Invited Research ArticleDietary reconstruction and evidence of prey shifting in Pleistocene and recent gray wolves (Canis lupus) from Yukon Territory
Introduction
The Canadian Arctic and northern boreal forest ecosystems are among those most severely affected by anthropogenically-driven climate change (Screen and Simmonds, 2010; Simmonds, 2015; Rowland et al., 2016). These ecosystems are experiencing increases in mean annual temperature far exceeding that of the global average (Glig et al., 2012; Rowland et al., 2016) and landscape-scale ecosystem changes such as shrubification of tundra environments (Danby et al., 2011; Hope et al., 2015). The long-term impacts of anthropogenic climate change on northern biota are, however, as of yet uncertain; whether northern species can and will adapt to changing environmental conditions in the long-term remains unknown. What is certain, however, is that the effects will reach far beyond our lifetimes (i.e., centuries to millennia; Karl and Trenberth, 2003). The fossil record is our only resource for understanding the past responses of organisms to global change, offering insights into the vulnerability and resilience of ecosystems and species on timescales over which the effects of global change are expected to play out (Dietl et al., 2015; Lanier et al., 2015). In particular, the fossil records of the Pleistocene (>52.8 ka BP to 26.5 ka BP [±170 y BP]) and Holocene (1960s) provide unparalleled opportunities for understanding the ecological responses of extant species to global change.
Gray wolves (Canis lupus Linnaeus, 1758) are among the best studied extant carnivores and their present-day ecology is well-understood (Gauthier and Theberge, 1986; Hayes, 1995; Hayes et al., 2000; Paquet and Carbyn, 2003; Merkle et al., 2017; Dalerum et al., 2018; Gable et al., 2018; Zrzavy et al., 2018). Records from North America suggest that wolves crossed the Bering Land Bridge from Eurasia during the mid-Pleistocene (800 ka BP) (Kurtén, 1968; Tedford et al., 2009), but were restricted to northern parts of the continent until the late Pleistocene (~28 ka BP), potentially due to competitive exclusion by the now-extinct dire wolves (Canis dirus Leidy, 1858) (Meachen et al., 2016; Meachen et al., 2021; Perri et al., 2021). During much of the Holocene, gray wolves ranged from the Canadian Arctic to northern Mexico (Paquet and Carbyn, 2003; Wang and Tedford, 2010). However, they have been recently extirpated from large portions of their range by intense human hunting and habitat loss (Paquet and Carbyn, 2003; Vilà et al., 2003). Still, gray wolves are well-represented as both fossils (Tedford et al., 2009; Harington, 2011) and living animals (Carmichael et al., 2001; Hayes et al., 2003) in the Yukon Territory of Canada. Genomic evidence suggests that Pleistocene gray wolves in Yukon had affinity with other Pleistocene wolves of Eurasia and Beringia (Koblmüller et al., 2016; Meachen et al., 2021; Wang et al., 2020), and these Beringian populations gave rise to modern lower latitude populations following an expansion at the end of the Last Glacial Maximum, ~21 ka (Clark et al., 2012; Loog et al., 2020). Though the gray wolves that inhabit the Yukon today may be morphologically distinct (Leonard et al., 2007; Meachen et al., 2016; Meachen et al., 2021), it is unclear whether they were ecologically distinct. The records from the Yukon bracket major climate change and extinction events during the latest Pleistocene and early Holocene (Guthrie, 2006), through which gray wolves persisted, providing the opportunity for comparing their ecologies.
The climate of the Yukon during the late Pleistocene was generally cooler and drier than today (Zazula et al., 2006b; Zimov et al., 2012), which allowed for the development of open, largely treeless habitats dominated by steppe-like grasslands (Zimov et al., 1995; Zazula et al., 2003). The northern Yukon Territory was part of the mammoth steppe, a megacontinental ecosystem characterized by the presence of herbivorous megafauna (>44 kg) (Harington, 2011; Jürgensen et al., 2017; Schwartz-Narbonne et al., 2019). During this time, the interiors of Alaska and the Yukon were too dry to permit the establishment of continental glaciers and served as glacial refugia (Zazula et al., 2006b; Froese et al., 2009; Schwartz-Narbonne et al., 2019). Fossils of gray wolves are commonly recovered at Yukon localities associated with the mammoth steppe fauna, including those in the Old Crow Basin and the Klondike goldfields (Harington, 2011). During the Pleistocene to Holocene transition (~11.7 ka), the global climate became progressively warmer and wetter (Nogués-Bravo et al., 2008; Rabanus-Wallace et al., 2017). This climate shift led to a transition from steppe-tundra towards boreal forest ecosystems, though some tundra ecosystems still remain in the northern Yukon and in alpine regions (Rowland et al., 2016).
During the late Pleistocene, gray wolves had access to a variety of large-bodied herbivores as potential prey or carrion, including both now-extinct and extant species, such as horses (Equus sp. Linnaeus, 1758), steppe bison (Bison priscus Bojanus, 1827), woolly mammoths (Mammuthus primigenius Blumenbach, 1799), Dall sheep (Ovis dalli Nelson, 1884), muskox (Ovibos moschatus Zimmermann, 1780), helmeted muskox (Bootherium bombifrons Harlan, 1825), saiga antelope (Saiga tatarica Linnaeus, 1766), and caribou (Rangifer tarandus Linnaeus, 1758) (Harington, 2011; de Manuel et al., 2020). Wolves also coexisted with several large-bodied carnivorous species, including the cave lion (Panthera leo spelaean Goldfuss, 1810) and giant short-faced bear (Arctodus simus Cope, 1879) (Harington, 2011), with which they may have competed for prey resources (Ripple and Van Valkenburgh, 2010; Pardi and Smith, 2016). After the arrival of humans in North America at ~14 ka (Lanoë and Holmes, 2016), populations of several large-bodied mammals began to decline (Lorenzen et al., 2011), culminating in the Quaternary Megafaunal Extinction (Koch and Barnosky, 2006; Barnosky, 2008; Fox-Dobbs et al., 2008; Ripple and Van Valkenburgh, 2010; Mann et al., 2015). By ~11.7 ka, most of the Arctic megafauna had become extinct in the Yukon (Harington, 2011), with North America as a whole having lost ~72% of large-bodied mammal genera (Barnosky, 2008). There were widespread, landscape-scale ecological consequences of the megafauna extinction, including changes to plant biomes, fire regimes, nutrient and seed transport, and how species were ecologically associated (Piers et al., 2015; Doughty et al., 2016; Lyons et al., 2016; Piers et al., 2018; Tóth et al., 2019; Pineda-Munoz et al., 2021). Gray wolves are among the few large predators that survived this extinction (Harington, 2011; Pardi and Smith, 2016), alongside a ‘skeleton crew’ of prey species including caribou, moose (Alces alces Linnaeus, 1758), and elk (Cervus canadensis Erxleben, 1777) (Harington, 2011; Yeakel et al., 2013). Modern Yukon gray wolves are, however, increasingly threatened due to climate change (Callaghan et al., 2011; Glig et al., 2012), habitat loss (Paquet and Carbyn, 2003), and decreases in large ungulate abundances (Boulanger et al., 2011; Callaghan et al., 2011; Klaczek et al., 2016).
To our knowledge, there has been no long-term study that explicitly focused on the dietary ecology of gray wolves from the Yukon, and that encompass the timescales over which the effects of anthropogenic perturbation are expected to operate (i.e. tens of thousands of years); further, no study has attempted to compare the dietary ecology of ancient and present-day Yukon wolves. The objective of the present study is to characterize and compare the dietary ecology of Pleistocene and recent gray wolves from the Yukon as a means of understanding their response to the late Pleistocene through Holocene climatic and ecological disturbance. We characterize the dietary ecology of gray wolves using dental microwear analysis and stable isotope analysis of oxygen (δ18O), carbon (δ13C), and nitrogen (δ15N) from bone. We use Bayesian stable isotope mixing models to estimate the primary prey species consumed by wolves during the Pleistocene and compare the results to recent and present-day observational studies (Gauthier and Theberge, 1986; Hayes et al., 2016; Merkle et al., 2017). We offer new insight into the feeding ecology of wolves over a period characterized by significant climate change and shifts in prey availability, providing novel information on the ecological flexibility of gray wolves over thousands of years.
Section snippets
Dental microwear analysis
Dental microwear analysis is the quantification of the patterns of microscopic wear in teeth generated by chewing (Walker et al., 1978). Animal diets are inferred based on reliable relationships between the relative proportions of scratches and pits and preferred food type (Walker et al., 1978; Grine, 1986; Van Valkenburgh et al., 1990; Solounais and Semprebon, 2002; Merceron et al., 2005; Fraser et al., 2009; Schubert et al., 2010; Ungar et al., 2010). Wear patterns on the teeth provide a
Materials and Methods
We obtained specimens of Pleistocene gray wolves (n = 31) from the Yukon Territory from the Canadian Museum of Nature (CMN) Palaeobiology Collection and the Yukon Government (YG) Palaeontology Program Collection (Table S1). Samples from recent Yukon specimens (n = 17) were obtained from the CMN Zoology Collection (Table S2). Specimens were selected based on the following criteria: 1) at least one well-preserved P4 or m1; and 2) no large cracks visible along the shearing facet to be molded. Due
Results
A subset of Pleistocene wolves (selected based on shared localities) were 14C dated and all fell within the Middle Wisconsinan interstadial of Marine Isotope Stage 3 (Harington, 2011), ranging from >52.8 ka BP to 26.5 ka BP (±170 y BP) (Table S1). These ages place the Pleistocene wolves in a warmer interstadial period that occurred between two glacial maxima (Lemieux et al., 2008; Harington, 2011). One wolf that was initially assigned to the Pleistocene bin (YG 498.1) yielded a 14C date of
Discussion
During the late Pleistocene (15–11.7 ka), invasion of North America by humans (Guthrie, 2006; Lanoë and Holmes, 2016), climate changes (Allen et al., 2012; Clark et al., 2009) and the loss of 72% of large bodied mammal genera (Barnosky, 2008) had profound ecological consequence, which included changes to plant biomes, fire regimes, nutrient and seed transport, among others (Piers et al., 2015; Doughty et al., 2016; Lyons et al., 2016; Piers et al., 2018; Tóth et al., 2019; Pineda-Munoz et al.,
Conclusion
During the Quaternary Megafaunal Extinction (~11.7 ka), North America saw widespread, landscape-scale ecological changes that ultimately contributed to the loss of many species, including horses (Guthrie, 2006) and mammoths (Fisher, 1996; Koch and Barnosky, 2006). We show that extinction of much of the mammal megafauna during the Pleistocene to Holocene transition induced a dietary change among wolves. Recent Yukon wolves rely primarily on the extant large ungulates, caribou and moose (Gauthier
Credit author statement
Zoe Landry: Conceptualization, Methodology, Software, Validation, Formal Analysis, Investigation, Data Curation, Writing – Original Draft, Visualization, Project administration.; Sora Kim: Validation, Investigation, Resources, Writing – Review & Editing.; Robin B. Trayler: Methodology, Validation, Investigation, Resources, Writing – Review & Editing.; Marisa Gilbert: Resources, Writing – Review & Editing.; Grant Zazula: Resources, Writing – Review & Editing, Funding acquisition.; John Southon:
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
This research was funded by a Canadian Museum of Nature Research Activity Grant and Natural Sciences and Engineering Research Council of Canada Discovery Grant (RGPIN-2018-05305) awarded to DF, and by funds of the Yukon Palaeontology Program of the Yukon Department of Tourism and Culture, Canada. We acknowledge that Carleton University and the Canadian Museum of Nature (where statistical analyses and data collection took place, respectively) are located on the traditional unceded territory of
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