Oxygen and carbon stable isotope records of marine vertebrates from the type Maastrichtian, The Netherlands and northeast Belgium (Late Cretaceous)

Palaeogeography, Palaeoclimatology, Palaeoecology 392 (2013) 71–78

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Oxygen and carbon stable isotope records of marine vertebrates from the type Maastrichtian, The Netherlands and northeast Belgium (Late Cretaceous) Remy R. van Baal a,⁎, Renée Janssen a, H.J.L. van der Lubbe b, Anne S. Schulp a,c,d, John W.M. Jagt c, Hubert B. Vonhof a a

Faculty of Earth and Life Sciences, VU University Amsterdam, De Boelelaan 1085, NL-1081 HV Amsterdam, the Netherlands Marine Climate Research, Institute of Geosciences, Christian-Albrechts-Universität zu Kiel, Ludewig-Meyn-Straße 10, D-24118 Kiel, Germany c Natuurhistorisch Museum Maastricht, De Bosquetplein 6-7, NL-6211 KJ Maastricht, the Netherlands d Naturalis Biodiversity Center, P.O. Box 9517, NL-2300 RA Leiden, the Netherlands b

a r t i c l e

i n f o

Article history: Received 25 June 2012 Received in revised form 8 August 2013 Accepted 28 August 2013 Available online 5 September 2013 Keywords: Carbon isotopes Cretaceous Diagenesis Oxygen isotopes Paleobiology Paleoceanography

a b s t r a c t Stable isotope analysis of marine skeletal carbonates is an important tool for palaeoenvironmental reconstructions. However, in Mesozoic sedimentary sequences, diagenetic alteration often overprints the original skeletal carbonate isotope values. Yet, even if carbonate diagenesis did occur in such sequences, the original oxygen isotope values can still be preserved in enamel or bone phosphate of vertebrate fossils. Here are analysed the isotope compositions of tooth enamel structural carbonate and phosphate of various late Maastrichtian and early Palaeocene shark and ray taxa, as well as carapace bone of a late Maastrichtian marine turtle, Allopleuron hofmanni, from the type area of the Maastrichtian Stage in the southeast Netherlands and northeast Belgium. No correlation is observed between δ18Osc and δ18Op, suggesting diagenetic alteration of at least one fraction. In comparison to modern shark teeth, oxygen isotope ratios of the Maastrichtian–Palaeocene structural carbonate (δ18Osc) are significantly lower (5‰). As expected from previous isotope studies of calcitic fossils from the Maastrichtian type area, we believe the δ18Osc values to have been altered by meteoric diagenesis. The oxygen isotope ratios of phosphate (δ18Op) in Maastrichtian–Palaeocene shark and ray teeth are relatively wide ranging (16.9‰ to 25.0‰ vs. VSMOW), with median values matching data for extant shark teeth δ18Op, suggesting retention of the in vivo δ18Op signal. Similarly, the δ18Osc in the cheloniid turtle A. hofmanni is apparently overprinted by meteoric diagenesis, while the cortical (compact) bone of the carapace is interpreted to reflect the in vivo δ18Op isotope composition. Using a phosphate–water fractionation equation for biogenic apatite and median isotope values of late Maastrichtian–early Palaeocene shark and ray teeth, a seawater temperature of 19.7 °C is calculated. This is in good agreement with temperatures expected for the Maastrichtian of this area. Carbon isotope analyses (δ13C) of structural carbonate in shark teeth have yielded isotope ratios that agree well with those of modern subtropical sharks, suggesting the in vivo carbon isotope signal to have been retained. A comparison of A. hofmanni bone carbonate δ13C values with those of extant marine turtle species, suggests A. hofmanni to have had a carnivorous lifestyle. Also, A. hofmanni shows δ13C values that are N10‰ lower than the average δ13C of sharks and rays, more similar to sympatric mosasaurs. This distribution is interpreted to be the effect of respiratory physiology on δ13C fractionation. © 2013 Elsevier B.V. All rights reserved.

1. Introduction During the latest Cretaceous (c. 67–65.5 Ma), the southeast Netherlands and northeast Belgium were flooded by a shallow, subtropical epeiric sea (Fig. 1; Felder, 1994; Schiøler et al., 1997; Van der Ham et al., 2003; Mulder et al., 2005; Jagt and Jagt-Yazykova, 2012). The highly ⁎ Corresponding author. Tel.: +31 20 5987327. E-mail addresses: [email protected] (R.R. van Baal), [email protected] (R. Janssen), [email protected] (H.J.L. van der Lubbe), [email protected] (A.S. Schulp), [email protected] (J.W.M. Jagt), [email protected] (H.B. Vonhof). 0031-0182/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.palaeo.2013.08.020

fossiliferous carbonate sediments of the main outcrop in this area, the ENCI–HeidelbergCement Group quarry (Maastricht), and various other quarries (both active and defunct), document the complete upper Maastrichtian and the lower and middle Danian (lower Palaeocene) (Felder, 1975, 1996; Jagt et al., 1996; Schiøler et al., 1997). A wide range of vertebrate fossils have been recovered from these marine strata, including mosasaurid squamates (Dortangs et al., 2002; Schulp, 2006) and cheloniid turtles (Mulder, 2003), but also rare remains of terrestrial taxa such as hadrosaurid dinosaurs (Jagt et al., 2003), birds (Dyke et al., 2008) and mammals (Martin et al., 2005). Shark and ray teeth are particularly abundant at several levels within this sequence, but little is known

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N

100 km

RHENISH MASSIF

Fig. 1. Palaeogeographic reconstruction of Maastrichtian north-western Europe (adapted from Ziegler, 1990), with a star marking the study area.

squaliforms (Squalidae, dogfish sharks), with little specialised, cuttingtype dentition, often occurring in bottom waters and probably preying on fish, crustaceans and cephalopods, as well as much larger-sized lamniforms and myliobatiforms. Lamniforms were pelagic apex predators, of medium to large size, with a generally rather wide range of prey (Kriwet and Benton, 2004). They comprise members of the families Odontaspididae (mackerel sharks, of moderate to large size, with long prehensile teeth with lateral cusplets, preying mostly on fish and squid), Mitsukurinidae (goblin sharks; small to medium sized, long snouted, with tearing-type dentition, mostly in deeper water, on or near the bottom), Cretoxyrhinidae (large, voracious forms, with tearingtype dentition, probably swift swimmers, hunting on a wide range of prey), Serratolamnidae (comparable to cretoxyrhinids, but smaller), Anacoracidae (of medium to large size, with serrated teeth, reminiscent of extant tiger sharks), and Sclerorhynchidae (medium-sized sawfishes, with long and slim shark-like body and rostrum armed with teeth on each side to slash prey or probe in the sea floor, mostly bottom dwellers inhabiting shallow waters and straying into brackish or fresh water). Myliobatiforms are rays and comprise rhombodontids; medium-sized, bottom-dwelling forms with high-crowned crushing and grinding teeth, specialised in durophagous feeding (Kriwet and Benton, 2004). Allopleuron hofmanni is a marine turtle with an uncertain phylogenic position (Mulder, 2003) found solely in the Maastrichtian type area in southern Limburg (the Netherlands) and the adjacent provinces of Limburg and Liège in northeast Belgium. The carapace of adult specimens measures 1.4 m on average and displays large intercostal fontanelles (Mulder, 2003; Janssen et al., 2011). 2.2. Experimental methods

of the palaeoecological and palaeoenvironmental conditions under which these vertebrates thrived. Stable isotope analyses of these fossils may help elucidate such boundary conditions (Kolodny et al., 1983; Vennemann et al., 2001; Billon-Bruyat et al., 2005). Here are analysed the stable isotope compositions of late Maastrichtian and early Palaeocene shark and ray teeth and a carapace fragment of a marine turtle, Allopleuron hofmanni (Gray, 1831). Two fractions of fossil biogenic apatite (general formula: Ca5(PO4, CO3, F)3(OH, F, Cl, CO3)) were analysed: oxygen in phosphate (δ18Op), as well as carbon and oxygen in structural carbonate (δ13C and δ18Osc, respectively). In general, oxygen isotopes in biogenic apatite are examined for (palaeo)climatological reconstructions (Longinelli and Nuti, 1973; Vennemann et al., 2001; Amiot et al., 2007; Coulson et al., 2008; Pucéat et al., 2010), while carbon isotopes are analysed in order to unravel (palaeo)ecological patterns (McConnaughey et al., 1997; Biasatti, 2004; Robbins et al., 2008; Schulp et al., 2013). Here, diagenetically robust δ18Op data from shark tooth enamel and turtle carapace bone are used to calculate late Maastrichtian and early Palaeocene seawater temperatures, as in this study area carbonate δ18O values are considered to have been affected by diagenetic alteration (Vonhof et al., 2011). Carbon isotope values of diagenetically screened shark tooth enamel and turtle bone are interpreted in terms of differences in respiratory physiology (McConnaughey et al., 1997; Biasatti, 2004; Robbins et al., 2008; Schulp et al., 2013). 2. Material and methods 2.1. Sample materials The biogenic apatite material analysed (Table 1) comprises a fragment of a carapace of marine turtle A. hofmanni (Natuurhistorisch Museum Maastricht collections, NHMM 2008 137), and a total of 43 shark and ray teeth from the same collections, documenting ten species and subspecies (Table 2). These were collected from various levels within the Maastrichtian Gulpen and Maastricht formations, and the early Palaeocene Houthem Formation (Table 1). The neoselachian (shark and ray) taxa include small and slender (up to 1 m in total length)

Phosphate δ18O values are more resistant to diagenetic alteration than those of (structural) carbonate δ18O (Tudge, 1960; Kolodny et al., 1983; Zazzo et al., 2004). Therefore, paired δ18Op and δ18Osc analyses on biogenic apatite, as performed in the present study, may be used to assess the extent of diagenetic alteration of fossil bone and tooth material (Stanton Thomas and Carlson, 2004; Zazzo et al., 2004). To minimise the potential impact of diagenesis on our dataset, tooth enameloid was sampled, rather than dentine, because the latter has a crystal structure that is more susceptible to diagenetic alteration (Kolodny and Raab, 1988; Wang and Cerling, 1994; Picard et al., 1998; Sharp et al., 2000; Lécuyer et al., 2003; Pucéat et al., 2003; Stanton Thomas and Carlson, 2004). Oxygen isotope values in biogenic apatite have been analysed using two techniques: acid-dissolution of the structural carbonate fraction (AD, Section 2.2.1; McCrea, 1950) and high-temperature reduction of the phosphate fraction (HTR, Section 2.2.2; Vennemann et al., 2002). Carbon isotope values were acquired using AD of the structural carbonate fraction. Prior to isotope analysis, tooth samples were soaked in a 1 M acetic acid solution for 45 min in order to remove diagenetic CaCO3, and subsequently washed with Milli-Q water (Bocherens et al., 1996). Approximately 7 mg of powdered sample material was taken from each tooth using a standard handheld dentist drill. The turtle carapace fragment was embedded in epoxy and cut dorsoventrally. Two separate growth incremental series, both from the cortical (compact) and the cancellous (spongy) bone (samples I to VIII; see Table 1) were sampled, using a Mercantech MicroMill for AD (~1 mg), and a standard handheld dentist drill for HTR (~7 mg). Unless stated otherwise, all reported uncertainties for stable isotope data are 1σ. 2.2.1. Acid dissolution Apatite powder samples of ~0.4 mg were placed in exetainer vials, which were then flushed with pure (99.99%) helium gas. Adding orthophosphoric acid and leaving the samples to digest for at least 24 h at 45° Celsius ensured quantative dissolution of the structural carbonate (McCrea, 1950). Subsequently, multiple samples of the CO2–He mixture gas were analysed using a Thermo Finnigan GasBench II

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Table 1 Stable isotope compositions of late Maastrichtian and early Palaeocene (early–middle Danian) shark and ray tooth enamel and Allopleuron hofmanni carapace bone. For a discussion of stratigraphic levels, reference is made to W.M. Felder (1975) and Jagt and Jagt-Yazykova (2012). Notes: sc, duplo analysis on structural carbonate fraction; p, duplo analysis on phosphate fraction. #

Species

Stratigraphic level

δ13C (‰ VPDB)

δ18Osc (‰ VSMOW)

δ18Op (‰ VSMOW)

1 2 3a 3b 4a 4b 5 6a 6b 7a 7b 8a 8b 8b p 8c 9a 9a sc 10a 10a p 10b 10c 10d 11a 11b 18a 18b 12a 12b 12c 13a 13b 13c 13d 13d p 13e 13f 13g 14a 14b 14c 15a 15b 16 17a 17b 17c 17d 17e I II III IV V VI VII VIII

Cretalamna appendiculata pachyrhiza Palaeohypotodus bronni Serratolamna serrata Serratolamna serrata Carcharias ? sp. Carcharias ? sp. Palaeohypotodus bronni Palaeohypotodus bronni Squalicorax pristodontus Palaeohypotodus bronni Pseudocorax affinis Indeterminate Indeterminate Indeterminate Indeterminate Palaeohypotodus bronni Palaeohypotodus bronni Pseudocorax affinis Pseudocorax affinis Rhombodus binkhorsti Palaeohypotodus bronni Palaeohypotodus bronni Palaeohypotodus bronni Palaeohypotodus bronni Anomotodon sp.? Palaeohypotodus bronni Squalicorax pristodontus Ganopristis leptodon Palaeohypotodus bronni Squalicorax pristodontus Palaeohypotodus bronni Pseudocorax affinis Palaeohypotodus bronni Palaeohypotodus bronni Pseudocorax affinis Palaeohypotodus bronni indeterminate Pseudocorax affinis Pseudocorax affinis Pseudocorax affinis Squalicorax pristodontus Palaeohypotodus bronni Palaeohypotodus bronni Palaeohypotodus bronni Palaeohypotodus bronni Palaeohypotodus bronni Centrophoroides appendiculatus Centrophoroides appendiculatus Allopleuron hofmanni Allopleuron hofmanni Allopleuron hofmanni Allopleuron hofmanni Allopleuron hofmanni Allopleuron hofmanni Allopleuron hofmanni Allopleuron hofmanni

Geulhem Member, middle Geulhem Member, base Meerssen Member, top Meerssen Member, top Meerssen Member, middle Meerssen Member, middle Meerssen Member, base Kanne horizon Kanne horizon Nekum Member, base Nekum Member, base Emael Member, Lava horizon Emael Member, Lava horizon Emael Member, Lava horizon Emael Member, Lava horizon Emael Member, base Emael Member, base Emael Member, base Emael Member, base Emael Member, base Emael Member, base Emael Member, base Schiepersberg Member, base Schiepersberg Member, base Kunrade Formation Kunrade Formation Gronsveld Member, base Gronsveld Member, base Gronsveld Member, base Valkenburg Member, base Valkenburg Member, base Valkenburg Member, base Valkenburg Member, base Valkenburg Member, base Valkenburg Member, base Valkenburg Member, base Valkenburg Member, base Lanaye Member, top Lanaye Member, top Lanaye Member, top Lanaye Member, base Lanaye Member, base Vijlen Member, middle Vijlen Member, base Vijlen Member, base Vijlen Member, base Vijlen Member, base Vijlen Member, base Maastrichtian, unspecified Maastrichtian, unspecified Maastrichtian, unspecified Maastrichtian, unspecified Maastrichtian, unspecified Maastrichtian, unspecified Maastrichtian, unspecified Maastrichtian, unspecified

5.1 3.2 5.4 5.5 −1.7 – 6.7 3.7 3.4 2.2 3.9 4.1 7.7 7.7 6.8 −1.8 −1.5 9.1 9.1 3.9 5.3 −3.8 4.6 3.5 1.6 0.0 1.7 −1.4 6.3 3.0 5.7 6.8 11.0 11.0 6.5 3.4 3.6 7.1 5.6 5.3 7.9 6.7 7.4 2.7 4.6 0.9 – – −7.5 −6.8 −7.1 −6.9 1.6 −4.0 −7.2 −7.2

25.7 21.8 26.1 25.5 25.6 – 26.4 27.1 26.6 26.2 25.7 27.3 28.6 28.6 27.3 26.6 26.7 27.5 27.5 26.7 28.2 26.7 26.0 26.1 26.4 26.7 26.8 26.6 26.7 26.5 28.0 27.9 27.9 27.9 27.0 26.5 28.1 28.2 27.8 27.7 26.9 27.2 26.9 26.8 27.3 25.9 – – 26.8 27.1 26.2 26.5 26.5 28.5 27.3 27.1

22.1 22.9 19.7 17.8 22.4 20.6 – – 23.3 16.9 23.4 19.6 24.4 25.0 21.0 17.8 17.8 22.0 21.7 23.3 23.6 19.9 24.5 22.6 22.7 22.2 23.0 21.7 18.3 22.3 – 23.4 20.1 21.4 22.2 23.1 – 23.4 23.7 22.2 21.5 22.5 23.2 20.2 22.0 24.2 21.7 20.3 20.4 20.8 20.4 20.5 20.5 19.9 19.2 –

preparation device interfaced with a Thermo Finnigan Delta + mass spectrometer. For both δ13C and δ18Osc the uncertainties were 0.13‰, as determined by multiple analyses of VICS (VU in-house Carbonate Standard; normalised to NBS 18, 19 and 20) in between samples. Data for δ13C are reported relative to the Vienna Peedee Belemnite (VPDB) standard, while δ18Osc data were recalculated relative to Vienna Standard Mean Ocean Water (VSMOW) using Eq. (1) (Friedman and O'Neil, 1977).

18

18

δ OVSMOW ¼ 1:03086  δ OVPDB þ 30:86:

ð1Þ

2.2.2. High-temperature reduction Biogenic apatite was converted to silver phosphate (Ag3PO4), following techniques described by Dettman et al. (2001). To verify the absence of fractionation during the conversion of biogenic apatite to Ag3PO4, two standard materials (SRM-120c Phosphate Rock and a powdered Megaselachus megalodon tooth, the latter being an in-house standard) were treated in the same way. Samples and standards were then analysed alternately using a Thermo Finnigan TC/EA interfaced with a Finnigan Delta + XP (Vennemann et al., 2002). Values for δ18Op were converted to the Vienna Standard Mean Ocean Water (VSMOW) scale, based on a δ18Op value of 22.58 for SRM-120c (Vennemann et al., 2002; Pucéat et al., 2010). Standard deviation of

74

R.R. van Baal et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 392 (2013) 71–78 Table 2 Shark and ray species analysed in the present study, with assignment to family and pertinent references (see also Kriwet and Benton, 2004). Species

Family

Reference

Centrophoroides appendiculatus (Agassiz, 1843) Cretalamna appendiculata pachyrhiza Herman, 1977 Palaeohypotodus bronni (Agassiz, 1843) Anomotodon sp. Serratolamna serrata (Agassiz, 1843) Carcharias sp. Squalicorax pristodontus (Agassiz, 1843) Pseudocorax affinis (Agassiz, 1843) Rhombodus binkhorsti Dames, 1881 Ganopristis leptodon (Arambourg, 1935)

Squalidae Cretoxyrhinidae Odontaspididae Mitsukurinidae Serratolamnidae Odontaspididae Anacoracidae Anacoracidae Rhombodontidae Sclerorhynchidae

Herman (1977), Cappetta (1987) Herman (1977) Herman (1977) Herman (1977), Cappetta (1987) Welton and Farish (1993) Cappetta (1987) Welton and Farish (1993) Herman (1977) Welton and Farish (1993) Herman (1977)

multiple standards, analysed in between the samples, were 0.28‰ (SRM120c Phosphate Rock), 0.17‰ (commercially available Sigma-Aldrich silver phosphate, St Louis, Missouri, USA) and 0.26‰ (M. megalodon tooth). An analytical uncertainty of 0.3‰ would therefore be appropriate for the samples analysed.

is of similar magnitude as the previously reported diagenetic δ18Osc shift in carbonate fossils from the type Maastrichtian (Vonhof et al., 2011). Together, this leads us to conclude that the δ18Osc values of Maastrichtian shark and ray teeth reported here are lowered by meteoric diagenesis.

3. Results and discussion

3.3. Shark and ray δ13C

Oxygen and carbon isotope ratios (δ13C, δ18Osc and δ18Op) of specimens analysed are summarised in Table 1. With regard to shark and ray teeth, both δ13C and δ18Op values fall in a relatively wide range (average 4.4 ± 3.3‰ and 21.9 ± 2.0‰, respectively), while values for δ18Osc fall in a more narrow range (average 27.0 ± 1.4‰).

Modern shark tooth enamel δ13C values are indistinguishable from Maastrichtian–Palaeocene δ13C values (Fig. 3B). This suggests that the Maastrichtian–Palaeocene neoselachian tooth δ13C data represent in vivo values. This is not surprising in view of the generally good preservation of the original δ13C signals in other marine carbonate fossils

3.1. Modern dataset for comparison

3.2. Diagenetic alteration The potential impact of diagenetic alteration in fossil teeth can be assessed by comparing values of δ18Osc with δ18Op, because they should plot along a correlation line intersecting at ~8‰ (Bryant et al., 1996; Iacumin et al., 1996; Zazzo et al., 2004). Fig. 2 shows the oxygen isotope values of phosphate and structural carbonate of all shark and ray teeth from which both fractions were analysed, including regression lines by Iacumin et al. (1996), Bryant et al. (1996) and Zazzo et al. (2004). All data points plot above the regression line, suggesting diagenetic alteration of at least one of the fractions. Zazzo et al. (2004, p. 2253) stated that “during inorganic oxygen isotope exchange at surface temperatures, only structural carbonate oxygen will exchange with oxygen from ambient water because of the very slow kinetics between phosphate oxygen and water at Earth surface temperatures”. A comparison of our Maastrichtian dataset with the modern shark teeth analysed by Vennemann et al. (2001) (Fig. 3A) shows a significant offset of ~5‰ for δ18Osc. Approximately ~1‰ of that can be accounted for by the fact that no ice caps were present during the Maastrichtian and early Palaeocene (Shackleton and Kennett, 1975). The remaining ~4‰ offset

25

24

23

δ18Op (‰ VSMOW)

In contrast to most other fossil biota, stable isotope records of late Maastrichtian and early Palaeocene shark and ray teeth can be compared with those of equivalent extant species. The basis for this comparison is an extensive dataset by Vennemann et al. (2001), which comprises tooth enamel and dentine isotope data from extant subtropical (South Africa) and cold-water sharks (Alaska and Canada). In view of the subtropical shallow water setting of the Maastrichtian type area, the isotope composition of the Maastrichtian and early Palaeocene taxa were compared only with subtropical sharks in the Vennemann et al. (2001) dataset. For correct comparisons of fossil neoselachian tooth enamel δ13C with that of modern sharks, dentine isotope data need to be excluded from the Vennemann et al. (2001) dataset, because carbon isotope fractionation has been observed between dentine and enamel of individual shark teeth. This is not the case for δ18Op and δ18Osc (Vennemann et al., 2001).

26

22

21

20

19

18

17

16 21

22

23

24

25

26

27

28

29

δ18Osc (‰ VSMOW) Anomotodon sp.? C. appendiculata pachyrhiza Indeterminate Pseudocorax affinis Serratolamna serrata

Carcharias? sp. Ganopristis leptodon Palaeohypotodus bronni Rhombodus binkhorsti Squalicorax pristodontus

Fig. 2. Oxygen isotope composition of shark and ray tooth enamel: phosphate (δ18Op) versus structural carbonate (δ18Osc) fractions. Unaltered δ18Op–δ18Osc correlation lines by Iacumin et al. (1996) and Bryant et al. (1996) (dashed), and Zazzo et al. (2004) (solid).

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δ18Osc (‰ VSMOW) 30

20

25

30

A 25

35

δ18Op (‰ VSMOW)

δ13C (‰ VPDB) 40

-10

0

10

B

75

15

20

25

30

C

26.8

Fossil

20 4.6

15 22.2

Frequencies

10 5 0 5

1.6

Modern

10 15 20

31.4

25 22.6

30 Fig. 3. Histograms of Maastrichtian–Palaeocene and extant shark and ray tooth enamel stable isotope data. Median values are depicted for each frequency distribution. The modern dataset is adapted from Vennemann et al. (2001) (see Section 3.1).

from the study area (Vonhof et al., 2011). The ~15‰ range of δ13C values observed cannot be attributed to species-specific fractionation, since several of the species plot throughout the entire range. This may reflect that, like today, these species occupy roughly similar trophic levels (Cortés, 1999; Pinnegar et al., 2002). We do not believe that the wide range of δ13C values is a diagenetic artefact, since a similarly wide and overlapping δ13C range can be observed in modern sharks (Vennemann et al., 2001). Although we have strived to sample enamel only, we cannot rule out that the lower values in the observed δ13C range might be the result of accidental addition of dentine into the sample powders — which is known to lower δ13C values (Vennemann et al., 2001). 3.4. Shark and ray δ18Op Late Maastrichtian–early Palaeocene and modern shark tooth δ18Op values compare relatively well (Fig. 3C). Both datasets have approximately the same median (i.e., 22.2‰ vs. 22.6‰), but the distribution in the former is of a considerably wider range. This is to be expected as these teeth originate from a ~4 myr interval, compared to the 4-year period (1996–1999) covered by the Vennemann et al. (2001) dataset. Even a single stratigraphic level, for which we record intraspecific differences in δ18Op values as large as 2.2‰ (modern sharks have up to 1.4‰ intraspecific differences), represents a considerable span of time (Jagt and Jagt-Yazykova, 2012). Section 3.5 discusses possible palaeoceanographical characteristics that could have contributed to the wide δ18Op range observed. Pucéat et al. (2007) reported a δ18Op value of 22.32‰ for a single indeterminate fish tooth from the “Maastricht (The Netherlands)” locality, close to the median δ18Op value of our dataset. The δ18Op dataset presented in Fig. 3C seems to deviate from a Gaussian frequency distribution, with a small but distinct cluster of samples at the lower end of the reported δ18Op values. Although we found no independent geochemical evidence to discard these samples, we suspect diagenetic alteration to have affected the five lowest δ18Op values observed. Exclusion of these δ18Op values from the dataset shifts the median δ18Op value of the entire dataset by only 0.2‰. In the absence of independent lines of evidence for diagenetic alteration of

these five samples we decided not to remove them and base further comparison and calculations using the shark and ray tooth δ18Op values on the statistical characteristics of the entire dataset. 3.5. Type Maastrichtian palaeoceanography Since Maastrichtian–Palaeocene shark and ray teeth yield in vivo δ18Op values, palaeo-seawater temperatures can be calculated by applying these in the recently revised phosphate–water fractionation equation for biogenic apatite (Eq. (2); Pucéat et al., 2010). The Pucéat et al. (2010) equation is arguably better constrained than those of Longinelli and Nuti (1973) and Kolodny et al. (1983), because it is based on a dataset of fish teeth from aquarium cultures and the HTR technique. Furthermore, Pucéat et al. (2010) included a thorough revision of earlier analytical work that demonstrates potential problems with comparison of older data with modern experiments. We therefore adopt the Pucéat et al. (2010) equation rather than earlier ones.   18 18 T ¼ 124:6−4:52 δ Op −δ Ow

ð2Þ

At a Maastrichtian δ18Ow value of −1‰ (VSMOW; Shackleton and Kennett, 1975), and an average Maastrichtian–Palaeocene neoselachian tooth enamel δ18Op value of 22.2‰, the water temperature calculated by Eq. (2) would be 19.7 °C. This is in good agreement with expected temperature ranges of Maastrichtian sea surface temperatures in this area (Lowenstam and Epstein, 1954, 1959; Zakharov et al., 2006; Pucéat et al., 2007). Conversely, we do not believe the wide range of δ18Op values recorded by the sharks and rays to have been caused by surface water temperature variation only: the most extreme δ18Op values in this dataset (16.9‰ low and 25.0‰ high) would imply an unfeasible temperature range from ~44 °C to ~7 °C. When the same data are plotted per species versus stratigraphic level (Fig. 4), it becomes clear that neither stratigraphic trends, nor species-specific distinction can be designated as possible causes for the wide range observed. Instead, we believe significant fluctuation of δ18Ow to be reflected in the wide δ18Op range. For instance, evaporation from a large surface of shallow

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125

cortical δ18Op (‰ VSMOW)

Geulhem 100

Meerssen Nekum

Stratigraphic level (m)

75

cancellous

21

Emael

20

19

Gronsveld I 50

II

III

IV

V

VI

VII

Specimen #

Lanaye

Fig. 5. Marine turtle Allopleuron hofmanni δ18Op values from a dorsoventral growth line (sclerochronological) series of carapace bone (NHMM 2008 137).

25

Lixhe environmental water (Barrick et al., 1999) and a correlation has been determined between the δ18Op values of aquatic turtle bone and the δ18Ow values of their host water (Eq. (3); Barrick et al., 1999; Coulson et al., 2008). This potentially enables direct calculation of Maastrichtian seawater δ18Ow values from A. hofmanni bone δ18Op data.

0

Vijlen 18

18

δ Ow ¼ 1:06  0:06  δ Op ‐22:7  1:3:

ð3Þ

-25 16

17

18

19

20

21

22

23

24

25

26

δ18Op (‰ VSMOW) Anomotodon sp.? Centrophoroides appendiculatus Indeterminate Pseudocorax affinis Serratolamna serrata C. appendiculata pachyrhiza

Carcharias? sp. Ganopristis leptodon Palaeohypotodus bronni Rhombodus binkhorsti Squalicorax pristodontus

Fig. 4. Shark and ray tooth enamel δ18Op values per species versus stratigraphic level. Name and thickness of stratigraphic members after Jagt and Jagt-Yazykova (2012): situated between the Lanaye and Gronsveld members is the Valkenburg member, and between the Gronsveld and Emael members is the Schiepersberg member. The stratigraphic level of 0 m is the current quarry floor at the ENCI–HeidelbergCement Group quarry, Maastricht. The stratigraphic position of the two shark teeth from the Kunrade Formation was extrapolated to fit the ENCI quarry stratigraphy.

water (Pucéat et al., 2003) and influx of freshwater from the nearby Rhenish Massif (Fig. 1) can cause significant variation in seawater δ18O values, effectively broadening the range of δ18Op values incorporated into shark and ray teeth. Thus, palaeotemperature reconstructions based on individual specimens have a relatively high degree of uncertainty, and replication of results by analysing multiple specimens is called for in order to arrive at robust reconstructions. 3.6. Marine turtle δ18O Diagenetic alteration of oxygen isotope values is readily visible in a dorsoventral growth line series of A. hofmanni carapace bone. The δ18Osc data fall within a wide range (26.2–28.5‰), presumably indicative of diagenetic alteration. In the δ18Op dataset, a decreasing isotopic trend is seen from the cortical (compact) towards cancellous (spongy) bone (Fig. 5). The cortical bone δ18Op values fall within a narrow range of 20.5 ± 0.2‰ (VSMOW), ~0.5–2.5‰ lower than δ18Op values of modern marine turtles (Coulson et al., 2008). Turtles are known to exhibit significant fractionation between body water and

Inserting in Eq. (3) a δ18Op value of 20.5‰ results in a palaeo-δ18Ow value of −1.0‰. This fits well with estimated ranges of Maastrichtian δ18Ow values, as discussed in Section 3.5. We take this to support that the δ18Op data of the A. hofmanni cortical bone have not been diagenetically altered. The cancellous bone of NHMM 2008 137 has up to 1.5‰ lower δ18Op values than the cortical bone, which is probably caused by a higher susceptibility to diagenetic alteration of the more porous and permeable cancellous bone tissue. 3.7. Marine turtle δ13C The average cortical bone δ13C value for A. hofmanni is −7.1 ± 0.3‰. This compares well with δ13C values of extant carnivorous marine turtles such as Dermochelys coriacea (Vandelli, 1761) and Lepidochelys olivacea (Eschscholtz, 1829), and contrasts with the ~8‰ higher values for the herbivore marine turtle Chelonia mydas (Linnaeus, 1758) (Fig. 6). This difference may be explained to a certain extent by the relatively higher δ13C value of seagrass, the diet of C. mydas, compared to δ13C values of a carnivorous diet (Biasatti, 2004). Fossil evidence for seagrass is present in the Maastrichtian stratotype area (Van der Ham et al., 2007). However, assuming that Maastrichtian seagrass was isotopically similar to modern seagrass (10‰ VPDB; Hemminga and Mateo, 1996), it is unlikely that A. hofmanni fed on seagrass. A carnivorous lifestyle, comparable to modern D. coriacea and L. olivacea, is isotopically more likely. Remarkably, A. hofmanni exhibits N10‰ lower δ13C values than the average δ13C values of the teeth of sympatric neoselachians (Fig. 6). This difference is far too great to be explained by differences in trophic level between these taxa, taking into account that generally a ~1‰ increase per trophic level is reported for δ13C (e.g. DeNiro and Epstein, 1978). In fact, A. hofmanni δ13C values are relatively close to those of sympatric mosasaurs — the taxa with the lowest δ13C values in the type Maastrichtian (Fig. 6; Schulp and Vonhof, 2010; Schulp et al., 2013). Th δ13C distribution outlined in Fig. 6 can be explained in terms of respiratory physiology: lung-breathing (pulmonate) marine reptiles versus gill-breathing fish. When pulmonates dive, the need to hold their breath causes accumulation of respired CO2 in the lungs (McConnaughey et al., 1997; Biasatti, 2004). The δ13C of respired CO2

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Neoselachians Allopleuron hofmanni Mosasaurs Chelonia mydas Dermochelys coriacea Lepidochelys olivacea -16

-14

-12

-10

-8

-6

-4

-2

0

2

4

6

8

10

12

δ13C (‰ VPDB) Fig. 6. δ13C values of neoselachians (this study), A. hofmanni (this study) and sympatric mosasaurs (Schulp et al., 2013), as well as several extant marine turtles (carnivorous Dermochelys coriacea and Lepidochelys olivacea, and herbivorous Chelonia mydas; see Biasatti, 2004).

gradually drops when breath is held, leading to incorporation of lower δ13C values in tissues of pulmonates (McConnaughey et al., 1997; Biasatti, 2004; Robbins et al., 2008; Schulp et al., 2013). This suggests that when dealing with marine pulmonates like cheloniids and mosasaurs, respiratory physiology is a more dominant factor in controlling δ13C fractionation than diet.

Acknowledgements

4. Conclusions

References 18

18

An internal δ Op–δ Osc comparison and external comparison with a modern shark teeth dataset (Vennemann et al., 2001) shows that shark and ray teeth from the upper Maastrichtian and lower Palaeocene of the Maastrichtian type area appear to have retained in vivo stable isotope compositions. The lowest δ18Op values in the dataset may be the result of diagenetic alteration, but this does not cause a significant shift in median δ18Op values. Maastrichtian and Palaeocene shark and ray tooth enamel δ13C values compare well with those of extant sharks, suggesting that the structural carbonate in these teeth retains the original δ13C values, while δ18Osc values have been altered towards lower values. This is in line with the isotope record of carbonate fossils from the Maastrichtian type area, which also display significant meteoric overprinting of δ18O values, while in vivo δ13C values are retained (Vonhof et al., 2011). Using a median neoselachian tooth enamel δ18Op value of 22.2‰ and a −1.0‰ δ18Ow value, an average Maastrichtian seawater temperature of 19.7 °C is calculated. This is in good agreement with previously calculated seawater temperatures for the Maastrichtian of this area. The wide range of δ18Op values recorded by neoselachians is possibly caused by significant variation in δ18Ow values due to evaporation and influx of freshwater in this nearshore, shallow-water environment. The oxygen isotope record of the late Maastrichtian marine turtle, A. hofmanni, shows significant sclerochronological variability. In a dorsoventral analytical series of A. hofmanni carapace bone, cancellous (spongy) bone δ18Op values display a distinct trend, which is interpreted to represent diagenetic alteration. In contrast, cortical (compact) bone δ18Op values fall within a narrow range (20.5 ± 0.2‰). Based on this δ18Op value, the well-established δ18Op–δ18Ow relationship for extant turtles (Coulson et al., 2008) yields a feasible late Maastrichtian δ18Ow value of −1‰ (Shackleton and Kennett, 1975). The combined evidence suggests that only the cortical bone retains in vivo δ18Op values. Comparison of A. hofmanni bone carbonate δ13C values with those of several extant marine turtles, suggests that A. hofmanni had a carnivorous lifestyle. A N 10‰ δ13C offset between A. hofmanni and the neoselachians cannot be explained by dietary fractionation. The data presented here support the notion that respiratory physiology must have been the dominant factor controlling δ13C fractionation in pulmonate marine reptiles like A. hofmanni and mosasaurs.

For technical assistance with isotope analyses, we wish to thank Suzan Verdegaal-Warmerdam. Comments on an earlier typescript by Aurélien Bernard and two anonymous journal reviewers greatly improved the present version.

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