LETTERS
PUBLISHED ONLINE: 18 SEPTEMBER 2011 | DOI: 10.1038/NGEO1264
Transient metazoan reefs in the aftermath of the
end-Permian mass extinction
Arnaud Brayard1 *, Emmanuelle Vennin1 , Nicolas Olivier2 , Kevin G. Bylund3 , Jim Jenks4 ,
Daniel A. Stephen5 , Hugo Bucher6 , Richard Hofmann6 , Nicolas Goudemand6 and Gilles Escarguel2
Recovery from the devastating Permian–Triassic mass
extinction about 252 million years ago is usually assumed
to have spanned the entire 5 million years of the Early
Triassic epoch1,2 . The post-crisis interval was characterized
by large-scale fluctuations of the global carbon cycle and
harsh marine conditions, including a combination of ocean
acidification, euxinia, and fluctuating productivity3 . During this
interval, metazoan-dominated reefs are thought to have been
replaced by microbial deposits that are considered the hallmark
of the Early Triassic4–7 . Here we use field and microscopic
investigations to document Early Triassic bioaccumulations
and reefs from the western USA that comprise of various
sponges and serpulids associated with microbialites and other
eukaryotic benthic organisms. These metazoan-rich reefs were
formed only 1.5 million years after the extinction, in contrast to
previous suggestions of a much delayed recovery of complex
benthic communities. We conclude that the predominance
of microbial reefs following the mass extinction is restricted
to short intervals of the earliest Triassic. We suggest that
metazoan reef building continued throughout the Early Triassic
wherever permitted by environmental conditions.
Contrasting with a delayed recovery paradigm, mostly derived
from diversity patterns of benthic organisms (for example,
bivalves, gastropods), recent analyses on nekto-pelagic taxa such as
ammonoids and conodonts document an explosive Early Triassic
rediversification within less than 2 million years (Myr) after the
Permian–Triassic (PT) crisis8,9 . Nevertheless, metazoan reefs (see
Supplementary Information for definition) formed by organisms
such as sponges or corals are still acknowledged to re-establish
during the Middle Triassic10–12 . Their reappearance often serves
as marker for the end of the recovery. Indeed, reports of welldated Early Triassic metazoan reef builders have been exceptional
(Fig. 1). Sponge concentrations are known from the Spathian of
Utah and Nevada13,14 . Small bivalve bioherms and a stromatolite–
sponge–Tubiphytes association are recognized in the Spathian of
Nevada15,16 , and a stromatolite–sponge association is known from
the late Lower Triassic of the Germanic basin17 . Some isolated
bryozoans and calcareous algae are also reported18,19 . Despite
these rare occurrences, a global Early Triassic metazoan reef gap
seems remarkable. This gap is often interpreted as the outcome
of combined persistent or intermittent harsh environmental
conditions and exacerbated biotic competitive pressures6,20 .
Here we present new evidence for large, in situ Early Triassic
metazoan bioaccumulations and reefs formed by various sponges
and serpulids associated with different microbial carbonates and
eukaryotic organisms (Fig. 1; Supplementary Fig. S1). The oldest
metazoan bioaccumulations and reefs are located near the base of
the Thaynes Group in sections of the Pahvant Range (PR) and
the Mineral Mountains (MM; Fig. 2). Ammonoid and conodont
biostratigraphy indicates an early Smithian age for these levels,
occurring within the ‘Meekoceras n. sp. 1 and 2 beds’ and below
the ‘Radioceras aff. evolvens bed’ for the PR, and within the
‘Vercherites aff. pulcher bed’ for the MM. U/Pb calibration of
the ammonoid zonation indicates that they postdate the PT
boundary by only ∼1.5 Myr2 .
In the PR, the oldest reefs consist of small (∼5 mm) sponges
encrusting thin bivalve shell layers (Figs 2i, 3a), which probably facilitated their settlement and enhanced their preservation. Although
these sponges are preserved in life position, their initial essentially
globular shape now seems compacted (Supplementary Fig. S2).
The sponges are associated with small serpulids within a very
abundant micritic matrix, and with common echinoderm plates
(probably crinoids) locally reworked as bioclastic accumulations
in storm-induced deposits. These biostromes, tens of centimetres
thick, are formed by alternating gregarious settling and hydraulic reworking. The latter leads to multiple short-term events of hard-part
concentrations in a low to moderate energy mid ramp environment.
Isolated sponges are also found within overlying beds, identified
only by sparse bundles of spicules. Sponges occur a few metres
higher in recurrent large (∼50 m of lateral exposure) lenticular ∼ 5cm-thick layers, throughout a ∼20 m-thick stratigraphic interval
(Figs 2ii, 3b,c; Supplementary Figs S4–S6). These sponges are preserved in situ as lenticular reefs composed of small coalesced spheres
(≤1 cm in diameter) that resemble lyssacine hexactinellids bound
by submillimetre-scale biofilms. Within the lowermost Spathian PR
beds, serpulids form small millimetre to centimetre-consortia with
abundant ostracods, brachiopods and rare gastropods, alternating
with tempestite deposits (Fig. 2iii; Supplementary Fig. S7).
Early Smithian reef deposits in the MM are characterized by
more diverse sponge morphologies (Figs 2iv–v, 3d–h; Supplementary Figs S8–S22). The oldest sponges are embedded within
microbialites forming reefs, tens of centimetres thick, distributed
throughout a massive (up to 10 m high) microbial carbonate unit.
These microbialites are composed of centimetre-scale stromatolitic
domes and thrombolites sealed off by micrite. Complete cup- to
flat-shape and dendroid centimetre-scale sponges are preserved,
resting on micrite matrix or encrusting microbialitic crusts. They
show an internal re-crystallized spiculitic network and are often
1 UMR
CNRS 5561 Biogéosciences, Université de Bourgogne, 6 boulevard Gabriel, 21000 Dijon, France, 2 UMR CNRS 5276 Laboratoire de géologie de Lyon:
Terre, Planètes, Environnement, Université Lyon 1, 27-43 Boulevard du 11 novembre 1918, 69622 Villeurbanne Cedex, France, 3 140 South 700 East, Spanish
Fork, Utah 84660, USA, 4 1134 Johnson Ridge Lane, West Jordan, Utah 84084, USA, 5 Department of Earth Science, Utah Valley University, 800 W.
University Parkway, Orem, Utah 84058, USA, 6 Paläontologisches Institut und Museum, Universität Zürich, Karl-Schmid Strasse 4, CH-8006 Zürich,
Switzerland. *e-mail: arnaud.brayard@u-bourgogne.fr.
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NATURE GEOSCIENCE DOI: 10.1038/NGEO1264
Pahvant Range
145 m
BM
iii
110 m
CR
Utah
Nevada
37° N
Associated
organisms
105 m
PR
MM
100 m
HC/BD
95 m
Arizona
Echinoderms
Brachiopods
Foraminifers
Ostracods
Conodonts
Microbial dep.
O.k.
90 m
MM: Mineral M.
PR: Pahvant R.
BM: Butte M.
WM: Wasatch M.
b
Fle.
110° W
80 m
100 m
LCS: Lost Cabin Spring
MU: Muddy M.
75 m
90 m
70 m
65 m
%)
δδ13Ccarb ( %
60 m
248.12 +
¬ 0.28
Thaynes Grp.
Smithian
HR: Humboldt R.
CR: Confusion R.
HC: Hurricane Cliffs
BD: Beaver Dam M.
Limestone
Sandy limest.
Shelly limest.
Calcareous
shale
Shale
See also:
vi Figs 3i¬k, S23¬S26
v Figs 3h, S21¬S22
iv Figs 3d¬g, S8¬S20
iii Fig. S7
ii Figs 3b¬c, S4¬S6
i Figs 3a, S2¬S3
Mineral Mountains
85 m
115° W
Sandstone
Stromatolites
Bivalves
Serpulids
Gastropods
Ammonoids
MU
LCS
Lithologies
Coalesced
spheres
Isolated
spheres
Bivalveencrusted
Encrusting
or branching
Plate
A.k.
115 m
WM
HR
Sponge
framework
85 m
I.n.
vi
Spathian
100 km
42° N
SP.
a
80 m
Xe.
75 m
A.k.
K.A.
55 m
Spathian
Early Triassic
50 m
50 m
45 m
45 m
HR
40 m
BD
HC
CR
250.55 +
¬ 0.4
40 m
M.2.
ii
35 m
30 m
Thaynes Grp.
Smithian
O.k.
I.n.
35 m
30 m
MM
Smithian
PR
251.22 +
¬ 0.2
25 m
25 m
M.1.
R.e.
Dienerian
20 m
Co
15 m
Griesbachian
252.6 +
¬ 0.2
Permian
20 m
i
10 m
¬2
0
2
4
v
V.p.
15 m
iv
10 m
?
5m
Figure 1 | Geographic and temporal overview of the studied Early Triassic
bioaccumulations and reefs from western USA. a, Present-day location.
White and black stars indicate Smithian and Spathian outcrops,
respectively (R.: Range; M.: Mountains); black circles indicate previously
described Spathian bivalve bioherms in the Muddy Mountains (ref. 15),
sponge reef in Lost Cabin Spring (ref. 16), and sponge occurrences in the
Butte Mountains and Wasatch Mountains (ref. 14). b, Early Triassic
timescale in Myr with simplified global δ 13 C trend (both adapted from
ref. 2). New reefs reported in this study are symbolized by grey circles.
5m
?
v v v v
0m
0m
Red beds
Permian
Red beds
Permian
partially to completely dissolved and replaced by calcite-cemented
cavities (Fig. 3e; Supplementary Fig. S10). Within the uppermost
part of this unit, some cylindrical or branching, imbricated
calcite-cemented cavities reach sizes of tens of centimetres. Their
external wall contacts are fringed by a complex network made
of regular, successive lined micritic pores or larger sprout-like
Figure 2 | Simplified litho- and biostratigraphy for the PR and MM
sections. Bioaccumulations and reefs with associated benthic and
nekto-pelagic organisms. Ammonoid-based biostratigraphy: Xe.,
Glyptophiceras-Xenoceltites beds; A.k., Anasibirites kingianus beds; O.k.,
Owenites koeneni beds; Fle., Flemingites beds; I.n., Inyoites n. sp. beds; K.A.,
Kashmirites-Arctoceras beds; M.2., Meekoceras n. sp.2 bed; M.1., Meekoceras
n. sp.1 beds; R.e., Radioceras aff. evolvens bed; V.p., Vercherites aff. pulcher
bed. Co: oldest occurrence of the Smithian conodont Furnishius triserratus.
Sp.: Spathian. Reefs and bioaccumulations are indicated by the symbols i-vi
with a key at the top right to the associated figures in the main paper and
the Supplementary Fig. denoted by S.
694
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NATURE GEOSCIENCE DOI: 10.1038/NGEO1264
a
b
c
20 mm
10 mm
2 mm
d
e
f
5 mm
2 mm
5 mm
g
h
Top
10 mm
20 mm
i
j
k
10 mm
Figure 3 | Most characteristic features of sponge bioaccumulations or reefs i-ii and iv–vi. a, Abundant sponges encrusting bivalves. b,c,h, Coalesced
spheroid sponges identified as lyssacine hexactinellids. d–g, Cavities, chambers or in situ spiculitic networks of various incrusting, planar and branched
sponges. i–k, Sponges encrusting bivalves co-occurring with lenticular to irregular sponge structures with centimetre-thick walls. The key to the levels is
given in Fig. 2. Level iii is illustrated in Supplementary Fig. S7.
openings and early cements (Supplementary Figs S13, S17–S18),
closely resembling hypercalcified sponge structures21 . Some
sponges clearly showing interconnected, superimposed chambers
can be assigned to sphinctozoan demosponges (Supplementary Fig.
S15). Isolated or clustered spheroid sponges similar to the PR also
occur in this part of the section. However, one spheroid specimen
differs by its internal thick labyrinthine structure (Supplementary
Fig. S14) and might be assigned to Calcarea. Therefore, at least two
different classes of sponges (Demospongiae and Hexactinellida) are
identified within the same reef exhibiting different morphologies,
thus supporting a multi-species sponge community. Associated
organisms include various foraminifers, common gastropods,
bivalves, serpulids, ammonoids, abundant ostracods, brachiopods,
echinoderms (crinoids and rare urchin spines) and conodonts
(Fig. 2iv–v; Supplementary Figs S8–S22). Combined interstitial
microbial structures are composed of flat to slightly undulating
dark laminae (up to 1 cm thick) with peloids, bounding
fenestral-dominant and oncoid–ooid grainstones. Microbialites
are frequently reworked under tidal wave influence in clast and
centimetre-ooid/oncoid-rich levels (Supplementary Fig. S11).
Changes in microbialite morphology, weak organism reworking,
complete large sponges and a decrease in ooid–oncoid grainstones
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NATURE GEOSCIENCE DOI: 10.1038/NGEO1264
indicate variations from high energy inner ramp to moderate energy
mid ramp domains, enhancing the settlement and development of
sponges tens of centimetres thick (Supplementary Fig. S30).
In the MM section, the upper sponge-rich layers are latest
Smithian and early Spathian in age (top of and above the
‘Glyptophiceras-Xenoceltites beds’; Figs 2vi, 3i–k; Supplementary
Figs S23–S26). They are similar to the lower Smithian PR reef,
showing a lenticular and sporadic distribution over a total thickness
of ∼15 m. These buildups contain centimetre-scale globular
sponges in life-position, encrusting bivalve shells embedded in
mud deposited in low to moderate energy environments. Locally,
sponges are accompanied by abundant gastropods, brachiopods
and moderately common serpulids. Overlying layers contain tens
of centimetres thick rolled up, cup-like and branching sponges
organized in metre-thick buildups exhibiting flat and dome shapes
(Fig. 3j,k; Supplementary Fig. S23). Internal sponge structures are
usually poorly preserved and microsparitized.
Furthermore, new Spathian sponge bioaccumulations and reefs
are reported from the Hurricane Cliffs (HC), Beaver Dam (BD) and
Humboldt Range (HR) sections (Fig. 1; Supplementary Figs S27–
S28). Based on ammonoids, they are early and middle Spathian
in age (HC, BD: Tirolites sp. beds; HR: Prohungarites gustadti
beds). Similar to the early Smithian of the PR, sponges (probably
lyssacine hexactinellids) are also preserved as small and densely
coalesced spheres up to ∼2 cm in diameter, showing a lenticular
distribution. We also resampled different sponge accumulations
from the Confusion Range (CR; Supplementary Fig. S29). Based
on ammonoids, they begin in the early Spathian (Columbites beds)
and contain abundant hexactinellid Cypellospongia fimbriartis13,14
associated with diverse and abundant organisms, including coiled
and orthoconic nautiloids, ammonoids, bivalves and crinoids.
These highly size-variable sponges (few mm up to >30 cm) exhibit
goblet-like to platter-like morphologies.
These occurrences of in situ sponge, sponge–bivalve and sponge–
microbe–bivalve–serpulid consortia associated with diversified
benthic and nekto-pelagic faunas provide new insights into the
Early Triassic metazoan ‘reef gap’. Indeed, the oldest metazoan
reefs illustrated here occur ∼1.5 Myr after the PT boundary,
thus drastically shortening the duration of the gap. The tacitly
acknowledged exclusive contribution of microbes as main reef
builders during the Early Triassic is challenged by these metazoan
bioaccumulations and reefs covering large areas within inner/outer
ramp settings. Differing from previously described latest Early
Triassic bivalve bioherms15 , these transient reefs and benthic
communities are ecologically more complex, showing diverse built
structures and organism interactions as well as tightly associated
growths of their components. Although the pre-extinction diversity
of sponges is not reached, different new taxa and morphologies
pertaining to various classes are here reported for the Early Triassic,
where a single one was previously documented13,14 .
These new findings profoundly alter the timing of the microbedominated benthic communities as well as reef reorganization
models after the PT mass extinction10,22,23 . It is often hypothesized
that the large Early Triassic carbon cycle perturbations are linked
with deleterious global oceanic conditions leading to a delayed
biotic recovery, at least up to the Spathian, when the amplitude
and the number of fluctuations decreased2,3 . However, the reefs
described here occur significantly earlier (Fig. 1b), indicating that
temporary favourable conditions (absence of anoxic, euxinic or
acidic waters) for a broad array of physiologically diverse organisms
had already returned, at least regionally. Hence, the Early Triassic
metazoan ‘reef gap’ may be better described as a reef low from
which a selective preservation bias and insufficient sampling efforts
still need to be factored out. The wide distribution of metazoan
reefs within eastern Panthalassic equatorial palaeolatitudes also
brings a different perspective to the large-scale palaeobiogeographic
696
recovery patterns of the benthos with respect to previous claims of
an earlier recovery within the mid/high palaeolatitudes24 .
Heterozoans dominate these new benthic communities, among
which filter-feeding and usually stress-tolerant sponges, together
with serpulids are the main metazoan builders. Such diversified
communities probably benefited from varied and abundant food
sources and adequate nutrient input from continental weathering
and/or regional oceanic currents and sea-level rise25 . During the
early Smithian, nutrient fluxes and productivity were effective
enough to sustain the development of these bioaccumulations and
reefs. This is in agreement with a previous hypothesis favouring
a rapidly restored, diversified primary productivity after the PT
crisis8 . Ultimately, once re-established, this community, including
microbial deposits, was directly affected by water depth and
current/wave energy (Supplementary Fig. S30).
Sponge–microbe reefs are not exceptional in the geological
record20,25 . However, some of these new Early Triassic sponges
are morphologically different from those of classical Late Permian
reefs but closer to other Mesozoic forms. Therefore, they do not
suggest a local survival in climatic or depth refuges but rather the
formation of a new reef ecology with different actors and roles.
Similar associations are also known in the immediate aftermath of
other mass extinctions26,27 , showing that only a short time interval
is required to rebuild new reefal communities, even if the main
builders differ from pre-crisis assemblages.
The absence of corals, or their failure to calcify28 , remains remarkable for the Early Triassic11 and contrasts with their flourishing
in later Triassic times. The absence could be due to the impossibility
for these stenotypic reef builders to cope with intermittent deleterious conditions. Furthermore, high temperatures could have been a
potential cause for the lack of heavily calcified organisms, as they
physiologically influence calcification11 . However, temperatures
probably fluctuated strongly during the Early Triassic2 . Lowered
pH, low O2 and high H2 S concentrations triggered by the Siberian
Traps2,29 may all have contributed to the temporary absence of heavily calcified organisms. However, the intense production of CaCO3
tests among Smithian and Spathian heterozoan communities from
the western USA, as well as abundant microbialites and micrite mud
support a high calcite saturation6 .
Ultimately, the observed proliferation of sponges predating the
supposed main recovery phase of the siliceous zooplankton30 raises
the question of the duration and intensity of the Early Triassic ‘chert
gap’. Clearly, our results also call for an in-depth reappraisal of the
biotic and abiotic limiting factors for silica biomineralization in the
Early Triassic Ocean.
Methods summary
The two main sections studied are located in the PR and the MM of Utah (Fig. 1;
Supplementary Fig. S1). We also report new early and middle Spathian metazoan
buildups formed by sponges from the Hurricane Cliffs (HC; Utah), Beaver
Dam Mountains (BD; Utah) and Humboldt Range (HR; Nevada), as well as
various bioaccumulations of sponges from the early Spathian of the Confusion
Range (CR; Utah). ∼300 samples were collected bed-by-bed from these sections.
Variably oriented polished slabs and thin sections were prepared from each sample
and we chose the best preserved metazoan builders for cathodoluminescence
analyses. Thin sections were observed by means of natural and polarized light
microscopy using a Leica M205C binocular microscope coupled with a Leica
DFC295 digital camera.
Received 11 May 2011; accepted 15 August 2011; published online
18 September 2011
References
1. Erwin, D. H. Extinction. How life on Earth Nearly Ended 250 Million Years Ago
(Princeton Univ. Press, 2006).
2. Galfetti, T. et al. Timing of the Early Triassic carbon cycle perturbations inferred
from new U–Pb ages and ammonoid biochronozones. Earth Planet. Sci. Let.
258, 593–604 (2007).
3. Payne, J. L. et al. Large perturbations of the carbon cycle during recovery from
the end-Permian extinction. Science 305, 506–509 (2004).
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© 2011 Macmillan Publishers Limited. All rights reserved.
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NATURE GEOSCIENCE DOI: 10.1038/NGEO1264
4. Baud, A., Richoz, S. & Pruss, S. The Lower Triassic anachronistic carbonate
facies in space and time. Global Planet. Change 55, 81–89 (2007).
5. Pruss, S. B., Bottjer, D. J., Corsetti, F. A. & Baud, A. A global marine
sedimentary response to the end-Permian mass extinction: Examples
from southern Turkey and the western United States. Earth Sci. Rev. 78,
193–206 (2006).
6. Woods, A. D. Anatomy of an anachronistic carbonate platform: Lower
Triassic carbonates of the southwestern United States. Aust. J. Earth Sci. 56,
825–839 (2009).
7. Woods, A. D. & Baud, A. Anachronistic facies from a drowned Lower Triassic
carbonate platform: Lower member of the Alwa Formation (Baïd Exotic),
Oman Mountains. Sediment. Geol. 209, 1–14 (2008).
8. Brayard, A. et al. Good genes and good luck: Ammonoid diversity and the
end-Permian mass extinction. Science 325, 1118–1121 (2009).
9. Orchard, M. J. Conodont diversity and evolution through the latest Permian
and Early Triassic upheavals. Palaeogeogr. Palaeoclimatol. Palaeoecol. 252,
93–117 (2007).
10. Weidlich, O., Kiessling, W. & Flügel, E. Permian–Triassic boundary interval
as a model for forcing marine ecosystem collapse by long-term atmospheric
oxygen drop. Geology 31, 961–964 (2003).
11. Payne, J. L., Lehrmann, D. J., Christensen, S., Wei, J. & Knoll, A. Environmental
and biological controls on the initiation and growth of a Middle Triassic
(Anisian) reef complex on the Great Bank of Guizhou, Guizhou Province,
China. Palaios 21, 325–343 (2006).
12. Flügel, E. in Phanerozoic Reef Patterns Vol. 72 (eds Kiessling,
W., Flügel, E. & Golonka, J.) 391–463 (SEPM Special
26 Publication Series, Society for Sedimentary Geology, 2002).
13. Pisera, A., Rigby, J. K. & Bylund, K. G. Lower Triassic hexactinellid sponges
from the Confusion Range, western Utah. BYU Geol. Stud. 41, 139–148 (1996).
14. Rigby, J. K. & Gosney, T. C. First reported Triassic lyssakid sponges from North
America. J. Paleontol. 57, 787–796 (1983).
15. Pruss, S. B., Payne, J. L. & Bottjer, D. J. Planucopsis bioherms: The first
metazoan buildups following the end-Permian mass extinction. Palaios 22,
17–23 (2007).
16. Griffin, J. M., Marenco, P. J., Fraiser, M. L. & Clapham, M. E. 2010 GSA Annual
Meeting Paper no. 21–16 (Denver, 2010).
17. Szulc, J. in The Global Triassic Vol. 41 (eds Lucas, S. G. & Spielmann, J. A.)
(New Mexico Museum of Natural History, 2007).
18. Baud, A., Brandner, R. & Donofrio, D. A. The Sefid Kuh Limestone—A late
Lower Triassic carbonate ramp (Aghdarband, NE-Iran). Abh. Geol. B. –A. 38,
111–123 (1991).
19. Baud, A. et al. Lower Triassic bryozoan beds from Ellesmere Island, High
Arctic, Canada. Polar Res. 27, 428–440 (2008).
20. Riding, R. Microbial carbonate abundance compared with fluctuations in
metazoan diversity over geological time. Sediment. Geol. 185, 229–238 (2006).
21. Senowbari-Daryan, B., Caruthers, A. H. & Stanley, G. D. Jr The First Upper
Triassic Silicified Hypercalcified Sponges from the Alexander Terrane, Gravina
Island and Keku Strait, Southeast Alaska. J. Paleontol. 82, 344–350 (2008).
22. Pruss, S. B. & Bottjer, D. J. The reorganization of reef communities following
the end-Permian mass extinction. C. R. Palevol 4, 553–568 (2005).
23. Schubert, J. K. & Bottjer, D. J. Early Triassic stromatolites as post-mass
extinction disaster forms. Geology 20, 883–886 (1992).
24. Twitchett, R. J. & Barras, C. J. The Application of Ichnology to
Palaeoenvironmental and Stratigraphic Analysis 397–418 (Geological
Society Special Publication, 2004).
25. Brunton, F. R. & Dixon, O. A. Siliceous sponge-microbe biotic associations
and their recurrence through the Phanerozoic as reef mound constructors.
Palaios 9, 370–387 (1994).
26. Wood, R. Palaeoecology of a post-extinction reef: Famennian (Late
Devonian) of the Canning Basin, North-western Australia. Palaeontology 47,
415–445 (2004).
27. Delecat, S. & Reitner, J. Sponge communities from the Lower Liassic of Adnet
(Northern Calcareous Alps, Austria). Facies 51, 385–404 (2005).
28. Stanley, G. D. Jr The evolution of modern corals and their early history.
Earth Sci. Rev. 60, 195–225 (2003).
29. Knoll, A. H., Bambach, R. K., Payne, J. L., Pruss, S. & Fischer, W. W.
Paleophysiology and end-Permian mass extinction. Earth Planet. Sci. Lett. 256,
295–313 (2007).
30. O’Dogherty, L., Carter, E. S., Š Goričan, Š. & Dumitrica, P. Triassic radiolarian
biostratigraphy. Geol. Soc. Lond. Spec. Publ. 334, 163–200 (2010).
NATURE GEOSCIENCE | VOL 4 | OCTOBER 2011 | www.nature.com/naturegeoscience
697
Acknowledgements
This article is a contribution to the teams FED and SEDS of the UMR CNRS 5561
(A.B., E.V.), and teams VP and BFFD of the UMR CNRS 5276 (N.O., G.E.). This
work was funded by the Région Bourgogne, the FRB, the INSU Interrvie (A.B.,
G.E., N.O., E.V.), and supported by the Swiss NSF project 200020-113554 (H.B.).
R. Bourillot, M. Hautmann, P. A. Hochuli, J. Vacelet, and D. Vachard are thanked
for discussions. G. D. Stanley is also thanked for his taxonomic advice regarding
organism determinations and for his contribution in improving an earlier version of
the manuscript. The authors appreciate access to lands managed by the BLM of the US
Department of Interior and the US Forest Service (Fishlake National Forest) of the US
Department of Agriculture.
Author contributions
Fieldwork was carried out by all authors. Thin section studies were performed by E.V.,
A.B. and N.O. Ammonoid determinations: A.B. and H.B. Conodont determinations:
N.G. Manuscript was written by A.B., E.V., N.O, G.E., H.B. with comments on
contents from all authors.
Additional information
The authors declare no competing financial interests. Supplementary information
accompanies this paper on www.nature.com/naturegeoscience. Reprints and permissions
information is available online at http://www.nature.com/reprints. Correspondence and
requests for materials should be addressed to A.B.
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