Arctic Biodiversity Assessment

Arctic biodiversity has been exposed to strong selection pressures in the harsh and highly fluctuating Arctic environment over periods of up to three million years with repeated glaciations interrupted by relatively short interglacial periods. Photo: dalish/shutterstock.com 67

Chapter 2 Species Diversity in the Arctic

Authors David C. Payer, Alf B. Josefson and Jon Fjeldså

Contents Summary �� 68 When there is an earthquake, we say that the mammoth 2.1. Introduction �� 68 » are running. We have even a word for this, holgot. 2.2. Characteristics of Arctic biodiversity �� 70 2.2.1. Biotic and abiotic factors that structure diversity �� 70 Vyacheslav Shadrin, Yukaghir Council of Elders, Kolyma River 2.2.2. Spatial distribution of Arctic biodiversity �� 71 Basin, Russia; Mustonen 2009. 2.3. Origins of Arctic biodiversity �� 72 2.3.1. Terrestrial and freshwater �� 73 2.3.2. Marine �� 73 2.4. Future prospects for Arctic biodiversity �� 74 Acknowledgements �� 75 References �� 75 68 Arctic Biodiversity Assessment

SUMMARY glaciations also resulted in a series of extinction and immigration events in the Arctic Ocean. During interglaci- Species richness is generally lower in the Arctic than at als, marine species immigrated mainly though the Arctic lower latitudes, and richness also tends to decline from gateways from the Pacific and Atlantic Oceans, a process the low to high Arctic. However, patterns of species that continues today. richness vary spatially and include significant patchiness. Further, there are differences among taxonomic groups, Throughout the Pleistocene, Arctic species responded to with certain groups being most diverse in the Arctic. climatic cycles by shifting their distributions, becoming extirpated or extinct, persisting in glacial refugia, and Many hypotheses have been advanced to explain the evolving in situ. Although the last 10,000 years have been overall decline of biodiversity with increasing latitude, characterized by climatic stability, the Earth has now although there is still no consensus about a mechanistic entered a period of rapid anthropogenic climate change explanation. Observed patterns are likely the result of that is amplified in the Arctic. Generalism and high va- complex interactions between various biotic and abiotic gility typical of many Arctic species impart resilience in factors. Abiotic factors include lower available energy the face of climate change. However, additional anthro- and area at high latitudes, and the relatively young age of pogenic stressors including human habitation, overhar- Arctic ecosystems. Among biotic factors, latitudinal dif- vest, industrial and agricultural activities, contaminants, ferences in rates of diversification have been suggested, altered food webs and the introduction of invasive spe- but empirical evidence for this as a general principle is cies pose new challenges. The consequences of current lacking. Recent evidence suggests that ‘tropical niche warming for Arctic biodiversity are therefore not readily conservatism’ plays a role in structuring latitudinal predicted from past periods of climate change. diversity. 2.1. Introduction Physical characteristics of the Arctic important for structuring biodiversity include extreme seasonality, short Arctic ecosystems are relatively young in a geological growing seasons with low temperatures, presence of sense, having developed mainly in the last 3 million permafrost causing ponding of surface water, and annual years (Murray 1995), although some Arctic species’ to multi-annual sea-ice cover. The Arctic comprises het- lineages diverged and adapted to cold, polar conditions erogeneous habitats created by gradients of geomorphol- much earlier (see Section 2.3). In general, species rich- ogy, latitude, proximity to coasts and oceanic currents, ness is lower in the Arctic than in more southerly regions among others. Superimposed on this is spatial variation (Fig. 2.1). This is consistent with the general observa- in geological history, resulting in differences in elapsed tion that biodiversity declines from the Equator to the time for speciation. poles (Rosenzweig 1995, Gaston & Blackburn 2000, Willig et al. 2003). The strength and slope of latitudi- Over 21,000 species of animals, plants and fungi have nal biodiversity gradients differ between regions and been recorded in the Arctic. A large portion of these are are more pronounced in terrestrial and marine systems endemic to the Arctic or shared with the boreal zone, than in freshwater environments, and, in general, most but climate-driven range dynamics have left little room pronounced in organisms with greater body mass and for lasting specialization to local conditions and specia- those occupying higher trophic levels (Hillebrand 2004). tion on local spatial scales. Consequently, there are With the recent development of global distributional and few species with very small distributions. In terrestrial phylogenetic datasets, however, it has become apparent regions, high-latitude forests were replaced by tundra that the pattern is much more complex than previously about 3 million years ago. Early Quaternary Arctic flora assumed (Jetz et al. 2012). included species that evolved from forest vegetation plus those that immigrated from temperate alpine habitats, A number of hypotheses have been advanced to explain but the most intensive speciation took place in situ in the the latitudinal trend of biodiversity, although no con- Beringian region, associated with alternating opportuni- sensus exists for a mechanistic explanation (Currie et ties for dispersal (over the Bering land bridge, when sea al. 2004). Hypotheses may be grouped into those based levels were low) and isolation (during high sea levels). In on ecological mechanisms of species co-occurrence, the marine realm, the evolutionary origin of many spe- evolutionary mechanisms governing rates of diversifica- cies can be traced to the Pacific Ocean at the time of the tion, and earth history (Mittlebach et al. 2007). Until opening of the Bering Strait, about 3.5 million years ago. recently, ecological hypotheses have dominated the dis- cussion, but with the development of large DNA-based More than 20 cycles of Pleistocene glaciation forced phylogenies there is now more focus on understanding species to migrate, adapt or go extinct. Many terrestrial the underlying historical processes. The hypotheses species occupied southern refugia during glaciations and proposed to date are not necessarily mutually exclusive, recolonized northern areas during interglacials. Ice-free and observed patterns are likely the result of complex refugia persisted within the Arctic proper; species occu- interactions between various biotic and abiotic factors. pying these refugia diverged in isolation, promoting Arc- tic diversification. The most significant Arctic refugium The decline of available energy (Allen et al. 2002) and was Beringia and adjacent parts of Siberia. Pleistocene decreasing biome area (Rosenzweig 1995) with increas- Chapter 2 • Species Diversity in the Arctic 69

A Figure 2.1. Global patterns of species richness for mammals (A) and birds (B). Maps produced by the Center for Macroecology, Evolution and Climate, University of Copenha- gen. See also Fig. 1.1 in Meltofte et al., Chapter 1.

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ing latitude should both contribute to declining species their adaptations to such conditions (Webb et al. 2002). richness in the North. Rohde (1992) posited that the Thus, as the global climate became cooler during the ultimate cause could be a positive relationship between Oligocene, and again in the late Miocene, the ancient temperature and evolutionary speed. Relative to the groups contracted their geographical distributions tropics, the Arctic has limited insolation (lower solar towards the Equator to maintain their original niches. energy input and thus colder temperatures) and a shorter The long time for speciation in tropical environments, elapsed time for diversification. In Rohde’s (1992) view, compared with cold environments, would explain the all latitudes could support more species than currently large accumulation of species, and phylogenetically exist, and, given adequate evolutionary time, the Arctic overdispersed communities, in the humid tropics (Wiens could support biodiversity rivaling that of lower lati- 2004). The most significant increases in speciation rates tudes. Because of great variation in speciation rates, are associated with ecological shifts to new habitats that however, the number of species in taxonomic groups is arose outside the humid tropics, notably in montane uncoupled from the age of groups (Rabosky et al. 2012). regions and archipelagos (Fjeldså et al. 2012, Jetz et al. Further, several Arctic groups (notably waterfowl and 2012; see also Budd & Pandolfi 2010). However, only gulls) underwent significant recent increases in specia- some groups have (yet) responded by adapting to these tion rates (Jetz et al. 2012). Thus, there is no general new environments, resulting in small and phylogeneti- latitudinal change in speciation rates (as assumed, e.g. by cally clustered communities in the Arctic. Wiens et al. [2010]), and Jetz et al. (2012) instead point out hemispheric or even more local differences. The diversification process within the Arctic may have been strongly affected by the climatic shifts caused by The recently proposed ‘tropical niche conservatism’ variations in Earth’s orbit known as Milankovitch oscil- hypothesis may reconcile some of these diverging ten- lations. This includes a tilt in the Earth’s axis that varies dencies. This hypothesis assumes that most organismal on a 41,000-year cycle (precession), an eccentricity in groups originated during times when the global climate Earth’s orbit that varies on a 100,000-year cycle, and was warm (paratropical), and these groups tend to retain 23,000 and 19,000-year cycles in the seasonal occur- 70 Arctic Biodiversity Assessment rence of the minimum Earth-Sun distance (perihelion; survival are limited by short, cold growing seasons, lack Berger 1988). Milankovitch oscillations cause variations of suitable substrates and nutrient deficiencies (Grace et in the amount of solar energy reaching Earth, and these al. 2002, Walker et al. 2012). Large areas of the Arctic’s variations interact with characteristics of the Earth’s land surface are characterized by flat terrain under- atmosphere such as greenhouse gas concentration and lain by permafrost, resulting in wetlands character- surface albedo, resulting in rapid, nonlinear climatic ized by waterlogged soils and ponding of surface water change (Imbrie et al. 1993). The present interglacial (Gutowski et al. 2007). The Arctic Ocean has a deep period, which has extended over the last 10,000 years, is central basin surrounded by the most extensive shelves a period of exceptional climatic stability; stable condi- of all the world’s oceans, and is characterized by exten- tions have typically lasted only a few thousand years, and sive (though declining) ice cover for much of the year > 90% of the Quaternary Period (2.6 million years ago (Michel, Chapter 14). to present) has been characterized by more climatically dynamic glacial periods (Kukla 2000). Species diversity is ultimately a product of both niche- based factors, e.g. adaptation to different environmental Webb & Bartlein (1992) noted that Milankovitch oscilla- conditions, and dispersal-based factors, e.g. immigration tions are associated with changes in size and location of from species pools. Of niche-based factors, adaptation to species’ geographical distributions. Dynesius & Jansson different environmental conditions or habitats is sig- (2000) called these recurrent changes “orbitally forced nificant for generating diversity worldwide (Whittaker species’ range dynamics” (ORD), and noted that they 1960). In general, complex, heterogeneous environ- constrain evolutionary processes acting on shorter time ments support higher diversity than homogeneous ones. scales. The effects of Earth’s precession and orbital Although the Arctic lacks the rich diversity provided by eccentricity on surface temperatures are greatest at multistoried canopies in forested regions, it is far from high latitudes (Wright et al. 1993), resulting in increas- homogeneous. The Arctic comprises vast numbers of ing ORD along the latitudinal gradient from tropics to different habitats created by gradients related to geo- poles. Predicted evolutionary consequences of enhanced morphology (e.g. depth in the marine environment and ORD are apparent in general characteristics of Arctic elevation in the terrestrial realm), latitude, history of biota, including enhanced vagility and larger species’ glaciation, proximity to coastlines, and oceanic currents, geographic range sizes (Rapoport’s rule), and there- among other factors. In the marine environment, ice fore increased mixing of locally-adapted populations, cover provides habitats unique to the Arctic with char- increased proportion of polyploids within plant taxa, and acteristic flora and fauna on both the bottom (secondary reduced rates of speciation (Dynesius & Jansson 2000, bottom habitats) and top (melt-water pools) of the ice Jansson & Dynesius 2002). There is spatial variation in surface. In the terrestrial Arctic, spatial heterogeneity these processes within latitude, however, which must be in ice-associated processes such as freeze-thaw cycles considered when evaluating current diversity patterns. and thermokarst create a dynamic mosaic of freshwater For example, the Pleistocene temperature amplitude was pools and shallow wetlands, which provide habitats for lower in E Siberia and the Bering Strait region than in diverse taxa. This habitat heterogeneity is superimposed areas around the North Atlantic, leading to less glacia- on spatial variation in geological history, resulting in dif- tion (Allen et al. 2010) and enhanced opportunities for ferences in elapsed time for speciation. speciation in the Siberian-Beringian region (see below). In addition to these niche-based factors, barriers for Although ORD increases risk of extinction associ- dispersal affect status and trends in regional biodiversity, ated with habitat change, this is mitigated by enhanced and, over the long term, opportunities for speciation. generalism, vagility and genetic mixing at high latitudes For example, terrestrial areas in the high Arctic com- (Dynesius & Jansson 2000). This has important impli- prise archipelagos separated from each other and from cations for risk of extinction associated with climate areas farther south by pack ice, which affects dispersal change and other stressors, as will be discussed in subse- rates for several species (e.g. Daniëls et al., Chapter 7). quent chapters of this Assessment. One well-known barrier in the marine environment is the huge ice plug occupying M’Clure Strait, Melville 2.2. Characteristics of Arctic biodiversity Sound and M’Clintock Channel in the Canadian High Arctic. This ice plug has persisted as a stable feature for > 1,000 years (although it is probably not stable on 2.2.1. Biotic and abiotic factors that structure diversity longer time scales), and effectively separates stocks of some marine mammals (Dyke et al. 1996). Polynyas Physical characteristics important for structuring Arctic (persistent open water areas within sea ice), which typi- biodiversity include extreme seasonality with dramatic cally form in the shear zone between landfast and pack intra-annual variation in insolation, generally cool ice, provide important foraging areas during the breed- summers, presence of permafrost resulting in unusual ing season and serve as winter refugia for a variety of landforms, and annual to multi-year sea-ice cover. The seabirds and marine mammals (Stirling 1997), thereby resulting landscape is generally devoid of trees (a defin- contributing to Arctic biodiversity. Similarly, ice cover ing feature of the Arctic; see Section 2 in Meltofte et al., on land (glaciers and ice sheets) fragments terrestrial and Introduction) because tree growth, reproduction and freshwater habitats. Such fragmentation may enhance Chapter 2 • Species Diversity in the Arctic 71 biodiversity (Fedorov et al. 2003), although the opposite In general, the terrestrial and marine Arctic are highly effect of reduced range size leading to increased risk of heterogeneous with many edge effects and potential dis- extirpation or extinction must be considered (Rosenz- persal barriers, creating the expectation of high species weig 1995). This relationship is reversed for some ice- diversity associated with differential adaptation to dis- adapted Arctic species, with warming leading to habitat tinct habitats. Despite this heterogeneity, however, the fragmentation, isolation and reduced ranges. Responses Arctic is less diverse than lower-latitude areas for several of Arctic biota to barriers related to climatic changes are taxa, including mammals (Fig. 2.1a), most birds (Fig. therefore complex and not completely analogous to those 2.1b), plants (Fig. 1.1 in Meltofte et al., Chapter 1) and of temperate taxa (Cook, Chapter 17). especially herpetofauna (amphibians and reptiles), which are represented by just six species at the southern rim of Another feature of importance for Arctic biodiversity the circumpolar Arctic (Kuzmin & Tessler, Chapter 5). is regional heterogeneity in productivity. This is par- As mentioned above, extreme seasonality, short growing ticularly true for the marine environment, where high seasons, overall harshness of climate, and widespread productivity occurs in open waters close to the ice edge persistent or seasonal ice cover are all likely factors (Michel, Chapter 14). Diversity is often related to pro- driving these relationships. Diversity in several other ductivity in a unimodal (hump-shaped) fashion (Currie groups of organisms may equal or exceed that of cor- 1991, Currie et al. 2004), with diversity being highest responding groups at lower latitudes, however. Exam- in systems with mid-range productivity. However, this ples include marine benthic invertebrates (Renaud et al. relationship is poorly documented in the Arctic, and may 2009, Piepenburg et al. 2011), marine crustaceans and vary by taxonomic group or community type (Witman phytoplankton (Archambault et al. 2010), and Calidris et al. 2008). Regardless of the exact relationship, differ- sandpipers (Fig. 1.2 in Meltofte et al., Chapter 1; Ganter ences in ice cover, mixing between warm- and cold-wa- & Gaston, Chapter 4). Very high species richness is also ter currents, or currents with different nutrient content displayed in some terrestrial and freshwater invertebrate create a mosaic of oligotrophic and more enriched areas, groups such as Collembola (springtails), which have the which is reflected in differences in population den- additional distinction of including many species that are sity and species diversity. Good examples of enriched endemic to the Arctic (Hodkinson, Chapter 7). areas are the Bering and Barents Seas, which harbour species-rich invertebrate, fish and avian faunas (Ganter 2.2.2. Spatial distribution of Arctic biodiversity & Gaston, Chapter 4, Christiansen & Reist, Chapter 6, Josefson & Mokievsky, Chapter 8). In contrast, the deep The Arctic supports > 21,000 species of mammals, seafloor of the central Arctic Ocean is oligotrophic and birds, fish, invertebrates, plants and fungi, plus an species poor. estimated several thousand species of endoparasites and

Table 2.1. Selected characteristics of species occurring in the Arctic, by taxonomic group. In addition to those species listed, there are an estimated 7,100 described and as-yet undescribed species of endoparasites and several thousand groups of microorganisms.

Group Species Ratio of Mainly IUCN Endangered, Extinct in occurring worldwide Arctic species Vulnerable, or modern times in the Arctic total Near Threatened Terrestrial mammals 67 1% 18 1 0 Marine mammals 35 27% 11 13 1 Terrestrial and freshwater birds 154a 2% 81a 17 0 Marine birds 45a 15% 24a 3 0 Amphibians/reptiles 6 < 1% 0 0 0 Freshwater and diadromous fishes 127 1% 18 Marine fishes c. 250b 1% 63 4c Terrestrial and freshwater invertebrates > 4,750 Marine invertebrates c. 5,000 Vascular plants 2,218 < 1% 106d 0 0 Bryophytes c. 900 6% Terrestrial and freshwater algae > 1,700 Marine algae > 2,300 Non-lichenized fungi c. 2,030 4% < 2% Lichens c. 1,750 10% c. 350 Lichenocolous fungi 373 > 20% a) Includes only birds that breed in the Arctic. b) Excludes the sub-Arctic Bering, Barents and Norwegian Seas. c) Most marine fish species have not been assessed by IUCN. d) Includes Arctic endemics only. 72 Arctic Biodiversity Assessment microorganisms, many of which have yet to be described (Tab. 2.1). Species richness varies spatially and is not uniform across taxa. Consistent with the global latitudinal gradient in diversity described previously, species richness generally declines from the low to the high Arctic. There are also distinct regional hotspots of high biodiversity found throughout the Arctic, suggesting that despite general geographic trends, local factors are important contributors to regional diversity. For example, extraordinarily high species diversity occurs in microalgae of Hudson Bay (Archambault et al. 2010), and in terrestrial and freshwater invertebrates in the Disco Bay area of W Greenland (Hodkinson, Chapter 7). Beringia, which is defined as the area from the Lena River in northeastern Siberia to the Mackenzie River in northwestern Canada, and from the Arctic Ocean to southern Alaska and the middle Kurile Islands (Fig. 2.2), was first identified as a biodiversity hotspot for vascular plants by Hultén (1937). Subsequent work demonstrated its significance for diversity in other groups like birds and mammals. Henningsson & Alerstam (2005) sug- Figure 2.2. Beringia and other glacial refugia in the Arctic: distri- gested that the high diversity observed in shorebirds of bution of ice cover (white shading) and ice-free areas in the North- Beringia results from geological history, high produc- ern Hemisphere during the last glacial maximum, 18,000 years ago tivity and accessibility to multiple flyways. Similarly, (after Ray & Adams 2001). Beringia is enclosed within the red oval. species richness of mammals is greatest in Quaternary glacial refugia, particularly those such as Beringia that maintained connections to boreal regions (Reid et al., 2.3. Origins of Arctic biodiversity Chapter 3). During and after the last glacial maximum (26,500-20,000 years ago), many herbivorous mammals It is evident that general conditions such as environ- persisted much longer in Beringia than western Eurasia, mental harshness can only partially explain observed possibly because their favored forage (mesophilous herbs) patterns of Arctic diversity. Although the proportion of persisted in this refugium (Allen et al. 2010). The role of Arctic biota comprising endemics is relatively low, there Siberia and Beringia as the cradles of Arctic terrestrial exist many examples of endemic species well adapted biodiversity is reflected in a recent reassessment of the to harsh conditions. In the marine realm, for example, biogeographic regions of the World, based on linkages about 20% of mollusks and echinoderms are consid- between distributions and phylogenetic relationships ered endemic (Briggs 2007). Endemic Arctic mammals of > 20,000 terrestrial vertebrate species (Holt et al. include polar bear Ursus maritimus and two monotypic 2013). This analysis identified a large Arctico-Siberian genera of whales belonging to the family Monodontidae, region, where the barren circumpolar Arctic environ- the beluga Delphinapterus and the narwhal Monodon. The ments associate with the wooded permafrost regions of degree of endemism at the level of both genera and spe- Siberia. cies, however, is far lower than in the Antarctic, which has a similarly harsh environment. One likely explana- In the marine realm, biodiversity tends to be high in the tion is the difference in geological age of the two sys- vicinity of the Arctic gateways from the North Atlantic tems. While Antarctic biota have evolved over about 25 and North Pacific Oceans (Christiansen & Reist, Chap- million years with cold conditions persisting for the last ter 6). This is true for such diverse taxa as mammals, 10-17 million years (Clarke & Johnston 1996, DeVries fish and invertebrates. Diversity of marine fish (mainly & Steffensen 2005, Patarnello et al. 2011; see also Box teleosts and cartilaginous fishes) is particularly high in Box 1.3 in Meltofte et al., Chapter 1), the correspond- the Bering and White Seas (Christiansen & Reist, Chap- ing elapsed time for Arctic biota is generally considered ter 6). Similarly, marine invertebrates have high species to be < 3.0 million years (Murray 1995, Briggs 2007). richness in Arctic areas close to the two gateways, with However, recent findings suggest that the modern circu- the highest diversity occurring in the Barents, Kara and lation in the Arctic Ocean actually dates back 17 million White Seas (Josefson & Mokievsky, Chapter 8). For both years, with perennial sea ice cover formed about 13 mil- fish and invertebrates, high diversity in the vicinity of lion years ago (Krylov et al. 2008), so the difference may the Arctic gateways is largely the result of mixing of sub- not be as great in the marine environment. The lower Arctic and Arctic fauna. Among marine mammals, the degree of endemism in the Arctic Ocean may also be a gateways provide corridors for seasonal migrations from function of less isolation from adjacent oceans compared temperate seas. The gateways are not true biodiversity with the Antarctic seas, which are effectively isolated by hotspots, however, in that there are few endemic species the Antarctic Circumpolar Current (e.g. Hassold et al. present. 2009). Chapter 2 • Species Diversity in the Arctic 73

Within the Arctic, regional variation in rates of end- been supported by evidence from paleoecology, ecologi- emism appears to be related to elapsed time for specia- cal niche modeling and molecular genetics (Cook, Chap- tion. For example, the opportunity for speciation has ter 17). Populations became fragmented and isolated in persisted longer in deep-sea areas than shelf and coastal these ice-age refugia, which has likely promoted diversi- marine areas, which have been free from bottom-cover- fication in the Arctic (Fedorov et al. 2003). ing glacial ice for a relatively short time (Weslawski et al. 2010). This is consistent with the observation that there An interesting example of the diversity-promoting are few endemic species in continental shelf and coastal effects of recurrent glaciations followed by interglacial areas (Dunton 1992, Adey et al. 2008). periods is found in vascular plants of the Arctic. Arctic plants have a particularly high incidence of polyploidy, Recent work in molecular phylogenetics suggests that the presence of more than two sets of chromosomes. some lineages of contemporary Arctic species adapted to These polyploids have arisen through recurrent episodes cold, polar conditions as early as the Oligocene (34-23 of population fragmentation associated with glaciations million years ago), during the first Tertiary polar chill, followed by range expansions and hybridization during although the precision of these estimates has been de- interglacials (Abbott & Brochmann 2003). New species bated (Dornburg et al. 2012). For example, right whales resulting from this process (allopolyploids) are more (Balaenidae) may have originated as early as 27 million successful than diploids in colonizing ice-free areas after years ago (Sasaki et al. 2005). The Pluvialis sandpipers deglaciation due to the buffering that their fixed-hetero- can be traced even further back, to 34 million years zygous genomes provide against inbreeding and genetic ago (Baker et al. 2007), and the divers Gavia represent drift. Further, polyploids have broader ecological toler- a lineage that dates back > 65 million years to the late ances than diploids, and are thereby able to more readily Cretaceous (Jetz et al. 2012), although it is not known adapt to diverse ecological niches and better cope with when these birds adapted to Arctic conditions. See also changing climate (Brochmann et al. 2004). Section 12.3.1 in Ims & Ehrich, Chapter 12. Beringia provided a land bridge between Eurasia and North America during most of the Tertiary, until it was 2.3.1. Terrestrial and freshwater severed by the Bering Strait at the shift between the Throughout most of the Tertiary Period (65-2.6 million Miocene and the Pliocene about 3.5 million years ago. years ago), high-latitude regions were forested (Murray The Bering Land Bridge repeatedly reformed throughout 1995, McIver & Basinger 1999). Tundra first appeared the Quaternary when sea levels fell during major glaci- during the late Pliocene in response to global cooling ations (Hopkins 1973, Clark & Mix 2002), providing (Matthews & Ovenden 1990). Tundra communities opportunities for biotic interchange between Eurasia and were initially distributed discontinuously, then expanded North America. This interchange included both terres- to occupy a circumpolar belt by three million years ago trial and freshwater species. An example of the latter is (Matthews 1979). The early Quaternary flora of the the Arctic grayling Thymallus arcticus, which apparently Arctic included species that evolved from high-latitude originated in eastern Siberia (Froufe et al. 2003, Weiss forest vegetation of the late Tertiary by adapting to et al. 2006) and dispersed to Arctic North America via colder conditions, along with others that immigrated freshwaters of the Bering Land Bridge. The importance from alpine habitats in temperate regions of Asia and of this alternation between opportunities for dispersal North America (Hultén 1937, Hedberg 1992, Murray and isolation is also well documented from fossil rodent 1995, Schönswetter et al. 2003, Ickert-Bond et al. 2009). faunas (Repenning 2001) and from phylogenies for other Dramatic climatic shifts subsequently occurred through- small mammals of the region (Hope et al. 2013). out the Pleistocene, with more than 20 cycles of glaciation punctuated by warm interglacial periods. 2.3.2. Marine The Pleistocene glaciations had a profound impact on Many marine mammals, invertebrates and algae of the Arctic biodiversity at all levels. Species had to migrate, Arctic Ocean appear to have an evolutionary origin adapt or go extinct. Many species occupied southern in the Pacific at the time of the opening of the Bering refugia during glacial maxima and recolonized north- Strait, about 3.5 million years ago (Adey et al. 2008). ward following retreat of the ice sheets (Stewart et al. Throughout most of the Tertiary, the Arctic Ocean 2010). Ice-free refugia also persisted within the Arctic region supported a temperate biota, although intermit- proper, including areas in eastern Europe, Siberia and tent polar sea ice formed as early as 47 million years ago North America. As mentioned above, the most signif- and perennial sea ice was probably present by 13 million icant Pleistocene refugium for Arctic and boreal biota years ago (Krylov et al. 2008, Polyak et al. 2010). Harsh was Beringia (Fig. 2.2; Hultén 1937). Arctic conditions developed only during the latter part of this period, however, beginning approximately three Additional glacial refugia included exposed continen- million years ago (Jansen et al. 2000). tal shelves and nunataks protruding above ice sheets in mountain ranges of the northern hemisphere (Abbott & Several endemic Arctic lineages started to develop Brochmann 2003). The existence of these refugia and during the glaciated periods of the Tertiary. For exam- their significance in structuring Arctic biodiversity has ple, the bowhead whale diverged from the right whale 16 74 Arctic Biodiversity Assessment million years ago (Sasaki et al. 2005), several ice-associ- For example, the Pacific boreo-Arctic echinoderms have ated seal species evolved 11 million years ago (Arnason a limited bathymetric range in the Arctic (often < 100 et al. 2006), and the beluga and the narwhal evolved 10 m), while the Atlantic boreo-Arctic species are mostly million years ago (Xiong et al. 2009). Over the last 2.6 eurybathic (capable of tolerating a wide range of ocean million years, recurrent glaciations punctuated with depths). This is believed to be the result of substantial shorter periods of de-glaciation resulted in a series of shelf glaciation on the Atlantic side that caused primarily extinction and immigration events, which are reflected eurybathic species to escape to great depths for survival, in contemporary patterns of diversity. Further, histor- and later re-invade the shelves when conditions changed ic events during the last 3.5 million years have driven (Nesis 1983). re-distributions of species from the boreal regions of the northern hemisphere, and are likely still affecting Arctic 2.4. Future prospects for Arctic biodiversity diversity today. The most pervasive change occurred during the late ice-free Pliocene, after the opening of Over the last 2.6 million years, throughout the cycles the Bering Strait, when extensive trans-Arctic move- of Pleistocene glaciations, Arctic species have shift- ments of invertebrate species occurred (Vermeij 1989, ed their distributions, become extirpated or extinct, 1991, Mironov & Dilman 2010). Known as ‘The Great persisted in glacial refugia, undergone hybridization, Trans-Arctic Biotic Interchange’ (Briggs 1995), this and evolved in situ. Although the last 10,000 years have movement was primarily from the species-rich Pacific been characterized by a relatively high degree of cli- center of diversity (Briggs 2003) to the North Atlantic, matic stability, the Earth has now entered a period of likely resulting in enrichment of the Arctic species pool. rapid anthropogenic climate change. Global tempera- At least in the marine realm, there is little evidence for tures have been warmer than today’s for less than 5% negative effects of these invasions on the native fauna of the last three million years (Webb & Bartlein 1992) (Briggs 2007). and are within 1 °C of the maximum over the last one million years (Hansen et al. 2006). Further, the rate and Following this interchange, periodic glaciations eradi- magnitude of warming is amplified in the Arctic (Mc- cated faunas in the shallower areas of the Arctic Ocean. Bean 2005, IPCC 2007, AMAP 2009, AMAP 2011). During inter-glacials, immigration of species from the This trend of accelerating climate change and Arctic Pacific and Atlantic boreal species pools was possible. amplification is expected to continue (Overland et al. This immigration occurred mainly through the two 2011). Global warming has caused species distributions major gateways into the Arctic, the Bering Strait in the to shift northward and to higher elevations for a wide Pacific sector and the Fram Strait/Barents Sea area in range of taxa worldwide (Walther et al. 2002), including the Atlantic sector. Water flux through the Atlantic species occupying the Arctic (e.g. Sturm et al. 2001, gateway is currently up to 10 times that of the Pacific Hinzman et al. 2005). The Arctic, being a region with gateway, providing immigrating species much easier high ORD and therefore populated by species that have access through the former. Therefore, it’s likely that the experienced selection pressure for generalism and high historic trans-Arctic enrichment of the Atlantic species vagility (Jansson & Dynesius 2002), should have inher- pool contributes significantly to increased immigration ent resilience in the face of climate change. Some extant through the Atlantic gateway to the Arctic Ocean today. Arctic species have survived population bottlenecks This is consistent with contemporary observations in driven by climatic change, including cetaceans (e.g. the White Sea/Barents Sea area, which has high species narwhal [Laidre & Heide-Jørgenson 2005]) and waders richness (Josefson & Mokievsky, Chapter 8). Further, (Kraaijeveld & Nieboer 2000), further suggesting some Atlantic boreal species as well as species with Pacific degree of climate-change resiliency. However, the rapid origin that have invaded via the northern Atlantic co-oc- rate of change occurring now and the amplification of cur here with true Arctic endemics (Mironov & Dilman this change at high latitudes pose unique challenges for 2010). Overall, species richness in the Arctic Ocean Arctic species. The Arctic has experienced less anthro- consists of a modest number of endemics together with pogenic habitat change and fragmentation than lower species that immigrated from areas outside the Arctic in latitudes, which favors the ability of species to track both historic and ecological time. shifting habitats. However, because of the limited area available in the polar regions, terrestrial Arctic biota Effects of Pleistocene glaciation differed in shelf and have limited ability to respond to warming by northward deep-sea areas. While some shelf areas were severely af- displacement (MacDonald 2010). Kaplan & New (2006) fected by ice groundings, the bathyal (deep sea) parts of predicted that Arctic tundra will experience a 42% the Arctic Ocean were not. Further, bathyal areas were reduction in area if global mean temperature is stabilized relatively more isolated from other oceans, in particular at 2 °C above pre-industrial levels. Although the rate from the Pacific because of the shallowness of the Bering of change is debated (e.g. Hofgaard et al. 2012), there is Strait. As a result, the bathyal zone contains a more general agreement that area of tundra will be significant- endemic fauna with few Pacific elements compared with ly reduced in this century. the shelves, as seen in the polychaetes (bristle worms) (Bilyard & Carey 1980) and several other groups (Vino- In addition to rapid and accelerating climate change, gradova 1997). Differential effects of glaciation history Arctic species are experiencing anthropogenic stress- are also seen in the bathymetric distributions of species. ors that did not exist during past periods of warming, Chapter 2 • Species Diversity in the Arctic 75 including human habitation, overharvest, industrial and Budd, A.F. & Pandolfi, J.M. 2010. Evolutionary novelty is concen- agricultural activities, anthropogenic contaminants, al- trated at the edge of coral species distributions. Science 328: 1558-1560. tered food webs, and the introduction of invasive species Clarke, A. & Johnston, I.A. 1996. Evolution and adaptive radia- (Meltofte et al., Chapter 1). The many migratory species tion of Antarctic fishes. Trends Ecol. Evol. 11: 212-218. that occur only seasonally in the Arctic face additional Clark, P.U. & Mix, A.C. 2002. Ice sheets and sea level of the Last and potentially cumulative anthropogenic stressors on Glacial Maximum. Quaternary Sci. Rev. 21: 1-7. migration routes and in overwintering areas that could Currie, D.J. 1991. Energy and large-scale patterns of animal and plant-species richness. Am. Nat. 137: 27-49. further impact their ability to adapt. The suite of stress- Currie, D.J., Mittelbach, G.G., Cornell, H.V., Field, R., Guegan, ors experienced by Arctic species today is therefore nov- J.-F., Hawkins, B.A. et al. 2004. Predictions and tests of el, making past periods of climatic change an imperfect climate-based hypotheses of broad-scale variation in taxonomic analogue for the challenges now facing Arctic biodiversi- richness. Ecol. Lett. 7: 1121-1134. ty. Future efforts to preserve Arctic biodiversity must be DeVries, A.L. & Steffensen, J.F. 2005. The Arctic and Antarctic polar marine environments. In: A.P. Farrell & J.F. Steffensen similarly novel and broad-reaching. (eds.). The Physiology of Polar Fishes, pp 1-24. Elsevier Aca- demic Press. Domburg, A., Brandley, M.C., McGowen, M.R. & Near, T.J. 2012. 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