Dinosaurs from the North Slope of Alaska pose a biological enigma. The Alaskan North Slope has remained at high latitudes since the Late Cretaceous, when diverse dinosaur groups (Fiorillo and Gangloff, 2000, 2001; Gangloff et al., 2005; Fiorillo and Tykoski, in press) experienced a cold-temperate climate (Spicer and Parrish, 1990). Sunlight departed the ancient Arctic Circle for up to 6 months, however, and would have reduced the nutritional quality of overwintering foliage (Miller and Tieszen, 1972; Chapin et al., 1975). Explanations for the occurrence of dinosaur fossils on the North Slope consequently centre around whether or not they migrated (Hotton, 1980; Fiorillo and Gangloff, 2000, 2001; Bell and Snively, 2008). Migration was proposed to associate polar discoveries with the abundant congeneric remains at temperate latitudes (Hotton, 1980). Recent sedimentary evidence (Fiorillo et al., 2010) instead supported a polar presence for Edmontosaurus immediately after winter's end. Dinosaurian lifestyles have previously been interpreted from bone histology (Erickson, 1996; Chinsamy et al., 1998; Chinsamy-Turan, 2005). Here polar and temperate Edmontosaurus bone histology was examined for evidence of life history.
Polar Edmontosaurus from Prince Creek Formation (69.5 ± 1.5 Ma) (Conrad et al., 1990; Flaig et al., 2011) was contrasted against temperate Edmontosaurus from Horseshoe Canyon Formation (70.0 ± 3.0 Ma) (Eberth and Currie, 2010). Histological sections were made from seven femora, four humeri, and two tibiae from polar Edmontosaurus, and three femora and one tibia from temperate Edmontosaurus (see Supporting Information). Sections were prepared according to Chinsamy and Raath (1992): long bone segments were embedded in resin and cut to expose a desired section, the section was ground flat and affixed to a glass side, the bulk of the mounted specimen was separated from the glass slide, and the remaining sample ground to a histologically informative thickness. Polar Edmontosaurus was collected from 70°N and represents a paleolatitude of 78 ± 7°N (Brouwers et al., 1987; Witte et al., 1987); temperate Edmontosaurus from 53°N was buried at paleolatitude 60°N (Fig. 1) (Scotese, 2002).
RESULTS AND DISCUSSION
Bone histology of polar and temperate Edmontosaurus differed substantially (see Supporting Information). The compacta of polar Edmontosaurus exhibited fibro-lamellar bone (FLB) with a large number of channels that in life would have been occupied by blood vessels, and other connective tissue (Starck and Chinsamy, 2002). Periodic changes in channel organization, that is, from a reticular to a more circumferential orientation are evident in the compacta (Fig. 2). All studied sections of polar Edmontosaurus bone exhibited periodic textural shifts. The largest polar Edmontosaurus femur studied (DMNH 22557, maximum diameter of 110 mm; ∼65% adult size) exhibited eight cycles of alternating reticular and circumferential FLB. In contrast, texture switches were not consistently observed in the bones of temperate Edmontosaurus. The compacta of temperate Edmontosaurus comprised reticular FLB (femur), reticular FLB with occasional switches to circumferential FLB (femora), or alternating cycles of circumferential and reticular FLB (tibia) (Fig. 3). Lines of arrested growth were absent from both polar and temperate Edmontosaurus.
We consider three scenarios for explaining the histological differences between polar and temperate Edmontosaurus. (1) Both polar and temperate Edmontosaurus were migratory, and histological differences are effectively stochastic. Signals of migration in bone histology have not previously been reported, although perturbations to energy intake and other environmental stresses are known to influence bone growth (Starck and Chinsamy, 2002). The well documented energy demands of migration (Alexander, 1998; Alexander, 2002; Wikelski et al., 2003) are expected to alter bone growth and result in histological variation in a migrating animal. The occurrence of uninterrupted reticular FLB likely indicates that temperate Edmontosaurus was nonmigratory. (2) Edmontosaurus included migratory and nonmigratory populations, and histological differences between polar and temperate dinosaurs reflect the stress of migration in polar populations. The regular switch from fast deposited reticular FLB to slower forming circumferential FLB is consistent with periodically increased energy demands potentially associated with migration. (3) Polar Edmontosaurus overwintered at Arctic latitudes. The switch between histological textures is consistent with polar winter darkness and subsequent, periodic reductions in the nutritional quality of forage, which was not regularly encountered by temperate Edmontosaurus.
The variable histology of temperate Edmontosaurus suggests that energy intake and demand varied during the lives of some animals, and reflects occasional difficulties in sourcing forage. In contrast, polar Edmontosaurus histology consistently recorded textural changes, which probably reflects shifts in energy balance. Bone histology alone is inconclusive regarding overwintering or migration in polar Edmontosaurus; also, bone chemistry is too altered for rare earth elemental profiles or stable isotopic compositions to recover geographic feeding patterns (see Supporting Information). Rather, extrinsic evidence coupled with bone histology must be considered to reconstruct the life history of polar Edmontosaurus. Evidence supporting migration includes the geographic range of polar and temperate Edmontosaurus, and the accumulation of bonebeds (Bell and Snively, 2008).
Extrinsic support for overwintering is derived from large juvenile populations of polar Edmontosaurus containing individuals likely too small to migrate ahead of the descending winter darkness (Alexander, 1998; Fiorillo and Gangloff, 2001; Bell and Snively, 2008). Further, the multiple mass death accumulations of these dinosaurs occurred in a distinct paleogeographic polar setting, that of a warm coastal plain in close proximity to a towering mountain range (Fiorillo et al., 2010). The sedimentological dynamics of this setting resulted in a substantial spring snow melt from the nearby ancestral Brooks Range creating annual flooding (Fiorillo et al., 2010). Hence, polar Edmontosaurus was present in the Late Cretaceous Arctic immediately after winter and exposed to snow melt floods: indeed, most specimens that we have studied were recovered from early-spring melt deposits and died while depositing circumferential FLB (i.e., the “winter” bone tissue). Further, dinosaurs were physiologically tolerant of overwintering, as evidenced by New Zealand polar dinosaurs that were obliged to endure the long polar night (Molnar and Wiffen, 1994; Bell and Snively, 2008).
Overwintering is better supported than migration as a life history for polar Edmontosaurus. Textural switches observed in the histology of polar Edmontosaurus are consequently interpreted as signaling overwintering. Switches from circumferential to reticular FLB are not unique to Edmontosaurus; indeed, temperate Hypacrosaurus stebingeri (75.5 ± 9.0 Ma) also exhibits textural switches (Horner et al., 1999), which were gradational and separated by lines of arrested growth (LAGs) that directly indicate a suspension in growth (e.g., Chinsamy-Turan, 2005). Horner et al. (1999) interpreted LAGs as perennial occurrences and consequently calculated a growth rate for Hypacrosaurus. Hence we deduce that the switch from reticular to circumferential FLB texture was perennial, and may correlate with reduced nutritional quality of winter forage. Temperate Edmontosaurus inconsistently exhibited bone textural switches, which probably indicates that they occasionally faced nutritional shortages. Thus polar Edmontosaurus and temperate Hypacrosaurus endured perennial reductions in forage.
Our findings suggest that polar Edmontosaurus histology is more consistent with the overwintering scenario. The onset of polar winter and loss of verdancy likely shifted bone deposition from faster, more energetically demanding reticular FLB, to a relatively slower-formed FLB with circumferentially oriented channels (Chinsamy-Turan, 2005). Summer heralded renewed foliage that sustained the deposition of reticular bone. Hence, polar Edmontosaurus histology reflects energetic changes that may be linked to seasonal changes in the nutritional quality of forage above the ancient Arctic Circle.
The authors thank Sandra Jasinoski for comments, Ruth Berry for negotiating the loan to AC from the University of Alaska Museum, Philip Currie and Nicola Howard for loaning material from University of Alberta laboratory of Vertebrate Paleontology, field crews that helped collect specimens used in this study, and the Arctic Management Unit of the Bureau of Land Management for administrative support for the collection of specimens used in this study.