Landscape Changes During the Pleistocene–Holocene Transition and Range Dynamics of Large Herbivorous Mammals of Northern Asia I

Home , Siberian musk deer

ISSN 2079-0961, Arid Ecosystems, 2018, Vol. 8, No. 4, pp. 245–253. © Pleiades Publishing, Ltd., 2018. Original Russian Text © I.S. Sheremetev, S.B. Rozenfeld, 2018, published in Aridnye Ekosistemy, 2018, Vol. 24, No. 4(77), pp. 21–30.

SYSTEMATIC STUDY OF ARID TERRITORIES

Landscape Changes during the Pleistocene–Holocene Transition and Range Dynamics of Large Herbivorous Mammals of Northern Asia I. S. Sheremeteva, * and S. B. Rozenfeldb, ** aFederal Scientific Center of the East Asia Terrestrial Biodiversity, Far East Branch, Russian Academy of Sciences, Vladivostok, 690022 Russia bSevertsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, 119071 Russia *e-mail: [email protected] **e-mail: [email protected] Received February 12, 2018

Abstract—This work studies the effect of the reduction of steppe and tundra landscapes in Northern Asia during the Late Pleistocene and Holocene climatic changes on the ranges of large herbivorous mammals. The relationship between a complex of characteristics of herbivore species and their landscape was evaluated. It is found that not only the Mongolian gazelle, saiga, and musk ox, but also the snow sheep, the ancestors of domestic sheep and goats, and probably the Amur goral may reduced their ranges during the late Quaternary landscape changes. The widening of the range of the sika deer, as well as the range of the Siberian musk deer associated exclusively with forest landscapes, can be explained by a reduction of open landscapes. Any significant changes in the ranges of roe deer, red deer, reindeer, elk, wild boar, steppe bison, mammoth, woolly rhinoceros, and ancestral and probably related forms of domestic horse and cattle could not be directly caused by landscape changes 17000–7000 years ago, even if they coincide chronologically.

Keywords: global changes, habitat, herbivores, steppe, range, tundra DOI: 10.1134/S207909611804011X

INTRODUCTION ones or primitive human extermination (Nazaretyan, 2010; Sandom et al., 2014; Stuart, 2015). The extermina- Geographic range is one of the most important tion magnitude is easy to imagine with archaeological ecological characteristics of species. Its reduction is data, historical and modern examples, the role of cli- always a reason for conservation efforts (Gaston and mate and the landscape conditions that it defines with Fuller, 2009). However, the reduction, as well as other boundaries of modern ranges (Heptner et al., 1961; range changes, is a widespread phenomenon rather Dinesman and Savinetskii, 2003; Danilkin, 1999, 2002, than an anomaly (Matyushkin, 1976). If the range of a 2005, 2016). It is difficult to separate the influence of species is determined by the complex of this species' landscape conditions from human influence in the adaptations and, thus, geographically corresponds to analysis of the events, both at the present and in the the realized ecological niche (Bigon et al., 1989), its late Pleistocene and Holocene (Nazaretyan, 2010; changes are a natural consequence of changes in envi- Sheremetev et al., 2014b; Stuart, 2015). Assessment of ronmental conditions and/or species characteristics. landscape condition fitness to specific characteristics On the scale of ecological time, the former are charac- of large herbivorous mammals is urgent (Nasimovich, terized by a high level of variability, while the latter by 1955; Gambaryan, 1972; Boeskorov, 2012; Boeskorov constancy. et al., 2016a; Boeskorov et al., 2016b). Changes in range boundaries of large herbivorous Transformation of the habitat conditions of large mammals, like all species with an important role in herbivorous mammals in Northern Asia provides an ecosystems, are visible and often have a simple expla- opportunity to distinguish two phases of their changes. nation (Danilkin, 1999, 2002, 2005). The basic task is In the first climatogenic phase, during climate soften- to analyze the factors determining the long-term ing and humidification, most of the territory of North- trends of these changes (Sheremetev and Panasenko, ern Asia, which was occupied by analogs of the Altai 2013). In paleoecology this task has much in common and Khakass steppes by the end of the last glacial max- with the determination of the main cause of late Qua- imum of the Pleistocene (about 17000 years ago), ternary extinctions: landscape changes follow climatic underwent forest expansion. This expansion ended at

245 246 SHEREMETEV, ROZENFELD the Holocene optimum, which began about 7000 years have a combination of characteristics that determine ago (Khotinskii, 1977; Monin and Shishkov, 1979; their association with only a certain type of landscape. Krasnoborov, 1989; Mol, 2008). An industrial life- support model of human spread about 6400 years ago during the second anthropogenic phase and was char- MATERIALS AND METHODS acterized by the end of human dependence on the Data Sources density of populations of large herbivorous mammals In our analysis of the range dynamics and species as the main prey (Kuz’min, 2005, Chernykh, 2009). characteristics of herbivores associated with their land- Thus, in the period 17000–7000 years ago, changes in scape distribution, we use data from Flerov (1979), Nasi- the ranges of large herbivorous mammals whose spe- movich (1955), Heptner et al. (1961), Tener (1965), cies characteristics fully or to a large extent correspond Sablina (1970), Gambaryan (1972), Matyushkin (1972), to only one landscape type in the region, should be Sisson et al. (1975), Vereshchagin and Baryshnikov associated with landscape changes. (Vereshchagin, 1977; Vereshchagin and Baryshnikov, The changes can be explained by landscape 1980; 1992), McKendrick (1981), Doleisch (1987), changes for only several species of large herbivorous Smuts and Benzuidenhout (1987), Park (1988), Gor- mammals of Northern Asia. These are the musk ox don and Prins (2008), Shoshani (1994), Robbins et al. Ovibos moschatus (tundra), the Mongolian gazelle (1995), Abaturov et al. (2005), Danilkin (1999, 2002, Gazella gutturosa, and the saiga Saiga tatarica (steppes), 2005, 2016), Quo and Zhenq (2000), Boeskorov et al. associated exclusively with open landscapes and the (Boeskorov et al., 2012, 2016), Prikhod’ko (2003), Siberian musk deer Moschus moschiferus associated Clauss et al. (2003, 2008), Sanon et al. (2007), only with forests (Geptner et al., 1961; Danilkin, 2005; McCullough et al. (2009), Nagata (2009), Sheremetev Prikhod’ko, 2003). The wild sika deer Cervus nippon, and Panasenko (2013), Feldhamer et al. (2015), the red deer C. elaphus, the Amur goral Nemorhaedus Kirillov et al. (2015), the sites The Form Gestures of caudatus, the wild boar Sus scrofa, the Siberian roe Animals (The form gestures…, 2014) and Traces of Capreoulus pygargus, and the moose Alces alces are animals (2016), and State Standard GOST 5408-77 known for their predominant use of forest landscape (GOST…, 1980). habitats, and the reindeer Rangifer tarandus and the snow sheep Ovis nivicola by their preference for open lanscapes (Danilkin, 1999, 2002, 2005). The real rea- Selection of Characteristics son for these species’ habitat choice and what the one The list of characteristics was determined by the was before the human activity rise is unknown. The main landscape differences in the herbivore habitat. conditions prior to the intensification of human activ- The specific features of steppe habitats are a lack of ity are also unknown. The habitat choices by the water (open water sources and precipitation including domesticated sheep Ovis aries, goat Capra hircus, cat- snow), dense soil, poor quality of food vegetation and tle Bos taurus, and horse Equus caballus are controlled the associated need for daily and long-term seasonal by humans (Sheremetev et al., 2014a). The landscapes movements in search of food, and the shelter lack due they may be predominantly associated with prior to to good visibility over long distances and mostly flat domestication and the reduction of populations of relief (Mil’kov and Gvozdetskii, 1975; Holechek, their wild ancestors are also unknown. An analysis of 1984; Abaturov et al., 2005; Gordon and Prins, 2008; the landscape associations of the extinct in the Late Sheremetev et al., 2017). The tundra conditions are Pleistocene and Holocene in northern Asia the Lena characterized more generally by a colder climate than horse Equus lenensis, the steppe bison Bison priscus, the by a lack of water. The Mongolian gazelle and saiga are mammoth Mammuthus primigenius, and the woolly rhi- most adapted to the steppe conditions and, like all noceros Coelodonta antiquitatis is still in process nonforest species, are characterized by minimal water (Ukraintseva, 2002; van Geel et al., 2008; Boeskorov, demand, nonselective feeding (grazing), a small foot- 2012; Kirillova et al., 2015; Boeskorov et al., 2016; Boe- print range, a capability of long high-speed running, skorov et al., 2016). The evaluation of the influence of good eyesight as compared to hearing and olfaction, a the Late Quaternary landscape changes on these spe- high degree of sociality, and long-distance daily and cies’ ranges can be justified only by the results of a seasonal movements (Heptner et al., 1961; Abaturov complex independent analysis of characteristics and et al., 2005; Danilkin, 2005; Sheremetev et al., 2014a, their relationship to landscape types that is identical 2017). The benefit of the nonselective feeding of large for all listed species. herbivores results in slow digestion, which favors the The goal of this work is to evaluate the relationships metabolism of methanogenic bacteria in large vol- between the specific characteristics of large herbivo- umes of the food bolus (Clauss et al., 2003, 2008). This rous mammals of Northern Asia and their landscape results in another feature of the steppe herbivore typi- distribution and to reveal specific events in the cal for the Mongolian gazelle and for saiga—a rela- dynamics of these mammals’ ranges in the Late Pleis- tively small size. The characteristics of the musk ox tocene and Holocene that were caused by landscape exclusive to the tundra are in many respects similar, changes. We hypothesize that most species do not except for its relatively large size as an adaptation not

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Table 1. Metric characteristics and indices of large herbivorous mammals of northern Asia Characteristics maximum footprint ear Species body size, footprint ear length, aggregation length/body length/body height, cm length, cm cm (hundreds size, % size, % of individuals) 1 Saiga 83 6 8 7.2 9.6 250 2 Mongolian gazelle 82 5 12 6.1 14.6 100 3 Snow sheep 104 7 10 6.7 9.6 0.72 4 Goat/sheep 100 6 11 6 11 0.5* 5 Horse 180 12 14 6.7 7.8 0.15* 6 Musk ox 152 14.5 15 9.5 9.9 1 7 Bison 210 13 18 6.2 8.6 0.7 8 Cow 200 11.5 15.2 5.8 7.6 0.5 9 Mammoth 280 44 38 15.7 13.6 –** 10 Woolly rhinoceros 200 18.5 12 9.3 6 – 11 Reindeer 141 15 17 10.6 12.1 10 12 Roe deer 90 5 14.2 5.6 15.8 0.31 13 Amur goral 81 6 17 7.4 21 0.16 14 Elk 221 25 28 11.3 12.7 0.1 15 Sika deer 119 7 18.6 5.9 15.6 0.35 16 Red deer 150 8 22 5.3 14.7 0.22 17 Wild boar 93 15 12 16.1 12.9 1 18 Siberian musk deer 60 7.3 9.8 12.1 16.3 0.04 *Aggregation size is determined by humans and can be significantly larger; **no data available. to a lack of water but to low temperatures. The habitats forest soil, etc. In addition, it is characterized by the of forest herbivores correspond mainly to the opposite footprint length (cm) and its ratio to body size (%). adaptations, most of which are expressed in the musk —The more developed hearing and/or olfaction are deer (Heptner et al., 1961; Prikhod’ko, 2003). We ana- in relation to vision, the higher the animals’ ability to lyzed 14 characteristics of herbivores and 2 indices navigate in conditions of poor visibility created by for- (Tables 1, 2). est vegetation. Relatively well-developed vision is an advantage in conditions of open landscapes. The Preliminary Analysis and Categorization development of hearing is additionally characterized of Characteristics by ear length (cm) and its ratio to body size (%). —More intensive daily and long-term seasonal The scheme for the assessment of species charac- movements results in a higher efficiency of the search teristics were based on the evaluation principles of the for food, which is vitally important in conditions of landscape association of extinct herbivores proposed open landscapes. by G.G. Boeskorov et al. (Boeskorov, 2012; Boeskorov et al., 2016) used analogs from modern related forms if —For trophic strategies, grazing is associated with some parameters were absent. Classification by the the large amount and effective use of forage with a Unweighted Pair-Group Method Using Arithmetic large portion of hardly digestible substances (herba- Averages (UPGMA) and discriminant analysis in the ceous, predominantly monocotyledons, plants) that assessment of the landscape distribution of the consid- are typical for open landscapes; browsing is associated ered species required the categorization of several initially with selectivity in accordance with the food qualities qualitative species characteristics (Reznikov, 1976). expressed in the primary feeding of succulent leaves, young shoots of trees and shrubs, and dicotyledonous The characteristics are represented by two main herbaceous plants of forest landscapes. Grazing is categories and are interpreted as follows. associated most often with foregut fermentation (the —The lower footprint load on the substrate is, the development of a differentiated stomach), and its greater ability to move on loose snow, relatively wet effectiveness increases with a decrease in herbivore

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Table 2. Categorical characteristics of large herbivorous mammals in northern Asia Characteristics

Species vision* hearing olfaction footprint load on the substrate seasonal movements movements daily trophic strategies water requirements type of running mechanics relief habitat 1Saiga 1222111311 2Mongolian gazelle1222111311 3Snow sheep1122112233 4Goat/sheep1122112233 5Horse 1111111212 6Musk ox1222112242 7Bison 2112212142 8Cow 2112211142 9Mammoth2111–**–215– 10Woolly rhinoceros2112––216– 11Reindeer2111112212 12Roe deer2112123222 13Amur goral1112222233 14Elk 2111212122 15Sika deer2112223122 16Red deer2111223122 17Wild boar2111214162 18Siberian musk deer2111223223 Vision*—good (1), weak (2); hearing—good (1), weak (2); olfaction—good (1), weak (2); footprint load on the substrate—small (1), large (2); seasonal and daily movements—expressed (1), not expressed (2); trophic strategy—grazers (1), mixed-feeder (2), browser (3), omnivore (4); water requirements—large (1), moderate (2), small (3); type of running mechanics—high-speed (1), jumping-high-speed (2), jumping (3), light heavy (4), heavy (5), rammed (6); habitat relief—plain (1), indefinite (2), mountainous (3); (–**), no data available. size due to methanogenic bacteria. Browsing is associ- —Increased body size (with terrestrial lifestyles) is ated with hindgut fermentation (the development of correlated with accessibility of tree and shrub shoots the appendix), excluding horses. Intermediate variants and with an increase in the tolerable depth of the snow are identified in the category of mixed-feeders. The cover and, probably, with the active predator resis- omnivorous wild boar is beyond this distribution. tance. All of these are attributes of forest habitats. It is expedient to characterize the size ratio by height —The water requirements vary in consequence, (height at withers, cm). from death without access to water (the sika deer in winter) to satisfaction by the moisture contained in —The higher degree of herbivores’ sociality (as plants and/or dew (Mongolian gazelle). Intermediate based on direct contacts) is, the greater possibility of variants are in a separate category. chase avoidance in open landscapes. The ability of con- tact and gather safety in forest landscape conditions is —The flat relief is indirectly associated with open much less. The sociality degree is characterized by the landscape use in saiga and Mongolian and the moun- number of individuals in the largest aggregations. tainous one with the forest landscape use as in musk deer. The general relationship of relief-type distribu- Of the five types of herbivore running mechanics as tion with the distribution to forest or open landscapes determined by their morphological features, the high still requires statistical verification and is represented speed type is the most consistent with the conditions in many species by a separate category. of open landscapes; the light-heavy type is less consistent. The conditions of forest landscapes correspond An interpretation of the metric characteristics is to the jumping–high speed type of running mechan- given below. ics. The jumping type corresponds to mountainous

ARID ECOSYSTEMS Vol. 8 No. 4 2018 LANDSCAPE CHANGES DURING THE PLEISTOCENE–HOLOCENE TRANSITION 249 rocky habitats, regardless of the type of landscape, and ̶I 9 the heavy and rammed types can hardly determine 60 ̶II directly the landscape distribution. 8

Statistics 40 6 7 The essence of the mechanism of the complex for- 3 5 10 malization of herbivore differences is represented by 2 4 the species ratio according to characteristics associ- 20 Length of intestine, m of intestine, Length ated with the trophic strategy (Fig. 1). The first part of 1 the analysis is the UPGMA classification of herbivores associated exclusively with open and forest land- 0.8 1.2 1.6 2.0 2.4 2.8 3.2 3.6 scapes and other modern and nondomesticated spe- Height at withers, m cies. The second part is the evaluation of the contribution of specific characteristics to this classification and Fig. 1. Length of intestine, height at withers, and fermenta- the grouping of extinct and domesticated species on tion type in some representatives of large herbivorous mam- the basis of the most significant ones. All calculations mals. Designations: (I) foregut fermentation; (II) hindgut were performed with the Statistica 10 software (Stat- fermentation; (1) roe deer; (2) Mongolian gazelle; (3) sheep/goat; (4) horse; (5) red deer; (6) cattle; (7) camel; soft Inc., 2011). (8) musk ox; (9) elk; (10) Asian elephant.

RESULTS 1 The subcluster that unites all the herbivores associ- 2 ated exclusively with open landscapes is of primary 3 interest at the first branch level of the UPGMA tree 6 (Fig. 2). It can be considered a group of open land- 13 scapes which is closest to the snow sheep respectively remaining species according to presented characteris- 11 tics. The eight species united in the second subclaster 14 can hardly be considered a group of forest landscapes 17 due to the wide variety of metric and categorical char- 12 acteristics (Tables 1 and 2) and the variety of their habitat types. An increase in the degree of association with Mammalian species 15 forest landscapes in this group can be expressed as dis- 16 tance to the Siberian musk deer; Old World deer are 18 the closest to them in the space of the presented characteristics (Fig. 2). 20 40 60 80 The absent metric and categorical characteristics Disagreement, % for extinct species (Tables 1 and 2) are not included in the list of those 11 that mostly contribute to the value Fig. 2. UPGMA classification of recent nondomesticated of the first two canonical variables (Table 3). In the large herbivorous mammals of northern Asia (1–3, 6, space of the first two canonical variables, the goat and 11–18) on the basis of characteristics of Tables 1 and 2. the sheep are closest to the types of the open landscape The numerical designations of herbivore species corre- group, and the Old World deer are, as in the UPGMA spond to the numbering in Tables 1 and 2. classification, close to the Siberian musk deer (Fig. 3). Other ten species compactly grouped cannot be asso- skorov, 2012; Boeskorov et al., 2016), are character- ciated exactly with either the open landscape group or ized by the same morphophysiological features of the with the Siberian musk deer. digestive tract as modern elephants and rhinos (Clauss et al., 2003, 2008; Gordon and Prins, 2008). Their DISCUSSION hindgut fermentation and size, even in the absence of The very limited list of species associated exclu- data on the length of the intestine, determine the tro- sively with forest (the Siberian musk deer) or open phic strategies of these species as browsing (Fig. 1). landscapes (Mongolian gazelle, saiga, and musk ox) This and the relatively small footprint load connects cannot be supplemented in strict accordance with the the mammoth and woolly rhinoceros more to forest presented analysis. The woolly rhinoceros and mam- rather than open landscapes, as G.G. Boeskorov and moth, which form the basis of the mammoth fauna his coauthors believed (Boeskorov, 2012; Boeskorov traditionally associated with open landscapes (Veresh- et al., 2016). The classic concept of horse grazing chagin and Baryshnikov, 1992; Tikhonov, 2005; Boe- (Gordon and Prins, 2008) may be the result of steppe-

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Table 3. Standardization coefficients for the first two discriminant functions F1 and F2 (Fig. 3). Variables Characteristics of large herbivorous mammals F1 F2 Body size, cm –5.4 –0.57 Footprint length, cm –3.35 4.8 Vision –0.91 0.18 Trophic strategy –0.32 –0.07 Water requirements 1.9 –1.97 Type of running mechanics 1.48 –0.54 Footprint length/body size, % 1.84 –3.13 Ear length/body size, % –5.5 2.21 Footprint load on substrate 1.3 –1.22 Ear length, cm 8.1 –4.1 Olfaction –1.9 –0.4 Mean value 52.13 4.35 Cumulative fraction 0.92 1 pasture degradation (Sheremetev et al., 2017), whereas fermentation (Clauss et al., 2003; Gordon and Prins, their size and hindgut fermentation also really corre- 2008). Bison can be associated with open landscapes spond to the trophic browsing strategy (Fig. 1; Clauss only according to particular characteristics, and they et al., 2003). cannot be characterized by landscape distribution by One more argument against their conclusive asso- complex analysis like horses (Fig. 1). And like horses, ciation with open landscapes is the later (19th century) the forest ecotype is considered to be later for bison extinction of forest tarpan (Heptner et al., 1961). Pas- (Danilkin, 2005). All of the other species that cannot tures of both open and forest landscapes are success- be attributed to herbivores of open or forest landscapes fully used in the management of horses and other according the distribution in the space of the first two domesticated species. Notably, the goat among canonical variables do not reveal landscape exclusivity domesticated species is usually classified as a browser in habitat use. In particular, this is typical for telemeta- despite the relatively small size and type of intestinal carpal deer (Danilkin, 1999) and the Amur goral, which E.N. Matyushkin (1972) categorizes as a moun- tain-rock species irrespective of the landscape type. The Old World deer, according to habitat use and also 10 14 to presented characteristics can be considered to be 17 species that are only predominantly associated with 2 13 12 forest landscapes. Also, sheep, goats, and snow sheep 16 8 5 can be considered to be predominantly associated with 11 open landscapes. It should be noted that the complex 0 9 15 7 18 of characteristics of large herbivorous mammals of

F2 4 Northern Asia (with the exception of the characteris- ‒2 tics of Mongolian gazelle, saiga, musk ox, and Sibe- 3 rian musk deer), as well as the specrum of habitat types 2 6 and in modern species are not characterized by land- ‒4 scape certainty. A reduction or expansion of their 1 ranges could not be directly affected by replacing open landscapes with forest ones. ‒15 ‒10 ‒5 0 5 The reconstruction of the late Quaternary range F1 dynamics of large herbivors in Northern Asia based on these data is as follows. The range reduction began for Fig. 3. Distribution of large herbivorous mammals of the saiga, Mongolian gazelle, and musk ox in the Northern Asia (1–18) in the space of the first two discrim- phase of the most intensive landscape changes inant functions F1 and F2 on the basis of the most significant characteristics (Table 3). The numerical designations (17000–7000 years ago). Their characteristics ceased of herbivorous species correspond to the numbering in to correspond to habitat conditions over the greater Tables 1 and 2. part of the former ranges. The ranges of the snow

ARID ECOSYSTEMS Vol. 8 No. 4 2018 LANDSCAPE CHANGES DURING THE PLEISTOCENE–HOLOCENE TRANSITION 251 sheep and the Amur goral at that time became frag- characteristics. Any significant changes in their ranges mented rather than decreased due to the characteris- within 17000–7000 years ago could not be directly tics that determine the possibility of using of moun- caused by landscape changes, even if they correspond tain-rock habitats. If the ranges of the main ancestral chronologically. forms of domestic sheep and goats were not initially located in more southern and continental ranges and were not expanded by humans, probably even before COMPLIANCE WITH ETHICAL STANDARDS the beginning of the Holocene optimum, their Сonflict of interests. The authors declare that they dynamics may have also been related to landscape have no conflict of interest. changes. The later reduction of the range of these spe- Statement on the welfare of animals. This article cies and the extinction of the musk ox in the tundra of does not contain any studies with animals performed Eurasia about 3000 years ago cannot be explained by by any of the authors. landscape changes. The significant range expansion of the Siberian musk deer in Northern Asia chronologically corresponds to the phase of the most intensive ACKNOWLEDGMENTS landscape changes and is explained by the correspon- This work was supported by the Program Biodiver- dence of its characteristics to the new landscape con- sity of the Presidium of Russian Academy of Sciences. ditions. The sika deer characteristics weaker correspond to the conditions, and the wild boar characteristics do not. However, the expansion of their ranges REFERENCES occurred at the same time. 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