High-Latitude Dinosaur Nesting Strategies during the Latest Cretaceous in North-Eastern Russia

: Dinosaur eggshell fragments attributed to the oofamilies Spheroolithidae and Prisma-toolithidae and recovered from the latest Cretaceous Kakanaut Formation of North-eastern Russia (Chukotka) constitute one of the northernmost records of dinosaur reproductive behaviors. The high palaeolatitude of the locality (~75 ◦ N), as well as the cool near-polar climate, where summer temperatures only averaged 20 ◦ C during the warmest month, dark near-freezing winters and egg incubation that could have lasted several months, raise questions about dinosaur reproductive strategies, particularly in terms of the timing of egg laying. In order to investigate seasonal aspects of Kakanaut dinosaur reproductions, carbonate from eggshell fragments have been analyzed for their oxygen and carbon isotope compositions, along with the oxygen and carbon isotope compositions of apatite phosphate and structural carbonate of associated theropod, hadrosaur and ankylosaur teeth as well as lepisosteid ﬁsh scales. Stable oxygen and carbon isotope compositions of eggshells from the Kakanaut Formation together with those of associated adult dinosaur teeth and ﬁsh scales reveal differences in mineralization timing between eggshells and teeth and show that eggs were laid at the very beginning of spring when snowmelt drained from nearby highlands. We propose that Kakanaut dinosaurs laid their eggs at the very beginning of spring in order to accommodate an incubation period that lasted several months. This timing would also beneﬁt from mild temperatures and increasing food availability when the eggs hatch, allowing the hatchlings to grow large enough to survive the next winter or perhaps follow adult animals in their migration southwards.


Introduction
Climate and especially seasonality act as major constraints on the reproductive strategies of reptiles (sensus Sauropsida) in terms of egg-laying periods [1] and egg incubation method [2].In turn, reproductive ecologies limit the geographic distribution of reptiles in terms of latitudinal range and environments [2,3].Some of the most challenging environments for successful reproduction are in near-polar regions, where extended periods of darkness and freezing winters reduce habitability and limit food availability to a few months between spring and autumn.Extant birds living at high latitudes as permanent residents, such as the North American white-winged crossbill (Loxia leucoptera), the great horned owl (Bubo virginianus) or the bald eagle (Haliaeetus leucocephalus), adapt their breeding strategy by either laying eggs during the harshest part of the winter so they hatch at the very beginning of the plant growing season or by adopting opportunistic breeding periods depending on the shift of seasons [4][5][6].Due to their exceptional range of body mass, from a few grams to several tens of tons, non-avian dinosaurs might have had various reproductive strategies adapted to their physiological and anatomical peculiarities [7].Paleoclimate studies document that such harsh near-polar conditions existed during the Cretaceous [8][9][10].
Based on these considerations, the discovery of dinosaur remains from Cretaceous high palaeolatitude sites in Alaska, North-eastern Russia and Australia raises questions as to whether they were able to live in near-polar regions year-round and how they reproduced or had to migrate seasonally [11][12][13].Recent discoveries of eggshell fragments in Northeastern Russia [11], as well as perinatal and very young individuals from Alaska [14,15], demonstrates that some dinosaurs, including large-sized species, were able to successfully reproduce at high latitudes and were most likely permanent residents of high latitudes.
As large dinosaurs such as hadrosaurs and tyrannosaurids were likely not able to brood their eggs like smaller theropods such as oviraptorosaurids [16,17], they had to rely on external sources of heat, such as solar irradiance or heat produced by the decay of plant debris, to warm their nests to an appropriate temperature for incubation.In the context of ecological and climatic constraints, along with egg incubation that could have lasted from a few weeks up to six months depending on the species [18,19], it seems likely that high-latitude dinosaurs had to optimize the timing of their egg laying in order for their hatchlings to have enough food to grow up sufficient to survive the next winter.
Seasonal aspects of egg laying can be investigated using the oxygen isotope composition of eggshell carbonate (δ 18 O c ) compared to that of adult teeth phosphate (δ 18 O p ). Indeed, the δ 18 O value of vertebrate mineralized tissues (bones, teeth, scales or eggshell) reflects the oxygen isotope composition of the animal body water with an isotopic fractionation that depends on body temperature [20,21].In turn, the δ 18 O value of the body water of vertebrates is controlled by that of the oxygen inputs (drinking and food water, oxygen in food and breathed oxygen) and outputs (water vapor exhaled and lost through transcutaneous evaporation and water in urine and feces), with some of these oxygen fluxes being associated with isotope fractionation [22,23].By applying appropriate oxygen isotope fractionation established between mineralized tissue (phosphate or carbonate) and ingested water, it is possible to estimate the oxygen isotope composition of local surface waters (δ 18 O w ) within the vertebrate living environment [24,25].Continental surface waters, such as ponds and streams, are derived principally from local meteoric waters, but larger rivers and lakes can mix waters from distant origins within the water catchment, including high-altitude 18 O-depleted snowmelt from nearby mountains.Because the δ 18 O value of meteoric waters is controlled by air temperature and the amount of precipitation [26], the oxygen isotope composition of surface waters varies seasonally, and these variations can be recorded in the hard tissues of vertebrates that mineralize incrementally [27].Moreover, precipitation of eggshell calcite takes place over only a few hours to a few tens of hours for each egg.Thus, the oxygen isotope composition of eggshell calcite records a very short period of water ingestion by the female, corresponding to the residency time and turnover rate of body water.This residency time varies from a few days to a few weeks depending on the body mass of the female.
The carbon isotope composition of eggshell calcite or the apatite-bound carbonate of bones or teeth (δ 13 C c ) belonging to air-breathing vertebrates reflects that of their diet, with a carbonate-diet 13 C enrichment that depends on their digestive physiology [28].Plant-eating animals have a δ 13 C c value that depends on the carbon isotope composition of consumed plant tissues, the latter having δ 13 C values mainly controlled by that of atmospheric CO 2 and with a carbon isotope fractionation that depends on the plant photosynthetic pathway [29].The C 3 pathway is the most common one, occurring in all trees, most shrubs, herbs and grasses in regions with a cool growing season.C 4 photosynthesis operates in grasses from regions with a warm growing season and in some sedges and dicots.Finally, crassulacean acid metabolism (CAM) occurs in succulent plants.C 4 and CAM plants were most likely absent in Late Cretaceous ecosystems [30] and they will not be discussed any further.Today, C 3 plants have a mean δ 13 C value of −27‰ V-PDB (ranging from −35‰ to −22‰), reflecting both the δ 13 C value of atmospheric carbon dioxide and local environmental conditions [31].Indeed, abiotic factors, such as water and osmotic stress, variations in light intensity, local temperature and pCO 2 , influence the carbon isotope compositions of C 3 plants by affecting leaf stomatal conductance, which, in turn, constrains the magnitude of CO 2 diffusion through the plant epidermis.All these factors result in variations in the δ 13 C values found in C 3 plants [29].
Knowing the apatite-diet carbon-heavy isotope enrichment (∆ 13 C ap-diet ) of plant-eating vertebrates, it is thus possible to estimate the carbon isotope compositions of their ingested local plants from the δ 13 C c value of their bone or tooth apatite carbonate [28], as well as of their eggshell calcite [32].For extinct dinosaurs, apatite-diet 13 C enrichments of about +18‰ have been estimated for two ornithischians, ceratopsians and hadrosaurs [33,34], and about +15-16‰ for the sauropods [35,36].
Based on the above considerations, we interpret the stable oxygen and carbon isotope compositions of dinosaur eggshell calcites and tooth apatites in terms of environmental conditions and timing of egg laying.We then discuss the possible reproductive strategies used by near-polar dinosaurs in the northeast of Russia during the latest Cretaceous.

Material and Method
Dinosaur teeth, eggshell fragments and fish scales were sampled for stable isotope analysis (Figure 1).They were collected from the Koryak Upland region of North-eastern Russia, in a volcaniclastic sedimentary succession comprising the Kakanaut Formation exposed along the Kakanaut River.This formation is a 1000 m thick continental sequence, the exact age of which is still debated.The bone-bearing layers are either dated as (1) early late Maastrichtian considering that the formation is underlain by marine deposits of late Maastrichtian age and overlain by marine sediments of the Kokuy Unit, which contain poorly preserved plant fossils and the latest Maastrichtian invertebrate fauna [10,37,38] or (2) late Campanian-early Maastrichtian considering that underlying and overlapping deposits do not directly contact marine layers containing stratigraphically important forms of mollusk fossils.Furthermore, the dinosaur remains were found together with plant representative of the Kakanaut flora, allowing the assignment of the bone-and plantbearing layers to the Gornaya River phytostratigraphic horizon dated as late Campanian, possibly early Maastrichtian [39].During the latest Cretaceous, the Koryak Upland region was situated at a paleolatitude of about 75 • N [40] (Figure 1).
The studied material consists of two hadrosaurid, three ankylosaurid and two theropod teeth, three spheroolithid and two prismatoolithid eggshell fragments and three lepisosteid fish scales, all collected from a single highly fossiliferous lens [11].When possible, enamel was extracted from the teeth and ground into fine powder using a microdrill but, for smaller teeth, scales and eggshell fragments, whole specimens were ground using an agate mortar and pestle (Table 1).Apatite samples were prepared following the wet chemistry protocol described in Lécuyer [42].For each sample, an aliquot of 30 mg of apatite powder was dissolved in 2 mL of 2 M HF.The CaF2 residue was separated by centrifugation and the solution neutralized by adding 2.2 mL of 2 M KOH.Amberlite™ anion-exchange resin beads were added to the solution to isolate the PO4 3− ions.After 24 h, the solution was removed, the resin was rinsed and eluted with 27.5 mL of 0.5 M NH4NO3 for 4 h.Then, 0.5 mL of NH4OH and 15 mL of an ammonia solution of AgNO3 were added and the solutions were placed in a thermostatic bath at 70 °C for 7 h, allowing the slow and quantitative precipitation of Ag3PO4 crystals.Oxygen isotope compositions of silver phosphate crystals were measured using a varioPYROcube Elemental Analyzer interfaced in continuous flow mode to an Isoprime Isotopic Ratio Mass Spectrometer.For each sample, 5 aliquots of 300 µg of Ag3PO4 were mixed with 300 µg of pure graphite powder loaded in silver foil capsules.Pyrolysis was performed at 1450 °C.Measurements have been calibrated against silver phosphate precipitated from the NBS120c (natural Miocene phosphorite from Florida), as well as with the NBS127 (barium sulfate precipitated using seawater from Monterey Bay, CA, USA).The value of NBS120c was fixed at 21.7‰ (V-SMOW; Vienna Standard Mean Ocean Water) according to Lécuyer et al. [43] and that of NBS127 set at the value of 9.3‰ V-SMOW [44] for correction of instrumental mass fractionation during CO isotopic analysis.Silver phosphate precipitated from standard NBS120c along with the silver   Apatite samples were prepared following the wet chemistry protocol described in Lécuyer [42].For each sample, an aliquot of 30 mg of apatite powder was dissolved in 2 mL of 2 M HF.The CaF 2 residue was separated by centrifugation and the solution neutralized by adding 2.2 mL of 2 M KOH.Amberlite™ anion-exchange resin beads were added to the solution to isolate the PO 4 3− ions.After 24 h, the solution was removed, the resin was rinsed and eluted with 27.5 mL of 0.5 M NH 4 NO 3 for 4 h.Then, 0.5 mL of NH 4 OH and 15 mL of an ammonia solution of AgNO 3 were added and the solutions were placed in a thermostatic bath at 70 • C for 7 h, allowing the slow and quantitative precipitation of Ag 3 PO 4 crystals.Oxygen isotope compositions of silver phosphate crystals were measured using a varioPYROcube Elemental Analyzer interfaced in continuous flow mode to an Isoprime Isotopic Ratio Mass Spectrometer.For each sample, 5 aliquots of 300 µg of Ag 3 PO 4 were mixed with 300 µg of pure graphite powder loaded in silver foil capsules.Pyrolysis was performed at 1450 • C. Measurements have been calibrated against silver phosphate precipitated from the NBS120c (natural Miocene phosphorite from Florida), as well as with the NBS127 (barium sulfate precipitated using seawater from Monterey Bay, CA, USA).The value of NBS120c was fixed at 21.7‰ (V-SMOW; Vienna Standard Mean Ocean Water) according to Lécuyer et al. [43] and that of NBS127 set at the value of 9.3‰ V-SMOW [44] for correction of instrumental mass fractionation during CO isotopic analysis.Silver phosphate precipitated from standard NBS120c along with the silver phosphate samples derived from fossil bioapatites were repeatedly analyzed (δ 18 O p = 21.70 ± 0.30‰, n = 4) to ensure that no isotopic fractionation occurred during the wet chemistry.Data are reported as δ 18 O values vs. V-SMOW (in ‰ δ units).
In order to remove potential organic contaminant as well as secondarily precipitated calcite, aliquots of about 10 mg of apatite powder were treated using the protocol of Koch et al. [45].Powders were reacted with a 2% NaOCl solution to remove organic matter, then rinsed five times with double deionized water and air-dried at 40 • C for 24 h.Acetic acid (0.1 M) was then added and left for 24 h, after which the powder was again rinsed five times with double deionized water and air-dried at 40 • C for 24 h.For both treatments, the powder/solution ratio was kept constant at 0.04 g mL −1 .The measurements were performed using an isoFLOW system connected online in continuous flow mode to a precisION mass spectrometer.For each sample, two aliquots of 2 mg of pretreated apatite and 300 µg of eggshell calcite powders were loaded in 3.7 mL soda glass vials, round bottomed with exetainers caps, and were reacted with oversaturated anhydrous phosphoric acid.The reaction took place at 90 • C in a temperature regulated sample tray.The CO 2 gas generated during the acid digestion of the carbonate sample was then transferred to the mass spectrometer via a centrION interface.Calibrated CO 2 gas was used as a monitoring gas.Typical reproducibility was 0.05‰ and 0.07‰ for δ 13 C and δ 18 O measurements, respectively.The calibrated materials used were Carrara Marble (δ 18 O V-PDB = −1.84‰;δ 13 C V-PDB = +2.03‰;[46]) and NBS18 (δ 18 O V-PDB = −23.2‰;δ 13 C V-PDB = −5.01‰).Isotopic compositions are quoted in the standard δ notation relative to V-PDB for carbon and V-SMOW for oxygen.

Results
Dinosaur teeth and eggshell, as well as fish scale oxygen and carbon isotope compositions are given in Table 1.The oxygen isotope composition of environmental water calculated using apatite phosphate-water [24] as well as eggshell calcite-water [25] oxygen isotope fractionation equations for birds (dinosaur extant relatives) are also provided in Table 1.Interestingly, environmental waters estimated from eggshell calcite have the lowest δ 18 O w values from −17.0‰ to −12.2‰, theropod dinosaurs have intermediate δ 18 O w values of −13.5‰ and −12.3‰, and plant-eating hadrosaurids and ankylosaurs have higher δ 18 O w values ranging from −9.8‰ to −7.5‰.It is worth noting that the hadrosaurid tooth KK06 yielded a δ 18 O w value of +1.0‰, corresponding to a highly evaporated water source.

Primary Preservation of the Carbon and Oxygen Isotope Compositions of Tooth Apatite and Eggshell Calcite
Based on the following considerations, it is assumed that both carbon and oxygen of tooth apatite and eggshell calcite have preserved at least part of their pristine stable isotope compositions: 1.
Oxygen isotope compositions of tooth phosphate show a large range of variation from 9.6‰ to 22.6‰, precluding any re-equilibration with diagenetic fluids that would tend to homogenize the oxygen isotope compositions of phosphate towards a possible diagenetic end member [47].

2.
Oxygen isotope compositions of tooth phosphate and corresponding structural carbonate are linearly correlated with a slope close to unity and an offset of 6‰ to 9‰ (Figure 2).This matches the expected fractionation of 8-9‰ observed between phosphate and carbonate in extant vertebrates [48][49][50].

3.
The relative amount of carbonate in dinosaur apatites estimated from the measured CO 2 peak intensity of the mass spectrometer ranges from 4.4 Wt% (weight percent) to 8.6 Wt% (Table 1), within the expected range of 2-13 Wt% measured in extant vertebrates [51][52][53].A higher amount would have indicated a contamination of the apatite carbonate stable isotope compositions with diagenetic calcite that would not have been removed during the chemical cleaning.

4.
No correlation is observed between the carbon and oxygen isotope compositions of eggshell calcite that would hint to a partial re-equilibration with environmental diagenetic fluids [54].

5.
Instead, a significant isotopic clustering is observed among analyzed taxa (Figure 3) and supports the preservation of an ecological signal in carbon isotopes reflecting diet preferences and in oxygen isotopes reflecting drinking water sources [33].Therefore, we consider that both oxygen and carbon isotope compositions of fossil teeth and eggshells are mostly pristine and can be interpreted in terms of dinosaur ecology and environmental conditions.

Environmental Conditions in the Kakanaut Area during the Latest Cretaceous
In a recent quantitative analysis of the Kakanaut palaeoflora using the Climate Leaf Analysis Multivariate Program (CLAMP), Zolina et al. [10] calculated a mean annual air temperature (MAAT) of 12.2 ± 2.0 • C for the Kakanaut area, located during the Maastrichtian at a paleolatitude of about 75 • N [40].This temperature of 12.2 ± 2.0 • C would correspond today to a mean annual meteoric water δ 18 O mw value of −8.4 ± 1.0‰, according to the recently established δ 18 O mw -MAAT relationship [55].Interestingly, the average local environmental water δ 18 O w value estimated from the δ 18 O p values of dinosaur phosphates has a similar value of −8.2 ± 4.7‰ (N = 7).Dinosaur teeth are continuously replaced during life and take several months to grow [56], thus recording in their bulk oxygen isotope composition of phosphate an average of the water δ 18 O w values ingested slightly before and during their mineralization time.Such a pattern was evidenced by the seasonal δ 18 O p variations previously measured along the growth axis of various dinosaur teeth [27,57,58].It can, therefore, be assumed that the average δ 18 O p value of dinosaur teeth reflects the mean δ 18 O w value of local surface waters and that these ingested waters are of meteoric origin.The consistency of both air temperatures provided by Zolina et al. [10] and δ 18 O w value estimated from dinosaur δ 18 O p can be tested using the δ 18 O p value measured on three bulk scales of lepisosteids (Table 1).The measured value of 14.2‰ indicates that these scales have mineralized from the local water δ 18 O w value of −8.2‰ at a temperature of about 17 • C according to the phosphate-water temperature scale proposed by Lécuyer et al. [59].This temperature is higher than the mean annual temperature of 12.2 • C but close to the warmest month mean temperature of 20.6 ± 2.5 • C estimated using the CLAMP method [10].Considering that the optimal growth period of extant lepisosteids occurs during the warm season [60], the measured δ 18 O p value is consistent with the rest of the dataset and the temperature estimates provided by Zolina et al. [10].We can reasonably consider that the sinusoid-like seasonal pattern in mean annual temperatures and meteoric water δ 18 O mw values experienced today at mid to high latitudes [61] prevailed during the Cretaceous [27,58,62].It follows that the calculated average meteoric water δ 18 O mw annual value of about −8.2‰ would also correspond to the values recorded during the inter-seasons (mid-spring or mid-autumn).The anomalously high δ 18 O p value of the tooth KK06 will need further studies beyond the scope of this paper to be correctly interpreted.All we can speculate is that this value may hint at a migratory behavior of this individual that likely spent some time in more arid areas, such as more inland, at lower latitude or in highland regions, while ingesting vegetation characterized by 18 O-enriched leaf water due to local evaporation and low amount of precipitation.In such areas, leaf water can be 18 O-enriched by up to 20‰ relative to local rainwater or groundwater [63].
Considering the reconstructed range in δ 18 O mw values for the Kakanaut area during the latest Cretaceous, the very low water δ 18 O w values ranging from −17.0 to −12.2‰, derived from the δ 18 O c values of eggshell carbonates of the two ootaxa Spheroolithidae and Prismatoolithidae, most likely represent winter waters.The Kakanaut dinosaurs probably laid their eggs at the beginning of spring because egg laying during winter seems unlikely due to freezing temperatures, prolonged or near darkness lasting about 2-3 months [8,9] and limited food availability.The waters ingested by egg-laying females and characterized by a winter isotopic signature could correspond to melted snow supplying local rivers and lakes.
The carbon isotope compositions of teeth and eggshells may also support an egglaying period at the beginning of spring.Considering that spheroolithid eggs were laid by hadrosaurs and prismatoolithid ones by theropods [11], measured eggshell δ 13 C c values are lower than those of the teeth of corresponding taxa (Figure 3), implying a consumption of food with a lower δ 13 C value prior to or during eggshell mineralization.It has been documented that leaf δ 13 C values of C 3 plants vary seasonally, with late spring and summer leaves having δ 13 C values up to 6‰ higher than autumn leaves [64], but this tendency does not seem to be a general trend [65].This high seasonal variability in extant C 3 leaf δ 13 C values could at least partly explain the 6.2‰ range of measured carbon isotope compositions of herbivorous dinosaur teeth (hadrosaurs and ankylosaurs), reflecting different timing and periods of tooth mineralization.It has also been observed that spring buds also have a δ 13 C value that can be significantly lower than leaves growing later during the year [66].Seasonal variations in δ 13 C values of leaves available for consumption, therefore, suggest that females consumed available early spring foliage when they produced their eggs.
Studies on the duration of egg incubation among dinosaurs show contrasting results.The duration has been estimated to last from a few weeks for small dinosaurs to three months for larger ones based on the size of the hatchling and assuming that dinosaurs possessed a bird-grade physiology [19].Incubation lasting up to 6 months has also been estimated for some hadrosaurids based on daily incremental line count in tooth dentine that would imply a slow, reptile-grade development [18].Whatever incubation duration is considered, laying eggs at the very beginning of spring would allow high latitude dinosaurs enough time for the hatchlings to benefit from a maximized period during which food availability and climate were most favorable for survival (Figure 4).It would allow them to reach a body size large enough to tolerate the harsh next winter period, either by migrating to lower latitudes for large species that were biomechanically and energetically capable of doing so or by overwintering under near-freezing to freezing conditions, with limited food availability and prolonged darkness [14,67].
are lower than those of the teeth of corresponding taxa (Figure 3), implying a consumption of food with a lower δ 13 C value prior to or during eggshell mineralization.It has been documented that leaf δ 13 C values of C3 plants vary seasonally, with late spring and summer leaves having δ 13 C values up to 6‰ higher than autumn leaves [64], but this tendency does not seem to be a general trend [65].This high seasonal variability in extant C3 leaf δ 13 C values could at least partly explain the 6.2‰ range of measured carbon isotope compositions of herbivorous dinosaur teeth (hadrosaurs and ankylosaurs), reflecting different timing and periods of tooth mineralization.It has also been observed that spring buds also have a δ 13 C value that can be significantly lower than leaves growing later during the year [66].Seasonal variations in δ 13 C values of leaves available for consumption, therefore, suggest that females consumed available early spring foliage when they produced their eggs.
Studies on the duration of egg incubation among dinosaurs show contrasting results.The duration has been estimated to last from a few weeks for small dinosaurs to three months for larger ones based on the size of the hatchling and assuming that dinosaurs possessed a bird-grade physiology [19].Incubation lasting up to 6 months has also been estimated for some hadrosaurids based on daily incremental line count in tooth dentine that would imply a slow, reptile-grade development [18].Whatever incubation duration is considered, laying eggs at the very beginning of spring would allow high latitude dinosaurs enough time for the hatchlings to benefit from a maximized period during which food availability and climate were most favorable for survival (Figure 4).It would allow them to reach a body size large enough to tolerate the harsh next winter period, either by migrating to lower latitudes for large species that were biomechanically and energetically capable of doing so or by overwintering under near-freezing to freezing conditions, with limited food availability and prolonged darkness [14,67].Another implication of laying eggs early during spring at high latitudes is that eggs cannot incubate by solar radiance alone, and additional sources of heat have to be used to supplement the need for the embryos to develop under a sufficient incubation temperature.Small theropods and small ornithischians might have been able to brood their eggs by lying on them and transferring their body heat to the clutch [16].Large species such as tyrannosaurids and hadrosaurids might have used alternative heat sources, such as nest mounds using fermentation of plant debris covering the clutches to warm up the nest [2,8].
This study highlights some crucial aspects of dinosaur reproduction at high latitudes, such as those from the latest Cretaceous Kakanaut area that had to accommodate their reproductive strategies to the challenging environments of high latitudes in terms of timing of egg laying and incubation method.

Conclusions
The discovery of Cretaceous dinosaur eggshell fragments in high palaeolatitude localities constitutes the most compelling evidence for their reproductive behavior.Oxygen and carbon stable isotope compositions of eggshell calcite and associated adult teeth apatite provided temporal constraint on the egg-laying strategies used by Kakanaut dinosaurs.Our results show that eggs were most likely laid in early spring, giving time for the hatchling to grow large enough to survive the harsh next winter period and possible southwards migration.Early spring egg laying implies nesting and incubation methods using enhanced heat sources, such as body heat transfer by brooding or nest mounds constructed of plant debris that produced heat by bacterial fermentation.The occurrences of high latitude reproduction among dinosaurs, as well as the inferred egg laying and nesting strategies in these challenging environments, open questions about the global pattern of dinosaur diversity at high latitudes and especially the conspicuous absence of some taxa, such as sauropods, above 50 • of latitude [70].Further studies on nesting strategies used by these dinosaurs might clarify if a causal link exists between their geographic distribution and possible thermal limitations in their egg incubation method and duration.

Table 1 .
Carbon and oxygen isotope compositions of apatite phosphate (δ18 O p ) and carbonate (δ 13 C c , δ 18 O c ) and eggshell calcite from vertebrates reported along with the weight percent of apatite-bound carbonate, sample number, apatite material and taxonomy.The last column corresponds to the oxygen isotope composition of water (δ 18 O w ) estimated from the δ 18 O p value of tooth apatite phosphate or the δ 18 O c value of eggshell calcite using existing fractionation equations (see text).

Figure 2 .
Figure 2. Oxygen isotope compositions of structural carbonate (δ 18 O c ) of all analyzed vertebrate apatites plotted against their corresponding oxygen isotope compositions of phosphate (δ 18 O p ).

Figure 3 .
Figure 3. Oxygen isotope compositions of local water (δ 18 O w ) estimated from the δ 18 O c values of dinosaur eggshells (triangles) and tooth apatite phosphate (circles), reported against the carbon isotope compositions of eggshell calcite or tooth apatite carbonate (δ 13 C c ).The black horizontal bar corresponds to the range of water δ 18 O w values estimated from the intra-tooth δ 18 O p value variation measured on the tyrannosaurid tooth KK12 [27].

Figure 4 .
Figure 4. Incubation periods of the eggs from the troodontid (orange arc) and hadrosaurid (blue arc) taxa are drawn based on the present study and the incubation duration estimated for both taxa [18,68], superimposed on the summary graphic of the annual cycle of light, temperature and phenology in the early Maastrichtian at 76° N published by Herman et al. [69].The outer ring shows

Figure 4 .
Figure 4. Incubation periods of the eggs from the troodontid (orange arc) and hadrosaurid (blue arc) taxa are drawn based on the present study and the incubation duration estimated for both taxa [18,68], superimposed on the summary graphic of the annual cycle of light, temperature and phenology in the early Maastrichtian at 76 • N published by Herman et al. [69].The outer ring shows the variations in insolation and the red numbers indicate the hours each day (24 h period) when the sun is above the horizon.The inner rings show the temperature regime.The solid red line shows the average temperature variations based on interpolations from the mean annual temperature, the cold month mean and the warm month mean temperatures.The pink line shows the estimated short-term temperature variations based on tree ring data.The center of the diagram shows the proportion of the year when plant growth and dormancy occurred.