I re-evaluate the specific biogeographical significance of each of the land bridges (Beringia, Thulean and De Geer) in the Northern Hemisphere during the latest Cretaceous–early Cenozoic, showing that the Thulean and De Geer routes did not operate contemporaneously.
Northern Hemisphere landmasses.
I review the recent climatic, sea-level, geotectonic, palaeofloristic, and marine and terrestrial faunal data that have emerged since the establishment in the 1980s of the biogeographical concepts of the early Cenozoic Northern Hemisphere land bridges and present a synthesis supporting a revised scenario for early Cenozoic biogeographical development.
Palaeogeographical and geotectonic data, supported by strong floral and faunal evidence, suggest that the palaeogeographical and chronological frames for the formation of all three land bridges are different from those originally proposed. Dispersal events via the causeways seem to have taken place during specific time intervals resulting from fluctuations in sea level and climate.
The De Geer and Thulean routes were not contemporaneous. The former existed during the latest Cretaceous to the early Palaeocene, joining North America with Eurasia. The Thulean route became established well after the interruption of the De Geer route, offering a southerly connection between western Europe and North America in at least two episodes: c. 57 Ma and c. 56 Ma. The Bering route functioned in two warm periods: 65.5 Ma (coinciding with the De Geer route) and c. 58 Ma, during the Palaeocene (possible Eocene exposures are not considered here). The formation of the De Geer route explains faunal similarities between the Puercan and Torrejonian North American land mammal ages (NALMAs) and the Shanghuan Asian land mammal age (ALMA). The Thulean route explains faunal similarities between the Clarkforkian (Cf1) and Wasatchian (Wa0, 1) NALMAs, and the Cernaysian and Neustrian (PE I, II) European land mammal ages. The Bering route explains faunal similarities between the Gashatan ALMA and the Tiffanian (Ti5) NALMA.
The early Cenozoic is a focal point in the biogeographical and morphological evolution of placental mammals, marking the time when the crown clades begin to appear in the Northern Hemisphere fossil record (McKenna, 1983a; Gingerich, 1989; Krause & Maas, 1990). During the Palaeocene, at least 20 placental orders arose, with seven more appearing in the early to middle Eocene, by which time almost all of the modern orders were established (e.g. Rose, 2006).
The development of warm environments on the Northern Hemisphere landmasses in the early Palaeogene in conjunction with the existence of high-latitude land bridges linking North America, Europe and Asia is considered to be responsible for the abrupt first appearances of the new taxa, thought to represent a synchronous dispersal across the Holarctic (Hooker, 2000; Gingerich, 2003; Bowen et al., 2005; Smith et al., 2006). To answer questions regarding where, when and why the new groups originated (Bowen et al., 2007), we must understand the changes that affected the palaeoecology of the Northern Hemisphere, especially the onset and disruption of the land bridges between the continents.
Biogeographical analyses of the Holarctic during the Palaeocene–Eocene refer to three intercontinental land bridges and one intracontinental land bridge: Beringia, connecting East Asia and North America; the De Geer route, connecting Greenland and Fennoscandia; the Thulean route, connecting North America and Europe via Greenland; and the junction–disjunctions of the Turgai Strait, connecting eastern and western Eurasia (Fig. 1) (Szalay & McKenna, 1971; McKenna, 1975, 1983a,b; Tarling, 1982; Tiffney, 1985, 1994, 2000; Krause & Maas, 1990; Marincovich et al., 1990; Janis, 1993; Knox, 1998; Manchester, 1999; Sanmartín et al., 2001; Tiffney & Manchester, 2001). To complete the complex biogeographical puzzle of the early Cenozoic, the following palaeogeographical events should also be considered: the collision of India with Asia (Krause & Maas, 1990), the impermanent joining of North America and South America near the Cretaceous/Palaeogene boundary (K/Pg; Iturralde-Vinent & MacPhee, 1999), and the possibility of an evanescent joining of western Europe and Africa in the late Palaeocene (Janis, 1993; Tabuce & Marivaux, 2005; Boyer et al., 2010; Smith et al., 2010a).
In the 1980s, McKenna (1983a,b) and Tiffney (1985) published papers establishing the original palaeogeographical concept of the three Northern Hemisphere land bridges. Their work was, for a time, an almost exclusive database for biogeographical analyses and was drawn upon by many (e.g. Sanmartín et al., 2001; Rose, 2006; Pramuk et al., 2008; Archibald et al., 2011). More recently, newer evidence has emerged suggesting a different palaeogeographical scenario for the occurrences of the three Northern Hemisphere routes, especially for the De Geer route. Despite its importance, the new evidence has escaped the attention of most biogeographers. As a result, the contribution of palaeogeography to shaping the perceptions of early Cenozoic biogeographical evolution remains tied to 30-year-old concepts.
Given the great historical biogeographical significance of the land bridges, the aim of this study is to review all of the recent evidence and stimulate new discussion that will hopefully begin to resolve the confusion concerning the significance of the De Geer route, the Thulean route and Beringia in the biogeographical evolution of mammalian faunas during the latest Mesozoic–early Cenozoic.
Materials and Methods
Appendix S1 in the Supporting Information documents the historical evolution of the concepts of the Northern Hemisphere land bridges up to McKenna (1983a,b) and Tiffney (1985), which have strongly influenced the current biogeographical paradigm. This study reconsiders the conclusions of McKenna and Tiffney with a thorough review of the geotectonic evidence that has emerged in recent years, juxtaposing recent palaeogeographical reconstructions that summarize the modern paradigms in geology and palaeogeography, proposing an updated and more detailed palaeogeographical scenario for the formation of the Northern Hemisphere land bridges.
Going a step further, this study incorporates a palaeogeographical perspective in a biogeographical scenario; palaeogeographical and ecological factors are co-evaluated, considering that both impacted on the biogeographical evolution of the Northern Hemisphere. For example, relatively short-term temporal climatic variations during the periods when the high-latitude land bridges were terrestrially exposed are likely to have affected biotic exchanges between the landmasses. Because knowledge of the long-term climatic variability is necessary to specify the time windows within which terrestrial biotic exchanges could have occurred, a reconstructed climatic fluctuation curve based on the eustatic sea-level oscillation (see Appendix S2) is used for biogeographical inferences. The biogeographical scenario deduced from the climatic evidence is then evaluated with the fossil record (including palaeofloras, dinosaurs and reptiles; see Appendix S3). Ιn this context, the mammalian fossil record is reinterpreted on the basis of the proposed biogeographical scenario.
McKenna (1983b) considered the Barents Shelf (Fig. 2) to be subaerial during the Palaeocene (probably in the Danian and certainly in the post-Danian; see McKenna, 1983b, p. 378) and Eocene, and thereby formed a continuous land link from North America to Fennoscandia. The latter was separated from the rest of Europe by the Danish-Polish Trough which connected the North Sea and Tethys. McKenna (1983b) also presented data supporting a single subaerial Thulean route [i.e. a continuous land passage from France and the British Isles to North America via the Greenland-Scotland Ridge (GSR)] spanning the late Palaeocene to early Eocene. Given its more southerly geographical position, the Thulean route was considered by McKenna (1983a,b) to be a more significant biogeographical junction than the De Geer route. McKenna further suggested that the two land bridges could have simultaneously connected North America to Great Britain and Scandinavia near the end of the Palaeocene and up to some point in the earliest Eocene. The claim of simultaneous connections via the two land bridges led to confusion among biogeographers.
In contrast to McKenna's view, the evidence presented here suggests that the De Geer route and the Thulean route were two different temporal and topographical biogeographical concepts. Specifically, contrary to McKenna's claim that the De Geer route was exposed from the Palaeocene to the end of the Eocene, geotectonic and palaeogeographical evidence (Appendix S1) suggests that the Barents Shelf was transgressed from the mid-Palaeocene to the late Eocene (Fig. 3), and furthermore, that the De Geer route was subaerial from the late Maastrichtian to earliest Palaeocene (around 71–63 Ma) (Fig. 3a). Climatic evidence (Appendix S2) suggests that two time windows, c. 69 Ma and 65.5 Ma, would favour biotic exchange across the De Geer route (Fig. 4), a biogeographical inference which is supported by fossilized floristic (Fig. 5a,b) and vertebrate evidence (Fig. 6, Appendix S3).
The Thulean route formed well after the interruption of the De Geer route and offered a southerly route connecting western Europe and North America. The combined geotectonic and sea-level evidence presented in Appendix S1 suggests that the first full exposure of the Thulean land bridge included at least two episodes (c. 57 Ma and c. 56 Ma) (see Fig. 3d and Fig. S1.3 in Appendix S1). This inference is supported by the mammalian (see below) and reptile fossil records (see Fig. 6; Appendix S3).
Understanding of the palaeogeography of Beringia in the early Cenozoic is quite confused, and in some palaeogeographical reconstructions it is emergent whilst in others it is submerged (see Appendix S1). In any case, on the basis of climatic (Fig. 4, Appendix S2), floristic and vertebrate evidence (Figs 5a,b & 6), two time windows are likely for biotic exchanges across Beringia during the Palaeocene: Bering route 1 c. 65 Ma (Fig. 7d) and Bering route 2 c. 58 Ma (see also Appendix S1 and Discussion). Possible Eocene exposures are not considered here.
Terrestrial biotic evidence for the existence of Northern Hemisphere land bridges
Rich floras and faunas have been recovered from around the K/Pg boundary in the peri-Arctic regions (e.g. Akhmetiev & Beniamovski, 2009; Herman et al., 2009). To understand the biogeographical changes that took place, as well as the role of the Arctic as a geodispersal field, the temperature and the available light affecting the biota should be co-estimated (see the recent reviews by Spicer & Herman, 2010, and Eberle & Greenwood, 2012).
During the latest Cretaceous, angiosperms prevailed over ferns, conifers and cycadophytes in all peri-Arctic palaeofloras except the Alaskan (although pollen data from the Maastrichtian beds of the Prince Creek Formation reveal a higher diversity of angiosperms than that which is evident from the megafossils) (Spicer & Herman, 2010; and references therein). A strong differentiation had arisen between the north Alaskan and the north-eastern Russian regional palaeofloras since the Coniacian (and possibly as early as the late Turonian), suggesting limited gene flow and/or climatic differentiation that persisted into the Maastrichtian (Herman, 2007). Various sources of evidence (Nordt et al., 2003; Frank et al., 2005, and references therein; see Appendix S2) suggest, however, that the mid-Maastrichtian (CH3 highstand in Fig. 4) was a hyperthermal period [known globally as the mid-Maastrichtian event (MME)]. Hence, the observed limited genetic connection between the North American and north-eastern Russian floras is likely to result from geographical isolation caused by a transgressed Bering Strait (Fig. 7b,c). On the other hand, extended floral exchanges had taken place between the two areas by the early Palaeocene (Herman, 2007) (summarized below), suggesting a terrestrial communication (Fig. 7d); although the period corresponds to a lower warming event in the Kominz et al. (2008) eustatic sea-level curve (PH5 highstand in Fig. S1.3). This phenomenon could be explained by supposing that warmer periods result in higher eustatic sea levels leading to extended transgressive effects in low altitude areas.
Since the early Palaeocene, the regional palaeofloras of the peri-Arctic regions (such as northern Alaska, north-eastern Russia and Spitsbergen to Ellesmere Island) indicate relationships even at the species level, suggesting strong similarities in climatic regimes and genetic-terrestrial connections between the regions. The exclusive floristic relationships among the areas, if they are not due to collecting bias, especially support distinct dispersals via both the De Geer and the Bering routes (see Fig. 5a,b). Thus, Alaska and north-eastern Russia shared taxa such as Onoclea hesperia, Phragmites sp., Quereuxia sp. and Liriophyllum sp. during the early Palaeocene, and Tiliaephyllum brooksense and Archeampelos sp. during the late Palaeocene. These similarities suggest two distinct dispersals through Beringia, 65.5 Ma and c. 58 Ma, corresponding to the PH1 and PH5 sea-level highstands shown in Fig. 4 and Fig. S1.3 [for other evidence supporting warming periods during the highstands, see Quillévéré et al. (2008), Cramer et al. (2009) and Appendix S2 for 65.5 Ma, and Tripati et al. (2001) for c. 58 Ma].
On the other hand, north-eastern Russia and Spitsbergen shared taxa such as Coniopteris tschuktschorum, Elatocladus sp., Pseudolarix sp., Glyptostrobus nordenskioeldii and Taxodium sp.; and north-eastern Russia, Spitsbergen and North America shared taxa such as Cupressinocladus interruptus and Nordenskioldia borealis (for references see Fig. 5). Although some of these might be elements of a more ancient native floristic composition, others could suggest dispersals exclusively through the De Geer route. Indeed, Akhmetiev & Beniamovski (2009) (see also Akhmetiev, 2010) proposed that the desiccation of the epicontinental seas and adjacent parts of the Palaearctic Basin coincided with the Maastrichtian–Danian boundary, allowing westward migrations of thermophylic Tsagayan flora (Ginkgo, Pinaceae, Taxodiaceae, Trochodendroides, Platanaceae and Hamamelidaceae; i.e. the typical warm-temperate plants from the middle Amur Area of eastern Asia). Thus, at high latitudes, boreal humid deciduous flora migrated from the east to the west along the northern margins of the Siberian Platform and along the desiccated West Siberian Plate in the Danian, reaching the northern and middle Urals as well as Spitsbergen (via the De Geer route), where the same type flora has been recovered (at the Barentsburg locality; Akhmetiev & Beniamovski, 2009, and references therein). The occurrence of Palaeocarpinus joffrensis during the Palaeocene in North America and Spitsbergen (Storvola flora) is evidence for the exposure of the De Geer route (Golovneva, 2002; although in a different timeframe) that is, in fact, corroborated by the occurrence of this taxon in north-western China (Manchester & Shuang-Xing, 1996).
The discovery of the marsupial Maastrichtidelphys in the Maastrichtian of the Netherlands (Martin et al., 2005) is strong evidence for the existence of the De Geer route. Maastrichtidelphys exhibits similarities to early Maastrichtian North American herpetotheriids, providing definitive evidence of a high-latitude northern Atlantic dispersal route between North America and Europe during the latest Cretaceous (Martin et al., 2005). The occurrence of Maastrichtidelphys also demonstrates the existence of a junction between western Europe and Fennoscandia during the latest Cretaceous, which is further supported by vertebrate similarities between North America and Europe (Fig. 6). Nevertheless, this connection would have disappeared by the time the pantodonts occurred in both Asia and North America (early Palaeocene), which is concordant with the lack of pantodonts in the late Palaeocene (Thanetian) Cernaysian faunas of western Europe.
Recently, Tabuce et al. (2011) reported the recovery of a new mammal, Mondegodon eutrigonus, from the earliest Eocene of Silveirinha, Portugal. Mondegodon eutrigonus is considered, along with the early Palaeocene North American species Oxyclaenus cuspidatus, to be a morphological intermediate between two groups of ungulate-like mammals: the triisodontids and the mesonychians. Considering that the triisodontids are early to early–late Palaeocene North American taxa, Tabuce et al. (2011) proposed that Mondegodon probably belongs to a group that migrated from North America to Europe during the earliest Palaeocene and could thus represent a relict genus belonging to the Ante-Eocene European mammalian fauna. As such, the presence of Mondegodon in Europe constitutes more mammalian evidence of the exposure of the De Geer route.
Among the early Palaeocene mammalian faunas of North America and eastern Asia, the carnivorans, the mesonychids and the pantodonts are currently the only known taxa that are common to both areas and demonstrate eutherian similarities. Unequivocal carnivora are first known from the Palaeocene of North America. The two primitive families, Viverravidae and Miacidae, are often grouped as the paraphyletic Miacoidea (e.g. Rose, 2006). The oldest securely dated carnivoran, Ravenictis, comes from the earliest Palaeocene of Saskatchewan, Canada (Fox et al., 2010, and references therein). Ictidopappus (North America) and Pappictidops (China) are nearly as old and are known only from dentitions (Rose, 2006). They are regarded either as primitive viverravids or as basal carnivorans of uncertain affinity.
Three mesonychid genera (Yantanglestes, Hukoutherium, Dissacus) are known from the Shanghuan Asian land mammal ages (ALMAs) (Missiaen, 2011), whereas two (Dissacus, Ankalagon) are known from the Torrejonian (To2) North American land mammal ages (NALMAs) (Lofgren et al., 2004). The clade represented by the genus Dissacus probably dispersed more than once between the continents.
The pantodonts possess traits common to the mammalian faunas of Asia, North America and South America (McKenna & Bell, 1997; Lucas, 1998). Among the early pantodonts are the primitive Alcidedorbignya from the Tiupampa in south-central Bolivia (de Muizon & Marshall, 1992, and references therein), the Chinese genera Bemalambda and Hypsilolambda (e.g. Missiaen, 2011), and the North American Pantolamda and Titanoides (Lofgren et al., 2004), all of which are from the early Palaeocene. Recently, large footprints of a Titanoides-like pantodont were discovered in the Todalen Member coal layers, providing the earliest evidence of a large mammal on Svalbard and the northernmost example of the presence of a land mammal from the Palaeocene (Lüthje et al., 2010). The presence of a Palaeocene pantodont on Svalbard is consistent with the concept of the De Geer route.
Primitive ungulates such as the rabbit-sized arctostylopids and the uintathere Prodinoceras are first known from the Nongshanian and the Gashatan ALMAs, the former from both and the latter from the Gashatan only (e.g. Missiaen, 2011). Since the Tiffanian (Ti5, c. 58 Ma), both clades are also represented in North America by the genera Arctostylops and Prodinoceras (Lofgren et al., 2004). These ungulates are proposed to have dispersed between Asia and North America via Beringia (e.g. Missiaen, 2011). This view is supported by evidence that the Ti5 age coincides with observed floristic similarities and the PH5 sea-level highstand suggested by the Kominz et al. (2008) eustatic curve. Therefore, all of the first occurrences within the Ti5 times of the North American taxa related to Asian forms are likely to have migrated to North America via Bering route 2. According to the North American mammalian biostratigraphy of Lofgren et al. (2004), such Ti5 migration events could include the first occurrences of the viverravid genera Viverravus and Didymictis; the anagalid Mingotherium, which has been related to the endemic Asian family Pseudictopidae (Rose, 2006); the metacheiromyid Propalaeanodon, which could be related to Asian palaeanodonts (Rose, 2006); the oxyaenid genera Oxyaena and Palaeonictis (oxyaenids are considered to be immigrants from Asia; Rose, 2006); as well as the carpolestid plesiadapiforms (Smith et al., 2004).
The largest arctocyonid was the dog-to-bear-sized Arctocyon, which was present in the late Palaeocene of both Europe and North America (in the Thanetian and the Torrejonian–Tiffanian, respectively) (Rose, 2006). The first occurrence of Arctocyon in Europe is dated to 58.5 Ma (Hooker & Collinson, 2012). This age is well after the exposure of the De Geer route, as proposed in the current study, and slightly before the exposure of Bering route 2 (c. 58 Ma). Given the absence of Arctocyon from Asia, the unexpected occurrence of Arctocyon is likely to be a ‘sweepstake’ dispersal through the early and incomplete formation of the Thulean route near the end of the first magmatic phase of the North Atlantic Igneous Province (NAIP) c. 58 Ma. In Fig. S1.3, the occurrence of the North American Arctocyon in Europe correlates with sea-level lowstand PL4 and the first unconformity of the Faeroe-Shetland Basin (as considered in Appendix S1), implying a restriction of the marine barrier.
The geological evidence hypothesized in Appendix S1 to document the first full exposure of the Thulean route (LGR81) c. 57 Ma (Fig. 3d, Fig. S1.3) is in agreement with additional mammalian evidence. The recently described plesiadapid Platychoerops antiquus from France may be the result of a dispersal of the North American Plesiadapis cookei in the late Thanetian (Boyer et al., 2012). A similar dispersal could account for the mesonychid Dissacus, known from the Torrejonian of North America and the Gashatan of Asia (Missiaen & Smith, 2008) as well as from the Cernaysian of Europe (first occurrence c. 57 Ma; Hooker & Collinson, 2012). The direction of these dispersals was probably from North America to Europe via the Thulean route and from Europe to Asia via a regressed Turgai Strait (Fig. S1.3). The likelihood of this scenario depends on the age of the first occurrence of Dissacus in Asia. If Dissacus appeared > 57 Ma, then it could have dispersed via Bering route 2 c. 58 Ma [the possible occurrence of the same genus in the Shanghuan ALMA (Missiaen, 2011) is not considered here]. The same course (i.e. via the Turgai Strait), but in the opposite direction could account for the dispersal of the Rodentia. Previously described only from the late Palaeocene of Asia and North America, they are now also known from comparable (late Thanetian) beds in Europe (Smith et al., 2010b). Thus, the Rodentia probably occurred first in Asia and then reached North America via Europe.
According to Lofgren et al. (2004), the first occurrence of Viverravus in North America is at Ti5, suggesting dispersal via Bering route 2 c. 58 Ma (PH5 sea-level highstand). Comparable morphotypes to Viverravus are also known from the Silveirinha Formation in Portugal (Antunes et al., 1997; Estravis, 2000) and are probably of latest Palaeocene age (Pais et al., 2012, and references therein). Therefore, the genus Viverravus may have dispersed to Europe either from Asia via the Turgai Strait or from North America via the Thulean route.
The first occurrence of Coryphodon in North America at the onset of Cf1 (Clarkforkian) (Lofgren et al., 2004), and not at Ti5 (Tiffanian) (i.e. at the time of favour climatic conditions for dispersal via the Bering route 2), suggests a later dispersal via the Thulean route in the late Palaeocene, although this inference cannot be confirmed by the current fossil record because in Europe Coryphodon is known only from the Palaeocene–Eocene boundary (PE I; Hooker & Collinson, 2012). Coryphodon teeth are among the most common mammalian fossils in the Eureka Sound Group of Ellesmere Island, where the mesonychid genus Pachyaena was also recovered (Eberle & McKenna, 2002). Pachyaena is known from the late Palaeocene of Asia (Meng et al., 2005) and the earliest Eocene of Europe (PE II; Hooker & Collinson, 2012). Its slightly earlier presence in North America (Wa0 versus PE II) could be interpreted as dispersal via a possible earliest Eocene exposure of Beringia (not considered here), rather than from Europe via a combination of the Turgai Strait and the Thulean route.
Since McKenna (1983a,b) and Tiffney (1985), many other authors have implicated the De Geer route (as originally defined) in shaping the historical biogeography of mammals (Woodburne & Swisher, 1995; Beard & Dawson, 1999; Smith, 2000; Lüthje et al., 2010), plants (Manchester, 1999; Tiffney, 2000) and insects (Petrulevičius et al., 2007; Archibald, 2009; Archibald et al., 2011). McKenna (1983b) suggested that, during the early Cenozoic, the De Geer and Thulean routes simultaneously connected North America and separate parts of Europe at different latitudes. The De Geer route was considered a high-latitude (‘northern’) route, and the Thulean route was considered a lower latitude (‘southern’) route. Because the southern route offered relatively greater palaeoecological benefits, the De Geer route was considered to be an alternative, filter passage. This view was asserted in the biogeographical discussions of many papers and reviews (e.g. Sanmartín et al., 2001; Rose, 2006; Pramuk et al., 2008; Archibald et al., 2011). More recent data and palaeogeographical reconstructions, however, do not support the scenario proposed by McKenna (1983b). Some palaeogeographical reconstructions are instead congruent with a prior subaerial exposure of the Barents Shelf [e.g. the early ‘Tertiary’ (Palaeocene) reconstruction of the North Atlantic by Ziegler (1988); the 70 Ma reconstruction by Stampfli & Borel (2004: Appendix 3 in CD-ROM), and the Maastrichtian–Danian boundary reconstruction of Akhmetiev & Beniamovski (2009: Figure 3)]. Furthermore, contrary to McKenna's view that the De Geer route was exposed from around the Palaeocene–Eocene boundary to the middle Eocene, the Barents Shelf was transgressed in most recent palaeogeographical reconstructions of that interval (e.g. since the mid-Danian: Akhmetiev & Beniamovski, 2009; c. 60 Ma: Torsvik et al., 2002; in the late Thanetian: Figure 4 in Brunstad et al., in press; in the early Cenozoic: Smelror et al., 2009; c. 50 Ma: Brinkhuis et al., 2006; Gleason et al., 2009; Eberle & Greenwood, 2012). Such reconstructions support the conclusion that marine barriers interrupted the De Geer route during the early Cenozoic, clearly suggesting that the scenario proposed by McKenna (1983b) should be reconsidered and updated.
The current study goes further by presenting a synthesis of all the currently available evidence concerning the exposure of the De Geer route (Appendix S1). Because of the major hiatus of the Barents Shelf, geological data are insufficient to resolve the issue of the subaerial exposure of the Barents Shelf. Nevertheless, the limited biostratigraphic evidence from marine faunas is enough to convince some researchers of the existence of such an event (e.g. Akhmetiev et al., 2012). Tectonic models suggesting the uplift of the area during the interval of interest (Nøttvedt et al., 1988; Lyberis & Manby, 1993) are still under discussion; recent uplift calculations seem to support such models (Setoyama et al., 2011). Floristic evidence (Fig. 5a,b) is congruent with the concept of the De Geer route as defined in the current study, and the same concept has been proposed by other authors (Akhmetiev & Beniamovski, 2009; Akhmetiev, 2010). Furthermore, floristic evidence is congruent with the dispersal via the De Geer route of dinosaur affinities previously thought to have dispersed via Beringia (see Appendix S3). Moreover, the concept of the De Geer route is strongly supported by exclusive vertebrate affiliations between Europe and North America among the crocodyloids Arenysuchus and Prodiplocynodon, the common gavialoid genus Thoracosaurus, the marsupials Maastrichtidelphys and the herpetotheriids, and the eutherians Mondegodon and Oxyclaenus.
The first magmatic phase of the North Atlantic Igneous Province (NAIP) was completed some 5 Myr after the De Geer route was interrupted [i.e. c. 58 Ma (e.g. Rousse et al., 2007) vs. 63 Ma]. Although the distance between the Shetland and Faeroe land margins diminished during the sea-level lowstand 59.2 Ma (PL4 in Fig. S1.3), the Thulean land bridge failed to fully connect. The only mammalian dispersal from North America to Europe at that time, that of the Arctocyon, was probably a ‘sweepstake’ dispersal. During the second magmatic phase of the NAIP, another sea-level lowstand (PL6 in Fig. S1.3) seems to have succeeded the first complete formation of the Thulean route, as suggested by the recent seismic and stratigraphical evidence mentioned in Appendix S1. This event took place at c. 57 Ma and is supported by extended vertebrate evidence including that of common genera as crocodilians, choristoderes, turtles and mammals (Fig. 6).
When was the De Geer route exposed?
In the basinal areas of the south-western Barents Sea, a major hiatus was recorded during the late Maastrichtian–early Danian (see Fig. S1.1 in Appendix S1). Although there have been several studies on Cenozoic erosions and uplifts in the region, the nature of the hiatus is still unclear (Setoyama et al., 2011, and references therein). Nagy et al. (1997) postulated the presence of periodic bottom currents as a cause of the hiatus, a suggestion also supported by the results of Setoyama et al. (2011). The subaerial exposure of the De Geer route at the time of the hiatus is congruent with the presence of bottom currents. The closure of the Barents seaway could have caused strong marine circular currents, thus preventing deposition. In this scenario, the exact interval of the exposure of the De Geer route can be assigned to the duration of the late Maastrichtian–early Danian hiatus in the basinal areas of the south-western Barents Sea, which have well-constrained ages based on biostratigraphy (Nagy et al., 2004). Thus, according to Nagy et al. (2004), the dinocyst species Psammosphaera fusca and Hyperammina rugosa that constitute the first Cenozoic biozone of the Barents Sea (BSP 1) rest unconformably on highly diverse and entirely agglutinated Campanian-to-Maastrichtian assemblages (as indicated by the Caudammina gigantea and Spongodinium delitiense) (Fig. 4). The late Danian age of the BSP 1 biozone corresponds to the PH2 sea-level highstand shown in Fig. 4 (c. 63 Ma) and can be interpreted as evidence of an initial (medium magnification) transgression of the shelf signalling the termination of the De Geer route. The relatively small magnitude of this flooding could explain why only limited Danian sediments were deposited. The higher PH3 sea-level highstand (61.8 Ma) would have transgressed a more extended area, and probably the entire Lancaster Sound Basin on western Greenland, interrupting the connection to North America (Fig. 3b).
The evidence presented in Appendix S1 suggests that the De Geer route formed from tectonic uplift of the Barents Shelf. The early Maastrichtian sea-level lowstand (c. 71 Ma, CL4 in Fig. 4) would have forced the subaerial procedure and thus the onset of the De Geer route exposure. Therefore, the exact time interval of the De Geer route is around 71–63 Ma. Furthermore, on the basis of climatic evidence (Appendix S2), two time windows would favour biotic exchanges across the De Geer route: c. 69 Ma and 65.5 Ma (Fig. 4).
Did the De Geer, Beringia and Thulean routes simultaneously connect North America and Asia?
The Thulean route formed after the De Geer route during two sea-level lowstands, c. 57 Ma and 55.8 Ma. Both lowstands are strongly supported by securely dated geotectonic and faunal evidence. Thus, the De Geer route and the Thulean were not formatted simultaneously, but rather sequentially.
In most biogeographical analyses, Beringia is considered to be an alternative to the De Geer route for early Cenozoic land dispersal. Indeed, although there is insufficient evidence to support a hypothesis of dinosaur faunal exchanges through Beringia during the latest Cretaceous (see Appendix S3), floristic evidence suggests that Beringia was probably later exposed contemporaneously with the De Geer route 65.5 Ma.
On the basis of continental reconstructions (Ziegler et al., 1983; Lawver et al., 2002) and recoveries of dinosaur remains, it appears that dinosaurs existed at the high latitudes of northern Alaska (c. 82°–85° N) during the latest Cretaceous. The tectonics of the Arctic are complex, however, and there are different hypotheses concerning the exact palaeolatitudinal history of the peri-Arctic regions (e.g. Spicer & Herman, 2010). In any case, the De Geer route was better positioned biogeographically for geodispersals than Beringia was. Around the K/Pg boundary, Beringia was located at a higher latitude (c. 75°) than it is today (Fig. 7). Hence, Beringia is considered to have been a filter rather than a corridor during the late Palaeocene and early Eocene (Szalay & McKenna, 1971; McKenna, 1983a, 2003). Some plate reconstructions place Spitsbergen 65°–68° N during the same period (Lüthje et al., 2010, and references therein), offering a more favourable climate and more winter daylight for plant production. Nevertheless, the evidence presented above suggests that relatively extensive mammalian dispersals took place via Bering route 2 at Ti5 (c. 58 Ma).
How the De Geer, Beringia and Thulean routes affected mammalian biogeography in the early Cenozoic
The key role played by the De Geer route in mammalian evolution during the early Cenozoic is more important if one considers that, at the time that the De Geer route formed a terrestrial conduit (latest Cretaceous–early Palaeocene), the Turgai Strait was also terrestrially passable (Akhmetiev & Beniamovski, 2009; Akhmetiev et al., 2012). Therefore, during the latest Cretaceous–early Palaeocene, eastern Asia should have been connected to north-eastern North America via Fennoscandia. Such a palaeogeographical continuity can be demonstrated by the (limited but existing) similarities between the early Palaeocene mammalian faunas of North America and eastern Asia; that is, the Puercan and Torrejonian NALMAs and the Shanghuan ALMA (Missiaen, 2011; Ting et al., 2011) (Fig. 8).
The Shanghuan ALMA is the first Cenozoic mammal age in Asia that forms an assemblage of primitive taxa, and there are no known Cretaceous Asian mammalian faunas that share taxa with the Shanghuan faunas. Hence, all of the Shanghuan taxa represent first appearances (Missiaen, 2011). Some Shanghuan taxa, such as the gliriforms, the tillodonts and the sarcodontids, are believed to be endemic to Asia. Others, such as the mesonychids and the carnivorans, are shared between Asia and North America; the pantodonts are even shared between Asia, North America and South America (McKenna & Bell, 1997; Lucas, 1998). These eutherian similarities are conspicuous, although limited. On the other hand, the onset of the endemic Nongshanian ALMA and the Tiffanian NALMA are dated near to the termination of the De Geer route (Fig. 8). This endemicity breaks at Ti5 (c. 58 Ma) via the presence of the Asian arctostylopid and uintather ungulates in North America, and probably of more taxa as previously mentioned. The occurrence of such taxa correlates with the presence of common floristic elements in north-eastern Russia and Alaska, as well as with the PH5 sea-level highstand shown in Fig. S1.3, and thus suggests dispersal via Beringia.
Missiaen (2011) correlated Ti5 with the onset of the Gashatan ALMA. A working hypothesis is that the new elements of the Gashatan ALMA are immigrants from an early connection of the Indian subcontinent with Southeast Asia during the PL4 sea-level lowstand shown in Fig. S1.3 (59.2 Ma). Furthermore, the common elements of the Gashatan, Cernaysian and Clarkforkian NALMAs may be attributed to dispersal via a combination of a regressed Turgai Strait and an early exposure of the Thulean route (Fig. S1.3). The subsequently observed earliest Eocene faunal commonality between the early Wasatchian NALMA (Wa0 to Wa4) and the early Neustrian European land mammal age (ELMA; PEI to early PEIII) (Hooker, 1996, 2010) can also be attributed to the operation of the Thulean route.
The evidence presented here suggests that the De Geer route and the Thulean route were two different temporal and palaeobiogeographical concepts. The De Geer route formed from the latest Cretaceous to the early Palaeocene and joined North America to the whole of Eurasia. During the same period, the seaways around the Turgai Strait were also passable to terrestrial biota. The early formation of the De Geer route (in the latest Cretaceous) might have also included a connection with western Europe. The Thulean route formed well after the interruption of the De Geer route and offered a southerly route connecting western Europe and North America in, at least, two time intervals during the late Palaeocene–early Eocene (c. 57 Ma and c. 56 Ma). Beringia was an essential biogeographical node during the warm period evidenced by the PH5 sea-level highstand (c. 58 Ma) of the New Jersey eustatic sea-level curve.
The formation of the De Geer route could explain the limited faunal similarities between the Puercan and Torrejonian NALMAs and the Shanghuan ALMA. The formation of the Thulean route accounts for the similarities between the Clarforkian (Cf1) and Wasatchian (Wa0, 1) NALMAs and the Cernaysian and Neustrian (PE I, II) ELMAs. Beringia could explain similarities between the Gashatan ALMA and the Tiffanian (Ti5) NALMA.
Leonidas Brikiatis is a non-affiliated researcher of vicariance biogeography. His current research focuses on investigating the degree to which vicariance and geodispersal have affected vertebrate evolution.