Partial collapse of the marine carbon pump after the Cretaceous-Paleogene boundary

The impact of an asteroid at the end of the Cretaceous caused mass extinctions in the oceans. A rapid collapse in surface to deepocean carbon isotope gradients suggests that transfer of organic matter to the deep sea via the biological pump was severely perturbed. However, this view has been challenged by the survival of deep-sea benthic organisms dependent on surface-derived food and uncertainties regarding isotopic fractionation in planktic foraminifera used as tracers. Here we present new stable carbon (d13C) and oxygen (d18O) isotope data measured on carefully selected planktic and benthic foraminifera from an orbitally dated deep-sea sequence in the southeast Atlantic. Our approach uniquely combines d18O evidence for habitat depth of foraminiferal tracer species with species-specific d13C eco-adjustments, and compares isotopic patterns with corresponding benthic assemblage data. Our results show that changes in ocean circulation and foraminiferal vital effects contribute to but cannot explain all of the observed collapse in surface to deep-ocean foraminiferal d13C gradient. We conclude that the biological pump was weakened as a consequence of marine extinctions, but less severely and for a shorter duration (maximum of 1.77 m.y.) than has previously been suggested. INTRODUCTION The Cretaceous-Paleogene (K-Pg, 66.02 Ma) boundary is defined by a major mass extinction of terrestrial and marine life (Schulte et al., 2010). One indication of the impact on marine life is the reduction, or reversal in some locations, of vertical marine carbon isotope gradients (Dd13C) between planktic and benthic species d13C, for as long as 3 m.y. (D’Hondt et al., 1998). This has been interpreted as a global reduction in the export of organic matter sinking to deep water in the post-extinction ocean, i.e., weakening of the marine biological carbon pump (Zachos et al., 1989; D’Hondt et al., 1998; Coxall et al., 2006; Esmeray-Senlet et al., 2015). However, the lack of significant extinction of benthic foraminifera that depend on delivery of organic matter to the deep sea, and only relatively brief periods of change in their community structure (Alegret and Thomas, 2007, 2009; Thomas, 2007), has led some to challenge the idea of a largescale prolonged (~3 m.y.) period of reduced carbon export (Culver, 2003; Alegret and Thomas, 2009). Analyzing isotopic patterns across this extinction event using depth-stratified foraminifera has special challenges: (1) the planktic foraminifera used as dissolved inorganic carbon (DIC) tracers are mostly lost to extinction (>90% taxonomic loss of Smit, 1982), such that no continuous single-species planktic d13C record crossing the K-Pg boundary has been generated; (2) the new species that evolved in the aftermath are typically small and have strong d13C vital effects resulting in test calcite that deviates from the DIC d13C (Alegret and Thomas, 2009); and (3) there may have been changes in ocean circulation patterns across the K-Pg boundary (Alegret and Thomas, 2009; Hull and Norris, 2011; MacLeod et al., 2011), which could have affected the foraminiferal d13C signal. To overcome these issues we have generated an open ocean record with robust dating, based on a firm understanding of paleoecology of the rapidly evolving post-extinction planktic taxa. The subsequent multispecies isotopic record improves estimates of vertical d13C changes and provide more robust constraints on the magnitude and duration of the K-Pg ocean carbon system perturbation. A comparison of our data with benthic assemblage records for the first time reveals commonalities between proxy observations that help harmonize perspectives on the pelagic ecosystem response. MATERIALS AND METHODS The K-Pg boundary event is captured in Ocean Drilling Program Site 1262 (Walvis Ridge; 27°11.15′S, 1°34.62′E; Fig. DR1 in the GSA Data Repository1). The K-Pg boundary occurs at ~216.6 m composite depth, calibrated to 66.02 Ma on an astronomically tuned time scale (Dinarès-Turell et al., 2014). We measured d13C and d18O on 10 species of planktic and 1 benthic foraminifera using a Thermo Finnigan MAT252 mass spectrometer equipped with an automated KIEL III carbonate preparation unit at Cardiff University, UK. Stable isotope results were calibrated to the Vienna Peedee belemnite (VPDB) scale by international standard NBS19 and analytical precision was better than ±0.05‰ for d18O and ±0.03‰ for d13C. The selection of species was guided by previous work on early Paleocene planktic foraminifera isotopic depth ecologies (Birch et al., 2012) (Fig. 1): thermocline dwellers—Subbotina trivalis to S. triloculinoides; mixed-layer dwellers—Praemurica taurica to Pr. Inconstans; and surface symbiotic—Morozovella praeangulata to M. angulata for downhole isotopic comparison. To establish a pre-extinction baseline of water column Dd13C for the Cretaceous, Globotruncana falsostuarti and Racemiguembelina fructicosa were chosen as mixed-layer dwellers and surface symbiotic, respectively (Houston and Huber, 1998). The benthic species Nuttallides truempyi was picked to record d13C of bottom water DIC because the species is considered to be in isotopic equilibrium with bottom waters (Shackleton et al., 1984). Guembelitria cretacea and Hedbergella holmdelensis were picked as the only mixed-layer dwelling species to range above the K-Pg boundary. Taxonomy follows Olsson et al. (1999) for the Paleocene and Bolli et al. (1985) for the Cretaceous. Planktic Foraminifera d13C Adjustment Factors Special challenges to reconstructing K-Pg upper ocean d13C arise due to the initial dominance of small (<150 mm) post-extinction opportunists 1 GSA Data Repository item 2016088, location figure, further details of d13C adjustment values with figure, and raw isotope data, is available online at www .geosociety.org/pubs/ft2016.htm, or on request from [email protected] or Documents Secretary, GSA, P.O. Box 9140, Boulder, CO 80301, USA. *Current address: RPS Energy, Goldvale House, 27-41 Church Street W, Woking, GU21 6DH, UK. GEOLOGY, April 2016; v. 44; no. 4; p. 287–290 | Data Repository item 2016088 | doi:10.1130/G37581.1 | Published online 7 March 2016 © 2016 The Authors. Gold Open Access: This paper is published under the terms of the CC-BY license. 288 www.gsapubs.org | Volume 44 | Number 4 | GEOLOGY and subsequent re-evolution of photosymbiotic foraminifera (Fig. 1); both ecologies are associated with distinct fractionation effects causing test calcite d13C to be depleted or enriched, respectively, relative to ambient DIC d13C values (D’Hondt and Zachos, 1993; Birch et al., 2012, 2013). Small test size has been linked with a relatively larger proportion of respired (metabolic) 12C being incorporated into the test calcite, resulting in offsets from inferred DIC d13C of 0.3‰–2‰. Conversely, high d13C (as much as 1.5‰ greater than other inferred surface taxa) and positive d13Csize signatures typify photosymbiotic species, including Praemurica and Morozovella, which acquired this ecology at ca. 63.5 Ma (Fig. 2; Birch et al., 2012). The net effect of these diverging vital effects would be to compress the d13C gradient just after the boundary (as photosymbiotic and large forms were lost) and exaggerate its recovery. To account for these effects we experimented with applying isotopic ecoadjustment factors (see the Data Repository).