THE ANATOMICAL RECORD 295:610–614 (2012)
Hadrosaurs Were Perennial Polar Residents ANUSUYA CHINSAMY,1* DANIEL B. THOMAS,1 ALLISON R. TUMARKIN-DERATZIAN,2 AND ANTHONY R. FIORILLO3 1 Department of Zoology, University of Cape Town, Rondebosch 7701, Cape Town, South Africa 2 Department of Earth and Environmental Science, Temple University, Philadelphia, Pennsylvania 3 Paleontology Department, Museum of Nature and Science, Dallas, Texas
ABSTRACT Recent biomechanical evidence has fuelled debate surrounding the winter habits of the hadrosaurian dinosaur Edmontosaurus (ca. 70 Ma). Using histological characteristics recorded in bone, we show that polar Edmontosaurus endured the long winter night. In contrast, the bone microstructure of temperate Edmontosaurus is inconsistent with a perennially harsh environment. Differences in the bone microstructure of polar and temperate Edmontosaurus consequently dispute the hypothesis that polar populations were migratory. The overwintering signal preserved in the microstructure of polar Edmontosaurus bone offers significant insight into the life history of dinosaurs within the Late Cretaceous Arctic. Anat C 2012 Wiley Periodicals, Inc. Rec, 295:610–614, 2012. V
Key
words: Alaska; dinosaur; Edmontosaurus; migration; overwintering
INTRODUCTION 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. C 2012 WILEY PERIODICALS, INC. V
histology;
Polar Edmontosaurus from Prince Creek Formation (69.5 6 1.5 Ma) (Conrad et al., 1990; Flaig et al., 2011) was contrasted against temperate Edmontosaurus from Horseshoe Canyon Formation (70.0 6 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 Additional Supporting Information may be found in the online version of this article. Grant sponsor: National Research Foundation of South Africa, University of Cape Town; Grant number: NRF 449538; Grant sponsor: National Science Foundation; Grant number: NSF OPP 0424594. *Correspondence to: Anusuya Chinsamy, Department of Zoology, University of Cape Town, Private Bag X3, Rondebosch 7701, Cape Town, South Africa. E-mail:
[email protected] Received 25 May 2011; Accepted 22 December 2011. DOI 10.1002/ar.22428 Published online 17 February 2012 in Wiley Online Library (wileyonlinelibrary.com).
PERENNIAL POLAR HADROSAURS
611
Fig. 1. Polar and temperate localities of Edmontosaurus during the the Maastrichtian (70 ma). Palaeogeographic data from Scotese, 2002.
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 6 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
612
CHINSAMY ET AL.
Fig. 2. Polar Edmontosaurus histology showing alternating cycles of reticular fibro-lamellar bone (R) and circumferential fibro-lamellar (C) bone. (a,b) femora (DMNH 22557; plane polarized light, and AK-83-V014; cross-polarized light) and (c) tibia (DMNH 22383; cross-polarized
light with sensitive tint plate). Images are oriented from peripheral edge of the bone (top) toward mid-compacta, and represent a transverse section of diaphysis. Original outer bone surface of AK-83-V-014 has been eroded.
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
PERENNIAL POLAR HADROSAURS
Fig. 3. Variable histology of temperate Edmontosaurus, showing no [a; UALVP 47920], one [b; UALVP 52731] and several [c; UALVP 52696] cycles of reticular fibro-lamellar (R) and circumferential fibro-lamellar bone (C).
Arctic latitudes. The switch between histological textures is consistent with polar winter darkness and subsequent, periodic reductions in the nutritional qual-
613
ity 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 6 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
614
CHINSAMY ET AL.
demanding reticular FLB, to a relatively slower-formed FLB with circumferentially oriented channels (ChinsamyTuran, 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.
ACKNOWLEDGEMENTS 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.
LITERATURE CITED Alexander RM. 1998. When is migration worthwhile for animals that walk, swim or fly? J Avian Biol 29:387–394. Alexander RM. 2002. The merits and implications of travel by swimming, flight and running for animals of different sizes. Integr Comp Biol 42:1060–1064. Bell PR, Snively E. 2008. Polar dinosaurs on parade: a review of dinosaur migration. Alcheringa 32:271–284. Brouwers EM, Clemens WA, Spicer RA, Ager TA, Carter LD, Sliter WV. 1987. Dinosaurs on the north slope, Alaska—high-latitude, latest Cretaceous environments. Science 237:1608–1610. Chapin FS, III, Van Cleve K, Tieszen LL. 1975. Seasonal nutrient dynamics of tundra vegetation at Barrow, Alaska. Arctic Alpine Res 7:209–226. Chinsamy-Turan A. 2005. The microstructure of dinosaur bone: deciphering biology with fine-scale techniques. Baltimore: Johns Hopkins University Press. Chinsamy A, Raath MA. 1992. Preparation of fossil bone for histological examination. Palaeontol Afr 29:39–44. Chinsamy A, Rich T, Vickers-Rich P. 1998. Polar dinosaur bone histology. J Vertebr Paleontol 18:385–390. Conrad JE, McKee EH, Turrin BD. 1990. Age of tephra beds at the Ocean Point Dinosaur Locality, North Slope, Alaska, based on K-Ar and 40Ar/39Ar analyses. US Geol Surv Bull C1–C12. Eberth DA, Currie PJ. 2010. Stratigraphy, sedimentology, and taphonomy of the Albertosaurus bonebed (upper Horseshoe Canyon Formation; Maastrichtian), southern Alberta, Canada. Can J Earth Sci 47:1119–1143.
Erickson GM. 1996. Incremental lines of von Ebner in dinosaurs and the assessment of tooth replacement rates using growth line counts. Proc Natl Acad Sci USA 93:14623–14627. Fiorillo AR, Gangloff RA. 2000. Theropod teeth from the Prince Creek Formation (Cretaceous) of Northern Alaska, with speculations on arctic dinosaur paleoecology. J Vertebr Paleontol 20:675–682. Fiorillo AR, Gangloff RA. 2001. The caribou migration model for Arctic hadrosaurs (Dinosauria: Ornithischia): a reassessment. Hist Biol 15:323–334. Fiorillo AR, McCarthy PJ, Flaig PB. 2010. Taphonomic and sedimentologic interpretations of the dinosaur-bearing Upper Cretaceous strata of the Prince Creek Formation, Northern Alaska: insights from an ancient high-latitude terrestrial ecosystem. Palaeogeogr Palaeocl Palaeoecol 295:376–388. Fiorillo AR, Tykoski RS. A new species of centrosaurine ceratopsid Pachyrhinosaurus from the north slope (Prince Creek Formation: Maastrichtian) of Alaska: Acta Palaeo Polonica. doi: 10.4202/ app.2011.0033. Flaig PP, McCarthy PJ, Fiorillo AR. 2011. A tidally influenced, high-latitude alluvial/coastal plain: the Late Cretaceous (Maastrichtian) Prince Creek Formation, North Slope, Alaska. In: North C, Davidson S, Leleu S, editors. From river to rock record: the preservation of fluvial sediments and their subsequent interpretation. SEPM Special Publication, Tulsa, Oklahoma, 97. p 233–264. Gangloff RA, Fiorillo AR, Norton DW. 2005. The first pachycephalosaurine (Dinosauria) from the paleo-Arctic of Alaska and its paleogeographic implications. J Paleontol 79:997–1001. Horner JR, de Ricqle`s A, Padian K. 1999. Variation in dinosaur skeletochronology indicators: implications for age assessment and physiology. Paleobiol 25:295–304. Hotton N, III. 1980. An alternative to dinosaur endothermy: the happy wanderers. In: Thomas RDK, Olson EC, editors. A cold look at warm-blooded dinosaurs. Boulder: Westview Press. p 311–350. Miller PC, Tieszen L. 1972. A preliminary model of processes affecting primary production in the Arctic Tundra. Arctic Alpine Res 4:1–18. Molnar RE, Wiffen J. 1994. A late cretaceous polar dinosaur fauna from New Zealand. Cret Res 15:689–706. Scotese CR. 2002. PALEOMAP website. Available at: http://www. scotese.com. Spicer RA, Parrish JT. 1990. Late Cretaceous Early Tertiary paleoclimates of northern high-latitudes—a quantitative view. J Geol Soc 147:329–341. Starck JM, Chinsamy A. 2002. Bone microstructure and developmental plasticity in birds and other dinosaurs. J Morphol 254:232–246. Wikelski M, Tarlow EM, Raim A, Diehl RH, Larkin RP, Visser GH. 2003. Costs of migration in free-flying songbirds. Nature 423:704. Witte KW, Stone DB, Mull CG. 1987. Paleomagnetism, paleobotany, and paleogeography of the Cretaceous, North Slope, Alaska. In: Tailleur I, Weimer P, editors. Alaska North Slope Geology: Pacific Section, Society of Economic Paleontologists and Mineralogists and the Alaska Geological Society. Bakersfield, California, p 571– 579.
