Pelagic evolution and environmental recovery after the
Cretaceous-Paleogene mass extinction
Helen K. Coxall 
 Graduate School of Oceanography, University of Rhode Island, Narragansett, Rhode Island 02874, USA
Steven D’Hondt 
James C. Zachos Earth Sciences Department, University of California–Santa Cruz, California 95064, USA
ABSTRACT
The evolutionary recovery of planktic foraminifera from the
Cretaceous-Paleogene mass extinction was closely linked to recovery of the marine carbon system. Both the evolutionary recovery
and the biogeochemical recovery occurred in two stages. The second stage of evolutionary radiation peaked nearly four million
years after the extinction, immediately after the abrupt final recovery of the organic flux to deep waters. The timing of these
events suggests that the final postextinction recovery of planktic
foraminiferal diversity was directly contingent on the final recovery of the marine carbon cycle. This second radiation was defined
by the diversification of tropical photosymbiotic forms that dominated low- and mid-latitude assemblages long into the Eocene. We
hypothesize that this diversification was a result of the reappearance of oligotrophic oceans as the organic flux from the surface
ocean to deep water fully recovered from the mass extinction.
Keywords: Cretaceous-Tertiary boundary, extinction recovery, carbon
system, organic flux, pelagic ecosystem, planktic foraminifera,
evolution.
INTRODUCTION
The marine ecosystem suffered tremendous taxonomic loss during
the Cretaceous-Paleogene mass extinction, with pronounced extinction
among vertebrates, invertebrates, phytoplankton, and zooplankton
(Sheehan et al., 1996). Entire groups of organisms completely disappeared. Marine fossil records from the ensuing Paleocene period exhibit multimillion-year delays in evolutionary recovery (Sepkoski,
1998; Kirchner and Weil, 2000). For example, more than 90% of Maastrichtian planktic foraminifera species disappeared abruptly at the
boundary (e.g., Smit, 1982; D’Hondt et al., 1996; Molina et al., 1998).
Postextinction planktic diversification involved evolution of entirely
new taxa from a few Cretaceous survivors (Olsson et al., 1999). Full
diversification was drawn out over a few million years (Corfield and
Shackleton, 1988; Olsson et al., 1999).
The mass extinction was associated with a catastrophic decline in
the flux of organic matter to the deep ocean (e.g., Hsü et al., 1982;
Zachos et al., 1989). Evidence suggests that the recovery from this
collapse took more than three million years (m.y.) (D’Hondt et al.,
1998; Adams et al., 2004), but little is known about the timing of
evolutionary diversification in relation to carbon cycling and the state
of the recovering pelagic ecosystem. Here we explore links between
the carbon system and the marine ecosystem by comparing Paleocene
planktic foraminiferal evolutionary histories with geochemical records
of Cretaceous-Paleogene environmental change from the Atlantic and
Pacific Oceans.
MATERIALS AND METHODS
Our studies focused on two Cretaceous-Paleogene boundary sections: Deep Sea Drilling Project (DSDP) Site 528 (28831.499S;
02819.449E) and Site 577 (32826.519N; 157843.409E), with paleolatitudes and depths of ;388S and 2500 m, and 8–108N and 2400 m,
respectively (D’Hondt et al., 1998). Stratigraphic control was achieved
through biostratigraphy and magnetostratigraphy (Moore et al., 1984;
Heath et al., 1985). The sequence at Site 528 is composed of Maastrichtian foram-nannofossil chalks overlain by Paleocene nannofossil
marls. Foraminiferal preservation is moderate in the Upper Cretaceous
and moderate to good in the Lower Paleocene. Site 577 sediments are
nannofossil ooze throughout. Upper Cretaceous planktic foraminifera
exhibit severe dissolution and fragmentation, but Paleocene specimens
are well preserved. Carbonate (CaCO3) accumulation decreased across
the Cretaceous-Paleogene boundary by ;85% at Site 528 and ;60%
at Site 577 (D’Hondt, 2006). The smaller decrease at Site 577 is the
result of lower CaCO3 accumulation in the Cretaceous, probably because of deposition at lysoclinal depths (Zachos et al., 1989). The accumulation of CaCO3 in the foraminiferal size fraction (.38 mm) at
Site 528 did not change appreciably at the boundary. In combination
with the greatly improved preservation of Paleocene foraminiferal tests
relative to Maastrichtian tests, the relative stability of mean foraminiferal accumulation indicates that decreased accumulation resulted from
decreased nannofossil accumulation rather than from increased dissolution (D’Hondt, 2006).
Paleocene planktic foraminifera stratigraphic distributions were
recorded using 140 core samples from Site 528 and 126 samples from
Site 577. Species identifications were cross-checked by R.K. Olsson
and I. Premoli-Silva. Evolutionary patterns were derived from range
charts by counting: (1) the number of first occurrences, (2) the number
of last occurrences, and (3) the total number of species present through
5 m intervals for Site 528 and 2.5 m intervals for Site 577. We used
the surface- to deep-water d13C differential as a proxy for the strength
of the carbon pump that delivers organic matter to the seafloor
(D’Hondt et al., 1998). The isotopic data presented in Figures 1 and 2
are from D’Hondt et al. (1998), supplemented with new analyses that
were performed at the University of Santa Cruz, California.
PLANKTIC FORAMINIFERA EVOLUTIONARY RECOVERY
Site 528 records reveal an initial burst of diversification within
300 k.y. of the extinction that contributed 18 new species in 8 new
genera, representing .60% of total Paleocene diversity (Fig. 1).
This occurred at the beginning of the first of two abrupt increases in
planktic-benthic and fine CaCO3-benthic calcite d13C, identified as
‘‘initial d13C recovery’’ (;404 m below seafloor [bsf], base of magnetochron C29n) (Fig. 1A). A second phase of diversification and turnover began almost 3 m.y. after the extinction between 375 m and 395
m depth, adding a further 3 genera and 16 species. This phase lasted
2–3 m.y. and spanned a second, final stage of d13C recovery when
planktic-benthic and fine-fraction CaCO3-benthic d13C gradients returned to pre-extinction values (Fig. 1A–C). Thereafter, extinctions and
originations stabilized until the Paleocene-Eocene boundary, when evolutionary turnover was renewed (Corfield and Shackleton, 1988; Kelly
et al., 2001).
Pacific Ocean Site 577 records show a similar relationship between the timing of the second phase of diversification and d13C
change (Fig. 2A–C). The lower stratigraphic occurrence of Praemurica
uncinata and its descendents, the morozovellids, at this site compared
to Site 528 suggests that either Morozovella began to diversify before
final d13C recovery in the tropics or a section of younger sediment was
displaced down-core. Despite the minor biostratigraphic differences,
q 2006 Geological Society of America. For permission to copy, contact Copyright Permissions, GSA, or [email protected].
Geology; April 2006; v. 34; no. 4; p. 297–300; doi: 10.1130/G21702.1; 2 figures.
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Figure 1. Planktic foraminiferal evolutionary records from Deep Sea Drilling Project (DSDP) Site 528 compared to Cretaceous-Paleogene
(K/Pg) boundary carbon isotopes (d13C). Isotopic analysis was performed on an Optima gas-source mass spectrometer equipped with an
Autocarb common acid bath. A: Differences between surface (planktic foraminifer and fine-fraction CaCO3) and deep-sea (benthic foraminifer 5 Gavelinella sp. 1 N. truempyi) calcite d13C (from D’Hondt et al., 1998, supplemented with 87 new data points). d13C is measured
in ‰ relative to the Peedee belemnite (PDB) standard; mbsf is m below seafloor. Major decrease in surface- to deep-water d13C gradients
occurs at the K/Pg boundary. Dashed gray lines mark (1) initial and (2) final d13C recovery from K/Pg excursion values. B: Foraminiferal
stratigraphic ranges, minimum 1 cm sample spacing across the K/Pg. Majority of Cretaceous species went extinct at the boundary. C:
Evolutionary turnover. Species first and last occurrences (FOs and LOs) were counted from B. Cretaceous diversity data are from D’Hondt
et al. (1996). Genus abbreviations: Ps.—Pseudotextularia, R.—Rugoglobigerina, Gu.—Guembelitria, Pv.—Parvularugoglobigerina, G.—
Globoconusa, Z.—Zeauvigerina, W.—Woodringina, C.—Chiloguembelina, H.—Hedbergella, Gl.—Globanomalina, E.—Eoglobigerina, P.—
Parasubbotina, S.—Subbotina, Pr.—Praemurica, I.—Igorina, M.—Morozovella, A.—Acarinina.
the pattern and timing of d13C recovery relative to the magnetic reversal sequence, and the timing of the main morozovellid diversification are consistent at the two sites.
DISCUSSION
The general pattern of planktic evolutionary recovery shown by
our data is one of initial colonization by a few Cretaceous-Paleogene
survivors, followed by two stages of diversification: (1) a rapid initial
phase, which established basic test shapes and generic diversity but
had relatively low species diversity, and (2) a delayed second phase,
which peaked ;4 m.y. after the extinction and contributed further important Paleogene lineages and returned Paleocene diversity to close
to pre-extinction levels. The timing of these evolutionary waves bears
a striking resemblance to the d13C recovery.
The d13C recovery has been shown to represent a multimillionyear staged recovery of surface to deep organic flux following a catastrophic decline at the Cretaceous-Paleogene boundary (D’Hondt et
al., 1998; Adams et al., 2004). This indicates that recovery of planktic
foraminifera from the mass extinction was closely linked to recovery
of marine carbon cycling. Reduced primary production is often invoked
to explain low surface to deep d13C gradients. Although productivity
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may have declined in the immediate aftermath of the extinction (e.g.,
Hsü et al., 1982; Zachos et al., 1989), it is unlikely to have persisted
for millions of years. An alternative hypothesis to explain the d13C
records is a living ocean model (D’Hondt et al., 1998). This assumes
that biological productivity returned rapidly (within years of the extinction), but that organic flux was drastically reduced for millions of
years because of a greatly altered ecosystem (such as a general absence
of larger grazers, e.g., macrozooplankton and fish), which normally acts
to export biomass to the deep sea, and/or a relatively low mean size
of phytoplankton (D’Hondt et al., 1998).
The model explains the two stages of d13C recovery as an initial
gradual recovery in the proportion of biological production that sank
to the deep sea followed by an abrupt final recovery a few million
years later as larger grazers evolved and/or average phytoplankton size
increased. This is consistent with ecological models of biodiversity
recovery after mass extinctions that predict multimillion-year lags in
diversification as consecutive tiers of trophic webs are reconstructed
(e.g., Kirchner and Weil, 2000). Paleontological evidence for this may
be lacking, because pelagic macrofossils are extremely rare (D’Hondt,
2006). The apparent contradiction of this interpretation with benthic
foraminifera records, which show no major extinction at the
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Figure 2. Planktic foraminiferal evolutionary records from Deep Sea Drilling Project (DSDP) Site 577 compared to Cretaceous-Paleogene
(K/Pg) boundary carbon isotopic (d13C) records of D’Hondt et al. (1998). A: Differences between surface (planktic foraminifer and finefraction CaCO3) and deep-sea (benthic foraminifer) d13C. Benthics: Nuttallides spp. between 85 and 104 m below seafloor (mbsf), Aragonia
aragonensis and Nuttallides spp. between 114 and 115 mbsf; despite different inferred paleoecologies (infaunal and epifaunal, respectively),
there was no discernible difference between d13C for paired species analyses, and values are combined uncorrected. Dashed lines 1 and
2 are same as in Figure 1. d13C is measured in ‰ relative to the Peedee belemnite standard. B: Foraminiferal stratigraphic ranges. C:
Evolutionary turnover. Generic abbreviations are as in Figure 1.
Cretaceous-Paleogene boundary (Culver, 2003), has been attributed to
the fact that deep-sea benthic foraminifera by their nature are tolerant
of low food supply and are well suited to survive periods of low productivity (e.g., Thomas, 1990). In any case, we do not argue that organic flux ceased completely but that it was greatly reduced for an
extended period. Transfer of particulate organic carbon to the deep sea
is a complex process, and other factors, such as biomineral ballasting
(e.g., Armstrong et al., 2002), may also have been important to carbon
flux recovery as the mean size of planktic foraminiferal shells (and
calcareous nannoplankton; P. Bown, 2005, personal commun.)
increased.
Planktic Foraminifera Ecological Radiation
The second major wave of diversification shortly followed full
carbon cycle recovery. Evolution was most pronounced in the genus
Morozovella, the dominant group of Paleocene-Eocene surface mixedlayer dwellers, and produced a series of large (200–400 mm) species
with peripheral keels and a pustulose (muricate) wall. The morozovellid radiation was shortly followed by diversification of two additional
muricate genera, Igorina and Acarinina. Muricate species exhibit
strong positive correlations between d13C and test size, which is
thought to result from d13C fractionation by algal symbionts (Spero
GEOLOGY, April 2006
and DeNiro, 1987; Pearson, et al., 1993; Norris, 1996). This symbiosisrelated d13C enrichment in Morozovella spp. exaggerates the d13C gradient (Figs. 1A and 1B). However, d13C increase during the final recovery is not limited to these taxa, and fine-fraction CaCO3 and
asymbiotic planktics (Subbotina spp.) to benthic d13C differentials increase at the same time (Figs. 1A and 2A). Moreover, it seems unlikely
that final d13C recovery in fine-fraction CaCO3 is the result of simultaneous changes in vital effects in all the fossil groups, including nannoplankton (Bralower, 2002). Instead, we interpret the results as representing an ocean-wide shift in the surface- to deep-water d13C
gradient and recovery of the carbon pump to pre-extinction strength.
The symbiotic ecology of the muricate taxa has interesting implications
for understanding the post–Cretaceous-Paleogene boundary
environment.
Symbiotic associations with alga are widespread among modern
planktic foraminifera and allow hosts to attain high-population densities in low-nutrient, central-ocean regions (Hemleben et al., 1989; Caron et al., 1995). Strong size-related d13C trends characteristic of symbiosis occur in M. praeangulata (Kelly et al., 1996) and all subsequent
species of Morozovella (Pearson et al., 1993; D’Hondt et al., 1994;
Norris, 1996). In contrast, species of Praemurica, with the possible
exception of P. uncinata (Norris, 1996), show no such trend and are
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considered asymbiotic. This suggests that the evolutionary transition
from Praemurica to Morozovella involved evolution of a symbiotic
ecology (Norris, 1996). Our results show that M. praeangulata and
muricate symbiosis evolved before final d13C recovery at Sites 528 and
577, but the main evolutionary diversification of Morozovella came
directly after. A concomitant increase in average test size (D’Hondt,
2006) supports this hypothesis, because symbiotic species tend to build
larger tests to maximize symbiont density (Spero and DeNiro, 1987).
A possible interpretation of this is that the pattern and timing of
radiation in Morozovella and other muricate genera represent diversification of oligotrophic specialists as organic flux to the deep ocean
fully recovered, stripping of nutrients from the surface ocean resumed,
and specialization to low food availability became a selective advantage. Although symbiosis appears to have been central to this final
stage of diversification (Koutsoukos, 1996; Norris, 1996), it could not
have been the key innovation that triggered the evolutionary event,
because the signature for this ecology was present in ancestral morozovellid species before the diversification occurred. Rather, the radiation appears to have principally resulted from diversification of symbiotic forms exploiting an expanding ecologic opportunity that in turn
resulted from final recovery of the marine carbon cycle
CONCLUSIONS
This study provides an ecological dimension to the understanding
of the Cretaceous-Paleogene boundary biotic crisis and recovery and
a broader window into the extent and impact of the perturbation in the
pelagic realm. The photic zone ecosystem is the principal driver of the
marine carbon pump, shunting organic carbon through increasingly
complex food chains into aggregates large enough to survive export to
the seafloor. Recovery of the carbon pump, therefore, is contingent on
recovery of integrated ecosystems. Our results suggest that this
ecosystem-driven cycling has the potential to provide a positive feedback once the system attains full complexity (i.e., when a broad spectrum of herbivores and predators involved in the trophic web have
evolved) by triggering diversification of low-food tolerant oligotrophic
specialists. The three million year delay in organic flux and planktic
foraminifer evolutionary recovery attests to the far-reaching effects of
the extinction in the marine realm and implies that the time required
to repair food chains and reestablish an integrated ecosystem is extremely long (millions of years) compared to the immediate physical
effects of the disaster.
ACKNOWLEDGMENTS
This work was supported by a U.S. National Science Foundation grant to
S. D’Hondt. We thank R.K. Olsson and I. Premoli-Silva for discussions and
assistance with Paleocene foraminiferal taxonomy, William Chaisson for assistance with planktic foraminiferal isotope samples, and Miranda Smith for assistance with data handling and drafting. Thanks also are due to Harriet Leong,
Julia Frazier, Steven Bohaty, and Robert Becker for assistance with isotope
analysis.
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Manuscript received 9 March 2005
Revised manuscript received 14 December 2005
Manuscript accepted 16 December 2005
Printed in USA
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