Palaeobiology of an extinct Ice Age mammal: Stable isotope and cementum analysis of giant deer teeth

Palaeogeography, Palaeoclimatology, Palaeoecology 282 (2009) 133–144

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Palaeogeography, Palaeoclimatology, Palaeoecology j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / p a l a e o

Palaeobiology of an extinct Ice Age mammal: Stable isotope and cementum analysis of giant deer teeth Kendra L. Chritz a,⁎, Gareth J. Dyke b, Antoine Zazzo c, Adrian M. Lister d, Nigel T. Monaghan e, Julia D. Sigwart b,e,1 a

Department of Biology, University of Portland, 5000 N Willamette Blvd., Portland, Oregon, 97203, USA School of Biology and Environmental Science, University College Dublin, Belfield Dublin 4, Ireland Muséum national d'Histoire naturelle, CNRS UMR 7209 Archéozoologie, Archéobotanique: Sociétés, Pratiques et Environnements—USM 303—Département Ecologie et Gestion de la Biodiversité, 55 rue Buffon F-75231 Paris cedex 05, France d Natural History Museum, Cromwell Road, London SW7 5BD, UK e National Museum of Ireland—Natural History, Merrion Street, Dublin 2, Ireland b c

a r t i c l e

i n f o

Article history: Received 17 December 2008 Received in revised form 19 August 2009 Accepted 30 August 2009 Available online 8 September 2009 Keywords: Pleistocene Cervid Palaeobiology Ireland Stable isotopes Cementum analysis

a b s t r a c t The extinct giant deer, Megaloceros giganteus, is among the largest and most famous of the cervids. Megaloceros remains have been uncovered across Europe and western Asia, but the highest concentrations come from Irish bogs and caves. Although Megaloceros has enjoyed a great deal of attention over the centuries, paleobiological study has focused on morphometric and distributional work until now. This paper presents quantitative data that have implications for understanding its sudden extirpation in western Europe during a period of global climate change approximately 10,600 14C years ago (ca. 12,500 calendar years BP). We report here the first stable isotope analysis of giant deer teeth, which we combine with dental cementum accretion in order to document age, diet and life-history seasonality from birth until death. Enamel δ13C and δ18O measured in the second and third molars from seven individual giant deer suggest a grass and forbbased diet supplemented with browse in a deteriorating, possibly water-stressed, environment, and a season of birth around spring/early summer. Cementum data indicate that the ages of the specimens ranged from 6.5 to 14 years and that they possessed mature antlers by autumn, similar to extant cervids. In addition, the possibility for combining these two techniques in future mammalian paleoecological studies is considered. The data presented in this study imply that Megaloceros would have indeed been vulnerable to extirpation during the terminal Pleistocene in Ireland, and this information is relevant to understanding the broader pattern of its extinction. © 2009 Elsevier B.V. All rights reserved.

1. Introduction The giant deer, Megaloceros giganteus (Blumenbach, 1803) is easily the most famous and abundant fossil vertebrate known from the island of Ireland (Figs. 1 and 2). Although often referred to as ‘giant Irish deer’, or incorrectly as ‘Irish Elk’, this massive cervid was neither strictly Irish in its distribution nor an elk (Monaghan, 1995)—Megaloceros is known to have roamed across much of Europe during the Pleistocene (ca. 400,000–10,600 14C years BP), disappearing from the fossil record in Ireland and the rest of western Europe around the time of the last glacial–interglacial transition (e.g. Barnosky, 1985, 1986; Lister, 1994; Monaghan, 1995; Woodman et al., 1997; Lister et al.,

⁎ Corresponding author. Current address: Department of Biology, University of Utah, 257 South 1400 East, Salt Lake City, Utah, 84112, USA. Tel.: +1 801 585 0415; fax: +1 801 581 4668. E-mail address: [email protected] (K.L. Chritz). 1 Current address: Queen's University Belfast, School of Biological Sciences, Marine Laboratory, Portaferry, BT22 1PF, UK. 0031-0182/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.palaeo.2009.08.018

2005; Lister and Stuart, 2008). These mysterious animals have enjoyed a great deal of popular appeal for hundreds of years. Highly prized as a trophy in the nineteenth century, ‘Irish’ giant deer have provided a focus for much morphometric work (e.g. Gould, 1973, 1974; Barnosky, 1985; Lister, 1994) largely because of their antlers, the largest of any living or fossil cervid (Richardson, 1846; Pohlig, 1892; Lister, 1994). These antlers, which could grow up to 3.6 m in total span and were shed annually, have also been the scapegoat to explain the giant deer's demise for centuries, from miring it in Ireland's characteristic sticky lime clays to increasing their nutritional demands at a time of deteriorating climate and dietary resources (Monaghan 1996; Moen et al. 1999; O'Driscoll-Worman and Kimbrell, 2008). Such explanations for how an apparently thriving population of this animal disappeared from Ireland over-simplify causes of its extinction; more probable reasons for the demise of giant deer at the end of the Pleistocene have been discussed in depth (Stuart et al., 2004). Two main hypotheses for their extirpation in Ireland have been proposed, relating either to food or to temperature change during the

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Fig. 1. The giant deer, Megaloceros giganteus (Blumenbach, 1803), articulated skeleton on display in the National Museum of Ireland.

Younger Dryas stadial (Woodman et al., 1997). Distributional information has also been considered to address such questions as why these cervids were most abundant in Ireland and why this population collapsed before those in western Asia (Lister and Stuart, 2008). Certainly, the ecological parameters of this species need to be understood before we can come to a meaningful conclusion about giant deer extinction: principally diet, seasonality of life-history events (i.e. birth, death and antler cycle) and life span. Currently, the fossil record indicates that Megaloceros giganteus's range extended from Ireland in the west to the Siberian Lake Baikal in the east, with the largest concentrations of Megaloceros individuals known from lacustrine and cave deposits in Ireland (Mitchell and Parkes, 1949; Monaghan, 1995; Fig. 2). Approximate distributional data have been collated and have been used to infer aspects of the biology of Megaloceros (e.g. Mitchell and Parkes, 1949). High concentrations of male individuals at the Irish Ballybetagh Bog locality, for example, have led to the suggestion that giant deer lived for at least part of the annual cycle in segregated herds, similar to many extant cervids (Clutton-Brock, 1982; Moen et al., 1999). The absence of female individuals from the Irish collection in general (Table 1) has been used by some authors to support this ‘segregated herding’ hypothesis (Barnosky, 1985; Monaghan, 1995; T. Hayden, UCD, pers. comm., 2007) but needs to be assessed in the light of the taphonomy of these fossils. Unfortunately, fossil collections of giant deer across Ireland were not made systematically. There exists a predominant male bias in museum collections, which has been explained as a result of collectors favouring the highly-prized antlered males over the less striking antler-less females. This selection has been suggested both in field discovery where males are larger and more likely to be encountered and selected for recovery, and in curatorial choice of acquisitions (Monaghan, 1996). The systematic field collection at Ballybetagh (Moss, 1876) produced an exclusively male set of skeletal remains, which was explained by Barnosky (1985) as a water hole attracting over-wintering males in a segregated bachelor herd.

Even available distributional data lack robust quantitative analysis. The distribution data presented here, which infer range of giant deer individuals based on the National Museum of Ireland's fossil collection (Table 1), is the most comprehensive assembled since the work of Mitchell and Parkes (1949). Even given the large sample represented by this collection, specific locality data are limited (Table 1). We argue that speculations about giant deer distributional biology cannot be made in the absence of such data. Similarly, Megaloceros's diet has been one of the central topics of debate concerning how and why it went extinct, and paleodiet reconstructions based on morphometric data of Megaloceros have yielded conflicting results. Microwear and maxilla profile analysis of Megaloceros teeth by Hayden (2000) determined that they were primarily grazers (i.e. eating grass and other low-growing plants), while microwear analysis by Sørenson and Liljegren (2004) determined it was a browser (eating the leaves of trees and shrubs) that supplemented its diet with grasses. Stuart et al. (2004) also suggested a generalist, mixed herbivorous diet based on tooth anatomy. Even so, the details of the animal's diet remain unclear. A clear understanding of giant deer dietary preferences and seasonality of life-history events should be central to any discussion of their ecology and extinction, especially since this large cervid experienced several geographically confined extirpations during strikingly different climatic conditions, such as the Late Pleistocene extirpation in the British Isles and Scandinavia, and the Holocene extinction in western Asia (Stuart et al., 2004). As we have seen, these factors are very hard to address accurately using traditional palaeobiological techniques. Stable isotope analysis of tooth enamel has the potential to resolve some of these issues. Carbon (δ13C) and oxygen (δ18O) stable isotope ratios recorded in carbonate substitutions in hydroxylapatite (bioapatite) during tooth enamel formation are dependent on a range of environmental, physiological and behavioural pressures (Koch, 1998; Kohn and Cerling, 2002). In mixed C3–C4 environments, carbon isotope analysis has been used to decipher grazing, browsing or mixed feeding in herbivores (Ambrose

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Fig. 2. Distribution of Megaloceros in Ireland. Redrawn from Mitchell and Parkes (1949). Red dots denote skull material in the National Museum of Ireland. Red plus signs (+) denote additional localities, not published in Mitchell and Parkes (1949), for skull material in the NMINH. All other localities may represent post-cranial material or additional skull material not currently in the NMINH. Black arrow indicates the location of the well-sampled Ballybetagh Bog locality in Co. Wicklow, eastern Ireland. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

and DeNiro, 1986; Cerling et al., 1997). Oxygen isotope ratios in bioapatite are known to be dependent on local temperature and precipitation, as well as on the water-source dependence of the animal in question (e.g. Kohn et al., 1996); they can thus yield information on climate at the time of bioapatite formation. In mammals, tooth formation proceeds from the tip of the crown (apex) to the neck (cervix), and enamel is not remodelled once formed. As a result, environmentally and climatically constrained changes in the isotopic value of water or food ingested by mammals are permanently recorded during tooth mineralization (Fricke and O'Neil, 1996; Balasse, 2002). The pattern of intra-tooth oxygen isotope variation can be used to infer season of birth when analyzing teeth

that start forming shortly before or after the time of birth (e.g., Balasse et al., 2003). Enamel mineralization (amelogenesis) is a two-stage process, in which a highly organic matrix with small ‘seedlings’ of mineralized enamel crystals precedes mature enamel deposition (Hillson, 2005). It is noteworthy that amelogenesis is far more complex than a simple accumulation of apatite from apex to cervix and requires several months in mammals (Balasse, 2002; Passey and Cerling, 2002; Zazzo et al., 2005). As a result, sequential sampling procedures do not allow isolation of truly discrete time intervals and the amplitude of environmental variation recorded in tooth enamel is usually attenuated (Passey and Cerling, 2002; Zazzo et al., 2005). Nevertheless, the sequence measured is still chronological, as

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Table 1 List of skull specimens of Megaloceros in the National Museum of Ireland with associated locality data. These specimens are a subset of the collection of approximately 300 skulls. Localities listed in bold text are collecting sites not included in the classic Mitchell and Parkes (1949) distribution map (Fig. 2). Specimens notes with an asterisk (⁎) are those used in isotope analyses. One specimen (†) is on long-term loan to NMI. Specimen number

County

Locality

NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING:

Cavan Cork Donegal Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin Dublin

River Erne, below Cloggy Bridge Mallow Mountcharles Townland, Mountcharles [unknown] Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Ballybetagh, Kiltiernan, Rathdown Chapelizod Chapelizod Mulligan's Bog, Ballybetagh, Kiltiernan, Rathdown Mulligan's Bog, Ballybetagh, Kiltiernan, Rathdown Mulligan's Bog, Ballybetagh, Kiltiernan, Rathdown Mulligan's Bog, Ballybetagh, Kiltiernan, Rathdown Mulligan's Bog, Ballybetagh, Kiltiernan, Rathdown Mulligan's Bog, Ballybetagh, Kiltiernan, Rathdown Ballyragget Sleaty Townland, Sleaty Parish, Barony of Slievemargy Carrigallen Cloone Grange Drumsha, in Shannon at Drumsna Bridge Kilnagross Townland ('Kiltoghert') Mohill, Cloone Parish [unknown] [unknown] [unknown] [unknown] [unknown] Ash Hill Townland, Kilmallock Ballyneety, Pallasgreen Cool Bog, Kilteely Cool Bog, Kilteely Cool Bog, Kilteely

F7783 F7880 F21647⁎ F21184⁎ F7770 F7782 F7801 F7802 F7803 F7804 F7805 F7806 F7807 F7808 F7809 F7810 F7811 F7812 F7813 F7814 F7815 F7816 F7817 F7818 F7819 F7820 F7821 F7822 F7823 F7824 F7825 F7826 F7827 F7828 F7829 F7830 F7834 F7891 F7913⁎ F7786 F7794 F7933

NMING: F7940

Dublin

NMING: F7942

Dublin

NMING: F7944

Dublin

NMING: F7954

Dublin

NMING: F7955

Dublin

NMING: F7775 NMING GE/2000/109†

Kilkenny Laois

NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING:

Leitrim Leitrim Leitrim Leitrim Leitrim Limerick Limerick Limerick Limerick Limerick Limerick Limerick Limerick Limerick Limerick

F7879 F7851 F7798 F7787 F7790 F7777 F7779 F7831 F7839 F7925 F15968 F7922 F21188 F7864 F7892

Table 1 (continued) Specimen number

County

Locality

NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING:

F7919 F7902 F7780 F7776 F7767 F7781 F7969 F7766

Limerick Limerick Limerick Limerick Limerick Limerick Limerick Limerick

NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING:

F7769 F7900 F7852 F7853 F7884 F7887 F7894 F7985 F20936 F20987 F7773 F21236 F7868 F7871 F7886 F21194 F7860 F21189 F21192

Limerick Longford Louth Louth Louth Louth Louth Louth Louth Louth Louth Meath Meath Meath Meath Meath Meath Meath Meath

Cool Bog, Kilteely Kilcullen Bog, near Lough Gur Knocklong Knocklong, Knockcarran Bog Lough Gur Lough Gur Lough Gur Rathcannon, hollow between Rathcannon and Knocktoo Red Cellar Cave Near River Inny, Ratharney Castlebellingham Castlebellingham Castlebellingham Castlebellingham Castlebellingham Castlebellingham Paddock Townland, Dunleer Paddock Townland, Dunleer Strabannan Bog Kilnew Bog, Grennanstown [sic] Kilnew Bog, Upper Duleek Kilnew Bog, Upper Duleek Kilnew Bog, Upper Duleek Lagore Lisnaboe, Kingscourt Liss House, Oldcastle Mountainstown, Wilkinstown, Castletown, Navan Newtown Estate, Drumcourath River Dee, in bed of river between Nobber and Whitewood Ballyhoe Bridge, River Lagan Lough Naglack Bumlin, Strokestown Rooskey Strokestown Loughs, Donahoe [unknown] Jamestown Littleton Bog, Leigh townland, Thurles Longford Pass, Urlingford Cappoquin Cappoquin Cappoquin Cappoquin Castleruddery Lower Townland, Donard

NMING: F7774 NMING: F7789

Meath Meath

NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING:

Monaghan Monaghan Roscommon Roscommon Roscommon Tipperary Tipperary Tipperary Tipperary Waterford Waterford Waterford Waterford Wicklow [no data] [no data]

F12240 F7765 F7796 F7795 F7788 F7849 F7768 F14071 F7898 F21792⁎ F7799 F7800 F7895 F20514⁎ F7943⁎ F7861⁎

evidenced by the pattern of sinusoidal change in oxygen isotope ratios representing the seasonal cycle measured in modern and fossil teeth (Balasse et al., 2003; Balasse, 2006). Because the isotopic signature of tooth enamel only contains a record of the first years of an animal's life, it can be useful to combine it with another palaeobiological tool: dental cementum accretion analysis. This approach is a widely-used method for determining age and seasonality of life-history events in mammals (Klevezal, 1996; Wittwer-Backofen et al., 2003). Periods of growth throughout the major seasons of the year are recorded in a layer of tooth material called ‘cementum’ which typically accretes continuously following eruption of the crown until death, creating a pad between the crown, roots and gums that affixes the tooth to the alveolar bone in vertebrates with brachyodont dentition (Fancy, 1980). Of the two varieties of dental cementum (acellular and cellular), acellular cementum accretes in layers, recording periods of substantial growth during the summer and slower growth in the winter (e.g., Low and Cowan, 1963; Reimers and Nordby, 1968). Thus, by counting the number of winter and summer layers in these accretions, a rough age estimate and death seasonality information can be obtained for the individual.

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In this paper we aim to document important aspects of the ecology of giant deer that have been quantitatively absent from previous studies of its extinction, such as age and season of death, season of birth, seasonal antler cycles and diet. To achieve this goal, we combine stable isotope analysis of tooth enamel and examination of dental cementum accretion across a range of specimens, which will provide important life-history information for the giant deer. These methods have never been used in conjunction before; thus, combining them for paleoecological reconstruction will help create a template for future paleoecological assessment in vertebrates. 2. Materials and methods 2.1. Stable isotope analysis Specimens used in this study are all held by the National Museum of Ireland, Natural History Division (NMINH, Dublin). Five individuals were chosen from the extensive giant deer collection of the NMINH Geology collections (NMING; Table 1). The specimens were selected, based on their age and quality of their enamel preservation, for minimal tooth wear, although there is likely to be some loss of tooth height due to post-eruption wear in all specimens. Few specimens met these criteria, so quality of taphonomic data, including stratigraphy and locality, were of secondary importance in selection (Table 1). Two modern cervids, red deer (Cervus elaphus) (NMINH: 2001.40.1) and fallow deer (Dama dama) (NMINH: 1932.27.14), were also sampled for comparison. Although present in many specimens, first molars (M1) were not used because they begin to form prior to birth (Rees et al., 1966; Carter, 1998). The concern in using teeth that start accreting prior to birth is that the preserved isotopic signal will reflect maternal inputs, and that they may record a ‘weaning signal’ from consumption of milk (Wright and Schwarcz, 1998). Weaning signals preserved in δ13C and δ15N values have been documented in collagenous material, such as bone or dentine (Balasse and Tresset, 2002; Rountrey et al., 2007). In enamel apatite, the weaning signal is also recorded but less pronounced, and differences do exist between δ13C and δ18O in teeth that form in utero and those that form post-

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birth (Balasse et al., 1999; Dupras and Tocheri, 2007). Thus, sampling second (M2) and third (M3) molars not only records a longer postbirth life-history record, but also minimizes maternal isotopic inputs. Permanent upper left M2 and M3 teeth were removed from all skulls. The enamel surface was cleaned using a dental drill with a diamond-tipped drill bit. Bands perpendicular to the growth axis were drilled sequentially from apex to cervix (i.e. down the tooth, approaching the alveolar bone), following the direction of mineralization (Fricke and O'Neil, 1996) (see Fig. 3). In total, 77 samples were collected for isotopic analysis, weighing between 6 and 10 mg each (Table 2). To remove organic contaminants, samples were soaked in 2–2.5% bleach (NaOCl) solution overnight and rinsed five times with distilled water. Samples were then treated with 0.1 M acetic acid solution (after Balasse et al., 2003) for 4 h, rinsed again five times with distilled water and placed in an oven at 50 °C overnight. This method of sample treatment is least likely to introduce significant isotopic fractionation (Koch et al., 1997). Carbon and oxygen isotope ratios were measured at the LOCEAN Laboratory (University Pierre et Marie Curie, Paris) on an Isoprime isotope ratio mass spectrometer coupled with a carbonate device, through a continuous flow inlet system using an Isoprime Multiflow interface. Analytical precision was ± 0.03‰ for δ13C and ±0.06‰ for δ18O (1σ), based on repeated analysis of our internal calcite standard. Stable isotope values are given using the permil (‰) notation, expressed as ratios of the heavier isotope to the lighter isotope in the sample, relative to V-PDB for both carbon and oxygen. 2.2. Dental cementum All the molars selected for stable isotope analysis were also sectioned for dental cementum analysis, as were molars from two other individual giant deer that were selected based on antler preservation to compare individuals that died at varying stages of the annual antler cycle (Table 3). Molars were sectioned transversely across lophs using a diamond-tipped saw and were then waterpolished to expose the cementum pad below the crown of each tooth (Fig. 3). Polished pieces were observed under a light-reflecting

Fig. 3. Cementum annuli in second (M2) and third (M3) molar teeth. Top row: M2, Bottom row: M3; whole tooth after extraction from skull, polished section showing cementum annuli; schematic drawing to highlight summer and winter bands. Summer layers are wide, light-coloured bands in the tooth, depicted as white bands in the schematic drawing; winter layers or ‘rest lines’ are thin, dark bands in the tooth depicted as grey lines in the schematic drawing (specimens figured are from NMING: F9173). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

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Table 2 Carbon (δ13C), oxygen (δ18O) isotope ratios and carbonate content of molar enamel bioapatite from fossil and modern deer. M2, M3 indicate second and third lower molars, respectively. Position of the samples is expressed as the distance (in mm) from the cervical margin. Values for δ13C of the food source were calculated assuming a dietapatite enrichment of + 14.1‰ (Cerling and Harris, 1999). Sample

Extant deer Fallow deer—M2

Sample Distance CO3% δ13C number from cervix (mm)

δ18O

δ13C (calculated)

1 2 3 4 5 6 1 2 3 4 5 6 1 2 3 4 5 6 7 8 9 1 2 3 4 5 6

10.11 8.21 6.29 5.35 3.5 2.45 13.1 11.3 9.15 7.27 5.24 4.2 14.82 13.61 12.12 10.29 8.42 6.93 5.11 4.12 2.49 12.82 10.49 8.24 6.87 5.50 4.19

3.3 3.0 2.9 3.3 3.3 3.0 3.7 2.7 3.1 2.8 3.5 2.9 2.9 3.2 2.8 3.1 2.8 2.5 3.3 2.9 3.0 2.8 3.5 2.7 3.1 3.1 3.5

− 15.9 −15.3 −15.2 −14.8 −14.5 −12.9 − 14.9 −15.0 −15.2 −15.2 −15.5 −16.0 − 17.1 −16.7 −16.4 − 15.9 − 15.3 − 15.1 − 15.3 − 14.8 − 14.3 −14.9 −15.8 −16.1 −16.0 −16.8 −17.2

− 4.9 − 4.5 − 4.5 − 4.4 − 4.2 − 4.6 − 6.1 − 5.9 − 6.1 − 6.5 − 6.4 − 6.2 −6.1 − 5.7 − 5.3 −5.2 −4.9 −4.8 −4.9 −4.5 −4.3 − 4.8 − 5.8 − 5.9 − 6.7 − 7.1 − 7.1

− 30.0 −29.4 −29.3 −28.9 −28.6 −27.0 − 29.0 −29.1 −29.3 −29.3 −29.6 −30.1 − 31.2 − 30.8 −30.5 − 30.0 − 29.4 − 29.2 − 29.4 − 28.9 − 28.4 −29.0 −29.9 −30.2 −30.1 −30.9 −31.3

1 2 3 4 5 6 7 NMING: F21647—M3 1 2 3 4 5 6 7 8 9 10 NMING: F7913—M2 2 3 4 5 6 7 NMING: F7913—M3 1 2 3 4 5 6 7 8 NMING: F20514—M2 1 2 3 4 5 NMING: F20514—M3 1 2 3

15.32 12.64 11.55 9.06 6.75 4.89 3.5 19.67 18.4 16.87 14.75 13.09 10.16 8.51 6.45 4.53 2.76 9.76 7.64 6.68 5.7 4.65 3.11 16.56 13.64 12.17 9.67 7.52 6.15 4.51 1.89 10.5 8.5 7.1 5.6 3.5 16.75 14.55 11.4

3.7 2.6 2.7 3.3 2.5 2.7 2.5 3.2 2.9 2.6 2.7 3.1 2.8 2.2 2.4 2.8 3.1 3.1 2.4 2.7 3.4 3.5 3.9 3.7 2.9 3.1 3.1 3.3 3.3 3.3 3.7 3.5 2.9 2.5 8.8 2.9 3.0 3.0 3.1

− 7.8 − 10.4 −9.5 −9.8 −9.5 −9.4 −9.3 −9.2 −9.9 −9.4 −9.5 −9.5 −9.5 − 10.2 −9.6 − 9.7 − 10 −9.9 −9.8 − 10.3 −9.3 −9.0 − 10.5 −8.4 −8.8 −8.5 −9.1 −9.1 − 10.3 − 9.1 −10.4 − 8.0 − 8.5 − 9.0 − 8.4 − 9.1 − 9.4 − 9.2 − 8.5

−4.7 −5.3 −3.4 −3.5 −3.4 −2.3 −1.8 −1.5 −2.2 −1.8 −3.0 −4.5 −4.1 −4.0 −4.6 − 5.0 −5.4 −4.9 −4.7 −4.2 −4.0 −3.9 −3.8 −4.9 −5.4 −5.5 −5.4 −5.0 −5.3 −4.6 −3.9 −5.4 −5.1 −5.1 −4.9 −4.6 −3.9 −4.4 −4.6

− 21.9 −24.5 −23.6 −23.9 −23.6 −23.5 −23.4 −23.3 −24.0 −23.5 −23.6 −23.6 −23.6 −24.3 −23.7 − 23.8 − 24.1 − 24.0 − 23.9 − 24.4 − 23.4 − 23.1 − 24.6 − 22.5 − 22.9 − 22.6 − 23.2 − 23.2 − 24.4 − 23.2 − 24.5 − 22.2 − 22.7 − 23.2 − 22.6 − 23.3 − 23.5 − 23.3 − 22.6

Fallow deer—M3

Red deer—M2

Red deer—M3

Giant deer NMING: F21647—M2

Table 2 (continued) Sample

Giant deer NMING: F20514—M3

NMING: F7943—M3

NMING: F21184—M2

Sample Distance CO3% δ13C number from cervix (mm) 4 5 6 7 8 1 2 3 1 2 3

8.0 5.77 4.31 2.44 1.06 13.24 10.43 7.46 12.65 9.56 5.92

2.8 2.7 2.7 3.1 3.7 3.1 3.2 3.2 2.9 2.5 2.7

−9.2 − 8.3 − 9.5 − 9.9 − 9.8 − 8.6 −8.6 − 9.1 − 9.5 − 9.6 − 10.2

δ18O

δ13C (calculated)

− 5.9 − 5.5 − 6.1 − 6.5 − 5.7 −4.5 − 4.7 − 5.1 − 4.6 − 5.6 −5.9

− 23.3 − 22.4 − 23.6 − 24.0 − 23.9 − 22.8 − 22.8 − 23.3 − 23.6 − 23.7 − 24.3

dissecting microscope and annuli (growth layers) were counted by eye. One ‘summer layer’, which typically forms from the beginning of spring until autumn (a wide, light-coloured line; white bands in Fig. 3) and one ‘winter layer’ or ‘rest line’, which typically forms during the rest of the year (a thin, black line; grey bands in Fig. 3), were interpreted as representing one year of growth, following standard procedures (Low and Cowan, 1963; Reimers and Nordby, 1968; Klevezal, 1996). Although just one molar is typically used to age extant cervids with this method, we counted the annuli of both molars for each individual to cross-check our age estimates and to account for differing mineralization times among the molars. Seasonal layers of acellular cementum were interpreted beginning with the first accreted layer below the dentino-cementum interface (observed as a thick, grainy black line; DC interface, dark grey band in Fig. 3); and season of death was determined by interpretation of the last accreted layer. We estimated the season of antler shedding by comparing the season of death recorded in molars from different specimens at varying stages of the antler cycle. 3. Results 3.1. Stable isotopes Intra-tooth isotope variations in C and O are plotted from the apex of the tooth crown to the cervix, following a time series (Figs. 4 and 5). In both fallow deer and red deer, an increasing trend in δ13C values is seen in M2s, followed by a decrease in M3. Giant deer δ13C values in second M2s decrease initially, then increase toward the cervical margin (Fig. 4). Variation in giant deer M3s is much less pronounced: δ13C values remain relatively constant from the crown apex toward the cervical root. Greatest variation in M3 δ13C values is seen in specimen NMING F20514 (Fig. 4). Overall intra-tooth amplitude of change in δ13C values is 3.1‰ in fallow deer molars (from −12.9‰ to −16.0‰) and 2.9‰ in red deer molars (from −14.3‰ to − 17.2‰). Intra-tooth amplitude of change among giant deer samples in which isotope values were taken in two molars of the same specimen is 2.6‰ (F21647), 2.1‰ (F7913) and 1.9‰ (F20514), slightly less than modern deer; however, δ13C values are 4 to 5‰ more positive than those of their extant counterparts and range from − 7.8‰ to − 10.5‰ (Table 2, Fig. 4). While both extant cervids show an increase in δ18O values in M2 (less marked in fallow deer), red deer exhibits a decreasing trend in the M3 δ18O values whereas the fallow deer δ18O values are stable (Fig. 5). In giant deer individuals (NMING F21647, NMING F7913, NMING F20514), a consistent inter-tooth variation in δ18O values is seen across the specimens as a sinusoidal pattern that initiates in M2 and terminates in M3 (Table 2; Fig. 5). For extant samples, the intra-tooth range of variation in fallow deer δ18O values is 2.3‰ (from −4.2‰ to −6.5‰) and

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Table 3 Interpretations of age, seasonality and antler cycling profiles from cementum annuli of M2 and M3 teeth from giant deer skulls. ‘Number of layers’ indicates the number of combined ‘summer’ and ‘winter’ annuli, indicating one full year of growth (one layer). A half-layer (‘0.5’) indicates the partial or incomplete formation of a summer layer. Growth time estimated in months. Specimen

Skull

Number of layers

Estimated age (months)

Season of first accretion

Season of death

NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING: NMING:

Both antlers intact Both antlers intact Shed one antler, one partially shed Shed one antler, one partially shed Both antlers intact Both antlers intact Shed one antler Shed one antler Shed one antler Shed one antler Shed both antlers (recently shed) Shed both antlers (recently shed) Shed both antlers Shed both antlers

7 6.5 8.5 7.5 10.5 10 13 12.5 6.5 5.5 8 7.5 12.5 12

84 78 96–100 90 126 120 156 150 72–76 66 96 90 150 144

Summer Summer Summer Partial summer Partial summer Summer Partial summer Partial summer Partial summer Partial summer Partial summer Partial summer [Undetermined] Partial summer

Late winter Late summer/autumn Early summer End of summer Late summer/autumn Late winter/early spring Spring Late summer/autumn Mid summer End of summer/beginning of winter Spring, early summer Autumn, beginning of winter [Undetermined] Late winter

F21647—M2 F21647—M3 F7913—M2 F7913—M3 F20514—M2 F20514—M3 F7943—M2 F7943—M3 F21184—M2 F21184—M3 F7861—M2 F7861—M3 F21792—M2 F21792—M3

2.8‰ in red deer δ18O values (from −4.3‰ to −7.1‰). The total range across all six sets of giant deer samples is 5.0‰ (from −1.5‰ to −6.5‰); these ranges are conservative and likely reflect directional, perhaps seasonal, fluctuations in temperature over the course of bioapatite formation. In all three giant deer M2 samples, δ18O values increase toward the root (Fig. 5), while samples from two of the M3 teeth show the opposite trend (Fig. 5). Variation in δ18O values is least marked in the M2 samples of specimen NMING F20514 (Fig. 5) and in M3 samples of specimen NMING F7913 (Fig. 5). Offset between δ18O values in M2 and M3 teeth is likely due to differences in the timing of enamel mineralization. The δ13C and δ18O values across molars co-vary only in red deer. 3.2. Cementum accretion Approximate age profiles estimated by counting cementum annuli are given in Table 3, alongside inferred season of death and antler cycling of individual giant deer. Because M2 erupts prior to M3, it is more likely to retain a longer cementum record, as cementum often does not begin to form until the tooth has fully erupted in order to secure the tooth properly into its socket (see Keiss, 1969; Hillson, 2005). Thus, we assume age and seasonal estimates of M2 to be more accurate than M3. Estimated cementum ages of the seven individual Megaloceros sampled range from 66 to 156 months (Table 3); however, these ages are likely to be younger than the actual age of the individual because of the time difference between crown and cementum formation, which is approximately six to twelve months in fallow deer (Chapman and Chapman, 1970). Linear regression analysis comparing assigned age profiles to molar crown height and to ratios of pedicle width over height (which decrease and increase, respectively, with age) also confirms the general validity of age determinations, as well as a tighter correlation between M2 cementum age estimates to these other age-related changes in tooth morphology (Table 4). When crown mineralization time was accounted for by adding 12 months to M2 cementum age assignments, which is slightly longer than the initialisation of root mineralization in red deer (9 months; Carter, 1998), the linear relationship between molar heights and age increased, particularly when compared to molar height averages. Adding a 12 month correction to M2 molars, our age estimates for giant deer range between roughly 78 and 168 months (6.5 and 14 years) of age. Our data from skull morphology and terminal seasonality of cementum layers would suggest that adult male Megaloceros shed their antlers in early spring (Table 3). Of the seven specimens sampled, two skulls (NMING F21647; NMING F20514) have both their antlers intact (inferred season of death from M2 cementum is early winter), while three (NMING F7913; NMING F7943; NMING F21184)

have lost one antler (inferred seasons of death is early summer). The two skulls (NMING F7841; NMING F21792) that lack both their antlers (exposed pedicles are present) are inferred from their cementum layers to have died in either late winter or early spring. Late winter or spring antler shedding corresponds with annual cycles in many extant northern cervids (Shackleton, 1999). Comparing annular cementum layers of M2 and M3 teeth within individual skulls, little correspondence is seen in termination of cementum annuli within specimens: of the seven giant deer sampled, six have incongruent termination times for layers of their dental cementum. This is likely a function of differences between tooth mineralization rates and eruption patterns between the M2 and M3 teeth (see above). Season of cementum termination could not be determined in one M2 tooth of a giant deer (NMING F21792) because of cementum diagenesis. 4. Discussion and conclusions 4.1. Diet and habitat Vegetation, mammalian diet, and climate are strongly interacting factors in assessing palaeoecology of animals such as Megaloceros (Bradshaw and Mitchell, 1999). Although glaciation has a strong causative impact on extinction and extirpation of mammals in Quaternary Ireland, our analysis allows more specific insights into dietary effects and potential environmental stress. In our results, the δ13Cdiet values were calculated using a well-established diet-toapatite fractionation factor of 14.1‰ (Cerling and Harris, 1999), which arises as a result of metabolic and catabolic processes once vegetation has been consumed. For modern cervids, a second correction was made to account for atmospheric δ13C depletion due to the combustion of fossil fuel (Francey et al., 1999). This correction is specific to the year of tooth formation; because this was not known for these specimens, we used the date of museum acquisition as a proxy, which is 2001 for the red deer and 1932 for the fallow deer. δ13Cdiet values range from − 26.6 to − 29.5‰ for red deer after adding a correction of +1.8‰, and from − 26.6 to −29.7‰ fallow deer after adding a correction of +0.38‰ (Francey et al., 1999). These values tend toward the more negative end of the C3 carbon isotope spectrum and are typical of δ13C values of C3 plants growing today in Ireland (Zazzo et al., 2008). Megaloceros δ13Cdiet values range from −21.9 to −24.6‰. Overall, δ13Cdiet values of giant deer samples are approximately 3 to 5‰ more positive than those from modern deer, but show slightly less variability (1.9‰ to 2.6‰ in Megaloceros vs. 2.9 to 3.1‰ in modern deer). Dietary isotope values in modern herbivores depend upon habitat, and are under both environmental and physiological control: the growing conditions of plant communities, climatic factors like

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Fig. 4. Carbon isotope variation recorded across the second (M2) and third (M3) molars from two species of modern deer and three specimens of fossil giant deer, Megaloceros. δ13C values from modern deer have been corrected (+0.38% for fallow deer and +1.8‰ for red deer, following Francey et al., 1999) to account for the Suess effect (open symbols).

drought or humidity, natural seasonal variation, or water use efficiency in source vegetation (Tieszen and Boutton, 1989; MacFadden and Higgins, 2004; Drucker et al., 2008).

Dietary δ13C values for modern deer calculated from this study are very similar to δ13C values calculated from bone collagen of modern red deer living in forested habitats across western Europe and Canada

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Fig. 5. Oxygen isotope variation recorded across the second (M2) and third (M3) molars from two specimens of modern deer and three specimens of fossil giant deer, Megaloceros.

(Drucker et al., 2008). Irish Megaloceros bone collagen δ13C values from post-cranial material that date between 11,820 and 10,900 14C years BP range from −18.5‰ to −20.7‰, respectively (Woodman et al., 1997; Stuart et al., 2004, unpublished material) and from −20‰ to −21.2‰ in

the Scandinavian population (between 11,875 and 10,870 14C years BP), with a maximum value of −19.1‰ at about 11,490 14C years BP (Sørenson and Liljegren, 2004). Carbon isotope values from post-cranial material of the recently-discovered Holocene population from Siberia

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Table 4 Linear regression statistics for molar crown height, pedicle width and pedicle height vs. assigned M2 cementum age. Cementum ages are taken from M2 teeth because mineralization is initiated before M3 teeth. Variable

R2

P-value(a = 95%)

Std. error

M2 M3 Average, M2 + M3 Pedicle width Pedicle height Ratio, pedicle w/h M2 vs. cementum age + 3 mos M2 vs. cementum age + 6 mos M2 vs. cementum age + 12 mos M3 vs. cementum age + 3 mos M3 vs. cementum age + 6 mos M3 vs. cementum age + 12 mos Molar average vs. cementum age + 12 mos Pedicle ratio vs. cementum age + 12 mos

0.554 0.609 0.703 0.783 0.071 0.769 0.560 0.556 0.574 0.700 0.698 0.626 0.833 0.769

0.01 0.004 < 0.001 < 0.0001 0.565 < 0.0001 0.011 0.01 0.009 0.001 0.001 0.003 << 0.0001 < 0.0001

1.316 0.032 0.036 0.066 0.069 0.003 0.036 0.034 0.032 0.023 0.022 0.028 0.009 0.003

are extremely similar to those from older material (ranging from −21.5‰ to −19.7‰ between 10,825 and 6800 14C years BP, respectively) (Stuart et al., 2004). Assuming a diet-to-collagen enrichment of about 5‰ in ungulates (van der Merwe, 1989), these values are indicative of δ13Cdiet values of −23.5‰ to 25.7‰ for the Irish population (Woodman et al., 1997; Stuart et al., 2004), −25.0‰ to −26.2‰ in the Scandinavian population (Sørenson and Liljegren, 2004) and −24.7‰ to −26.5‰ in the Siberian population (Stuart et al., 2004). When collagen-derived and enamel-derived δ13Cdiet values are compared, however, we notice that enamel-derived δ13Cdiet values obtained in this study are on 1.0 to 1.5‰ more positive than those derived from bone collagen obtained from the Irish population. This difference is most likely the result of uncertainties in the estimation of diet-tissue fractionation factors in collagen and apatite. The 4–5‰ discrepancy between δ13Cdiet values between the giant deer and modern deer can most likely be explained by differences between Pleistocene and modern vegetation. Vegetation patterns of the Bølling–Allerød Interstadial are characterised by woody taxa (notably Betula, Salix and Juniperus) in scattered assemblages dominated by open grasslands with herbs (Watts, 1977; Andrieu et al., 1993; Ahlberg et al., 1996; O'Connell et al., 1999; Johnson, 2009). Near the end of the Bølling–Allerød (about 13,000 years BP), pollen and sedimentary records from Ireland indicate a general climatic downturn, with cooler temperatures and succession of more cold-tolerant (predominantly herbaceous) plants (O'Connell et al., 1999). Modern vegetation in Ireland is quite different: at the beginning of the 20th Century, only about 1% of land cover was forested land and re-forestation efforts saw the plantation of many exotic species, such as beech (Fagus sylvatica), sycamore (Acer pseudoplatanus) and larch (Larix europaea) (Cross, 2006). When considering the diet of Megaloceros, the animal's degree of selectivity may play an important role in determining δ13C values. In general, woody C3 vegetation tends to give lower δ13C values than herbaceous C3 vegetation in open environments (Tieszen and Boutton, 1989), which means that the high δ13C values could reflect a feeding strategy that favoured herbaceous forage with supplemental woody browse. Many extant cervids are generalist, opportunistic feeders, which may have been the feeding strategy of giant deer. There are very important ecological factors that must to be considered in order to properly interpret Megaloceros's δ13C values. Even though vegetation of the Late Pleistocene in Ireland was very different from today, it is still possible that both the Bølling–Allerød giant deer and modern deer were feeding on similar general categories of plant material. In this case, differences in δ13C values may be a result of environmental or climatic variation (e.g., Stevens and Hedges, 2004; Ward et al., 2005). Water stress has an impact on δ13C values in C3 plants, resulting in more positive values in plant tissues as leaf conductance decreases and intercellular CO2 is taken up

more quickly, decreasing isotopic discrimination (Farquhar et al., 1989). Lower temperature can also result in decreased isotope discrimination in C3 plants (Körner et al., 1991). Salix, Betula and other Alaskan arctic shrub species, which are all C3 plants that experience stress from both drought and cold, have δ13C values more negative than −26.5‰, while graminoid and forb species have more positive δ13C values, between − 24‰ and − 26.5‰. In these communities, drought-tolerant species like forbs and graminoids give δ13C values that are more positive when growing in places with lower water-availability (Barnett, 1994). Thus, accounting for the 1.8‰ depletion in δ13C values of modern vegetation (Francey et al., 1999), all of these cold-tolerant plants are within isotopic range of Megaloceros's diet. Finally, it is also possible that these high δ13C values are results of local climatic stress, possibly reflecting largerscale climatic downturn at the end of the Allerød and at the Allerød– Younger Dryas transition, the time-range of most of the dated giant deer remains uncovered in Ireland (Barnosky, 1985; Woodman et al., 1997; Stuart et al., 2004). 4.2. Oxygen isotopes and season of birth The sinusoidal shapes of the oxygen isotope profiles are indicative of annual variation in climate, where higher relative δ18O values imply warmer/drier conditions during mineralization (Kohn et al., 1996). All three of the oxygen curves for modern deer and giant deer initiate in M2 with some of the lowest δ18O values among the samples (Table 2). Assuming that M2 mineralization begins at birth (Kohn et al., 1998) the lower δ18O values at the apex of the tooth imply a spring/early summer season of birth. Although weaning may have occurred sometime during the mineralization of M2, the potential isotopic δ18O input of milk is small and unlikely to distort the overall sinusoidal seasonal signal (see Wright and Schwarcz, 1998; FranzOdendaal et al., 2003). Climate in Ireland deteriorated sharply at the time of giant deer extirpation: temperature dropped as much as 12 °C from the previous interstadial during both the summer and winter, and climate was much drier (Ahlberg et al., 1996; Stuart et al., 2004; Lister and Stuart, 2008). The precise age of our specimens within the interstadial– stadial cycle is not known, but at their likely position in the late Allerød to earliest Younger Dryas, spring and early summer would have been considerably colder than during the preceding Bølling to early Allerød, with depressed plant productivity, producing suboptimal conditions for young deer with high energetic demands. What is surprising is that oxygen isotope values do not differ much between the giant deer and modern deer: giant deer δ18O values are approximately 1 to 2‰ more positive than those from modern deer (from −1.5‰ to −6.5‰ across all giant deer samples, as opposed to −4.2‰ to −7.1‰ in modern samples) (Table 2). Meteoric δ18O values, and thus the giant deer δ18O values, might be expected to be lower than those of modern deer as a result of the cooler Allerød environment they lived in; however, this phenomenon is also observed in δ18O values for Younger Dryas soil sequences in Ireland, and it has been speculated that the dry conditions of the end-Pleistocene and possibly increased residence time of lake water are responsible for higher-than-usual 18O/16O ratios (O'Connell et al., 1999). Another important consideration is that physiology and water conservation can vary considerably even among organisms of the same taxon, depending on their ecology and behaviour, and these can have a significant effect on body water δ18O composition (see Willmer et al., 2005). Without a solid understanding of metabolism and osmoregulatory mechanisms in the study taxon, these effects cannot be ruled out (see Kohn et al., 1996). 4.3. Age estimates and individual history Counts of accreted cementum layers were consistent with those of earlier work. Barnosky (1985) used pedicle width, tooth height and

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molar size to estimate a mean age of individuals from the classical locality, Balleybetagh Bog, Co. Wicklow, Ireland (Fig. 2) at 8.7 years (specimen age estimates range from 2 to 13 years), while Sørenson and Liljegren (2004) estimated an age from two incisors of a single Scandinavian Megaloceros skull at 23 years. Although Sørenson and Liljegren (2004) used the cementum accretion method, the mean ‘cementum age’ of our sample of specimens (n = 14 teeth) closely corresponds with age estimates given by Barnosky (1985) at 8.8 years (Table 3). Seasonality estimates of the first accretions of cementum layers are consistent across the sample. Season of first accretion is recorded in all individuals and all teeth (n = 14) as summer or partial summer (an incomplete summer layer) (Table 3). M3 molars in fallow deer can erupt any time between 13 and 27 months of age (Chapman and Chapman, 1970); thus, cementum accretion time in M3 molars could be lagging considerably behind those of the M2 molars. It seems that there is a considerable lag in time between the termination of enamel formation and the initialisation of cementum accretion. Oxygen isotope curves imply a spring/summer birth for giant deer (Fig. 5). Since the first cementum layer in M2 teeth is consistently either a summer or partial summer layer, initialisation of acellular cementum mineralization must have begun near the end of or shortly following winter, approximately one year after birth (Table 4). In addition, since the first accretion is the same (or very similar) in almost every sample, it may be inferred that there is approximately one year between the initiation of cementum mineralization in the second and third molar. In third molars, the seasonality of the first accretion appears to complete an annual cycle that is initiated in the M3 enamel, which consistently gives a late summer signal at the apex of the crown (Fig. 4). In other words, despite the lag between the formation of enamel and cementum in the second molar, it appears that there is a continuous seasonal signal that is initiated in M2 cementum and is recorded in both M3 enamel and cementum until death. Estimated seasons of death for individuals in our giant deer sample, based on termination of cementum accretion, range throughout the year and vary between teeth from the same individual (Table 3). This suggests that estimating the season of death in giant deer is highly dependent on tooth selection and may give conflicting results. The six month difference between the seasonality of the terminal cementum layers between the two molars is easily explained by the six month lag between the end of the enamel formation and the initiation of cementum accretion in M2. This time-lag was only recognisable by comparing oxygen isotope signals and cementum layers together, and the temporal information in these different tooth materials appears to be complementary. The information given in the cementum layers can serve as independent check for the duration of enamel formation, which is quite helpful when interpreting annual cycles in oxygen isotope curves. In the context of life history, the seasonal information given in cementum layers conveys important information. Most northern and temperate cervids rut and mate in the autumn after males have fully re-grown their antlers; typically, antlers are shed and females give birth to young starting in the spring (Shackleton, 1999). Autumnal antler maturation is consistent with our data for giant deer with very recently shed antlers, which may also imply an autumnal rut (Table 3). However, not every modern cervid species follows this annual cycle and such a conclusion must be made with caution. Cementum annuli accretions have never been studied in conjunction with enamel oxygen isotope analysis before; thus, the relationship between the seasonal information of the two tissues is not understood. Like enamel, the accretion and mineralization of cementum apatite is a discontinuous process, in which a preliminary protein-rich matrix is deposited before cementum apatite mineralizes (Limeback, 1991; Yamamoto et al., 2005). This means that the deposition of mineralized tissues lags behind the deposition of a pre-

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cementum matrix by an amount of time that is highly dependent on the species in question. What is puzzling is how cementum annuli accretions can correlate so well to age in mammals despite: (1) the overall delay in cementum formation until after tooth eruption, and (2) a lack of understanding of the time-sequence for mineralizing dental tissues. In order for this method to be used with confidence in the future, it needs to be examined with more scrutiny on animals raised under controlled, or at least semi-controlled conditions.

4.4. Paleoecology and giant deer extinction The data presented in this study suggest possible explanations for giant deer extirpation in Ireland. The general ecological information obtained from this study—the generalist feeding behaviour and spring/early summer season of birth—indicate that giant deer would have been vulnerable at the onset of the Younger Dryas Stadial in Ireland due to the decrease in annual temperature and overall vegetation productivity (Andrieu et al., 1993; Ahlberg et al., 1996). In addition, the high metabolic demands of their large body size would have stressed them significantly during this time of vegetational decline (Gould, 1974; Moen et al., 1999; O'Driscoll-Worman and Kimbrell, 2008). As an insular population, Irish Megaloceros giganteus could not expand its range to find alternative sources of food. A seasonality of birth in the spring/early summer, in conjunction with a shortened growing season as suggested by Barnosky (1986), would have stressed young giant deer. Future stable isotope studies of temporally-constrained extinct mammal populations have potential to address such ideas in greater detail.

Acknowledgements We thank Mike Bolshaw, Dave Spanner and Clive Trueman (National Oceanography Centre, Southampton) for their help and advice with isotope analyses. We also thank Robert Feranec, Anthony Barnosky and two anonymous reviewers for their insightful comments and suggestions on earlier drafts of this manuscript. Tom Culligan and Frank McDermott (Geological Sciences, UCD) kindly assisted KLC with sample preparation. KLC was supported by the Science Foundation Ireland (UREKA site grant to JDS).

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