Carya as marker for tree refuges in southern Italy (Boiano basin) at the Middle Pleistocene

Palaeogeography, Palaeoclimatology, Palaeoecology 369 (2013) 295–302

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Carya as marker for tree refuges in southern Italy (Boiano basin) at the Middle Pleistocene R. Orain a,⁎, V. Lebreton a, E. Russo Ermolli b, N. Combourieu-Nebout c, A.-M. Sémah d a

Département de Préhistoire, Muséum National d'Histoire Naturelle, UMR 7194 CNRS, 1 rue René Panhard, F-75013 Paris, France Dipartimento di Arboricoltura Botanica e Patologia vegetale, Università di Napoli Federico II, via Università 100, I-80055 Porticini (NA), Italy Laboratoire des Sciences du Climat et de l'Environnement, UMR 8212 CNRS-CEA-UVSQ, Orme des Merisiers, F-91191 Gif-sur-Yvette, France d Institut de Recherche pour le Développement, LOCEAN — Paléoproxus, UMR 7159, 32 avenue Henri Varagnat, F-93143 Bondy Cedex, France b c

a r t i c l e

i n f o

Article history: Received 4 June 2012 Received in revised form 22 October 2012 Accepted 27 October 2012 Available online 6 November 2012 Keywords: Palynology Hickory Mediterranean Quaternary vegetation Paleoenvironment Paleoecology Ecological refuge Tertiary relic

a b s t r a c t The Carya genus, a tree of the Juglandaceae family, has a restricted geographical distribution today, mainly confined to North America and Southeast Asia and with a precise range of ecological requirements. During the Neogene, Carya had a wide distribution across the northern hemisphere; however, its habitat was reduced progressively in response to Pliocene and Quaternary climate changes. In the Early and Middle Pleistocene paleobotanical records, Carya is considered a relic which testifies to the final climatic deterioration of the Pliocene and to the global effect of the Quaternary climate cycles. The lacustrine and fluvio-palustrine sequence of Boiano (Molise, Italy) records the paleoenvironmental and climate changes since the Middle Pleistocene. The chronological framework is based on several tephra layers, related to known eruptions or directly dated, and indicates that the basal deposits are older than 440 ka. Palynological study of the sedimentary filling highlights vegetation changes from Oxygen Isotopic Stage (OIS) 13 to 2. The Boiano biotope, characterized by a continuous edaphic and climatic humidity, favored the persistence of hygrophilous tree taxa. Thus, Carya is present until the OIS 9, which represents its latest occurrence in Western Europe. The Boiano basin could have been an ecological refuge for the Middle Pleistocene arboreal flora. In fact, the physiography of the basin certainly softened the impacts of climatic deterioration during glacial episodes. Therefore, the late Carya occurrence within the Boiano palynological record in a time period when it is commonly supposed to be extinct from Europe, leads to a consideration of its ecological requirements as a tool for Quaternary paleoenvironmental reconstructions and for identification of refuge areas. © 2012 Elsevier B.V. All rights reserved.

1. Introduction The Plio–Pleistocene climate dynamics globally affected the world's ecosystems due to their response to the progressive cooling and increase in aridity (Lisiecki and Raymo, 2005). This led to a redistribution or reduction of vegetation diversity. In Europe, the Mediterranean Sea represented a physical limit to the southward migration of vegetation communities. As a result the climate changes constrained the most exigent taxa to refuge areas, such as the Caucasus or the southern regions of Italy and Greece (Suc et al., 1995; Svenning, 2003; Bertini, 2010; Popescu et al., 2010). Climate cyclicity and ecological competition controlled the progressive disappearance of several tree taxa, such as the Taxodioideae, Sequoioideae, Sciadopitys, Tsuga, Castanea, Liquidambar Engelhardia, Diospyros (Suc et al., 1995; Svenning, 2003; Farjon, 2005; Bertini, 2010; Popescu et al., 2010). Climate changes throughout the Mid–Pleistocene Transition strongly impacted the ecosystems, especially at the mid latitudes (Lisiecki and Raymo, 2005; Joannin et al., 2010). In Mediterranean Europe, the ⁎ Corresponding author. E-mail address: [email protected] (R. Orain). 0031-0182/$ – see front matter © 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.palaeo.2012.10.037

transition from 41-ka to 100-ka dominant climatic oscillations was associated with a crisis in aridity thus increasing the global impoverishment of vegetation communities driven by the long-term cooling trend (Joannin et al., 2010). This led to the gradual extinction of other tree taxa such as Carya, Pterocarya, Juglans and Zelkova (Suc et al., 1995; Svenning, 2003; Bertini, 2010). However, the rather discontinuous and scattered records provide only a partial chronostragraphical overview of their distributions and extinctions, thus scenarios have had to be adapted to macroregional scales. In the case of the Italian Peninsula (Bertini, 2010), the heterogeneous climatic and physiographic patterns led to environmental fragmentation (Bertini, 2010; Russo Ermolli et al., 2010a; Manzi et al., 2011) the history of which can be disclosed through the study of a large number of continuous high resolution paleoenvironmental records. Pollen archives from central and southern Apennine sedimentary basins constitute propitious sites which have recorded the environmental changes at regional and local scales. The Boiano basin (41°29′N, 14°28′E; ca. 500 m a.s.l., Molise Italy) is one of the places which allow us to reconstruct European vegetation history towards its present-day composition and structure. The Boiano sequence recorded the trends of environment and vegetation between OIS 13 and 2 (Aucelli et al., 2011; Orain et al., 2012) and delivers new pollen

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data to provide a long Middle Pleistocene paleoenvironmental record and to address key issues such as the potentiality of southern Italy as a refuge area. 2. Paleoenvironmental setting of the Boiano basin Located in Molise (Italy), the Boiano basin is an intramontane tectonic depression confined between the Matese and Montagna di Frosolone massifs and the Sannio hills (Fig. 1). This 20 km long and 4 km large plain stretching in the NW–SE direction, is now drained by the Biferno river. The current mean annual temperature is 13.4 °C (with average temperatures of 1 °C for the coldest month and 26 °C for the warmest month) and mean annual precipitation between 600 and 700 mm (data from the Servizio Meteorologico dell'Aeronautica Militare). The basin was warped by several compression phases from the Miocene to the Pliocene, followed by strike-slip tectonics and then, extensional tectonics from the Middle Pleistocene. The main faults show a NW–SE trend; among them several are still active (Amato et al., 2010, 2011; Aucelli et al., 2011). Recent investigations have been conducted on the Quaternary infilling of the Boiano basin (Amato et al., 2010). Several boreholes were drilled in the plain, two of which (S1 and S6) provided long

Fig. 1. Location, geological and morphotectonic contexts of the Boiano basin and of the main close sedimentary basins of the Molise region (from Aucelli et al., 2011). 1) Fluviopalustrine deposits (Quaternary), 2) siliciclastic deposits (Miocene), 3) clays, marls and limestones of Sannio (Upper Cretaceous Miocene), 4) limestones, dolomites, marls of carbonate plateform (a) and carbonate slope deposits (b) (Triassic/Miocene), 5) main thrusts, 6) Main extensional faults.

sediment cores without reaching the bedrock (Amato et al., 2010; Aucelli et al., 2011). The sedimentologic records of the two cores are consistent (as detailed in Aucelli et al., 2011). The different lithofacies of S6 core show successive phases of lacustrine and fluvio-palustrine deposits with several intercalated tephra layers (Fig. 2). Three 40Ar/39Ar datings were performed on the S1 core tephra layers. The lowest layer indicates that the basal deposits are older than 426±5.5 ka, while the second level was directly dated to 311±4.7 ka and chemically correlated to the White Trachytic Tuff from the Roccamonfina volcano (Amato et al., 2010; Aucelli et al., 2011). Within the upper deposits, the youngest tephra layer was identified as the Tufo Giallo Napoletano, dated to ca. 15 ka (Amato et al., 2010; Aucelli et al., 2011). These ages provide a reliable chronological framework for the Boiano series. The palynological results obtained from the S6 core were supported by a constrained cluster analysis as in Di Donato et al. (2008; Fig. 3, Table 1; Orain et al., 2012) which highlighted four Local Pollen Zones (LPZ). LPZ 1 and 3 were related to interglacial phases, while the heterogeneous spectra of LPZ 2 represents several phases, dominated by a glacial tendency. The most important feature of the whole sequence is the persistence of a local edaphic humidity. This assertion is supported by the continuous occurrence of Cyperaceae and Ranunculaceae, associated with Poaceae, even during the glacial phases. This local humidity coupled with the morphology of the basin certainly influenced the ecosystems and softened the impacts of the Quaternary climatic deterioration. Such peculiar edaphic conditions could have favored the local persistence of the more humidity-demanding genera (Carya, Juglans,

Fig. 2. Lithographic log of the Boiano S6 core. Modified from Aucelli et al., 2011.

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Fig. 3. Synthetic pollen diagram of core S6 from Boiano, with position of barren samples (■). Taxa are grouped according to their ecological significance. After Orain et al., 2012.

Zelkova, Ulmus), despite an unsuitable Middle Pleistocene climate (Bertini, 2010). The Boiano vegetation was most likely dominated by humid deciduous forest in the valley and by a mixed forest with coniferous trees in the low altitude slopes surrounding the basin (Amato et al., 2011; Aucelli et al., 2011). The latter were probably dominated by Fagus, potentially associated with Cedrus, only represented by a few grains, although a long distance transport could not be excluded for this taxon (Magri, 2012). Higher elevations were dominated by Abies and Picea (Orain et al., 2012). Carya was probably a secondary component of the vegetation which would have been globally organized as a temperate continental deciduous forest (Wang, 1961; Delcourt et al., 1983; Barbour and Billings, 1988). Indeed, Carya is represented by a few grains at the beginning of the sequence in the LPZ1 related to OIS 13, while the second development recorded in the LPZ3 is related to OIS 9 and characterized by a maximum tree species diversity (Amato et al., 2010; Aucelli et al.,

Table 1 Isotopic correlations and summary description of the palynological sequence of the Boiano basin, including main biome deduced from pollen assemblages. OIS Pollen correlation zone

Pollen signature

Main biome

OIS 8 to OIS 2

LPZ 4

–

OIS 9

LPZ 3b

Heterogenous pollen and sedimentary records Sedimentary fillings of the basin?a Abies dominant with Picea, Mixed decidous forest decreasing and impoverishinga Quercus/ Fagus (dominant) decreasing, Progressive augmentation of decidous trees diversity, Carya present (max ≈ 5% of AP), Coniferous (Abies, Picea, Cedrus) increasinga Herbs dominance with steppic association, Local evidences of reworked material, Occasional occurrences of several treesa Abies and Picea increasing (10 to 30%), Pinus progressing (concentration), Fagus decreasing (10 to 0%), Mixed decidous forest (with Carya) around 10%, Hygrophylous locally decreasinga

LPZ 3a

OIS 12 to OIS 10

LPZ 2

OIS 13

LPZ 1

a

Coniferous forest Mesophilous forest

Steppe

Coniferous forest

Continuous occurrences of local edaphic humidity (attested by hygrophylous plants).

2011; Orain et al., 2012). Although Carya is considered a relatively important pollen producer, its pollen dispersal remains limited (Delcourt et al., 1983; Delcourt and Delcourt, 1985). According to the statistical model expressing the ratio pollen/trees presence of Delcourt et al. (1983), the abundance of Carya during OIS 9 at Boiano (maximum = 4.17% of the AP) attests the presence of the taxon. 3. Modern Carya 3.1. Ecology and distribution of Carya Modern Carya populations are strictly confined to subtropical and temperate continental biomes (Fig. 4). Carya populations are widespread over North America in the United States, Canada and Mexico, and Southeast Asia in China, Viet Nam, Laos and India (Braun, 1950; Wang, 1961; Manning, 1962, 1963; Wolfe, 1979; Manchester, 1987; Barbour and Billings, 1988; Ho et al., 1992). Today, Carya species are located in areas exposed to important maritime influence, mainly concerning humidity, and with rainfall values between 1000 and 1500 mm/year (or more). In such regions, precipitation is not evenly distributed through the year (Wang, 1961; Delcourt et al., 1983; Barbour and Billings, 1988; Ho et al., 1992; Peel et al., 2007; Rudolf et al., 2010). Mean annual temperature is around 16–18 °C, with a limited period of temperatures below zero (Barbour and Billings, 1988; Peel et al., 2007). Due to these conditions, Carya never lives above 1000 m (Braun, 1950; Manning, 1963; Barbour and Billings, 1988). The environmental conditions of modern Carya species are summarized in Table 2. 3.2. Pollen morphology Carya pollen morphology allows their easy determination (Punt and Blackmore, 1991). Grains are 3–4 zonoporate (with a maximal range of 1–6 porate in abnormal grains) on a circular to rounded-triangular shape in polar view and elliptic to circular shape in equatorial view (transverse to pertransverse Polar/Equator ratio). The ecto- and endoapertures are pori, usually more or less elliptic to sometimes circular, situated in the equatorial zone slightly shifted to one side of the pollen grain (para-isopolar) (Punt and Blackmore, 1991). Pollen exine varies from relatively thin on the proximal face to thick on the distal face, and is slightly thickened at the pori. Pollen

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Fig. 4. Modern Carya ecosystems repartition.

ornamentation is scabrate at optical microscope (OM). Pollen grains measure in average 33–55 μm, which is larger than the other triporate tribes of the Juglandaceae family (Punt and Blackmore, 1991). There is no clear palynological distinction between the different Carya species, but Eucarya section tends to be larger than Apocarya and Sinocarya section. This difference could be linked to the occurrence of polyploidy in the Eucarya section grains. However, the intra- and inter-specific size variability of the Carya pollen grains limits the potential discrimination of a section among the others (Punt and Blackmore, 1991; Manos and Stone, 2001). Some observations and measurements have been undertaken on nine Carya species from the reference collection of the ISEM Laboratory (UMR 5554, Montpellier University). Based on length of the pollen grains and thickness of their exine, no morphologic or morphometric characteristics afford distinguishing different species or sections for Carya pollen taxa. The Carya grains identified at Boiano reflect this heterogeneity (size between 40 and 52 μm, rather thin to thick exine), which prevent section or species identifications.

4. Carya in the past 4.1. Prior to the Neogene Within and since the Paleogene, the paleobotanical evidence of Carya illustrates the biological evolution of the genus and its spread throughout the northern hemisphere (Manchester, 1987). Today, data give a global vision of Carya expansion since its first appearance and allow us to follow the story of this spread (Manchester, 1987; Manos and Stone, 2001). The first occurrence of Carya-like pollen grains is noted in the Upper Paleocene from Western Europe and Northern America. Such pollen grains corresponded to the primitive form of the Caryapollenites type (frequently referred to as Subtriporopollenites type in Europe, Manchester, 1987). The pollen morphology, although very similar to Carya morphology, shows a smaller size, around 25 μm (Manchester, 1987; Utesher and Mosbrugger, 2007). Caryapollenites type grains are thereafter locally present during the Early to Middle Eocene in North

Table 2 List of the main modern Carya species with their related environmental and climate conditions. Species marked with an asterisk are also present in Mexican mesophytic forest environment. On the right, Koppen climate classification items refers to the following climate types: (Cfa) Temperate without dry season and hot summer, (Dfa) Cold without dry season and hot summer and (Cwa) Temperate with dry winter and hot summer (see Peel et al. (2007) for detailed index); and the annual precipitation values. Carya species (section)

Environment

Köppen Climate

Precipitation (mm/y)

C. (Wangenh.) K. Koch (Apocarya) C. illinoensis (Wangenh.) K. Koch (Apo.)* C. alba (Poir.) Nutt. (Eucarya) C. glabra (Mill.) Sweet (Euc.) C. lacinosa (Mill.) K. Koch (Euc.) C. myristiricaeformis (F. Michx.) Nutt. (Euc.)* C. ovalis (Wangenh.) Sarg. (Euc.) C. ovata (Mill.) K. Koch (Euc.)* C. taxana Buckley (Euc.) C. tomentosa (Poir.) Nutt. (Euc.) C. floridana Sarg. (Euc.) C. pallida (Ashe) Engl. and Graebn. (Euc.) C. aquatica (F. Michx.) Nutt. (Apo.) C. palmeri W.E. Manning (Euc.) [with *] C. cathayensis Sarg. (Sinocarya) C. dabieshanensis M.C. Liu (Sino.) C. hunanensis W.C. Cheng and R.H. Chang (Sino.) C. kweichowensis Kuang and A.M. Lu (Sino.) C. poilanei Leroy (Sino.) C. tonkinensis Lecomte (Sino.)

North American mixed mesophytic forests (notably Oak-Hickory Formation, Western USA)

Cfa (Dfa up north)

≥1000

Floridian sand based mesophytic forest

Cfa

≥1000

Southern USA and Mississippi blackswamps forest Mexican mesophytic forest Southeastern Asian mixed mesophytic forests

Cfa Cwa Cwa

≥1500 (seasonal floodings) ≥1000 ≥1000

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America, Europe and eastern Asia (Cavagnetto and Anton, 1996; Oboh et al., 1996; Richter and LePage, 2005; Lenz et al., 2007; Wang et al., 2010). Although both morphologic and size characteristics of Carya pollen grains are identified in the Oligocene in North America, Europe and Asia, including Japan (Manchester, 1987), recent discussions still consider this taxon closer to Caryapollenites type (Mai, 1998; Akkiraz and Akgün, 2005). 4.2. Neogene period From the Early Miocene onwards, the complete development of Carya is attested by the pollen and fruit morphologies (Manchester, 1987). Taking advantage of the benefits of the climate conditions during the Miocene, Carya develops, and reaches its assumed widest extension in the middle Miocene (Fig. 5). It is then recorded across Eurasia, including Siberia and Japan, and in North America (Manchester, 1987; Harrison and Harrison, 1989; Liu and Leopold, 1994; Suzuki and Watari, 1994; Wehr, 1995; White et al., 1996; Pazzaglia et al., 1997; Figueral et al., 1999; Roiron et al., 1999; Martinez-Hernandez and Ramirez-Arriaga, 2006; Akgün et al., 2007; Jimenez-Moreno and Suc, 2007; Leopold et al., 2007; Kuz'mina and Volkova, 2008; Jeong et al., 2009; Jiang and Ding, 2009; JimenezMoreno et al., 2010; Larsson et al., 2010; Lim et al., 2010; Gnibidenko et al., 2011; Miao et al., 2011). During the Messinian aridity crisis, the subtropical humid forest and a part of the temperate broadleaved decidous forests almost disappeared from around the Mediterranean, constraining Carya development within the deciduous forests (Su and Bessais, 1990; Bertini, 1994; Suc et al., 1995; Bertini, et al., 1998; Bertini, 2006). During the Pliocene, Carya was still widely distributed throughout the northern hemisphere. The paleobotanical evidence indicates the presence of Carya in Japan, eastern Asia, Europe and northern America (Monohara, 1992; Leroy and Roiron, 1996; Pontini and Bertini, 2000; Demske et al., 2002; Liu et al., 2002; Groot, 2003; Fujiki and Ozawa, 2008; Bertini, 2010; Jimenez-Moreno et al., 2010; Wu et al., 2011). However, the continuous cooling recorded during the Pliocene (Lisiecki and Raymo, 2005) progressively constrained the Neogene vegetation to more southern latitudes (Salzmann et al., 2011). Pliocene climate changes in Siberia, central Asia and north-western America led to the first regional disappearance of Carya (Chlachula, 2001; Liu et al., 2002; Leopold et al., 2007; Wu et al., 2011). 4.3. Quaternary period The 41-ka Pleistocene climate cycles, starting at 2.588 Ma, and the regular intensification of the glacial phases (Lisiecki and Raymo, 2005), contributed to the ongoing impoverishment of plant diversity in Europe. This reduction in diversity is particularly notable in Europe,

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where clear differences can be observed between temperate northern and Mediterranean southern regions. Within this general decrease in diversity, Carya distribution was progressively constrained. In North America, Carya retreated towards the Gulf of Mexico during the glacial phases, and then re-expanded during the interglacial phases. Following this pattern, Carya distribution moved progressively towards the south east of North America and towards continental south-eastern Asia until the Holocene (Delcourt and Delcourt, 1985; Manos and Stone, 2001; LaMoreaux et al., 2009). During the Early Pleistocene in Asia, Carya completely disappeared from Siberia and Japan (Monohara, 1992; Demske et al., 2002). The continental mixed mesophytic forests of south-eastern Asia migrated progressively southward (Wang, 1961; Ho et al., 1992). Carya, as with other climatically exigent trees, was strongly reduced in the north, although it remained well represented in continental south-eastern Asia (Wang, 1961; Ho et al., 1992; Liu et al., 2002). In Europe, “Tertiary relics” subsisted temporarily under locally favorable conditions in Mediterranean regions and in eastern refuges such as the Caucasus (Svenning, 2003). Thus Carya remained present until the Middle Pleistocene, mainly up to OIS 13, with local persistence during OIS 11 (Ber, 2006; Bertini, 2010; Russo Ermolli et al., 2010a). The Boiano palynological sequence records Carya presence in the OIS 9, more recent than its current known limit in Western Europe. In the east, Carya was recorded in Greece in the same time period (Tenaghi Philippon; Tzedakis et al., 2006). 5. Discussions 5.1. Vegetation and climate implications from the Boiano record The link between pollen grains and plant occurrence represents an important question for the Carya genus. Carya is a relatively high pollen producer, although its pollen dispersal remains limited (Delcourt et al., 1983; Delcourt and Delcourt, 1985). The Boiano palynological record proves the local presence of Carya in the basin, although it does not directly indicate its abundance within the vegetation. Present day difference between pollen and tree representation has already shown that Carya pollen representation versus tree abundance may vary from over- (including pollen occurrence without the local presence of the tree) to equally- and under-representation (Delcourt et al., 1983; Delcourt and Delcourt, 1985). Carya representation at values lower than 2% of the arboreal pollen (AP) could not be related to significant amounts of Carya in the vegetation, although it does demonstrate its regional presence. On the other hand, values over 2% are statistically significant and reflect the effective Carya presence in close proximity to the investigated spot (Delcourt et al., 1983). However, the effective Carya abundance remains difficult to deduce, as the ratio pollen/vegetation of Carya does not follow a linear model (Delcourt et al., 1983). At Boiano,

Fig. 5. Location of the currently known occurrence of Carya during its widest extension at the Middle Miocene, with position of the site and potential area of presence of environing Carya populations.

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Carya percentages are over 4% of the AP, too low to consider Carya as a sub-dominant to dominant forest taxon (20–40%). However, such pollen amounts do indicate that Carya was a component of the vegetation. The Boiano vegetation, similar to that identified in other Italian Middle Pleistocene records (Bertini, 2010), testifies to an overall humid temperate climate. A regular precipitation regime is one of the main criteria allowing Carya expansion (Northern America, Asia; Table 2; Delcourt and Delcourt, 1985; Ravazzi and Strick, 1995). It has been demonstrated that Carya development may be favored by marine humidity inputs. Thus, in the coastal plain of south-eastern North America, the Atlantic oceanic influence has a direct impact on precipitation abundance and edaphic moisture (Delcourt et al., 1983; Delcourt and Delcourt, 1985; Barbour and Billings, 1988; Peel et al., 2007). Similar climatic conditions are encountered in continental southeastern Asia (Wang, 1961; Manning, 1963; Wolfe, 1979; Manos and Stone, 2001; Peel et al., 2007; Rudolf et al., 2010). Furthermore, the Carya climax, reached in the Oak-Hickory (OH) sub-zonobiome, a semi-open woodland of North America, corresponds to a relatively humid continental climate largely influenced by oceanic moisture (Cfa; Barbour and Billings, 1988; Peel et al., 2007; Rudolf et al., 2010). In Europe, the progressive increase in aridity during the Pleistocene glacial phases resulted in heterogeneous moisture patterns (Fauquette et al., 2011) and consequently to the subtropical taxa extinctions (Bertini, 2010; Russo Ermolli et al., 2010a). Carya occurrence in the Boiano record indicates a humidity pattern singular to the Boiano basin. The hygrophilous taxa abundance recorded in the Boiano sequence during the glacial phases associated with the continuous record of Abies up to OIS 9, the presence of Cedrus, Ulmus, Zelkova and the riparian forest (Orain et al., 2012), strengthen the assumption of an important atmospheric and edaphic humidity input under a temperate climate. However, the morphology of the basin, including the surrounding paleoelevations, certainly limited the marine influence (Santangelo et al., 2012). The exceptional Carya persistence at Boiano could then be considered as reflecting an increase in humidity, highlighting the regional and micro-regional climate contrasts in southern Europe, and especially in Italy (Bertini, 2010; Russo Ermolli et al., 2010a,b; Manzi et al., 2011). In several Pliocene and Early Pleistocene palynological sequences in Italy, Carya reaches 40% of the total pollen account, which is considered as a dense temperate humid forest (see Ravazzi and Strick, 1995; Russo Ermolli et al., 2010a). However, the current climax of Carya corresponds to a semi-open woodland rather than to a dense forest (OH subzonobiome; Braun, 1950; Barbour and Billings, 1988). The other forest elements (Quercus, Carpinus, Ulmus, Zelkova, Juglans, etc.) remain essential to draw a full picture of the regional vegetation. In Leffe (northern Italy), the forest was dominated by Carya with only a few Quercus (Ravazzi and Strick, 1995), which directly contests the attribution of this forest to the OH sub-zonobiome, where Quercus is always dominant (Braun, 1950; Delcourt et al., 1983; Barbour and Billings, 1988). However, the high Carya pollen abundance reached at Leffe (northern Italy) does not correspond to any surface pollen spectra from present day vegetation (Delcourt et al., 1983; Delcourt and Delcourt, 1985). The reconstructed environment of Boiano could then be closer to the present day coastal plain forest of the south-eastern United States, corresponding to humid to palustrine ecosystems, with subtropical conditions (Barbour and Billings, 1988) Therefore, the Pleistocene Carya dominated forest would probably correspond to those of the south-eastern American coastal plain, without Taxodioideae and Sequoioideae (Braun, 1950; Barbour and Billings, 1988). Taxodioideae and Sequoioideae, major Carya competitors of the south-eastern North American forest, disappeared from the northern Mediterranean ecosystems in the Early Pleistocene (Suc et al., 1995; Bertini, 2010), although the taxa is still present at Valle di Manche at the Early to Middle Pleistocene transition (Capraro et al., 2005). Carya could then have benefited from the ecological niche released by the Taxodioideae and Sequoioideae disappearance, leading to the emergence of this singular vegetation.

These assumptions are supported by the records from the Lamone marine sequence in the northern Apennines, where Juglandaceae (mainly Carya) strongly redeveloped during the climate optima of the Early Pleistocene, while Taxodioideae and Sequoioideae had already declined (Fusco, 2007). Local climate conditions, mostly characterized by the maintenance of humidity, allowed Carya to persist in the Boiano basin. 5.2. Carya as a marker of the Boiano refuge Carya disappeared gradually from palynological assemblages in northern and in most of the central Italian sites at the end of the Early Pleistocene, around OIS 21 (Bertini, 2010; Bertini and Sadori, 2010; Russo Ermolli et al., 2010a; Corrado and Magri, 2011), with an exceptional presence at Ceprano (central Italy), within levels attributed to OIS 15 or 13 (Manzi et al., 2010). In southern Italy, its representation becomes more and more fragmented during the Middle Pleistocene, with early absences in several Molise sites; prior to OIS 15 at La Pineta (Lebreton, 2002) and prior to OIS 13 at Sessano (Russo Ermolli et al., 2010a,b) and later local presences until the OIS 11 in Campania (Bertini, 2010; Bertini and Sadori, 2010; Russo Ermolli et al., 2010a). Considering the slow recovery of Carya species (Barbour and Billings, 1988), the re-colonization of Carya from long distance refuges, such as the Caucasus (Svenning, 2003), seems unlikely (Bennett et al., 1999). The complex physiography of Italy certainly led to a mosaic of environments with micro-regional climatic conditions, eventually modified at local scales by edaphic characters (Bertini, 2010; Russo Ermolli et al., 2010a). The climatic evolution of the Pleistocene accentuated the fragmentation of environments within these regions (Bennett et al., 1999; Manzi et al., 2011). The position of the Boiano basin, its geomorphology and singular climate with continuous humidity persistence generated an exceptional set of conditions which led to the formation of a vegetation refuge for the Italian Middle Pleistocene allowing the persistence of Carya (Orain et al., 2012). Thus, in the Boiano refuge, Carya could have survived during the glacial phases, probably using vegetative reproduction (Elias, 1972; Ernst and Brooks, 2003), and potentially re-expanding over larger areas under more favorable climatic conditions during the Middle Pleistocene interglacial episodes (Bennett et al., 1999). 6. Conclusions Carya disappeared from northern and central Italy around OIS 21, but has been recorded locally up to OIS 11 in southern regions. The new pollen data from the Boiano basin sequence extends its survival to OIS 9, highlighting the fragmentation of the environments along the southern peninsula. The complex physiography of Italy combined with the Pleistocene climate evolution certainly led to a mosaic of environments with micro-regional climate variations, eventually amplified by local edaphic characters. Thus, the Boiano basin morphology and location allowed the maintenance of edaphic humidity, constituting an ecological refuge for tree communities. Considering the slow growing rhythm of Carya, the trees' recovery during late Early- and Middle Pleistocene interglacial episodes has certainly been determined by the regional presence of vegetation refuge areas offering suitable environmental conditions and limited ecological competition. The maintenance of Carya among pollen records then constitutes a marker of these singular ecological conditions. In the case of the Boiano refuge, Carya could have survived up to OIS 9, potentially using vegetative reproduction during the glacial phases, and re-expanded over larger areas under more favorable climatic conditions during the Middle Pleistocene interglacial episodes. Acknowledgment This paper has been realized with the benefit of a doctoral fellowship of the French MESR. The authors also thank the French MNHN

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Transversal Action “Relations Sociétés-Natures dans le long terme”, its project “Chronologie des occupations acheuléennes d'Europe occidentale” and its supervisor J.-J. Bahain. This is LSCE contribution n° 4933. We also thank P. Aucelli and V. Amato, respectively from Napoli and Isernia universities, for the parallel researches and the opportunity of investigation they granted us. The authors thank our collaborator who wanted to stay anonymous for the English proof reading, and J. Oprescu for the figures management or improvement. The authors are also grateful to R. Cheddadi, who allowed the access to ISEM pollen collection for morphologic analysis. Finally, we thank D. Magri, A. Bertini and P. Kershaw for improvement of the manuscript.

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