Hypothesis for the role of toxin-producing algae in ...newsstand.clemson.edu/.../uploads/2009/2336_295_mass_extinction… · munities, which they attributed to the Late Devonian mass

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.


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.


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


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),


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),


Lyngbyatoxin-a Skin, gastrointestinal tract Lyngbya, Schizothrix, Planktothrix (Oscillatoria) Alkaloids; inflammatory agents, protein

kinase C activators

Codd et al. (1999, 2005),


Saxitoxins Neurotoxin, nerve axons Anabaena, Aphanizomenon, Lyngbya,

Cylindrospermopsis, Planktothrix (Oscillatoria)

Carbamate alkaloids, sodium

channel-blockers

Codd et al. (1999, 2005),


LipopolysaccharidesG� cyanobacteria General irritant, affects

any exposed tissue

‘‘All’’ G� cyanobacteria (prokaryotes) Lipopolysaccharides; endotoxins,

inflammatory agents, gastrointestinal

irritants


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.


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)


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)


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)


Vindhyan Supergroup (1050 Ma); India McMenamin et al. (1983)


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)




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)


Lakhanda Formation (950 Ma); Siberia German (1981b)


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)


Miroyedikha Formation (1000 Ma); Siberia German (1981a)

Burovaya Formation and Shorikha Formation

(1000 Ma); Siberia

Sergeev (2001)


Hunnberg Formation (775 Ma); Svalbard and

Jan Mayen Island

Knoll (1984)





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)



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


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.


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.


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Hypothesis for the role of toxin-producing algae in ...newsstand.clemson.edu/.../uploads/2009/2336_295_mass_extinction… · munities, which they attributed to the Late Devonian mass