The planktonic foraminiferal response to the Paleocene-Eocene thermal maximum on the Atlantic coastal plain

Marine Micropaleontology 146 (2019) 39–50

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Research paper

The planktonic foraminiferal response to the Paleocene-Eocene thermal maximum on the Atlantic coastal plain Caitlin M. Livseya,

T

⁎,1

, Tali L. Babilab, Marci M. Robinsonc, Timothy J. Bralowera

a

Department of Geosciences, Pennsylvania State University, University Park, PA 16802, USA Department of Earth and Planetary Sciences, University of California, Santa Cruz, CA 95064, United States c Eastern Geology and Paleoclimate Science Center, US Geologic Survey, Reston, VA 20192, United States b

A B S T R A C T

Planktonic foraminiferal assemblages in two cores from Maryland and New Jersey show evidence for significant changes in surface ocean habitats on the continental shelf during the Paleocene-Eocene Thermal Maximum (PETM). At both sites, significant assemblage shifts occur immediately before the onset of the event. These changes include the appearance of abundant triserial/biserial species as well as rare excursion taxa, which are limited to the interval of the carbon isotope excursion at deep-sea sites. The assemblage shifts signal the development of new habitats immediately prior to the onset of the PETM, likely involving warming, surface ocean acidification, increased stratification and oligotrophy. A sharp increase in diversity at the onset of the event is interpreted as a further increase in stratification and warming, as well as increased water depth and more eutrophic conditions. Finally, we observe variant morphologies of several planktonic foraminifera, which may also signal the response of the assemblage to environmental perturbation.

1. Introduction Abrupt warming at the Paleocene-Eocene Thermal Maximum (PETM; 55.8 Ma) led to upheaval of the global carbon cycle (e.g., Kennett and Stott, 1991; Zachos et al., 2001; Bowen et al., 2006; Pagani et al., 2006; McInerney and Wing, 2011) and transformation of both marine and terrestrial ecosystems. On the continents, high-latitude warming opened up land bridges for mammal dispersal (Gingerich, 2003), while paratropical floras temporarily spread to temperate latitudes (Wing et al., 2005). In the oceans, the event was characterized by blooms of the dinoflagellate genus Apectodinium (Crouch et al., 2001; Sluijs et al., 2007), a significant turnover in nannoplankton assemblages (e.g., Bralower, 2002; Gibbs et al., 2006a; Schneider et al., 2013), and the extinction of 35–50% of deep-sea benthic foraminiferal species (e.g., Tjalsma and Lohmann, 1983; Thomas, 1990, 2003). The PETM was associated with the release of a significant volume of carbon into the atmosphere-ocean reservoirs as indicated by a pronounced 4–5‰ decrease in marine and terrestrial carbon isotopic values (e.g., Koch et al., 1992; Dickens et al., 1995). The initial phase of carbon release encompassed 5–20 kyr (e.g., Farley and Eltgroth, 2003; Röhl et al., 2007; Charles et al., 2011; Kirtland Turner et al., 2017), suggesting rates of CO2 emission about 10× lower than today (Cui et al., 2011; Zeebe et al., 2016). Nevertheless, the event provides an opportunity to investigate how biogeochemical systems operate in a warmer and higher CO2 world.

The PETM was the most extreme of several rapid “hyperthermal” events that occurred during the early Paleogene (Thomas and Shackleton, 1996; Thomas et al., 2000; Nicolo et al., 2007; Westerhold et al., 2008; Zachos et al., 2008; Stap et al., 2010). Surface and deepwater temperatures rose between 5 and 9 °C as suggested by planktonic and benthic foraminiferal δ18O and Mg/Ca data, as well as TEX86 values (e.g., Kennett and Stott, 1991; Thomas and Shackleton, 1996; Zachos et al., 2003, 2005; Tripati and Elderfield, 2005; Sluijs et al., 2007; Jones et al., 2013; Aze et al., 2014; Frieling et al., 2014). The combination of warming, increased stratification, fluctuations in carbonate chemistry, deoxygenation and shifting trophic structure caused diversification of planktonic foraminifera (e.g., Barrerra and Huber, 1991; Lu and Keller, 1993; Kelly et al., 1996, 1998, 2012; Kelly, 2002; Petrizzo, 2007; Peters et al., 2013; Babila, 2014; Babila et al., 2016; Penman et al., 2014; Zhou et al., 2014; Fraass et al., 2015), involving the evolution of short-lived morphotypes: Acarinina sibaiyaensis, Acarinina africana, Morozovella allisonensis (Kelly et al., 1996, 1998) and Acarinina multicamerata (Guasti and Speijer, 2008). Appearance of these species in tropical and subtropical deep-sea sections is coincident with the onset of the carbon isotopic excursion (CIE; e.g. Kelly et al., 1996; Pardo et al., 1997; Arenillas et al., 1999; Berggren and Ouda, 2003; Petrizzo, 2007; Bown and Pearson, 2009; Fig. S1). These species exclusively record negative carbon isotopic values, indicating that they were transient and restricted to the CIE core interval in the deep ocean (Kelly et al., 1996, 1998). However, it is currently unclear whether the so-called

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Corresponding author. E-mail address: [email protected] (C.M. Livsey). 1 Present address: Department of Earth and Planetary Sciences, University of California Davis, Davis, CA 95616, USA. https://doi.org/10.1016/j.marmicro.2018.12.001 Received 20 May 2017; Received in revised form 26 November 2018; Accepted 1 December 2018 Available online 05 December 2018 0377-8398/ © 2018 Elsevier B.V. All rights reserved.

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“excursion taxa” evolved during the PETM, or whether they originated before the event in a marginal location and dispersed during it. Acarinina sibaiyaensis and A. africana have been observed just below the PETM in Egypt (El-Naggar, 1966; Speijer et al., 2000), but the significance of this occurrence has not been fully explored. The input of carbon at the onset of the PETM caused significant (up to 2 km) shoaling of the lysocline and calcite compensation depth (CCD; e.g., Zachos et al., 2005; Colosimo et al., 2006; Zeebe et al., 2009), resulting in a highly condensed record of the onset of the event in deepocean sediment cores. Moreover, dissolution on the seafloor has left the early part of the event void of calcareous plankton in many deep-sea sections (e.g., Bralower et al., 2014). By contrast, the PETM is highly expanded in cores from the US Atlantic Coastal Plain, where siliciclastic sediments were deposited at rates up to 20 cm/kyr during the peak CIE (John et al., 2008; Stassen et al., 2012). These cores have the potential for ultra-high resolution, possibly sub-millennial, studies of the PETM. Here we present the first high-resolution records of planktonic foraminiferal assemblages from the onset of the PETM in cores from Maryland and New Jersey on the Mid-Atlantic Coastal Plain. Our data illustrate dramatic changes in shelf habitats immediately before and during the onset of the event. We document the occurrence of the excursion taxa in detail, and describe previously unobserved morphologies that allow us to elucidate how the surface ocean habitats evolved during the early stages of the PETM.

washed > 63-μm samples were studied from a 2-m interval across the base of the PETM at BR with a sample spacing of 90 to 120 cm. Given the low abundances of foraminifera in the cores, a small sieve size was necessary to maximize our sample sizes. Micropaleontological samples from both cores were split and a fixed aliquot was spread over a gridded picking tray. A total of 200 planktonic foraminiferal specimens in each sample were identified at the species level using the taxonomy described in Olsson et al. (1998) and Pearson et al. (2006); Table S1). Foraminifera are very rare in samples at the base of the PETM in both sections. One full tray was counted in those samples. Relative abundance counts at the species level were used to calculate species richness. Species were subsequently combined into morphological groups (using descriptions by Pearson et al., 2006; Fig. 3) that occupy particular habitats in terms of depth and nutrient levels (e.g., Douglas and Savin, 1978; Berggren and Norris, 1997; Quillevere and Norris, 2003). Interpretation of assemblages at the morphological group level allows results to be compared between studies with variable taxonomic concepts. Moreover, since understanding of ecological preferences does not extend below species groups, such classification does not result in loss of ecological information. The count data were compared to assemblage data from ODP Site 1209 on Shatsky Rise, Central Pacific Ocean (32°30.1081′N, 158°15.5623′E, water depth 2387 m; Petrizzo, 2007). Each of the binned datasets was converted to percent abundances, and species groups with < 2% of the total counts were omitted to remove outliers from the analysis. The datasets were analyzed statistically in R Studio (www.r-project.org) using the “vegan” package. The species group data were divided by total counts, allowing uniform comparison of samples with varying total individuals. The three datasets were standardized by performing a log transform, which compresses the high values and spreads the low values while maintaining the original order of magnitude (McCune and Grace, 2002). A Sorensen (Bray-Curtis) distance matrix was calculated on the standardized data, and then a nonmetric multidimensional scaling (NMS) ordination was performed. NMS is an ordination technique that makes no prior assumptions about the relationship between samples, and is therefore the preferred method for ecological datasets (McCune and Grace, 2002). NMS takes the calculated distance matrix and iteratively arranges the samples and species on a specified number of axes, until the configuration with the least amount of “stress” (goodness-of-fit metric) is converged upon. The resulting plots illustrate samples and species in NMS space based on their similarities (in species composition and sample abundance respectively), which reveals underlying patterns and relationships in the data. A FEI Quanta 200 Environmental scanning electron microscope (SEM) was used to assess and document the morphological variation and shell preservation in individual foraminifera. Representative specimens were picked, mounted on SEM stubs backed with carbon tape, and imaged under low vacuum using a backscatter electron detector.

2. Materials and methods Samples were taken from cores at Bass River, New Jersey (BR; 39°36′42”N, 74°26′12”W, 140–150 m paleo depth; Stassen et al., 2015), drilled by the Ocean Drilling Program (ODP) during Leg 174× (Miller et al., 1998) and Cambridge-Dorchester, Maryland (CD; 38°32′4”N, 76°1′44”W) drilled by the US Geological Survey (Fig. 1). We estimate the paleo depth of CD to be ~130–140 m based on the proximity of this site to South Dover Bridge (~130–140 m paleo depth) and the similarity between the foraminiferal assemblages in the two cores (Robinson and Spivey, in review). The two Atlantic Coastal Plain cores contain an expanded upper Paleocene to lower Eocene sequence, including a well-defined CIE (BR: John et al., 2008, Fig. 2; CD: Lyons et al., submitted). The upper Paleocene Vincentown Formation at BR and the correlative Aquia Formation at CD consist of glauconitic, quartzose silty sands that were deposited on a sediment-starved, siliciclastic shelf (Olsson and Wise, 1987; Browning et al., 2008). The early Eocene Marlboro Clay at both BR and CD consists of silty clays, indicating a shift to a river-dominated shelf with high sediment input (e.g., Gibson et al., 1993; Kopp et al., 2009). The CD core was sampled approximately every 10 cm and up to 2 cm near the CIE onset for bulk sediment geochemical analysis. Total inorganic carbon content (TIC) measurements were carried out on a UIC Coulometer at the University of Santa Cruz (UCSC) and converted into percent calcium carbonate (CaCO3). Stable isotope analyses were carried out on a Finnigan MAT253 mass spectrometer interfaced with a Kiel Device at UCSC. In this system, the sample is reacted under vacuum with phosphoric acid at 75 °C with the resulting gas distilled in a single step. Stable isotope values are reported in per mil (‰) relative to Vienna Pee Dee belemnite standard (VPDB). Analytical precision (1 s) is based on repeat analyses of an in-house standard (Carrara marble), calibrated to the international standards NBS 18 and NBS 19, and averages ± 0.05‰ for δ13C and ± 0.08‰ for δ18O. Insufficient CaCO3 content between 224.28 and 222.23 m at CD prevented collection of stable isotope analysis. Only the δ13C data are interpreted here. A total of 40 micropaleontological samples were taken from the CD core at approximately 1.2 cm to 5 cm spacing over a 1.5-m interval encompassing the Paleocene-Eocene boundary. Samples were treated with a sodium hexametaphosphate solution for two hours, washed with buffered water through a 63-μm sieve, filtered through grade P5 filter paper, and oven dried at 40 °C overnight. Fifteen previously

3. Results 3.1. Planktonic assemblages 3.1.1. Upper Paleocene Planktonic foraminiferal species counts at Bass River (BR) and CamDor (CD) reveal significant shifts in assemblage structure, species richness, and total abundance across the Paleocene-Eocene boundary (Figs. 4, 5). The > 63 μm fractions of the upper Paleocene Vincentown (in BR) and Aquia Formations (in CD) are composed of abundant mineral grains (e.g., mica, quartz, pyrite and glauconite) with sparse, fragile and highly fragmented (average of ~65%) foraminifera (Table S2). It must be noted that the interpretation of the 63 μm sediment fraction diverges from the conventional use of the > 150 μm fraction for foraminiferal studies, and may have allowed higher resolution patterns to be exposed. Planktonic foraminifera in upper Paleocene samples are small (average size ~150 μm), dominated by the spinose 40

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Fig. 1. Map showing the Atlantic Coastal Plain with the locations of the Bass River (BR; New Jersey), and USGS Cambridge-Dorchester (CD; Maryland) cores.

prep; Fig. 2) respectively. Planktonic foraminiferal preservation in the Marlboro Clay above the dissolution interval is moderate to excellent, with delicate tests and fragmentation of ~30% in both sections (Table S2). There is a notable increase in the size of individuals. The average species richness in each sample increases from 21 to 26 in BR, and almost twofold from 17 to 33 in CD (Table S2). The muricate and keeled genera increase in relative abundance, while the smooth, biserial/triserial (mostly Chiloguembelina spp.) and spinose cancellate genera decrease (Figs. 4, 5). At BR, a number of spinose cancellate, muricate and keeled individuals show textural irregularities and possible chamber malformation (Fig. 6).

cancellate, triserial/biserial and muricate groups (Figs. 4, 5), and low in diversity (species richness averages 21 and 17 at BR and CD, respectively; Table S2). A spike of the triserial/biserial planktonic foraminifera (i.e., Chiloguembelina spp.) occurs in the three samples from the 1 m interval directly below the onset of the CIE at CD (Fig. 5). These taxa are also abundant in the five samples from the 1 m interval prior to the CIE in BR (Fig. 4). Fragile and rare specimens of Acarinina sibaiyaensis are found in three samples in the 24 cm interval below the onset of the CIE in both cores (Figs. 4, 5).

3.1.2. Lower Eocene The transition from the Vincentown (in BR) and Aquia Formations (in CD) to the lower Eocene Marlboro Clay is characterized by an abrupt shift in sediment composition, a sharp decrease in CaCO3 to near 0%, and the onset of the CIE (Figs. 4, 5). The interval with near 0% carbonate (here termed the dissolution interval) has extremely rare foraminifera (mostly benthic agglutinated forms), and extends for 1.8 m in CD (from 224.1 m to 222.3 m) and 0.3 m in BR (357.3 m to 357 m). The dramatic decrease in CaCO3 is coeval with the lower part of the CIE in bulk CaCO3 δ13C values in BR (John et al., 2008) and CD (Babila, in

3.2. “Excursion” taxa The first occurrence of the “excursion” species Acarinina sibaiyaensis (Fig. 7) is 24 cm below the onset of the CIE at both CD and BR. In the Aquia Formation (at CD) and the Vincentown Formation (at BR), A. sibaiyaensis is thin, fragile, and rare (Fig. 8). This species is more abundant in the samples above the dissolution zones in both sections (Figs. 4, 5; Table S3), with a larger test size and improved preservation. 41

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Bass River

Ccarb 0

357 358

223

CIE “core”

Depth (m)

Phase I

NP 10a

353 354 355 356

2

222

C CIE “core”

Depth (m)

352

0

Ph. II

-2 347 348 349 350

Acarinina sibaiyaensis ranges considerably in size and shape but is characterized by distinctly lenticular or petalloid chambers, and a dorsally flattened test (Fig. 7). This species is more abundant and shows better preservation in the samples above the dissolution zone in both sections (Figs. 4, 5,8), where it occurs with Acarinina multicamerata (Guasti and Speijer, 2008). Acarinina multicamerata has not been found outside the CIE core and is combined here with A. sibaiyaensis counts within the CIE core as it simplifies interpretation of results. Acarinina africana is rare at CD above the dissolution zone, and was not found at BR. Acarinina africana resembles A. sibaiyaensis and A. multicamerata, though it has a significantly flatter test and an acutely pinched peripheral margin (El-Naggar, 1966). The “excursion” species Morozovella allisonensis has not been observed in either section.

CD

Ccarb

224

3.3. Multivariate analysis

365 366 367

225

The Nonmetric Multidimensional Scaling (NMS) ordination reveals distinct gradients in time and environment as determined by sample and species groups (Fig. 9). Samples cluster by site, with ODP Site 1209 samples showing positive NMDS1 values, and the BR and CD samples showing negative values. At each site, the samples cluster into two recognizable groups, with samples prior to the CIE having lower NMDS2 values, and those within the CIE having higher NMDS2 values. The spinose cancellate, muricate, and smooth species groups plot between ODP Site 1209 and the shelf sites on NMDS1, but more closely to the CIE samples on NMDS2. The biserial/triserial and keeled groups share similar scores on NMDS2, plotting near to the samples at the CIE onset; the keeled group lies within the ODP Site 1209 sample cluster, whereas the biserial/triserial group plots with the CD and BR samples. The non-spinose cancellate group shows negative scores on both axes, plotting close to the Paleocene sample clusters at BR and CD. The excursion taxa, A. sibaiyaensis and A. africana lie below all samples and species groups on NMDS2. On NMDS1, A. sibaiyaensis plots between the

Pre-CIE

363 364

NP 9a

362

Pre-CIE

359 360

226

Fig. 2. Stratigraphic column for the Paleocene-Eocene Thermal Maximum at Bass River and Cambridge-Dorchester. BR plot includes phases of the event, as defined by Stassen et al. (2012) using chronology of Röhl et al. (2007) and the lowest occurrence of Tribrachiatus bramlettei; nannoplankton biostratigraphy from Gibbs et al. (2006a) and Aubry et al. (2000); and δ13C bulk carbonate from John et al. (2008). The CD plot includes δ13C bulk carbonate (this study) and phases of the event defined using δ13C values and preservational changes. The shaded boxes correspond to the intervals used in this study.

Fig. 3. Scanning electron micrographs of representative individuals of the six species groups used in this study: spinose cancellate (BR 357.8 m), muricate (CD 221.6 m), smooth (BR 356.8 m), keeled (CD 221.6 m), triserial/biserial (BR 357.8 m), and non-spinose cancellate (BR 356.9 m). 42

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Fig. 4. Planktonic foraminiferal assemblages from Bass River. δ13C values of bulk carbonate from John et al. (2008). The occurrence of Acarinina sibaiyaensis is shown on the right. The dissolution zone is shown by the shaded gray boxes.

Fig. 5. Planktonic foraminiferal assemblages from CamDor. δ13C values of bulk carbonate. The occurrence of Acarinina sibaiyaensis and A. africana are shown on the right. The dissolution zone is shown by the shaded gray boxes. 43

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Fig. 6. Scanning electron micrographs of representative planktonic foraminifera with possibly abnormal morphologies from Bass River samples 356.71–357.04 m. The “malformations” are divided into diminutive/kummerform final chambers, final chamber “oddities”, and overall variant shapes. Arrows point to the most obvious “malformation”. (1) Acarinina sp. with diminutive and abnormally placed final chamber (356.8 m). (2) Acarinina sp. with diminutive and abnormally placed final chamber (356.9 m). (3) Subbotina sp. with irregularly shaped and abnormal number and placement of chambers (356.9 m). (4) Subbotina patagonica with abnormally elongate shape and subrounded final chamber (356.9 m). (5) Subbotina triangularis with abnormal shape and placement of final chamber (356.9 m). (6) Acarinina sp. with abnormal shape and placement of final chamber (356.9 m). (7) Subbotina sp. with irregularly shaped and placed final chamber (356.4 m). (8) Acarinina sp. with abnormal shape and size of final chamber (356.9 m). (9) Acarinina sp. with diminutive final chamber and anomalous overall shape (356.9 m). (10) Subbotina sp. with diminutive and abnormally placed final chamber, and strange overall shape (356.9 m). (11) Acarinina sp. with abnormally loose coiling of chambers and diminutive final chamber (356.4 m). (12) Morozovella acuta/parva with flattened final chamber and irregular overall chamber structure (356.7 m). (13) Morozovella acuta with abnormal shapes of chambers and decreased structure to each individual chamber (356.9 m).

groups plot along the time and environment axes depending on when and where they are most abundant in the two sections. The known symbiont-bearing foraminifera, the muricate and keeled species groups, show higher NMDS1 scores than any other species group. The biserial/ triserial and non-spinose cancellate foraminifera, which are known to thrive in harsh environments (e.g., Coxall et al., 2006; Darling et al.,

shelf samples and the open ocean samples, and A. africana lies markedly closer to the open ocean samples. The clear separation of the open ocean and shelf samples along NMDS1 (Fig. 9) suggests that this axis corresponds to environment. NMDS2 appears to correspond to time, with all of the Paleocene samples showing lower values, and the CIE samples higher. The species 44

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Fig. 7. Scanning electron micrographs of PETM “excursion taxa” from CamDor. (1, 2) Ventral and edge view of an Acarinina sibaiyaensis from prior to the CIE (CD 224.2 m). (3) Ventral view of A. multicamerata from above the dissolution zone (CD 221.6 m). (4, 5) Ventral and dorsal view of an A. multicamerata missing a final chamber above the dissolution zone (CD 221.6 m). (6–8) Ventral, dorsal, and edge view of Acarinina africana above the dissolution zone (CD 221.6 m). (9) Ventral view of a small A. africana from after the dissolution zone (CD 222 m). Scale bars apply to each micrograph. Fig. 8. Scanning electron micrographs of representative individuals of Acarinina sibaiyaensis from below and within the CIE at CamDor (specimen A from CD 224.3 m and B from 224.4 m and specimens C and D are from CD 221.6 m). Specimens from samples prior to the CIE (A and B) are underdeveloped, and many do not have all 6 chambers in their final whorl. Samples from the CIE onset (C and D) include a combination of A. sibaiyaensis and A. multicamerata, depending on the number of chambers in the final whorl.

45

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48 43 44 Biserial/Triserial

9

Spinose Cancellate Muricate Smoot h

4939 38 Keeled

CIE

Paleocene

8 Non spinose cancellate 4 3 33 34

Fig. 9. Ordination of sample scores (samples plotted as sample number), species groups including the excursion taxa (in red). Site 1209 is represented by green numbers, BR by purple numbers, and CD by blue numbers. The dashed line represents the split in sample scores between samples from the Paleocene and the CIE, and the solid line illustrates the split between open ocean and shelf samples. Sample numbers for each site are compiled in Table S4. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

A. sibaiyaensis

Shelf

Open ocean

A.africana

ocean, whereas the muricate species, dominated by the genus Acarinina, are thought to host photosymbionts and live in the warmer mixed layer (e.g., D'Hondt et al., 1994; Berggren and Norris, 1997). Even though CD is shallower (~130–140 m) than typical open ocean thermocline depth and BR is close to it (~140–150 m; Stassen et al., 2015), the shared dominance of these two morphologic groups during the latest Paleocene at CD and BR suggests that the shelf was more stratified, allowing the two ecological groups to coexist. The benthic foraminiferal assemblage at BR provides strong evidence of long-term stratification at the PETM onset due to a strong river influence (Stassen et al., 2015), indicating that these depths are sufficient for stratification of the water column. Latest Paleocene planktonic assemblages also contain significant numbers of the triserial/biserial forms dominated by the genus Chiloguembelina. Extant biserial/triserial forms are able to occupy both planktic and benthic niche space, and thus are thought to be adapted to harsh environmental conditions (Darling et al., 2009). Inferring that Paleocene/Eocene forms had similar ecologies to their extant relatives, this species group likely lived in an environment characterized by a combination of low nutrients, above or below average temperatures, low salinity, low oxygen concentration or, possibly, low pH. DʼHaenens et al. (2012) also recorded abundant biserial planktonic foraminifera at the Paleocene-Eocene boundary at Deep Sea Drilling Project Site 401 in the North Atlantic Ocean and concluded that their presence during the PETM was due to the extreme environmental fluctuation (most notably temperature). Planktonic foraminiferal diversity is controlled in part by the thermal structure of the near surface ocean, which is regulated by sea surface temperatures (SSTs; e.g., Rutherford et al., 1999). The increase in species richness across the Paleocene/Eocene boundary at BR and CD (Figs. 4, 5, Table S2) suggests that niches were created during the PETM interval on the shelf due to a combination of increased stratification of the water column, and increased water depth resulting from local sealevel rise (e.g., Harris et al., 2010), and eutrophic conditions (e.g., Gibbs et al., 2006; Stassen et al., 2012). The hypothesized change in water structure is supported by δ18O measurements on multiple foraminiferal species occupying different depth habitats on the MidAtlantic Coastal Plain. These results also suggest a deepening of the mixed layer and a deeper thermocline during the CIE core (Makarova et al., 2017). Alternatively, they could record a change in depth habitat of the species analyzed, but this response also indicates a change in water column structure that could relate to temperature, productivity, pH, or salinity.

2009; DʼHaenens et al., 2012) show the lowest scores on NMDS1, suggesting that this axis may also correspond to the amount of stress in the environment.

4. Discussion 4.1. Assemblage shifts before and during the onset of the PETM The lithologic transition between the upper Paleocene Aquia Formation at CamDor (CD) or the Vincentown Formation at Bass River (BR), and the early Eocene Marlboro Clay corresponds to shifts in the preservation and abundance of foraminifera. Generally, specimens in the Aquia and Vincentown Formations are rare and fragmented while those in the Marlboro Clay are abundant, more robust, and less fragmented. An exception to this pattern is within the interval immediately below the dissolution zone in each section where foraminifera show increased levels of fragmentation (Table S2). Foraminiferal preservation in the Marlboro Clay is generally better than that in the underlying sandier formations, as clay tends to limit dissolution and overgrowth (e.g., Pearson et al., 1993). In addition, the rarity of planktonic foraminifera in the Aquia and Vincentown Formations is potentially a result of a shell breakage or non-deposition under a regime of greater hydraulic energy, while a smaller specimen size suggests that environmental factors may have limited growth rates (Bijma et al., 1990). Planktonic assemblages on the shelf undergo distinct changes in relative species abundances, diversity, and community structure across the onset of the PETM. However, changes are less extreme than those documented in the open ocean (e.g., Kelly, 2002; Petrizzo, 2007), as illustrated by tighter NMS clustering of samples (Fig. 9). The assemblage shift begins just below the onset of the CIE at both BR and CD with the appearance of the excursion species Acarinina sibaiyaensis. Conversely, the bulk of the turnover occurs at the base of the CIE, within the dissolution zone. At BR and CD, planktonic assemblages transition from being dominated by a few morphological groups with large fluctuations in species abundances in the upper Paleocene, to marginally more stable communities (here defined as less stratigraphic variability in the abundances of species groups) in the lower Eocene. The spinose cancellate and triserial/biserial planktonic foraminifera dominate assemblages prior to the onset of the CIE in both sections (Figs. 4, 5). At CD, the muricate species group is as abundant as the spinose cancellate species group, but at BR, the spinose cancellate group dominates. Spinose cancellate forms including the dominant genus, Subbotina, inhabited depths close to the thermocline in the open 46

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significant variations in morphology and size (Fig. 7), raising the possibility that these short-lived morphotypes may represent ecophenotypes (i.e., variants that developed in response to changing environmental parameters) rather than distinct species (e.g., Kelly et al., 1998). On the shelf, Acarinina soldadoensis/esnehensis, the ancestral species to A. sibaiyaensis, do not significantly decrease in abundance when the excursion taxa appear. This contrasts with deep sea Site 865 where the ancestral taxon Morozovella velascoensis morphotypes disappeared during the peak of the event (Kelly et al., 1998), presumably because it temporarily morphed into weakly calcified M. allisonensis due to low pH, only to subsequently revert back to the antecedent M. velascoensis following the PETM (Fraass et al., 2015). The excursion foraminifera have previously been considered an example of parapatric speciation (Kelly et al., 1998), arising in response to harsh surface water environments, which temporarily excluded their ancestors during the peak of the PETM in certain locations. However, the appearance of A. sibaiyaensis prior to the CIE and the sustained presence of the “ancestral” A. soldadoensis and A. esnhensis throughout the study interval suggests that A. sibaiyaensis is likely an ecophenotype rather than a distinct species. Previously, it has not been clear whether the “excursion” taxon Acarinina sibaiyaensis originated rapidly at the onset of the PETM in the open ocean, or whether it migrated from a marginal location at that time. The discovery of A. sibaiyaensis prior to the PETM in the two shelf sites, as well as the sites in Egypt, solves this mystery, suggesting that the taxon originated as a result of warming, increased stratification and oligotrophy on the shelf, and then colonized more diverse ocean habitats during the event as the open ocean environment became less hospitable to existing taxa.

4.2. Evolution of excursion taxa Acarinina sibaiyaensis emerged prior to the CIE in the two shelf sections studied. This taxon and A. africana have been observed up to 6 m below the CIE in shelf sections in Egypt (El-Naggar, 1966; Speijer et al., 2000), however these sections may have been extensively reworked (Zhang et al., 2018). In other slope and deep ocean sections, these species are restricted to the onset and peak of the event (e.g., Arenillas and Molina, 1996; Kelly et al., 1996; Arenillas et al., 1999; Molina et al., 1999; Norris and Röhl, 1999; Bolle et al., 2000; Berggren and Ouda, 2003; Petrizzo, 2007). Here we explore the significance of this diachrony. A possible explanation for the earlier shelf occurrence is that the specimens at BR and CD (and Egypt) were displaced from the PETM levels into lower horizons by bioturbation. However, the stark distinction in the well-preserved specimens of A. sibaiyaensis in the lowermost Eocene and the small and fragmented specimens in the uppermost Paleocene in BR and CD indicates that specimens have not been mixed across the dissolution zone (Fig. 8). Another possible explanation is that the interval just prior to the CIE at the deep-sea sites was dissolved via burndown during the early part of the event (e.g., Bralower et al., 2014). Although it is difficult to dismiss this possibility, we interpret the timing as having an environmental explanation. Thus we suggest that A. sibaiyaensis originally evolved on the shelf and subsequently migrated to the open ocean (e.g., Speijer et al., 2000). Kelly et al. (1998) proposed that the excursion taxa evolved in response to increased stratification of the ocean and deepening of the mixed layer, which led to increased oligotrophy. Several genera of planktonic foraminifera are known to host algal photosymbionts as an adaption to low nutrient waters (e.g., Norris, 1996). These genera host symbionts only in their later ontogenetic stages, and therefore exhibit size-dependent tendencies in their isotopic signatures (e.g., Pearson et al., 1993; D'Hondt et al., 1994; Kelly et al., 1996; Norris, 1999). Kelly et al. (1998) discovered similar size-dependent trends in the stable isotopes of specimens of A. sibaiyaensis and M. allisonensis from Ocean Drilling Program Site 865, suggesting that these taxa likely lived in the euphotic zone and hosted algal symbionts. Both A. sibaiyaensis and A. africana lie close to the symbiont-bearing species groups (muricate and keeled) along NMDS1 (Fig. 9), indicating that they share a similar ecology. The upper Paleocene Vincentown Formation (BR) and Aquia Formation (CD) are known to represent a shelf with restricted sediment input (Gibson et al., 2000; Stassen et al., 2015). Stassen et al. (2015) interpreted the outer shelf at BR to be oligotrophic at this time based on an assemblage dominated by the benthic foraminiferal species Gavelinella beccariiformis (Widmark and Speijer, 1997; Thomas, 1998). Warming during the latest Paleocene (e.g., Sluijs et al., 2007), immediately prior to the PETM would have led to a more stratified surface ocean. The rapid shift in environment (warming, stratification, oligotrophy) created more unfavorable conditions for foraminifera in the latest Paleocene. Therefore, we interpret the first occurrence of A. sibaiyaensis and the abundance of biserial/triserial species as adaptations to warm, stratified, oligotrophic environments. Though A. sibaiyaensis is present prior to the CIE in both CD and BR, A. africana and A. multicamerata are exclusive to the CIE as in other sections suggesting that A. sibaiyaensis originated first (Table S3). The increase in the relative abundances of A. sibaiyaensis, A. multicamerata and A. africana at CD and BR during the PETM, when coastal waters likely became more eutrophic (Gibbs et al., 2006; Kopp et al., 2007; Lippert and Zachos, 2007; Stassen et al., 2015), deeper, and very warm (Sluijs et al., 2007), suggests that the abundance of these species is more strongly controlled by temperature and water column structure than by nutrient levels. Therefore, we conclude that A. sibaiyaensis evolved in response to warming and increased stratification on the shelf just prior to the PETM, and subsequently tracked these conditions into the open ocean during the event, where it was able to become abundant in the oligotrophic environment. Acarinina sibaiyaensis, A. multicamerata and A. africana display

4.3. Malformation of foraminiferal tests Samples from above the dissolution zone (within the CIE) at BR (357 m through the highest sample studied at 356.4 m) contain a large proportion (~ 25%) of planktonic foraminifera that exhibit abnormal morphologies (Fig. 6). This abnormality manifests itself as extra or malformed chambers, as well as diminutive final chambers, and is observed on individuals of the muricate, keeled and spinose cancellate species groups. We note that the abnormal morphologies observed are not notably outside of the range of variation seen in these species, but the high proportion of variants in a restricted range of samples constitutes a significant signal. An unusual number of malformed or teratoid planktonic foraminifera were also reported from a PETM section in Tanzania (Bown and Pearson, 2009). Test malformation has been documented in numerous studies of planktonic and benthic foraminifera and also in shells of other marine organisms (such as diatoms, acritarchs, and nannoplankton) during times of enhanced environmental stress (e.g., Coccioni and Luciani, 2006; Falasco et al., 2009; Raffi et al., 2009; Munnecke et al., 2012; Bralower and Self-Trail, 2016). Numerous hypotheses have been suggested for the origin of malformation in foraminifera, including rapid climate fluctuations, hypersalinity, variation in rate/volume of sedimentation, heavy metal pollution, ash fall, and changes in seawater pH (e.g., Le Cadre et al., 2003; Coccioni and Luciani, 2006; Falasco et al., 2009). In BR, the samples in which malformed individuals are observed lie above the onset of the CIE, so the malformation is possibly a response to either rapid fluctuations in temperature or nutrients, increased freshwater creating suboptimal conditions on the shelf, or decreases in calcite saturation (e.g., Babila et al., 2016). The lack of malformed specimens among planktonic foraminifera at CD is notable, and may be due to better preservation of foraminifera at BR. However, this prevents us from making more firm conclusions about the significance of the specimens at BR and indicates that more research must be devoted to determining exactly where and when these variants occur as well as understanding their full significance. 47

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5. Conclusions

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Planktonic foraminifera from the Bass River and CambridgeDorchester cores on the Mid-Atlantic Coastal Plain reveal intriguing information about the changes that occurred on the shelf immediately before and during the PETM. The rarity, small size, and poor preservation of uppermost Paleocene taxa coupled with the spike of triserial/biserial forms indicates that the habitat was harsh for many species. A key finding, the presence of Acarinina sibaiyaensis in samples prior to the PETM in both sections, offers insights on the origination of the excursion species, which is restricted to the event in the deep sea. Our results suggest that this species arose as a result of warming and stratification on the shelf immediately prior to the PETM, then migrated into open ocean surface waters during the event as temperatures rose and nutrient levels declined. The distinct turnover in assemblage structure during the onset of the PETM suggests that the shelf developed to become a more hospitable, stratified, and eutrophic environment, with the keeled, spinose cancellate, smooth, and muricate species groups exhibiting relatively similar abundances and the overall diversity and preservation of planktonic foraminifera increasing. Finally, the occurrence of planktonic foraminifera variants in select samples in BR during the PETM onset may be evidence for a localized environmental perturbation, i.e., lower pH and carbonate unsaturation during the event consistent with proxy data. Supplementary data to this article can be found online at https:// doi.org/10.1016/j.marmicro.2018.12.001. Acknowledgments Research funded by NSF OCE-1416663. We acknowledge helpful discussions with James Zachos, Kate Freeman and Mark Patzkowsky. We appreciate the valuable help from Clay Kelly on foraminiferal taxonomy. We thank Ellen Thomas for providing sediment samples from the Bass River core. We thank Cheyne Hirota, Nathan Marshall, Rob Franks, Colin Carney and UCSC Stable Isotope Laboratory for technical assistance. This paper greatly benefited from the comments from two anonymous reviewers and the editorial handling by Richard Jordan. This research was supported in part by the USGS Land Change Science Program. Any use of trade, firm, or product names is for descriptive purposed only and does not imply endorsement from the U.S. Government. References Arenillas, I., Molina, E., 1996. Bioestratigrafia y evolucion de las asociaciones de foraminiferos planctonicos del transito Paleoceno-Eoceno en Alamedilla (Cordilleros Beticas). Revista Espanola de Micropaleontologia 28, 75–96. Arenillas, I., Molina, E., Schmitz, B., 1999. Planktic foraminiferal and 13C isotopic changes across the Paleocene/Eocene boundary at Possagno (Italy). Int. J. Earth Sci. 88, 352–364. Aubry, M.P., Cramer, B.S., Miller, K.G., Wright, J.D., Kent, D.V., Ollson, R.K., 2000. Late Paleocene event chronology; unconformities, not diachrony. Bulletin de la Sociètè Gèologique de France 171, 367–378. Aze, T., Pearson, P.N., Dickson, A.J., Badger, M.P.S., Bown, P.R., Pancost, R.D., Gibbs, S.J., Huber, B.T., Leng, M.J., Coe, A.L., Cohen, A.S., Foster, G.L., 2014. Extreme warming of tropical waters during the Paleocene-Eocene thermal Maximum. Geology 42, 739–742. Babila, T.L., 2014. Boron/Calcium in Planktonic Foraminifera: Proxy Development and Application to the Paleocene-Eocene Boundary. Rutgers The State University of New Jersey-New Brunswick. Babila, T.L., Rosenthal, Y., Wright, J.D., Miller, K.G., 2016. A continental shelf perspective of ocean acidification and temperature evolution during the Paleocene-Eocene thermal Maximum. Geology 44, 275–278. Barrerra, E., Huber, B.T., 1991. Paleogene and early Neogene oceanography in the southern Indian Ocean; Leg 119, foraminifer stable isotope results. Proc. Ocean Drilling Prog. Sci. Res. 119, 693–717. Berggren, W.A., Norris, R.D., 1997. Biostratigraphy, phylogeny and systematics of Paleocene trochospiral planktic foraminifera. Micropaleontology 43, 1–116. Berggren, W.A., Ouda, K., 2003. Upper Paleocene-lower Eocene planktonic foraminiferal biostratigraphy of the Dababiya section, Upper Nile Valley (Egypt). Micropaleontology 49, 61–92. Bijma, J., Faber, W.W.J., Hemleben, C., 1990. Temperature and salinity limits for growth

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