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AUTHORS
James W. Castle � Department of Environ-mental Engineering and Earth Sciences,Clemson University, Clemson, South Carolina29634; [email protected]
Jim Castle is a professor at the Departmentof Environmental Engineering and Earth Sciencesat Clemson University, where he investigatesgeological and environmental aspects of energyresources. He also studies modern natural andexperimental systems to better understandprocesses relevant to past and future environ-mental change. He received his Ph.D. in geologyfrom the University of Illinois.
John H. Rodgers Jr. � Department ofForestry and Natural Resources, Clemson Uni-versity, Clemson, South Carolina 29634;[email protected]
John Rodgers received his Ph.D. from VirginiaPolytechnic Institute and State University in1977. He is currently a professor at ClemsonUniversity, the director of the EcotoxicologyProgram in the Department of Forestry andNatural Resources, and the codirector of theClemson Environmental Institute. His researchinvolves a quest for accurate risk character-izations and development of sustainable riskmitigation tactics.
ACKNOWLEDGEMENTS
We gratefully acknowledge Lee Gerhard andFred Rich for their insightful and very helpfulreviews. We also thank Gerald Baum, Editor ofEnvironmental Geosciences at the time themanuscript was submitted, who very capablymanaged the review and editorial process forthe article from start to finish.
Hypothesis for the role oftoxin-producing algae inPhanerozoic mass extinctionsbased on evidence fromthe geologic record andmodern environmentsJames W. Castle and John H. Rodgers Jr.
ABSTRACT
Mass mortalities of invertebrates, fish, birds, and mammals caused
by algal-produced toxins are occurring in modern environments. In
addition to direct effects of these toxins, the large mass of organic
material produced by algal blooms can lead to oxygen depletion
during decay, which indirectly causes death of some biota. Toxin-
producing algae occupy a wide range of modern marine, brackish,
and freshwater environments. Their growth is favored by warm wa-
ter temperatures, increased inorganic carbon concentrations (e.g.,
CO2), and abundant nutrient supplies in aquatic environments. Cya-
nobacteria (blue-green algae) are responsible for most of the disease
and death caused by algal toxicity today.
Based on characteristics and occurrences of algae in modern
aquatic environments and on observations from the fossil record, we
propose that toxin-producing algae were present in the geologic past
and were an important factor in Phanerozoic mass extinctions. The
geologic record demonstrates a pronounced increase in abundance
and environmental range of algae, including stromatolitic cyanobac-
terial mats, coincident withmajor Phanerozoicmass extinctions. Dur-
ing these past events of algal expansion, population decline of meta-
zoan taxa could have been caused by effects of algal blooms, including
algal-produced toxins, at a scale sufficient to generate a fossil record of
mass extinction. Environmental changes such as climaticwarming, sea
level fluctuation, and increased nutrient supply may have promoted
algal blooms over vast expanses ofmarine to freshwater environments.
From the increasing frequency of modern, toxin-producing algal
blooms, which may be related to global warming, another massive bi-
otic crisis could be forthcoming.
Environmental Geosciences, v. 16, no. 1 (March 2009), pp. 1–23 1
Copyright #2009. The American Association of Petroleum Geologists/Division of EnvironmentalGeosciences. All rights reserved.
DOI:10.1306/eg.08110808003
INTRODUCTION
We hypothesize that cyanobacteria, and probably other
types of algae, produced toxins in the geologic past that
caused or contributed to Phanerozoic mass extinctions.
To test this hypothesis, we examined the chronologic
distribution of cyanobacteria during the Phanerozoic
and studied the array and effects of toxins produced by
modern cyanobacteria. Recent data show that certain
species of algae, particularly cyanobacteria (blue-green
algae), produce quantities and types of toxins sufficient
to cause mass mortalities of organisms.
Global warming is interpreted as contributing to
Phanerozoic mass extinctions by decreasing biodiver-
sity and populations (Hallam, 2004;Mayhew et al., 2008).
However, modern, toxin-producing species of algae
are demonstrating the ability to expand their range and
drastically increase their densities as global tempera-
tures increase (Paul, 2008). Warmer temperatures are
causing increased frequency of toxic algal blooms (Hal-
legraeff, 1993; Harvell et al., 1999).
Only a few studies have considered the potential
role of algal toxins in causing mass deaths in prehis-
toric time. Toxic algal blooms were interpreted by
Emslie et al. (1996) to be associated with a death assem-
blage of marine birds found in late Pliocene sediments
of Florida. Braun and Pfeiffer (2002) interpreted toxic
algal blooms as causing the death of a large mammal
assemblage preserved in Pleistocene lake beds of Ger-
many. Their conclusionwas based on biochemical data
indicating that pigments and possibly toxins character-
istic of cyanobacteria are present in carbonate sediment
layers containing physical evidence of algal origin. Based
on studies of Holocene coral reefs, Hallock and Schlager
(1986) suggested that increased nutrient supply, caus-
ing the growth of plankton and mucilage-producing
algae, resulted in the death of coral reefs during extinc-
tions.They concluded that corals are injured by increased
bacterial densities, which cause oxygen depletion, by
sulfide poisons that accumulate at the coral surface
below themucous layer, and by predation of weakened
coral polyps.
GEOLOGIC EVIDENCE
Cyanobacterial Stromatolites
Algal growth occurs in marine and freshwater environ-
ments as planktonic blooms, benthic mats, and benthic
domes and columns (Figure 1A). The geologic record
of benthic algae is much more complete than that of
planktonic forms, which are poorly preserved during
sediment accumulation and burial. In the rock record,
direct evidence for benthic algal abundance is preserved
primarily in cyanobacterial stromatolites (Awramik,
1990; Riding, 1991a; Schopf, 2000a) (Figure 1B). A
stromatolite was defined by Pratt (1982) as an organo-
sedimentary structure produced by activities of micro-
organisms. Stromatolites are formed by microbial mats
Figure 1. (A) Modern cyanobacterial mat of supratidal zone onAndros Island, Bahamas. Mat growth produces sediment lam-ination and doming. Genera of cyanobacteria identified in matson Andros Island includeGloeocapsa, Aphanocapsa, Phormidium,Schizothrix, Plectonema, and Scytonema (Black, 1933; Monty,1972), all of which have ancient counterparts in the geologicrecord (Schopf, 2004). Length of scale bar (lower left) = 5 cm(1.9 in.). (B) Ancient stromatolite showing sediment laminationand doming. Green River Formation (Eocene), Wyoming. Origininterpreted as algal-formed stromatolite in a lacustrineenvironment (Surdam and Stanley, 1979; Lamond and Tapanila,2003). Length of scale bar (lower left) = 5 cm (1.9 in.).
2 The Role of Toxin-Producing Algae in Phanerozoic Mass Extinctions
that trap andbind sediments (Sheehan andHarris, 2004).
Cyanobacteria are responsible for forming marine and
nonmarine stromatolites over a wide span of geologic
time, with the first stromatolites appearing at approxi-
mately 3450Ma (Awramik, 1984, 1990; Riding, 2000).
Ancient stromatolites are strikingly similar in their in-
ternal structure and distribution to modern cyanobac-
terial mats, which are found in diverse areas, including
Andros Island in the Bahamas, Shark Bay and Spencer
Gulf of Australia, the Arabian Gulf, Solar Lake (Sinai),
and the Vizcaino Peninsula of Baja California (Black,
1933; Golubic, 1976a, b; Krumbein et al., 1977; Bauld,
1984; Upfold, 1984; Bauld et al., 1992; Farmer, 1992).
Lyngbya and other genera of cyanobacteria form stro-
matolitic structures in a variety of modern freshwater
andmarine environments (Golubic, 1976b; Gerdes and
Krumbein, 1994). Environmental conditions that pro-
mote the growth of stromatolites and oncolites in shal-
low waters would also favor extensive growths of plank-
tonic algae in limnetic or littoral zones of aquatic systems.
Cyanobacteria are important in the geologic record
because of their ability to precipitate, trap, and bind sed-
iment and because of their extreme versatility, thriving
under normal to extreme conditions of salinity, pH, tem-
perature, humidity, oxygen and carbon dioxide levels,
and light (Schopf, 2000b, 2004). Cyanobacteria are re-
markable in that they have the longest well-defined
fossil record of all major organism types (Riding, 1991b)
and have changed little over billions of years (Schopf,
1993, 1999). Geologic data demonstrate that the rela-
tive abundance of stromatolites varied chronologically
during the Phanerozoic, with increased abundance co-
incident with mass extinctions (Figure 2).
Mass Extinctions
In terms of geologic time, mass extinctions are cata-
strophic events through which many species do not sur-
vive. These events are characterized by a severe decline
in species diversity (Figure 2); the numbers of organisms
affected are not taken into account. Based on biostrati-
graphic and lithostratigraphic studies of the rock record,
five major mass extinctions during the Phanerozoic
have been recognized: end Ordovician, Late Devonian
(boundary between Frasnian and Famennian stages),
end Permian, end Triassic, and end Cretaceous (Raup
and Sepkoski, 1982; Sepkoski, 1986;Hallam andWignall,
1997; Hallam, 2004). Evidence for an increase in stro-
matolite abundance associated with these mass extinc-
tions has been reported from the rock record for all
except the end-Cretaceous event (Figure 2, Table 1).
End Ordovician
The end-Ordovician extinction is unique in that it fol-
lowed one of the greatest biotic radiations of the Phan-
erozoic (Brenchley, 1989). Most major fossil groups,
including trilobites, echinoderms, nautiloids, corals, bra-
chiopods, graptolites, conodonts, and acritarchs, de-
clined in abundance and diversity during this event
(Brenchley, 1989, 1990). The end-Ordovician mass ex-
tinction has been attributed to temperature and sea
level changes associated with growth and subsequent
melting of the Gondwanan ice sheet (Barnes, 1986;
Brenchley 1989, 1990; Hallam, 1990) (Table 2); wide-
spread anoxia, represented in the rock record by black
shales, may have also contributed (Hallam, 2004).
From studies of Lower Silurian rocks, Sheehan (2001)
and Sheehan and Harris (2004) noted a resurgence
of stromatolites associated with the end-Ordovician
extinction.
Late Devonian
During the Frasnian–Famennian (Late Devonian) mass
extinction, pelagic and shallow-water ecosystems of trop-
ical and subtropical regions were most severely affect-
ed; fauna living in deep water or high latitudes were
impacted to a lesser extent (Joachimski and Buggisch,
1993). Major groups that declined include corals, stro-
matoporoids, brachiopods, foraminifera, bryozoans, tri-
lobites, fishes, cephalopods, and conodonts; reef systems
were severely affected globally (McGhee, 1990, 1996).
Anexception is the glass sponges (hexactinellids),which
diversifiedwhile other organismswere declining greatly
(McGhee, 1990, 1996). As many organisms were ex-
periencing a drastic decline during this time, cyanobac-
terial colonies initiated extensive expansions in platform-
margin environments and formed reeflikemound struc-
tures atop dead coral and stromatoporoid reefs (McGhee,
1996; Chen et al., 2001, 2002; Chen and Tucker, 2003).
Calcispheres, probably representing phytoplankton,
also flourished at this time (Chen and Tucker, 2003).
Relative abundance of stromatolites, calcified marine
cyanobacteria, and microbial carbonates increased at the
approximate time of the Frasnian–Famennian extinc-
tion (Figure 2).
The Frasnian–Famennian mass extinction has been
attributed to sea level fluctuations, anoxic conditions,
and global climatic changes (Johnson et al., 1985; Mc-
Ghee, 1989; Joachimski and Buggisch, 1993; Chen et al.,
2002).Copper (1986) suggested that themass extinction
was caused by climatic change induced by paleogeogra-
phy (i.e., ocean closure between Laurussia and Gond-
wana), whereas Sandberg et al. (1988) interpreted the
Castle and Rodgers 3
cause of the Frasnian–Famennian mass extinction to be
climatic change triggered by bolide impact. McLaren
(1970) andMcGhee (1996) suggested bolide impact as
catastrophically causing the mass extinction.Wilde and
Berry (1984) interpreted the cause of the mass extinc-
tion to be poisoning by overturn of deep anoxic waters.
Isotopic data and atomic ratios of carbon, nitrogen, and
phosphorous from rocks near the Frasnian–Famennian
boundary are consistent with eutrophication as causing
the extinction (Murphy et al., 2000). Large masses of
algal material may have accumulated on the sea floor
leading to anoxia (Chen and Tucker, 2003).
In a study of strata in the Canning Basin of Aus-
tralia, Stephens and Sumner (2000) described Famen-
nian reef platforms constructed solely of microbial com-
munities, which they attributed to the Late Devonian
mass extinction of metazoans. The reefs contain algal
filaments and probable cyanobacteria. Similarly, large-
scale microbial thombolites and oncolites that mark
the Frasnian–Famennian boundary in Upper Devonian
strata ofAlbertawere interpretedbyWhalen et al. (1998)
as disaster forms (opportunistic taxa commonly restricted
in occurrence but becoming abundant and widespread
as competing organisms die off during biotic crises).
Figure 2. Major Phanerozoic mass extinctions and variation in approximate relative abundance of stromatolites through geologictime. Occurrences of calcified marine cyanobacteria from open-marine settings (from Arp et al., 2001) and relative abundance ofmicrobial carbonates in reefs are also shown (from Riding, 2006). Increase in stromatolite abundance is associated with all majorPhanerozoic extinctions except the end-Cretaceous event, which is the smallest of the major extinctions (Hallam, 2004). The end-Cretaceous extinction is attributed to bolide impact, whereas the others are associated with global temperature variation and sea levelchange. Relatively high abundance of microbial carbonates, and to some extent calcified marine cyanobacteria, occurs at approximatelythe Late Devonian and end-Permian extinctions. As noted by Arp et al. (2001), the relative abundance of stromatolites through geologictime does not necessarily coincide with that of calcified marine cyanobacteria because calcification is dependent on chemical conditionssuch as supersaturation of the ambient water with respect to CaCO3. The relative abundance of microbial carbonates in reefs is limitedto occurrences in shallow marine strata. The trend in diversity of marine animals is from Raup and Sepkoski (1982). The trend instromatolite abundance is from Awramik (1984) and sources listed on the figure.
4 The Role of Toxin-Producing Algae in Phanerozoic Mass Extinctions
In carbonate platform successions of China, the ex-
pansion of cyanobacteria and flourishing of microbial
buildups are reported at the Frasnian–Famennian bound-
ary and attributed to major environmental changes that
wereprobably associatedwith themass extinction,which
lasted approximately 450 k.y. (Chen et al., 2002; Chen
and Tucker, 2003). These buildups contain massive mi-
crobial boundstones, minor stromatolites, and thombo-
lites; microbial micrite with fenestrae, tepee structures,
and algal filaments is present (Chen and Tucker, 2003).
The dominant biota in the microbial facies are the cya-
nobacteria Renalcis and Epiphyton; minor other cyano-
bacteria, includingRothpletzella andWetheredella, alongwithminor red algae are also reported (Chen andTucker,
2003). Chen et al. (2002) suggested that the cyanobac-
terial blooms at the Frasnian–Famennian boundary oc-
curred in response to increased nutrient flux to the ocean
because of proliferation of land plants. They proposed
Table 1. Major Groups of Organisms Affected by Mass Extinctions and Evidence for Increased Microbial Activity Associated with
Mass Extinctions
Major Groups of Organisms Affected (Decline in
Abundance and Diversity)
Evidence for Increased Microbial Activity Associated
with Mass Extinctions
End Ordovician Trilobites, echinoderms, nautiloids, corals,
brachiopods, graptolites, conodonts, and
acritarchs (Brenchley, 1989, 1990)
United States (Great Basin): Stromatolites recorded in
strata immediately above mass extinction (Sheehan,
2001; Sheehan and Harris, 2004).
Late Devonian Corals, stromatoporoids, brachiopods, foraminifera,
bryozoans, trilobites, fishes, cephalopods, and
conodonts (McGhee, 1990, 1996)
Australia (Canning Basin): Extensive microbial reef
platforms, including probable cyanobacterial facies
(Stephens and Sumner, 2000).
Alberta, Canada: Large-scale thombolites and oncolites
(Whalen et al., 1998).
China: Carbonate platform successions containing
microbial boundstones, stromatolites, thombolites;
cyanobacterial colonies interpreted as blooms in
response to increased nutrient flux (Chen et al., 2002;
Chen and Tucker, 2003).
End Permian Crinoids, brachiopods, bryozoans, cephalopods,
corals, ostracods, foraminifera, and tetrapods
(Maxwell, 1989, 1992; Erwin, 1990b, 1993)
South China (Nanpanjiang Basin): Regionally extensive
microbial framestone constructed by cyanobacteria
(Lehrmann et al., 2003).
Southwest Japan: Flourishing of cyanobacteria recorded
in shallow marine carbonate buildup at the beginning
of the Triassic (Sano and Nakashima, 1997).
United States (Great Basin): Stromatolites and microbial
facies recorded in strata immediately above mass extinction
(Schubert and Bottjer, 1992; Pruss et al., 2005).
Hungary: Bloom of microbial communities, including
stromatolites, at the Permian–Triassic boundary in
open-marine strata (Hips and Haas, 2006; Haas et al., 2007).
Widespread and abundant stromatolites reported from
other areas including Italy, Armenia, Slovenia, Turkey,
Oman, Iran, Greenland, Canada (Pruss et al., 2006;
Baud et al., 2007; Yin et al., 2007).
End Triassic Tetrapods, cephalopods, gastropods, brachiopods,
bivalves, and sponges (Olsen et al., 1987;
Benton, 1990; McElwain et al., 1999)
British Columbia, Canada: Expansion of nitrogen-fixing
cyanobacteria coincident with mass extinction caused
by widespread ocean stagnation (Sephton et al., 2002).
End Cretaceous Dinosaurs, plankton, ammonites, belemnites,
bivalves, bryozoans, brachiopods, and land
plants (Kauffman, 1984, 1986; Hallam, 2004)
None reported.
Castle and Rodgers 5
Table 2. Factors Interpreted as Contributing to Phanerozoic Mass Extinctions (Indicated by X)*
Bolide Impact Volcanism Global Warming
Ocean Anoxia and
Transgression
Increased Nutrient Input to
Oceans and Eutrophication Algal-Produced Toxins
End Ordovician X X X
Late Devonian X X X X X
End Permian X X X X X
End Triassic X X X X X
End Cretaceous X X X X X
Modern:
observations
and effects
Release of CO2 from
bolide impact may
contribute to global
warming (O’Keefe
and Ahrens, 1989;
Jablonski, 1990;
Hildebrand et al.,
1991) and to
environmental stress
leading to increased
algal toxin production.
Volcanism affects
environmental
conditions, which
may lead to
environmental
stress causing
increased production
and potency of algal
toxins (Landsberg,
2002).
Warmer temperatures
cause increased
frequency of toxic
algal blooms
(Hallegraeff, 1993;
Harvell et al., 1999).
Anoxia from decay
of a large mass of
organic material
produced by algal
blooms causes
organism mortalities
(Skulberg et al., 1984).
Increased nutrient input to
oceans and eutrophication
cause increased production
of algal toxins (Paerl and
Whitall, 1999; Van Dolah,
2000).
Algal-produced toxins cause
mass mortality of organisms
(Collins, 1978; Carmichael
and Falconer, 1993;
Falconer, 1999) and may
lead to another mass
extinction event.
*Observations and interpretations regarding algal-produced toxins are from this article and references cited in the table; other interpretations are from Hallam (2004) and references cited in the text.
6The
Roleof
Toxin-ProducingAlgae
inPhanerozoic
Mass
Extinctions
that the blooms caused a stressed and fragile ecosystem
for benthicmarine organisms, which contributed to their
mass extinction.
End Permian
The largest of all extinctions, with amassive decrease in
numerousmarine and terrestrial species, including non-
marine tetrapods, occurred at the end Permian (Raup,
1979;Maxwell, 1989, 1992; Erwin, 1990a, b, 1993, 1994;
King, 1991; Retallack, 1995). This extinction may be
related to climatic changes (Maxwell, 1989, 1992; Erwin,
1994), but other causes have been suggested. Based on
stratigraphic studies, anoxia of deep to shallowmarine
environments has been interpreted as a possible cause
(Wignall and Hallam, 1992, 1993;Wignall et al., 1995;
Wignall and Twitchett, 1996; Isozaki, 1997; Kato et al.,
2002). Knoll et al. (1996) attributed the event to over-
turn of deep, anoxic oceans, which moved high con-
centrations of carbon dioxide into shallow waters.
Volcanic activity, which may have led to global warm-
ing and ocean anoxia, has also been suggested as a cause
of the end-Permian mass extinction (Renne et al., 1995;
Kamo et al., 2003; Bottjer, 2004; Hallam, 2004; Isozaki
et al., 2004; Knoll et al., 2007; Yu et al., 2007). Bolide
impact was interpreted by Retallack et al. (1998) and
Becker et al. (2001) as causing the end-Permian extinc-
tion. In a study of stable carbon isotopes in Permian–
Triassic paleosols of Antarctica, Krull and Retallack
(2000) found evidence for increased methane content
of the atmosphere, which may have contributed to
globalwarming and sea level rise. They interpretedmeth-
ane release to the atmosphere as gradual instead of
catastrophic.
A widespread resurgence of stromatolites and in-
creased abundance of cyanobacteria coincident with
and immediately following the end-Permian mass ex-
tinction have been observed in various areas of Europe,
Asia, and North America (Schubert and Bottjer, 1992;
Bottjer et al., 1996; Sano and Nakashima, 1997; Xie
et al., 2005, 2007; Pruss et al., 2006; Baud et al., 2007;
Kershaw et al., 2007; Yin et al., 2007). In the Upper
Permian carbonate platform strata of the Nanpanjiang
Basin of south China, Lehrmann et al. (2003) described
diverse open-marine fossil assemblages in skeletal pack-
stones overlain by calcareous microbial framestone built
by cyanobacteria and lacking macrofossils; the cyano-
bacteria are globular to tufted in form similar toRenalcis.They interpreted origin of the cyanobacterial frame-
stone, which may have covered more than 10,000 km2
(3861mi2) in depositional extent, as related to an anom-
alous oceanic event coincident with and/or immedi-
ately following the end-Permian extinction. As the
authors point out, strata containing the microbial frame-
stones are shallow-marine facies and lack evidence of
an abrupt change in depositional environment or wa-
ter depth. Lehrmann et al. (2003) noted that carbonate
microbial facies are widespread globally after the end-
Permian mass extinction.
The fossil record demonstrates that a dramatic in-
crease in microbial activity at the Permian–Triassic
boundary is not limited to cyanobacteria. A spike in mi-
crobial remains identified initially as fungi (Eshet et al.,
1995; Visscher et al., 1996) and more recently as green
algae (Afonin et al., 2001; Foster et al., 2002) occurs
near the boundary in both marine and terrestrial rocks.
The increase in these remains began at least 500 k.y.
before the Permian–Triassic mass extinction of marine
organisms and may suggest that environmental changes
occurred that caused algal blooms in shallow aquatic
environments (Erwin, 2006).
End Triassic
Major extinctions at the end of the Triassic have been
recognized among many groups of organisms, especial-
ly tetrapods, cephalopods, gastropods, brachiopods, bi-
valves, and sponges (Olsen et al., 1987; Benton, 1990;
McRoberts and Newton, 1995; McElwain et al., 1999).
A major faunal mass extinction at the Triassic–Jurassic
boundary was reported by McElwain et al. (1999), who
interpreted global cooling of 3–4jC from paleobotanical
evidence. Based on shocked quartz grains found in sedi-
mentary rocks at the Triassic–Jurassic boundary, Bice
et al. (1992) suggested that the extinctionwas causedby
bolide impact. Olsen et al. (2002) identified an iridium
anomaly at the Triassic–Jurassic boundary, which they
cited as support for bolide impact causing the mass ex-
tinction. Hesselbo et al. (2002) noted that large-scale
volcanic eruptions occurred at the same time as the mass
extinction. Ocean anoxia and global warming, possibly
associatedwith volcanic eruptions,mayhave contributed
tomassmortalities (Hallam,2004). Sephton et al. (2002)
interpreted ocean stagnation as causing nutrient deple-
tion that led to the end-Triassic mass extinction and to
the expansion of nitrogen-fixing cyanobacteria. Schubert
and Bottjer (1992) interpreted stromatolite abundance
immediately following the end-Triassic extinction as a
replacement of benthic invertebrate faunas.
End Cretaceous
Although the end-Cretaceous mass extinction is the
smallest of the five major extinctions (Hallam, 2004),
it is well known as marking the end of the dinosaurs
Castle and Rodgers 7
Table 3. Toxins Produced by Modern Cyanobacteria
Toxin General Characteristics Taxa-Producing Toxin Structure and Activity References
Cyclic peptidesMicrocystins Hepatotoxin, liver toxin Microcystis, Anabaena, Planktothrix
(Oscillatoria), Nostoc, Haplosiphon,
Anabaenopsis, Nodularia, Anacystis,
Gloeocapsa, Synechococcus, Eucapsis,
Aphanocapsa, Rivularia, Entophysalis,
Schizothrix, Phormidium, Microcoleus
Cyclic heptapeptides; hepatotoxic,
protein phosphatase inhibition,
membrane integrity, and
conductance disruption, tumor
promotors
Carmichael (1997), Falconer
(1998), Codd et al. (2005)
Nodularins Hepatotoxin, liver toxin Nodularia Cyclic pentapeptides; hepatotoxins, protein
phosphatase inhibition, membrane
integrity, and conductance disruption,
tumor promoters, carcinogenic
Sivonen and Jones (1999)
AlkaloidsAnatoxin-a (including
homoanatoxin-a)
Neurotoxin-nerve synapsis Planktothrix (Oscillatoria), Anabaena,
Plectonema, Aphanizomenon, Rhaphidiopsis,
Hyella
Alkaloids; postsymaptic, depolarizing
neuromuscular blockers
Sivonen and Jones (1999),
Namikoshi et al. (2003)
Anatoxin-a(S) Neurotoxin-nerve synapsis Anabaena Guanidine methyl phosphate ester;
inhibits acetylcholinestenase
Sivonen and Jones (1999),
Namikoshi et al. (2003)
Aplyslatoxins Dermal toxin, skin Lyngbya, Schizothrix, Planktothrix
(Oscillatoria), Microcoleus
Alkaloids; inflammatory agents, protein
kinase C activators
Osborne et al. (2001), Mastin
et al. (2002), Codd et al. (2005)
Cylindrospermopsins Hepatotoxins, liver, kidney,
and lymphoid tissue
Cylindrospermopsis, Aphanizomenon, Umezakia,
Raphidiopsis
Guanidine alkaloids; liver necrosis
(also kidneys, spleen, lungs, intestine);
protein synthesis inhibitor, genotoxic
Lagos et al. (1999), Li et al.
(2001), Schembri et al. (2001),
Namikoshi et al. (2003)
Lyngbyatoxin-a Skin, gastrointestinal tract Lyngbya, Schizothrix, Planktothrix (Oscillatoria) Alkaloids; inflammatory agents, protein
kinase C activators
Codd et al. (1999, 2005),
Sivonen and Jones (1999)
Saxitoxins Neurotoxin, nerve axons Anabaena, Aphanizomenon, Lyngbya,
Cylindrospermopsis, Planktothrix (Oscillatoria)
Carbamate alkaloids, sodium
channel-blockers
Codd et al. (1999, 2005),
Sivonen and Jones (1999)
LipopolysaccharidesG� cyanobacteria General irritant, affects
any exposed tissue
‘‘All’’ G� cyanobacteria (prokaryotes) Lipopolysaccharides; endotoxins,
inflammatory agents, gastrointestinal
irritants
Sivonen and Jones (1999)
Uncharacterized structureNeurotoxin Brain, vacuolar mylinopathy Unnamed Stigonematales species Undescribed; avian vacuolar mylinopathy Birrenkott et al. (2004), Wilde
et al. (2005)
8The
Roleof
Toxin-ProducingAlgae
inPhanerozoic
Mass
Extinctions
and has been interpreted as caused by a bolide impact
(Alvarez et al., 1980, 1984; Alvarez, 1987). The impact
may have resulted in a large release of carbon dioxide
into the atmosphere and subsequent global warming
(O’Keefe andAhrens, 1989; Jablonski, 1990;Hildebrand
et al., 1991). The fossil record indicates that mass ex-
tinctions among plankton, ammonites, belemnites, bi-
valves, bryozoans, brachiopods, and land plants occurred
in response to environmental changes at the end of the
Cretaceous; however, these extinctions occurred more
gradually than expected if caused solely by a catastrophic
event (Kauffman, 1984, 1986; Hallam, 2004). A com-
bination of volcanism and sea level change, along with
associated climatic changes,may have contributed to the
end-Cretaceous extinction (Hallam, 1990). Oxygen de-
pletion in the water column and temperature change
are likely factors in the end-Cretaceous extinction
(Kauffman, 1984).
Increase in stromatolite occurrence or other direct
evidence for cyanobacterial expansion associated with
the end-Cretaceous mass extinction has not been re-
ported from the rock record. If cyanobacteria or other
microbes increased in abundance, the evidence may be
preserved too poorly for recognition.
MODERN TOXIN-PRODUCING ALGAE
Algae that produce toxins occur in the divisions Chryso-
phyta (class Prymnesiophyceae), Pyrrhophyta (class
Dinophyceae or dinoflagellates), and Cyanophyta (cya-
nobacteria, also called blue-green algae), with the latter
group being most responsible for toxicity-caused dis-
ease and death (Carmichael and Falconer, 1993). Cya-
nobacteria are aerobic phototrophs that use sunlight as
an energy source. Toxins produced by modern cyano-
bacteria have resulted directly in the death of a wide
range of organisms, including invertebrates, fish, birds,
cattle, sheep, dogs, monkeys, and rhinoceros (Carmi-
chael and Bent, 1981; Skulberg et al., 1984; Carmichael
and Falconer, 1993; Falconer, 1999; Duy et al., 2000;
Carmichael et al., 2001; Mastin et al., 2002). Cyano-
bacterial toxins in drinking water have caused human
deaths, and recreational exposures to water containing
toxin-producing cyanobacteria have caused a range of
human illnesses, including acute pneumonia, hepato-
enteritis, papulovesicular dermatitis (swimmers’ itch),
and gastroenteritis (Cardellina et al., 1979; Carmichael
and Falconer, 1993; Teixeira et al., 1993; Falconer,
1996, 1999).
Algal toxins are produced in both aquatic and ter-
restrial environments. They are dispersed by water cur-
rents, transported in the air, and transmitted through
food webs. Toxins produced by planktonic species can
become aerosolized after lysis, which can adversely af-
fect air-breathing mammals and reptiles (Pierce et al.,
1990; Landsberg, 2002). Toxins released by cyanobac-
teria living in roots of terrestrial plants can move up the
food chain to plant-eatingmammals and to humans (Cox
et al., 2005). Results from laboratory and field studies
byWilde et al. (2005) suggested that an increasingly com-
mon bird disease, avian vacuolar myelinopathy (AVM),
which is killing growing numbers of herbivorous water-
birds and their avian predators in the southern United
States, is linked to toxins produced by cyanobacteria.
The cyanobacterium implicated in producing the neuro-
toxin may be expanding its range as the exotic aquatic
macrophyte, hydrilla (Hydrilla verticillata), invades ad-ditional water bodies to the north.
Toxins produced by cyanobacteria include hepato-
toxic peptides, a cytotoxic alkaloid, neurotoxic alkaloids,
Figure 3. (A) Structure of modern filamen-tous cyanobacterium (e.g., Lyngbya orOscillatoria) showing sites of toxin produc-tion. Width of cell = 8 mm. (B) Photomicro-graph of Lyngbya majuscula, a modern,toxin-producing, filamentous cyanobacteri-um. Width of cyanobacterium = 8 mm.
Castle and Rodgers 9
Table 4. Toxins Produced by Modern Cyanobacteria and Selected Occurrences of their Ancestors in the Geologic Record*
Ancient Modern
Taxon Taxon
Formation/Group (Approximate Age); Location Reference Toxins Produced by Genus References
Palaeoanacystis Anacystis
Belcher Supergroup (2100 Ma); Canada Hoffman (1976) Microcystins; lipopolysaccharides (LPS) Elleman et al. (1978), Hunter (1998),
McArthur Group (1600 Ma); Australia Muir (1976) Steffensen et al. (1999), Oberholster
Balbirini Dolomite (1500 Ma); Australia Oehler (1978) et al. (2005)
Changcheng Group (1425 Ma); China Zhang (1981)
Vindhyan Supergroup (1050 Ma); India Nautiyal (1983)
Mbuji Mayi Supergroup (1020 Ma); Zaire Maithy (1975)
Bitter Springs Formation (850 Ma); Australia Schopf (1968)
Muhos Formation (650 Ma); Finland Tynni and Uutela (1984)
Palaeomicrocystis Microcystis
Mbuji Mayi Supergroup (1020 Ma); Zaire Maithy (1975) Microcystins; lipopolysaccharides (LPS) Neilan et al. (1999), Sivonen and
Jones (1999), Codd et al. (2005)
Eogloeocapsa Gloeocapsa
Billyakh Group (1325 Ma); Siberia Golovenok and Belova (1984) Microcystins; lipopolysaccharides (LPS) Carmichael and Li (2006)
Eosynechococcus Synechococcus
Belcher Supergroup (2100 Ma); Canada Hoffman (1976) Microcystins; lipopolysaccharides (LPS) Carmichael and Li (2006)
Amelia Dolomite (1700 Ma); Australia Hofmann and Schopf (1983)
Billyakh Group (1325 Ma); Siberia Golovenok and Belova (1984)
Debengda Formation (1040–1265 Ma); Siberia Sergeev et al. (1994)
Vindhyan Supergroup (1050 Ma); India McMenamin et al. (1983)
Sukhaya Tunguska Formation (1000 Ma); Siberia Mendelson and Schopf (1982)
Shorikha Formation (1000 Ma); Siberia Sergeev (2001)
Bitter Springs Formation (850 Ma); Australia Knoll and Golubic (1979)
Kirgitey Formation (800 Ma); Siberia Golovenok and Belova (1985)
Draken conglomerate (750 Ma); Spitsbergen Knoll (1982)
Min’yar Formation (740 Ma); Russia Nyberg and Schopf (1984)
Gangolihat dolomites (735 Ma); India Nautiyal (1980)
Thule Group (688 Ma); Greenland Strother et al. (1983)
Muhos Formation (650 Ma); Finland Tynni and Uutela (1984)
10
TheRole
ofToxin-Producing
AlgaeinPhanerozoic
Mass
Extinctions
Eoaphanocapsa Aphanocapsa
Min’yar Formation (740 Ma); Russia Nyberg and Schopf (1984) Microcystins; lipopolysaccharides (LPS) Domingos et al. (1999), Carmichael
and Li (2006)
Eocapsamorpha Eucapsis
Kirgitey Formation (800 Ma); Siberia Golovenok and Belova (1985) Microcystins; lipopolysaccharides (LPS) Visser et al. (2005)
Eopleurocapsa Pleurocapsa
Jiudingshan Formation (800 Ma); China Liu et al. (1984) Microcystins; lipopolysaccharides (LPS) Christiansen et al. (2001)
Palaeopleurocapsa Pleurocapsa
Vindhyan Supergroup (1050 Ma); India Nautiyal (1983) Microcystins; lipopolysaccharides (LPS) Christiansen et al. (2001)
Neleger Formation (1000 Ma); Siberia Golovenok and Belova (1990)
Skillogalee Dolomite (800 Ma); Australia Knoll et al. (1975)
Eleonore Bay Group (750 Ma); Greenland Green et al. (1988)
Min’yar Formation (740 Ma); Russia Sergeev and Krylov (1986)
Chichkan Formation (650 Ma); Kazakhstan Ogurtsova and Sergeev (1987)
Muhos Formation (650 Ma); Finland Tynni and Uutela (1984)
Palaeocalothrix Calothrix
Miroyedikha Formation (1000 Ma); Siberia German (1981a) Calothrixine A; b-N-methylamino-L-alanine(neurotoxic amino acid)
Doan et al. (2000), Cox et al. (2005),
Leflaive and Ten-Hage (2007)
Primorivularia Rivularia
Gunflint Iron Formation (2090 Ma); Canada Edhorn (1973) Microcystins Aboal et al. (2005)
Eoentophysalis Entophysalis (Chamaesiphon)
Belcher Supergroup (2100 Ma); Canada Hoffman (1976) Microcystins; lipopolysaccharides (LPS) Ehrenreich et al. (2005)
Amelia Dolomite (1700 Ma); Australia Hofmann and Schopf (1983)
Bungle Bungle Dolomite (1600 Ma); Australia Hofmann and Schopf (1983)
Balbirini Dolomite (1500 Ma); Australia Oehler (1978)
Changcheng Group (1425 Ma); China Zhang (1981)
Dismal Lakes Group (1400 Ma); Canada Horodyski and Donaldson (1983)
Debengda Formation (1040–1265 Ma); Siberia Sergeev et al. (1994)
Vindhyan Supergroup (1050 Ma); India McMenamin et al. (1983)
Sukhaya Tunguska Formation (1000 Ma); Siberia Mendelson and Schopf (1982)
Bitter Springs Formation (850 Ma); Australia Knoll and Golubic (1979)
Jiudingshan Formation (800 Ma); China Liu et al. (1984)
CastleandRodgers
11
Table 4. Continued
Ancient Modern
Taxon Taxon
Formation/Group (Approximate Age); Location Reference Toxins Produced by Genus References
Eleonore Bay Group (750 Ma); Greenland Green et al. (1988)
Min’yar Formation (740 Ma); Russia Sergeev and Krylov (1986)
Thule Group (688 Ma); Greenland Strother et al. (1983)
Chichkan Formation (650 Ma); Kazakhstan Ogurtsova and Sergeev (1987)
Palaeolyngbya LyngbyaChangcheng Group (1425 Ma); China Zhang (1981) Lyngbyatoxin-a (skin and gastrointestinal
toxin); ichthyotoxin; invertebrate toxin;
dermatitis toxin (aplyslatoxins);
neurotoxin (saxitoxins); microcystins;
lipopolysaccharides(LPS)
Sivonen and Jones (1999), Osborne
et al. (2001), Mastin et al. (2002),
Carmichael and Li (2006)
Debengda Formation (1040–1265 Ma); Siberia Sergeev et al. (1994)
Lakhanda Formation (950 Ma); Siberia German (1981b)
Bitter Springs Formation (850 Ma); Australia Schopf (1968)
Hailuoto sequence (650 Ma); Finland Tynni and Donner (1980)
Doushantuo Formation (600 Ma); China Zhang (1982)
Palaeospirulina Spirulina
Gunflint Iron Formation (2090 Ma); Canada Edhorn (1973) Calcium spirulan (antiviral) Skulberg (2000)
Eomicrocoleus Microcoleus
Dismal Lakes Group (1400 Ma); Canada Horodyski and Donaldson (1983) Microcystins; lyngbyatoxin-a Pennings et al. (1996), Capper et al.
(2005)Burovaya Formation (1000 Ma); Siberia Sergeev (2001)
Eophormidium Phormidium
Changcheng Group (1425 Ma); China Xu (1984) Microcystins; lipopolysaccharides
(LPS); b-N-methylamino-L-alanine(neurotoxic amino acid)
Sivonen and Jones (1999), Aboal
et al. (2005), Cox et al. (2005),
Carmichael and Li (2006)
Oscillatoriopsis Oscillatoria (Planktothrix)
Duck Creek Dolomite (2000 Ma); Australia Knoll et al. (1988) Microcystins; anatoxin-a; aplyslatoxins;
saxitoxins; lyngbyatoxin-a;
lipopolysaccharides(LPS)
Sivonen and Jones (1999), Namikoshi
et al. (2003), Codd et al. (2005)McArthur Group (1500 Ma); Australia Oehler (1977)
Barney Creek Formation (1500 Ma); Australia Oehler (1977)
Changcheng Group (1425 Ma); China Xu (1984)
Dismal Lakes Group (1400 Ma); Canada Horodyski and Donaldson (1983)
Jixian Group (1325 Ma); China Zhang (1985)
12
TheRole
ofToxin-Producing
AlgaeinPhanerozoic
Mass
Extinctions
Vindhyan Supergroup (1050 Ma); India Maithy and Shukla (1977)
Sukhaya Tunguska Formation (1000 Ma); Siberia Mendelson and Schopf (1982)
Miroyedikha Formation (1000 Ma); Siberia German (1981a)
Burovaya Formation and Shorikha Formation
(1000 Ma); Siberia
Sergeev (2001)
Bitter Springs Formation (850 Ma); Australia Schopf (1968)
Hunnberg Formation (775 Ma); Svalbard and
Jan Mayen Island
Knoll (1984)
Min’yar Formation (740 Ma); Russia Sergeev and Krylov (1986)
Thule Group (688 Ma); Greenland Strother et al. (1983)
Chichkan Formation (650 Ma); Kazakhstan Ogurtsova and Sergeev (1987)
Hailuoto sequence (650 Ma); Finland Tynni and Donner (1980)
Doushantuo Formation (600 Ma); China Zhang (1986)
Vampire Formation (540 Ma); Canada-Yukon Hofmann (1984)
Schizothropsis Schizothrix
Changcheng Group (1425 Ma); China Xu (1984) Dermatitis toxin (aplyslatoxins);
lyngbyatoxin-a; lipopolysaccharides (LPS)
Sivonen and Jones (1999), Carmichael
and Li (2006)
Palaeonostoc Nostoc
Gangolihat dolomites (735 Ma); India Nautiyal (1980) Microcystins (Including hepatotoxic cyclic
heptapeptides); lipopolysaccharides (LPS);
nostocine A; nostocyclamide;
b-N-methylamino-L-alanine (neurotoxic
amino acid)
Namikoshi et al. (1990), Todorova
and Juttner (1996), Neilan et al.
(1999), Sivonen and Jones (1999),
Hirata et al. (2003), Codd et al.
(2005), Cox et al. (2005), Leflaive
and Ten-Hage (2007)
Anabaenidium Anabaena
Gunflint Iron Formation (2090 Ma); Canada Edhorn (1973) Microcystins; anatoxin-a; anatoxin-a(S);
saxitoxins; lipopolysaccharides (LPS)
Neilan et al. (1999), Sivonen and Jones
(1999), Namikoshi et al. (2003), Codd
et al. (2005)
Changcheng Group (1425 Ma); China Xu (1984)
Bitter Springs Formation (850 Ma); Australia Schopf (1968)
Hailuoto sequence (650 Ma); Finland Tynni and Donner (1980)
Eoplectonema Plectonema
Jiudingshan Formation (800 Ma); China Liu et al. (1984) Anatoxin-a; b-N-methylamino-L-alanine(neurotoxic amino acid); antibacterial toxins
Pandey and Pandey (2002), Cox et al.
(2005), Soltani et al. (2005)
CastleandRodgers
13
and saxitoxin derivatives (Table 3); allergens and lipo-
polysaccharides are also produced (Collins, 1978; Car-
michael andBent, 1981;Carmichael, 1992;Sivonen,1996;
Falconer, 1999; Landsberg, 2002; Van Apeldoorn et al.,
2007). Laboratory experiments have demonstrated that
toxins produced by cyanobacteria can be potent inhib-
itors of protein phosphatases 1 and2A fromhigher plants
as well as mammals (MacKintosh et al., 1990). The
main genera of toxin-producing cyanobacteria include
Anabaena, Aphanizomenon, Cylindrospermopsis, Lyng-bya,Microcystis,Nodularia, andOscillatoria (Cardellinaet al., 1979; Fujiki et al., 1984; Skulberg et al., 1984,
1993; Carmichael and Falconer, 1993; Schrader and
Blevins, 1993; Falconer, 1996; Mastin et al., 2002). All
of these genera can form blooms that are potentially
toxic (Carmichael and Falconer, 1993). Both the pro-
duction rate and toxicity of cyanobacterial toxins are
affected by environmental factors such as light inten-
sity, pH, temperature, and nutrient availability (Utkilen
and Gjolme, 1992; Sivonen, 1996; Mastin et al., 2002).
Toxins are produced and contained within the algal cell
structure (Figure 3),with onlyminor quantities of toxins
released until the cell lyses (Landsberg, 2002; White
et al., 2005). The release of toxins by cell lysis is in-
duced by environmental stress, including ultraviolet
irradiation, physical injury, or changes in water chem-
istry such as increased salinity (Falconer, 1999; Ross
et al., 2006). In addition, environmental stress can in-
duce algae to produce increased quantity and potency of
toxins (Landsberg, 2002). Lawrence et al. (2002) iden-
tified viruses living in sediments that cause cell lysis of
toxin-producing cyanobacteria. Algal blooms can pro-
vide a natural refuge for disease-causing bacteria, which
are dormant and are released when the blooms are ac-
tivated (Colwell, 1996; Haines et al., 2000). In addition
to direct poisoning and harboring disease-causing or-
ganisms, cyanobacterial blooms cause mortality indi-
rectly by asphyxia from the organic mass produced and
from anoxia during decomposition of the organic mat-
ter (Skulberg et al., 1984).
In modern environments, cyanobacterial blooms
occur worldwide in fresh, brackish, and marine waters.
Cyanobacteria are commonly the dominant phytoplank-
ton group in eutrophic freshwater bodies and can thrive
in polluted water low in oxygen (Oberholster et al.,
2004). Cyanobacterial growth is favored by warm tem-
peratures and abundant nutrient supply (Sivonen, 1990;
Wicks and Thiel, 1990;Gerten andAdrian, 2000;Haines
et al., 2000). Black (1933) noted the similarities of
modern cyanobacterial mats and domes on Andros Is-
land toPaleozoic stromatolites.Genera of cyanobacteriaPalaeoscytonema
Scytonem
a
Gunflint
Iron
Form
ation(2090Ma);Canada
Edhorn
(1973)
Tolytoxin;
scytophycins;hepatotoxin;
cyanobacterin(algicide);
b-N-methylamino-L-alanine(neurotoxic
aminoacid)
Gleason
andBaxa
(1986),Carmelietal.
(1990),Patterson
andBolis
(1994),
Kumaretal.(2000),Dhananjayaetal.
(2003),Cox
etal.(2005),Leflaiveand
Ten-Hage(2007)
Vindhyan
Supergroup
(1050Ma);India
MaithyandShukla(1977)
Eohyella
Hyella
ChangchengGroup
(1650Ma);China
Zhang(1988)
Anatoxin-a;
organochlorines(carbazoles)
Gribble(1996)
Eleonore
BayGroup
(750
Ma);Greenland
Green
etal.(1988)
*Occurrences
ofAncient
Taxa
afterMendelson
andSchopf
(1992)
andReferences
Listed;ModernCounterpartsto
Ancient
CyanobacteriaafterSchopf
(2004).
Table
4.Continued
Ancient
Modern
Taxon
Taxon
Form
ation/Group
(ApproximateAge);Location
Reference
Toxins
Produced
byGenus
References
14 The Role of Toxin-Producing Algae in Phanerozoic Mass Extinctions
identified in mats on Andros Island includeGloeocapsa,Aphanocapsa, Phormidium, Schizothrix, Plectonema, andScytonema (Black, 1933; Monty, 1972). All of these
genera produce toxins and all have ancestors preserved
in the geologic record (Tables 3, 4). Mohamed et al.
(2006) detected neurotoxins and hepatotoxins, includ-
ing microcystins, produced by cyanobacteria forming
benthic (stromatolitic) mats on modern sediments along
the Nile River and irrigation canals. Genera identified as
producing toxins included Anabaena, Calothrix, Nostoc,Plectonema, and Phormidium.Mez et al. (1997) identified
Oscillatoria and Phormidium in benthic cyanobacterial
mats growing on sediments and submerged rocks in al-
pine lakes as the source of toxins responsible for cattle
deaths in southeastern Switzerland.
DISCUSSION
Schopf (2004) recognized 22 genera of ancient cyano-
bacteria that have modern counterparts. From our study
of cyanobacteria and their toxins, the modern forms of
all 22 of these genera produce toxins (Table 4). We pro-
pose that sufficient amounts of potent toxins were pro-
duced by cyanobacteria in the geologic past to contribute
directly to Phanerozoic mass extinctions by acting as a
kill mechanism. Consistent with our hypothesis is in-
creased algal abundance and evidence for global warm-
ing reported coincidentwithmass extinctions (Figure 2;
Table 2). Sea level rise combined with global warming
can cause expansion of the environments and condi-
tions, such as nutrient supply, favorable for algal growth
(Figure 4). The biomass produced by increased algal
productivity is likely to have contributed to anoxia in
aquatic environments, which has been interpreted for
all five major Phanerozoic mass extinctions (Table 2).
Bolide impact or volcanic eruptionmayhavebeen a source
of environmental stress that caused or contributed to in-
creased production or potency of algal-produced toxins.
The ability of cyanobacteria to produce toxins and
to survive over an extremely wide range of conditions
very likely influencedmortality, survival, and adaptation
of many taxa in the past, just as organisms are affected
today. Previous investigators have noted the widespread
occurrence ofmicrobial facies associatedwithmajormass
extinctions, and some have suggested thatmicrobial taxa
expanded as postmass extinction disaster forms (Sano
and Nakashima, 1997; Whalen et al., 1998; Kershaw
et al., 1999; Lehrmann, 1999). This microbial growth
and the expansion of stromatolites have been attributed
to the loss of metazoan grazers and framebuilders (e.g.,
Schubert and Bottjer, 1992; Kershaw et al., 1999). How-
ever, Riding (1997, 2006) suggested that stromatolites
are not disaster biota and that their decline cannot be
accounted for bymetazoan interference.He interpreted
the increase in stromatolite abundance at times of mass
extinctions as caused by environmental conditions fa-
vorable for growth and suggested that metazoan decline
at mass extinctions may be caused by microbial inter-
ference. Pratt (1982) concluded that because algal mats
commonly coexist with grazing organisms, environmen-
tal conditions exert a greater control on the survival of
mat-producing microbes than competition from other
organisms. Studies of modern algae, including toxicity
Figure 4. Schematic profiles illustrating theinfluence of climate-induced sea levelchange on algal growth. (A) Sea level is low,shelves are narrow, and water temperaturesare less favorable for algal growth duringperiods of cool global climate. (B) Duringperiods of warm global climate, sea level ishigh resulting in extensive areas of shallowmarine and coastal environments favorablefor algal growth. Warm water temperaturespromote the growth of algal blooms, domaland columnal stromatolites, and stromato-litic mats, which increases the potential fortoxin production and release.
Castle and Rodgers 15
tests, suggest that production of toxins by cyanobacteria
can serve as a defense mechanism against grazers
(Lampert, 1981; Nizan et al., 1986;Mastin et al., 2002).
Adverse effects on grazers upon ingesting toxic phyto-
plankton include reduced feeding, reduced survival rate,
regurgitation of toxic phytoplankton, and lethargy or
paralysis (Turner and Tester, 1997; Turner et al., 1998).
Riegman (1998) suggested that the major ecological role
of algal toxins may be the protection of populations
against predation losses. Some previous investigators
(Knoll et al., 1996; Lehrmann, 1999; Lehrmann et al.,
2003) have suggested that the increased occurrence of
microbial facies in the stratigraphic record was caused
by changes in oceanic conditions, such as upwelling
of anoxic or carbon-dioxide-rich waters, instead of ori-
gin as default facies or disaster taxa.Hsu (1986) reported
that dissolved carbon dioxide levels in the oceans were
abnormally high during times of biotic crises, which
could have favored algal growth. Blooms of green algae
disaster species contemporaneous with the end-Triassic
extinction were recognized in the stratigraphic record
by Van de Schootbrugge et al. (2007). They attributed
the blooms to elevated carbon dioxide in the atmosphere
caused by flood basalt volcanism or methane hydrate
dissociation.
Our study focused on cyanobacteria because of
their predominance in producing toxins in modern
environments and their preservation in the rock re-
cord. However, other types of algae may have been
equally or more important in contributing to mass ex-
tinctions. Several types of algae, including diatoms, di-
noflagellates, and cyanobacteria, produce toxins that
can cause death of higher organisms (e.g., Falconer,
1993). Although some genera of modern cyanobacteria
and other algae are clearly demonstrated to produce
toxins, direct evidence for toxin production by ancient
microbes is much more difficult to obtain because of
lack of toxin preservation in the rock record. Addition-
al data from the geologic record are needed to fully
test our hypothesis that toxin-producing algae contrib-
uted to Phanerozic mass extinctions. Questions include
the following:
1. To what extent is the presence of toxin-producing
algae recorded in the stratigraphic record?
2. What was the specific role of each type of toxin-
producing algae (i.e., diatoms, dinoflagellates, and
cyanobacteria) in mass extinctions?
3. To what extent did the role of toxin-producing algae
in mass extinctions vary among various marine and
terrestrial environments?
Analysis of geologic strata for the presence, quantity,
and distribution of metabolites from ancient toxin-
producing algae will contribute to answering these
questions.
The abundance of modern toxin-producing algae is
presently increasing, and their geographic distribution
is expanding, which previous investigators have attrib-
uted to global warming and increased anthropogenic
input of nutrients to aquatic environments (Shumway,
1990; Smayda, 1990; Harvell et al., 1999; Haines et al.,
2000; Van Dolah, 2000; Shumway et al., 2003; Phlips
et al., 2004; Yan and Zhou, 2004; Luckas et al., 2005).
Warming of the oceans decreases dissolved oxygen con-
tent,which favors the growth of cyanobacteria and other
algae (Epstein and Ford, 1993). From the increasing fre-
quency of modern, toxin-producing algal blooms, an-
other massive biotic crisis may be forthcoming.
CONCLUSIONS
From observations of modern algae, we interpret in-
creased stromatolite abundance in the rock record to be
related to episodes of global warming and increased
nutrient supply in aquatic systems. Increased stromat-
olite abundance in the rock record occurs at times of
Phanerozoic mass extinctions. This recorded increase
in algal productivity may have contributed to mass
extinctions through toxin production combined with
eutrophication and anoxia. Our hypothesis is consis-
tent with previous theories of mass extinction in which
evidence for eutrophication and anoxia has been rec-
ognized. Extinctions duringwhich toxin-producing algae
were a factor could have occurred gradually or sudden-
ly. Environmental stress can induce toxin production in
modern algae, and catastrophic events are likely to have
induced toxin production in the geologic past. Cata-
strophic events triggering increased toxin production
by algae may have included bolide impact, volcanic
eruptions, or other causes of environmental stress.
Our conclusions regarding the role of cyanobac-
teria and toxin production in mass extinctions lead to
predictions for times of global warming. We anticipate
continued increase in algal blooms with more frequent
and persistent production of potent toxins. The algal
blooms and toxin production will likely lead to intense
impacts on aquatic and semiaquatic species with an
increase in extinction rates. This hypothesis gives us
cause for concern and underscores the importance of
careful and strategic monitoring as we move into an era
of global climate change.
16 The Role of Toxin-Producing Algae in Phanerozoic Mass Extinctions
REFERENCES CITED
Aboal, M., M. A. Puig, and A. D. Asencio, 2005, Production ofmicrocystins in calcareous Mediterranean streams: The Alhar-abe River, Segura River basin in south-east Spain: Journal ofApplied Phycology, v. 17, p. 231–243.
Afonin, S. A., S. S. Barinova, and V. A. Krassilov, 2001, A bloom ofTympanicysta Balme (green algae of zygnematalean affinities)at the Permian–Triassic boundary:Geodiversitas, v. 23, p. 481–487.
Alvarez, L. W., 1987, Mass extinctions caused by large bolide im-pacts: Physics Today, v. 40, no. 7, p. 24–33.
Alvarez, L. W., W. Alvarez, F. Asaro, and H. V. Michel, 1980, Extra-terrestrial cause for the Cretaceous–Tertiary extinction: Science,v. 208, p. 1095–1108.
Alvarez, W., E. G. Kauffman, F. Surlyk, L. Alvarez, F. Asaro, andH. V. Michel, 1984, The impact theory of mass extinctions andthe marine and vertebrate fossil record across the Cretaceous–Tertiary boundary: Science, v. 223, p. 1135–1141.
Arp, G., A. Reimer, and J. Reitner, 2001, Photosynthesis-inducedbiofilm calcification and calcium concentrations in Phanero-zoic oceans: Science, v. 292, p. 1701–1703.
Awramik, S. M., 1984, Ancient stromatolites and microbial mats, inY. Cohen, R. W. Castenholz, and H. O. Halvorson, eds., Mi-crobial mats: Stromatolites: New York, Alan R. Liss, p. 1–22.
Awramik, S. M., 1990, Stromatolites, in D. E. G. Briggs and P. R.Crowther, eds., Paleobiology a synthesis: Oxford, BlackwellScientific, p. 336–341.
Barnes, C. R., 1986, The faunal extinction event near theOrdovician–Silurian boundary: A climatically induced crisis,inO.H.Walliser, ed.,Global bio-events: LectureNotes in EarthSciences: Berlin, Springer-Verlag, v. 8, p. 121–126.
Baud, A., S. Richoz, and S. Pruss, 2007, The lower Triassic anach-ronistic carbonate facies in space and time:Global and PlanetaryChange, v. 55, p. 81–89.
Bauld, J., 1984, Microbial mats in marginal marine environments:Shark Bay, western Australia, and Spencer Gulf, South Australia,in Y. Cohen, R. W. Castenholz, and H. O. Halvorson, eds., Mi-crobial mats: Stromatolites: New York, Alan R. Liss, p. 39–58.
Bauld, J., E. D’Amelio, and J. D. Farmer, 1992, Modern microbialmats, in J. W. Schopf and C. Klein, eds., The Proterozoicbiosphere: Cambridge, Cambridge University Press, p. 261–269.
Becker, L., R. J. Poreda, A. G. Hunt, T. E. Bunch, and M. Rampino,2001, Impact event at the Permian–Triassic boundary: Evi-dence from extraterrestrial noble gases in fullerenes: Science,v. 291, p. 1530–1533.
Benton, M. J., 1990, Mass extinction: Events—End-Triassic, inD. E. G. Briggs and P. R. Crowther, eds., Paleobiology a syn-thesis: Oxford, Blackwell Scientific, p. 194–198.
Bice, D. M., C. R. Newton, S. McCauley, P. W. Reiners, and C. A.McRoberts, 1992, Shocked quartz at the Triassic–Jurassic bound-ary in Italy: Science, v. 255, p. 443–446.
Birrenkott, A. H., S. B.Wilde, J. J. Hains, J. R. Fischer, T.M. Murphy,C. P. Hope, P. G. Parnell, and W. W. Bowerman, 2004, Estab-lishing a food-chain link between aquatic plant material andavian vacuolar myelinopathy in mallards (Anas platyrhynchos):Journal of Wildlife Diseases, v. 40, p. 485–492.
Black, M., 1933, The algal sediments of Andros Island, Bahamas:Philosophical Transactions of the Royal Society of London,Series B, v. 222, p. 165–191.
Bottjer, D. J., 2004, The beginning of the Mesozoic: 70 million yearsof environmental stress and extinction, in P. D. Taylor, ed., Ex-tinctions in the history of life: Cambridge, CambridgeUniversityPress, p. 99–118.
Bottjer, D. J., J. K. Schubert, and M. L. Droser, 1996, Comparativeevolutionary paleoecology: Assessing the changing ecology ofthe past, inM.B.Hart, ed., Biotic recovery frommass extinctionevents: Geological Society (London) Special Publication 102,p. 1–13.
Braun, A., and T. Pfeiffer, 2002, Cyanobacterial blooms as the causeof a Pleistocene large mammal assemblage: Paleobiology, v. 28,p. 139–154.
Brenchley, P. J., 1989, The Late Ordovician extinction, in S. K.Donovan, ed., Mass extinctions: Process and evidence: NewYork, Columbia University Press, p. 104–132.
Brenchley, P. J., 1990, Mass extinction: Events—End-Permian, inD. E. G. Briggs and P. R. Crowther, eds., Paleobiology a syn-thesis: Oxford, Blackwell Scientific, p. 187–194.
Capper, A., I. R. Tibbetts, J. M. O’Neill, and G. R. Shaw, 2005, Thefate of Lyngbya majuscula toxins in three potential consumers:Journal of Chemical Ecology, v. 31, p. 1595–1606.
Cardellina II, J. H., F.-J. Marner, and R. E. Moore, 1979, Seaweeddermatitis: Structure of lyngbyatoxinA: Science, v. 204, p. 193–195.
Carmeli, S., R. E. Moore, and G. M. L. Patterson, 1990, Tolytoxinand new scytophycins from three species of Scytonema: Journalof Natural Products, v. 53, p. 1533–1542.
Carmichael, W. W., 1992, Cyanobacteria secondary metabolites—The cyanotoxins: Journal of Applied Bacteriology, v. 72, p. 445–459.
Carmichael, W. W., 1997, The cyanotoxins, in J. A. Callow, ed.,Advances in botanical research: London, Academic Press, v. 27,p. 211–256.
Carmichael,W.W., and P. E. Bent, 1981, Hemagglutinationmethodfor detection of freshwater cyanobacteria (blue-green algae) tox-ins: Applied and Environmental Microbiology, v. 41, p. 1383–1388.
Carmichael, W. W., and I. R. Falconer, 1993, Diseases related tofreshwater blue-green algal toxins, and controlmeasures, in I. R.Falconer, ed., Algal toxins in seafood and drinking water: London,Academic Press, p. 187–209.
Carmichael, W. W., and R. Li, 2006, Cyanobacteria toxins in theSalton Sea: Saline Systems, v. 2, no. 5, doi: 10.1186/1746-1448-2-5.
Carmichael, W. W., S. M. F. O. Azevedo, J. S. An, R. J. R. Molica,E. M. Jochimsen, S. Lau, K. L. Rinehart, G. R. Shaw, and G. K.Eaglesham, 2001, Human fatalities from cyanobacteria: Chem-ical and biological evidence for cyanotoxins: EnvironmentalHealth Perspectives, v. 109, p. 663–668.
Chen, D., and M. E. Tucker, 2003, The Frasnian–Famennian massextinction: Insights from high-resolution sequence stratigraphyand cyclostratigraphy in south China: Palaeogeography, Palaeo-climatology, and Palaeoecology, v. 193, p. 87–111.
Chen, D., M. E. Tucker, J. Zhu, and M. Jiang, 2001, Carbonatesedimentation in a starved pull-apart basin, Middle to LateDevonian, southern Guilin, south China: Basin Research, v. 13,p. 141–167.
Chen, D., M. E. Tucker, Y. Shen, J. Yans, and A. Preat, 2002,Carbon isotope excursions and sea-level change: Implicationsfor the Frasnian–Famennian biotic crisis: Journal of the Geo-logical Society, v. 159, p. 623–626.
Christiansen, G., E. Dittmann, L. V. Ordorika, R. Rippka, M.Herdman, and T. Borner, 2001, Nonribosomal peptide synthe-tase genes occur in most cyanobacterial genera as evidenced bytheir distribution in axenic strains of the PCC: Archives of Mi-crobiology, v. 176, p. 452–458.
Codd, G. A., S. G. Bell, K. Kaya, C. J. Ward, K. A. Beattie, and J. S.Metcalf, 1999, Cyanobacterial toxins, exposure routes and hu-man health: European Journal of Phycology, v. 34, p. 405–415.
Codd, G. A., J. Lindsay, F. M. Young, L. F. Morrison, and J. S.
Castle and Rodgers 17
Metcalf, 2005, Harmful cyanobacteria: From mass mortalitiesto management measures, in J. Huisman, H. C. P. Matthijs, andP.M. Visser, eds., Harmful cyanobacteria: Dordrecht, Springer,p. 1–23.
Collins, M., 1978, Algal toxins: Microbiological Reviews, v. 42,p. 725–746.
Colwell, R. R., 1996, Global climate and infectious disease: Thecholera paradigm: Science, v. 274, p. 2025–2031.
Copper, P., 1986, Frasnian/Famennian mass extinction and cold-water oceans: Geology, v. 14, p. 835–839.
Cox, P. A., S. A. Banack, S. J. Murch, U. Rasmussen, G. Tien, R. R.Bidigare, J. S. Metcalf, L. F. Morrison, G. A. Codd, and B.Bergman, 2005, Diverse taxa of cyanobacteria produce b-N-methylamino-L-alanine, a neurotoxic amino acid: Proceedingsof the National Academy of Sciences of the United States ofAmerica, v. 102, p. 5074–5078.
Dhananjaya, P. S., A. Kumar, and M. B. Tvagi, 2003, Biotoxic cya-nobacterial metabolites exhibiting pesticidal and mosquito lar-vicidal activities: Journal of Microbiology and Biotechnology,v. 13, p. 50–56.
Doan, N. T., R. W. Rickards, J. M. Rothschild, and G. D. Smith,2000, Allelopathic actions of the alkaloid 12-epi-hapalindole Eisonitrile and calothrixin A from cyanobacteria of the generaFischerella and Calothrix: Journal of Applied Phycology, v. 12,p. 409–416.
Domingos, P., T. K. Rubim, R. J. R. Molica, S. M. F. O. Azevedo,and W. W. Carmichael, 1999, First report of microcystin pro-duction by picoplanktonic cyanobacteria isolated from a north-east Brazilian drinking water supply: Environmental Toxicology,v. 14, p. 31–35.
Duy, T. N., P. K. S. Lam, G. R. Shaw, and D. W. Connell, 2000,Toxicology and risk assessment of freshwater cyanobacterial(blue-green algal) toxins in water: Reviews of EnvironmentalContamination and Toxicology, v. 163, p. 113–186.
Edhorn, A. S., 1973, Further investigations of fossils from theAnimikie, Thunder Bay, Ontario: Proceedings of theGeologicalAssociation of Canada, v. 25, p. 37–66.
Ehrenreich, I. M., J. B. Waterbury, and E. A. Webb, 2005, Dis-tribution and diversity of natural product genes in marine andfreshwater cyanobacterial cultures and genomes: Applied andEnvironmental Microbiology, v. 71, p. 7401–7413.
Elleman, T. C., I. R. Falconer, A. R. Jackson, and M. T. Runnegar,1978, Isolation, characterization and pathology of the toxinfrom a Microcystis aeruginosa (= Anacystis cyanea) bloom: Aus-tralian Journal of Biological Sciences, v. 31, p. 209–218.
Emslie, S. D., W. D. Allmon, F. J. Rich, J. H. Wrenn, and S. D. deFrance, 1996, Integrated taphonomy of an avian death assem-blage in marine sediments from the late Pliocene of Florida:Palaeogeography, Palaeoclimatology, andPalaeoecology, v. 124,p. 107–136.
Epstein, P. R., and T. E. Ford, 1993, Marine ecosystems: Lancet,v. 342, p. 1216–1219.
Erwin, D. H., 1990a, Mass extinction: Events—End-Permian, inD. E. G. Briggs and P. R. Crowther, eds., Paleobiology a syn-thesis: Oxford, Blackwell Scientific, p. 187–194.
Erwin, D. H., 1990b, The end-Permian mass extinction: Annual Re-view of Ecology and Systematics, v. 21, p. 69–91.
Erwin, D. H., 1993, The great Paleozoic crisis: Life and death in thePermian: New York, Columbia University Press, 327 p.
Erwin, D. H., 1994, The Permo-Triassic extinction: Nature, v. 367,p. 231–236.
Erwin, D. H., 2006, Extinction: Princeton, Princeton University Press,296 p.
Eshet, Y., M. R. Rampino, and H. Visscher, 1995, Fungal event andpalynological record of ecological crisis and recovery across thePermian–Triassic boundary: Geology, v. 23, p. 967–970.
Falconer, I. R., ed., 1993, Algal toxins in seafood and drinking water:London, Academic Press, 224 p.
Falconer, I. R., 1996, Potential impact on human health of toxiccyanobacteria: Phycologia, v. 35, supplement 6, p. 6–11.
Falconer, I. R., 1998, Algal toxins and human health, in J. Hrubec,ed., The handbook of environmental chemistry 5: PartC: Berlin,Springer-Verlag, p. 53–82.
Falconer, I. R., 1999, An overview of problems caused by toxic blue-green algae (cyanobacteria) in drinking and recreational water:Environmental Toxicology, v. 14, p. 5–12.
Farmer, J. D., 1992, Grazing and bioturbation in modern microbialmats, in J. W. Schopf and C. Klein, eds., The Proterozoic bio-sphere: Cambridge, Cambridge University Press, p. 295–297.
Foster, C. B., M. H. Stephenson, C. Marshall, G. A. Logan, and P. F.Greenwood, 2002, A revision of Reduviasporonites Wilson 1962:Description, illustration, comparison andbiological affinities: Paly-nology, v. 26, p. 35–58.
Fujiki, H., M. Suganuma, H. Hakii, G. Bartolini, R. E. Moore, S.Takayama, and T. Sugimura, 1984, A two-stage mouse skincarcinogenesis study of lyngbyatoxin A: Journal of Cancer Re-search and Clinical Oncology, v. 108, p. 174–176.
Gerdes, G., and W. Krumbein, 1994, Peritidal potential stromato-lites, in J. Bertrand-Sarfati and C. Monty, eds., Phanerozoicstromatolites: Dordrecht, Kluwer, p. 101–129.
German, T. N., 1981a, Filamentousmicroorganisms in the LakhandaFormation on the Maya River: Paleontological Journal, v. 15,no. 2, p. 100–107.
German, T. N., 1981b, Filamentous algae from the MiroyedikhaFormation of the upper Precambrian: Paleontological Journal,v. 15, no. 4, p. 111–116.
Gerten, D., and R. Adrian, 2000, Climate-driven changes in springplankton dynamics and the sensitivity of shallow polymicticlakes to the North Atlantic Oscillation: Limnology and Ocean-ography, v. 45, p. 1058–1066.
Gleason, F. K., and C. A. Baxa 1986, Activity of the natural algicide,cyanobacterin, on eukaryotic microorganisms: FEMS Microbi-ology Letters, v. 33, p. 85–88.
Golovenok, V. K., and M. Y. Belova, 1984, Riphean microbiota incherts of the Billyakh Group on the Anabar uplift: Paleonto-logical Journal, v. 18, no. 4, p. 20–30.
Golovenok, V. K., and M. Y. Belova, 1985, Riphean microbiota incherts of the Yeniseyskiy Kryazh (Ridge): Paleontological Jour-nal, v. 19, no. 2, p. 88–99.
Golovenok, V. K., and M. Y. Belova, 1990, Palaeopleurocapsa in theRiphean deposits of the north of the Siberian craton: Trans-actions Doklady of the U.S.S.R. Academy of Sciences: EarthScience Sections, v. 310, no. 1, p. 236–240.
Golubic, S., 1976a, Organisms that build stromatolites, in M. R.Walter, ed., Stromatolites: Developments in Sedimentology 20:Amsterdam, Elsevier, p. 113–140.
Golubic, S., 1976b, Environmental microbiology of living stromat-olites, in M. R. Walter, ed., Stromatolites: Developments inSedimentology 20: Amsterdam, Elsevier, p. 141–148.
Green, J. W., A. H. Knoll, and K. Swett, 1988, Microfossils fromoolites and pisolites of the Upper Proterozoic Eleonore BayGroup, central East Greenland: Journal of Paleontology, v. 62,p. 835–852.
Gribble, G. W., 1996, The diversity of natural organochlorines inliving organisms: Pure and Applied Chemistry, v. 68, p. 1699–1712.
Haas, J., A. Demeny, K. Hips, N. Zajzon, T. G. Weiszburg, M.Sudar, and J. Palfy, 2007, Biotic and environmental changes inthe Permian–Triassic boundary interval recorded on a westernTethyan ramp in the Bukk Mountains, Hungary: Global andPlanetary Change, v. 55, p. 136–154.
Haines, A., A. J. McMichael, and P. R. Epstein, 2000, Environment
18 The Role of Toxin-Producing Algae in Phanerozoic Mass Extinctions
and health: 2. Global climate change and health: CanadianMedical Association Journal, v. 163, p. 729–734.
Hallam, A., 1990, Mass extinction: Processes—earth-bound causes,in D. E. G. Briggs and P. R. Crowther, eds., Paleobiology asynthesis: Oxford, Blackwell Scientific, p. 160–164.
Hallam, A., 2004, Catastrophes and lesser calamities—The causesof mass extinctions: Oxford, Oxford University Press, 274 p.
Hallam, A., and P. B. Wignall, 1997, Mass extinctions and theiraftermath: Oxford, Oxford University Press, 320 p.
Hallegraeff, G. M., 1993, A review of harmful algal blooms andtheir apparent global increase: Phycologia, v. 32, p. 79–99.
Hallock, P., and W. Schlager, 1986, Nutrient excess and the demiseof coral reefs and carbonate platforms: Palaios, v. 1, p. 389–398.
Harvell, C. D., et al., 1999, Emerging marine diseases-climate linksand anthropogenic factors: Science, v. 285, p. 1505–1510.
Hesselbo, S. P., S. A. Robinson, F. Surlyk, and S. Piasecki, 2002, Ter-restrial and marine extinction at the Triassic–Jurassic boundarysynchronized with major carbon-cycle perturbation: A link toinitiation of massive volcanism?: Geology, v. 30, p. 251–254.
Hildebrand, A. R., G. T. Penfield, D. A. Kring, M. Pilkington, A.Camargo, S. B. Jacobsen, and W. V. Boynton, 1991, Chicxulubcrater—A possible Cretaceous–Tertiary boundary impact crateron the Yucatan Peninsula: Geology, v. 19, p. 867–871.
Hips, K., and J. Haas, 2006, Calcimicrobial stromatolites at thePermian–Triassic boundary in a western Tethyan section, BukkMountains,Hungary: SedimentaryGeology, v. 185, p. 239–253.
Hirata K., S. Yoshitomi, S. Dwi, O. A. M. Iwabe, J. Polchai, and K.Miyamoto, 2003, Bioactivities of nostocine A produced by afreshwater cyanobacterium Nostoc spongiaeforme TISTR 8169:Journal of Bioscience and Bioengineering, v. 95, p. 512–517.
Hoffman, P., 1976, Environmental diversity of middle Precambri-an stromatolites, in M. R. Walter, ed., Stromatolites: Develop-ments in Sedimentology 20: Amsterdam, Elsevier, p. 599–611.
Hofmann, H. J., 1984, Organic-walled microfossils from the latestProterozoic and earliest Cambrian of the Wernecke Moun-tains, Yukon: Geological Survey of Canada, Paper 84-1B, p.285–297.
Hofmann, H. J., and J. W. Schopf, 1983, Early Proterozoicmicrofossils, in J. W. Schopf, ed., Earth’s earliest biosphere:Its origin and evolution: Princeton, Princeton University Press,p. 321–360.
Horodyski, R. J., and J. A. Donaldson, 1983, Distribution andsignificance of microfossils in cherts of the Middle ProterozoicDismal Lakes Group, District of Mackenzie, Northwest Terri-tories, Canada: Journal of Paleontology, v. 57, p. 271–288.
Hsu, K. J., 1986, Environmental changes in times of biotic crisis, inD. M. Raup and D. Jablonski, eds., Patterns and processes inthe history of life: Berlin, Springer-Verlag, p. 297–312.
Hunter, P. R., 1998, Cyanobacterial toxins and human health:Journal of Applied Microbiology, Symposium Supplement 84,p. 35S–40S.
Isozaki, Y., 1997, Permo-Triassic boundary superanoxia and strati-fied superocean; records from lost deep sea: Science, v. 276,p. 235–238.
Isozaki, Y., et al., 2004, Stratigraphy of the Middle–Upper Permianand lowermost Triassic at Chaotlan, Sichuan, China: Record ofLate Permian double mass extinction event: Proceedings of theJapan Academy, Series B: Physical and Biological Sciences,v. 80, p. 10–16.
Jablonski, D., 1990, Mass extinction: Processes—Extra-terrestrialcauses, inD.E.G.Briggs andP.R.Crowther, eds., Paleobiology asynthesis: Oxford, Blackwell Scientific, p. 164–171.
Joachimski, M. M., and W. Buggisch, 1993, Anoxic events in thelate Frasnian—Causes of the Frasnian–Famennian faunalcrisis?: Geology, v. 21, p. 675–678.
Johnson, J. G., G. Klapper, and C. A. Sandberg, 1985, Devonianeustatic fluctuations in Euramerica: Geological Society of Amer-ica Bulletin, v. 96, p. 567–587.
Kamo, S. L., G. K. Czamanske, Y. Amelin, V. A. Fedorenko, D. W.Davis, and V. R. Trofimov, 2003, Rapid eruption of Siberianflood-volcanic rocks and evidence for coincidence with thePermian–Triassic boundary and mass extinction at 251 Ma:Earth and Planetary Science Letters, v. 214, p. 75–91.
Kato, Y., K. Nakao, and Y. Isozaki, 2002, Geochemistry of LatePermian to Early Triassic pelagic cherts from southwest Japan:Implications for an oceanic redox change: Chemical Geology,v. 182, p. 15–34.
Kauffman, E. G., 1984, The fabric of Cretaceous marine extinc-tions, in W. A. Berggren and J. A. Van Couvering, eds., Catas-trophes and earth history: Princeton, Princeton University Press,p. 151–246.
Kauffman, E. G., 1986, High-resolution event stratigraphy:Regional and global Cretaceous bio-events, in O. H. Walliser,ed., Global bio-events: Lecture Notes in Earth Sciences 8:Berlin, Springer-Verlag, p. 279–335.
Kershaw, S., T. Zhang, and G. Lan, 1999, A microbialite carbonatecrust at the Permian–Triassic boundary in south China, and itspaleoenvironmental significance: Palaeogeography, Palaeocli-matology, and Palaeoecology, v. 146, p. 1–18.
Kershaw, S., Y. Li, S. Crasquin-Soleau, Q. Feng, X. Mu, P. Collin,A. Reynolds, and L. Guo, 2007, Earliest Triassic microbialitesin the South China block and other areas: Controls on theirgrowth and distribution: Facies, v. 53, p. 409–425.
King, G. M., 1991, Terrestrial tetrapods and the end Permian event:A comparison of analyses: Historical Biology, v. 5, p. 239–255.
Knoll, A. H., 1982, Microfossils from the late Precambrian Drakenconglomerate, Ny Friesland, Svalbard: Journal of Paleontology,v. 56, p. 755–790.
Knoll, A. H., 1984, Microbiotas of the late Precambrian HunnbergFormation, Nordaustlandet, Svalbard: Journal of Paleontology,v. 58, p. 131–162.
Knoll, A. H., and S. Golubic, 1979, Anatomy and taphonomy of aPrecambrian algal stromatolite: Precambrian Research, v. 10,p. 115–151.
Knoll, A. H., E. S. Barghoorn, and S. Golubic, 1975, Paleopleur-ocapsa wopfnerii gen. et sp. nov.: A Late Precambrian alga andits modern counterpart: Proceedings of the National Academyof Sciences of the United States of America, v. 72, p. 2488–2492.
Knoll, A. H., P. K. Strother, and S. Rossi, 1988, Distribution anddiagenesis of microfossils from the lower Proterozoic Duck CreekDolomite, western Australia: Precambrian Research, v. 38,p. 257–279.
Knoll, A. H., R. K. Bambach, D. E. Canfield, and J. P. Grotzinger,1996, Comparative earth history and Late Permian mass ex-tinction: Science, v. 273, p. 452–457.
Knoll, A. H., R. K. Bambach, J. L. Payne, S. Pruss, and W. W.Fischer, 2007, Paleophysiology and end-Permian mass extinc-tion: Earth and Planetary Science Letters, v. 256, p. 295–313.
Krull, E. S., and G. J. Retallack, 2000, dC13 depth profiles frompaleosols across the Permian–Triassic boundary: Evidence formethane release: Geological Society of America Bulletin, v. 112,p. 1459–1472.
Krumbein, W. E., Y. Cohen, and M. Shilo, 1977, Solar Lake (Sinai):4. Stromatolitic cyanobacterial mats: Limnology and Ocean-ography, v. 22, p. 635–656.
Kumar, A., D. P. Singh, M. B. Tyagi, A. Kumar, E. G. Prasuna, andJ. K. Thakur, 2000, Production of hepatotoxin by the cyano-bacterium Scytonema sp. Strain BT 23: Journal of Microbiologyand Biotechnology, v. 10, p. 375–380.
Castle and Rodgers 19
Lagos, N., H. Onodera, P. A. Zagatto, D. Andrinolo, S. M. F. O.Azevedo, and Y. Oshima, 1999, The first evidence of paralyticshellfish toxins in the freshwater cyanobacterium Cylindros-permopsis raciborskii, isolated from Brazil: Toxicon, v. 37,p. 1359–1373.
Lamond, R. E., and L. Tapanila, 2003, Embedment cavities in la-custrine stromatolites: Evidence of animal interactions fromCenozoic carbonates in U.S.A. and Kenya: Palaios, v. 18,p. 445–453.
Lampert, W., 1981, Toxicity of the blue-green Microcystis aeru-ginosa: Effective defense mechanism against grazing pressureby Daphnia: Internationale Vereinigung fur Theoretische undAngewandte Limnologie, v. 21, p. 1436–1440.
Landsberg, J.H., 2002, The effects of harmful algal blooms on aquaticorganisms: Reviews in Fisheries Science, v. 10, p. 113–390.
Lawrence, J. E., A. M. Chan, and C. A. Suttle, 2002, Virusescausing lysis of the toxic bloom-forming alga Heterosigmaakashiwo (Raphidophyceae) are widespread in coastal sedi-ments of British Columbia, Canada: Limnology and Ocean-ography, v. 47, p. 545–550.
Leflaive, J., and L. Ten-Hage, 2007, Algal and cyanobacterial sec-ondary metabolites in freshwaters: A comparison of allelopathiccompounds and toxins: Freshwater Biology, v. 52, p. 199–214.
Lehrmann, D. J., 1999, Early Triassic calcimicrobial mounds andbiostromes of the Nanpanjiang Basin, south China: Geology,v. 27, p. 359–362.
Lehrmann, D. J., J. L. Payne, S. V. Felix, P. M. Dillett, H. Wang, Y.Yu, and J. Wei, 2003, Permian–Triassic boundary sectionsfrom shallow-marine carbonate platforms of the NanpanjiangBasin, south China: Implications for oceanic conditions asso-ciated with the end-Permian extinction and its aftermath: Palaios,v. 18, p. 138–152.
Li, R., W. W. Carmichael, S. Brittain, G. Eaglesham, G. Shaw, Y.Liu, and M. M. Watanabe, 2001, First report of the cyano-toxins cylindrospermopsin and deoxycylindrospermopsin fromRaphidiopsis curvata (Cyanobacteria): Journal of Phycology,v. 37, p. 1121–1126.
Liu, X., Z. Liu, L. Zhang, and X. Xu, 1984, A study of late Pre-cambrian microfossil algal community from Suining County,Jiangsu Province: Acta Micropalaeontologica Sinica, v. 1,p. 171–182.
Luckas, B., J. Dahlmann, K. Erler, G. Gerdts, N. Wasmund, C.Hummert, and P. D. Hansen, 2005, Overview of key phyto-plankton toxins and their recent occurrence in the North andBaltic seas: Environmental Toxicology, v. 20, p. 1–17.
MacKintosh, C., K. A. Beattie, S. Klumpp, P. Cohen, and G. A.Codd, 1990, Cyanobacterial microcystin-Lr is a potent andspecific inhibitor of protein phosphatases 1 and 2A from bothmammals and higher plants: FEBS Letters, v. 264, p. 187–192.
Maithy, P. K., 1975, Micro-organisms from the Bushimay System(late Precambrian) of Kanshi, Zaire: The Palaeobotanist, v. 2,p. 133–149.
Maithy, P. K., and M. Shukla, 1977, Microbiota from the SuketShales, Ramapura, Vindhyan system (late Precambrian), MadhyaPradesh: The Palaeobotanist, v. 23, p. 176–188.
Mastin, B. J., J. H. Rodgers Jr., and T. L. Deardorff, 2002, Riskevaluation of cyanobacteria-dominated algal blooms in a NorthLouisiana reservoir: Journal of Aquatic Ecosystem Stress andRecovery, v. 9, p. 103–114.
Maxwell, W. D., 1989, The end Permian mass extinction, in S. K.Donovan, ed., Mass extinctions: Process and evidence: NewYork, Columbia University Press, p. 152–173.
Maxwell, W. D., 1992, Permian and Early Triassic extinction ofnon-marine tetrapods: Palaeontology, v. 35, p. 571–583.
Mayhew, P. J., G. B. Jenkins, and T. G. Benton, 2008, A long-termassociation between global temperature and biodiversity,
origination and extinction in the fossil record: Proceedings ofthe Royal Society B: Biological Sciences, v. 275, p. 47–53.
McElwain, J. C., J. Wade-Murphy, and S. P. Hesselbo, 1999,Changes in carbon dioxide during an oceanic anoxic eventlinked to intrusion into Gondwana coals: Nature, v. 435, p. 479–482.
McGhee Jr., G. R., 1989, The Frasnian–Famennian extinctionevent, in S. K. Donovan, ed., Mass extinctions: Process andevidence: New York, Columbia University Press, p. 133–151.
McGhee Jr., G. R., 1990, Mass extinction: Events—Frasnian–Famennian, in D. E. G. Briggs and P. R. Crowther, eds.,Paleobiology a synthesis: Oxford, Blackwell Scientific, p. 184–187.
McGhee Jr., G. R., 1996, The Late Devonian mass extinction: TheFrasnian/Famennian crisis: New York, Columbia UniversityPress, 303 p.
McLaren, D. J., 1970, Time, life, and boundaries: Journal of Pa-leontology, v. 44, p. 801–815.
McMenamin, D. S., S. Kumar, and S. M. Awramik, 1983, Microbialfossils from the Kheinjua Formation, Middle Proterozoic SemriGroup (lower Vindhyan), Son Valley area, central India: Pre-cambrian Research, v. 21, p. 247–271.
McRoberts, C. A., and C. R. Newton, 1995, Selective extinctionamong end-Triassic European bivalves: Geology, v. 23, p. 102–104.
Mendelson, C. V., and J. W. Schopf, 1982, Proterozoic microfossilsfrom the Sukhaya Tunguska, Shorikha, and Yudoma forma-tions of the Siberian Platform, U.S.S.R.: Journal of Paleontol-ogy, v. 56, p. 42–83.
Mendelson, C. V., and J. W. Schopf, 1992, Proterozoic and selectedEarly Cambrian microfossils and microfossil-like objects, inJ. W. Schopf and C. Klein, eds., The Proterozoic biosphere:Cambridge, Cambridge University Press, p. 865–952.
Mez, K., K. A. Beattie, G. A. Codd, K. Hanselmann, B. Hauser, H.Naegeli, and H. R. Preisig, 1997, Identification of a micro-cystin in benthic cyanobacteria linked to cattle deaths on alpinepastures in Switzerland: European Journal of Phycology, v. 32,p. 111–117.
Mohamed, Z. A., H. M. El-Sharouny, and W. S. M. Ali, 2006,Microcystin production in benthic mats of cyanobacteria in theNile River and irrigation canals, Egypt: Toxicon, v. 47, p. 584–590.
Monty, C. L., 1972, Recent algal stromatolitic deposits, AndrosIsland, Bahamas, preliminary report: Geologische Rundschau,v. 61, p. 742–783.
Muir, M. D., 1976, Proterozoic microfossils from the AmeliaDolomite, McArthur Basin, Northern Territory: Alcheringa,v. 1, p. 143–158.
Murphy, A. E., B. B. Sageman, and D. J. Hollander, 2000,Eutrophication by decoupling of the marine biogeochemicalcycles of C, N, and P: A mechanism for the Late Devonianmass extinction: Geology, v. 28, p. 427–430.
Namikoshi, M., K. L. Rinehart, R. Sakai, K. Sivonen, and W. W.Carmichael, 1990, Structures of three new cyclic heptapeptidehepatotoxins produced by the cyanobacterium (blue-greenalga)Nostoc sp. strain 152: Journal of Organic Chemistry, v. 55,p. 6135–6139.
Namikoshi, M., T. Murakami, M. F. Watanabe, T. Oda, J. Yamada,S. Tsujimura, H. Nagai, and S. Oishi, 2003, Simultaneousproduction of homoanatoxin-a, anatoxin-a, and a new non-toxic 4-hydroxyhomoanatoxin-a by the cyanobacteriumRaphidiopsis mediterranea Skuju: Toxicon, v. 42, p. 533–538.
Nautiyal, A. C., 1980, Cyanophycean algal remains and paleoecol-ogy of the Precambrian Gangolihat dolomites formation of theKumaun Himalaya: Indian Journal of Earth Sciences, v. 7,p. 1–11.
20 The Role of Toxin-Producing Algae in Phanerozoic Mass Extinctions
Nautiyal, A. C., 1983, Algonkian (upper to middle) micro-organisms from the Semri Group of Son Valley (MirzapurDistr.), India: Geoscience Journal, v. 4, p. 169–197.
Neilan, B. A., E. Dittmann, L. Rouhiainen, R. A. Bass, V. Schaub,K. Sivonen, and T. Borner, 1999, Nonribosomal peptide syn-thesis and toxigenicity of cyanobacteria: Journal of Bacteriol-ogy, v. 181, p. 4089–4097.
Nizan, S., C. Dimentman, and M. Shilo, 1986, Acute toxic effectsof the cyanobacterium Microcystis aeruginosa on Daphniamagna: Limnology and Oceanography, v. 31, p. 497–502.
Nyberg, A. V., and J. W. Schopf, 1984, Microfossils in stromatoliticcherts from the upper Proterozoic Min’yar Formation, south-ern Ural Mountains, U.S.S.R.: Journal of Paleontology, v. 58,p. 738–772.
Oberholster, P. J., A. M. Botha, and J. U. Grobbelaar, 2004,Microcystis aeruginosa: Source of toxic microcystins in drinkingwater: African Journal of Biotechnology, v. 3, p. 159–168.
Oberholster, P. J., A. Botha, and T. E. Cloete, 2005, An overview oftoxic freshwater cyanobacteria in South Africa with specialreference to impact and detection by molecular marker tools:Biokemistri, v. 17, p. 57–71.
Oehler, J. H., 1977, Microflora of the H. Y. C. Pyritic ShaleMember of the Barney Creek Formation (McArthur Group),Middle Proterozoic of northern Australia: Alcheringa, v. 1,p. 315–349.
Oehler, D. Z., 1978, Microflora of the middle Proterozoic BalbiriniDolomite (McArthur Group) of Australia: Alcheringa, v. 2,p. 269–309.
Ogurtsova, R. N., and V. N. Sergeev, 1987, The microbiota of theupper Precambrian Chichkanskaya Formation in the LesserKaratau region (southern Kazakhstan): Paleontological Jour-nal, v. 21, no. 2, p. 101–112.
O’Keefe, J. D., and T. J. Ahrens, 1989, Impact production of CO2
by the Cretaceous–Tertiary extinction bolide and the resultantheating of the Earth: Nature, v. 338, p. 247–249.
Olsen, P. E., N. H. Shubin, and M. H. Anders, 1987, New EarlyJurassic tetrapod assemblages constrain Triassic–Jurassic tet-rapod extinction event: Science, v. 237, p. 1025–1029.
Olsen, P. E., D. V. Kent, H. D. Sues, C. Koeberl, H. Huber, A.Montanari, E. C. Rainforth, S. J. Fowell, M. J. Szajna, andB. W. Hartline, 2002, Ascent of dinosaurs linked to an iridiumanomaly at the Triassic–Jurassic boundary: Science, v. 296,p. 1305–1307.
Osborne, N. J., P. M. Webb, and G. R. Shaw, 2001, The toxins ofLyngbya majuscula and their human and ecological healtheffects: Environment International, v. 27, p. 381–392.
Paerl, H. W., and D. R. Whitall, 1999, Anthropogenically-derivedatmospheric nitrogen deposition, marine eutrophication andharmful algal bloom expansion: Is there a link?: Ambios, v. 28,p. 307–311.
Pandey, U., and J. Pandey, 2002, Antibacterial properties ofcyanobacteria: A cost-effective and eco-friendly approach tocontrol bacterial leaf spot disease of chilli: Current Science,v. 82, p. 262–264.
Patterson, G. M. L., and C. M. Bolis, 1994, Scytophycin productionby axenic cultures of the cyanobacterium Scytonema ocellatum:Natural Toxins, v. 2, p. 280–285.
Paul, V. J., 2008, Global warming and cyanobacterial harmful algalblooms, in H. K. Hudnell, ed., Cyanobacterial harmful algalblooms: State of the science and research needs: Advances inExperimental Medicine and Biology: New York, Springer,v. 619, p. 239–257.
Pennings, S. C., A. M. Weiss, and V. J. Paul, 1996, Secondarymetabolites of the cyanobacteriumMicrocoleus lyngbyaceus andthe sea hare Stylocheilus longicauda: Palatability and toxicity:Marine Biology, v. 126, p. 735–743.
Phlips, E. J., S. Badylak, S. Youn, and K. Kelley, 2004, Theoccurrence of potentially toxic dinoflagellates and diatoms in asubtropical lagoon, the Indian River Lagoon, Florida, U.S.A.:Harmful Algae, v. 3, p. 39–49.
Pierce, R. H., M. S. Henry, L. S. Proffitt, and P. A. Hasbrouck,1990, Red tide toxin (brevetoxin) in marine aerosol, in E.Graneli, B. Sundstrom, L. Edler, and D. M. Anderson, eds.,Toxic marine phytoplankton: Amsterdam, Elsevier, p. 397–402.
Pratt, B. R., 1982, Stromatolite decline—A reconsideration:Geology, v. 10, p. 512–515.
Pruss, S. B., F. A. Corsetti, and D. J. Bottjer, 2005, The unusualrock record of the Early Triassic: A case study from the south-western United States: Palaeogeography, Palaeoclimatology,and Palaeoecology, v. 222, p. 33–52.
Pruss, S. B., D. J. Bottjer, F. A. Corsetti, and A. Baud, 2006, Aglobal marine sedimentary response to the end-Permian massextinction: Examples from southern Turkey and the westernUnited States: Earth-Science Reviews, v. 78, p. 193–206.
Raup, D. M., 1979, Size of the Permo-Triassic bottleneck and itsevolutionary implications: Science, v. 206, p. 217–218.
Raup, D. M., and J. J. Sepkoski Jr., 1982, Mass extinction in themarine fossil record: Science, v. 215, p. 1501–1503.
Renne, P. R., Z. Zichao, M. A. Richards, M. T. Black, and A. R.Basu, 1995, Synchrony and causal relations between Permian–Triassic boundary crises and Siberian flood volcanism: Science,v. 269, p. 1413–1416.
Retallack, G. J., 1995, Permian–Triassic life crisis on land: Science,v. 267, p. 77–80.
Retallack, G. J., A. Seyedolali, E. S. Krull, W. T. Holser, C. P.Ambers, and F. T. Kyte, 1998, Search for evidence of impact atthe Permian–Triassic boundary in Antarctica and Australia:Geology, v. 26, p. 979–982.
Riding, R., 1991a, Classification of microbial carbonates, in R.Riding, ed., Calcareous algae and stromatolites: Berlin, Springer-Verlag, p. 21–51.
Riding, R., 1991b, Calcified cyanobacteria, in R. Riding, ed.,Calcareous algae and stromatolites: Berlin, Springer-Verlag,p. 55–87.
Riding, R., 1997, Stromatolite decline: A brief reassessment: Facies,v. 36, p. 227–230.
Riding, R., 2000, Microbial carbonates: The geological record ofcalcified bacterial-algal mats and biofilms: Sedimentology, v. 47,p. 179–214.
Riding, R., 2006, Microbial carbonate abundance compared withfluctuations in metazoan diversity over geological time: Sedi-mentary Geology, v. 185, p. 229–238.
Riegman, R., 1998, Species composition of harmful algal blooms inrelation to macronutrient dynamics, in D. M. Anderson, A. D.Cembella, and G. M. Hallegraeff, eds., Physiological ecology ofharmful algal blooms: Berlin, Springer-Verlag, p. 475–488.
Ross, C., L. Santiago-Vazquez, and V. Paul, 2006, Toxin release inresponse to oxidative stress and programmed cell death in thecyanobacterium Microcystis aeruginosa: Aquatic Toxicology,v. 78, p. 66–73.
Sandberg, C. A., W. Ziegler, R. Dreesen, and J. L. Butler, 1988,Late Frasnian mass extinction: Conodont event stratigraphy,global changes, and possible causes: Courier ForschungsinstitutSenckenberg, v. 102, p. 263–307.
Sano, H., and K. Nakashima, 1997, Lowermost Triassic (Griesba-chian) microbial bindstone-cementstone facies, southwest Japan:Facies, v. 36, p. 1–24.
Schembri, M. A., B. A. Neilan, and C. P. Saint, 2001, Identificationof genes implicated in toxin production in the cyanobacteriumCylindrospermopsis raciborskii: Environmental Toxicology, v. 16,p. 413–421.
Castle and Rodgers 21
Schopf, J. W., 1968, Microflora of the Bitter Springs Formation, latePrecambrian, central Australia: Journal of Paleontology, v. 42,p. 651–688.
Schopf, J. W., 1993, Microfossils of the Early Archean Apex chert:New evidence of the antiquity of life: Science, v. 260, p. 640–646.
Schopf, J. W., 1999, Cradle of life: The discovery of earth’s earliestfossils: Princeton, Princeton University Press, 367 p.
Schopf, J. W., 2000a, The fossil record: Tracing the roots of thecyanobacterial lineage, in B. A. Whitton and M. Potts, eds.,The ecology of cyanobacteria: Dordrecht, The Netherlands,Kluwer Academic Publishers, p. 13–35.
Schopf, J. W., 2000b, The paleobiologic record of cyanobacterialevolution, in Y. V. Brun and L. J. Shimkets, eds., Prokaryoticdevelopment: Washington, D.C., American Society of Micro-biology Press, p. 105–129.
Schopf, J. W., 2004, Extinctions in life’s earliest history, in P. D.Taylor, ed., Extinctions in the history of life: Cambridge,Cambridge University Press, p. 35–60.
Schrader, K. K., and W. T. Blevins, 1993, Geosmin-producingspecies of Streptomyces and Lyngbya from aquaculture ponds:Canadian Journal of Microbiology, v. 39, p. 834–840.
Schubert, J. K., and D. J. Bottjer, 1992, Early Triassic stromatolitesas post-extinction disaster forms: Geology, v. 20, p. 883–886.
Sephton, M. A., K. Amor, I. A. Franchi, P. B. Wignall, R. Newton,and J. P. Zonneveld, 2002, Carbon and nitrogen isotopedisturbances and an end-Norian (Late Triassic) extinctionevent: Geology, v. 30, p. 1119–1122.
Sepkoski Jr., J. J., 1986, Phanerozoic overview of mass extinction, inD. M. Raup and D. Jablonski, eds., Patterns and processes inthe history of life: Berlin, Springer-Verlag, p. 277–295.
Sergeev, V. N., 2001, Paleobiology of the Neoproterozoic (upperRiphean) Shorikha and Burovaya silicified microbiotas, Tur-ukhansk uplift, Siberia: Journal of Paleontology, v. 75, no. 2,p. 427–448.
Sergeev, V. N., and I. N. Krylov, 1986, Microfossils of the Min’yarFormation of the Urals: Paleontological Journal, v. 20, no. 1,p. 63–75.
Sergeev, V. N., A. H. Knoll, S. P. Kolosova, P. N. Kolosov, 1994, Mi-crofossils in cherts from the Mesoproterozoic (middle Riphean)Debengda Formation, the Olenek uplift, northeastern Siberia:Stratigraphy and Geological Correlation, v. 2, no. 1, p. 19–33.
Sheehan, P. M., 2001, The Late Ordovician mass extinction: AnnualReview of Earth and Planetary Sciences, v. 29, 331–364.
Sheehan, P. M., and M. T. Harris, 2004, Microbialite resurgenceafter the Late Ordovician extinction: Nature, v. 430, p. 75–78.
Shumway, S. E., 1990, A review of the effects of algal blooms onshellfish and aquaculture: Journal of the World AquacultureSociety, v. 21, p. 65–104.
Shumway, S. E., S. M. Allen, and P. D. Boersma, 2003, Marinebirds and harmful algal blooms: Sporadic victims or under-reported events?: Harmful Algae, v. 2, p. 1–17.
Sivonen, K., 1990, Effects of light, temperature, nitrate, ortho-phosphate, and bacteria on growth of and hepatotoxin pro-duction by Oscillatoria agardhii strains: Applied and Environ-mental Microbiology, v. 56, p. 2658–2666.
Sivonen, K., 1996, Cyanobacterial toxins and toxin production:Phycologia, v. 35, supplement 6, p. 12–24.
Sivonen, K., and G. Jones, 1999, Cyanobacterial toxins, in I. Chorusand J. Bartram, eds., Toxic cyanobacteria in water: A guide totheir public health consequences, monitoring and manage-ment: London, Spon, p. 41–111.
Skulberg, O. M., 2000, Microalgae as a source of bioactivemolecules—Experience from cyanophyte research: Journal ofApplied Phycology, v. 12, p. 341–348.
Skulberg, O. M., G. A. Codd, and W. W. Carmichael, 1984, Blue-green algal blooms in Europe: A growing problem: Ambio,v. 13, p. 244–247.
Skulberg, O. M., W. W. Carmichael, G. A. Codd, and R. Skulberg,1993, Taxonomy of toxic Cyanophyceae (cyanobacteria), inI. R. Falconer, ed., Algal toxins in seafood and drinking water:London, Academic Press, p. 145–164.
Smayda, T. J., 1990, Novel and nuisance phytoplankton blooms inthe sea: Evidence for a global epidemic, in E. Graneli, B.Sundstrom, L. Edler, and D. M. Anderson, eds., Toxic marinephytoplankton: Amsterdam, Elsevier, p. 29–41.
Soltani, N., R. A. Khavari-Nejad, M. T. Yazdi, S. Shokravi, andFernandez-Valiente, 2005, Screening of soil cyanobacteria forantifungal and antibacterial activity: Pharmaceutical Biology,v. 43, p. 455–459.
Steffensen, D., M. Burch, B. Nicholson, M. Drikas, and P. Baker,1999, Management of toxic blue-green algae (cyanobacteria)in Australia: Environmental Toxicology, v. 14, p. 183–195.
Stephens, N. P., and D. Y. Sumner, 2000, Paleoecology of aFamennian (Late Devonian) microbial reef, Canning Basin,western Australia: Geological Society of America Abstractswith Program, v. 32, no. 7, p. 278–279.
Strother, P. K., A. H. Knoll, and E. S. Barghoorn, 1983, Micro-organisms from the late Precambrian Narssarssuk Formation,north-westernGreenland: Palaeontology, Part 1, v. 26, p. 1–32.
Surdam, R. C., and K. O. Stanley, 1979, Lacustrine sedimentationduring the culminating phase of Eocene Lake Gosiute, Wyo-ming (Green River Formation): Geological Society of AmericaBulletin, v. 90, p. 93–110.
Teixeira, M. G. L. C., M. C. N. Costa, V. L. P. Carvalho, M. S.Pereira, and E. Hage, 1993, Gastroenteritis epidemic in thearea of the Itaparica Dam, Bahia, Brazil: Bulletin of the PanAmerican Health Organization, v. 27, p. 244–253.
Todorova, A., and F. Juttner 1996, Ecotoxicological analysis ofnostocyclamide, a modified cyclic hexapeptide from Nostoc:Phycologia, v. 35, p. 183–188.
Turner, J. T., and P. A. Tester, 1997, Toxic marine phytoplankton,zooplankton grazers, and pelagic food webs: Limnology andOceanography, v. 42, p. 1203–1214.
Turner, J. T., P. A. Tester, and P. J. Hansen, 1998, Interactionsbetween toxic marine phytoplankton and metazoan andprotistan grazers, in D. M. Anderson, A. D. Cembella, andG. M. Hallegraeff, eds., Physiological ecology of harmful algalblooms: Berlin, Springer-Verlag, p. 453–474.
Tynni, R., and J. Donner, 1980, A microfossil and sedimentationstudy of the late Precambrian formation of Hailuoto, Finland:Geological Survey of Finland, Bulletin, v. 311, 27 p.
Tynni, R., and A. Uutela, 1984, Microfossils from the PrecambrianMuhos Formation in western Finland: Geological Survey ofFinland Bulletin, v. 330, 38 p.
Upfold, R. L., 1984, Tufted microbial (cyanobacterial) mats fromthe Proterozoic Stoer Group, Scotland: Geology Magazine,v. 121, p. 351–355.
Utkilen, H., and N. Gjolme 1992, Toxin production by Microcystisaeruginosa as a function of light in continuous cultures and itsecological significance: Applied and Environmental Microbi-ology, v. 58, p. 1321–1325.
Van Apeldoorn, M. E., H. P. Van Egmond, G. J. A. Speijers, andG. J. I. Bakker, 2007, Toxins of cyanobacteria: MolecularNutrition and Food Research, v. 51, p. 7–60.
Van de Schootbrugge, B., F. Tremolada, Y. Rosenthal, T. R. Bailey,S. Feist-Burkhardt, H. Brinkhuis, J. Pross, D. V. Kent, and P. G.Falkowski, 2007, End-Triassic calcification crisis and blooms oforganic-walled ‘‘disaster species’’: Palaeogeography, Palaeocli-matology, and Palaeoecology, v. 244, p. 126–141.
Van Dolah, F. M., 2000, Marine algal toxins: Origins, health effects,
22 The Role of Toxin-Producing Algae in Phanerozoic Mass Extinctions
and their increased occurrence: Environmental Health Per-spectives, v. 108, supplement 1, p. 133–141.
Visscher, H., H. Brinkhuis, D. L. Dilcher, W. C. Elsik, Y. Eshet,C. V. Looy, M. R. Rampino, and A. Traverse, 1996, The ter-minal Paleozoic fungal event: Evidence of terrestrial ecosystemdestabilization and collapse: Proceedings of the National Acad-emy of Sciences of the United States of America, v. 93, p. 2155–2158.
Visser, P. M., B. W. Ibelings, L. R. Mur, and A. E. Walsby, 2005,The ecophysiology of the harmful cyanobacterium Microcystis,in J. Huisman, H. C. P. Matthijs, and P. M. Visser, eds., Harm-ful cyanobacteria: Dordrecht, Springer, p. 109–142.
Whalen, M. T., G. P. Eberli, and P. W. Homewood, 1998, Mi-crobial carbonates as indicators of environmental change andbiotic crises in carbonate systems: Examples from the UpperDevonian, Alberta Basin, Canada: Geological Society of Amer-ica Abstracts with Program, v. 30, no. 7, p. 195.
White, S. H., L. J. Duivenvoorden, and L. D. Fabbro, 2005, Adecision-making framework for ecological impacts associatedwith the accumulation of cyanotoxins (cylindrospermopsinand microcystin): Lakes and Reservoirs: Research and Manage-ment, v. 10, p. 25–37.
Wicks, R. J., and P. G. Thiel, 1990, Environmental factors affectingthe production of peptide toxins in floating scums of thecyanobacterium Microcystis aeruginosa in a hypertrophic Afri-can reservoir: Environmental Science and Technology, v. 24,p. 1413–1418.
Wignall, P. B., and A. Hallam, 1992, Anoxia as a cause of thePermian/Triassic mass extinction: Facies evidence from north-ern Italy and the western United States: Palaeogeography,Palaeoclimatology, and Palaeoecology, v. 93, p. 21–46.
Wignall, P. B., and A. Hallam, 1993, Griesbachian (Earliest Triassic)paleoenvironmental changes in the Salt Range, Pakistan andsoutheast China and their bearing on the Permo-Triassic massextinction: Palaeogeography, Palaeoclimatology, and Palaeo-ecology, v. 102, p. 215–237.
Wignall, P. B., and R. J. Twitchett, 1996, Oceanic anoxia and the endPermian mass extinction: Science, v. 272, p. 1155–1158.
Wignall, P. B., A. Hallam, X. Lai, and F. Yang, 1995, Paleoenviron-mental changes across the Permian/Triassic boundary at Shangsi(N. Sichuan, China): Historical Biology, v. 10, p. 175–189.
Wilde, P., and W. B. N. Berry, 1984, Destabilization of the oceanicdensity structure and its significance to marine ‘‘extinction’’
events: Palaeogeography, Palaeoclimatology, and Palaeoecol-ogy, v. 48, p. 143–162.
Wilde, S. B., T. M. Murphy, C. P. Hope, S. K. Haburn, J. Kempton,A. Birrenkott, F. Wiley, W. W. Bowerman, and A. J. Lewitus,2005, Avian vacuolar myelinopathy linked to exotic aquaticplants and a novel cyanobacterial species: Environmental Toxi-cology, v. 20, p. 348–353.
Xie, S., R. D. Pancost, H. Yin, H. Wang, and R. P. Evershed, 2005,Two episodes of microbial change coupled with Permo/Triassicfaunal mass extinction: Nature, v. 434, p. 494–497.
Xie, S., R. D. Pancost, J. Huang, P. B. Wignall, J. Yu, X. Tang, L.Chen, X. Huang, and X. Lai, 2007, Changes in the globalcarbon cycle occurred as two episodes during the Permian-Triassic crisis: Geology, v. 35, p. 1083–1086.
Xu, Z. L., 1984, Investigation on the procaryotic microfossils fromthe Gaoyuzhuang Formation, Jixian, North China: Acta Bo-tanica Sinica, v. 26, p. 216–222.
Yan, T., and M.-J. Zhou, 2004, Environmental and health effects asso-ciated with harmful algal bloom and marine algal toxins in China:Biomedical and Environmental Sciences, v. 17, p. 165–176.
Yin, H., Q. Feng, X. Lai, A. Baud, and J. Tong, 2007, Theprotracted Permo-Triassic crisis and multi-episode extinctionaround the Permian–Triassic boundary: Global and PlanetaryChange, v. 55, p. 1–20.
Yu, J. X., Y. Q. Peng, S. X. Zhang, F. Q. Yang, Q. M. Zhao, andQ. S. Huang, 2007, Terrestrial events across the Permian–Triassic boundary along the Yunnan-Guizhou border, SW China:Global and Planetary Change, v. 55, p. 193–208.
Zhang, Y., 1981, Proterozoic stromatolite microfloras of the Gao-yuzhuang Formation (early Sinian:Riphean), Hebei, China: Jour-nal of Paleontology, v. 55, p. 485–506.
Zhang, Y., 1985, Stromatolitic microbiota from the Middle Prote-rozoic Wumishan Formation (Jixian Group) of the Ming Tombs,Beijing, China: Precambrian Research, v. 30, p. 277–302.
Zhang, Y., 1988, Proterozoic stromatolitic micro-organisms fromHebei, North China: Cell preservation and cell division: Pre-cambrian Research, v. 38, p. 165–175.
Zhang, Z., 1982, Filamentous microfossils from the DoushantuoFormation (late Sinian) of South China: Journal of Paleontol-ogy, v. 56, p. 1251–1256.
Zhang, Z., 1986, New material of filamentous fossil cyanophytesfrom the Doushantuo Formation (late Sinian) in the easternYangtze Gorge: Scientia Geologica Sinica, v. 1986, p. 30–37.
Castle and Rodgers 23