COMMENTARY
COMMENTARY
The curious case of the Arctic mastodons Duane Froese1 Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, AB, Canada T6G 2E3
In 1796, the French anatomist Georges Cuvier sparked widespread interest in the idea that many organisms, including some large mammals, had gone extinct in the recent geologic past (1). He proposed, based on the morphology and function of molars, that African and Indian elephants were separate species and that they were distinct from at least two additional elephants known only from fossils: taxa that we now recognize as mammoths (Mammuthus sp.) and the American mastodon (Mammut americanum). Cuvier reasoned that because these fossils were typically well-preserved and often found at shallow depths, they had likely disappeared recently as a result of environmental changes affecting their habitat. Since that time, the timing of the disappearance of these iconic megafauna in relation to the two leading hypotheses, namely environmental changes vs. the potential role of humans, has been central to trying to understand the late Pleistocene extinctions 10,000 14C (radiocarbon) y ago, a time in which about 70% of largebodied mammals went extinct in North America (2). The article by Zazula et al. (3) in PNAS tackles a longstanding enigma of mastodon biogeography: namely, the curious presence of mastodons in Arctic Alaska and the Yukon during Late Pleistocene full-glacial conditions, a time when there should have been no suitable habitat to support them. In an elegant piece of detective work, Zazula et al. demonstrate convincingly that these mastodons were not in the wrong place, but rather—because of problems in the radiocarbon dating of some of the fossils—they are simply of the wrong time. Of Mammoths and Mastodons
The woolly mammoth (Mammuthus primigenius) is far and away the most common probiscidean found in northern Canada and Alaska. Mastodons are present in this region, and perhaps even underreported because most of their fossils are not easily distinguished from mammoths in the field. Mammoths and mastodons diverged more than 20 million y ago, and whereas the woolly mammoth underwent much of its evolution in the Arctic (4), the mastodon occupied www.pnas.org/cgi/doi/10.1073/pnas.1422018112
continental North America, eventually evolving into the American mastodon. Despite the success of the lineage, the mastodon never crossed back into the Old World. Mastodons were smaller than mammoths, bearing a sloped forehead, straighter and shorter tusks, and they are, as Cuvier (1) noted, easily distinguished from mammoths by their teeth. Mastodon molars have two rows of raised and rounded cusps that were effective at crushing branches and leaves (Fig. 1). This morphology is consistent with their dietary preference as browsers. Their fossils are found across North America, but have a concentrated occurrence south of the Great Lakes, where coniferous forests, bogs, and marshes characterized the Late Pleistocene environment (5). Mammoths were larger than mastodons both in body and tusk size, and had teeth with a flatter morphology characterized by low enamel ridges across their width (Fig. 1), reflecting a dietary preference as a grazer of grasses and forbs (6). South of the ice sheets, at least three species of mammoths were present that are largely associated with grasslands or parkland ecosystems (7). In the north though, in the nonglaciated area of Alaska and Yukon referred to as eastern Beringia, only the woolly mammoth was present in the Late Pleistocene. The woolly mammoth occupied eastern Beringia, an area characterized by steppe-tundra, an expansive grass and forb-rich biome, and ranged repeatedly across the Bering land bridge with Eurasia (6, 8). Herein lies the problem that Zazula et al. (3) address: within this region of Arctic mammoths, the fossils of mastodons regularly appear in collections, but what is their significance? Mastodon fossils occur much less frequently compared with the most common large herbivores of eastern Beringia, such as mammoth, horse, and bison, and at least some have radiocarbon dates between 35,000 and 18,000 14C y B.P. This time represents the interval leading to the height of the last glacial maximum, when multiple lines of evidence indicate that Eastern Beringia was a cold, dry steppe-tundra environment presumably lacking in mastodon-suitable habitat (6, 9). Given this environmental setting, along with the adaptations and dietary preferences
Fig. 1. Sketch of American mastodon (Top) and mammoth (Bottom) molars by Cuvier. Mastodon molars show a browser morphology specialized for crushing branches and leaves of trees and shrubs, whereas mammoth molars have the morphology of a grazer adapted to grasses and forbs. A few mastodon fossils appear in the late Pleistocene of northwestern North America (Alaska and Yukon), dating to a time when the vegetation was dominated by grasses and forbs and mammoths were common. Zazula et al. (3) resolve this problem by demonstrating that mastodons in this region date to a much earlier time, when boreal forest was present.
of mastodons, just what were they doing in the Arctic at this time? Or, as Zazula et al. (3) ask, were they actually in the Arctic at this time? Importance of Accurate Ages to Understand Extinction
The concentration of Quaternary fossils in most geologic records is so sparse that we depend on the ages of detrital fossils from radiocarbon dating to estimate the timing of extirpation or extinction (e.g., refs. 10 and 11). Since the 1980s these estimates have improved with the advent of accelerator mass spectrometry radiocarbon dating. This method allows smaller samples to be dated with greater precision, and in the case of Author contributions: D.F. wrote the paper. The author declares no conflict of interest. See companion article on page 18460. 1
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PNAS | December 30, 2014 | vol. 111 | no. 52 | 18405–18406
bones and teeth, this has been especially important because dating can focus on particular organic compounds, components that are less likely to be contaminated with extraneous carbon from the environment (12). The Zazula et al. (3) paper exploits what has become standard for high-quality radiocarbon dating of bones and teeth: ultrafiltration of the collagen. This technique, pioneered in the late 1980s (13), separates the higher molecular weight proteins from shorter fragments that are most commonly the source of contaminants that have infiltrated the bone following burial. Because these contaminants may be sourced from the environment and not the organism, they may be of a different (and typically younger) age, so their removal is critical to determine an accurate date. This aspect is particularly true for fossils beyond a few half-lives in age (one 14 C half-life = 5,730 y), for which even a small amount of contamination with younger carbon can make an old fossil date appear tens of thousands of years younger than it is. Zazula et al.’s (3) use of this protocol when applied to dating the “young” mastodons from the Arctic, demonstrates that most of these fossils are in fact beyond the practical limit of radiocarbon dating (>∼50,000 y). However, interestingly even with the use of ultrafiltration, several fossils still appear sufficiently young to give the impression that mastodons were present around the time of the last glacial maximum. For these last few specimens Zazula et al. (3) use a more involved separation to isolate the single amino acid hydroxyproline, a bone-specific biomarker that is highly specific to bone protein collagen and, hence, unlikely to represent exogenous contamination (14). This approach proved the remaining “young” mastodon specimens as being either near or beyond background detection limits, in keeping with the population of redated specimens. Thus, the paper by Zazula et al. (3) removes any compelling evidence for the presence of mastodons during the height of the last glacial maximum in eastern Beringia. Waxing and Waning Megafaunal Populations and Environmental Change
Most evidence bearing on the causal mechanisms underlying extinction or extirpation of Pleistocene megafauna is largely circumstantial: the age of a fossil’s last occurrence is correlated to external events without direct proof of their association. In the case of the Pleistocene megafauna, the two leading hypotheses are the appearance of humans and their impact, or environmental changes accompanying the last termination. The evi-
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dence presented by Zazula et al. (3) clearly shows that all dated mastodons from the north predate the arrival of humans by tens of millennia, and most likely date to the last interglacial period (125,000– 75,000 y ago) when boreal forest and shrubs characterized eastern Beringia (15, 16). The corollary being that extirpation of the northern mastodons was quite independent of their extinction to the south of the ice sheets, where they survived until ∼10,000 14C y B.P. Zazula et al.’s (3) paper underscores the importance of establishing individual species’ responses to forcing mechanisms to understand the collective problem of the late Pleistocene megafauna extinctions. The regular oscillation of environmental extremes between boreal forest during interglacials and steppe-tundra during glacials has been established through diverse archives of late Quaternary environmental data in northwestern Canada and Alaska (17). Given the habitat preference of mastodons and mammoths, we predict that their populations similarly waxed and waned during these oscillations. In the case of grazers, one should expect an inverse response to that of a browser such as the mastodon; that is, the grazer populations should contract and browser populations expand during an interglacial as steppe-tundra is replaced by boreal forest. During the latest Pleistocene (14,000–10,000 14C y B.P.), when we have precise radiocarbon chronologies available, this was the case as elk and moose replaced mammoths and horses (10). However, what about during previous interglacials, like the one 125,000 y ago?
For more than a decade phylogeographic studies across space and time, elucidated from ancient DNA, have shown the complex history of species across the Arctic (18, 19). Based on genetic data, both mammoths and horses appear to have undergone population minima during the last interglacial, including an extirpation of some mammoths in Eurasia (8, 20). As the climate cooled after 75,000 y B.P. and steppe-tundra replaced boreal forest, it appears that both populations expanded (8, 21). However, these inferences are based on indirect data that still have large errors and relatively small numbers of individuals for most taxa. Zazula et al.’s (3) new dating provides a context for these models, while removing once and for all the confounding image of a large and specialized browser at a time of extensive steppe-tundra. Collectively, great progress has been made toward understanding the dynamics of the Late Pleistocene megafauna extinctions over the last decade (e.g., refs. 2, 10, 11, and 19). The debate has shifted from competing single hypotheses applied to all extinctions (e.g., ref. 22) toward an understanding that increasingly recognizes that complex, out-of-phase and species-specific responses of large mammals were the norm and not the exception. Given the central role of chronologies to this discussion, the Zazula et al. (3) paper leads the way by demonstrating the careful chronological cleansing of radiocarbon datasets that must be done to inform the future debate.
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