation up to the outer shelf, and development of
graptolites.
The middle Ashgillian global warming that pre-
ceded the Hirnantian glaciation is evident from the
migration of low-latitudinal benthic trilobites and bra-
chiopods to higher latitudes and from the increase in the
endemic faunas at low latitudes [22].
Assuming that the development of the glaciation on
the near-polar Gondwana occurred under conditions
similar to those responsible for the Cenozoic continen-
tal glaciation of Antarctica (location of the continental
block near the South Pole, formation of the Circum-
Antarctic Current, and others), the determining factor
of the crises was related to the horizontal motion of
lithospheric plates, i.e., to tectonics.
The Silurian
(443.7–416.0 My B.P.). The begin-
ning of the Silurian (early Llandoveri, approximately
443 My B.P.) was marked by postcrisis environments:
no reef buildups, impoverished bottom communities of
cosmopolitan species, and many surviving species were
scarce and missing in oryctocoenoses. During the first
5 My, the biota radiation was very slow. Lazarus taxa
and reefs appeared again only in the Wenlockian
(approximately 425 My B.P.), when faunal provinces
were restored, i.e., marine ecosystems entirely recov-
ered after the mass extinction in the terminal Ordovi-
cian [27].
In the Silurian, radiation of bathyal conodonts was
in progress. The first Silurian conodonts that appeared
in high latitudes originated from their thermophilic
taxa. In the Early Silurian, the number of conodont
families increased from seven to ten. Graptolites that
almost entirely disappeared in the terminal Ordovician
became widespread again in the Silurian: over 200 spe-
cies are known from the Lower Silurian sediments.
Cosmopolitan species appeared in brachiopod commu-
nities. The endemism degree and the diversity of faunal
assemblages reached the precrisis Late Ordovician
level. Radiation of corals commenced at the same time
(Late Llandovery) with formation of coral and stro-
matoporoid reefs. The sea level rise that started in the
terminal Ordovician was in progress in the initial Sil-
urian as well.
The Devonian
(416.0–359.2 My B.P.). The biotic
crisis at the Frasnian–Famennian (F–F) transition
period 374.5 My B.P. is one of the five great Phanero-
zoic mass extinction events. An additional Devonian
mass extinction took place in the terminal Famennian
Age, i.e., at the Devonian–Carboniferous (D–C) transi-
tion. An analysis of the extinction events discloses the
intricate patterns of the crisis: some groups of organ-
isms were subjected to the ecological stress in different
periods. Nevertheless, most extinction events corre-
spond to three Late Devonian crises. It is known that the
first of them that happened in the terminal Givetian
mostly affected shallow-water benthic communities of
low latitudes (brachiopods, rugose corals, and
ammonoids) [18, 27].
The second, most dramatic mass extinction (F–F)
affected thermophilic organisms (brachiopods and oth-
ers). At the same time, glassy sponges developed at low
latitudes, which indicates a cooling. Stromatoporoids,
tabulates, large foraminifers, and trilobites were among
the most affected reefal communities. Pelagic organ-
isms were also subjected to substantial changes: crico-
conarids became extinct; Agnatha representatives dis-
appeared almost entirely; and the conodont, ammonoid,
and placoderm diversities decreased. The third phase of
the mass extinction during the Devonian–Carbonifer-
ous (D–C) transition was marked by a disappearance of
OCEANOLOGY
Vol. 46
No. 6
2006
DEVELOPMENT OF MARINE BIOTA IN THE PALEOZOIC 851
placoderms and almost all of the ammonoid taxa. This
crisis strongly affected pelagic organisms, while
benthic taxa suffered to a lesser degree.
The Late Devonian sea level rise was maximal in the
Frasnian and terminated with its largest fall in the
Famennian. This general trend was complicated by sev-
eral fluctuations of a lower order. The sea level fall was
related to the formation of the Gondwana ice sheet as is
evident from the glacial sediments in South America. It
is assumed that the impact of glaciation on the biota
development was more significant during the last Devo-
nian crisis (D–C) as compared with the second mass
extinction event (F–F) [13].
In South China, the F–F boundary is marked by an
iridium anomaly, which is interpreted as either indicat-
ing an impact event or resulting from reducing pro-
cesses [43] (hereinafter, extraterrestrial impact events
or collision of the earth with extraterrestrial bodies, i.e.,
asteroids or cometary nuclei, are meant). Additional
evidence for extraterrestrial influence (microtektites
and impact craters) is known from China and Sweden.
Microtektites have also been found in the D–C bound-
ary layers. The most distinct signs of the asteroid
impact in the early Frasnian Age (approximately
380 My B.P.) are registered in North America (Nevada
and neighboring states). There, the corresponding sedi-
ments contain shocked quartz and an iridium anomaly and
involve the Alamo impact breccia representing a 70-m-
thick layer of shallow-water marine limestones frag-
mented into large blocks and covering an area 4000 km
2
in size [33]. Different hypotheses were proposed to
explain the influence mechanism of this impact event
on organisms. According to one of them, it was a giant
tsunami. The fall of a large asteroid into the ocean could
distort the water structure and poison the surface waters
with hydrogen sulfide from the near-bottom waters,
which is confirmed by the presence of pyrite enriched
in
δ
34
S.
The formation of anoxic conditions during the two
last Late Devonian (F–F and D–C) extinction events is
confirmed by the global accumulation of black shales,
the enrichment of the sediments with rare trace metals,
the increase in the
δ
34
S content in pyrite, the positive
δ
13
C shifts, and the dominant development of benthic
organisms tolerant to low oxygen concentrations in the
waters.
The cooling during the Frasnian and/or Famennian
ages is evident from the dominant extinction of reefal
and low-latitudinal organisms, the survival of cold-
resistant organisms during and after the crises, the gla-
ciation signs in Gondwana, and from the rapid sea level
changes. Copper [18] believes that this cooling could
have resulted from the convergence between the Gond-
wana and Eurasia continents, the blockage of equatorial
circulation, and the deviation of cold high-latitudinal
waters to the tropical zone. It is conceivable, however,
that the glaciation could have been caused by the devi-
ation of tropical waters to high latitudes, the formation
of frontal hydrological zones, elevated evaporation and
intense atmospheric precipitation on cold land areas,
the accumulation of snow, and the growth of the conti-
nental ice sheet. As is known, a similar tectonic and
paleoceanographic situation became the prerequisite
for the Pliocene–Quaternary glaciation in the Northern
Hemisphere. According to these concepts, global tec-
tonics was the main triggering factor responsible for the
cooling and relevant biota extinction.
The model proposed by Buggish in [16] and subse-
quent works also seems well substantiated. This model
describes the processes that could follow the above-
mentioned paleoceanographic changes. It assumes suc-
cessive events that constitute a closed cycle. The sea
level rise results in the flooding of shelves and the pro-
ductivity increase. The enhanced influx of organic mat-
ter stimulated the formation of anoxic conditions and
provoked the mass extinction of organisms. As in the
Late Cretaceous ocean, flooding of tropical shelves
resulted in the formation of high-salinity waters, which
spread over the Late Devonian deep ocean bottom and
provided stratification of the water column that pre-
vented vertical circulation and water ventilation. The
mass burial of organic carbon in the sediments
decreased the
ëé
2
content in the atmosphere to cause
cooling, formation of continental glaciers, and regres-
sion. These events were followed by shelf draining, a
productivity decrease, erosion and oxidation of black
shales, an increase in the
ëé
2
concentrations in the
atmosphere, transgression, etc. Thus, Buggish’s model
implies alternation of greenhouse and glacial condi-
tions in the Late Devonian.
The Carboniferous
(359.2–299.0 My B.P.). After the
Late Devonian mass extinction, the marine biota evolved
during 120 My without crises. In the initial Carboniferous,
actinopterids, gastropods, crinoids, rugose corals, brachi-
opods, foraminifers, bryozoans, ostracodes, and
ammonoids increased their diversity. The Tournaisian
epoch of the Carboniferous (359.2–345.3 My B.P.) was
also characterized by the radiation of fishes, which
resulted in the development of actinopterygians.
At the Early–Middle Carboniferous transition
(326.4 My B.P.) and in the initial Middle Carboniferous
(Serpukhovian Age), many organisms experienced,
however, an ecological stress, which resulted in the dis-
appearance of some ammonoid phyletic lineages.
Simultaneously, crinoids lost 42% of their genera or at
least suffered rapid and strong changes. The Giganto-
productidae family became extinct among brachiopods
and the diversity of Gondwanan brachiopod communi-
ties decreased from 51 to 5 genera. Although the reduc-
tion of the diversity among several groups of organisms
cannot be classed as mass extinctions, the environmen-
tal changes were significant at that time. The main
phase of glaciation in Gondwana that commenced in
the Late Devonian was in progress and resulted in a
substantial sea-level fall and narrowing of the climatic
852
OCEANOLOGY
Vol. 46
No. 6
2006
BARASH
belts, which should have provoked fauna migration
[37].
The Permian
(299–251 My B.P.). The mass extinc-
tion of organisms in the terminal Permian was the most
catastrophic in the earth’s history. The significant
changes in biotic communities determined the position
of the boundary between the Paleozoic and Mesozoic
eras. According to different estimates, from 75 to 96%
of all the species became extinct. The biodiversity of
marine organisms comparable with the present-day one
(approximately 250000 species) appeared to be
reduced down to the post-Ordovician minimal level
(less than 10000 species) with the number of families
being decreased from 650 to 420 [35]. The main feature
of the Permian paleogeography was the extension of
the Pangea supercontinent between the earth’s poles
and the existence of two oceans (Panthalassa and
Tethys) partly isolated by small continental blocks at
the eastern margin of the Tethys ocean.
The Late Permian was marked by the development
of large reefal buildups, which stopped for 7–8 My at
the end of the period. The Upper Permian boundary
limited the development of rugose and tabulate corals.
Bryozoans and echinoderms experienced almost simi-
lar mass extinctions. Benthic foraminifers suffered
strong changes: many of their families and all fusulin-
ids became extinct [4]. Complex tropical forms were
first subjected to the changes. Nodosariids and textu-
lariids appeared to be the least-affected groups among
foraminifers probably because of their feeding on detri-
tus, lower dependence on primary production, and bet-
ter adaptation to oxygen-poor environments. Shallow-
water ostracoda taxa experienced strong changes in the
terminal Permian, while their deepwater cosmopolitan
counterparts capable of living in oxygen-poor settings
were unaffected. The mass extinction at the end of the
Permian Period was the most dramatic in the brachio-
pod evolution: 90% of the families and 95% of the gen-
era became extinct [19]. Long-living groups populating
oxygen-poor zones more easily survived the crisis.
Among gastropods, forms with a wide geographic
distribution suffered less during the crisis. Prior to the
Permian–Triassic boundary, gastropods were diverse,
although not very abundant, while, in the Early Trias-
sic, they became less diverse and more abundant. It is
assumed that, similar to other predators (fishes, con-
odonts), ammonoids and nautiloids survived the crisis
relatively less damaged.
An analysis of the changes in the carbon isotope
ratios allows inference of a rapid decrease in the pri-
mary production at the end of the Permian. Radiolari-
ans passed through the entire Phanerozoic easily sur-
viving mass extinction events. Radiolarian cherts char-
acteristic of several Upper Paleozoic sections suddenly
disappear to appear again only 7–8 My later in the mid-
Triassic [28]. Nevertheless, 52% of the radiolarian fam-
ilies became extinct at the end of the Permian, which
resulted from the combined effect of the “volcanic win-
ter” and superanoxia [34].
The Late Permian extinction was in progress during
the Kazanian and Tatarian ages consisting of two
phases separated by a recovery period. The first phase
(Late Maokouan, approximately 262 My B.P.) was
marked by the extinction of most taxa of the Tethyan
fauna, while Boreal communities survived almost
unchanged. Later on (Lopingian, 260.4–253.8 My B.P.),
some groups (foraminifers; bryozoans; gastropods;
ammonoids; and, partly, brachiopods and bivalves)
increased their diversity. This was followed by the main
phase of mass extinction (Late Changxingian, approxi-
mately 250 My B.P.) [29].
Let us consider the possible factors responsible for
the extinction in the Late Permian. The terminal Per-
mian is traditionally considered to represent the period
of the lowest sea-level standing, which was followed by
the rapid Triassic transgression. The biotic crisis hap-
pened, however, several million years after the regres-
sion and, consequently, has nothing to do with sea-level
changes. The
δ
13
C
/
δ
12
C values in the Permian–Triassic
boundary period experienced sharp changes [11]. There
are several hypotheses proposed to explain this fact:
(1) oxidation of
δ
12
C-enriched organic matter (coal),
which accumulated in glossopterid bogs and was
exposed during the regression or orogenic uplift of the
southern Gondwana margins; (2) a catastrophic pri-
mary production decrease; (3) transition from the con-
ditions of a well-ventilated ocean with oxygen-
enriched waters to a stratified ocean with oxygen-free
near-bottom waters. The assumed stratified vertical
water structure and the primary production drop are
supported by the ceased accumulation of biogenic sil-
ica in the sediments and the radiolarian crisis.
The
18
O
/
16
O values changed in a similar way.
Among the hypotheses available, a rapid temperature
rise approximately by
6°ë
best explains the observable
negative
δ
18
O shift. The same effect could result from
the freshening of the upper water layer, which should
cause sharp vertical stratification and collapse of the
primary production. The Permian–Triassic boundary
period was characterized by a rapid
δ
34
S increase in the
sulfates of the seawater, which was caused by the
intense precipitation and burial of pyrite enriched in
the
32
S isotope. This confirms the wide development of
anoxic conditions in the ocean [17].
Several scenarios of the great extinction in the ter-
minal Permian were proposed based on an analysis of
the biological data and abiotic indicators; some of these
scenarios are alternative. The impact hypothesis is
poorly substantiated: only insignificant iridium anoma-
lies are found, although chondrite asteroids could leave
no notable impact traces. The sudden extinction of the
terrestrial flora and the temporal phytoplankton produc-
tivity collapse could have been caused precisely by an
impact event.
OCEANOLOGY
Vol. 46
No. 6
2006
DEVELOPMENT OF MARINE BIOTA IN THE PALEOZOIC 853
The relatively better-grounded hypothesis of the
global cooling explaining the mass extinction at the end
of the Permian has vulnerable points as well: the global
Gondwana glaciation terminated by the beginning of
the Permian. Cooling as a factor responsible for the
Permian extinction event is acceptable only for its first
phase (Maokouan), when precisely tropical taxa were
affected, regression was in progress, and glaciations
happened in Siberia and Gondwana.
Knoll with colleagues [31] proposed an hypothesis
that combines cooling and poisoning of organisms by
ëé
2
. The anoxic environments in the Late Permian
ocean and the burial of organic matter in the sediments
should have resulted in a seawater enrichment with car-
bon dioxide and hydrogen sulfide and a reduction of the
ëé
2
contents in the atmosphere. This could reduce, in
turn, the greenhouse effect and result in a global cool-
ing. The data available show, however, that opposite
trends were characteristic of the Late Permian: warm-
ing and transition from an oxygen-rich to an anoxic
ocean.
One more hypothesis explains the crisis by a cooling
caused by eruptions of tremendous volumes of tholei-
itic basalts in West Siberia estimated at
1.5–2.5
×
10
6
km
3
[38]. This was the largest on-land eruption of basalts in
the Phanerozoic. The formation of the Siberian traps
coincides with the mass extinction event in the terminal
Permian (
250
±
1.6
My B.P.). The assumption that this
eruption should have resulted in a global darkening is
supported by several facts: large sulfide ore bodies are
enclosed in trap formations, and the eruption was likely
accompanied by ejection of large SO
2
amounts. The
eruptions would have to have been largely explosive to
eject tremendous volumes of volcanic ash and sulfate
aerosols and cause a global darkening. This suppressed
photosynthesis, which is evident from the negative
δ
13
ë
shift, and destroyed food chains. The temperature fall
triggered glaciation and regression, shelf draining, and
destruction of shelf communities. The acid rains pro-
vided an additional stress for organisms. The taxa that
survived were then subjected to a pernicious overheat-
ing caused by the ejection of volcanic
ë
O
2
into the
atmosphere. Some aspects of this hypothesis are criti-
cized: there are no cooling indications, ash and lava
eruptions alternated and lasted for long periods, and so
on.
Sufficiently well grounded is also the hypothesis of
a sudden warming in the terminal Permian. This is con-
firmed, for example, by the negative
δ
18
O shift corre-
sponding to a warming by
6°ë
in the tropical zone of
the western Tethys. In the high southern paleolatitudes
of Antarctica and Australia, peat accumulation in the
Permian–Triassic transition period was replaced by for-
mation of temperate soils, and, in South Africa, the
moderate humid climate was replaced by a hot semi-
desert one [40]. Cold-resistant glossopterids became
extinct to give way to the flora of the temperate climate.
Eruptions of Siberian traps are considered to represent
a source of
ë
O
2
necessary for the greenhouse effect.
Inasmuch as the negative
δ
13
ë
shift commenced long
before the eruptions, an additional source of isotopi-
cally light
ë
O
2
was proposed: the oxidation of glossop-
terid coals of South Gondwana that were exhumed by
orogenic processes in the terminal Permian [20]. It is
assumed that the warming was accompanied by a gas
hydrate decomposition, which strengthened the green-
house effect. The global climate became regularly
warm or hot. The terrestrial fauna and, probably, tropi-
cal marine organisms could have died because of the
extremely high temperature, although, for the high-lat-
itude marine fauna, such warming could not be so per-
nicious.
The anoxic environments in the seas and oceans of
the Permian–Triassic transition period are confirmed
by many geological facts. The dominant survival of
nektonic and benthic organisms tolerant to oxygen-
poor environments, as well the accumulation of black
shales, suggest a stagnation of the near-bottom waters.
The extremely low
δ
34
S values similar to those in the
present-day Black Sea indicate the presence of free H
2
S
in the lower part of the water column.
The Late Permian anoxia event, which accompanied
the biotic crisis, lasted up to 8 My, being most mani-
fested during the period of 1–3 My [25]. The latter
authors share the opinion that this factor played the
main role in the biotic crisis. The advection of H
2
S-con-
taminated waters up to the surface and the emission of
hydrogen sulfide into the atmosphere provided condi-
tions ruinous to marine and terrestrial organisms. This
assumption is supported by the presence of diageneti-
cally transformed components of sulfuric Chloro-
phyceae algae as well as by the data on the C and S iso-
tope compositions, biomarkers, and iron.
Hallam and Vignall [27] assume the following sce-
nario. Oxidation of coals and eruptions of Siberian
traps increased the
ëé
2
concentration in the atmo-
sphere. The global warming resulted in a reduction of
dissolved oxygen in the seawater due to the decreased
solubility of oxygen in the water because of the ele-
vated temperature and the weakened circulation deter-
mined by the lowered temperature gradient between the
poles and the equator. The temperature-induced stratifi-
cation prevented the influx of nutrients into the near-
surface waters and resulted in a sharp reduction of the
primary production and stagnation. Some taxa disap-
peared, however, slightly prior to the Permian–Triassic
boundary period in response to the developing anoxia;
the sharp drop in the primary production immediately
at that period was just the last impact for the already
impoverished ecosystems.
According to the scenario proposed for the Per-
mian–Triassic biotic crisis in [32], eruptions of traps
were accompanied by ejection of tremendous ash and
aerosol volumes into the atmosphere: only in the east-
ern Tethys realm did volcanic ash cover an area at least
2
×
10
6
km
2
in size. This resulted in a sharp temperature
854
OCEANOLOGY
Vol. 46
No. 6
2006
BARASH
fall in the low latitudes with a volcanic winter lasting
3
−
6 months. Explosive eruption in the eastern Tethys
destroyed the ozone layer. Strong ultraviolet radiation
was responsible for the disappearance of almost all the
previously blooming fungi. One of such events
occurred prior to the Permian–Triassic boundary period
and another one followed 100–200 ky later. The high
content of aerosols in the atmosphere stimulated
intense atmospheric precipitation in the previously dry
areas. The freshened surface waters in the high latitudes
hampered vertical circulation and influx of the oxygen-
rich near-bottom waters into the low latitudes. This
stimulated wide development of anoxia in the ocean up
to shallow levels. Because of these events, thermophilic
benthic organisms of shelf communities that survived
the crisis in the tropical Panthalassa ocean could not
return to the Tethyan shelves during a period lasting
over 5 My. With the termination of the eruption of the
Siberian traps, volcanic ash and sulfate aerosols repre-
senting the main cooling factors ceased to neutralize
the global warming induced by the high
ëé
2
and water
vapor contents in the atmosphere. This global warming,
which was particularly strong in the high latitudes, was
responsible for the partial extinction of some taxa that
survived the main phase of the biotic crisis.
FACTORS RESPONSIBLE
FOR MASS EXTINCTIONS
An analysis of the biota development during the
Paleozoic reveals its relationships with abiotic factors,
i.e., the changes and events that are confirmed by geo-
logical and geochemical evidence. In many cases, such
biotic events appear to be synchronous or almost syn-
chronous (table).
The table shows that anoxia was the ultimate univer-
sal factor; practically always, it is responsible for mass
extinctions of marine organisms. It was combined with
other factors or was induced by them. Taken alone,
these factors could cause only partial extinctions of
marine organisms and reductions of their distribution
areas and ecological niches rather than a global crisis.
Mass extinctions could occur under conditions com-
pletely unsuitable for living in the marine environment:
anoxia, contamination of the waters with harmful
chemical substances, sharply reduced photosynthesis
and primary production (resulting from intense volcan-
ism or a “cosmic winter”), hard cosmic radiation, and
others.
Some studies [30] show that, when anoxia exceeds
a certain level of the H
2
S concentration, a chemocline
separating the H
2
S-saturated deep waters and the oxi-
dized near-surface layer could rapidly rise to the sur-
face. The H
2
S flux to the atmosphere should reach the
toxic level. This resulted in the destruction of the ozone
layer to increase the methane content up to 100 ppm.
The authors of [30] believe that similar conditions per-
nicious for organisms were characteristic of the termi-
nal Permian, Late Devonian, and Cenomanian–Turo-
nian periods. Other authors [39] consider mass extinc-
tions during the Permian–Triassic boundary crisis as
resulting from an extremely rapid release of methane,
ëé
2
, and H
2
S dissolved in deep waters in the case of
stagnation. The rapid rise of methane from deep waters
to the oceanic surface could result in mass deaths of
marine organisms, while its ejection into the atmo-
sphere to reach explosive concentrations of up to
5
−
15% could cause conflagrations ruinous for terres-
trial communities.
The above-mentioned and other hypotheses repre-
sent attempts to find genetic relationships between such
changes and the events or their parallel independent
influence on the environments and biota. These changes
result from some fundamental prime mover of terres-
trial or extraterrestrial origin.
After receiving evidence on the relation between the
mass extinction of organisms at the Cretaceous–Paleo-
gene transition and an impact event [8], a collision of
the earth with a bolide is considered as one of such
prime causes. Unambiguous features indicating impact
events such as large iridium anomalies, shocked quartz,
tektites, and others are, however, rare, while the insig-
Possible causes of mass extinctions in the Paleozoic
Geological time (My B.P.) Impact event Volcanism Cooling Warming Regression Anoxia and
transgression
Terminal Permian (251) ? + +
×
+
Late Maokouan (262) +
Devonian/Carboniferous (359.2) +
××
+
Frasnian/Famennian (374.5) + ?
××
+
Late Ashgillian (~450) + + + +
Terminal Early Cambrian (~513) + +
Late Precambrian (
≥
540) +
Note: (+) higher confidence level; (
×
) lower confidence level; (?) assumed.
OCEANOLOGY
Vol. 46
No. 6
2006
DEVELOPMENT OF MARINE BIOTA IN THE PALEOZOIC 855
nificant iridium anomalies can be explained by diage-
netic processes.
The earth is a typical object of the solar system;
meanwhile, abundant craters cover the surfaces of the
Moon, Mars, and the other nearest planets. Approxi-
mately 250–300 large asteroids, which are potentially
dangerous in the case of collision with them, are
located close to the earth. Craters observed on the
earth’s surface provide evidence for its multiple colli-
sions with asteroids during the Phanerozoic. Approxi-
mately 150 impact craters of different sizes and ages
are known nowadays. Intense exogenic processes on
the earth with its hydro- and atmosphere destroyed or
masked the signs of most of the impact events. In addi-
tion, it should be noted that selected impact events
could leave no notable signatures in the geological
record: falls of chondrite asteroids, collisions with com-
ets, or falls of extraterrestrial objects into the ocean. (The
only known evidence for an asteroid falling into the ocean
was found in the Bellingshausen Sea, where it is dated
back to the Late Pliocene (
~2.15
My B.P.); the size of the
extraterrestrial body is estimated to be over 1 km across
[23]).
Small impact events accompanied by insignificant
energy release are more frequent and less dangerous as
compared with their large and powerful counterparts
[42]. In the cases of collision with asteroids 4.5–6.0 km
across, the concentrations of dust and sulfates in the
atmosphere can reach values sufficient for reduction of
illumination to a level preventing photosynthesis. Con-
flagrations can involve areas exceeding
10
7
km2 in size
and, thus, additionally reduce the illumination. With an
energy release exceeding 107 megatons, the destruction
caused by the explosion and relevant earthquakes can
be of a regional scale (106 km2). They should be accom-
panied by tsunamis up to 100 m high, which would
cause destruction on shelves and coastal plains. In the
cases of impact events with an energy exceeding
109 megatons, surface waters might be globally oxi-
dized by the sulfur from the internal parts of comets and
asteroids, while the sulfate aerosol might provoke a cli-
matic shift. All these factors might provide global
stresses for the biota. Nevertheless, the role of impact
events in particular biotic crisis remains insufficiently
clear so far.
Some authors consider the intense eruption of trap
basalts as the main cause of mass extinctions. The rela-
tions between these phenomena are best exemplified by
the relations between such eruptions in Siberia and the
biotic catastrophe at the Permian–Triassic boundary,
eruptions in India (Deccan traps) and the great extinc-
tion at the Cretaceous–Paleogene boundary, and erup-
tions of basalts in the Arctic–Britain Province and the
biotic crisis in the terminal Paleocene. The influence of
the eruptions on the biota can be realized through sev-
eral potential mechanisms: ejection of large volumes of
CO2, SO2, and volcanic ash into the atmosphere; global
darkening; acid rains; and warming and anoxia devel-
opment in the ocean.
Mass extinctions usually coincide with climatic
changes reflected in both cooling and warming. Cool-
ing in high latitudes increases the temperature gradient
between the poles and equator; displaces climatic belts
and, correspondingly, distribution areas of organisms;
strengthens hydrodynamics; enhances water saturation
with oxygen; and can stimulate development of conti-
nental glaciations. It can also immediately negatively
influence thermophilic organisms by destroying their
biotopes. Short-term cooling episodes are related to
impact events and global darkening, while long-term
cooling events are explained by the decrease in the CO2
concentration in the atmosphere. “Terminations” or
rapid warming events after glaciations appear to be also
stressful for organisms because they reduce or destroy
habitat areas, weaken oceanic circulation, and stimulate
the development of anoxia in the ocean and mass
extinctions (terminal Ordovician, terminal Permian).
Recurrent alternation of continental glaciations and
interglacial periods during the Quaternary was deter-
mined by changes in the parameters of the earth’s orbit.
The reduction of epicontinental seas during the
regressions resulted in a disappearance of neritic organ-
isms. This explains the extinction of many shelf and
planktonic taxa during the terminal Ordovician regres-
sion in response to the formation of the Gondwana gla-
ciation, the first phase of the Permian extinction (Maok-
ouan), when the biotic crisis affected the low-latitudinal
fauna of limestone platforms and slopes and some oth-
ers.
The wide development of disoxia and anoxia in the
ocean is considered as the main immediate cause of
mass extinctions. This standpoint is supported by many
paleontological, geological, and geochemical data. The
development of oxygen-free zones is explained by
transgressions and reduced vertical oxygen advection.
The transgressions and regressions that occurred during
the entire Phanerozoic influenced biotic communities
only in the periods when they were rapid, significant in
amplitude, and global. They could have been caused by
short continental glaciations.
In addition to the above-mentioned abiotic factors
influencing the biota development, which are more or
less grounded by the geological and geochemical data,
there are also hypothetical causes based largely on the-
oretical calculations and assumptions. A significant
role in these hypotheses belongs to the concepts of
recurrent biotic crises. According to different calcula-
tions, there is a periodicity ranging from 20 to 30 My
depending on the basic data accepted. None of the val-
ues obtained predicts all the known extinctions: some
of them fall outside the calculated temporal interval or
do not correspond to the outlined periodicity.
If distinct periodicity were the case, this would con-
firm a common cause for the mass extinctions and make
its disclosure easier.
856
OCEANOLOGY Vol. 46 No. 6 2006
BARASH
The hypotheses of recurrent processes in the outer
core of the earth and at its boundary with the mantle
that are responsible for tectonic activity, contraction
and extension of the crust, and the changes in the mag-
netic field imply the influence of these phenomena on
the biosphere development [4, 6]. As is known, the
intensity of the geomagnetic field during polarity rever-
sals should decrease while irradiation of the earth’s sur-
face should correspondingly sharply increase. This
should unavoidably influence the biota development.
The distribution of the last and first appearance levels of
oceanic microplankton species suggests such a relation:
the number of these datum levels distinctly increases
during the Quaternary geomagnetic reversals [2].
There is also an opposite relation: the organisms
influence the geological and paleoceanographic pro-
cesses. Organic remains buried in the course of sedi-
mentation to form carbonate, siliceous, coaliferous, and
hydrocarbon-bearing sequences influenced the
geochemical processes in the external spheres of the
earth and changed the composition of the atmosphere
and the climate [7].
The background global evolution determined by
internal terrestrial causes was complicated by external
factors such as, for example, changes in the orbital
parameters and the precession of the earth’s axis, which
played a decisive role in the Quaternary continental gla-
ciations. Extraterrestrial factors also include an
increase in the cosmic radiation, intensification of elec-
tromagnetic and gravity fields, supernova star explo-
sions, and passing of the solar system through jets. It is
conceivable that the tidal forces in the earth–moon–
planets–sun system are also among the extraterrestrial
factors influencing the processes on the earth [1]. Such
a mechanism does not explain, however, impact events.
The idea of changes in the galaxy gravity field
related to the solar system motion is an inherent ele-
ment of the hypotheses assuming the influence of fac-
tors that are external relative to the solar system on the
terrestrial processes [5]. Of great interest is the calcula-
tion-supported viewpoint that assumes passing of the
earth, together with the solar system, through cosmic
jets originating in the galactic nucleus to be important
for terrestrial processes including tectonics, the cli-
mate, and mass extinctions [3].
CONCLUSIONS
An analysis of the marine biota development and its
relation to the changes in abiotic factors shows that the
long-term stable periods of transgressions, high-energy
hydrodynamics, and diverse ecological niches are
favorable for diversification and quantitative bloom of
organisms. Rapid environmental changes, particularly
multiple alternation of opposite development trends
(transgression–regression, warming–cooling, and so
on) result in biota reduction. In addition, other phenom-
ena such as global anoxia in the ocean, intense erup-
tions of trap basalts and volcanism, and collision of the
earth with extraterrestrial bodies (impact events) play
an unambiguously negative role in the biota develop-
ment.
Some of the above-mentioned factors, which pre-
sumably immediately influenced the ecological
medium and, correspondingly, biotic communities, are
partly subordinate and interrelated. Others acted simul-
taneously or successively and, probably, autonomously
(Fig. 2). The study of different factors that are synchro-
nous or almost synchronous in terms of geological time
implies some prime causes of a higher order.
The particular abiotic factors of the biota evolution
can be reduced to three basic prime causes. The tec-
tonic factor is undoubtedly decisive in determining the
large-scale paleoceanographic evolution of the ocean
and its organisms. Horizontal movements of lithos-
pheric plates formed the global patterns of the spatial
location of the continents and oceans over the earth’s
surface. Their spatial combinations determined the con-
figuration of different World Ocean segments and their
interrelationships. In addition, the spreading rates influ-
enced the sizes of the mid-oceanic ridges and the depths
of the basins, i.e., the integral capacity of oceanic reser-
voirs and, consequently, the sea level standing as well
as the outlines of the oceans and shelf seas. Vertical tec-
tonic movements opened and closed seaways that were
important for the oceanic circulation system. The loca-
tion of oceans, continents, and geographic poles deter-
mined the circulation in the ocean and its hydrological
structure, the atmospheric circulation, and the develop-
ment of continental glaciations in the Northern and
Southern hemispheres.
Accumulation of significant volumes of fresh water
in ice sheets decreased the integral volume of the
ocean; lowered its level; and, correspondingly, changed
the configuration of the shoreline, increased the seawa-
ter salinity, the earth’s albedo, and the temperature gra-
dient between the poles and the equator. These pro-
cesses strengthened both the surface and deep oceanic
circulations. Degradation of continental glaciations
stimulated the development of opposite processes.
The chemical composition and physical properties
of the atmosphere and ocean changed under the influ-
ence of volcanism. Other forms of matter and energy
release from the earth’s interior such as hydrothermal
solutions, methane emanations due to the gas hydrate
decomposition, and others, as well as opposite pro-
cesses such as accumulation and fixation of different
chemical components from the seawater and atmo-
sphere in the sediments, also influenced these parame-
ters.
The background global evolution determined by
internal terrestrial causes was complicated by external
factors such as, for example, changes in the orbital
parameters and precession of the earth’s axis, which
played a decisive role in the Quaternary continental gla-
ciations. As was shown, some biotic crises occurred
OCEANOLOGY Vol. 46 No. 6 2006
DEVELOPMENT OF MARINE BIOTA IN THE PALEOZOIC 857
synchronously or almost synchronously with cata-
strophic extraterrestrial impact events, i.e., falls of large
asteroids on the earth or its collisions with comets. The
paleoceanographic evolution resulted from and was the
core of these processes. The marine biota development
occurred against the background of the paleoceano-
graphic evolution and was largely determined by the
later.
The evidence for sharp changes in the biota develop-
ment in different periods or several almost synchronous
abiotic events with unknown cause–effect relationships
or undoubtedly lacking them provide grounds to
believe that large-scale changes in the natural environ-
ment on the earth are influenced by general extraterres-
trial factors originating beyond the solar system.
REFERENCES
1. Yu. N. Avsyuk, Tidal Forces and Natural Processes
(OIFZ RAN, Moscow, 1996) [in Russian].
2. M. S. Barash, Quaternary Paleoceanology of the Atlan-
tic Ocean (Nauka, Moscow, 1988) [in Russian].
3. A. A. Barenbaum, Yu. B. Gladenkov, and N. A. Yasa-
manov, “Geochronological Scales and Astronomic Time
(State-of-the-Art),” Stratigr. Geol. Korrelyatsiya 10 (2),
3–14 (2002).
4. N. L. Dobretsov, “Geological Factors of Global
Changes. Significant of Catastrophes and Periodicity of
Processes,” Geol. Geofiz. 35 (3), 3–19 (1994).
5. V. P. Korchagin, “Changes in the Gravity Field of the
Galaxy and the Relation of the Organic Evolution on the
Earth to Them,” in Most Important Biotic Events in the
Earth’s History. Trans. 32nd Session of VPO (Tallinn,
1991), pp. 27–34 [in Russian].
6. E. E. Milanovskii, “On the Phase Correlation of the Fre-
quencies of Geomagnetic Field Inversions, Level Falls of
the World Ocean, and Enhancement of the Compression
Deformations of the Earth’s Crust in the Mesozoic and
Cenozoic,” Geotektonika, No. 1, 3–11 (1996).
7. O. G. Sorokhtin and S. A. Ushakov, Evolution of the
Earth (MGU, Moscow, 2002) [in Russian].
8. L. W. Alvarez, W. Alvarez, F. Asaro, and H. V. Michel,
“Extraterrestrial Cause for the Cretaceous–Tertiary
Extinctions: Experimental Results and Theoretical Inter-
pretation,” Science 208, 1095–1108 (1980).
9. H. A. Armstrong, “Biotic Recovery after Mass Extinc-
tion: The Role of Climate and Ocean State in the Post-
Glacial (Late Ordovician–Early Silurian) Recovery of
the Conodonts,” in Biotic Recovery from Mass Extinc-
tion. Geol. Soc. Spec. Publ. 102 (1996), pp. 105–117.
10. L. E. Babcock, “Interpretation of Biological and Envi-
ronmental Changes across the Neoproterozoic–Cam-
brian Boundary: Developing a Refined Understanding of
the Radiation and Preservational Record of Early Multi-
cellular Organisms,” Palaeogeography, Palaeoclimatol-
ogy, Palaeoecology 220 (1-2), 1–5 (2005).
11. A. Baud, M. Magaritz, and W. T. Holser, “Permian–Tri-
assic of the Tethys: Carbon Isotopes Studies,” Geol.
Rundsch. 78, 649–677 (1989).
12. M. J. Benton, “Diversification and Extinction in the His-
tory of Life,” Science 268, 52–58 (1995).
13. U. Brand, “Global Climatic Change in the Devonian–
Mississippian: Stable Isotope Biogeochemistry of Bra-
chiopods,” Palaeogeography, Palaeoclimatology, Palae-
oecology 75, 311–320 (1989).
Biota development
Connections
between basins
Tectonics (horizontal
and vertical
movements) Volcanism
Terrestrial processes Orbital Extraterrestrial
Biota degradation,
biotic crises
Stagnation
Hydrological structure
of the ocean
Cosmic
winter,
Greenhouse
effect,
Chemical
changes
Climate
Impact event
and dynamics
Sea
level
Fig. 2. Causes and factors responsible for marine biota development and degradation.
858
OCEANOLOGY Vol. 46 No. 6 2006
BARASH
14. M. D. Brasier, R. M. Corfield, L. A. Derry, et al., “Mul-
tiple δ13ë Excursions Spanning the Cambrian Explosion
to the Botomian Crisis in Siberia,” Geology 22, 455–458
(1994).
15. P. J. Brenchley, J. D. Marshall, G. A. F. Carden, et al.,
“Bathymetric and Isotopic Evidence for a Short-Lived
Late Ordovician Glaciation in a Greenhouse Period,”
Geology 22, 295–298 (1994).
16. W. Buggisch, “The Global Frasnian–Famennian "Kell-
wasser Event”," Geol. Rundsch. 80, 49–72 (1991).
17. G. E. Claypool, W. T. Holser, I. R. Kaplan, et al., “The
Age Curves of Sulfur and Oxygen Isotopes in Marine
Sulfate and Their Mutual Interpretation,” Chem. Geol.
28, 199–259 (1980).
18. P. Copper, “Frasnian–Famennian Mass Extinction and
Cold-Water Oceans,” Geology 14, 835–839 (1986).
19. D. H. Erwin, “The Permo–Triassic Extinction,” Nature
367, 231–236 (1994).
20. K. Faure, M. J. de Wit, and J. P. Willis, “Late Permian
Global Coal Hiatus Linked to13C-depleted CO2 Flux into
Atmosphere during the Final Consolidation of Pangaea,”
Geology 23, 507–510 (1995).
21. R. A. Fortey, “There Are Extinctions and Extinctions:
Examples from the Lower Palaeozoic,” Phil. Trans. Roy.
Soc. London B325, 327–355 (1989).
22. R. A. Fortey and L. R. M. Cocks, “Late Ordovician Glo-
bal Warming—The Boda Event,” Geology 33 (5), 405–
408 (2005).
23. R. Gersonde, F. T. Kyte, U. Bleill, et al., “Geological
Record and Reconstruction of the Late Pliocene Impact
of the EItanin Asteroid in the Southern Ocean,” Nature
390, 357–363 (1997).
24. F. M. Gradstein, L. G. Ogg, A. G. Smith, et al., A Geo-
logical Time Scale (Columbia Univ. Press, New York,
2004).
25. K. Grice, C. Cao, G. D. Love, et al., “Photic Zone Eux-
inia During the Permian–Triassic Superanoxic Event,”
Science 307, 706–709 (2005).
26. A. Hallam, “The Case for Sea-Level Change As a Dom-
inant Causal Factor in Mass Extinction of Marine Inver-
tebrates,” Phil. Trans. Roy. Soc. London B325, 437–455
(1989).
27. A. Hallam and P. B. Wignall, Mass Extinctions and Their
Aftermath (Univ. Press, N.Y. Oxford, 1997).
28. Y. Isozaki, “Superanoxia across the Permo–Triassic
Boundary Recorded in Accreted Deep-Sea Pelagic Chert
in Japan,” Canadian Soc. Petrol. Geol. Memoir. 17, 805–
812 (1994).
29. Y. Jin, J. Zhang, and Q. Shang, “Two Phases of the End-
Permian Mass Extinction,” Canad. Soc. Petrol. Geol.
Memoir. 17, 813–822 (1994).
30. L. R. Kump, A. Pavlov, and M. Arthur, “Massive Release
of Hydrogen Sulfide to the Surface Ocean and Atmo-
sphere During Intervals of Oceanic Anoxia,” Geology 33
(5), 397–400 (2005).
31. A. H. Knoll, R. K. Bambach, D. E. Canfield, and J. P. Grot-
zinger, “Comparative Earth History and Late Permian Mass
Extinction,” Science 273, 452–457 (1996).
32. H. W. Kozur, “Some Aspects of the Permian–Triassic
Boundary (PTB) and of the Possible Causes for the
Biotic Crisis Around This Boundary,” Palaeogeography,
Palaeoclimatology, Palaeoecology 143 (4), 227–272
(1998).
33. H. Leroux, J. E. Warme, and J.-C. Doukman, “Shocked
Quartz in the Alamo Breccia, Southern Nevada: Evi-
dence for Devonian Impact Even T,” Geology 23, 1003–
1006 (1995).
34. G. Racki, “Silica-Secreting Biota and Mass Extinctions:
Survival Patterns and Processes,” Palaeogeography,
Palaeoclimatology, Palaeoecology 154, 107–132 (1999).
35. D. M. Raup, “Size of the Permo–Triassic Bottleneck and
Its Evolutionary Implications,” Science 206, 217–218
(1979).
36. D. M. Raup and J. J. Sepkoski, Jr., “Mass Extinction in
Marine Fossil Record,” Science 215, 12501–1503
(1982).
37. A. Raymond, P. H. Kelley, and C. B. Lutken, “Dead by
Degress: Articulate Brachiopods, Paleoclimate, and the
Mid-Carboniferous Extinction Event,” Palaios 5, 111–
123 (1990).
38. P. R. Renne, Z. Zhang, M. A. Richardson, et al., “Syn-
chrony and Causal Relations between Permo–Triassic
Boundary Crises and Siberian Volcanism, Science 269,
1413–1416 (1995).
39. G. Ryskin, “Methane-Driven Oceanic Eruptions and
Mass Extinctions,” Geology 31 (9), 741–744 (2003).
40. R. M. H. Smith, “Changing Fluvial Environments across
the Permian-Triassic Boundary in the Karoo Basin,
South Africa and Possible Causes of Tetrapod Extinc-
tions,” Palaeogeography, Palaeoclimatology, Palaeo-
ecology 117, 81–104 (1995).
41. H. Tappan and A. R. Loeblich, Jr., “Foraminiferal Evolu-
tion, Diversification, and Extinction,” J. Paleontology
62, 695–714 (1988).
42. O. B. Toon, K. Zahnle, D. Morrison, et al., “Environ-
mental Perturbations Caused by the Impact of Asteroids
and Comets,” Reviews of Geophysics 35 (1), 41–78
(1997).
43. K. Wang, C. J. Orth, M. Attrep, et al., “Geochemical Evi-
dence for a Catastrophic Biotic Event at Fras-
nian/Famennian Boundary in South China,” Geology 19,
776–779 (1991).
