The edge of two worlds : A new review and synthesis on Eurasian forest-steppes

1Institute of Ecology and Botany, MTA Centre for Ecological Research, Vácrátót, Hungary 2Faculty of Agriculture and Natural Sciences, Düzce University, Konuralp, Turkey 3Institute of General and Experimental Biology SB RAS, Ulan-Ude, Russia 4Department of Ecology, University of Szeged, Szeged, Hungary 5Department of Botany, University of Veterinary Medicine, Budapest, Hungary 6Department of Climatology and Landscape Ecology, University of Szeged, Szeged, Hungary 7College of Urban and Environmental Sciences, Peking University, Beijing, China 8Institute of Plant Sciences, University of Graz, Graz, Austria 9Department of Biology, Faculty of Basic Sciences, University of Mazandaran, Mazandaran, Iran 10Department of Biology, I. G. Petrovsky Bryansk State University, Bryansk, Russia 11MTA-DE Lendület Functional and Restoration Ecology Research Group, Debrecen, Hungary


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Applied Vegetation Science ERDŐS Et al. Asia, the terms "forest-steppe" or "wooded-steppe" are used, compared to "steppe forest", "open woodland" and "sparse arid woodland" in southwestern Asia. In this paper, we treat these terms as synonyms.
The majority of researchers mention one or more of the following points as decisive characteristics in defining forest-steppes: (a) the transitional spatial position (between closed forests and treeless steppes), (b) semi-humid to semi-arid climatic features, and (c) a mosaic-like vegetation pattern. (d) Special soil characteristics as key drivers for vegetation may be considered a fourth criterion (soil is a basic part of nearly all steppe definitions; see for example : Allan, 1946;Berg, 1958;Chibilyov, 2002;Dokuchaev, 1899;Walter & Breckle, 1989). We henceforth discuss the suitability of each of the above four points for defining forest-steppes.
For example, the definition is problematic in both the Carpathian Basin and the Russian Far East, due to the lack of a southern steppe border (Fekete, Molnár, Magyari, Somodi, & Varga, 2014;Ivanov, 2002). Furthermore, forest-steppes occur not only near the northern edge of the steppe zone, but also in the steppe region of the Middle East, without necessarily forming a transition towards the closed forests (Wesche et al., 2016). For instance, in some Iranian and Afghan mountain ranges, open woodlands can be found between low-elevation semi-desert-like steppes and high-mountain thorn cushion communities (Breckle, 2007;Sagheb-Talebi, Sajedi, & Pourhashemi, 2014;Zohary, 1973). In the Qilian Mts, forest-steppes have developed above the lower (arid) timber line, but the closed forest zone is lacking due to the proximity of the upper (cold) timber line (Walter & Breckle, 1989).
A simplistic definition of forest-steppe as a transitional zone between treeless steppe and closed forest may therefore be inadequate, and other factors such as topography or soil grain size should be considered.
Another recurring element of forest-steppe definitions is that the grassland component is represented by meadow steppes (e.g. Chibilyov, 2002;Kleopov, 1990;Lavrenko, 1980;Lavrenko & Karamysheva, 1993;Müller, 1981;Zlotin, 2002), i.e. rather mesic tall grasslands with numerous forbs. Several cases, most notably in regions with considerable mediterranean influences, demonstrate that the grassland component is in fact a dry grassland with short grasses, and limited number and cover of forbs.
Based on the reviewed criteria we argue that a broad yet accurate definition of forest-steppes requires both climatic (semi-humid to semi-arid) and physiognomic (a mosaic of arboreal and herba- 2012; Mayer, 1984;Walter & Breckle, 1989). When the distribution of forest-steppe is determined primarily by macroclimate, the foreststeppe is zonal. However, forest-steppes may also develop outside this transitional climatic range, provided that local factors modify water availability so that neither component has a competitive advantage. For example, in a region of sufficient humidity to support forests, soils with an extremely low water retention capacity or steep south-facing slopes with a warm microclimate may result in a forest-grassland mosaic. In this case, the forest-steppe is considered extrazonal.
Many additional drivers contribute to the dynamics of the forestgrassland co-existence. The interplay of climate, competition, facilitation, fire, grazing and browsing in maintaining the vegetation mosaic is as yet not fully understood for complex forest-grassland ecosystems (e.g. House, Archer, Breshears, Scholes, & Tree-Grass Interactions Participants, 2003;Sankaran, Ratnam & Hanan, 2004;Scholes & Archer, 1997;Stevens & Fox, 1991).
An exact definition and the accurate delineation of foreststeppes is complicated by inherent ambiguity. The grassland-forest continuum ranges from totally treeless grasslands to closed forests (Breshears, 2006). Based on the physiognomy, forest-steppes lie somewhere between the two extremes, but the proportion of grasslands and forest patches varies widely (Illyés et al., 2007).
The middle of the continuum (i.e. 50% arboreal and 50% grassland vegetation) is clearly a forest-steppe, but the designation of lower and upper thresholds is necessarily arbitrary and often difficult (e.g. Berg, 1958;Chibilyov, 2002).
An additional question is whether a mosaic of grasslands and shrubby vegetation should be regarded as forest-steppe. If low shrubs occur only, such as Prunus tenella, the complex may be termed shrub-steppe and classified among steppes (Berg, 1958;Lavrenko & Sochava, 1956;Lavrenko, Karamysheva & Nikulina, 1991). In contrast, 2-6-m tall Pistacia spp., Juniperus excelsa or Quercus pubescens individuals or small stands in a grassland matrix are usually classified among forest-steppes.
Considering the arguments outlined above, our definition of forest-steppes is as follows: forest-steppes are natural or nearnatural vegetation complexes of arboreal and herbaceous components (typically distributed in a mosaic pattern) in the temperate zone (excluding the Mediterranean), where the co-existence of forest and grassland is enabled primarily by the semi-humid to semiarid climate, complemented by complex interactions of biotic (e.g. grazing, land use) and abiotic (e.g. soil, topography) factors operating at multiple scales. The arboreal cover (with a minimum height of 2 m) is 10%-70% across the entire landscape mosaic. The vascular vegetation cover within the grassland is at least 10% (correspond- Our forest-steppe definition therefore rests on physiognomic features and the underlying environmental factors, the most important of which is climate. This broad understanding of foreststeppes includes lowland forest-grassland macromosaics (e.g. in Eastern Europe and the southern parts of West Siberia), exposurerelated mountain forest-steppes (e.g. in Inner Asia), fine-scale forestgrassland mosaics (e.g. in the Carpathian Basin) and open woodlands (e.g. in the Middle East).

| ARE FORE S T-S TEPPE S A B I OME?
Whether forest-steppe is a biome in its own right or only a transition between two neighbouring biomes may be considered a merely semantic question. However, it should be pointed out that foreststeppes differ considerably from both closed forests and treeless steppes in terms of numerous features, including physiognomy, habitat complexity, ecological functions and abiotic parameters, as has been shown for a number of forest-grassland mosaic ecosystems (e.g. Bannikova, 2003;Breshears, 2006;Erdős et al., 2014;Scholes & Archer, 1997;Wendelberger, 1989).
Based on the biogeographic view of Lomolino et al. (2010) and Cox, Moore, and Ladle (2016), who define biomes based on their climate and physiognomy (i.e. vegetation structure), we may conclude that forest-steppes satisfy the criteria to be considered a biome as they have a specific climate and a characteristic physiognomy. Here we have to emphasize that this concept includes latitudinal as well as altitudinal vegetation zones, which fits well with our understanding of forest-steppes. However, the recognition of forest-steppes as a biome is a subject of scientific controversy. Some of the well-known global classification systems treat forest-steppes as a mere contact area between two adjacent biomes or zones (rather than a separate biome or zone in its own right). For example, in the classification of Walter (1979), our forest-steppe definition is equivalent to those of zonoecotone VI/ VII (transition between nemoral forest and steppe), zonoecotone VII/VIII (transition between taiga and steppe) and zonoecotone IV/VII (transition between the Mediterranean and steppe), complemented by some parts of the Tibetan subzonobiome (within zonobiome VII) and areas from mountain orobiomes (e.g. Crimean Mts, Caucasus, Kopet Dag, Pamir-Alai, Tian Shan). Regarding the scheme of Schultz (2005), our forest-steppe definition is included in the ecozone "dry midlatitudes" and the contact zone between the ecozones "subtropics with winter rain" and "dry tropics and subtropics". In the system of Pfadenhauer and Klötzli (2014), our forest-steppes are included mainly in the dry nemoral subzone, but considerable parts belong to the subtropical subzone with winter rain.

| PHYS I OG EOG R APHI C S E T TING
Forest-steppes cover vast areas in Eurasia (2.9 million km 2 according to Wesche et al., 2016; although the figure may be higher, depending on the defining criteria). The altitudinal range of foreststeppes extends from sea level (e.g. Turkey-in-Europe and Crimea) up to some 3,500 m a.s.l. (Qilian Mts), including lowlands, hilly The most important latitudinal climatic gradient is along the increase in aridity to the south (Zlotin, 2002). Plant species richness usually decreases toward the steppe zone (Liu & Cui, 2009;Zlotin, 2002), although the most obvious change is the reduction of tree abundance (Schultz, 2005). In forest-steppe areas within the proximity of the closed forest zone, steppes are limited to small patches (Walter & Breckle, 1989). As aridity increases towards the south, grasslands become more extensive, while forest patches become smaller. Within the southern forest-steppe belt, forest patches are almost always very small.

| FORE S T-S TEPPE S ON A COAR S E SC ALE: MA JOR D IVIS I ON S
A north-south divide bisects forest-steppes into a western and an eastern part. The transition zone is considered to be either near Lake Baikal (Berg, 1958) or near the Altai Mts and the Yenisei River (Lavrenko, 1969;Lavrenko et al., 1991). Phytogeographic ranges of forest-steppe species lend support to both of these propositions, suggesting a blurred boundary (Hilbig, Jäger, & Knapp, 2004;Nimis et al., 1994;Popov, 1963). However, given that the main floristic and vegetation changes begin in the western part of the Altai Mts, classifying the Altai-Sayan-Baikal area to the eastern foreststeppe section appears well founded. In terms of climate, plant species composition and syntaxa, a major boundary exists at the F I G U R E 1 The distribution of Eurasian forest-steppes and the main forest-steppe regions. Region A: Southeast Europe, Region B: East Europe, Region C: North Caucasus and Crimea, Region D: west Siberia and north Kazakhstan, Region E: Inner Asia, Region F: Far East, Region G: Middle East, Region H: Central Asia and southwestern Inner Asia, Region I: eastern Tibetan Plateau. The GIS map (shp file) may be found in Appendix S1. Methods and sources used for delineating forest-steppe areas are given in Appendix S2
While northern forest-steppes occupy space between mesic steppes and forests, southern forest-steppes usually appear in a transitional zone (a) between forests and semi-desert-like steppes, (b) between forests and alpine communities, or (c) between steppes and alpine/ sub-alpine communities.

| MAIN FORE S T-S TEPPE REG I ON S
We here provide a basic description of the main regions ( Figure 1).
Our delineation rests on a combination of floristic and physiognomic characteristics, as well as relief and climate features. We relied on previously published material and expert knowledge, complemented by climatic data of selected stations located within forest-steppe areas. Climate data, as well as information about the remaining forest-steppe areas and current land-use practices are given in Table 1.
Forest-steppes in this region are under considerable mediterranean climatic influences, with increasing continental effects towards the northeast. Thrace is transitional towards the Anatolian foreststeppes (Region G). Forest-steppes typically occupy plains (from sea level to 250 m a.s.l.), but some hills and mountains (often on southfacing slopes) also host similar forest-grassland mosaics. Mean annual temperature is 9.0-12.5°C (up to 13.5°C in Thrace). Summers are hot, winters are mild. Mean annual precipitation is 420-600 mm, with a maximum in early summer, a secondary maximum in autumn and a semi-arid period in between.

| Region B -East Europe
Southern part of the East European Plain (northeast Romania, Moldova, southeast Poland, Ukraine, southwest Russia; Milkov, Box 1 Eurasian forest-steppes: A fact sheet Definition: natural or near-natural vegetation complexes of arboreal and herbaceous components (typically distributed in a mosaic pattern) in the temperate zone, where the co-existence of forest and grassland is enabled primarily by the semi-humid to semi-arid climate, complemented by complex interactions of biotic and abiotic factors operating at multiple scales. The arboreal cover (height >2 m) is 10-70% across the entire landscape mosaic, while the vascular vegetation cover within the grassland is at least 10%.
Forest-steppes as a transitional zone or a separate biome: as biome definitions usually rest on climate and physiognomy, it may be concluded that forest-steppes satisfy the criteria to be considered a biome. However, this is a subject of scientific controversy, and some well-known global vegetation classification schemes treat forest-steppes as a mere contact area between two adacent biomes, rather than a separate biome in its own right.
Stretching from Podolia and the eastern foothills of the Carpathians to the southern foothills of the Ural Mts, forest-steppes of this region occupy lowlands and hilly areas between ca. 90 and 500 m a.s.l. Climate is temperate continental, with some mediterranean influence in the westernmost parts. Mean annual temperature is approximately 9°C in the west, and ca. 3°C in the east. Summers are warm, winters are moderately cold. Mean annual precipitation varies between 400-600 mm (up to 660 mm in Podolia), with a peak in June (-July) and a semi-arid period in late summer.
Large and mesic forest patches are formed mainly by broadleaved deciduous trees (Acer platanoides, Fraxinus excelsior, Q. robur, Tilia cordata, Ulmus glabra), although Populus tremula and Betula pendula are also common. The grassland patches are mesic, hence the names "meadow steppe" and "steppified meadow" (the two differ regarding the role of xeric species, although the distinction is used mainly by Russian and Ukrainian authors; e.g. Kuzemko, 2009;Semenishchenkov, 2009;Averinova, 2010
Forest-steppes occupy substantial areas from sea level up to ca. 600 m a.s.l. The whole region is under marked mediterranean climatic influence. Mean annual temperature is 9.5-12.0°C. Mean annual precipitation varies from 300 to 600 (-770) mm, with the maximum in summer.
In the North Caucasus, mesic forest patches are composed of Acer campestre, Carpinus betulus, Q. petraea, Q. robur and Tilia dasystyla. In the Crimea, forest-steppes are more xeric and show remarkable similarities with those of the Middle East (Region G) and the Lower Danube Plain (in Region A) (Donită, 1970). In the northwest- TA B L E 1 Basic climatic parameters (to the nearest 0.5°C and 10 mm), remaining areas (+: small, ++: medium, +++: large) and current land-use practices (−: absent or very rare, +: rare, ++ moderately widespread, +++: widespread) of forest-steppes

| Region I -Eastern Tibetan Plateau
Eastern parts of the Tibetan Plateau (southwest China; Wu, 1980;Chang, 1981;Zhao, Wu, Yin & Yin, 2011). Forest-grassland mosaics of the eastern areas of the Tibetan Plateau may only tentatively be classified among forest-steppes owing to the ambiguity of the primary cause underlying the mosaic pattern. From the southeastern periphery to the central parts of the Plateau, forests gradually give way to meadows and steppes, with a broad transitional zone. The opening up of the forest is a result of a combination of decreasing temperature and decreasing precipitation, although temperature appears as the primary driver in most cases. The elevation is 3,200-4,000 m a.s.l. Mean annual temperature is between −3°C and +7°C.
Consequently, forest-steppes should by no means be conceived as simple two-phase systems. Instead, they are characterized by multi-level spatial heterogeneity, where forest, scrub and grassland patches of many types and different sizes, connected by a network of differently oriented edges, form an intricate and highly complex system. An integrated view of these complex ecosystems, including all components, is a prerequisite for the efficient conservation and sustainable use of forest-steppes (cf. Luza, Carlucci, Hartz & Duarte, 2014).
The functional diversity of forest-steppes is exceptionally high.

| CO N S E RVATI O N S TATUS
Forest-steppes and steppes have been transformed by human activity more than any other part of Northern Eurasia (Chibilyov, 2002), although there are regional differences concerning the level of anthropogenic impacts (Table 1). The proportion of destroyed or severly degraded forest-steppes generally decreases towards the east, where agriculture began later (Zlotin, 2002). Forest-steppes have largely persisted in many Asian landscapes east of the Ural Mts (Lavrenko & Karamysheva, 1993;Smelansky & Tishkov, 2012).
However, the situation is much worse in the western parts of the forest-steppe zone.
Forest-steppes are highly sensitive to even small changes in factors determining forest/grassland proportion and distribution (Bartha et al., 2008;Kovács-Láng et al., 2000). In many European  (Breckle, 2007). The biodiversity of the Kazakh forest-steppe is highly threatened by farming and collection of plants (Rachkovskaya & Bragina, 2012). The rapid increase in the number of grazing livestock (especially goats) and logging negatively affect the flora and fauna of the Mongolian forest-steppes (Liu, Evans, et al., 2013;Wallis de Vries et al., 1996). However, since the regime change in the eastern bloc around 1990, abandonment of former croplands has increased (Alcantara et al., 2013;Schierhorn et al., 2013;Smelansky & Tishkov, 2012), providing a unique opportunity for the spontaneous recovery or planned restoration of ERDŐS Et al.
Forest-steppe conservation requires addressing certain knowledge gaps. First of all, conservation targets at continental, regional, national and local levels must be identified. Second, more research is needed to decide where the conservation of the status quo is a realistic goal, and where inevitable changes must be accepted or even facilitated. Third, practitioners must be equipped with adequate knowledge to choose between non-intervention and active management strategies. It is not yet fully known where the re-establishment of traditional practices in forest-steppe landscapes is a useful strategy, and where land-use pressure should be reduced. While identifying optimal management is challenging, we believe that a thorough knowledge of local circumstances combined with trial-and-error may be the way to success.

| CLIMATE CHANG E
Although climate change is not yet considered the greatest threat to forest-steppes Kamp et al., 2016), these ecosystems, where both forests and grasslands are near the margin of their tolerances, may be particularly vulnerable. Although droughtadapted forest types such as those in forest-steppes may be able to withstand short (seasonal) droughts, they are threatened by long (multi-year) droughts .
Vegetation responses to changing climate may include (a) changing species composition within patches but sustained patchwork of grassland and forest stands, (b) altered pattern of grassland and forest patches, such as shrinkage or expansion of one patch type at the expense of the other, and (c) complete disappearance of one patch type and thus a shift of biome boundaries.
In Trans-Baikalian and northern Mongolian forest-steppes, Pinus sylvestris may replace Larix sibirica in a drier climate due to its capacity to cope with drought stress (Anenkhonov et al., 2015;Dulamsuren et al., 2009). In the Carpathian Basin, species diversity in forest-steppe grasslands may decrease with increasing aridity, while interannual variability and the number of annual species may increase (Bartha et al., 2008;Kovács-Láng et al., 2000).
The response of forest patches to future climatic changes may mimic behaviour along climatic gradients, where forest patch size and cover decrease with increasing aridity (Kovács-Láng et al., 2000;Xu et al., 2017). Xu et al. (2017) found that small forest patches had increased mortality and decreased regeneration after disturbances than larger patches. A recent field study in Inner Asia has already revealed widespread tree mortality and decreased tree growth at the most xeric sites in response to increased water deficit (Liu, Williams, et al., 2013). Permafrost melting is likely to affect vegetation, including reducing forest cover (Sharkhuu & Sharkhuu, 2012).
Continued warming and drying may lead to broad-scale biome shifts.
Northward movement of vegetation belts is predicted for several parts of Eurasia (e.g. Angerer et al., 2008;Ishii & Fujita, 2013;Kamp et al., 2016;Zhang et al., 2011). This would lead to an overall decline of forest-steppes in Mongolia (Angerer et al., 2008). Central parts of the Carpathian Basin may be replaced by treeless steppes in the long term (Hickler et al., 2012), with an increase in the proportion of Mediterranean species (Thuiller, Lavorel , Araújo, Sykes & Prentice, 2005).
The non-linear nature of climate change impacts renders detection difficult; systems may resist certain levels of environmental change, which may then be followed by a sudden and large-scale vegetation shift (Liu & Piao, 2013). Extreme climatic events or disturbances may be catalysts of such changes (Kröel-Dulay et al., 2015).
Changing climate may affect ecosystems not only directly, but also in combination with other factors, such as land use or biological invasion. For example, in the forest steppe of the Mongolian Altai Mts, earlier snow melt resulting from warming climate caused reduced migration of pastoral nomads, which, in turn, led to an intensified use of local forest patches (Lkhagvadorj et al., 2013). Drought and associated insect damage resulted in severe forest mortality in Anatolian forest-steppes .
All these examples demonstrate that forest-steppe ecosystems are already responding to changing climate. With predicted
further warming and changing precipitation regimes in the 21st century (IPCC 2014), climate change may become one of the most important threats to the biodiversity and integrity of numerous ecosystems (Sala et al., 2000), including forest-steppes.
Moreover, it has been suggested that the interaction of climate change and habitat fragmentation may have disastrous consequences for biodiversity (Travis, 2003), worsening forest-steppe prospects, given the high level of habitat loss in the biome (Hoekstra et al., 2005).

ACK N OWLED G EM ENTS
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