Chemical Geology 411 (2015) 81–96

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Chemical Geology

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Carbon isotope composition in modern brachiopod calcite: A case ofequilibrium with seawater?

Uwe Brand a,⁎, K. Azmy b, E. Griesshaber c, M.A. Bitner d, A. Logan e, M. Zuschin f, E. Ruggiero g, P.L. Colin h

a Department of Earth Sciences, Brock University, St. Catharines, Ontario L2S 3A1, Canadab Department of Earth Sciences, Memorial University of Newfoundland, St. John's, Newfoundland A1B 3X5, Canadac Department für Geo- und Umweltwissenschaften, Ludwig Maximillians Universität, München D-80333, Germanyd Institute of Paleobiology, Polish Academy of Sciences, ul. Twarda 51/55, 00-818 Warszawa, Polande Centre for Coastal Studies, University of New Brunswick, Saint John, New Brunswick E2L 4 L5, Canadaf University of Vienna, Department of Paleontology, A-1090 Wien, Austriag Dipartimento di Scienze della Terra, Università di Napoli Frederico II, 801380 Napoli, Italyh Coral Reef Research Foundation, P.O. Box 1765, Koror 96940, Palau

http://dx.doi.org/10.1016/j.chemgeo.2015.06.0210009-2541/© 2015 Elsevier B.V. All rights reserved.

⁎ Corresponding author.E-mail address: uwe.brand@brocku.ca (U. Brand).

a b s t r a c t

a r t i c l e i n f o

Article history:Received 19 June 2014Received in revised form 22 June 2015Accepted 23 June 2015Available online 26 June 2015

Keywords:Modern brachiopod calciteδ13C valuesEquilibrium fractionation?Secondary & tertiary layersCarbon-isotope associated effectsDissolved inorganic carbonProductivityUpwelling

We examined a large number of modern, shallow-water articulated brachiopods representing the ordersTerebratulida, Rhynchonellida, Thecideida and one inarticulated brachiopod of the order Craniida from polar totropical regions for their carbon isotope compositions. Based on our detailed investigation, we recommendavoiding fast growth areas such as the youngest shell increments; in addition, the primary layer and transitionzone calcites of brachiopods must be avoided because they are in carbon and oxygen isotope disequilibriumwith ambient seawater. After adjusting isotope compositions for theMg effect, we observed no significant differ-ence (p N 0.05) in δ13C values between dorsal and ventral valves of our articulated brachiopods.Using the calcite-bicarbonate enrichment factor (ε) in conjunctionwith δ13C values of dissolved inorganic carbonof habitat seawater, we conclude that modern shallow-water articulated and some inarticulated brachiopods in-corporate oxygen (Brand et al., 2013) and carbon isotopes into shell calcite of secondary and/or tertiary layers inapparent equilibriumwith ambient seawater.Within the general concept of equilibrium incorporation, with sea-water, shell δ13C values are an excellent recorder of local/global seawater environments and water mass circula-tion. Thus, application of theMg-effect permits brachiopods to be an extremely powerful archive, and δ13C valuesmore precise proxy and tracer of past changes in marine productivity, evolution of seawater carbon chemistryand variation in the global carbon cycle.

© 2015 Elsevier B.V. All rights reserved.

1. Introduction

Articulated brachiopods secrete calcite shells with low to intermedi-ate amounts of MgCO3 that makes them quite resistant to post-depositional alteration (Brand and Veizer, 1980), and coupled withtheir high diversity, abundance and ubiquity makes them excellent ar-chives to carry primary isotopic signals of the ambient environment(e.g., Brand et al., 2003; Parkinson et al., 2005). This, of course, is subjectto them incorporating stable isotopes into shell calcite in or near equi-librium with the ambient seawater. Lowenstam (1961) in his seminalstudy concluded that brachiopods incorporate oxygen isotopes intoshell calcite in equilibrium with seawater, which has been confirmedfor them as a group by Brand et al. (2013). Unfortunately, the same can-not be said for their carbon isotope compositions, especially, sinceWefer (1985) concluded that brachiopods from Bermuda incorporate

carbon isotopes into shell calcite in disequilibrium with seawater.Since that study, many subsequent attempts at reconciling brachiopodshell carbon isotope compositions with those of ambient seawater re-main inconclusive (e.g., Carpenter and Lohmann, 1995; Buening andSpero, 1996; Auclair et al., 2003; Brand et al., 2003; Parkinson et al.,2005; Yamamoto et al., 2010, 2013; Takayanagi et al., 2013).

Using a global δ13CDIC value range of 1.5 to 2.0‰ (Kroopnick, 1985)for surface ocean-waters in conjunctionwith the range of the calcite en-richment factor, ε, (Romanek et al., 1992), we constructed a δ13C andδ18O value cross-plot but most δ13C values of our modern brachiopodsfall outside the range of calcite precipitated in isotope equilibriumwith seawater (Fig. 1). However, this interpretationmay be complicatedby the highly variable nature of surface seawater δ13C value of dissolvedinorganic carbon. For example, the negative covariance of δ13C–δ18Ovalues determined for brachiopods from polar and temperate regions(Fig. 1, slopes ranging from 1.1 to 1.7 for brachiopods from Signy Islandand Friday Harbor, respectively) are similar to those noted for somemodern forams and corals (cf. McConnaughey, 1989a, 1989b; Spero

-3

-2

-1

0

+1

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-4 -3 -2 -1 0 +1 +2 +3 +4 +5

δ13C

(‰

)

δ18O (‰)

Tropics (30°-30°)Temperate (30°-60°)Polar (>60°), AntarcticaPolar, Arctic

Fig. 1. Carbon and oxygen isotope results of shallow-water articulatedmodern brachiopods frompolar, temperate and tropical regions (adjusted for MgCO3 effects on carbon and oxygenisotopes; Jiménez-López et al., 2004, 2006; Brand et al., 2013 using the Mg content of shells/growth increments, Appendix 1). In modern and fossil brachiopods the negative isotope co-variation trendmay be ascribed to a kinetic effect (e.g., Gabitove et al., 2012), or to a diagenetic impact (cf. Brand and Veizer, 1981), or both. Shaded field represents calcite precipitated incarbon isotope equilibrium constructed with the dissolved inorganic carbon δ13C value of global seawater and the empirically determined enrichment factor (cf. Kroopnick, 1985;Romanek et al., 1992; see supplementary text for details).

82 U. Brand et al. / Chemical Geology 411 (2015) 81–96

et al., 1997). The apparent negative covariance noted for the brachio-pods may be simply an alignment of several populations from warmerand less productive waters. The cause of this carbon–oxygen isotopenegative co-variation in biogenic carbonates (with slopes rangingfrom 1.3 to 3.7) remains unresolved to this date (McConnaughey,2003) despite the advancement of carbonate and kinetic effect models(Spero et al., 1997; Adkins et al., 2003; Gabitov et al., 2012). It is not in-conceivable that brachiopods will precipitate shell calcite throughoutthe year and thus during times of variable temperature and productivi-ty, which are reflected by the observed co-variation in both δ13C andδ18O values. However, in ancient carbonates and biogenic calcite thenegative co-variation of δ13C and δ18O values often is ascribed to post-depositional alteration (e.g., Zhou and Xiao, 2007), but some studies ofdetailed horizon-by-horizon allochem and concurrent whole rock in-vestigations discount this as the operational parameter (cf. Brand,2004; Knauth and Kennedy, 2009; Brand et al., 2012).

The complex issue of proportional fractionation during calcification(cf. McConnaughey, 2003) may hamper using δ13C values of ancientbrachiopods as paleoceanographic proxies of Phanerozoic seawatercomposition and evolution (cf. Brand et al., 2009). Most studies circum-vent these issues by simply assuming a ‘case’ of equilibrium incorpora-tion for both isotopes in brachiopod calcite and/or by limiting studies toone or a few species, and assuming similarity between water masses(e.g., Veizer et al., 1986, 1999; Bates and Brand, 1991; Grossman et al.,1991). The use of the carbon isotope composition of ancient brachio-pods as a robust proxy of seawater composition is further complicatedby the apparent δ13C value — fabric relationship observed in extinctStrophomenata and extant Rhynchonellata by Garbelli et al. (2014),and thus, conclusions and interpretations of some studies of ancientbrachiopod δ13C values may need to be re-evaluated.

Carbon isotopes are an important proxy because they may reflectchanges in productivity of past oceans and the global carbon cycle asdocumented by carbon isotope excursions (CIEs) in marine carbonates(e.g., Saltzman, 2005; Azmy et al., 2014). In addition, they may providecritical information about atmospheric CO2 and greenhouse conditionsand their climatic relationship (e.g., Postma, 1964; Siegenthaler and

Münnich, 1981; Keeling et al., 1989; Brand et al., 2014), and have highpotential for tracing diagenetic events and hydrocarbon seep activities(cf. Brand and Veizer, 1981; Gischler et al., 2003). Brachiopods andtheir carbon isotopes hold great promise in unraveling many of theseprocesses in the Phanerozoic, especially for the Paleozoic. Unfortunate-ly, progress is hampered by the lack of knowledge of the type of frac-tionation process(es) governing carbon isotopes in this importantcarbonate archive (cf. McConnaughey, 2003). Experimental work pro-vides some information pertaining to the enrichment factors controllingthe carbon isotope distribution in calcite and aragonite. But many stud-ies are constrained by limitations of mineralogy, temperature, solutionchemistry, and precipitation rate (e.g., McCrea, 1950; Vogel, 1961;Rubinson and Clayton, 1969; Emrich et al., 1970;Mook et al., 1974). For-tunately, some of these issues have been resolved by the studies ofTurner (1982) and Romanek et al. (1992).

Turner (1982) conducted open-system calcite precipitation experi-ments and determined that the equilibrium calcite-bicarbonate enrich-ment factor (ε) may vary from 0.1 to 3.7‰ (this includes the full rangeof his observations). Similarly, Romanek et al. (1992) conducted open-system chemo-stat experiments to determine the effects of tempera-ture, mineralogy and rate of precipitation on δ13C values during calciteand aragonite formation. They found the calcite-bicarbonate enrich-ment (ε) to be independent of rate and temperature, and varied from0.56 to 1.52‰ (includes range of observationswithout attached errors).We adopted a weightedmean enrichment factor (ε) of 0.95‰ plus theirambient seawater δ13CDIC values to assesswhether articulated and someinarticulated brachiopods incorporate carbon isotopes into shell calcitein equilibriumwith ambient seawater (for detailed explanation of com-putations see Supplementary text). Thus,wewill be able to test for equi-librium incorporation of carbon isotopes by individual brachiopods inconjunction with their oxygen isotope equilibrium established byLowenstam (1961) and Brand et al. (2013; Fig. 2).

Our primary objective is to determine whether articulated brachio-pods incorporate carbon isotopes into shell calcite in equilibrium withseawater using a weighted mean enrichment (ε) factor determined byRomanek et al. (1992) and ambient seawater δ13C values of dissolved

83U. Brand et al. / Chemical Geology 411 (2015) 81–96

inorganic carbon. All carbon and oxygen isotope compositions will beadjusted for the Mg effect to ensure that resultant brachiopod δ13Cand δ18O values are more precise proxies of ambient environmentalconditions. Specifically, we plan to evaluate the carbon isotope fraction-ation property of the primary, secondary and tertiary layers in articulat-ed brachiopods. A secondary objective consists of evaluating carbonisotope variations in brachiopod shell calcite with respect to Mg con-tent, valve type, water depth, fabric – shell layer, ontogenetic locationand variation related to different local environmental conditions. An-other objectivewill evaluate an inarticulated brachiopod, after adjustingits carbon isotope compositions for the Mg effect, whether its shell cal-cite is in equilibrium with seawater.

2. Study material

Our results constitute part II of a greater study evaluating the isotopecompositions and elemental contents (Zaky et al., 2015) inmodern bra-chiopod shell calcite, and to establish baseline parameters for readingand evaluating fossil proxy data (cf. Brand et al., 2013). Only somemod-ern brachiopods of older studies are included in this study, because am-bient seawater δ13C values of dissolved inorganic carbon and/or shellMg content information may be lacking. Despite these issues, our data-base draws on the results of Wefer (1985), Carpenter and Lohmann,1995; Rao (1996), Marshall et al. (1997), Auclair et al. (2003), Brandet al. (2003), Parkinson et al. (2005), von Allmen et al. (2010),Yamamoto et al. (2010, 2013), Henkes et al. (2013), Takayanagi et al.(2013), and Came et al. (2014).

2.1. Brachiopods

A total of 428 shallow-water (b200 m, with some select deeperwater specimens) articulated plus 19 inarticulated brachiopods wereexamined for their carbon isotope compositions and Mg contents (Ap-pendix 1 — includes their δ18O values from Brand et al., 2013). The

150°

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60°

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120° 90° 30° 0°60°

60°

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Ocean

S o u t h

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Ocean

HudsonBay

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1,4,12

1,11

1

1,3

1,2

1,2,10,111,9 1

1,11

11

1,2,8,9

1,2,4,5

Fig. 2. Localities of modern brachiopods evaluated in this study (#1, solid dots and triangles, incet al. (2005), 3—Wefer (1985), 4— Carpenter and Lohmann (1995), 5— Auclair et al. (2003), 6(2013), 10— Marshall et al. (1997), 11— Came et al. (2014), and 12 — von Allmen et al. (2010

total brachiopod database (including supplements from other studies)covers twenty-seven localities from polar to tropical regions, and ambi-ent seawater temperature ranges from−2 to 32 °C, salinity from 29 to42, and they represent the Orders Rhynchonellida, Terebratulida,Thecideida and Craniida (Fig. 2, Table 1; see Supplementary Text andSuppl. Table 1 for additional information).

2.2. Seawater

Seawater was collected at eighteen of twenty-seven localities tocharacterize the δ13C values of dissolved inorganic carbon— all supple-mented by ambient water temperature, salinity and elemental contents(Appendix 2). Seawater was collected with a polyethylene Kemmerersampler closed by brass messenger for salinity, trace element content,and CDIC, δ13CDIC and δ18OSW values (Appendix 2). We tried to collectsamples at different times of the year to capture seasonal effects. Unfor-tunately this was not always possible and results of other studies out ofnecessity supplement our seawater database (see SupplementaryTable 2). Despite our best attempts, the constructed δ13CDIC fields areconsidered small snapshots of an integrated signal over the growth-time of brachiopods, and the limitation is considered in our interpreta-tions. To better define the natural variation, all possible seawater δ13CDICinformation was used in the construction of the equilibrium fields; fullydescribed in the Supplementary text.

2.3. Scanning electron microscope examination

Select specimens were examined by scanning electron microscope(SEM) to delineate their shell macro-, micro- and nanostructures (cf.Griesshaber et al., 2007; Goetz et al., 2009); this investigation is partof a larger study. Specimens were cut and polished with an Ultracut ul-tramicrotome, and polished surfaces were etched for 30–90 s with 2.5%glutaraldehyde and 0.01 mol/L MOPS buffer solutions. The etching pro-cess was stopped by washing specimens three times with 100%

90° 120° 150° 180°30° 60°

Pacific

OceanIndian

Ocean

e r n O c e a n

1

1

1

1,11

6

1,4,11

11

2

4

1,2,7

1,2,7

ludes some results from Brand et al., 2003); supplemented bymaterial from 2— Parkinson— Takayanagi et al. (2013), 7— Yamamoto et al. (2010), 8— Rao (1996), 9—Henkes et al.).

Table 1Locality summary of modern shallow-water articulated and inarticulated brachiopods(Appendix 1).

Locality Species Depth (m) Salinity

CanadaHudson Bay Hemithiris psittacea 10–20 29.7–32.6Bonne Bay H. psittacea 30 30.6–31.6

Terebratulina septentrionalis 30Bay of Fundy T. septentrionalis 15 32.2–32.3

BermudaNorth Rock Argyrotheca bermudana 10–12 36.3–37.1South Shore A. bermudana 37

A. bermudana 18 37.1Canary Islands

Palma Pajaudina atlantica 100Hispanirhynchia cornea* ~1343

JamaicaDiscovery Bay Thecidellina barretti 94 35.5

Grand CaymanOff Seaview Argyrotheca woodwardiana 20 36.4–38.0Off Eden Rock A. woodwardiana 10Off Soto's Dock Thecidellina barretti 8 37.4Off Galleon Beach A. woodwardiana 10

BarbadosPaynes Bay Argyrotheca lutea 137 37.3–37.4

Terebratulina cailleti 137 37.4Telegraph Station A. schrammi rubrotincta 54–127

VenezuelaNorth of Caracas Tichosina obesa 67–97

JapanSagami Bay Laqueus rubellus 84 34.5Otsuchi Bay Terebratulina crossei 70 33.3–34.0

U.S.A.Friday Harbor Hemithiris psittacea 85 30.5–30.7

Terebratulina unguicula 85Terebratalia transversa 85

PalauRock Island Thecidellina congregata 1–2 33.2–34.4

New ZealandDoubtful Sound Calloria inconspicua 1

Liothyrella neozelanica 15–22 34.8Notosaria nigricans 15–22Calloria inconspicua 15–22Terebratella sanguinea 15–22

Red SeaSharm el Sheik Cryptopora curiosa 8 40.6

C. curiosa 10Abu Sauatir C. curiosa 12 40.5

MaldivesGan Island Ospreyella sp. nov. 37 34.8–35.4Addu Atoll O. maldiviana 34

Europa Island Thecidellina blochmanni* 55South Africa

Kidds Beach Megerlina pisum 1–2 36.5Antarctica

Signy Island Liothyrella uva 12 32.9–34.7Weddell Sea Magellania fragilis 210–220 34.7Arthur Harbor Liothyrella notorcadensis* 15

PortugalSagres Novocrania anomala 20

ItalyISCA N. anomala 4 37.4–38.5

Note: * material and results from Brand et al. (2003).

84 U. Brand et al. / Chemical Geology 411 (2015) 81–96

isopropanol alcohol. Dried specimens were rotary shadowed with3–4 nmplatinumat an angle of 45° and analyzed at 4.0 kVwith aHitachiS-5200 Field Emission SEM (Griesshaber et al., 2007).

2.4. Analytical methods

Epibionts, organic tissue and periostracum of brachiopods weremanually removed from the interior and exterior of the valves, theseand other contaminants were removed with a razor blade or by millingthe surface clean with a minidrill. Subsequently, shells were immersed

in 10% (v/v) HCl to remove surface contaminants, but also to dissolveand remove the primary layer and transition zone calcite (cf. Brandet al., 2012, 2013). Finally, clean shells were rinsed with distilledwater and left to air dry before further processing. Depending on size,shells were sub-sampled with a minidrill (WE-Cheer WE 248) andtungsten carbide drill bits to capture their ontogenetic variation follow-ing along the growth increment axis (cf. Lee et al., 2004; Appendix 1).

5–20 mg of powder was digested in 7–10 mL of 2% (v/v) HNO3 (dis-tilled) and analyzed on a Varian 400P atomic absorption spectropho-tometer (AAS) for trace element content (cf. Brand et al., 2012, 2013).Precision and accuracy are better than ± 5% compared to certifiedvalues for Ca andMg of NBS (NIST) SRM633 (N= 78). Aliquots of sam-ples were also analyzed for their carbon and oxygen isotope composi-tions (Appendix 1). Each sample was reacted with ultrapure 100%orthophosphoric acid at 70 °C and analyzed in a Thermo-FinniganDelta V+ isotope ratio mass spectrometer. Reproducibility of δ13Cvalues of NBS-19 standard rock material is within 0.05‰ (1σ) V-PDB.Procedures, standards, reproducibility, and standards for δ18O valueswere fully described by Brand et al. (2013).

Seawater destined for dissolved inorganic carbon (DIC) and carbonisotope composition of DIC analyses was either filtered through a0.45 μm PCTE membrane filter (Supor™; cf. Wassenaar et al., 1990;Beirne et al., 2012) or poisoned with saturated HgCl to suppress micro-biological activity (cf. Kroopnick, 1985). Water temperature was mea-sured with a Fish Hawk TD probe and a NIST calibrated thermometer.Water aliquots were stored in 50mL brown borosilicate vials and septalcaps fitted with extra PTFE-rubber discs to limit gas diffusion, kept cooland in the dark until analysis. Carbon isotope analysis employed thefastest possible turn-around time from time of collection (usually with-in aweek or two atmost). Salinitywasmeasured, in the lab, with aHachSensION5 meter calibrated to 35 ppt. Separate brown borosilicate vialsof seawater were collected each for trace element and oxygen isotopeanalyses (cf. Brand et al., 2013). Trace elements were analyzed on aVarian 400P AAS and results of standard solutions (Delta High PurityStandards) were within ±4.5% of certified values.

δ13CDIC (V-PDB) and δ18O values of seawater (V-SMOW, cf. Brandet al., 2013) were analyzed by the G.G. Hatch Isotope Lab, Departmentof Earth Sciences, University of Ottawa, Canada. The dissolved inorganiccarbon (DIC) and δ13CDIC (V-PDB) were measured on an OI Analytical“TIC-TOC” Analyzer Model 1030 interfaced to a Finnigan Mat DeltaPlusisotope ratio mass spectrometer for analysis by continuous flow (St.Jean, 2003). DIC determination consists of, 1) sample acidificationwith 5% H3PO4 to convert DIC into CO2, 2) moisture removal fromgaseswithNafion™ tubing and indicating desiccant, 3) CO2 is thenmea-sured by a NDIR (non-dispersive infra-red detector) for concentration,and 4) CO2 is then sent to the continuous-flow isotope-ratio mass spec-trometer for δ13C analysis (St. Jean, 2003). Data were normalized usinginternal standards (Potassium biphatalate (KPH) and Sucrose-1; St.Jean, 2003), and the 2σ analytical precision is 2% for the quantitativecarbon analyses, and ± 0.2‰ for δ13CDIC values. Reproducibility of rep-licate analyses is better than 0.01‰ for δ13CDIC values (V-PDB; Appendix2). For further standard, sample preparation and analytical proceduressee St. Jean (2003).

3. Evaluation of carbon isotope compositions

Recently, Brand et al. (2013) confirmed that articulated brachiopodsas a group incorporate oxygen isotopes into shell calcite in equilibriumwith ambient seawater (cf. Lowenstam, 1961), but questioned byTakayanagi et al., 2013, nevertheless which makes them (modern andfossils) powerful archives and proxies of seawater temperature and iso-tope composition, and tracers of the thermal evolution of seawater.However, the status of the carbon isotope incorporation by brachiopodsremains unresolved (e.g., Wefer, 1985; Carpenter and Lohmann, 1995;Brand et al., 2003; Parkinson et al., 2005; Yamamoto et al., 2010;

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Bermuda

δ13 C

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δ18O (‰)

-2Walsingham PondNorth ShoreSouth ShoreA. bermudana

Fig. 3. Carbon and oxygen isotope results of open-ocean articulated brachiopods off Ber-muda and counterparts from Walsingham Pond, Bermuda. Results of this study and ofBrand et al. (2003) are adjusted for the respective MgCO3 effects on carbon and oxygenisotope compositions (δ13C values by 0.024‰ /mol% MgCO3 and δ18O values by 0.17‰/mol% MgCO3; Jiménez-López et al., 2004, 2006; Brand et al., 2013 using the Mg contentof shells/growth increments, Appendix 1). Walsingham Pond brachiopod isotope resultsare fromWefer (1985). Equilibrium fields are based on seawater δ13C dissolved inorganiccarbon values of a) open ocean locality and b) fromWalsingham Pond, of Bermuda, andthe weighted mean enrichment factor (ε) of Romanek et al. (1992), and the oxygen iso-tope equilibrium parameters are from Brand et al. (2013). Construction of the carbonand oxygen isotope equilibrium field is further described in the supplementary text.

85U. Brand et al. / Chemical Geology 411 (2015) 81–96

Takayanagi et al., 2013), but we hope to address this in the presentstudy.

Generally, we construct cross plots to identify either vital effects(metabolic or kinetic) or preservation/alteration of isotopic composi-tions in whole rock and fossil material (includingmodern counterparts;e.g., Brand and Veizer, 1981; Grossman et al., 1991; Carpenter andLohmann, 1995; Brand, 2004; Mii et al., 2013). It may be a convenientway of identifyingmajor issues but it masks local processes and naturaloceanographic variations. Fig. 1 is a compilation of the modern brachio-pod database classified bymajor climatic regionswithmost results clus-tering between 0 to 3‰, and it is punctuated by several negativecovariation trends between δ13C and δ18O values. Generally, thedepicted trendsmay be interpreted to represent diagenetic trends or ki-netic fractionation or both (e.g., Brand and Veizer, 1980; Auclair et al.,2003; Gabitov et al., 2012). Furthermore, if we assume global values(upper and lower limits; Anderson and Arthur, 1983) for the δ13CDIC

and a general enrichment factor of 1‰, the majority of our brachiopodswould be deemed to precipitate carbon isotopes in disequilibrium withambient seawater (Fig. 1). We shall address this concern by examiningindividual brachiopod populationswhile considering their ambient sea-water δ13CDIC values,Mg contents and isotope compositions of shells (cf.McConnaughey, 1989a, b; Brand et al., 2013).

3.1. Carbon isotopes: equilibrium evaluation

To determine whether brachiopods incorporate carbon isotopes inequilibrium into shell calcite with seawater, all isotope results were ad-justed for the Mg-effect to be more precise proxies of environmentalconditions based on the assessment by Brand et al. (2013). Specifically,the carbon and oxygen isotope compositions of all brachiopod materialwere adjusted by 0.024 and 0.17‰/mol% MgCO3, respectively(Jiménez-Lopez et al., 2004, Jiménez-López et al., 2006, and Brandet al., 2013) using the concurrently analyzedMg contents of the studiedmaterial (Appendix 1). Armed with this information we constructedequilibrium fields for seawater δ13C and δ18O (the constraints for thelatter are from Brand et al., 2013) for individual brachiopod populationsand used them to evaluate whether carbon isotope compositions ofshells, or their specific growth increments are in equilibriumwith ambi-ent seawater (for details of construction of equilibrium fields see sup-plementary text).

3.2. Case study — Bermuda

Lowenstam (1961) concluded that articulated brachiopods incorpo-rate oxygen isotopes into shell calcite in equilibrium with ambient sea-water, whereas Wefer (1985) suggested that their carbon isotopecomposition was in steep disequilibrium with seawater. Interestingly,the brachiopods studied by Wefer (1985) did not come from the openocean but fromWalsingham Pond an anchialine pondwith bottom sed-iments rich in organic detritus and surrounded by a massive vegetativecover (Thomas et al., 1991). We believe that the landlocked nature andhigh organic matter content of the sediments may have a significant in-fluence on the isotope compositions of the brachiopods studied byWefer (1985).

A re-examination of Bermuda brachiopods was considered a prima-ry focus of our study. A number of specimens of Argyrotheca bermudanawere collected from the south and north shore reef zones of the Bermu-da Platform (Coates et al., 2013), and their δ13C and δ18O values are plot-ted in Fig. 3 in addition to those from Walsingham Pond collected byWefer (1985). The isotope results of the open ocean reefal-zone bra-chiopods fall into the isotope equilibrium field constructed for offshoreBermuda seawater whereas those from Walsingham Pond fall wellbelow it. Examination of the dissolved inorganic carbon and carbon iso-tope compositions of Walsingham Pond seawater suggest equilibriumparameters are shifted towards more negative values for carbon butonly slightly for oxygen isotopes (Fig. 3). This clearly demonstrates the

need for constructing equilibrium fields for each and every site beforemaking an assessment and interpretation about the carbon and oxygenisotope compositions of brachiopod populations. The oxygen isotopeobservations for the open sea and the pond agree with their respectivesalinities and temperatures (Appendix 2; Thomas et al., 1991; Coateset al., 2013), and point to the big difference in organic matter contentof the ambient sediments (Thomas et al., 1991) as an influencing factoron the carbon isotope composition. Our results confirm that1) A. bermudana incorporates carbon and oxygen isotopes into shell cal-cite in near equilibriumwith ambient seawater (open ocean and pond),and 2) to establish equilibrium fractionation it is critical that ambientseawater parameters are used in the evaluation process. Since, speci-mens of A. bermudana are quite small it was only possible to conductbulk elemental and isotopic analyses. Thus, the question as to whetherall or some brachiopod shell layers (primary, secondary and/or tertiary)are in carbon isotope disequilibrium or equilibrium with seawater re-mains to be addressed.

3.3. Shell layer fractionation

Carpenter and Lohmann (1995) demonstrated that primary layercalcite of brachiopods is deposited in oxygen isotope disequilibriumwith ambient seawater, with a similar observation inferred for their car-bon isotopes. Subsequent studies by other authors appear to supporttheir conclusion of carbon isotope disequilibrium with the exception

86 U. Brand et al. / Chemical Geology 411 (2015) 81–96

of Takayanagi et al. (2013). The brachiopod fauna from Friday Harborrepresents an ideal population for an in-depth analysis because of themany detailed studies by authors (Carpenter and Lohmann, 1995;Auclair et al., 2003; Parkinson et al., 2005, and this study). Based on sea-water parameters, we are able to define a field for calcite precipitated incarbon and oxygen isotope equilibrium with ambient seawater off Fri-day Harbor (Fig. 4; cf. Brand et al., 2013). The large population ofTerebratulina transversa, from multiple studies, is ideal for assessingthe equilibrium incorporation of both carbon and oxygen into shell cal-cite of their primary and secondary layers with ambient seawater. It isclear from Fig. 4 that the δ13C and δ18O values, with few exceptions, ofthe primary layer of T. transversa fall well outside the constructed equi-librium field and become increasingly negative with decreasing waterdepth. In contrast, most δ13C and δ18O values of secondary layer calciteof all studies fall within the constructed equilibrium field.

We propose that the isotope anomalies noted in some secondarylayer calcite of T. transversa (Fig. 4)may be attributable to incorporationof disequilibrium carbon and possibly oxygen isotope compositionsfrom transition zone calcite. The contact between primary layer calciteand secondary layer fibers in most instances is highly irregular butsharp (Fig. 5a), whereas in some other instances it is irregular and gra-dational. This gradational interval documents the transition from den-dritic calcite of the primary layer to the fibers of the secondary one(Fig. 5b; cf., Schmahl et al., 2004; Goetz et al., 2009; Griesshaber et al.,2007). Yamamoto et al. (2010) found that calcite of the innermostpart of the secondary layer is in carbon and oxygen isotopic disequilib-riumwith seawater, whichmay be equivalent to the transition zone cal-cite of this study.

-215.5 8°C

-3

-4

-5

-6

-1

0

+1

-2-3-4 -1 0 +1

δ13 C

(‰

)

δ18O (‰)

this study (85m)

T. transversa

C&L (SL)

P (SL)

A (SL)

C&L (PL; 24m)

P (PL; 45m)

A (PL; intertidal)

Friday Harbor, U.S.A.

Fig. 4. Evaluation of carbon and oxygen isotope compositions in the modern brachiopodTerebratulina transversa from Friday Harbor, U.S.A. Supplementary material (TZ — transi-tion zone; PL — primary layer; SL — secondary layer) is from Carpenter and Lohmann(1995; C&L), Auclair et al. (2003; A), and Parkinson et al. (2005; P). Isotope adjustmentsand equilibriumfield construction are asdescribed in Fig. 3, and in the supplementary text.

Two other brachiopods, Hemithiris psittacea and Terebratulinaunguicula, from Friday Harbor were also studied for their geochemicalcontents including stable isotope compositions. The secondary layer car-bon and oxygen isotope results of this study and those of Carpenter andLohmann (1995) are presented in Fig. 6, and most results fall within thecarbon-oxygen isotope equilibrium field constructed for ambient seawa-ter. Although, the isotope results of Carpenter and Lohmann (1995) coin-cide with the equilibrium field, the δ13C values tend to be slightly morepositive than of the specimens collected for this study (Fig. 6a, b). Theonly difference between the two populations is in their respective waterdepths and/or time of collection, which may account for the slight δ13Cvariations observed between the two datasets. Overall though, the resultsconfirm that the carbon and oxygen isotope compositions of secondarylayers of subtidal H. psittacea, T. transversa and T. unguicula from FridayHarbor were incorporated into shell calcite in near equilibriumwith am-bient seawater (Fig. 6), while the carbon and oxygen isotope composi-tions of the primary layer and transition zone are definitely indisequilibrium (Fig. 4; cf. Carpenter and Lohmann, 1995). Thus, we haveunequivocal proof that carbon and oxygen isotope compositions of pri-mary layer calcite in articulated brachiopods should not be used forpaleoclimatological or paleoceanographic investigations.

3.4. Shell valve evaluation

A number of brachiopods from seven localities were evaluated as towhether the δ13C and δ18O values of secondary and/or tertiary layers ofdorsal (brachial) and ventral (pedicle) valves represent uniform andequilibrium biomineralization with seawater. Specimens used in thisanalysis are grouped according to valve specified under heading ‘shellincrement’ in Appendix 2. The statistical p value of the examinationsfor dorsal–ventral pairs ranges from 0.950 to 0.173, with only two ex-ceptions and p values of less than 0.050 (Table 2). The Δ13C differencefor the first group ranges from 0.0 to 0.18‰ between dorsal and ventralvalves, but it climbs to 0.31‰ for the valves of T. unguicula from FridayHarbor and to 1.45 of those of Terebratulina septentrionalis from BonneBay (Table 2). The first exception is relatively small and may be, inpart, related to analytical and/or sampling bias, whereas the differencebetween the dorsal and ventral valves of T. septentrionalis from BonneBay is a mystery especially since the same valves of the same speciesfrom the Bay of Fundy are in general agreement (Table 2). Despite theexceptions, we conclude that dorsal (brachial) and ventral (pedicle)valves (based on secondary and tertiary layers) of modern articulatedbrachiopods incorporate carbon isotopes into shell calcite in near equi-librium with ambient seawater, and will be treated as one database.

4. Brachiopod population evaluation

4.1. North Atlantic Ocean

Brachiopods and seawater were collected from Bonne Bay and theBay of Fundy to evaluate the physicochemical conditions for incorporat-ing carbon isotopes into shell calcite with North Atlantic seawater(Fig. 2). The δ13C and δ18O values of the brachiopods H. psittacea andT. septentrionalis from Bonne Bay fall within the isotope equilibriumfield for shell calcite precipitated in near equilibriumwith ambient sea-water (Fig. 7a). Similarly, the δ13C and δ18O values of T. septentrionalisfrom the Bay of Fundy and those of Brand et al. (2003) and of vonAllmen et al. (2010) fall within its site-specific isotope equilibriumfield with ambient bay seawater (Fig. 7b). Furthermore, the δ13C resultsof secondary layer calcite of T. septentrionalis of Carpenter and Lohmann(1995) overlap with the results of our study, but those of the primarylayer are more negative and fall outside the equilibrium field, and thusclearly were precipitated in disequilibrium with ambient seawater(Fig. 7b). The mean δ13C value of the brachiopods from the two NorthAtlantic localities amounts to +1.10 ± 0.57‰ (Table 2), and is similarto the value of +1.3 ± 0.8‰ determined by Brand et al. (2003) for

A

Primary Layer

Secondary Layer

B 1 µm2 µm

Primary Layer

Secondary Layer

TZ

Fig. 5. Scanning electron microstructural analysis of modern Terebratalia transversa andMegerlia truncata shell layers. Panel (a) shows the sharp but highly irregular contact between thedendritic calcite of the primary layer and the fibers of the secondary layer in Terebratalia transversa. Panel (b) shows the highly irregular and gradational contact, termed the TransitionZone' sandwiched between the primary layer calcite and the sharp and well-defined fibers of the secondary layer inM. truncata.

87U. Brand et al. / Chemical Geology 411 (2015) 81–96

North Atlantic brachiopods, and thus, their carbon isotope compositionsrepresent near equilibrium conditions with their respective ambientseawater.

4.2. Caribbean Sea and Canary Islands

Articulated brachiopods were collected from Jamaica, CaymanIslands and Barbados in the Caribbean, and from the Canary Islands inthe Atlantic for stable isotope investigation (Fig. 8). The species,Thecidellina barretti from Jamaica was examined by Parkinson et al.(2005), Henkes et al. (2013) and in this study for their carbon and oxy-gen isotope compositions. The δ13C values of the brachiopod specimensdefine two distinct areas but only the ones of our study fall within theconstructed isotope equilibrium field (Fig. 8a). Our δ13C and δ18O valueswere adjusted for the Mg effect (cf. Brand et al., 2013) whereas those ofParkinson et al. (2005) and Henkes et al. (2013) were not, since the au-thors provided no Mg content information. This readily explainsthe ~ +1.5‰ offset in δ18O values and the slight offset in δ13C values,and more importantly without the Mg adjustment calculated ambientseawater temperatures would be lower than measured ones for thesampling sites in Jamaica. These observations and conclusions support

-2

-1

0

+1

+2

-2 -1 0 +1 +2

Friday Ha

δ13 C

(‰

)

δ18

this study (85 m)

H. psittacea

C&L (24 m)

(a)

Fig. 6. Evaluation of carbon and oxygen isotope compositions themodern brachiopodsHemithirterial (secondary layer, C&L) are from Carpenter and Lohmann (1995). Sample preparation, isotplementary text.

the need for Mg adjustment for these biogenic carbonates with the re-cently proposed oxygen isotope thermometer (cf. Brand et al., 2013).

Two species of brachiopods were tested for their shell δ13C and δ18Ovalues from the Cayman Islands, and their isotope compositions wereadjusted for the Mg effect (Brand et al., 2013). Similar to the specimensfrom Jamaica, the unadjusted populations and their δ13C and δ18Ovalues are from significantly to slightly more positive than their adjust-ed counterparts (Appendix 1). The slight differences in δ13C and δ18Ovalues between Argyrotheca woodwardiana and T. barrettimay be relat-ed to differences in sites and water depths they occupy in the offshorewaters of the Cayman Islands (Appendices 1, 2).

Similarly, the δ13C values of the three brachiopod species fromBarbados, including the δ13C value of Came et al. (2014) fall withintheir site-specific equilibrium field. The small differences in isotopevalues between Argyrotheca schrammi rubrotincta and Argyrothecalutea and Terebratulina cailleti reflect differences in water depths =water temperature (Fig. 8c; Appendix 2). Overall, our δ13C values ofthe Caribbean brachiopods cluster about +2.03 ± 0.31‰ reflectingthe relative constancy of seawater δ13CDIC observed throughout the Ca-ribbean for open ocean settings (Kroopnick, 1985).

Two brachiopods, Pajaudina atlantica and Hispanirhynchia cornea,from the Canary Islands were investigated for their carbon and oxygen

+2

+1 +2

rbor, U.S.A.

O (‰)

-2

-1

0

+1

-2 -1 0

this study (85 m)T. unguicula

C&L (24 m)

(b)

is psittacea (a), and Terebratalia unguicula (b) from FridayHarbor, U.S.A. Supplementalma-ope adjustments and equilibrium field(s) are as described in Figs. 3, and 4, and in the sup-

Table 2Statistical (ANOVA) analysis of carbon isotopes in modern shallow-water brachiopodvalves from various localities. Evaluation of the same/different species and valves (d =dorsal [brachial]; v = ventral [pedicle]) with significance (p) at the 95% confidence inter-val, and absolute difference between means of valves (Δ13C).

Species valve N δ13C SD p Δ13C

BarbadosTh. cailleti d 8 +1.97 0.12 0.946 0.00

v 8 +1.97 0.17Bay of Fundy

T. septentrionalis d 22 +1.01 0.29 0.508 0.06v 22 +0.95 0.23

Bonne BayH. psittacea1 d 5 +1.54 0.18 0.1731–2 0.18T. septentrionalis2 d 6 +1.72 0.23T. septentrionalis3 v 7 +0.27 0.71 0.0012–3 1.45

Friday HarborH. psittacea d 10 −0.88 0.45 0.614 0.12

v 12 −0.76 0.55T. unguicula d 11 −0.21 0.30 0.036 0.31

v 12 −0.52 0.38T. transversa d 17 −0.55 0.53 0.563 0.10

v 20 −0.65 0.59Palau

T. congregata d 8 +0.84 0.33 0.950 0.01v 5 +0.85 0.29

Doubtful SoundL. neozelanica d 5 +2.46 0.25 0.773 0.04

v 5 +2.50 0.21N. nigricans d 3 +1.33 0.17 0.379 0.13

v 3 +1.20 0.15T. sanguinea d 5 +1.25 0.23 0.255 0.16

v 6 +1.09 0.23C. inconspicua d 2 +1.37 0.06 ND 0.13

v 2 +1.24 0.18Signy Island

L. uva d 6 +1.22 0.29 0.676 0.07v 6 +1.15 0.25

Note: N— number of results, δ13C—mean value, SD— standard deviation, all δ13C valuesadjusted for Mg effect. p values in bold are the exceptions; superscript numbers refer tospecies from Bonne Bay.

88 U. Brand et al. / Chemical Geology 411 (2015) 81–96

isotope compositions (Fig. 8d). These brachiopods retain their δ13C andδ18O differences, despite the fact that isotopes of both species were ad-justed for the Mg effect. The Canary Islands are in a zone of upwelling

-3

-2

-1

0

+1

+2

+3

+4

δ13 C

(‰

)

δ1

-3 -2 -1 0 +1 +2

Bonne Bay, Canada (a)

T.septentrionalisH.psittacea

Fig. 7. Evaluation of carbon and oxygen isotope compositions in modern brachiopods from Boisotope results of Brand et al. (2003) and von Allmen et al. (2010) areMg effect adjusted (cf. Braand Lohmann (1995), and with noMg contents offered by the authors' isotope results are not Mdescribed in Figs. 3, 4 and 5, and in the supplementary text.

water (Hernandez-Guerra et al., 2003) and the fauna from Brand et al.(2003) is from a depth of ~1340 m and the one of this study and fromCame et al. (2014) is from 100 m. Thus, the δ18O and δ13C values ofthe two brachiopod populations off the Canary Islands clearly demon-strate differences in water temperature and productivity with waterdepth. The brachiopods from the nutrient-depleted shallow water dueto phytoplankton productivity trend towards more positive δ13C values(Fig. 8d; Ciais et al., 1995).

Overall, our δ13C and δ18O values withMg effect adjustment confirmprecipitation in near isotope equilibriumwith seawater for the shallow-water brachiopod fauna from the Canary Islands and those from otherlocalities in the Caribbean.

4.3. Red Sea and Indian Ocean

Modern brachiopods from the Red Sea and Indian Ocean are under-represented in the geochemical literature, in part, reflecting their smallsize and paucity in the marine environment (Fig. 2). Brachiopods fromseveral localities within the Red Sea represent different water depths,but the δ13C values of Cryptopora curiosa from shallow water fall intothe constructed equilibrium field with some exceptions (Fig. 9a). Themore positive δ13C values probably reflect the lack of DIC datarepresenting the full growth conditions for the brachiopods from theRed Sea.

The isotope compositions of Indian Ocean brachiopods from theMaldives and Europa Island (Fig. 2, Brand et al., 2003) fall within theirrespective equilibrium fields after due consideration for the effect ofMg content on their δ13C and δ18O values (Fig. 9b, c). Overall, their col-lective δ13C value of +1.42 ± 0.47‰ is similar to the value reported byBrand et al. (2003; +1.3 ± 0.6‰) for Indian Ocean brachiopods, butmore importantly it suggests that they incorporate carbon isotopesinto shell calcite in near equilibrium with ambient seawater.

The brachiopod, Megerlina pisum, from the coast of South Africa in-habits the intertidal zone at Kidds Beach (Fig. 2). Either, we have insuf-ficient δ13CDIC data and/or this brachiopod species incorporates carbonand oxygen isotopes in disequilibrium, which is highly unlikely in theface of the overwhelming evidence supporting equilibrium incorpora-tion for articulated brachiopods. Thus, more work is needed on brachio-pods from the intertidal zone.

-3 -2 -1 0 +1 +2 +3

Bay of Fundy, Canada (b)

C&L (secondary layer)von Allmen et al.

C&L (primary layer)Brand et al. (SL)

T.septentrionalisthis study (SL)

8O (‰)

+3

nne Bay (a) and the Bay of Fundy (b), Canada, North Atlantic. Supplemental material andnd et al., 2013). C&L are brachiopod results (primary and secondary layers) from Carpenterg effect adjusted. Sample preparation, isotope adjustments and equilibrium field(s) are as

0

+1

+2

+3

+4

0

+1

+2

+3

+4

-4 -3 -2 -1 0

Jamaica (a)

-4 -3 -2 -1 0

Cayman Islands (b)

-2 -1 0 +1 +2 -2 -1 0 +1 +2

Barbados (c) Canary Islands (d)δ13 C

(‰

)

δ18O (‰)

Parkinson et al.Henkes et al.

this studyTh. barretti

Th. barrettiA. woodwardiana

T. cailletiA. schrammiCame et al.

A. lutea

Brand et al.P. atlantica

Came et al.

Fig. 8. Evaluation of carbon and oxygen isotope compositions in modern brachiopods from Jamaica (a), Cayman Islands (b), Barbados (c) and the Canary Islands (d). Isotope results ofParkinson et al. (2005) and Henkes et al. (2013) represent supplemental material from Rio Bueno, Jamaica (with no Mg content offered by authors, isotope results are not Mg effect ad-justed). In contrast, Came et al. (2014) isotope results areMg effect adjusted. Canary island brachiopods of Brand et al. (2003) are from awater depth of about 1343m. Sample preparation,isotope adjustments and equilibrium field(s) are as described in Figs. 3, 4 and 5, and in the supplementary text.

89U. Brand et al. / Chemical Geology 411 (2015) 81–96

4.4. Pacific Ocean

This section deals with tropical and temperate brachiopods fromPalau, Sagami and Otsuchi Bays of Japan and Doubtful Sound of NewZealand (Fig. 2), all supplemented by results of other studies(Carpenter and Lohmann, 1995; Parkinson et al., 2005; Yamamotoet al., 2010, 2013; Came et al., 2014). The isotope equilibrium field forSagami Bay brachiopods (Fig. 10a) is based on seawater δ13CDIC data ofYamamoto et al. (2010) and the data for the δ18O range are fromBrand et al. (2013). The δ13C values of our brachiopod Laqueus rubellus(using results exclusively from the secondary layer) fall within thelower end of the equilibrium field (Fig. 10a). Also, the δ13C values ofthe material from the shell ‘Depth’ sampling strategy place the resultsof Yamamoto et al. (2010) within the equilibrium field (Fig. 10a),which is at odds with the conclusion of Yamamoto et al. (2010). Theydeemed their δ13C results to be in disequilibrium with seawater, butthis may be related of how they evaluated individual calcite δ13C valuesand compared them to an average enrichment value for isotope equilib-rium. Instead, with due consideration of all factors (range of seawaterδ13CDIC), we consider all δ13C and δ18O values for L. rubellus from SagamiBay to be in near carbon and oxygen isotope equilibrium with ambientseawater.

The δ13C values of Terebratulina crossei and Terebratalia coreanicafrom Otsuchi Bay using exclusively secondary layer results of this

study, Parkinson et al. (2005; range of values) and Yamamoto et al.(2013) fall within the isotope equilibrium field with seawater(Fig. 10b; δ18O parameters from Brand et al., 2013). Yamamoto et al.(2013, their fig. 3) considered the δ13C results for T. coreanica to be indisequilibrium with seawater and somewhat for T. crossei. Similar tothe argument presented above for the Sagami Bay brachiopods, we con-sider their equilibrium parameter of just an average value to be too re-strictive since it does not encompass the total variation in seawaterδ13CDIC values. Since all, except for one data point, fall within the con-structed isotope equilibrium field (Fig. 10b), we consider all δ13C andδ18O values of T. coreanica and T. crossei from Otsuchi Bay to be in nearisotope equilibrium with ambient seawater.

Brachiopods studied from Palau are exclusively Thecidellinacongregata and their δ13C values form two clusters (one for this study in-cludes those of Came et al., 2014, and one for the results of Carpenterand Lohmann, 1995). The δ13C and δ18O values of the former populationoverlaps with the isotope equilibrium field with ambient seawater,whereas the latter ones do not (Fig. 10c). Previously, T. congregata wasdeemed to precipitate shell carbonate in δ18O disequilibrium with re-spect to ambient seawater, and with a similar inference for their δ13Cvalues (e.g., Carpenter and Lohmann, 1995; Parkinson et al., 2005).However, this brachiopod has shells with Mg contents as high as8.55mol%MgCO3 (Appendix 1), andwith 0.17 and0.024‰ enrichmentsper mol% MgCO3 for δ18O and δ13C values, respectively, this may cause

0

+1

+2

+3

+4

-2 -1 0 +1 +2-4 -3 -2 -1 0

Red Sea (a) Maldives (b)

δ13 C

(‰

)

δ18O (‰)

Maldives, this studyBrand et al., 2003

0

+1

+2

+3

+4Europa Island (c)

-1

0

+1

+2

+3South Africa (d)

Megerlina pisumCame et al.Brand et al.

C. curiosa

Fig. 9. Evaluation of carbon and oxygen isotope compositions in modern articulated brachiopods from the Red Sea (a), Maldives (b), Europa Island (c) and South Africa (d). The brachio-pods from the Maldives, Europa Island (including Came et al., 2014) and South Africa are presented as Mg adjusted δ13C and δ18O values. Sample preparation, isotope adjustments andequilibrium field(s) are as described in Figs. 3, 4 and 5, and in the supplementary text.

90 U. Brand et al. / Chemical Geology 411 (2015) 81–96

significant shifts in isotope compositions (Jimenez-Lopez et al., 2004,Jiménez-López et al., 2006; Brand et al., 2013). TheMg effect readily ex-plains the difference in the isotopic values for T. congregata of this studyand Came et al. (2014) and of those obtained by Carpenter andLohmann (1995), because only the Mg-adjusted database falls withinthe isotope equilibrium field (Fig. 10c). Thus, we consider the carbonand oxygen isotope compositions of shells of this thecideid brachiopodto be in equilibrium with ambient seawater (cf. Brand et al., 2013).

New Zealand waters are home to large and diverse brachiopod pop-ulations (Lee et al., 2011). Isotope results of our subtidal brachiopodpopulation from Doubtful Sound fall within and outside the isotopeequilibrium field with seawater and form two distinct clusters(Fig. 10d). Cluster 1 is comprised of Liothyrella neozelanicawith an aver-age δ13C value of +2.46 ± 0.23‰, while cluster 2 is comprised ofNotosaria nigricans, Calloria inconspicua and Terebratella sanguineawith an average δ13C value of +1.21 ± 0.20‰ (Appendix 1). The fourbrachiopod species were collected at a single location and water depthto exclude extrinsic environmental factors. The four brachiopods havesimilar shell growth rates of 3.5 to 5 mm/y (Baird et al., 2013) andthat excludes this parameter as a controlling factor. Otherwise, the bra-chiopod of cluster 1 secretes shells with primary and tertiary layerswhereas the brachiopods of cluster 2 secrete shells with primary andsecondary layers (Parkinson et al., 2005). Furthermore, the brachiopodsof cluster 2 have similar spawning periods while brachiopod of cluster 1spawns earlier in the year than the others (Lee et al., 2011; Baird et al.,

2013). Based on their spawning period and δ18O values, L. neozelanicatend to preferentially precipitate their shells during the cooler parts ofthe year, whereas those of cluster 2 preferentially precipitate shell cal-cite throughout the year (Fig. 10d). Overall, we consider the δ13C andδ18O values of the secondary layer of N. nigricans, C. inconspicua andT. sanguinea from Doubtful Sound to be in near isotope equilibriumwith their ambient seawater, whereas more work is needed to charac-terize and identify the reasons behind the offset in δ13C and δ18O valuesfor the tertiary layer of L. neozelanica.

4.5. Arctic and Southern Oceans

Few studies with stable isotope results are available for brachiopodsfrom the Arctic Ocean or associated water bodies such as Hudson Bay(ACIA, 2005) and from the Southern Ocean. Fortunately, this limitationis being alleviated by the recent studies of Carpenter and Lohmann(1995), Marshall et al. (1997), Brand et al. (2003, 2013, 2014),Parkinson et al. (2005), Henkes et al. (2013), and Came et al. (2014).

The δ13C values of the secondary layer of several specimens ofH. psittacea collected in 2010 from offshore Churchill (Hudson Bay)fall within the isotope equilibrium field constructed for this specific lo-cality and seawater (Fig. 11a). In contrast, Liothyrella uva from Signy Is-land and their isotope results depict a complex scenario that suggestsincorporation of δ13C and δ18O values into shell calcite in equilibriumby some and in disequilibrium by some others with ambient seawater

0

+1

+2

+3

+4

-5 -4 -3 -2 -1 -1 0 +1 +2 +3

+3 +4 00 +1+1 +2+2 +3 +4

Sagami Bay, Japan (a) Otsuchi Bay, Japan (b)

δ13 C

(‰

)

δ18O (‰)

Yamamoto et al.this studyL. rubellus

T. c. (Yamamoto et al.)T. crossei (this study)

T. coreanica (Yet al.)

-1

0

+1

+2

+3 +4

+3

+2

+1

0

+4

+3

+2

+1

0

Palau (c) Doubtful Sound, NZ (d)

L. neozelanicaN. nigricansC. inconspicuaT. sanguinea

C&Lthis study

Th. congregata

Parkinson et al.

Parkinson et al.

Came et al.

Fig. 10. Evaluation of carbonand oxygen isotope compositions inmodern brachiopods fromSagamiBay (a), Otsuchi Bay (b), Palau (c) andDoubtful Sound (NewZealand; d). Supplementalmaterial Y and C&L are from Yamamoto et al. (2010, 2013) and Carpenter and Lohmann (1995), respectively, as well as from Parkinson et al. (2005) and from Came et al. (2014). Samplepreparation, isotope adjustments and equilibrium field(s) are as described in Figs. 3, 4 and 5, and in the supplementary text.

91U. Brand et al. / Chemical Geology 411 (2015) 81–96

(Fig. 11b). L. uvaprecipitates shellswith primary, secondary and tertiarylayers, with tertiary layer development being incomplete (Parkinsonet al., 2005,fig. 3c). The isotope results of Fig. 11b are from four studies—Marshall et al. (1997), Parkinson et al. (2005), Came et al. (2014) andfrom this study. One batch of specimens, in this study, were preparedfrom the thicker mid section of the shell and used by Came et al.(2014), another batch sampled the brachial shell in ontogenetic incre-ments from the umbo to the shell edge (Appendix 1). Parkinson et al.(2005) sampled the primary and tertiary layer in various regions, butonly isotope results from the un-specialized area of the tertiary layerwas used in the comparison. Marshall et al. (1997) did not specifywhat layer they removed or what layer(s) they sampled and thus it isnot clear what their isotope results represent.

Incorporation of isotope compositions from the primary layer may,in part, explain the more negative δ18O values for L. uva of Marshallet al. (1997). In contrast, the δ13C and δ18O results of L. uva from themid section of shells from this study (Appendix 1) and of Came et al.(2014) unequivocally fall into the carbon and oxygen isotope equilibri-umfieldwith ambient seawater, whereas some results from theontoge-netic sample strategy (this study, Appendix 1) and some from the non-specialized tertiary layer of Parkinson et al. (2005) fall outside theequilibrium field (Fig. 11b). The isotope equilibrium field is tightlyconstrained by the narrow seawater temperature and isotope

composition at Borge Bay, and the limited acclimation potential ofL. uva to survive in higher water temperatures (Peck et al., 2010). An-other explanation for this dilemma, may reside in the fact that seawaterδ13CDIC values were extrapolated from other parts of the Weddell Sea(open sea) and thus may not reflect local conditions at Borge Bay,Signy Island. However, this explanation does not apply to the oxygenisotopes that are from ambient seawater, and water temperatures arewell constrained for the sample site (Marshall et al., 1997; Brand et al.,2013). Only, the results of the four youngest ontogenetic shell incre-ments fall outside the equilibrium field. This suggests that the youngestshell increments and some unspecialized sample material of Parkinsonet al. (2005) may represent faster growing shell segments and thusmimic disequilibrium δ13C and δ18O values (Fig. 11b; Gabitov et al.,2012).

Based on the majority of δ13C and δ18O values, we feel justified toconclude that ‘mid-section’ calcite of L. uva is precipitated in near equi-librium with ambient Borge Bay, Signy Island seawater. But, a detailednanostructural investigation of the tertiary layer calcite and especiallyof the youngest growth increments of L. uva is underway to clarify theobserved carbon and oxygen isotope anomalies.

Antarctic brachiopods from theWeddell Sea and Ross Island fall with-in the constructed carbon and oxygen isotope equilibrium fields for theirrespective ambient seawater (Fig. 11c, d). The δ13C and δ18O results of

0

+1

-1

+2

+3

-2 -1 0 +1 +1+2 +2 +3 +4 +5

+1 +2 +3 +4 +5 +1 +2 +3 +4 +5

Hudson Bay, Canada (a)

Weddell Sea, Antarctica (c) Ross Island, Antarctica (d)

Signy Island, Antarctica (b)

δ13 C

(‰

)

δ18O (‰)

-2

-1

0

+1

+2

H. psittacea

Magellania fragilisStethothyris sp. (Secondary layer)S. sp. (Primary layer)

this studyParkinson et al.Marshall et al.

L. uva

-1

0

+1

+2

+3

-1

0

+1

+2

+3

Came et al. Came et al.

+2 -2°C

Fig. 11. Evaluation of carbon and oxygen isotope compositions inmodern brachiopods fromHudson Bay (a), Signy Island (b), Weddell Sea (c) and Ross Island (d). Hudson Bay results aresupplemented by results of Came et al. (2014). Signy Island results are supplemented by material fromMarshall et al. (1997), Parkinson et al. (2005) and Came et al. (2014). Ross Islandresults are from Carpenter and Lohmann (1995). Sample preparation, isotope adjustments and equilibrium field(s) are as described in Figs. 3, 4 and 5, and in the supplementary text.

92 U. Brand et al. / Chemical Geology 411 (2015) 81–96

primary layer calcite of Stethothyris sp. are clearly outside the equilibriumfield and confirm that these isotope results are in disequilibrium andshould not be used for paleoclimatological and other oceanographic

Table 3Carbon isotope compositions (max, mean andmin) inmodern articulated brachiopods fromlow-, mid- and high-latitude localities (Appendix 1, supplemented by results of Carpenterand Lohmann, 1995CL; Brand et al., 2003B; Parkinson et al., 2005P; Henkes et al., 2013H).

Low-latitude

Barbados GrandCayman

Jamaica Bermuda CanaryIslands

Venezuela Maldives Palau

+2.67 +2.55 +2.49 +2.72 +2.37 +3.60 +2.03 +1.33+2.01 +2.01 +2.01 +2.07 +2.00 +3.15 +1.32 +0.75+1.69 +1.77 +1.70 +1.55 +1.77 +2.72 +0.70 −0.23

Mid-latitude

DoubtfulSound

StewartIslandB

Otago Shelf FridayHarbor

Bay ofFundy

MediterraneanB

+1.51 +2.28 +2.72 +0.32 +1.64 +1.91+1.21 +1.98 +2.01 −0.62 +0.96 +1.60+0.65 +1.12 +1.15 −1.72 +0.38 +1.13

High-latitude

Hudson Bay ArthurHarborB

AdmiraltyBayH

SignyIsland

WeddellSea

Ross IslandCL

+2.44 +0.99 +1.63 +1.98 +1.61+1.84 +0.40 +0.77 +0.92 +1.71 +1.34+1.13 +0.54 +0.09 +1.33 +1.04

studies. Otherwise, our Arctic and Antarctic brachiopods precipitate car-bon and oxygen isotope compositions of secondary layer shells (and pos-sibly tertiary layer) in near equilibrium with ambient seawater, andaccurately reflect local environmental conditions (cf. Came et al., 2014).

5. Geographic variation

5.1. Low-latitude brachiopod populations

Brachiopods from six localities in the Caribbean and tropical AtlanticOcean have carbon isotope compositions with similar mean δ13C valuesand rangeswith one exception (Table 3). This attests to the relative con-stancy of seawater δ13CDIC values throughout the Caribbean (Kroopnick,1985). The δ13C values of brachiopods from the open ocean localities ofBarbados, Grand Cayman, Jamaica, Bermuda and the Canary Islands arelower than the ones close to the South American landmass (offVenezuela, Fig. 2, Table 3). Indeed, the δ13C values of the brachiopodsfrom northwest of Caracas, Venezuela are more positive by about 1‰than their other Caribbean counterparts, and probably reflect locally en-hanced phytoplankton productivity (Table 3). In contrast, the δ13Cvalues of the brachiopods from the Indian (Maldives) and Pacific(Palau) Oceans are significantly different than those of the previousgroup (Table 3). These observations suggest a commonality in δ13Cvalues between tropical Caribbean and low-latitude Atlantic seawater,but to differences with other localities due to potentially lower/higherproductivity and differences in seawater δ13CDIC values in the otherwatermasses. This disparity observed in tropical brachiopod δ13C values

166° 168° 170 ° 172°

44°

46°

48°

S o u t h I s l a n dN e w Z e a l a n d

StewartIs.

T a s m a nS e a

0 100 km

DoubtfulSound

Port Pegasus

OtagoShelf

0 +1 +2

δ13 C

(‰

)

δ18O (‰)

+3

+2

+1

+4New Zealand (b)

Doubtful SoundS

I

Port PegasusOtago Shelf

(a)

Fig. 12. Carbon and oxygen isotope compositions of three populations of brachiopods from three localities off New Zealand's South and Stewart Islands (Fig. 1). Blue shading— populationfrom Port Pegasus, Paterson Inlet, Stewart Island (B— Brand et al., 2003); green shading— population from the Otago Shelf (P— Parkinson et al., 2005); pink shading— population fromDoubtful Sound (this study). Isotope values are not adjusted for Mg effect (since no Mg results available for the Parkinson et al., 2005 population) to facilitate comparison. Diagonallyhatched pink field are C. inconspicua from the intertidal zone at Doubtful Sound, and horizontally hatched fields are L. neozelanica fromDoubtful Sound (pink) and theOtago Shelf (green).

93U. Brand et al. / Chemical Geology 411 (2015) 81–96

suggest caution when comparing and evaluating fossil brachiopod andwhole rock isotope results from similar latitudes but from different ba-sins and water masses (cf. Brand et al., 2012).

5.2. Mid-latitude brachiopod populations

The isotope compositions and trends of our intertidal and subtidalbrachiopod populations from Doubtful Sound are compared to onesfrom Port Pegasus, Stewart Island (Brand et al., 2003), to the OtagoShelf off New Zealand (Fig. 12; Parkinson et al., 2005), and to resultsfrom Friday Harbor, the Bay of Fundy, and the Mediterranean Sea(Brand et al., 2003; Table 3).

Isotope compositions of the intertidal brachiopod C. inconspicuafrom Doubtful Sound partly overlap with the isotope equilibrium fieldbased on subtidal Doubtful Sound seawater (Fig. 12b). This observationis in contrast to the isotope results of intertidal specimens from KiddsBeach (South Africa, Fig. 9d), where most values do not overlap withtheir subtidal seawater isotope equilibrium field. Perhaps, the isotopeequilibrium fields at the former two localities are too restrictive sincethey are based on seawater chemistry from the subtidal environment,which supports the suggestion that equilibrium fields should beconstrained and based on local or ambient oceanographic seawaterparameters.

Isotope compositions of the brachiopods from Port Pegasus, StewartIsland only partly concur with the isotope equilibrium field based onsubtidal seawater at Doubtful Sound (Fig. 12b). Since the oceanographyis markedly different between the water-stratified fjordic environmentof Doubtful Sound and the mud–sand–gravel bottom of Port PegasusInlet of Stewart Island (Hayward et al., 1994; Lee et al., 2011; Bairdet al., 2013), itmakes sense as suggested above, that local oceanographicconditions must be considered when assessing equilibrium incorpora-tion of isotopes into shell calcite.

Parkinson et al. (2005) evaluated a brachiopod populationconsisting of L. neozelanica, N. nigricans, C. inconspicua and T. sanguineafrom the Otago Shelf off New Zealand (Fig. 12a). Overall, their δ13Cand δ18O values are shifted towards more positive values relative tothose from Doubtful Sound and Port Pegasus, Stewart Island (Fig. 12b,Table 3) clearly reflecting the open ocean conditions on the shelf.

δ13C and δ18O values of L. neozelanica from Doubtful Sound fall out-side the local equilibrium field (Fig. 10d), and it is apparent that similar-ly the isotope results of L. neozelanica from theOtago Shelf are also offsetto those values of their concomitant brachiopod cousins (Fig. 12b).Thus, a there is something unique about L. neozelanica that sets it isoto-pically apart from its co-habitant brachiopods, and a detailed study ofthe nanostructure, biology and chemistry of L. neozelanica is warrantedto solve this mystery.

Although, theΔ13C values ofmid latitude brachiopods showgreat var-iation in their maximum (2.40‰), mean (2.63‰) andminimum (2.87‰)values, they are similar to those from tropical latitudes (max = 2.27‰,mean = 2.40‰, min = 3.00‰, Table 3). This variation is especially pro-nounced between the populations from Friday Harbor, the Bay of Fundyand the Mediterranean. Their overall δ13C values range from a lowof−0.62 to+1.60‰, which represents a 2‰ range for themeans of bra-chiopods from similar latitudes but different water masses (Table 3). Theplus 2‰ variation in δ13C values of low andmid-latitude brachiopods ad-vises caution when it comes to interpreting isotope values and trends offossil brachiopods based on strictly mean values and/or latitude withoutdue consideration for local influences on isotope compositions. It is in-cumbent upon the researcher to be cognizant of potentially large oceano-graphic variation(s) when making interpretations of fossil brachiopodpopulations from similar latitudes (cf. Brand et al., 2003). This importantobservation may easily explain the observed differences in δ13C and δ18Ovalues of Carboniferous brachiopods from North America and Russia(e.g., Mii et al., 2001; Brand et al., 2012).

5.3. High latitude brachiopod populations

It is generally assumed that high latitudewaters, with few exceptions,contain high concentrations of nutrients and thus are highly productivewaters. Although, recent studies confirm the generally high nutrientlevel but document moderate to low productivity levels that is referredto, by some, as the Antarctic Productivity Paradox (e.g., Tréguer andJacques, 1992; Clarke and Leakey, 1996). The δ13C values of brachiopodsfrom the Southern Ocean circumnavigating Antarctica speak directly tothis observation with their moderate values (Fig. 13a). Their meanvalues range from +0.40‰ at Arthur Harbor, to +0.77‰ at Admiralty

80°

100°

60° 40° 20°W

20°E

40°

60°

80°

100°120°140°160°E

180°

160°

W14

0°12

0°

0°

Signy Is.Admiralty Bay

Arthur Harbour

Weddell Sea

Ross Is.

Antarctic Circle

A n t a r c t i c a

-1

0

+1

+2

+3Antarctica (b)

Arthur

Har

bour

Admira

lty B

ay

Signy I

sland

Wed

dell S

ea

Ross I

sland

δ13 C

(‰

)

0 1000 km

(a)

Fig. 13. Evaluation of carbon and oxygen isotope compositions infive brachiopod populations from the Southern Ocean (Antarctica). Results for Arthur Harbor are fromBrand et al. (2003),for Admiralty Bay are from Henkes et al. (2013), for Signy Island andWeddell Sea from this study, and for Ross Island from Carpenter and Lohmann (1995). Symbols are mean values andbars represent range of values for individual populations (dashed — estimated).

94 U. Brand et al. / Chemical Geology 411 (2015) 81–96

Bay, to +0.92‰ at Signy Island, increasing further to + 1.71‰ for theWeddell Sea, but declining to +1.34‰ at Ross Island (Fig. 13b; Table 3).The highest δ13C value is recorded by brachiopods from the WeddellSea with +1.98‰ and the lowest from Arthur Harbor along the westcoast of the Antarctic Peninsula (Fig. 13b). This pattern of δ13C valuesabout the Antarctic continent is most interesting and in the context ofocean currents, continental influence and sea ice fluctuations deservesfurther study.

-1

0

+1

+2

+3

-2 -1 0 +1 +2

Isca, Italy

δ13 C

(‰

)

δ18O (‰)

shellN. anomala

umbo

Fig. 14. Evaluation of carbon and oxygen isotope compositions in themodern inarticulatedbrachiopodNovocrania anomala from Isca, Italy. Isotope adjustments and equilibriumfieldare as described in Fig. 3 and in the supplementary text.

6. Inarticulated brachiopods

Generally, inarticulated brachiopods are deemed to incorporate iso-topes in disequilibrium into shell calcite with ambient seawater, how-ever, Brand et al. (2013) demonstrated that Novocrania anomalaincorporates oxygen isotopes into shell calcite in equilibrium withseawater. Equilibrium fractionation is achieved by compensating forthe Mg effect impact on its isotope compositions. Consequently,N. anomala obtained from submarine caves of Isca, Italy have δ13C valuesin equilibrium with ambient habitat water conditions (Fig. 14). Thetrend towards the positive section of the equilibrium fieldsmay supportthe assertion of an extremely slow growth rate for this brachiopod andslightly faster rate for the calcite of the umbo region (Ruggiero, 2001).These observations fully support the concept that N. anomala and possi-bly other inarticulated brachiopods and marine invertebrates secretingcalcitic shells, tests/shells with elevated Mg contents may actually pos-sess equilibrium isotope compositions (cf. Brand et al., 2013).

7. Implications of carbon isotope equilibrium

The most important observation is that carbon isotopes composi-tions in articulated brachiopods as a group are incorporated in equilib-rium into their shell calcite. This is important to researchers workingwith calcitic brachiopods and possibly other calcite-secretingmarine in-vertebrates to evaluate Deep-Time paleoceanography and paleoclima-tology problems. Fossil brachiopods are important archives ofgeochemical proxies related to their paleoceanography and paleoclima-tology, and armedwith the knowledge that they incorporate carbon andoxygen isotopes in equilibrium into shell calcite with seawater weshould be able to re-construct higher resolution seawater and carbonatecurves. Especially, knowing the limitations and associated carbon iso-tope effects should aid in defining and establishing curves of the highestpossible resolution and thus provide the best possible interpretations ofpast ocean chemistry and temperature, and climate change impacts(glaciations–deglaciations, global icehouses, hothouses).

Our study advises caution when it comes to assembling curves ofDeep-Time seawater and carbonate with unscreened and unadjustedMg effect material, and without due consideration of fabric impacts(cf. Garbelli et al., 2014). Assemblages of brachiopod populations from

95U. Brand et al. / Chemical Geology 411 (2015) 81–96

temperate and tropical regimes suggest thatmean δ13C valuesmay varyby up 3.77‰, whereas their δ18O values may vary by up to 1.80‰(Table 3; Brand et al., 2013). Since most Deep-Time studies of brachio-pods deal with populations from tropical and subtropical regions, anevaluation of isotope results from the tropical Pacific and Caribbeanare all-important. Their differences in δ13C and δ18O values of 2.40‰and 1.25‰, respectively, speak clearly to the fact that all factors of thelocal environment must be addressed before attempting correlationsat the regional to global levels. Considering δ18O results without properknowledge of the brachiopods Mg content and without the relevantseawater-δ18O and DIC compositions (Table 1), their calculated watertemperatures may be underestimated by as much as 10 °C, while thedifference of 2.40‰ in δ13C valuesmay draw equally flawed conclusionsabout their correlation potential (Table 3). Thus, we need to be flexibleand cognizant of extrinsic environmental and intrinsic (Mg, fabric) con-trols that may influence isotope compositions.

8. Conclusions

The carbon isotope analysis and evaluation of a large modernshallow-water brachiopod population supplemented by results ofother studies covering the widest possible range of localities, majorwater bodies, temperatures and salinity, allows us to suggest thefollowing:

1) Modern shallow-water articulated brachiopods, as a group, with ap-plication of the Mg-effect incorporate carbon and oxygen isotopesinto shell calcite (secondary and tertiary layers) in apparent equilib-rium with ambient seawater,

2) Also, there is incontrovertible evidence that primary layer calcite isformed in carbon and oxygen isotope disequilibriumwith seawater,and furthermore, transition zone calcite and ‘fast growing’ areas,such as the youngest growth increments should be avoided,

3) Inarticulated brachiopods, specificallyN. anomala, oncewe apply theMg effect adjustment may also incorporate carbon and oxygen iso-topes into shell calcite in equilibrium with seawater,

4) The carbon isotope compositions of valves (ventral and dorsal)are both in apparent equilibrium (with few exceptions) and similarin magnitude, thus both and/or either may be used forpaleoenvironmental evaluations,

5) The moderate δ13C values of Southern Ocean (Antarctica) brachio-pods support the notion that high nutrient levels do not necessarilytranslate into high productivity and consequently positive δ13Cvalues,

6) The apparent carbon and oxygen isotope equilibrium with seawaterexhibited by the articulated brachiopods emphasize their importanceas archives of storing primary oceanographic information related tothe evolution of the marine hydrosphere, to paleoclimatology and tothe global carbon cycle.

Supplementary data to this article can be found online at http://dx.doi.org/10.1016/j.chemgeo.2015.06.021.

Acknowledgments

We thank the reviewers and editor-in-chief M. Boettcher for theirhelpful comments that improved the manuscript. M. Lozon (drafting)andM. Ouellette (laboratory) of BrockUniversity, and PatriciaWickhamof the University of Ottawa (isotopes) are acknowledged for technicalassistance. Other individuals provided valuable field assistance: B.Durzi, T. Durzi, N. Buckles (Cayman Islands), G. Maddock (Bermuda),S. Thomas (Barbados), D. Duggins, D. Willows, W. Krieger (FridayHarbor), G. Lundie, J. Batstone, CNSC (Churchill — Hudson Bay), M.Strong, M. Ines-Buzeta (Bay of Fundy), R. Donnel (OSC-MUN), and A.Zaky (Red Sea). Specimens were collected under license RE-12-23 is-sued by the Bureau of Marine Resources, Republic of Palau, and undersection 52 by the Department of Fisheries and Oceans (Canada) for

Bay of Fundy National Marine Park. A special thank you to L. Peck (Brit-ish Antarctic Survey) who provided specimens from Signy Island. Thiswork was supported by a Brock University Chancellor's Research Chairaward CRC-08 and by NSERC grant 7961-09 to UB.

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