Victim to the Woods: Souslik and Steppe Dynamics in the European Holocene
Introduction
The European souslik is an endangered species of ground squirrel, and in decline throughout Europe. Although it is absent from Germany today, and the nearest populations can be found in neighbouring Bohemia, this had not always been so. Still in the 1930s sousliks, or Ziesel (Spermophilus citellus), were reportedly a common sight in the eastern Ore Mountains of Germany. Still in the 19th century, sightings of sousliks had been reported from a wider area in Saxony as well as, according to one account at least, from the most eastern regions of neighbouring Thuringia (1, 2). Locally, they were apparently so common that some considered them an agricultural pest (1, 2). The souslik is innately connected to the steppe, but it can make do with other, comparable habitats as well. In Germany and then-German Silesia, it was reported to do particularly well on fallow land, pasture and meadows (2). Its decline, then, was inextricably tied to changes in land use in the wake of the so-called British Agricultural Revolution, whose innovations in productivity took hold in Saxony at the end of the 18th century. Far-reaching in its consequences for the souslik population was especially the abolition of the three-field system, which always left one field fallow, for more productive systems that allowed active cultivation on all fields and at all times. This, and the ever-increasing hunger for more land to cultivate, was apparently enough to seal the souslik’s fate in what was then East Germany, and reports of its existence ceased in the 1980s (3). A reintroduction project, initiated in 2006, was eventually halted after 10 years (4).
The plight of the German souslik population is a tragic one, and it is remarkable as a comparably recent case of disappearance of a conspicuous mammal from a wealthy, Western European country. And yet on its own, it hardly warrants a retelling on a site devoted to the Quaternary extinctions. However, what it lacks in significance for the Quaternary Extinctions at first glance, it gains upon comparison with a prehistoric relative, the elusive Spermophilus citelloides of Central Europe. This is its story, but it is also the story of the European souslik. Ultimately, this is the story of how sousliks disappeared from Central Europe—twice.
Spawn of the Steppe
The Late Miocene was an era of change. Faced with desiccation and increasing cold, the erstwhile lush subtropical forests of Europe were disappearing, making way for a type of habitat the continent had not seen before: extensive grasslands. The increasing patchiness of canopy cover took a heavy toll on the creatures of the forest, a great diversity of apes among them (5). For others, however, the Late Miocene marked the beginning of a new era, one of diversification, adaptation and dominance under these newly developing realities.
With machairodontine sabertoothed cats on the prowl, the ancestors of the modern conical-toothed cats were still small, but diversified rapidly (6, 7). Their prey—bovids, cervids and equids—evolved at the same time into large forms that would be familiar to us today, as they adapted to the expanding stretches of open space (8). On the elephantine scale, gomphotheres, amebelodontids and deinotheres—proboscideans primarily adapted to a browsing diet—dwindled, heralding the rise of the “true” elephants with their long, prehensible and grazing-adapted trunks (certain mammutids such as Mammut and gomphotheres such as Notiomastodon evolved these features independently) (9). Slowly at first, elephantids became steadily dominant after their first appearance around 10 mya, and by the middle Pleistocene most proboscideans outside the Americas—with the exception of the southeast Asian Stegodontids—were elephants (10). Whilst this was happening aboveground, the sweeping grasslands fostered the ascent of more modest lifeforms below. Among these were the ancestors of the ground squirrels or sousliks of the genus Spermophilus.
Figure 1: Laurisilva at Cubo de la Galga, La Palma. The laurel forests of Macaronesia may provide a glimpse into Europe’s subtropical past
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The latest taxonomic revision by Simonov and colleagues (2024) recognises 18 species of Spermophilus, with a distribution across mid-latitude Eurasia, from the Czech Republic to China, along the Eurasian steppe belt. New species continue to be described, and some have only recently gained scientific acceptance in the light of genomic studies. One of these cases is Spermophilus odessanus with 36 chromosomes to the west of the river Dnieper and Spermophilus suslicus, with 34 chromosomes, to its east (11). Together, the two species were and still are commonly treated as Spermophilus suslicus sensu lato, the speckled souslik. In this essay, we will adopt this latter designation for the sake of simplicity, although it should be borne in mind that Spermophilus suslicus s.l. actually refers to two sister species.
Sousliks are smallish creatures, decidedly smaller than some of their close relatives within the squirrel family (Sciuridae), the marmots (Marmota) and prairie dogs (Cynomys). They are of a long and slender physique with short extremities, and tend to be coloured in light hues of brown, yellow or grey; only the speckled souslik is strongly spotted. Like most of their kin, sousliks are for the most part gregarious animals that live in colonial burrows underground. During the course of a year they spend varying but significant amounts of time in aestivation (in summer) or hibernation (in winter) underground to evade harsh conditions, and accordingly, their size and weight fluctuates considerably: Before winter hibernation the largest species may weigh up to 2kg, but during the rest of the year, especially after hibernation, they are much leaner (12). As their scientific name suggests (gr. σπέρμα sperma – seed; φίλος philos – friend, lover) they are fond of seeds especially, but generally subsist on a variable diet that may also include other plant parts, as well as small invertebrates.
Although the genus’ genesis is complicated and kinship ties between the different species are not easily established, it appears that when the genus arose in the Late Miocene, it diverged into four distinct lineages. One of these contains all living representatives in Western Eurasia: the European souslik, the Anatolian souslik (Sp. xanthoprymnus) and the Taurus souslik (Sp. taurensis) and, as sister to this group, the speckled souslik (11). During the Pleistocene and early Holocene, however, there was a sixth species in this lineage: Spermophilus citelloides, which henceforth we will call the Pannonian souslik, after the Pannonian Basin, where its centre of distribution appears to have been. Its range was not, however, limited to this region, but instead extended into Dobrudja, Serbia and Germany, especially during glacial periods. The species is known from a number of localities in this area from the middle Pleistocene onwards, before going extinct sometime in the first half of the Holocene (13). As hinted at by its scientific name, when the Hungarian palaeontologist Tivadar Kormos described it in 1916, he saw in the Pannonian souslik (Sp. citelloides) an ancestor of the European souslik (Sp. citellus) which has since taken its place in Central Europe (13). Instead, recent research paints a different, much more intricate picture of the relationship between the two species, and how one came to eventually replace the other.
In lieu of being ancestral to the European souslik, as assumed by Kormos, the Pannonian souslikis now consideredas sister to the speckled souslik, whose range extends from easternmost Poland and Moldova through Ukraine and into southern Russia, in keeping to the east of the Carpathians (13). During the Pleistocene the speckled souslik lineage (here defined as Sp. citelloides + Sp. suslicus s.l.) thus inhabited a broad belt between Central Europe and the Ural Mountains. By contrast, the European souslik belongs in a primarily Anatolian kinship group, and was for the entirety of the Pleistocene limited essentially to areas south of the Danube, with the potential exception of the Serbian Vojvodina and the Wallachian Plain (14). Then, commencing around 6kya, it suddenly mounted a comparably rapid invasion along the Danube and into Central Europe (14, 15). To understand how the modern situation came about, with the European souslik as the only species in Central Europe, the speckled souslik lineage restricted to Eastern Europe and the Pannonian souslikextinct, it is necessary to seek for clues in both the past and the present, and what they can tell us about what might potentially have taken place.
Figure 2. A Podolian souslik (Spermophilus odessanus). Given their close relationship, the Pannonian souslik may also have had a speckled pelt.
Terms of use: This image is licensed under a Creative commons attribution 3.0 unported license, and is attributed to Grzegorz Leśniewski. It is unedited and the original can be found here.
Ground squirrels are strongly allopatric creatures, meaning that their ranges overlap only marginally, if at all. There are two main reasons for this, the first being geographical barriers. Large bodies of water or mountain ranges pose hardly crossable obstacles to sousliks. Importantly, even where they are crossable in principle, these barriers retain their function due to the second factor: fierce interspecific competition, which only permits the existence of one species at any place and time (15). White-tailed prairie dogs (Cynomys leucurus) go so far as to kill competitors in the form of smaller Wyoming ground squirrels (Urocitellus elegans), even habitually (16). Due to these limitations, the ranges of sousliks tend to be fairly stationary, climate and habitat permitting, and generally do not expand into another species’ range.
Substantial range overlap, or even outright sympatry, occurs only under the necessary condition of sufficient size differences to allow a higher degree of niche partitioning and thus coexistence. Such is the case in the little souslik (Sp. pygmaeus), one of the smallest species, which coexists almost throughout its range with other species, in particular the yellow souslik (Sp. fulvus) and the russet souslik (Sp. major), the two largest species (11). In the past a similar arrangement seems to have been in place in Central Europe between the Pannonian souslik and Kaup’s souslik (Sp. superciliosus), a close western relative of the yellow souslik, also extinct (15). Of the two species of souslik, Kaup’s was significantly larger, allowing for the coexistence of both (15). The Pannonian souslik, on the other hand, was similar in size to the European souslik (13) and during the Pleistocene, both species appear to have mutually excluded each other (15). This suggests that when the European souslik arrived in Central Europe during the course of the Holocene, the Pannonian souslik was likely already extinct (15). The alternative scenario of displacement by the European souslik cannot be ruled out, but seems unlikely given the pronounced allopatry in sousliks, and the fact that the two species had already coexisted alongside for millennia up to this point. A potential factor that may have hypothetically tipped the balance, however, may be found in large-scale habitat changes. These, and the role they may have played in the Pannonian souslik’s extinction, will be our focus in the next chapter.
The Collapsing Premise
During the middle and Late Pleistocene (from about 700kya), Europe was home to two sets of herbivore assemblages: the warm-temperate Palaeoloxodon fauna and the cold-adapted mammoth steppe fauna. The former included such creatures as the European elephant (Palaeoloxodon antiquus), two species of rhinoceros (Stephanorhinus kirchbergensis, S. hemitoechus), the hippopotamus (Hippopotamus amphibius), aurochs (Bos primigenius) and water buffalo (Bubalus murrensis), while HHH Hthe mammoth steppe fauna included, among others the woolly mammoth (Mammuthus primigenius), the woolly rhinoceros (Coelodonta antiquitatis), steppe bison (Bos priscus), reindeer (Rangifer tarandus) and saiga antelope (Saiga tatarica) (17). These herbivore assemblages were spatially separated by preferences of climate and habitat—one occurring mainly in Mediterranean Europe and the other in northeastern Europe and Siberia— but penetrated into Central Europe whenever the climate was suitable. Together they ensured that herbivory was maintained throughout the Pleistocene in Central Europe, so that grasslands were able to prevail. Doubtless these grasslands were less expansive during interglacial periods, when warmth and humidity allowed temperate forests to develop, and yet insight drawn from pollen deposits indicates that grasslands persisted on a large scale even during the particularly warm Eemian interglacial (ca. 130 to 115kya), most likely as a result of the grazing, browsing and disturbance the megafauna provided (18). Another indicator for the widespread presence of open grassland, however, is the presence of Pannonian sousliks in Eemian-aged sites in Central Europe (13, 19). As recent sousliks are steppe specialists for whom open and short vegetation is essential, its presence suggests that these habitats must have been available.
Figure 3: Two European elephants (Palaeoloxodon antiquus) in a mixed Eemian landscape in the European temperate forest biome.
Terms of use: This image is licensed under a Creative commons attribution 4.0 international license, and is attributed to Brennan Stokkermans. It is unedited and the original can be found here.
With the end of the Last Glacial and the—initially stagnant but ultimately inevitable—advent of the most recent interglacial, the Holocene, all of this was about to change at unprecedented scale. How modern humans made their way into Europe—and the dire consequences this had for the natural world—has been illuminated on other occasions, and shall not be our concern here. And yet the end result was decisive: Between 50 and 40kya humans gained a definite footing in Europe (20) and by around 30kya, the decapitation of the Palaeoloxodon fauna was complete, with the elephant and both species of rhino extinct (21, 22). The consequences were profound: As the climate warmed and the mammoth steppe fauna that had characterised the last Ice Age declined, Europe was left without an intact community of megafauna for the first time in millions of years. As the large animals disappeared, so did their impact—the grazing, browsing and habitat maintenance—and in response a proliferation of vegetation began, the likes of which where probably unprecedented (23). The extent to which pre-Neolithic Europe was covered by forest remains a matter of debate, with Vera's wood-pasture hypothesis being the strongest voice of dissent, but the evidence suggests that forest cover was at least higher than it had been in previous interglacials, suggesting that the megafauna’s demise had far-reaching consequences (24).
Figure 4: The existence of sousliks depends on open, short vegtation. With the megafauna extirpation this prerequisite was often lost and the vegetation grew tall, as in this case, turning into forest eventually.
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For the continent’s remaining steppe fauna, the unfolding of these events proved catastrophic. The European wild ass or hydruntine (Equus hemionus hydruntinus), a steppe inhabitant and one of the few large mammals to make it past the early Holocene in Europe, increasingly found itself trapped in the shrinking remains of steppe. Under the sustained pressure of human hunting it maintained its last European footholds in southern France, Spain and along the Danube, some of the last regions to harbour open vegetation. As these remnants declined, so did the hydruntine, succumbing as the forest canopy closed above it and extinguished its grassy food source and biome. It seems to have vanished from the Pannonian Basin, and thus Europe, in the Late Neolithic or perhaps Chalcolithic (~5000 to 2000 BC in Europe), although there is evidence to indicate a late survival into classical times (the 1st millennium BCE) in Asia Minor (25-27).
The Pannonian Basin, the last place in Europe to provide the European hydruntine a refuge, is also the place where the youngest remains of Pannonian sousliks have been unearthed. Here, a continental climate appears to have permitted the local survival of steppe remnants throughout the Holocene (28). In these refuges, steppe specialists lasted until the arrival of farming in the 6th century BC, but without sufficient grazing pressure, they seem to have been of no avail to the Pannonian souslik. Although its date of extinction is impossible to determine with precision, it can be approximated. The youngest remains are dated to the early Holocene (13). Assuming that the range expansion of the European souslik followed upon the spread of farming—which, as we will see, appears likely—and that the Pannonian souslik’s extinction was needed for this range expansion, due to their strict allopatry, this leaves us a time frame between the early and early mid-Holocene. This contrasts with Kaup’s souslik, the larger souslik of the European middle and late Pleistocene. While this species also seems to have disappeared from much of its range during the Pleistocene-Holocene transition, it inhabited a broader area that during the late Pleistocene that extended beyond Central Europe into Ukraine and southern Russia. Intriguingly enough, remains are known from the middle and late Holocene of Ukraine, and it quite possibly persisted here into the 1920s, when Pidoplichko observed a large “red-cheeked” souslik of a kind unknown from the region today (29).
This allows for an instructive comparison with the Pannonian souslik. Since both species coexisted in Central Europe and went extinct there, with Kaup’s surviving significantly longer elsewhere, this strongly suggests that the cause of extinction for both species was specific to that region. The Holocene reforestation, especially vigorous in temperate Europe, suggests itself as a likely cause. This could mean that had the Pannonian souslik’s range extended further into Eastern or Southern Europe, it may have survived. Apart from the Pannonian and Kaup’s, a third extinct species of souslik is recorded from the European late Pleistocene: Sp. severkensis. With the narrowest geological and geographic range of all Eurasian ground squirrels, being known only from the Desna River area in Ukraine during the Last Ice Age, it appears to have been an offshoot of the little souslik that subsequently adapted to periglacial conditions close to the glaciers, and in the process became the Eurasian souslik most specialised for grazing. Its extinction in the latest Pleistocene or early Holocene has been attributed to the collapse of mammoth steppe in the region (15) or, to put it a different way, a change from short-grass steppe to first tall-grass steppe and finally forest.
Figure 5. Scene set in the early-middle Holocene of the Pannonian Basin, showcasing a colony of Pannonian sousliks, alongside other contemporary steppe fauna. These are, from left to right, Asiatic lions (Panthera leo leo), European wild ass (Equus hemionus hydruntinus), European rollers (Coracias garullus),great bustards (Otis tarda) and a lesser grey shrike (Lanius minor).
Terms of use: Artwork by Hodari Nundu and Commissioned by The Extinctions
Souslik declines and extinctions today follow this pattern. As diurnal and strongly visual creatures, sousliks are especially vulnerable to increases in vegetation height (30), and there is ample reference in the literature for a close association between thriving souslik colonies and grazing animals (14, 15). Where animals graze sousliks prefer to found their colonies, reintroductions are more successful there, and where they disappear, the sousliks follow suit (15). As the Pannonian souslik’s closest living relative, it is perhaps worth pointing out here that the speckled souslik is at times claimed to be less sensitive in this regard, and tolerant of taller vegetation (31). This claim traces back to a 2008 investigation into the relationship between alarm-call qualities and population density in speckled sousliks (32). There is, however, good reason for caution. The souslik colony found itself smothered in vegetation already a month after emergence from hibernation, and while the authors concluded that this gave the animals the advantage of cover, other sources are quite implicit in pointing out that the opposite is true: Tall vegetation equals an impending death sentence to sousliks, turning them into proverbial sitting ducks (30, 33). The population density of sousliks on the site declined by two thirds (from 300 to 100 animals per ha) within a mere three years (the study period). While it is true that souslik populations may fluctuate tremendously in time, the severity of the decline strongly indicates that the conditions the colony found itself in were not ideal, but far from it.
The diagnosis therefore remains that sousliks depend on short vegetation, and that wherever the grass grows, the souslik goes. In here may also lie the solution to the problem posed by the Pannonian souslik’s unusually early extinction. The Holocene of the Carpathian Basin saw also the local extinctions of the steppe pika (Ochotona pusilla) and the bobak marmot (Marmota bobak), as well as the global extinction of Lasiopodomys anglicus, a close relative of the narrow-headed vole (Lasiopodomys gregalis) (34). These, however, occurred much later in time (27). The potential reasons for this discrepancy shall briefly be entertained here. Voles have been shown to respond well to the expansion of tall-grass steppe (30), and the narrow-headed vole is certainly adaptable with regards to vegetation height (35). The steppe pika, perhaps counter-intuitively, is largely nocturnal, and seeks out dense, lush grass (36). Perhaps crucial here is that while for the larger, diurnal sousliks tall vegetation hampers sight and flight, it presents the smaller, less visual rodents with more hiding opportunities (60). The local survival of the bobak marmot into the late Neolithic, finally, presents us with a more pressing problem. As a fellow ground squirrel, the bobak is one of the few species of marmot that have adapted to lowland steppe, and it is similar to sousliks in its habitat requirements (37, 38). How it managed to persist into the late Neolithic of Central Europe, in defiance of the detrimental mechanisms outlined above, is a legitimate question to ask. Still, the bobak is known from only a single find during the Holocene, and nothing precludes the assumption of rarity. Nonetheless, bobaks exhibit a remarkable resilience to land-use changes, and appear to be fairly adaptable (39). Their larger size might also have given them an advantage over the sousliks, somewhat alleviating hunting pressure and possibly even allowing them to monopolise favourable sites. Whatever the case, all of these steppe specialists were extinct by the Bronze Age (27). On a related note, differences in habitat requirements, and in particular a greater tolerance to tall grass cover, are likely to have helped other, surviving steppe rodents such as hamsters (Cricetus cricetus, Mesocricetus newtonii) and blind mole-rats (Spalacidae spp.) make it past the mid-Holocene steppe bottleneck.
Figure 6: A photograph of a Romanian hamster (Mesocricetus newtoni). This species is a little-known, threatened endemic of Southern Romania, and a close relative of the golden hamster, a common pet animal.
Terms of use: This image is licensed under a Creative commons attribution 4.0 international license, and is attributed to Demian Hiß. It is unedited, and the original can be found here.
There is no shortage of comparable cases. There is, for example, Aztlanolagus, an extinct genus of rabbit and a specialised grazer. Known mostly from the North American Southwest, it went extinct in the late Pleistocene, at a time when the local megafauna collapsed (40, 41). Its relatively restricted range, and a high degree of specialisation would have made it vulnerable to habitat alterations. The omission of megafauna engineering is likely to have contributed here. Similarly, precipitous declines in genetic diversity in curlews (Numenius), a genus of waders, have been blamed on a lack of habitat maintenance by megafauna, namely a lack of adequate breeding habitat in the form of grassland (42). The slender-billed curlew (N. tenuirostris), declared extinct in 2024, seems to have historically bred mainly in only a small band of steppe south of the Siberian forest steppe (43), making it seem plausible at least that without the extinction of megafauna, much greater areas of suitable grassland would have been available to it in place of the forest steppe. Finally, another wader presents itself as a particularly interesting parallel to the sousliks: The sociable plover (Vanellus gregarius) is a critically endangered inhabitant of Central Eurasian short-grass steppe, whose breeding has become virtually tied to livestock husbandry following the population collapse of the saiga antelope (Saiga tatarica) (44). The bird’s breeding success depends on short vegetation, which is now in short supply.
Figure 7: A sociable plover (Vanellus gregarius)in its habitat, accompanied by a range map on the bottom. Summer breeding areas are green and wintering areas are blue; areas from where the species has been extirpated are indicated by dashed lines.
Terms of use: The image on the top is licensed under a Creative commons attribution 4.0 international license, and is attributed to andrewbazdyrev. The image on the bottom is licensed under a Creative commons Attribution-share Alike 4.0 license, and is attributed to the user The Great Mule of Eupatoria. Both images are unedited and the originals can be found here and here.
For the narrative’s completion, we must now turn our attention to an area approximately 1000 kilometres to the southeast of the Pannonian Basin. Nestled between Bulgaria, Greece and Turkey lies the Thracian Plain, and in this region lie also the origins of our second grand ground squirrel protagonist: the European souslik. From here the species seems to have expanded its range into Greece and the Serbian Vojvodina during the Eemian (14). However, its deep expansion into Central Europe is much more recent in origin. Being mesophilic (preferring temperate, balanced climatic conditions) (15), the warming climate of the Holocene presumably facilitated this expansion, but human assistance was probably needed. Thrace was one of the first regions in Europe to be settled by Neolithic farmers, and as agriculture advanced along the course of the Danube, so did the European souslik (14). With them the farmers brought their livestock, for whom the forests were cleared for pastures, reversing the vegetational trends manifested earlier. Other steppe rodents—the European hamster (Critetus cricetus) as well as voles (Microtus spp.)—also expanded into Central Europe at the same time (14). Eventually, the European souslik inhabited a range extending from eastern Germany through Czechia and the Pannonian Basin into Thrace and Greece, as well as into Moldova east of the Carpathians.
Figure 8: A map of the spread of farming from the fertile crescent into Europe up to about 3800 BC.
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With the coming of the modern age, however, the European souslik’s fortunes were affected by agriculture once more, and this time for the worse. In the introduction, we have retraced the beginnings of this decline, fuelled by improvements in agricultural efficiency. More recently, the abandonment of marginal farmland in Europe is posing an additional threat. Widely cherished as “spontaneous rewilding” and an expression of nature’s resilience, the uncontrolled encroachment of woody plants into formerly agricultural land presents considerable downsides for many organisms. The European souslik is among those most affected, as testified by steep declines throughout its range. Having disappeared already from many regions, with populations at the periphery especially suffering from genetic isolation, future prospects are grim (45).
In this fate the European souslik is not alone: Other Spermophilus species are declining, too, mainly in Western Eurasia. Strongly affected is also the speckled souslik, and the recognition of the Podolian souslik (Sp. odessanus) as distinct may have alarming consequences here (46). The little souslik, although broadly distributed and apparently not threatened overall, has suffered sharp declines locally, due to a widespread post-soviet cessation of grazing (30). In Kazakhstan, this same development has led to a surge in wildfires, endangering the yellow souslik (33). These dynamics have had an influence on other inhabitants of the steppe, too. Sousliks are ecosystem engineers: their burrows create microhabitats for a range of animals and plants (30) and they play an important role in bioturbation, and hence in the cycling of nutrients and the sequestration of carbon in the ground (33). Additionally, a number of dung beetles (Scarabidae spp.) frequent souslik dens to feed on their pellets, and many appear to be species-specific in their souslik associations (47). For these dung beetles, many of them with very restricted ranges, the disappearance of sousliks from an area may mean extinction, with cascading effects on food webs and nutrient cycling, for instance (48, 49). Finally, sousliks are a staple in the diet of a variety of predators. Both the Imperial (Aquila heliaca) and the steppe eagle (Aquila nipalensis) are known to regularly feed on them. When available in numbers, sousliks constitute the bulk of the diet of both species, but while the imperial eagle has been shown to be rather opportunistic, this is less the case for the steppe eagle. This peculiar, ground-nesting, migratory eagle is a souslik specialist in every respect, with the little souslik historically accounting for more than 95% of diet of some populations during the breeding season (30). The steppe eagle has disappeared already from Romania, Moldova and Ukraine (50), and a decline in sousliks is thought to be a contributing factor in its ongoing, sharp decline especially in the western half of its range (30). Additionally, sousliks are an important prey also for the long-legged buzzard (Buteo rufinus) and the saker falcon (Falco cherugg) throughout much of their ranges (61, 62).
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Figure 9: An image of an adult steppe eagle (Aquila nipalensis). The species is strongly dependent on sousliks, and declines in population are associated with declines in souslik populations.
Terms of use: This image is licensed under a Creative Commons Attribution 4.0 Attribution International license. It is attributed to PJeganathan. The image is unedited, and the original can be found here.
Crucially, sousliks are also the main prey item of the steppe polecat (Mustela eversmanni), and are of similar importance to the endangered marbled polecat (Vormela peregusna), to the point where the local extirpation of both species from parts of their range in Europe has been attributed, in part at least, to a decline in souslik populations (51). This invites comparison with the black-footed ferret (Mustela nigripes) of the American prairie, which only just avoided extinction in the 1970s, the cause of which had been an plague-induced collapse in the population of prairie dogs, its main prey.
It appears, then, that sousliks are keystone species in a grand trophic cascade of the steppe. The term—trophic cascade—was popularised in the wake of the reintroduction of wolves into Yellowstone National Park. This led to the recovery of riparian vegetation and local beaver populations through changes in the foraging activity of wapiti deer (Cervus canadensis) (52). Before, the deer had browsed intensively on the willow and aspen growth, causing erosion. In our case, the roles are somewhat inverted, but the basic findings still apply. The removal of large herbivores elicits vigorous grass growth, dealing a heavy blow to sousliks, who detest the rambunctious tangle. The extirpation of the sousliks ultimately deprives predators such as the steppe eagle and the steppe polecat of their staple food, leading to precipitous declines. The end result is an impoverished ecosystem, and the first stone to fall was the large herbivores.
Conclusion
Since the early days of biogeographic study, the European steppe remnants have been considered a curiosity (53-55). As the new field of pollen analysis provided solid data for the preponderance of primeval forest during the continent’s past, these tiny remnants were seen either as the Ice Age’s vestige, relics of the mammoth steppe, or as the result of Neolithic forest clearance. From this perspective, the demise of steppe inhabitants such as sousliks in the pre-Neolithic Holocene seemed almost inevitable in the face of forest expansion, putting an end to the Pleistocene condition. This narrative, as recent scientific insight demonstrates, is false. The origin of the European steppe harks back much further than the Neolithic, further still than the end of the Last Ice Age. Its origins, as shown by several lines of evidence, date back to the beginnings of the Pleistocene, when the climatic ebbs and flows were becoming more pronounced, gradually escalating into the bedlam of the late Pleistocene. It was during the initial advances of cold steppe into Europe that the ancestors of several modern steppe species first made their way into the continent, and they have never left since (28). As a result of this continuity, European grasslands hold world records in plant richness on small scale, with up to 98 species per 10 square metres (56, 57). This diversity persisted throughout all Quaternary interglacials and even, if only just, throughout the Holocene, and its salvation there can certainly be credited to people. However, this is an ambiguous credit, since the continued existence of the megafauna would have rendered rescue superfluous. Today, the European steppe is threatened once again, and this time more than ever. With only a meagre 6841 km² under protection within the European Union, woody encroachment, conversion into farmland, ongoing development and the abandonment of traditional use are putting the biome’s very survival in Europe at risk (28). Among the creatures most affected by this ongoing loss, the European souslik is only one of many. In its stead, we could have recounted here the decline of the steppe pika—whose fossil record in Europe extends into the latest Pliocene, about 2 mya (58)—or the Oltenia blind mole-rat (Spalax istricus), a potentially extinct animal that was observed for the last time in 1983 (59). The future outlook for Europe's steppe dwellers is bleak, and yet, then as now, there is a salvation. Since the forests fell, grazing animals and grassland ecosystems have evolved alongside, their fates inextricably intertwined. By reviving that ancient link, the resurrection of the European steppe to a status on a par with beech forest and bog is within reach still. For the Pannonian souslik, all is lost, and yet the lesson it teaches us, if heeded, may still spare its modern relatives a similar fate.
References
1. Jacobi, A. Der Ziesel in Deutschland nach Verbreitung und Lebensweise. Arbeiten aus der Biologischen Abtheilung für Land- und Forst- wirthschaft am Kaiserl. Gesundheitsamte 2, 506–511 (1902).
2. Zimmermann, R. Über das Vorkommen des Ziesels in Sachsen. Naturwissenschaftliche Wochenschrift 20, 102–104 (1921).
3. Feiler, A. Über das ehemalige Zieselvorkommen in der DDR (Rodentia, Sciuridae, Spermophilus c. citellus L., 1766). Rudolstädter Naturhistorische Schriften 1, 115–118 (1988).
4. Brückner, M. Die Ziesel verlassen Rudolfsdorf. Sächsische Zeitung (2016).
5. Merceron, G., Kaiser, T. M., Kostopoulos, D. S. & Schulz, E. Ruminant diets and the Miocene extinction of European great apes. Proceedings of the Royal Society B: Biological Sciences 277, 3105–3112 (2010).
6. Turner, A. & Antón, M. The Big Cats And Their Fossil Relatives: An Illustrated Guide To Their Evolution And Natural History. (Columbia University Press, New York, 1997).
7. Johnson, W. E. et al. The Late Miocene Radiation of Modern Felidae: A Genetic Assessment. Science 311, 73–77 (2006).
8. Levering, D., Hopkins, S. & Davis, E. Increasing locomotor efficiency among North American ungulates across the Oligocene-Miocene boundary. Palaeogeography, Palaeoclimatology, Palaeoecology 466, 279–286 (2017).
9. Li, C. et al. The trunk replaces the longer mandible as the main feeding organ in elephant evolution. eLife 12, RP90908 (2024).
10. Cantalapiedra, J. L. et al. The rise and fall of proboscidean ecological diversity. Nat Ecol Evol 5, 1266–1272 (2021).
11. Simonov, E. et al. Traditional multilocus phylogeny fails to fully resolve Palearctic ground squirrels (Spermophilus) relationships but reveals a new species endemic to West Siberia. Molecular Phylogenetics and Evolution 195, 108057 (2024).
12. Vasilieva, N. A. & Tchabovsky, A. V. Reproductive Decisions in a “Fast-Living” Sciurid: A Case Study of the Yellow Ground Squirrel (Spermophilus fulvus). Biol Bull Rev 8, 12–22 (2018).
13. Sinitsa, M. V., Virág, A., Pazonyi, P. & Knitlová, M. Redescription and phylogenetic relationships of Spermophilus citelloides (Rodentia: Sciuridae: Xerinae), a ground squirrel from the Middle Pleistocene – Holocene of Central Europe. Historical Biology 33, 19–39 (2021).
14. Rammou, D.-L. et al. Phylogeography of the European ground squirrel, Spermophilus citellus (Rodentia: Sciuridae), in the Balkans. Biological Journal of the Linnean Society 139, 158–172 (2023).
15. Popova, L. V. et al. ‘Good fences make good neighbours’: Concepts and records of range dynamics in ground squirrels and geographical barriers in the Pleistocene of the Circum-Black Sea area. Quaternary International 509, 103–120 (2019).
16. Hoogland, J. L. & Brown, C. R. Prairie dogs increase fitness by killing interspecific competitors. Proc Biol Sci 283, 20160144 (2016).
17. Kolfschoten, T. van. The Eemian mammal fauna of central Europe. Netherlands Journal of Geosciences 79, 269–281 (2000).
18. Pearce, E. A. et al. Substantial light woodland and open vegetation characterized the temperate forest biome before Homo sapiens. Science Advances 9, (2023).
19. Markova, A. K. & Puzachenko, A. Yu. Small mammal fauna in Europe during the second half of the Middle Pleistocene. FI 73, 48–66 (2017).
20. Mylopotamitaki, D. et al. Homo sapiens reached the higher latitudes of Europe by 45,000 years ago. Nature 626, 341–346 (2024).
21. de Carvalho, C. N. et al. Tracking the last elephants in Europe during the Würm Pleniglacial: the importance of the Late Pleistocene aeolianite record in SW Iberia. Ichnos 27, 352–360 (2020).
22. Sala, N. et al. Cueva de los Torrejones revisited. New insights on the paleoecology of inland Iberia during the Late Pleistocene. Quaternary Science Reviews 253, 106765 (2021).
23. Bakker, E. S. et al. Combining paleo-data and modern exclosure experiments to assess the impact of megafauna extinctions on woody vegetation. Proc Natl Acad Sci U S A 113, 847–855 (2016).
24. Sandom, C. J., Ejrnæs, R., Hansen, M. D. D. & Svenning, J.-C. High herbivore density associated with vegetation diversity in interglacial ecosystems | PNAS. PNAS 111, 4162–4167 (2014).
25. Özkan, M. et al. The first complete genome of the extinct European wild ass (Equus hemionus hydruntinus). Molecular Ecology 33, e17440 (2024).
26. Crees, J. J. & Turvey, S. T. Holocene extinction dynamics of Equus hydruntinus, a late-surviving European megafaunal mammal. Quaternary Science Reviews 91, 16–29 (2014).
27. Németh, A. et al. Holocene mammal extinctions in the Carpathian Basin: a review. Mammal Review 47, 38–52 (2017).
28. Kirschner, P. et al. Long-term isolation of European steppe outposts boosts the biome’s conservation value. Nat Commun 11, 1968 (2020).
29. Popova, L. V. Small mammal fauna as an evidence of environmental dynamics in the Holocene of Ukrainian area. Quaternary International 357, 82–92 (2015).
30. Surkova, E., Popov, S. & Tchabovsky, A. Rodent burrow network dynamics under human-induced landscape transformation from desert to steppe in Kalmykian rangelands. Integrative Zoology 14, 410–420 (2019).
31. Matrosova, V. A., Blumstein, D. T., Volodin, I. A. & Volodina, E. V. The potential to encode sex, age, and individual identity in the alarm calls of three species of Marmotinae. Naturwissenschaften 98, 181–192 (2011).
32. Volodin, I. A. et al. Population density does not affect the alarm call characteristics in the Speckled Ground Squirrel (Spermophilus suslicus). Lynx 39, 333–342 (2008).
33. Koshkina, A. et al. Post-Soviet fire and grazing regimes govern the abundance of a key ecosystem engineer on the Eurasian steppe, the yellow ground squirrel Spermophilus fulvus. Diversity and Distributions 29, 395–408 (2023).
34. Baca, M. et al. Highly divergent lineage of narrow-headed vole from the Late Pleistocene Europe. Sci Rep 9, 17799 (2019).
35. Batsaikhan, N. IUCN Red List of Threatened Species: Lasiopodomys gregalis. IUCN Red List of Threatened Species (2016).
36. Smith, A. T. & Lissovsky, A. IUCN Red List of Threatened Species: Ochotona pusilla. IUCN Red List of Threatened Species (2016).
37. Bibikov, D. I. The steppe marmot—its past and future. Oryx 25, 45–49 (1991).
38. Savchenko, G. & Ronkin, V. Grazing, abandonment and frequent mowing influence the persistence of the steppe marmot, Marmota bobak. Hacquetia 17, 25–34 (2018).
39. Koshkina, A. et al. Marmots from space: assessing population size and habitat use of a burrowing mammal using publicly available satellite images. Remote Sensing in Ecology and Conservation 6, 153–167 (2020).
40. Johnson, E. & Moretti, J. Identification of Aztlanolagus agilis from the Early Pleistocene of Texas using micro-computed tomography. in Late Cenozoic Vertebrate Paleontology: Tribute to Arthur H. Harris (eds. Morgan, G. S. et al.) vol. 88 (New Mexico Museum of Natural History and Science, 2022).
41. Moretti, J. & Johnson, E. Micro computed tomography provides insights into Aztlanolagus (Mammalia, Lagomorpha, Leporidae) reentrant pattern. in Miocene Rodents (Sciuridae, Jimomydae, Heteromyidae, Cricetidae) from Panama, (Dallas, Texas, 2015).
42. Tan, H. Z. et al. Megafaunal extinctions, not climate change, may explain Holocene genetic diversity declines in Numenius shorebirds. eLife 12, e85422 (2023).
43. Buchanan, G. M. et al. The potential breeding range of Slender-billed Curlew Numenius tenuirostris identified from stable-isotope analysis. Bird Conservation International 28, 228–237 (2018).
44. Kamp, J., Sheldon, R. D., Koshkin, M. A., Donald, P. F. & Biedermann, R. Post-Soviet steppe management causes pronounced synanthropy in the globally threatened Sociable Lapwing Vanellus gregarius. Ibis 151, 452–463 (2009).
45. Hegyeli, Z. IUCN Red List of Threatened Species: Spermophilus citellus. IUCN Red List of Threatened Species (2019).
46. Ferguson, A. & Kennerley, R. IUCN Red List of Threatened Species: Spermophilus suslicus. IUCN Red List of Threatened Species (2019).
47. Carpaneto, G. M., Mazziotta, A., Pittino, R. & Luiselli, L. Exploring co-extinction correlates: the effects of habitat, biogeography and anthropogenic factors on ground squirrels–dung beetles associations. Biodivers Conserv 20, 3059–3076 (2011).
48. Young, O. P. Predation on Dung Beetles (Coleoptera: Scarabaeidae): A Literature Review. taes 141, 111–155 (2015).
49. Nichols, E., Gardner, T. A., Peres, C. A., Spector, S. & Network, T. S. R. Co-declining mammals and dung beetles: an impending ecological cascade. Oikos 118, 481–487 (2009).
50. Meyburg, B. U., Boesman, P., Marks, J. S. & Sharpe, C. J. Steppe Eagle (Aquila nipalensis). in Handbook of the Birds of the World Alive 194 (Lynx Edicions, Barcelona, 2016).
51. Šálek, M. et al. Population status, habitat associations, and distribution of the steppe polecat Mustela eversmanii in Europe. Acta Theriol 58, 233–244 (2013).
52. Beschta, R. L. & Ripple, W. J. Can large carnivores change streams via a trophic cascade? Ecohydrology 12, e2048 (2019).
53. Joseph K. A. Das Pflanzenleben der Donaulaender. (Wagner’sche Universitäts-Buchhandlung, Innsbruck, 1863).
54. Gradmann, R. Die Steppenheidetheorie. Geographische Zeitschrift 39, 265–278 (1933).
55. Divíšek, J. et al. Origin of the central European steppe flora: insights from palaeodistribution modelling and migration simulations. Ecography 2022, e06293 (2022).
56. Wilson, J. B., Peet, R. K., Dengler, J. & Pärtel, M. Plant species richness: the world records. Journal of Vegetation Science 23, 796–802 (2012).
57. Dengler, J., Janišová, M., Török, P. & Wellstein, C. Biodiversity of Palaearctic grasslands: a synthesis. Agriculture, Ecosystems & Environment 182, 1–14 (2014).
58. Fostowicz-Frelik, Ł. & Frelik, G. J. The earliest occurrence of the steppe pika (Ochotona pusilla) in Europe near the Pliocene/Pleistocene boundary. Naturwissenschaften 97, 325–329 (2010).
59. Csorba, G., Németh, A. & Hegyeli, Z. IUCN Red List of Threatened Species: Spalax istricus. IUCN Red List of Threatened Species (2018).
60. Cao C, Shuai L, Xin X, Liu Z, Song Y, Zeng Z. Effects of cattle grazing on small mammal communities in the Hulunber meadow steppe. PeerJ 4:e2349 (2016)
61. Dravecký, Miroslav, et al. Diet composition of the long-legged buzzard (Buteo rufinus) in southeastern Bulgaria. Raptor Journal, 16, 1, 1-15, Sciendo (2022).
62. Chavko, Jozef, et al. Changes in nesting habitat of the saker falcon (Falco cherrug) influenced its diet composition and potentially threatened its population in Slovakia in the years
1976–2016. Raptor Journal, 13, 1, 75-104, Sciendo (2019)