The spread of grass-dominated habitats in Turkey and surrounding areas during the Cenozoic: Phytolith evidence

Palaeogeography, Palaeoclimatology, Palaeoecology 250 (2007) 18 – 49 www.elsevier.com/locate/palaeo

The spread of grass-dominated habitats in Turkey and surrounding areas during the Cenozoic: Phytolith evidence Caroline A.E. Strömberg a,b,⁎, Lars Werdelin a , Else Marie Friis b , Gerçek Saraç c a b

Department of Palaeozoology, Swedish Museum of Natural History, Box 50007, 104 05 Stockholm, Sweden Department of Palaeobotany, Swedish Museum of Natural History, Box 50007, 104 05 Stockholm, Sweden c MTA Genel Müdürlügü, 06520 Ankara, Turkey Received 8 October 2006; received in revised form 22 January 2007; accepted 27 February 2007

Abstract The arrival of hipparionine horses in the eastern Mediterranean region around 11 Ma was traditionally thought to mark the simultaneous westward expansion of savanna vegetation across Eurasia. However, recent paleoecological reconstructions based on tooth wear, carbon isotopes, and functional morphology indicate that grasses played a minor role in Late Miocene ecosystems of the eastern Mediterranean, which were more likely dry woodlands or forests. The scarcity of grass macrofossils and pollen in Miocene floras of Europe and Asia Minor has been used to support this interpretation. Based on the combined evidence, it has therefore been suggested that Late Miocene ungulate faunal change in the eastern Mediterranean signals increased aridity and landscape openness, but not necessarily the development of grass-dominated habitats. To shed new light on the Miocene evolution of eastern Mediterranean ecosystems, we used phytolith assemblages preserved in direct association with faunas as a proxy for paleovegetation structure (grassland vs. forest). We extracted phytoliths and other biogenic silica from sediment samples from well-known Early to Late Miocene (∼20–7 Ma) faunal localities in Greece, Turkey, and Iran. In addition, a Middle Eocene sample from Turkey yielded phytoliths and served as a baseline comparison for vegetation inference. Phytolith analysis showed that the Middle Eocene assemblage consists of abundant grass phytoliths (grass silica short cells) interpreted as deriving from bambusoid grasses, as well as diverse forest indicator phytoliths from dicotyledonous angiosperms and palms, pointing to the presence of a woodland or forest with abundant bamboos. In contrast, the Miocene assemblages are dominated by diverse silica short cells typical of pooid open-habitat grasses. Forest indicator phytoliths are also present, but are rare in the Late Miocene (9–7 Ma) assemblages. Our analysis of the Miocene grass community composition is consistent with evidence from stable carbon isotopes from paleosols and ungulate tooth enamel, showing that C4 grasses were rare in the Mediterranean throughout the Miocene. These data indicate that relatively open habitats had become common in Turkey and surrounding areas by at least the Early Miocene (∼ 20 Ma), N 7 million years before hipparionine horses reached Europe and arid conditions ensued, as judged by faunal data. © 2007 Elsevier B.V. All rights reserved. Keywords: Cenozoic; Grassland evolution; Phytoliths; Europe; Mediterranean; Paleoecology

1. Introduction ⁎ Corresponding author. Current address: Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560-0121, USA. Fax: +1 202 786 2832. E-mail address: [email protected] (C.A.E. Strömberg). 0031-0182/$ - see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.palaeo.2007.02.012

Savanna-mosaic, open habitats are dominant habitat types in the modern world (Archibold, 1995). Their global spread during the Cenozoic is thought to have

C.A.E. Strömberg et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 250 (2007) 18–49

profoundly influenced the biotic and abiotic environment (Jacobs et al., 1999; Retallack, 2001; Kidder and Gierlowski-Kordesch, 2005). Not least, the evolution and dispersal of hominins have been linked to the widely distributed Old World savanna habitats (Dennell and Roebroeks, 2005). However, the origin and distribution of these open habitats in the mid to late Cenozoic, as well as the timing of their establishment in modern form, have been much debated over the past decades (Fortelius et al., 1996; Jacobs et al., 1999; Solounias et al., 1999). Nor is the floral composition of these open habitats well understood (e.g., Leopold et al., 1992; Quade et al., 1994; Solounias et al., 1999; Fortelius et al., 2002). The strongest evidence for the spread of open, savannamosaic habitats has traditionally been changes in the functional morphology of fossil mammals. Locomotory specializations, dietary preferences, and body size distributions of extinct mammalian faunas inferred from modern analogues has provided the basis for inferences about vegetation type (e.g., Kurtén, 1952; Janis, 1993; Fortelius et al., 1996; Hernández Fernández and Peláez-Campomanes, 2003). Above all, weight has been placed on the independent, parallel changes in cheek tooth crown height, from low-crowned (brachydont) to high-crowned (hypsodont), in several ungulate lineages (e.g., horses, rhinocerotids and bovids) during the Miocene (e.g., Osborn, 1910; Stirton, 1947; Kurtén, 1952; Janis and Fortelius, 1988; Janis, 1993; MacFadden, 1997; Fortelius et al., 2002, 2003, 2006). It has thus been assumed that hypsodonty was an adaptive response to the more abrasive foodstuffs associated with open habitats, in particular grasses (e.g., Simpson, 1951; Stebbins, 1981). In addition, wind-blown dust ingested along with grasses and other low-growing plants would have selected for ungulates with hypsodont cheek teeth (e.g., Stirton, 1947; Janis, 1988). Analyses of diversity and ecomorphological proxies in the Oligocene to Miocene of Western Eurasia indicate the successive replacement of faunas interpreted to have been adapted to warm, subtropical forests by faunas characteristic of more open, seasonally arid habitats (Janis, 1993; Bernor et al., 1996a; Fortelius et al., 1996, 2002, 2003; Jacobs et al., 1999; Collinson and Hooker, 2003). This change was not uniform across the region, but occurred later in western Europe (Spain, Portugal, France) compared to the eastern Mediterranean and Asia Minor [a biogeographic region, defined for the Turolian (9–5.3 Ma), which, with somewhat varying content, has been referred to as the Sub-Paratethys (Bernor, 1984), the Greco-Iranian Province (Bonis et al., 1979), the Greco-Irano-Afghan (GIA) Province (Bonis et al., 1992), the Balkano-Iranian Province (Spassov et al.,

19

2004), and the Middle Asiatic Province (Geraads et al., 2002)] (Bernor et al., 1979; Fortelius et al., 1996, 2006; Fortelius and Hokkanen, 2001). In the east, the change to more open habitat-adapted vertebrate faunas appeared to have occurred incrementally since at least the Middle Miocene (15–11 Ma). In contrast, with the exception of certain mesodont and hypsodont taxa in the Early Miocene of Spain (“Hispanotherium fauna”), faunas in western Europe indicate closed habitats until the Late Miocene [9.6–9.2 Ma, spanning the ‘Mid-Vallesian Crisis’ and the subsequent ‘sigmodont event’ (Agustí et al., 1999; Fortelius et al., 1996, 2002, 2003; van der Made et al., 2006)]. Faunal data from the central and north-eastern parts of Europe point to forested conditions throughout the Cenozoic (Fortelius et al., 2002, 2003). Of particular importance for inferring the spread of open habitats has been the Late Miocene (11.1– 10.7 Ma) immigration to Eurasia, from North America via Bering's Strait, of hypsodont hipparionine horses and their subsequent, extensive, adaptive radiation in Europe (Gromova, 1952; Bernor and Hussain, 1985; MacFadden, 1992; Woodburne et al., 1996; Garcés et al., 1997; Jacobs et al., 1999; Bernor and Scott, 2003). In the eastern Mediterranean, the arrival of hipparionine equids coincided with a dramatic diversification of the native ungulate groups (e.g., bovids), leading to the establishment of the so-called Hipparion fauna characterized by extraordinary diversity of large ungulates (e.g., equids, giraffids, rhinos, and antelopes) and other animals (e.g., hyenas) (Kurtén, 1952, 1971). Because of the general taxonomic affinities and superficial ecomorphological resemblance to faunal communities of modern East African savannas, the Hipparion faunas have by tradition come to mark the advent of grassdominated, savanna-like ecosystems in the Old World (e.g., Gaudry, 1862–1867; Osborn, 1910; Abel, 1927; Gabunia and Chochieva, 1982; Bonis et al., 1992; for a review, see also Solounias et al., 1999). In the Late Miocene (9–7 Ma), Hipparion faunas ranged from the eastern Mediterranean to central Asia, across the GrecoIrano-Afghan region (Kurtén, 1952). Solounias et al. (1999) suggested that these faunas represented a distinct, wide-ranging ecosystem, and dubbed it the “Pikermian Biome” after Pikermi, Greece, arguably the most famous of the early Turolian Hipparion faunas. However, in recent years, refinement of the analysis of existing sources of data [e.g., through compilations of large databases such as Neogene of the Old World (NOW, Fortelius, 2006)] and the application of new paleoecological proxies (e.g., tooth wear data, stable isotopes) have challenged the idea of widespread Late Miocene savanna ecosystems.

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First, it is no longer clear that hypsodonty evolved as a response to the spread of grass-dominated vegetation (Fortelius et al., 2002, 2003; Strömberg, 2006). Instead, it has been suggested that the advent of hypsodonty was more closely linked to reduced precipitation, resulting in generally more fibrous and abrasive plants (Damuth and Fortelius, 2001; Fortelius et al., 2002, 2003). Studies of functional morphology and tooth wear of early hipparionines support a modified view of the functional implications of hypsodonty, indicating that these horses were not necessarily the zebra-like obligate grass-eaters they were once envisioned to be. Instead, hipparionine taxa appear to have adopted diverse feeding strategies, ranging from grazing to mixed feeding or even browsing (Hayek et al., 1992; Bernor et al., 2003a; Kaiser, 2003; Kaiser and Fortelius, 2003; Kaiser and Solounias, 2003). Thus, the appearance of hipparionine horses may have signaled a shift in habitat openness, but it probably did not herald the spread of open-habitat grasses (e.g., Agustí et al., 1999). Second, cheek tooth wear data and analysis of masticatory morphology in the Late Miocene fauna of Pikermi indicate that most ungulate taxa, including equids, were browsers or mixed feeders, with no true grazers (Solounias and Dawson-Saunders, 1988; Hayek et al., 1992; Solounias and Moelleken, 1992, 1993; Solounias and Hayek, 1993; Solounias et al., 1999). Meanwhile, Samos, another important Turolian Hipparion faunal locality on the island of Samos, Greece, contains several ungulates (hipparionines, antelopes, giraffids) that have been interpreted as grazers (Solounias et al., 1988, 1995, 1999; Hayek et al., 1992; Solounias and Hayek, 1993; Solounias and Moelleken, 1993). These studies therefore question the homogeneity of Late Miocene eastern Mediterranean aridland ecosystems. Third, stable carbon isotope data from paleosols and ungulate tooth enamel show a predominantly C3 vegetation in Europe and Asia Minor throughout the Neogene (Quade et al., 1994; Cerling et al., 1997; Zazzo et al., 2002). This invalidates a perfect analogy between modern East African savanna ecosystems dominated by tropical C4 grasses and Late Miocene eastern Mediterranean ecosystems. Some authors (Zazzo et al., 2002) maintain that the Pikermian Biome was likely grasslands, but dominated by cool temperate C3 grasses. Others (Quade et al., 1994; Solounias et al., 1999) interpret this isotopic signal in light of the associated palynological records (see below) as reflecting forest or woodland. The fourth line of evidence that casts doubt on the Pikermian savanna hypothesis is the Cenozoic paleobotanical record of Eurasia. Unfortunately, the vast majority of published macrofossil assemblages and palynofloras, in particular the Neogene assemblages, are

from areas north and west of the region corresponding to the Pikermian Biome (Kovar-Eder et al., 1996, 2006; Suc et al., 1999; Collinson and Hooker, 2003; KovarEder, 2003). As a result of the spotty record, Cenozoic paleovegetational patterns are not as well understood for the eastern Mediterranean as for northern and central Europe. Grass fossils are known from the Early Eocene onward (London Clay flora, Chandler, 1964; Thomasson, 1987), but remain rare in Europe and Asia Minor during most of the Cenozoic (Mai, 1995; Jacobs et al., 1999; Worobiec and Worobiec, 2005; Popescu, 2006). Indeed, paleobotanical evidence for grass-dominated habitats, such as savannas, is absent until the Miocene– Pliocene boundary, when records in western Turkey show a massive occurrence of grass pollen (Benda, 1971; Benda and Meulenkamp, 1979; Traverse, 1982; see also Fauquette et al., 2006). There are a few exceptions to this, notably in the late Middle Miocene of the Duero Basin in Spain, where grass pollen constitute ≤29% of certain palynofloras (Rivas-Carballo et al., 1994). In one dominant school of thought, these macrofloral and palynofloral records are taken to primarily document a change in forest composition; from Paleocene paratropical/subtropical evergreen broad-leaved forests to Miocene (warm-) temperate forests dominated by deciduous angiosperms and conifers in north-western and central Eurasia, and to subtropical, subhumid to dry sclerophyllous forests and woodlands in south-eastern Europe (Palamarev, 1987; Axelrod, 1975; Kovar-Eder et al., 1996, 2006; Suc et al., 1999; Collinson and Hooker, 2003; Kovar-Eder, 2003; Ioakim et al., 2005; but see Suc, 1984; Gregor, 1990; Velitzelos and Gregor, 1990; Bruch et al., 2006). In particular, palynological records from Greece, including Samos, show an increase in the abundance of grasses and other herbaceous plants during the Late Miocene (∼10– 7 Ma), which has been interpreted as indicating the presence of more open woodland growing under warm and moist temperate climate, reminiscent of today's wetter Mediterranean uplands (Ioakim and Solounias, 1985; Mettos et al., 2000; Ioakim et al., 2005). This transition is viewed as a change towards cooler climates or a cooler winter season (Mosbrugger et al., 2005), with the development of seasonal aridity at more southern latitudes (Palamarev, 1987; Collinson, 1992; KovarEder et al., 1996; Akgün et al., 2002; Collinson and Hooker, 2003; Kovar-Eder, 2003). The wealth of evidence contesting the ecological importance of grasses in Late Miocene open habitats led many authors to reject the hypothesis of widespread Late Miocene savanna ecosystems, labeling the

C.A.E. Strömberg et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 250 (2007) 18–49

hypothesis the “savanna myth” (Solounias et al., 1999). Instead it was proposed that many of the Pikermian faunas inhabited an evergreen, sclerophyllous woodland or forest ecosystem where grasses were rare (Bernor, 1983; Quade et al., 1994; Solounias et al., 1999). Direct tests of the traditional savanna hypothesis versus the sclerophyllous woodland hypothesis are impeded by difficulties with fully integrating floral and faunal data from Europe and Asia Minor resulting mainly from the different preservation potential of animals versus plants. Plants tend to preserve in moister climates and under anaerobic, nonalkaline, low-energy conditions, whereas animal remains are often found in alkaline, well-oxidized, high-energy deposits (but see Akgün et al., 2000). As a result, macrofossils and palynomorph floras commonly reflect different depositional facies, positions on the landscape, or parts of climatic cycles than do vertebrate fossils, preventing detailed paleoecological comparisons. In addition, for a majority of floral localities, which are not found with intercalated marine sediments, in association with mammalian faunas, or in sections where radiometric or magnetostratigraphic measurements are possible, the age control is often poor (Kovar-Eder et al., 1996; Kovar-Eder, 2003), further complicating temporal comparisons. To resolve this dilemma, we make use of an alternative paleobotanical source of information in the form of siliceous plant microfossils, or phytoliths. Phytoliths form as microscopic bodies of hydrated opal (opal-A) in and around cells in many vascular plants (e.g., Piperno, 1988, 2001, 2006; Sangster et al., 2001). They are deposited in the soil when plants decay, either in situ or after transportation (e.g., through wind or river action or as part of animal droppings), or when plant material is combusted through fire (Piperno, 1988; Fredlund and Tieszen, 1994). Previous work has demonstrated the potential for phytoliths to preserve in Cenozoic vertebrate-bearing deposits (Retallack, 1990; Strömberg, 2002). Phytolith analysis has proven to be a powerful tool for studying vegetation structure in both the submodern and deeper-time record (e.g., Alexandre et al., 1997; Barboni et al., 1999; Runge, 2001; Strömberg, 2005). Despite the idiosyncrasies of phytolith production and preservation – for example that grasses tend to contain more silica than most dicotyledons and conifers – phytolith assemblages appear to faithfully mirror the relationship between grasses and other plants in many ecosystems (see reviews in Piperno, 1988, 2006; Strömberg, 2004). Unlike palynomorphs or macrofossils, phytolith assemblages can thereby often provide a proxy for habitat openness (see discussion in Janis, 1984; Strömberg, 2004). In addition, the relative taxonomic specificity of grass phytoliths (see Dugas and Retallack, 1993; Piperno and Pearsall, 1998; Strömberg, 2004, 2005;

21

Prasad et al., 2005; Piperno and Sues, 2005; Piperno, 2006) allows ecological characterization of the grasses present in fossil assemblages, further enhancing habitat characterization (Strömberg, 2004, 2005). Herein we describe a temporally extensive paleobotanical record (Early–Late Miocene), in the form of phytolith assemblages from well known faunal localities in Turkey, Greece, and Iran. It represents the first such record in immediate association with eastern Mediterranean faunas (but see Akgün et al., 2000), providing direct information about habitat changes through time in this region. With the exception of a pioneering study by Pinilla and Bustillo (1997) in the Middle Miocene of Spain, it also signifies the first application of phytolith analysis to pre-Quaternary sediments in western Eurasia. 2. Materials and methods 2.1. Geologic framework and sample collecting Throughout the Cenozoic, the eastern Mediterranean region has been the subject of dramatic tectonic and volcanic activity linked to the convergence and collision between the Eurasian and Afro-Arabic plates and the intervening microplates (Bozkurt, 2001; Maas et al., 2001; Gürbüz and Gül, 2005). The compressional and extensional processes resulting from these crustal movements led to the progressive formation of complex series of fault-bounded and intermontane basins, into which Cenozoic terrestrial and near-shore sediments accumulated (Koçyığıt, 1991; Sakınç et al., 1999; Bozkurt, 2001; Lunkka et al., 2003; Kelling et al., 2005). In addition, folding and continued faulting has complicated the geological makeup of this region (Innocenti et al., 2005). Consequently, the Cenozoic, and particularly the Neogene, faunal localities of the eastern Mediterranean are largely found as isolated outcrops. Historically, temporal correlation among these sites proved somewhat challenging, as workers had to rely primarily on faunal (or rarely, floral) biostratigraphy (e.g., Steininger et al., 1996). However, in recent years, the application of magnetostratigraphy and, occasionally, radiometric dating to old and new sections has significantly increased our ability to temporally link up faunas from different areas (e.g., Bernor et al., 1996b; Fortelius, 2006) (Table 1). Neotectonism and volcanism associated with the closure of the Neotethyan Ocean also controlled fluctuating sea levels in the Anatolian–Aegean region since the Late Cretaceous (Scotese, 1997; Rögl, 1999; Maas et al., 2001). During the Middle to Late Eocene, central Anatolia was part of a system of Neotethyan island arcs (Maas et al., 2001; Popov et al., 2004). In

Locality name

Ankara–Çubuk– Susuzköy

Çankırı–Orta

Ankara–Kızılcahamam– Keseköy 1–2 A

Ankara–Kızılcahamam– Keseköy 1–2 B

Ankara–Kalecik– Hancılı 1

Izmir–Mordoğan– Ardıç

Ankara–Kazan– Sarılar–İnönü 1 (24, 24A)

Afyon–Suzuk–Gebeciler

Ankara–Kazan–Yassıören, Lower Sinap

Uşak–Eşme–Akçaköy

Ankara–Kazan– Yassıören–Sinaptepe Northeast (T5–95)

Ankara–Kazan– Sarılar–İnönü 2

Kütahya–Çavdarhisar road separation 300 m

Sample number

EM1

EM2

EM3

EM4

EM5

EM6

EM7

EM8

EM9

EM10

EM11

EM12

EM13

n/a

Field (H. de Bruijn)

MN9

MN9-10

Field

Inönü 2; 23321

MN9

MN7+8

MN7+8

MN6

MN5

MN3

MN3

MN3

MN3

Middle Eocene

n/a

b 10.69 (fauna)

11.2–11.0 (magn.)

basal MN9 (fauna); 11.6 ± 0.5 Ma (radio.)

n/a

Sinap (Lower Sinap Member)

Sinap (Lower Sinap Member)

Pazar

∼ 15–16 (lith. + radio.)

n/a

Ardıç

somewhat older than 16.2 (fauna)

Hancılı

Güvem

b 20.1 ± 2.2 Ma (magn.)

n/a

Güvem

b 20.1 ± 2.2 Ma (magn.)

Volcaniclastic (?) clayey siltstone Calcareous clayey siltstone

Sandy siltstone

Calcareous sandy siltstone

Clayey siltstone

Silty sandstone

Calcareous sandy siltstone

Sandy siltstone w/ gastropods, ostracods Clayey siltstone

Carbonaceous clayey siltstone

Laminated siltstone w/ fossil leaf impressions

Bedded silty sandstone

Güvem

N 20.1 ± 2.2 Ma (magn.+ lith.)

Sample lithology

Volcaniclastic silty sandstone (tuff)

Geologic formation

n/a

(Bio-) Other age determination chronozonationc (Ma)d

Field MN9 (J.-P. (lowermost) Lunkka)

NHM, EU

MNHN

MAT

Field

NHM, EU

Field

Field

Field

Field

Field

Sample sourceb

Sinap 65 or Sinap 64; 20535 or 20536

Esme Akçaköy; 20213

Lower Sinap; 20207

Gebeciler; 23271

Inönü 1 (Sinap 24A); 20205

Ardic–Mordogan; 23187

Hancili 1; 23286

Keseköy; 23311

Keseköy; 23311

n/a

n/a

Locality name in NOW

Table 1 Sample and locality information for Cenozoic samples from Greece, Turkey, and Irana

Fluvial overbank (paleosol?) Lacustrine

Fluvial overbank (paleosol)

Fluvial overbank (paleosol) Fluviallacustrine

Lacustrine?

Lacustrine?

close to F level

F level

1.5 m below T5 (magn.)

F level

F level

F level

8–10 m above F level

F level; upper part of formation

F level

Lacustrine

Fluvial

b 2 m above Keseköy 2

Just above lower Keseköy coal eq.; below Keseköy 1 level 1 m above Keseköy 2 (top F level)

Fossil (F) level

Position in section

Lacustrine

Lacustrine

Fluvial overbank (paleosol) Lacustrine

Depositional environment

de Bruijn et al. (1992), Krijgsman et al. (1996), Rummel (1999), Lopéz-Antoñanzas et al. (2004), Fortelius (2006) de Bruijn et al. (1992), Krijgsman et al. (1996), Rummel (1999), Lopéz-Antoñanzas et al. (2004), Fortelius (2006) Kaymakçı (2001), Saraç (2003), Savaşçı and Seyıtoğlu (2004), Fortelius (2006) Krijgsman (2002), Begun et al. (2003), Kaya et al. (2003) Gürbüz (1981), Geraads et al. (1995), Kappelman et al. (1996b, 2003), Steininger et al. (1996), Lunkka et al. (1999), Kaymakçı (2001), Güleç et al. (2003), Fortelius (2006) Kaymakçı (2001), Sickenberg (1975), Saraç (2003), Fortelius (2006) Kaymakçı (2001), van der Made (1996, 1998, 2003), Fortelius (2006) Sickenberg (1975), Sen (1989), de Bruijn et al. (1992), Kaymakçı (2001), Koufos (2003), Fortelius (2006) J.-P. Lunkka, personal communication; Kappelman et al. (2003), Lunkka et al. (2003) Saraç (1994, 2003), Bernor et al. (2003b), Fortelius (2006) H. de Bruijn, unpublished data

G.S., unpublished data; Krijgsman et al. (1996)

G.S., unpublished data

Reference

22 C.A.E. Strömberg et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 250 (2007) 18–49

Ankara–Kazan–Yassıören– Delikayıncak (A23)

Ankara–Kazan– Yassıören–Kayıncak A (Ozansoy's loc. II; loc. 12 in Fortelius et al. (2003)) Afyon–Sandıklı–Selçik

Konya–Merkez– Hatunsaray–Kayadibi

Lower Maragheh

Çanakkale–Ayvacık– Gülpınar

Ankara–Kazan– Sarılar–Kavakdere

EM15

EM16

EM18

EM19

EM20

EM21

EM17

Ankara–Kazan–Yassıören– Delikayıncak (A13)

EM14

NHM, EU

MNHN

Kavakdere (Turolian); 20209

MNHN

MAT

BSPG

Field

Field (J.-P. Lunkka)

Field (J.-P. Lunkka)

Gülpinar; 23373

Maragheh; 20024

Kayadibi; 20216

Selcik; 23276

Sinap 12; 20512

n/a

n/a

MN11

MN11(–12)

MN11

MN11

MN9–12

MN10

MN10 (lowermost)

MN9 (upper)

8.8–8.15 (magn.)

n/a

basal MN11 (fauna); 9–8.24 Ma (radio.)

lowermost MN11 (fauna+ paly.); 9.4 ± 0.2–7.95 ± 0.25 Ma (radio.)

n/a

9.453–9.441 (magn.)

9.5–9.4 (magn.)

10.1–10.0 (magn.)

Calcareous clayey siltstone

Volcaniclastic silty sandstone

Fluvial?

Calcareous sandy siltstone Volcaniclastic (?) sandy siltstone

Fluvial overbank

Lacustrine

Fluvial overbank

Fluvial

Distal alluvial fan (paleosol)

Distal alluvial fan (paleosol)

Distal alluvial fan (paleosol)

Sandy siltstone

Unsorted sandy siltstone

Unsorted sandy siltstone

Sinap Calcareous sandy (Kavakdere Member) siltstone

Maragheh

Yatağan

Sinap (Middle Sinap Member)

Sinap (Middle Sinap Member)

Sinap (Middle Sinap Member)

F level

F level

F level

F level

F level

F level

(continued on next page)

J.-P. Lunkka, personal communication; Kappelman et al. (2003), Lunkka et al. (2003) J.-P. Lunkka, personal communication; Kappelman et al. (2003), Lunkka et al. (2003) Alpagut et al. (1996), Kappelman et al. (2003), Lunkka et al. (2003), Fortelius (2006) Sickenberg (1975), Saraç (2003), Fortelius (2006) Tekkaya (1969), Sickenberg (1975), Köhler (1987), Steininger et al. (1989, 1996), de Bruijn et al. (1992), Tobien (1996), Heissig (1999), Koufos (2003), Fortelius (2006) de Mecquenem (1925), Campbell et al. (1980), Bernor (1986), Bernor et al. (1996c), Steininger et al. (1996), Swisher (1996), Koufos (2003), S. Sen, personal communication T. Kaya, personal communication; Tekkaya (1973), Sickenberg (1975), Kaya (1982), Forstén and Kaya (1995), Geraads and Güleç (1999b), Fortelius (2006) Sickenberg (1975), Geraads and Güleç (1999a),

C.A.E. Strömberg et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 250 (2007) 18–49 23

Uşak–Ulubey– Karacaahmet– Kemiklitepe D

Ankara–Ayaş–Pınaryaka (Seylek)–Asarıntepe Samos Q4

EM22

EM23

Kırıkkale–Keskin– Aşağışıh–Akkaşdağı

Samos Q5

Ankara–Ayaş– Evciköy–Çobanpinar

EM26

EM27

EM28

Field

MNHN

Sample sourceb

Field (S. Sen)

MNHN

Çobanpinar (Sinap 42); 20210

MAT

Locality falls within Samos AMNH Main Bone beds; 20484

Akkasdagi; 23659

Kemiklitepe A–B; 20468

Samos White Sands; 20483 AMNH

Asarintepe; 23315

Kemiklitepe D; 20469

Locality name in NOW

MN13

MN13

MN12 (latest)

MN12

MN12

MN12

MN11

n/a

7.0–6.7 (magn. +radio.)

middle–upper MN12 (fauna); 7.19–6.90 Ma (magn.+ lith.) 7.0–7.2 (radio.)

7.65–7.45 (magn.+ lith.)

n/a

upper MN11 (fauna); 7.89–7.64 Ma (magn. + lith.)

(Bio-) Other age determination chronozonationc (Ma)d

Sinap

Mytilinii (Main Bone Beds)

Silty fine sandstone

Calcareous volcaniclastic sandy siltstone

Tuff

Calcareous clayey siltstone

Ahmetler

Akkaşdağı

Calcareous volcaniclastic siltstone

Sandy siltstone

Silty sandstone

Sample lithology

Mytilinii (White Beds)

Ahmetler

Geologic formation

Fluvial

Pyroclastic flow deposits on distal alluvial fan Fluviallacustrine

Fluviallacustrine

Fluviallacustrine

Fluvial

Fluvial

(paleosol)

Depositional environment

F level

F level; upper part of Main Bone Beds

Just below F level

F level (marly pocket)

F level; top of White Beds member

Below F level

F level (0.5 m above tuff)

Position in section

Solounias (1981), Weidmann et al. (1984), Bernor et al. (1996c), Giaourtsakis (2003), Kostopoulos et al. (2003), Fortelius (2006) Ozansoy (1965), van der Made et al. (2002, 2003)

Kappelman et al. (2003), Lunkka et al. (2003) Bonis et al. (1994), Sen et al. (1994), Geraads and Güleç (1999b), Fortelius (2006) Saraç (1994, 2003), Fortelius (2006) Solounias (1981), Weidmann et al. (1984), Bernor et al. (1996c), Giaourtsakis (2003), Kostopoulos et al. (2003), Fortelius (2006) Bonis et al. (1994), Sen et al. (1994), Geraads and Güleç (1999b), Fortelius (2006) Kazanci et al. (1999, 2005), Karadenizli et al. (2005)

Reference

b

For geographic locations, see Fig. 1. Institutional abbreviations: AMNH = American Museum of Natural History, New York, USA; BSPG = Bayerische Staatssammlung für Paläontologie und Geologie, München, Germany; MAT = Natural History Museum of the Geological Survey of Turkey, Ankara, Turkey; MNHN = National Museum of Natural History, Paris, France; NHM, EU = Natural History Museum, Ege University, Izmir, Turkey. c The biochronological zones for the localities are with a few exceptions taken from the Neogene of the Old World (NOW) database (Fortelius, 2006), which compiles current lithostratigraphical, biostratigraphical, magnetostratigraphical, and radiometric information; name and number for the corresponding NOW locality is indicated for comparison. “MN9” (etc.) refers to Mammal Neogene zones (Mein, 1989). d Other age determination (Ma): fauna = faunal correlation; lith. = lithostratigraphical correlation; magn. = magnetostratigraphy; paly. = palynological correlation; radio. = radiometric dating.

a

Uşak–Ulubey– Karacaahmet–Kemiklitepe B

EM25

EM24

Locality name

Table 1 (continued)

Sample number

24 C.A.E. Strömberg et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 250 (2007) 18–49

C.A.E. Strömberg et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 250 (2007) 18–49

Neogene times, the eastern parts of Anatolia constituted either upland areas or lowlands covered by freshwater lakes, whereas the Aegean basin remained partly inundated (Popov et al., 2004, 2006). As a result of the changing geomorphology of the eastern Mediterranean, the Cenozoic terrestrial deposits of this region reflect a range of sedimentary settings, including marine deltaic, fluvial, lacustrine, and alluvial (Popov et al., 2004) (Table 1). As will be discussed later, this variation impacts somewhat on our ability to directly compare habitat reconstructions through time. Sediment samples for this study were collected at several well-known and well-dated Cenozoic faunal localities in the area around Ankara, Turkey, by C.A.E.S. and G.S. Sediment was also retrieved (by C.A.E.S.) from Turkish and Iranian (Maragheh) faunal collections in several museums (National Museum of Natural History, Paris, France; Natural History Museum, Ege University, Izmir, Turkey; Natural History Museum of the Geological Survey of Turkey, Ankara, Turkey; Bayerische Staatssammlung für Paläontologie und Geologie, München, Germany) (Fig. 1, Table 1). Additional Turkish material was provided from private collections by H. de Bruijn, S. Sen, and J.-P. Lunkka. N. Solounias supplied sediment from Samos faunal collections kept at the American Museum of Natural History, New York, USA, as well as from the field. Samples taken from museum collections represent sediment in which fossil vertebrates were found; field samples were collected from faunal levels as well as from other levels in the same sections. Information on geology and stratigraphy for each locality is given in Table 1 together with relevant references; geographic locations are shown in Fig. 1.

25

magnification of 1000x. Mounting in immersion oil allowed rotation of grass silica short cells for determination of three-dimensional shape. The preservational status of phytoliths in the productive samples was estimated semi-quantitatively by examining the presence and abundance of (a) occluded carbon, (b) fine ornamentation, (c) etching, (d) fragmentation of phytoliths, (e) structural/textural alteration of phytoliths, and (f) secondary silicification (Strömberg, 2003). Emphasis was placed on evaluating these characteristics for diagnostic phytoliths. Note that this classification of phytolith preservation differs from that used by Fredlund and Tieszen (1997), which focuses on quantifying the degree of pitting and erosion of elongate and bulliform cells. Our scheme is quantitatively less well defined, but it attempts to take into account the many different ways in which transport, pedogenesis, and diagenesis may affect a biosilica assemblage. In samples with fair to very good preservation, at least 200 diagnostic phytoliths (classes FI TOT and GSSC in Table 2 and below) were counted on the Meltmount slide, a number which produces statistically reliable results (Pearsall, 2000; Albert and Weiner, 2001; Strömberg, 2003, C. Strömberg, unpublished data). For three samples with poorly preserved phytoliths somewhat less than 200 diagnostic forms were counted and for five other samples, preservation allowed only semi-quantitative description of assemblage composition (see Table 3). Phytoliths were classified according to Strömberg (2005, 2004) using information from the literature (references in Table 2) and a reference collection of phytoliths from modern plants (Strömberg, 2003, C. Strömberg, unpublished data), into the following main categories (Table 2, Figs. 2 and 3):

2.2. Phytolith extraction and classification Close to 200 samples from Greece, Turkey, and Iran were processed for phytoliths using modified standard methods (Strömberg, 2004, 2005). Accordingly, a subsample of 2 g from a larger sample was crushed in a mortar and treated with hydrochloric acid to remove carbonates. The 0–250 μm fraction was isolated by means of sieving and oxidized in Schultze's solution in a hot bath; clays were eliminated through centrifuging (Lentfer et al., 2003). A heavy liquid solution of zinc bromide with a specific gravity of 2.3 was used to isolate biogenic silica (phytoliths, diatoms, sponge spicules, and chrysophyte cysts), which was dried and mounted in a permanent plastic medium (Cargille Meltmount, Cargille Laboratories, Cedar Grove, NJ), as well as in immersion oil, and viewed under a light microscope at a

(1) Forest indicator morphotypes (FI TOT) from (a) palms, and (b) woody or herbaceous dicotyledons, conifers, and ferns; (2) Grass silica short cells (GSSC) produced exclusively by grasses (Poaceae). Grass silica short cells are further subdivided into GSSC morphotypes typical of (a) closed-habitat grasses [in the (Bambusoideae + Ehrhartoideae) (BE) clade, and a variety of basal grasses; (GPWG, 2001)] (CH TOT), (b) openhabitat grasses in the Pooideae [POOID-D (diagnostic), POOID-ND (not diagnostic, but abundantly produced)], (c) open-habitat grasses in the PACCAD clade (Panicoideae + Arundinoideae + Chloridoideae + Centothecoideae + Aristidoideae + Danthonioideae) (PACCAD TOT) and (d) other (unidentified) Poaceae (OTHG);

26

C.A.E. Strömberg et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 250 (2007) 18–49

Fig. 1. Geographic location of sites sampled for this study. For further information, see text and Table 1. Localities: 1 = Susuzköy; 2 = Orta/Keseköy 1–2A, B; 3 = Hancılı 1; 4 = Mordoğan–Ardıç; 5 = İnönü 1 (24, 24A); Yassiören, Lower Sinap; Sinaptepe Northeast (T5–95); İnönü 2; Delikayıncak (A13); Delikayıncak (A23); Kayıncak A (Sinap 12); 6 = Gebeciler; 7 = Eşme–Akçaköy; 8 = Kütahya–Çavdarhisar road separation 300 m; 9 = Selçik; 10 = Kayadibi; 11 = Lower Maragheh; 12 = Gülpinar; 13 = Kavakdere; 14 = Kemiklitepe D; Kemiklitepe B; 15 = Asarıntepe; 16 = Samos Q4; Samos Q5; 17 = Akkaşdağı; 18 = Çobanpinar.

(3) Phytoliths from wetland plants, such as Equisetum and sedges (Cyperaceae) (AQ). An important contributor to this class is silicified stellate facetate parenchyma cells, previously described from Cenozoic sediments from the Great Plains and hypothesized to derive from aquatic monocotyledons (Strömberg, 2003); (4) Non-diagnostic “grass” phytoliths (NDG); (5) Non-diagnostic and unclassified phytoliths (NDO). The latter two groups (NDG, NDO) encompass certain phytolith morphotypes that are used to diagnose grasses by many workers (e.g., Alexandre et al., 1997; Barboni et al., 1999), namely elongate psilate (NDO) and elongate sinuous, echinate, and dendritic (NDG), cuneiform bulliform cells (NDG), and acicular hair cells (NDG). However, many of the NDG and NDO phytoliths are also found in varying abundances in other, non-grass plants (Piperno, 1993, 2006; Strömberg, 2004) and therefore not included in our vegetation analysis (see also Strömberg, 2004, 2005). Specifically, the morphotypes sorted in NDG are often produced by other monocotyledon taxa and certain conifers (Strömberg, 2003; Carnelli et al., 2004), whereas the nondiagnostic morphotypes in NDO are found in a broad range of vascular plants, including dicotyledons, ferns, and lycopsids (Piperno, 1988; Strömberg, 2003). In addition, the production of elongate sinuous and cuneiform bulliform cells seems to be strongly controlled by factors relating to

water availability and rates of evapotranspiration (water stress) (Sangster and Parry, 1969; Madella, 2002; Bremond et al., 2005b; Piperno, 2006). 2.3. Phytolith analysis Habitat structure was inferred through a comparison of (1) the phytolith input from forest indicator taxa vs. grasses (FI TOT vs. GSSC) and (2) the relative GSSC contribution from grasses with different autecologies (e.g., with preference for open vs. closed habitats) (Strömberg, 2005). The importance of GSSC assemblage composition for habitat inference cannot be overestimated. For example, whereas the bamboo vegetation on Mount Kenya is grassdominated, and produces a phytolith assemblage dominated by grass morphotypes (Barboni et al., 2007), it is most appropriately characterized as a bamboo forest (e.g., Edwards, 1940). Phytoliths from wetland plants, semi-quantitative estimates of the relative abundances of diatoms, sponge spicules, and chrysophyte cysts, as well as available sedimentological data provide information about proximity to water, important in determining microhabitat (position on the landscape). Such information is crucial for evaluations of the context and extent of vegetation change, as discussed by Wing (1998). Other phytolith morphotypes, such as elongate facetate and (cuneiform) bulliform cells, which were excluded from

Sedge, Equisetum, unknown aquatic monocotyledon

Unknown Poaceae

PACCAD clade

Phytolith morphotypes (main categories)

Based on quantitative study of a reference collection of phytoliths from modern plants and the literature (e.g., Twiss et al., 1969; Postek, 1981; Mulholland, 1989; Piperno, 1988, 2006; Bozarth, 1992; Watson and Dallwitz, 1992 onwards; Fredlund and Tieszen, 1994; Kondo et al., 1994; Runge, 1996; Kealhofer and Piperno, 1998; Piperno and Pearsall, 1998; Pearsall, 2000; Wallis, 2003; Carnelli et al., 2004; Thorn, 2004; Strömberg, 2004, 2005; Blinnikov, 2005). Descriptors defined by ICPN Working Group (2005) are used in the description of morphotypes whenever possible; for further explanation of morphotypes, see cited references and Strömberg (2004). b FI = forest indicator; GSSC = grass silica short cell; BE clade = clade consisting of the common ancestor of Bambusoideae and Ehrhartoideae and its descendants; Pooideae, diagnostic (POOID-D) = GSSC morphotypes that are generally diagnostic of grasses in the Pooideae; Pooideae, non-diagnostic (POOID-ND) = GSSC morphotypes that are produced in high frequencies by many grasses in the Pooideae, but that are also found in other grasses; PACCAD clade = clade consisting of the common ancestor of Panicoideae, Arundinoideae, Chloridoideae, Centothecoideae, Aristidoideae, and Danthonioideae and its descendants. For further explanation of abbreviations, see text.

a

Various plants and unknown

Grasses and other monocotyledons, conifers

Wetland plant

Closed-habitat grasses (basal Poaceae + BE clade)

Poaceae (GSSC)

Pooideae

FI TOT FI TOT

Forest indicator taxa (FI)

Globular echinate Globular granulate (3–10 μm), globular verrucate (N15 μm), simple and compound globular psilate (3–15 μm), polyhedral epidermis (various types), anticlinal epidermis, silicified non-grass (reniform) guard and subsidiary cells, globular and variously shaped laminar vesicular infilling, irregular sulcate or facetate vascular cell (including Magnolia-type “terminal tracheid” and tuberculate rounded sclereid/tracheid; Postek, 1981), favose aggregate, sclerenchyma and similar (irregular clavate body, often branched, sometimes facetate or papillate surface), “blocky polyhedron” (equidimensional irregular or facetate body) CH TOT Chusquoid body/cross with irregular/spiked “top,” Chusquea-type rondel, Chusquea-type bilobate, collapsed saddle, regular chusquoid body (Piperno and Pearsall, 1998), crescentic keeled rondel Diagnostic POOID-D Crenate (“trapeziform polylobate”; ICPN Working Group, 2005), Stipa-type bilobate NonPOOID-ND Conical and keeled rondel, trapeziform short cells diagnostic (“pyramidal”; Fredlund and Tieszen, 1994) Panicoideae PACCAD TOT Panicoid bilobate and polylobate (Fredlund and Tieszen, 1994), various crosses Chloridoideae PACCAD TOT Saddle, saddle-like PACCAD PACCAD TOT Inverted bilobate/cross (Strömberg, 2005), near-panicoid bilobate, near-panicoid cross, general Merxmuellera-type rondel (convex/concave “base” with bulging sides in side view and flat “top”) OTHG Various GSSC NDG (Cuneiform) bulliform cell, short unciform prickle (“scutiform opal”; e.g., Parry and Smithson, 1966) AQ Epidermal plate with cone shapes (“papillae”; ICPN Working Group, 2005), papillate epidermis, silicified stellate facetate parenchyma (Strömberg, 2003) NDG Elongate sinuous, echinate, and dendritic long cell, acicular hair cell, silicified monocotyledon stomatal complex, monocotyledon tracheary element (cylindric scalariform or scrobiculate), etc. NDO Elongate psilate, cylindric psilate, elongate facetate, cylindric papillate, various unknown morphotypes

Phytolith class

Palm Other FI: woody/herbaceous basal angiosperms and eudicotyledons, conifers, ferns etc.

Plant group b

Table 2 Phytolith classification used herein a

C.A.E. Strömberg et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 250 (2007) 18–49 27

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C.A.E. Strömberg et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 250 (2007) 18–49

the vegetation analysis, were also monitored. Elongate facetate (“blocky”; not to be confused with elongate psilate) phytoliths, while found in low abundances in grasses, are formed in high numbers in certain conifers (e.g., Picea, Rovner, 1971; Blinnikov et al., 2002; Strömberg, 2003; Carnelli et al., 2004). High frequency of elongate facetates in a soil sample is therefore more likely to reflect a conifer element than grasses. As mentioned above, it has been suggested that the abundance of silicified bulliform cells correlates positively with water stress (Bremond et al., 2005b), but it has also been noted that grasses in locally wet habitats form high frequencies of these morphotypes (Sangster and Parry, 1969). Bulliform cells may therefore add to an interpretation of microhabitat or, alternatively, climate. For example, in association with chloridoid openhabitat GSSC, high frequencies of bulliform cells may indicate arid conditions; in association with closed-habitat GSSC and abundant diatoms, they may point to local wetland conditions. The abundance of bulliform cells was roughly estimated by comparing the number of these forms to the number of GSSC morphotypes (bulliform cells/ GSSC). This metric differs slightly from the so-called fanshaped index [Fs: (bulliform cells/(acicular hair cells+ bulliform cells+ GSSC))%], devised by previous authors (Bremond et al., 2005b), mainly by excluding the nondiagnostic acicular hair cell morphotypes. 2.3.1. FI TOT vs. GSSC The ratio of the total sum of FI phytoliths (FI TOT) to the sum of FI TOT and GSSC, herein referred to as the FI-t ratio, was used to trace changes in forest indicator taxa versus grasses through time. Ninety-five percent confidence intervals (unconditional case, using the total count as the sample size) were calculated for the FI-t ratio (Table 3). Because it is generally not possible to directly translate relative abundances in the phytolith record to exact relative abundances of plants in ancient ecosystems (Strömberg, 2004), only relative changes in vegetation structure are considered. To get a more thorough understanding of vegetation, the types and abundances of FI TOT morphotypes were recorded in detail, particularly forms produced by key indicator taxa (e.g., palms, Marantaceae, see Strömberg, 2004). 2.3.2. GSSC assemblage composition A straightforward reading of relative abundances of GSSC morphotypes to infer grass community composition is complicated by non-negligible overlap (‘redundancy’, Rovner, 1971) between GSSC assemblages produced by closed-habitat grasses and open-habitat grasses (Strömberg, 2005). In particular, closed-habitat grasses can sometimes produce fair amounts of phytoliths typical of open-habitat

grasses (Piperno and Pearsall, 1998; Strömberg, 2003). For this reason, we investigated the composition of each fossil GSSC assemblage by comparing it to the assemblage composition of modern grasses, following methods outlined in detail in Strömberg (2005). Accordingly, the assemblages were compared through hypothesis testing using bootstrapping (Simon, 1997). The hypotheses tested differed depending on the overall composition of the short cell assemblages; the various cases are summarized in Table 4. For example, in assemblages with high relative frequencies of closed-habitat GSSC morphotypes (CH TOT), presumably reflecting a high abundance of closed-habitat grasses, we first tested the hypothesis that the assemblage likely reflects the presence of open-habitat grasses in addition to closed-habitat grasses, based on the abundance of morphotypes typical of openhabitat grasses, OH TOT (total sum of open habitat morphotypes = POOID-D + POOID-ND + PACCAD TOT). The null hypothesis is that the variation observed in the GSSC assemblage can be entirely explained by the phytolith production of closed-habitat grasses. The background universes (or urns) used in the tests were obtained from quantitative analysis of the modern reference collection (Strömberg, 2003, C. Strömberg, unpublished data). For each ratio, separate background universes were constructed for leaf and reproductive material, as these materials often have very different GSSC composition (Mulholland, 1989; Piperno and Pearsall, 1998; Strömberg, 2003). Following a conservative approach, maximum ratios were used in each case (Strömberg, 2005). The 95% confidence intervals for the expected ratios (urns) were calculated for each fossil sample using bootstrapping with 1,000 replicates using Resampling Stats 5.0 (available at http://www.resample. com/), and the upper limit of these confidence intervals was compared to the actual ratio of morphotypes observed in the fossil sample (this corresponds to a one-tailed test at α = 0.025; Simon, 1997). If the test metric in the fossil GSSC assemblage exceeds the upper 95% confidence limit for both leaf and reproductive material of the background universe, the null hypothesis can be rejected (i.e., in the example case, it is likely that open-habitat grasses were present in the grass community in addition to closed-habitat grasses). If it does not exceed either of the upper 95% confidence limits, the null hypothesis cannot be rejected. If the test metric exceed the upper 95% confidence limit for the background universe of leaf, but not reproductive material, it is somewhat equivocal and more careful judgment is necessary (see further below). Note that non-diagnostic and unknown GSSC (contained in OTHG in Table 2) were excluded from these calculations because it is not clear whether this

G G G G VP (alt) G(-P) G-P G-P P (alt, et) VP (et) G-P G P (et) G-P G-P P (et) VP (et) G G G P (et) G-P VP (et) G-P P (et) G G-P VP (et)

EM1 EM2 EM3 EM4 EM5⁎ EM6 EM7 EM8 EM9⁎⁎ EM10⁎

EM14 EM15 EM16⁎⁎ EM17⁎ EM18 EM19 EM20 EM21⁎⁎ EM22 EM23⁎ EM24 EM25⁎⁎ EM26 EM27 EM28⁎

EM11 EM12 EM13⁎⁎

Preservationc

Sample numberb

0.2 0.3 1.8 0.0 p 0.2 0.4 0.6 0.5 n.o. p 1.1 p 0.6 0.8 0.7 n.o. 0.0 0.9 0.0 p 0.2 n.o. 0.0 0.0 0.6 0.0 p

AQ (%) 20.5 0.5 1.8 1.3 p 1.6 0.9 0.3 0.0 n.o. 0.7 1.2 0.0 1.3 0.6 0.0 n.o. 0.0 0.2 0.2 0.6 0.2 n.o. 0.7 0.2 0.0 0.0 n.o.

CH TOT

15.2 27.2 10.4 20.2 ab 14.7 7.7 2.7 5.3 n.o. 6.0 6.7 4.1 5.8 11.6 6.0 n.o. 14.9 11.3 5.1 2.0 9.5 ab 2.8 1.8 3.0 5.7 p

Palm

11.4 0.9 0.2 1.7 p 6.7 0.2 0.0 14.0 p 0.9 0.2 0.3 1.0 0.2 3.7 n.o. 0.0 0.2 1.5 0.2 p p 0.6 0.3 0.0 1.2 p

GSSC (%)

FI TOT (%) Other FI

Table 3 Assemblage data for Cenozoic biosilica assemblages from Greece, Turkey, and Irana

POOID-D 6.5 7.6 22.5 13.5 ma 10.8 13.7 20.2 15.9 p 16.2 21.6 19.7 18.2 11.0 10.4 p 14.0 18.7 14.6 9.7 10.8 mab 9.1 19.4 13.3 8.3 mab

POOID-ND 9.0 13.8 10.8 2.2 ab 5.6 11.9 27.3 30.4 p 16.0 7.2 25.2 18.8 16.9 29.5 p 14.5 15.6 23.8 25.4 33.6 ab 27.3 33.9 23.5 24.8 ab

Panicoideae 2.3 0.6 2.0 1.5 p 0.9 0.9 0.9 1.4 n.o. 0.2 0.0 0.7 0.6 0.7 0.7 n.o. 0.6 0.1 0.2 0.1 0.0 n.o. 0.5 0.2 0.6 0.0 n.o.

Chloridoideae 0.0 0.5 0.2 0.0 p 0.0 0.0 0.3 0.0 n.o. 0.0 0.0 0.0 0.7 0.5 0.0 n.o. 0.3 1.9 0.0 0.4 0.0 n.o. 0.2 0.0 0.2 0.6 n.o.

PACCAD general 0.0 2.8 0.2 0.6 mab 7.4 8.4 2.4 3.9 n.o. 5.6 1.3 3.1 2.0 3.7 3.0 n.o. 5.9 0.6 8.1 3.1 3.2 p 16.8 6.6 5.1 9.2 mab

OTHG 3.2 1.0 8.4 3.5 p 1.6 6.4 8.3 10.6 n.o. 5.3 0.6 5.9 2.1 2.0 6.7 n.o. 0.8 1.0 0.4 3.2 0.6 p 1.2 0.9 1.0 4.9 p

Pooideae – POO-1, POO-2 POO-1, POO-2 POO-1, POO-2 POO-1 POO-1, POO-2 POO-1 POO-1, POO-2 POO-1, POO-2 POO-1 POO-1, POO-2 POO-1, POO-2 POO-1, POO-2 POO-1, POO 2 POO-1, POO-2 POO-1 POO-1 POO-1, POO-2 POO-1 POO-1, POO-2 POO-1, POO-2 POO-1 POO-1 POO-1 POO-1, POO-2 POO-1 POO-1, POO-2 POO-1

(continued on next page)

BB-1 BB-1 BB-1 – BB-1 BB-2, BB-3 – – – – BB-3 BB-2, BB-3 – BB-3 BB-2 – – – – B B-2 – – – – – – –

Closed-habitat grasses

Highly diagnostic GSSC (presence)d

C.A.E. Strömberg et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 250 (2007) 18–49 29

– – – – – – –

(CHL-1) CHL-1 CHL-1 – – – – – – CHL-1 –

EM11 EM12 EM13⁎⁎ EM14 EM15 EM16⁎⁎ EM17⁎

EM18 EM19 EM20 EM21⁎⁎ EM22 EM23⁎ EM24 EM25⁎⁎ EM26 EM27 EM28⁎

PAC-2 PAC-2

PAC-3 PAC-3

PAC-2, PAC-3

13.4 13.7 10.4 6.8 7.4 vab 9.7 5.9 8.7 6.0 vab

17.8 25.0 5.5 15.0 6.8 8.7 n.o.

15.0 7.1 2.9 n.o.

8.2 11.3 10.8 14.0 vab 16.2

NDG (%)

35.5 35.6 35.6 48.5 34.5 vab 31.1 30.8 44.0 39.2 vab

31.3 35.3 35.5 33.9 45.4 30.5 n.o.

34.7 30.0 15.0 n.o.

23.6 33.5 31.1 41.4 vab 34.4

NDO (%)

516 547 393 501 475 n/a 351 393 504 418 n/a

432 556 290 499 646 298 n/a

548 337 207 n/a

501 654 502 712 n/a 655

Total # phytoliths counted

29.2 23.2 12.3 4.9 16.4 n/a 5.8 3.2 6.4 12.7 n/a

13.6 17.7 7.6 13.5 25.0 16.2 n/a

15.7 4.3 23.7 n/a

39.0 51.3 18.7 49.2 n/a 43.3

FI TOT/ (FI TOT + GSSC) (%)

FI-t ratio

5.4 5.2 4.3 2.8 4.3 n/a 3.0 2.2 3.1 4.3 n/a

4.7 5.1 4.1 4.0 4.8 5.3 n/a

4.3 2.6 6.1 n/a

5.1 5.4 4.4 5.6 n/a 5.3

95% confidence interval (±%)

1.1 0.5 0.5 4.2 0.0 38.2 0.5 0.0 0.0 0.5 n/a

10.5 35.0 0.6 1.8 2.2 1.3 n/a

2.2 0.0 0.8 n/a

1.9 4.0 0.0 4.3 24.2 3.3

Bulliform cells/GSSC

p p mab p p n.o. ab p p vab n.o.

p mab ab p vab n.o. n.o.

p p p n.o.

p vab vab vab ab mab

Diatoms

Other biosilicae

p n.o. p n.o. p n.o. p p p n.o. mab

p n.o. vab p vab n.o. n.o.

n.o. p n.o. n.o.

n.o. mab vab mab vab mab

Chrysophyte cysts

n.o. n.o. p p n.o. p p n.o. n.o. n.o. p

p n.o. vab n.o. n.o. n.o. n.o.

n.o. n.o. p n.o.

n.o. vab vab vab vab p

Sponge spicules

OH OH OH? OH-grass present OH (CG) OH (CG) OH? OH (CG) OH (CG) OH? OH-grass present OH OH OH OH (CG) OH OH? OH OH OH OH OH?

CF-OF w CG CF-OH (CG) OH (CG) CF-OH OH? (CG) OH (CG)

Vegetation inferencef

b

For explanation of morphotype classes, see text and Table 2; for explanation of statistical procedures, see text. Samples: *assemblages not included in quantitative analysis because of insufficient preservation (n.o. = not observed; p = present; mab = moderately abundant; ab = abundant; vab = very abundant); **assemblages in which counts are likely biased because of poor preservation. c G = good-pristine (occluded organic material and fine ornamentation routinely preserved on GSSC; elongates and bulliform cells may be etched or broken); P = poor (occluded material often missing and GSSC commonly broken or etched; elongates and bulliform cells often etched or broken); VP = very poor (phytoliths fragmentary or structurally/texturally altered to such a degree that identification is complicated); alt = altered; et = etched. d BB-1 = “Chusquoid body”/cross with irregular/faceted top (bambusoid? grass); BB-2=Chusquea-type rondel, Chusquea-type rondel bilobate (bambusoids); BB-3 = collapsed saddle (BE grasses, certain basal grasses); POO-1 = crenate (pooids); POO-2 = ornamented Stipa-type bilobate (stipoid pooids); CHL-1 = true saddle or assemblage of saddle-like GSSC morphotypes; PAC-1 = near-panicoid bilobate; PAC-2 = Merxmuellera-type rondel; PAC-3 = inverted bilobate; PAC-4 = polylobate (except Stipa-type polylobate). Parentheses around GSSC morphotypes signify a single specimen of the morphotype in the sample. e Semi-quantitative assessment of abundances of diatoms, chrysophyte cysts, and sponge spicules: n.o. = not observed; p = present; mab = moderately abundant; ab = abundant; vab = very abundant. f Vegetation inference, including interpretation of grass community composition using information from statistical comparisons with the modern reference collection (in Tables 4 and 5) and the presence of specific GSSC morphotypes: CF = closed forest; OF = open forest; w CG = understory of closed-habitat grasses; OH = open, grass-dominated habitat; CF-OH = open forest-woodland; (CG) = low frequencies of closed-habitat grasses present).

a

PAC-1, PAC-3 PAC-1, PAC-3, PAC-4 PAC-2 – – PAC-3 –

– (CHL-1) – –

EM7 EM8 EM9⁎⁎ EM10⁎

PAC-2, PAC-3

– PAC-1 – – PAC-2 PAC-1, PAC-2, PAC-3, PAC-4 PAC-2, PAC-3 PAC-3 PAC-3 –

– (CHL-1) – – – –

EM1 EM2 EM3 EM4 EM5⁎ EM6

PAC-1, – PAC-1, PAC-2 PAC-2 PAC-2, PAC-2, PAC-2 PAC-2 PAC-1, PAC-1,

Other C3/C4 PACCAD

Highly diagnostic GSSC (presence)d

Chloridoideae

Sample numberb

Table 3 (continued )

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Fig. 2. Selected non-grass phytolith morphotypes used in vegetation analysis herein (Table 2). Scale bar 10 μm. (a) Magnolia-type sclereid/tracheid (diagnostic of dicotyledons, Other FI), Kemiklitepe B (EM25). (b) Silicified stellate facetate parenchyma (aquatic monocotyledon(?), AQ), Lower Maragheh (EM19). (c) Equidimensional irregular or facetate body (“blocky polyhedron”; Other FI), Akkaşdağı (EM26). (d) Sulcate vascular cell (silicified tracheary element; Other FI), Orta (EM2). (e) Epidermal plate with cone-shapes (Cyperaceae, AQ), Lower Maragheh (EM19). (f) Cystolith (dicotyledons, Other FI), Lower Maragheh (EM19). (g) Polyhedral epidermis with surface ornamentation (dicotyledons, Other FI), Mordoğan-Ardıç (EM6). (h) Globular echinate (Palm), Susuzköy (EM1). (i) Globular laminar vesicular infilling (Other FI), Lower Maragheh (EM19). (j). Globular granulate (Other FI), Mordoğan-Ardıç (EM6).

compound variable encompasses hitherto undescribed closed-habitat morphotypes. Also, the sample from Otatea culm, which only contains GSSC morphotypes that are not typical of closed-habitat grasses (Strömberg, 2003), was not considered for the calculations of background universes. Importantly, the background universe ratios are based on a limited data set; this analysis is therefore a first attempt at quantifying the relative contribution of closed and open-habitat grasses.

In addition to the various ratios, we also documented the presence of GSSC morphotypes considered particularly diagnostic for, respectively, closed-habitat, pooid, chloridoid, and PACCAD grasses in general (Table 3) (Piperno, 1988; Fredlund and Tieszen, 1994; Piperno and Pearsall, 1998; Strömberg, 2003, 2005, C. Strömberg, unpublished data). This detailed information was used to detect low abundances of open-habitat grasses, even in cases where the bootstrap tests failed to reject null hypotheses 1–3

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Fig. 3. Selected fossil GSSC morphotypes used herein (Table 2). Scale bar 10 μm. (a, b) Chusquoid body with irregular/spiked top (morphotype BB-1 in Table 3; class CH TOT in Table 2), Susuzköy (EM1). (c-d, f, i) Various crenate GSSCs (POO-1; POOID-D). (c, f) Kemiklitepe B (EM25). (d, i) Mordoğan-Ardıç (EM6). (e) Merxmuellera-type rondel (PAC-2; PACCAD general), Kemiklitepe B (EM25). g. Stipa-type bilobate (POO-2; POOID-D), Lower Maragheh (EM19). (h) Inverted bilobate (PAC-3; PACCAD general), Mordoğan-Ardıç (EM6). (j) Saddle (CHL-1; Chloridoideae), Lower Maragheh (EM19).

(Table 4). In Fig. 4, grass groups are only marked when they were judged to have been clearly present. 3. Results 3.1. Biosilica yield and preservation The extraction process resulted in 28 biosilica assemblages considered sufficiently informative for closer study (EM1–EM28 in Tables 1 and 3 and Figs. 2–4). In addition to phytoliths from vascular plants, the assemblages were often made up of diatoms, sponge spicules, chrysophyte cysts, and (rarely) heliozoans, as well as volcanic ash and other non-biogenic silica particles with a specific gravity b 2.3 (Table 3). The productive samples represent a variety of sediment types, ranging from laminated diatomaceous shale to sandy siltstone, and

including tuff and coal. Several depositional environments such as lacustrine, fluvial, and overbank paleosol are also represented (Table 1). Using the classification outlined above, the preservational status of the Cenozoic assemblages from Greece, Turkey, and Iran was shown to be highly variable, ranging from pristine, with intact occluded organic material and detailed ornamentation, to extremely poor, either heavily etched or severely structurally altered (Table 3). Whereas absolute yield was not estimated, it can be noted that well-preserved assemblages were often also abundant. 3.2. Middle Eocene assemblage (EM1: Susuzköy) The assemblage consists of a mixture of forest indicator phytoliths (FI TOT) and GSSCs, which are in dominance

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Table 4 Hypotheses that are tested regarding GSSC assemblage composition in Cenozoic samples from Greece, Turkey, and Iran Fossil GSSC assemblages

Hypothesis

Null hypothesis

No.

Description

GSSC assemblages 1 with high % of CH TOT 2

3

GSSC assemblages 4 with high % of OH TOT 5

Description

Assemblage contains openhabitat grasses Assemblage contains pooid grasses Assemblage contains PACCAD grasses Assemblage contains closedhabitat grasses

Assemblage contains no openhabitat grasses Assemblage contains no pooid grasses Assemblage contains no PACCAD grasses Assemblage contains no closed-habitat grasses Assemblage Assemblage contains no contains PACCAD grasses PACCAD grasses

Test metrica

Modern grass samples used for bootstrap test

(OH TOT)/ (CH TOT)

Closed-habitat (excluding Otatea “woody” culm) (POOID-D)/ Closed-habitat (CH TOT) (excluding Otatea “woody” culm) (PACCAD TOT)/ Closed-habitat (CH TOT) (excluding Otatea “woody” culm) (CH TOT)/ Open-habitat (OH TOT) (pooid, PACCAD)

Organb Urn (max ratio of test metric in modern samples)c

Modern sample used for urn

LE RE

0.954 1.083

Otatea LE Pharus RE

LE RE

0.039 0.583

Chusquea LE Pharus RE

LE RE

0.749 Otatea LE n/a (bratio n/a in LE) 0.008 Sporobulus LE 0.010 Calamagrostis RE 0.095 Festuca LE 0.104 Nassella RE

LE RE

(PACCAD TOT)/ Pooid grasses (POOID TOT)

LE RE

a

CH TOT = closed-habitat GSSC morphotypes; OH TOT = POOID-D + POOID-ND + PACCAD GSSC morphotypes; POOID TOT = POOID-D + POOID-ND GSSC morphotypes. b LE = leaf; RE = reproductive material. c The various urns, or background universes, against which the fossil assemblages were statistically compared, are based on the ratios of relevant GSSC morphotype classes in a reference collection of phytoliths from modern grasses (Strömberg, 2003, C. Strömberg, unpublished data). The maximum ratio in modern samples is used in each case, both for leaf and reproductive material (which tend to differ). Note that this represents a very conservative approach.

(FI-t ratio = 39 ± 5%). The FI TOT phytoliths include morphotypes from woody/herbaceous dicotyledons, including “terminal tracheid” morphotypes commonly produced by various woody dicotyledons (e.g., Magnolia, Postek, 1981) and relatively abundant palm phytoliths (11% of the total assemblage; 17% of the morphotypes used in vegetation analysis). The GSSC assemblage contains a large component (49%) of a morphological spectrum of GSSCs with no direct modern counterpart. These morphotypes, herein referred to as BB-1 (see Table 3), are characterized by a bilobate to cross-shaped base that is reminiscent of the so-called chusquoid bodies of Piperno and Pearsall (1998). Chusquoid bodies have been shown to have a fairly wide distribution primarily among bambusoid and basal grasses (Piperno and Pearsall, 1998; Strömberg, 2003; Prasad et al., 2005). Furthermore, the fossil morphotypes (BB-1) are very tall with elaborate and irregular ornamentation and faceting of the “top” [sensu Mulholland, 1989, but usually facing the interior of the leaf (Parry and Smithson, 1964)] aspect – “spiked” in side view – similar to rondels and bilobates found in, for example, Chusquea (Piperno and Pearsall, 1998; Strömberg, 2003). Although we have not been able to locate identical morphotypes in modern grasses, the combination of

features suggests that the morphotypes were produced by grasses with affinity to either basal grasses or grasses in the BE (Bambusoideae+ Ehrhartoideae) clade. Bootstrap analysis suggests that the whole GSSC assemblage can be explained by phytolith production by closed-habitat grasses, although the frequency of pooid morphotypes is slightly elevated (Table 5). Further, the assemblage does not contain any highly diagnostic pooid or PACCAD morphotypes that could support the presence of open-habitat grasses (Table 3). 3.3. Early Miocene assemblages (EM2–EM5) The assemblages from Orta and Keseköy 1–2 B contain FI TOT phytoliths and GSSCs in roughly equal amounts (Table 3), whereas Keseköy 1–2 A is dominated by GSSCs (FI-t ratio = 19 ± 4%). In all three samples, FI TOT phytoliths comprise a wide diversity of forms typical of woody/herbaceous dicotyledons. It should be noted that the Orta assemblage contains relatively high frequencies of dicotyledonous phytolith types that are seldom preserved in fossil assemblages, such as fragile mesophyll fragments and weakly silicified tracheary elements; if these are excluded, the

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Fig. 4. The record of vegetation changes in Turkey and surrounding areas based on phytolith assemblages (represented as pie charts) shows that relatively open habitats dominated by open-habitat grasses spread by the Early Miocene. Pie charts in lighter shades signify assemblages for which counts are likely to be biased because of poor preservation; grass symbols represent assemblages that were not included in the quantitative analysis because of insufficient preservation. Percentages in pie charts from Table 3 (Palm, Other FI, CH TOT, POOID-D+ POOID-ND, Chloridoid, Panicoid+ PACCAD general, OTHG), but see text for explanation of interpretation of grass community composition.

FI-t ratio would be somewhat lower in this assemblage. Palm phytoliths are relatively rare (b 4% of the morphotypes used in vegetation analysis). The GSSC assemblages are dominated by a range of pooid morphotypes (diagnostic + non-diagnostic), including several distinct crenate morphotypes and Stipa-type bilobates. In addition, some samples have low frequencies of closed-habitat grass morphotypes (e.g., BB-1), and bootstrap analysis supports the occurrence of closed-habitat grasses in the vegetation (Table 5). Bootstrap analysis and identification of highly diagnostic PACCAD morphotypes also point to the presence of PACCAD grasses in the oldest sample (Orta). The assemblage from Hancılı 1 is very poorly preserved, but appears to be similar to Orta and Keseköy 1–2 B in composition. The Early Miocene assemblages preserve sedge phytoliths (except Keseköy 1–2 B) and

abundant diatoms, sponge spicules, and chrysophyte cysts, consistent with habitats close to water. 3.4. Middle–Late Miocene assemblages (EM6–EM28) The Middle–Late Miocene assemblages studied herein are similar to the Early Miocene in their basic composition, showing high frequencies of primarily open-habitat pooid morphotypes mixed with FI TOT phytoliths. With the exception of the sample from Mordoğan–Ardıç, all assemblages are clearly grass dominated (FI-t ratio bb50%; Table 3), although there is great variation in the abundances of FI TOT morphotypes relative to GSSCs (3–29%). Non-palm FI types show a similar morphological range as in Early Miocene samples, although the dataset is currently too small to evaluate this statement statistically. The abundances of

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Table 5 Hypothesis testing concerning the composition of fossil GSSC assemblages in Cenozoic samples from Greece, Turkey, and Irana A. GSSC assemblages with high frequencies of closed-habitat GSSC morphotypes Sample Sample number nameb

Hypothesis 1: Assemblage contains open-habitat grasses

Hypothesis 2: Assemblage contains pooid grasses

Hypothesis 3: Assemblage contains PACCAD grasses

Rejection Max 95% Fossil Rejection Max 95% Max 95% Fossil Rejection Max 95% Max 95% Fossil expected expected GSSC of H0 expected GSSC of H0 expected expected GSSC of H0 (LE) (RE) assemblage (LE, RE) assemblage (LE) (RE) assemblage EM1

Suzusköy 1.211

1.377

0.867

NR

0.072

0.780

0.319

R/NR

1.027

0.111

NR

B. GSSC assemblages with high frequencies of open-habitat GSSC morphotypes Sample number

EM2 EM3 EM4 EM6 EM7 EM8 EM9 EM11 EM12 EM13

EM14 EM15 EM16 EM18 EM19 EM20 EM21 EM22 EM24 EM25 EM26 EM27

Sample nameb

Orta Keseköy 1–2 A Keseköy 1–2 B Mordoğan–Ardıç İnönü 1 (24, 24A) Gebeciler Yassıören, Lower Sinap⁎⁎ Sinaptepe NE (T5–95) İnönü 2 Kütahya– Çavdarhisar road separation 300 m⁎⁎ Delikayıncak (A13) Delikayıncak (A23) Kayıncak A (Sinap 12)⁎⁎ Kayadibi Lower Maragheh Gülpınar Kavakdere⁎⁎ Kemiklitepe D Samos Q4 Kemiklitepe B⁎⁎ Akkaşdağı Samos Q5

Hypothesis 4: Assemblage contains closed-habitat grasses

Hypothesis 5: Assemblage contains PACCAD grasses

Max 95% expected (LE)

Max 95% expected (RE)

Fossil GSSC assemblage

Rejection of H0

Max 95% expected (LE)

Max 95% expected (RE)

Fossil GSSC assemblage

Rejection of H0

0.020 0.022 0.030 0.025 0.021 0.024 0.029

0.025 0.022 0.030 0.025 0.026 0.030 0.029

0.020 0.050 0.071 0.063 0.026 0.006 0.000

NR R R R R NR NR

0.143 0.147 0.165 0.152 0.151 0.147 0.163

0.163 0.155 0.176 0.162 0.158 0.154 0.189

0.183 0.072 0.134 0.508 0.364 0.075 0.115

R NR NR R R NR NR

0.025

0.025

0.018

NR

0.155

0.163

0.180

R

0.024 0.022

0.024 0.029

0.038 0.000

R NR

0.142 0.156

0.155 0.165

0.045 0.085

NR NR

0.021 0.021 0.024

0.024 0.021 0.032

0.032 0.018 0.000

R NR NR

0.140 0.141 0.161

0.149 0.150 0.171

0.088 0.174 0.092

NR R NR

0.023 0.020 0.023 0.019 0.021 0.022 0.019 0.023 0.024

0.023 0.024 0.028 0.023 0.026 0.026 0.023 0.023 0.024

0.000 0.007 0.005 0.015 0.004 0.013 0.004 0.000 0.000

NR NR NR NR NR NR NR NR NR

0.144 0.137 0.144 0.133 0.145 0.144 0.143 0.140 0.141

0.150 0.151 0.153 0.153 0.150 0.155 0.148 0.150 0.153

0.240 0.076 0.218 0.105 0.072 0.481 0.129 0.159 0.294

R NR R NR NR R NR R R

a

Rejection of H0: R = H0 rejected using both leaf and reproductive material urns (when used); NR = H0 not rejected using both leaf and reproductive material urns; R/NR = H0 rejected using leaf material urn, but not using reproductive material urn. For further explanation, see text. b Samples (samples marked with ⁎ in Table 3 excluded): ⁎⁎assemblages in which counts are likely biased because of poor preservation.

palm phytoliths is, with few exceptions, low, often constituting ≤ 2% of morphotypes included in the vegetation analysis. Pooid GSSC diversity is comparable to that in Early Miocene samples. Closed-habitat GSSCs are found in limited numbers and bootstrap analysis shows that low abundances of closed-habitat grasses are necessary to

explain GSSC assemblage composition only in a few Middle–Early Miocene samples. The presence of a number of GSSC morphotypes that are highly diagnostic of PACCAD grasses, as well as bootstrapping tests, indicate the presence of PACCAD grasses in a majority of the assemblages. In several cases, typical PACCAD forms reach high relative abundances (up to 31% of

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GSSCs; Table 3). The PACCAD morphotypes recorded in these assemblages correspond to forms that are found in both C3 and C4 PACCAD taxa (Table 2). In the easternmost Late Miocene Lower Maragheh assemblage, a low frequency of saddle morphotypes supports the presence of potentially C4 chloridoid grasses. Many of the Middle to Late Miocene assemblages have low abundances of phytoliths indicative of wetland plants, including sedge phytoliths. The content of biosilica from diatoms, sponge spicules, and chrysophyte cysts is also low in most assemblages, suggesting habitats distal to water. Exceptions are Delikayıncak (A23), Kütahya–Çavdarhisar road separation 300 m, Samos Q4, and Samos Q5. The sedimentology at the latter three localities also indicates lacustrine or proximal fluvial (or deltaic) settings (Table 3). Elongate facetate phytoliths and other potential conifer types are present in many of the Early–Late Miocene assemblages (data not shown); however, because of their low abundances, it is not possible with certainty to assign them to conifers (as opposed to grasses). Bulliform cells are present in small numbers in most assemblages; however, in Hancılı 1, T5-95, İnönü 2, and Asarıntepe, these morphotypes are extremely abundant (Table 3). The implied occurrence of closedhabitat grasses and/or the high abundances of diatoms and sponge spicules at these sites may reflect a signal of local wetland habitats.

imply a near-shore location for Susuzköy. However, the sedimentology and the very low abundance of diatoms and other siliceous microfossil freshwater indicators suggest that the phytolith assemblage derives from a more well-drained part of a floodplain (Table 3). Our phytolith data are consistent with previous vegetation and climate inferences for Middle Eocene western Eurasian ecosystems, which are based mainly on the rich record of pollen and spores in Turkish coal deposits (for review, see Akgün et al., 2002). In contrast, reports of Eocene macrofossil floras and mammalian faunas from the areas south and southeast of today's Black Sea are rare (Palamarev, 1987; Mai, 1987, 1995; Kappelman et al., 1996a; Maas et al., 2001; Collinson and Hooker, 2003). Palynological evidence indicates that a range of angiosperm taxa that today are limited to tropical or subtropical areas, including palms and mangroves, existed on the Anatolian landmasses during the Eocene (Norris, 1986; Akgün et al., 2002). The vegetation has been interpreted as dense, tropical lowland and swamp forest growing in tidal swamps in a deltaic setting (Akgün et al., 2002). Climate reconstructions based on lithological (and fossil) indicators (Scotese, 2002) similarly show a paratropical climate for the eastern Mediterranean during the Eocene. Phytolith data add to our knowledge of Middle Eocene Eurasian ecosystems by demonstrating the presence and ecological importance of (closedhabitat) grasses.

4. Discussion

4.2. Miocene vegetation

4.1. Eocene vegetation

Until phytolith data from modern analog vegetation types in the eastern Mediterranean have been collected, the Middle Eocene Susuzköy serves as a baseline comparison for the Miocene samples. In contrast to Susuzköy, all Miocene phytolith assemblages investigated here point to relatively open vegetation, such as savanna or open woodland (using the modern definition of these vegetation types with no reference to climate, sensu Dansereau, 1957; see also Scholes and Archer, 1997) dominated by open-habitat grasses, or a mixture of grassland and wooded areas (Fig. 4). The non-grass component of the Miocene floras consisted primarily of dicotyledons and rare palms, as indicated by phytoliths. Palms were present in low but variable abundance throughout the Miocene, showing no clear trend through time in this limited dataset. The Miocene grass communities were dominated by diverse (species rich) C3 pooid grasses. Several types of C3 or C4 PACCAD grasses were also moderately common at some localities, whereas closed-habitat grasses were represented only in very low frequencies at certain sites. The

We assume that the BB-1 GSSC morphotypes found in abundance in the Susuzköy sample can be referred to basal grasses or the BE-clade. This interpretation is supported by impression fossils of bamboo-like culms found at the Susuzköy site (G. Saraç, unpublished field notes), suggesting the presence of closed-habitat grasses of some stature. Accordingly, we interpret this Middle Eocene assemblage as reflecting a primarily dicotyledonous forest with palms and abundant, closed-habitat grasses with woody culms (Fig. 4). There may also have been a low abundance of open-habitat pooid grasses in the understory or in vegetation gaps. We speculate that this habitat was fairly closed, in the same sense that bamboo-dominated vegetation is characterized as forest (e.g., Edwards, 1940; Yamamoto et al., 1995; Jacinto Tabanez and Viana, 2000; Banana and Tweheyo, 2001). Paleogeographical reconstructions of central Anatolia as consisting of a series of island arcs (see above) (Scotese, 1997; Rögl, 1999; Maas et al., 2001; Popov et al., 2004)

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strongest evidence for C4 grasses is in the form of low abundances of chloridoid GSSC phytoliths at the easternmost Late Miocene locality Maragheh (Fig. 4). This predominantly C3 savanna, open woodland, or grassland–forest mosaic vegetation appears to have spread in Anatolia before or during the Early Miocene, and by at least the Late Miocene (∼9 Ma; Fig. 4) it was represented from Samos in the west to Maragheh in the east. Variation in sedimentology and in the abundance of diatoms and other siliceous microfossils suggest that this general vegetation type was not restricted to certain microhabitats, but characteristic for entire ecosystems. This interpretation is valid even when poorly preserved assemblages are excluded (Fig. 4). The faunal record of the Greco-Iranian region is fairly complete for the Neogene, in particular for the Middle Miocene onward (Fortelius, 2006). Consistent with phytolith data, it points to the presence of open habitats in Turkey and surrounding areas during the Middle to Late Miocene. This interpretation is based on analysis of data on faunal abundance and ungulate functional morphology (e.g., cheek tooth crown height, masticatory morphology, locomotory morphology) from several faunal localities studied herein [Mordoğan–Ardıç, Kaya et al., 2003; İnönü 1 (24, 24A), Geraads et al., 2005; Kemiklitepe D, Kemiklitepe AB, Bonis et al., 1994; Maragheh, Campbell et al., 1980; Gülpinar, Kaya, 1982; Akkaşdağı, Kazanci et al., 1999; Scott and Maga, 2005; Asarıntepe, Saraç et al., 2002; Samos, Solounias and Dawson-Saunders, 1988; Solounias and Moelleken, 1993; Solounias et al., 1995] as well as other contemporaneous faunas (see Bernor, 1984; Andrews, 1990; Janis, 1993; Bernor et al., 1996a; Fortelius et al., 1996, 2002, 2003; Geraads et al., 2003). However, phytolith analysis shows that these open habitats were also grass-dominated, with a diverse C3 pooid understory, rather than the grass-free – or nearly so – woodlands or open forests hypothesized by Solounias et al. (1999). The presence of savanna, woodland, or grassland–forest mosaic vegetation is corroborated by tooth wear studies of ungulates from various parts of the Greco-Irano-Afghan region (Greece, including Samos, and Maragheh, Hayek et al., 1992; Solounias and Moelleken, 1992; Solounias and Hayek, 1993; Merceron et al., 2005a,b; Afghanistan, Merceron et al., 2004). These faunas appear to comprise a range of feeding ecologies, from grazers to mixed feeders and browsers, suggesting habitats characterized by a mixture of grasses and trees (Hayek et al., 1992; Solounias and Moelleken, 1992; Solounias and Hayek, 1993). Stable isotope data from Miocene to Pliocene paleosols spanning the Greco-Iranian region (Quade et al., 1994; Cerling et al., 1997) agree with our reconstruction of mainly C3 pooid grass communities in Turkey and

37

surrounding areas until at least ∼6 Ma. In addition, δ13C values of tooth enamel from Late Miocene ungulates [from e.g., Kemiklitepe (Bocherens et al., 1994), Samos (Quade et al., 1994)] have shown that, with the possible exception of the giraffid Samotherium at Samos, eastern Mediterranean ungulates fed exclusively on C3 plants during most of the Late Miocene (see also Quade et al., 1995; Bocherens and Sen, 1998; Zazzo et al., 2002). Paleobotanical research has previously failed to demonstrate a substantial grass cover in Early Miocene ecosystems of the eastern Mediterranean (see earlier discussion and Solounias et al., 1999), although palynological evidence for an increasing importance of grasses and other herbs in the Turolian is starting to be uncovered (Ioakim et al., 2005). However, palynofloras and macrofossil floras have provided information about the woody component of these ecosystems, suggesting increasingly arid-adapted dicotyledonous angiosperms in southern and south-eastern Europe and Asia Minor by the Late Miocene (Traverse, 1982; Ioakim and Solounias, 1985; Palamarev, 1987; Kovar-Eder and Kvaček, 2003; Ioakim et al., 2005; Kovar-Eder et al., 2006; but see also Gregor, 1990; Velitzelos and Gregor, 1990 Akgün et al., 2000, 2002). 4.3. Variation in tree cover through the Miocene Habitats in Anatolia appear to have been fairly open from the Early Miocene (∼20 Ma) onward, but the phytolith analysis indicates marked variation in the degree of tree cover (Fig. 4). To better appreciate the temporal variation in habitat openness, we plotted the FI-t ratio against time as a crude proxy for changes in the relationship between trees and the understory grasses. This temporal comparison indicates that there was a general decrease in tree cover throughout the Miocene (Fig. 5a), consistent with environmental and climatic reconstructions based on faunal information (e.g., Bernor, 1984; Nagatoshi, 1987). We investigated the statistical significance of this apparent time series trend through regression analysis, after tests conducted using the statistical software PAST version 1.6 (Hammer et al., 2001) and 95% confidence intervals showed that autocorrelation was not significant for any lag. The regression analysis yielded a significant negative relationship between FI-t and time (FI-t = 2.27× time − 6.78; r = 0.707; p b 0.001). However, within each time zone there is high variability in FI-t ratio suggesting a more complex scenario. On the one hand, this variation may be due to vegetation heterogeneity across the landscape, which became less pronounced as habitats became increasingly open. On the other hand, the disparities in FI-t ratio among

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Fig. 5. Forest indicator abundance [FI-t ratio = FI TOT / (FI TOT + GSSC)] as a rough measure of habitat openness through time suggests that habitats generally became more open in Turkey and surrounding areas during the Miocene. Five of the assemblages (Hancılı 1, Eşme–Akçaköy, Selçik, Asarıntepe, and Çobanpinar) were excluded due to poor preservation. The ages of the samples are in most cases approximate and were estimated as follows: (1) for samples with age data based on magnetostratigraphy or radiometric dating as well as biochronology of the associated fauna (MN zones), and for which these ages roughly agree, the mid-point of the paleomagnetic or radiometric age estimate was used; (2) for samples for which these dating methods are incongruent, the emphasis was placed on biochronology; (3) in cases where paleomagnetic or radiometric data are missing, the mid-point of MN zones was used, potentially modified if a closer age estimate (e.g., “lowermost MN9”) is indicated in the literature (Table 1). (a) Assemblages from coastal sites contrasted with assemblages from inland sites. Based on paleogeographic reconstructions (Scotese, 1997; Rögl, 1999), sites that are currently located close to the Mediterranean Sea were assumed to have been located fairly close to the sea (East Mediterranean Basin) during the Miocene as well. (b) Assemblages from sites assumed to have been situated close to open water or in wetlands, coastal and inland sites combined. (c) Assemblages from more upland sites (all from inland sites). Interpretation of proximity to water is based mainly on abundance of diatoms, sponge spicules, and chrysophyte cysts, as well as sedimentology (Table 3). For further explanation, see text.

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roughly contemporaneous samples – and indeed the trend towards more open habitats as a whole – may simply be an artefact of the diverse array of samples included in the study. The variation could, for example, reflect differences in climate across the eastern Mediterranean. Presently, coastal Turkey receives considerably more annual precipitation than central Anatolia, which exerts strong influence over the natural vegetation in these regions (Akman and Ketenoğlu, 1986; Leemans and Cramer, 1991). As outlined above, today's coastal Anatolia similarly bordered shallow shelf areas during long periods of the Miocene, whereas central Anatolia was continental (Rögl, 1999; Vasiliev et al., 2004; Popov et al., 2004, 2006). A climatic difference between the western, near-shore parts of the eastern Mediterranean and more inland areas is also suggested by a variety of paleoclimate proxies during parts of the Miocene (e.g., Zazzo et al., 2002; Merceron et al., 2004, 2005a,b; Geraads et al., 2005, see below for discussion). To examine the effect of proximity to the ocean, we divided the Miocene localities into what were likely coastal and continental sites, respectively, and contrasted the FI-t ratios of these groups (Fig. 5a). The comparison shows that, during the later Late Miocene (after 9 Ma), seaward sites are no more forested than sites further inland [a permutation t-test with 1000 permutations in PAST (Hammer et al., 2001) is not significant; p N 0.1]. By contrast, in the early Middle Miocene (∼16–15 Ma) the phytolith assemblage from the coastal Mordoğan– Ardıç site indicates considerably more closed vegetation than an assemblage from the roughly coeval, eastern site İnönü 1 (24, 24A) (Fig. 4). The relatively high abundance of palm phytoliths as well as several unique forest indicator phytolith types in the Mordoğan–Ardıç assemblage (Strömberg et al., in prep.) also point to somewhat different ecological conditions in coastal habitats. If inland phytolith assemblages are studied separately, the pattern of decreasing tree cover is still significant, but relies heavily on the lacustrine assemblages from Keseköy and Orta (FIt = 3.1324 × time− 17.451; r = 0.663, p b 0.005, no autocorrelation). Hence, another possibility is that the fluctuations in FI-t ratio throughout the Miocene could relate to facies variation. Because phytoliths are commonly deposited through in situ plant decomposition, plant silica assemblages tend to reflect more local vegetation patterns than, for example, pollen and spores (for review, see Piperno, 1988, 2006). Studies of modern and submodern ecosystems have amply demonstrated the ability of phytolith assemblages to reconstruct forest– grassland transitions over distances b 1 km and to distinguish riparian forest in a savanna landscape

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(Alexandre et al., 1997, 1999; Barboni et al., 1999; Bremond et al., 2005a). The spatial resolution of phytolith assemblages is highest in closed habitats, where lateral transport and mixing due to eolian transport, herbivore migration, and fires play a lesser role; in savanna grasslands, phytolith deposition tends to be extra-local to regional (Piperno, 1988, 2006; Fredlund and Tieszen, 1994; Alexandre et al., 1997). We studied the correlation between FI-t ratio and microhabitat type to examine whether the differences in openness observed in the Miocene samples may simply be a function of spatial heterogeneity in vegetation due to hydrological conditions (proximity to water). Proximity to water was reconstructed using mainly semi-quantitative estimates of relative abundance of diatoms, sponge spicules and chrysophyte cysts associated with each phytolith assemblage (Table 3). Sedimentological data were also considered. However, because the available facies information was often too imprecise (“floodplain”) to allow detailed reconstruction of microhabitat (e.g., streamside vs. distal floodplain), less emphasis was placed on this information. The survey showed that the coastal assemblages all display moderate to high relative abundances of diatoms and other siliceous microfossils, whereas inland assemblages are more variable (note that some of the excluded assemblages have high frequencies of diatoms etc.; Table 3). The coastal assemblages and the inland assemblages with high diatom abundances are too few for meaningful analysis if studied separately. Taken together – disregarding for a moment the potential of mixing assemblages from different climates – these samples tentatively suggest a shift towards more open habitats that is recorded in local wetland settings (Fig. 5b); regression analysis supports this idea (FI-t = 2.479 × time− 7.864; r = 0.787; p b 0.01, no autocorrelation). This could result either from a change to increasingly grass-dominated vegetation in these particular microhabitats, or from a general opening up of the landscape manifested as a more regional phytolith signal (see discussion above). If the inland assemblages reflecting upland environments are considered alone, the pattern becomes more diffuse, showing only a weak trend towards more open habitats (Fig. 5c). Likewise, regression analysis yields no significant relationship between FI-t and time (FI-t = 0.593 × time + 8.362; r = 0.171, p N 0.5, no autocorrelation). Finally, because of the low sample number for the Early–Middle Miocene, the differences in variation between the Early and Late Miocene may simply reflect sampling error. This can only be tested through collection of more data, as the number of data points in each subcategory (i.e., correcting for facies as well as

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biogeography/climate) currently is insufficient for statistical analysis. Similarly, more data are needed to examine the distribution of PACCAD grasses. PACCADs appear to have been common at coastal sites, but they also show high abundances at particular inland localities (Fig. 4). In the limited dataset available to date, the distribution of PACCAD morphotypes suggests no clear correlation with either distance to the coast or to local wet microhabitats, as estimated by sedimentology and/or siliceous microfossils (diatoms etc.). 4.4. Homogeneity of the Pikermian Biome Although we subscribe to a view in which generally grass-dominated ecosystems span the Greco-Iranian region by at least the Late Miocene (MN11; ∼ 9 Ma), we recognize that there may have been considerable biogeographical variation within its limits. Many previous authors have argued for a climatic and vegetational gradient across the eastern Mediterranean during the Late Miocene, with more arid, open environments to the east. Kurtén (1952: Fig. 5) for example, used functional morphology of ungulates to separate mainland Greek faunas, Pikermi and Saloniki in north-eastern Greece, which he considered to represent “forest faunas”, from the more eastern Hipparion faunas (including Samos), which he labeled “steppe faunas”. In keeping with this description, the horses at Pikermi have, in more recent studies, been described as either browsers or mixed-feeders, whereas the equid taxa at Samos have been interpreted as mixed feeders or grazers (Solounias et al., 1999). Similarly, the composition of carnivore faunas differs between these localities, indicating the presence of substrate variation (L. Werdelin, personal observation). Beden and Brunet (1986, cited in Zazzo et al., 2002) viewed a pattern of decreasing mammalian biodiversity toward the east in the Greco-Irano-Afghan region as a sign of eastwardly increasing aridity and faunal exchange. A comparison between the microwear of Turolian ungulate faunas of the Axios Valley, north-eastern Greece, and Molayan, Afghanistan, respectively, lends credence to these ideas, reconstructing vegetation as substantially more forested in Greece compared to Afghanistan (Merceron et al., 2004, 2005a,b). Zazzo et al. (2002) examined δ18O from tooth enamel of members of the genus Tragoportax at Samos and at Molayan, respectively, and found an ∼8‰ increase in δ18O from Greece to Afghanistan. This corresponds to either heightened temperature or evaporation in the east compared to the west, supporting a climatic gradient across the Greco-Irano-Afghan province.

Another set of hypotheses concerns the homogeneity of the Sub-Paratethyan region during the preceding time period (late Vallesian; MN10; 9.5–9 Ma). Based on faunal evidence it has recently been proposed that coastal Anatolia and Thrace was more humid and forested, and thus more similar to western Europe, than central Anatolia and areas further east (Geraads et al., 2005). This “Eastern Aegean Province” would have functioned as an ecological barrier between the more open, savanna/woodland-dominated regions in the western and eastern part of the Sub-Paratethys province, resulting in significant endemism in large mammal faunas between these regions (Geraads et al., 2005). As discussed above, our dataset of phytolith assemblages is too small to address these hypotheses in any detail. However, it can be noted that although Turolian and younger phytolith assemblages show substantial variation in composition, both in terms of inferred tree cover and in the abundance of PACCAD grasses, there is no clear east-to-west pattern. An exception may be the presence at Maragheh (9–8.2 Ma) of potential C4 chloridoid grasses, which could imply somewhat hotter climates further east. Evidence is currently lacking that this area experienced a rise to dominance of C4 grasses; in northern Pakistan, the C3–C4 shift occurred primarily after 8.1 Ma (e.g., Cerling et al., 1997). There are no late Vallesian phytolith assemblages from coastal Anatolia or Thrace that would allow us to test the Eastern Aegean Province hypothesis, but the unique biosilica assemblage at Mordoğan–Ardıç does point to a difference in vegetation between coast and inland during the Middle Miocene, as stated above. 4.5. Potential biases in phytolith analysis Previous work demonstrates that, despite the documented preservational bias against non-grass phytoliths (reviewed in Strömberg, 2004; Piperno, 2006), analysis of changes in relative abundances of phytolith morphotypes in pre-Quaternary biosilica assemblages results in straightforward interpretations of changes in tree cover through time (Strömberg, 2004, 2005). Thus, the Cenozoic phytolith record of North America shows a shift from Eocene and Oligocene assemblages made up of high frequencies of forest indicator phytoliths and closed-habitat grasses combined with very rare openhabitat grasses to assemblages with very high abundance of open-habitat grass phytoliths (Strömberg, 2005). This pattern unambiguously marks a change in plant community structure, presumably from closed to open. By contrast, none of the samples described from Turkey, Greece, or Iran are clearly dominated by non-grass forest

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indicator phytoliths (Figs. 4 and 5); therefore, the shift to open habitats is primarily expressed in a change in grass communities. It may well be that phytoliths closely mirror the relative abundance of dicotyledons and other forest indicator taxa in plant communities, and the observed changes reflect true biological patterns — indeed, that is the assumption under which we are working. However, a possibility that must be considered is that forest indicator taxa are underrepresented owing to production or preservation biases. Several studies point to the limited value of phytolith analysis for reconstructing forest communities in certain northtemperate ecosystems, because of the low silica production and poorly silicified morphotypes of many conifers and other north-temperate forest taxa (Bozarth, 1993; Blinnikov et al., 2002; Bremond et al., 2004; for review see Strömberg, 2004). In these ecosystems, the phytolith assemblages of both forests and grasslands tend to be dominated by grass phytoliths. For the present study, such biases would lead to a potential masking of the actual timing for the opening up of landscapes in Turkey and surrounding areas. We argue that this is a less likely explanation for the observed phytolith assemblage patterns. First, because of floral interchange throughout the Cenozoic, western Eurasia and North America hosted the same range of dicotyledons and other forest indicator taxa during the Miocene (Gregor, 1990; Mai, 1995; Graham, 1999; Manchester, 1999; Tiffney and Manchester, 2001), many of which are known phytolith producers (Piperno, 1988, 2006; Strömberg, 2003). Therefore, phytolith analysis should work similarly on the two continents (see Strömberg, 2004, 2005). Second, phytolith assemblages analyzed from the Middle and Late Miocene of Spain (Pinilla and Bustillo, 1997, C. Strömberg., unpublished data) and from the Oligocene of Germany (C. Strömberg., unpublished data) consist almost exclusively of forest indicators. These results suggest that phytolith-producing non-grass plants were indeed present in the Cenozoic of western Eurasia and that phytolith analysis should be useful for reconstructing habitat openness. However, it should be noted that because of the spatial resolution of the phytolith record (discussed above), analysis of single phytolith assemblages cannot resolve the degree of spatial heterogeneity in vegetation that may exist in an area and which may be of great importance for understanding ecosystem structure. This problem is illustrated by comparing the vegetation inference for the Late Miocene locality Akkaşdağı based on hipparionine locomotory variation as implied by metapodial morphology (a mix of relatively open to fully open habitats, Scott and Maga, 2005) and phytolith analysis (open habitat with only

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modest tree cover; Fig. 4), respectively. To fully address this issue, it may be necessary to study biosilica assemblages representing several microhabitats at a particular site. 5. Conclusions We analyzed phytolith assemblages extracted from Greece, Turkey, and Iran to test the long-standing hypothesis that grass-dominated savannas spread in the eastern Mediterranean during the Late Miocene, resulting in the establishment of the Pikermian Biome across the Greco-Irano-Afghan region. The analysis indicates that C3 grass-dominated savanna-mosaic vegetation had become widespread in Turkey and surrounding areas by the Late Miocene (∼9 Ma). These results are in agreement with the traditional savanna model and reject the recently proposed hypothesis that the vegetation of the Pikermian Biome consisted of a sclerophyllous woodland or forest with rare grasses (Solounias et al., 1999). Phytolith data further reinforce previous studies showing that C4 grasses were of little ecological importance in western Eurasia until at least the Late Miocene (∼7 Ma). However, counter to the savanna hypothesis as traditionally conceived (e.g., Kurtén, 1952; Bonis et al., 1992; MacFadden, 1992), our data suggest that relatively open, grass-dominated habitats were established in central Anatolia by at least the Early Miocene as a result of the rise to ecological dominance of open-habitat grasses, mainly pooids. This pattern implies that the faunal changes that led to the establishment of the Hipparion faunas, such as the diversification of bovids, giraffids, and horses (Bernor, 1983; Janis, 1993; Bernor et al., 1996a; Garcés et al., 1996; Fortelius et al., 1996, 2002, 2003; Jacobs et al., 1999; Koufos, 2003), were not responses to the initial ecological expansion of open-habitat grasses in this region. Instead, they may have been triggered by changes in vegetation structure or in climate in the context of open, grass-dominated habitats, such as the trend towards increasingly open habitats hinted at by phytolith data (Fig. 5). Similarly, the immigration of hipparionine horses to western Eurasia in the earliest Late Miocene (11.1–10.7 Ma, Woodburne et al., 1996; Garcés et al., 1998; Agustí et al., 1999; Koufos, 2003) was not likely linked to paleoenvironmental change (the spread of grassdominated habitats). Instead, it may have been a chance dispersal event correlated with a glacioeustatic sea level lowstand leading to the development of a land bridge at Bering's Strait at 11.4–11.3 Ma (Garcés et al., 1997; Agustí et al., 1999). Such a lowstand has been proposed for the early part of sea level cycle TB3.1 (11.3–8.9 Ma) (Haq et al., 1987; Berggren et al., 1995). Note, however,

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that the role of habitat structure and climate in northeastern Asia in controlling the immigration of hipparionines across Bering's Strait has yet to be rigorously tested. More phytolith assemblage data are necessary to test vegetation models developed in the current paper. In particular, more information is needed for the Oligocene and earliest Miocene to understand the tempo and mode of the transition between forest habitats and grassdominated vegetation. Phytolith data recently reported from the Great Plains of North America showed that open-habitat grasses were present in the vegetation 6– 10 Ma prior to becoming ecologically dominant, suggesting a lag between taxonomic and ecological radiation (Strömberg, 2005). Could the same pattern hold true for western Eurasia? The Middle Eocene assemblage, which contains no diagnostic open-habitat grass GSSC morphotypes, is not sufficient to evaluate this idea. A more complete phytolith record is also needed to correlate vegetation patterns during the Miocene, such as a progressive reduction in tree cover, with potential climatic causes in a meaningful manner. Acknowledgements This work was funded by a Swedish Research Council Grant to E. M. Friis and L. Werdelin. The Geologic Survey of Turkey in Ankara (MTA) provided logistical support during fieldwork in Turkey and many samples; the Aristotle University of Thessaloniki facilitated field work in Greece. We thank Thomas Denk, Ayan Ersoy, Mikael Fortelius, Erksin Güleç, Kurt Heissig, Tanju Kaya, Dimitris Kostopoulos, George Koufos, Serdar Mayda, Claire Sagne, Sevket Sen, Nikos Solounias, and Pascal Tassy for providing help with retrieving samples in the field and in museums (American Museum of Natural History, New York, USA; National Museum of Natural History, Paris, France; Natural History Museum, Ege University, Izmir, Turkey; Natural History Museum of the Geological Survey of Turkey, Ankara, Turkey; Bayerische Staatssammlung für Paläontologie und Geologie, München, Germany). We are indebted to Hans de Bruijn, Hans-Joachim Gregor, John Kappelman, Juha-Pekka Lunkka, Sevket Sen, Nikos Solounias, and Engin Ünay for contributing sediment and information from private collections. Comments from D. Geraads and an anonymous reviewer substantially improved the manuscript. References Abel, O., 1927. Lebensbildler aus der Tierwelt der Vorzeit. G. Fischer, Jena. 714 pp.

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