a hydraulic conductivity model points to post-neogene
Transcription
a hydraulic conductivity model points to post-neogene
3158 NOTES Ecology, Vol. 85, No. 11 Ecology, 85(11), 2004, pp. 3158-3165 © 2004 by the Ecological Society of America A HYDRAULIC CONDUCTIVITY MODEL POINTS TO POST-NEOGENE SURVIVAL OF THE MEDITERRANEAN OLIVE J.-F. TERRAL,1,4 E. BADAL,2 C. HEINZ,1 P. ROIRON,1 S. THIEBAULT,3 AND I. FIGUEIRAL1 1 Centre de Bio-archéologie et d’Ecologie (CNRS UMR 5059), Institut de Botanique, Université Montpellier 2, 163 rue Auguste Broussonet, 34090 Montpellier, France 2 Dpt. Prehistoria y Arqueologia, Universitat de València, av. Blasco Ibañez 28, 46010 Valencia, Spain 3 Archéologie et Sciences de l'Antiquité (CNRS UMR 7041), Maison de l'Archéologie et de l'Ethnologie, allée de l’Université, 92023 Nanterre cedex, France Abstract. Research on the subfossil record and paleoecology of Olea europaea suggests a new interpretation of its history and ecology with reference to the Mediterranean climate since the Neogene. New results are based on the wood anatomy of ancient and extant Olea and a model estimating hydraulic conductance established for wild forms belonging to Olea europaea subsp. europaea. These suggest that during glacial periods wild olive populations survived in protected microenvironments, particularly riparian habitats. Thereafter, the postglacial expansion of olive associated with climatic warming took place from these refuge areas. This new evidence suggests that the continued existence of Olea in Mediterranean areas since the Neogene was made possible either by preferential survival of Olea lineages adaptable to the Holocene climate or from enhanced adaptation to extreme environmental variation, a trait possibly originating from Tertiary predecessors and maintained in postglacial olive populations. Key words: Last Glacial Maximum; Mediterranean; Neogene; Olea; palaeoecology; quantitative ecoanatomy; riparian refuge areas . THE OLIVE TREE AS A PRODUCT OF THE NEOGENE FLORA The olive tree of the Mediterranean Basin is part of the “Olea europaea complex”, which consists of six different subspecies (Tab. 1) (Green and Wickens 1989, Hess et al. 2000, Besnard et al. 2002). The genus Olea is considered to have existed in the western Mediterranean area since the Late Paleogene (Arambourg et al. 1953, Suc 1984, Bessedik 1985, Palamarev 1989). Olea pollen (Bessedik 1985) and macrofossils (Palamarev 1989) are recorded as early as the Aquitanian (25-20 Ma, Early Miocene). In the northwestern Mediterranean area, Olea has been recorded unequivocally in strata as old as 3.2 Ma (million years) from the Middle Pliocene (Arambourg et al. 1953, Palamarev 1989). During the beginning of the Pliocene, palynological data show that this area was dominated by subtropical species such as palms, laurels, swamp cypresses and magnoliaceous dicotyledons, indicating a warm and humid climate (Suc et al. 1995, Fauquette et al. 1999). Certain western Mediterranean elements such as evergreen and deciduous Quercus, Carpinus, Fagus and eastern Mediterranean species such as Zelkova and Manuscript received 22 May 2003; revised 3 March 2004; accepted 1 April 2004. Corresponding Editor:C.C. Labandeira. 4 E-mail: [email protected] Celtis, also were present. In view of this floristic association, it is possible that Olea was present in western and central Europe as early as the Eocene to Oligocene (Mai 1989), and distributed around the Tethys Basin since at least the Miocene (Figueiral et al. 1999). Presumably, this early genus was an ancestor of modern Olea and well adapted to a subtropical climate, probably growing on drained soils and sunlit slopes. The Eocene to Oligocene transition was marked by important climatic cooling, possibly coinciding with the decline of laurophyll tropical and subtropical plants (Mai, 1989). The tectonic convergence between northwestern Africa and southwestern Europe, which led to the Messi-nian salinity crisis (5.59 to 5.33 Ma, Krijgsman et al. 1999), may have resulted in the Pliocene migration of African species into Europe, along with Olea (Médail et al. 2001, Quézel and Médail, 2003). During this period, the Macaronesian archipelagos emerged (except the islands of La Palma and El Hierro) and Olea may have been progressively introduced by birds that colonized dry areas (Hess et al. 2000). The subspecies O. cerasiformis and O. guanchica (Table1, Fig. 1) may have been differentiated by reproductive isolation. During the Pliocene, extreme climatic events (4.5 and 3.6 Ma) led to the desertification of the Sahara and the expansion of a Sahelian vegetation (Suc et al. November 2004 NOTES 3159 TABLE 1. Present-day distribution and ecological range of Olea. Olea L. material studied Olea europaea L. subsp. europaea Location Mediterranean Basin subsp. maroccana Western High Atlas subsp. cerasiformis Madeira Islands subsp. guanchica Canary Island subsp. laperrinei central Sahara and Sahel subsp. cuspidata africana phenotype chrysophylla phenotype cuspidata phenotype Olea capensis L. Olea woodiana Knobl. Olea perrieri Chev. Olea lancea Lam. South Africa (Capetown region) from South Africa to Kenya from Ethiopia to the Arabian Peninsula from Iran to western China central, southern, and eastern Africa eastern and southern africa Madagascar Mauritius Vegetation belt sclerophyllous shrub and forest (matorral) sclerophyllous shrub and preforest sclerophyllous shrub and forest (matorral) sclerophyllous shrub and forest (matorral) Saharo-sahelian mountain shrub Bioclimatic context† thermomesomediterranean/ humid to semiarid arid inframediterranean dry infracanarian dry infracanarian Saharian and Sahelian/semiarid to hyperarid thermomediterranean/dry sclerophyllous shrub and forest (matorral) evergreen and semideciduous shrub and forest mountain evergreen forest subtropical/subhumid to arid mountain evergreen forest subtropical/dry-semiarid mountain evergreen forest evergreen forest tropical-subtropical/humid to semiarid tropical/dry-semiarid evergreen forest evergreen mountain forest tropical/humid-subhumid tropical/dry-semiarid subtropical/dry-semiarid †Definitions are as follows: inframediterranean and infracanarian, T (mean annual temperature; °C) > 19; thermomediterranean, 17 ≤ T < 19; mesomediterranean, 13 ≤ T < 17. Ombroclimatic parameters are : hyperhumid, P (mean annual precipitation; mm) ≥ 1600; humid, 1000 ≤ P < 1600; subhumid, 600 ≤ P < 1000; dry: 350 ≤ P < 600; semiarid, 200 ≤ P < 350; and arid, p < 200. The mediterranean bioclimatic context is based on thermic parameters defined by Rivas Martinez (1987). 1995). Thus, the Hoggar (Algeria) and Marra (Sudan) mountains, and the eastern part of the Anti-Atlas Cordillera (Morocco) may have represented relictual areas for O. europaea laperrinei and O. europaea maroccana, respectively (Quézel and Médail, 2003). The Middle Pliocene (3.15 to 2.85 Ma) corresponded to a period of widespread climatic and floral change with the gradual disappearance of subtropical plants and the establishment of Mediterranean elements (Michaux et al. 1979). The emerging northwestern Mediterranean flora included relatively thermophilic and xerophytic elements such as Olea (possibly Olea europaea subsp. europaea), Pistacia and evergreen Quercus, as well as mesic taxa such as deciduous Quercus. The ecological success of these relatively xeric elements resulted from drier climatic conditions following the expansion of the polar ice sheets (Shackleton et al. 1988). The onset of a drier temperate climate may have been triggered by two factors: (1) a change in atmospheric circulation and deflection of anticyclone systems to lower latitudes linked to the establishment of the Gulf Stream (Haywood et al. 2000), and (2) increasing CO2 levels (Raymo et al. 1996). Around the Late Pliocene (c. 2.8 to 2.6 Ma) the first major glaciation in northern Europe marked the begin- ning of Pleistocene climatic oscillations (1.88 Ma to 10 Ka), during which Olea managed to survive, becoming a major element of the Mediterranean sclerophill vegetation over the last 10 millennia. But the question remains as to how and where did olive survive during the Last Glacial Würm Maximum (LGM) ? THE SURVIVAL OF THE OLIVE TREE DURING THE LAST GLACIAL MAXIMUM (LGM) In the northwestern Mediterranean, Olea has been identified only sporadically in the pollen record up to 8000 yr BP (Pons and Reille 1988, Carrión and Dupré 1996, Carrión et al. 1995, Carrión and Van Geel 1999). However, Olea pollen has been recorded during the LGM, in archaeological sites located in southeastern Spain (Carrión et al. 2003). Other thermophilic and xerophytic plants such as Pistacia lentiscus, which today is associated with Olea europaea, also have been identified during the early Holocene in this area (Pons and Reille 1988). Identification of archaeological charcoals has provided evidence of early occurrences of Olea associated with human settlements since ca. 24000 yr BP in Portugal (Zilhão et al. 1995, Figueiral 1998, Figueiral and 3160 NOTES Ecology, Vol. 85, No. 11 FIG. 1. Distribution of Olea species and Olea europaea subspecies, location of plant material studied, and archaeological sites and layers. Radiocarbon dates (calibrated according to CALIB 4.2 program [Stuiver et al. 1998] based on charcoal fragments are also presented. Circles represent the distribution of the species and subspecies studied. Terral 2002), and ca. 7500 yr BP in Spain (Barton et al. 1990) and France (Solari and Vernet 1992). Olive wood has been used as fuel long before its cultivation, domestication, and widespread nutritional and economic use in the Mediterranean Basin. Quantitative eco-anatomical analyses were carried out on charcoal fragments assigned to Olea europaea, from the sites of Buraca Grande (Upper Palaeolithic to Neolithic, Portugal), Cova de les Cendres (Neolithic, Spain) and Giribaldi (Neolithic, France) (Fig. 1). These investigations combine measurements of wood characters following the methodological and analytical protocols developed previously by Terral and Arnold-Simard (1996) and Terral and Mengüal (1999). Data obtained also were compared to those measured from the anatomical analysis of material from living subspecies of the O. europaea complex and from other Olea species (Table 1; Fig. 1). Anatomical correlates of ecological parameters revealed a very heterogeneous conductance surface of vessels. Results indicate that in some archaeologically documented intervals, the olive charcoal assemblage was formed from two statistically distinct populations (Fig. 2). These populations correspond to two different ecological habitats from where wood fuel was collected by humans around settlements. In fact, while some specimens present small surface vessels (mean = 730.89 µm², 95% CI = 15.78), as expected from plants growing on slopes and/or well drained soils, others show very large vessels (mean = 1038.13 µm², 95% CI = 27.03) and consequently very high calculated water conductivity, representing highly efficient sap transport through xylem vessels. These plants must have developed in riparian habitats. So far, modern analogues for these subfossil specimens have not been found in the extant material studied of Olea europaea subsp. europaea. A recent study based on living wild olive populations from the western Mediterranean (Table. 2) that correlates anatomical features with climatic data indicates that “vessel conductivity” depends on annual mean rainfall (Terral and Mengüal 1999; Fig. 3). Variations in “conductivity” in relation to mean annual rainfall also may be modulated by factors such as soil fertility November 2004 NOTES 3161 FIG. 2. Distribution of frequencies of olive charcoal from archaeological assemblages (see insert in Fig. 1) in relation to “vascular conductivity.” Results of normality tests (Kolmogorov-Smirnov) are presented for each population identified corresponding to a distinct habitat. Dashed lines indicate the range of conductivities for each population. For all tests shown, P > 0.01. and humidity. This model, when applied to other Olea europaea subspecies and other Olea species (Table 1, Fig. 1), allows us to distinguish trees growing in typical conditions and belonging to Olea europaea subsp. europaea (defining the interpolation zone) from olive adapted to arid conditions (extrapolation zone 1) vs. olive growing under hyperhumid conditions (extrapolation zone 2) (Fig. 3). Today, olive (O. europaea subsp europaea) grows mostly on well draining soils and in bioclimatic conditions ranging from semiarid to subhumid. In semiarid areas, wild olive trees can also grow beside ephemeral streams called Oued in the Maghreb and Barrancos in the Iberian Peninsula (Bensettiti and Lacoste 1999), as seen in Northern Africa and Southern Spain. Their analysis (Fig. 3) allows an interpretation of why some of the subfossils from supposedly two different habitats have such high calculated values of “hydraulic conductivity”. A riparian habitat alone can explain high “vessel conductivity” values in terms of ecophysiological and adaptive responses of wood growth to water availability. At the end of winter and early spring, temporary streams fed by abundant rain would have supplied growing olive trees with an added water supply and thus affected the spring wood growth. Interestingly, these samples also exhibited similar values of conductance to those of tropical species, such as O. capensis (see Plate 1) and O. perrieri, growing under humid to very humid conditions, from central, southern to eastern Africa, and in Madagascar respectively, (Fig. 3; Table 1). From both ecological and functional viewpoints, wood anatomy in Olea could be considered a dynamic compromise between water transport efficiency and structural support (Bass et al. 1988). These fea- 3162 NOTES Ecology, Vol. 85, No. 11 TABLE 2. Bioclimatic context and plant associations of Olea europaea subsp. europaea populations from which wood samples were collected for quantitative anatomical analysis. Bioclimatic context† No. Station (population) Modern olive trees growing in typical conditions La Clape (France) 1 Teulada (Spain) 2 Montroy (Spain) 3 Les Baux (France) 4 Frontignan (France) 5 St. Jean de Védas (France) 6 Nyons (France) 7 Remoulin (France) 8 Simat de Valldigna (Spain) 9 Quissac (France) 10 Cuers ‘France) 11 meso/dry meso/dry meso/dry meso/subhumid meso/subhumid meso/subhumid meso/subhumid meso/subhumid meso/subhumid meso/humid meso/humid 12 13 14 Sauve (France) Vic-le-Fesq (France) Crevillente (Spain) meso/humid meso/humid thermo/semiarid 15 16 17 18 19 20 21 22 23 24 25 26 27 Elche (Spain) Elda (Spain) San Juan de Alicante (Spain) Villajoyosa (Spain) Moraira (Spain) Dos Aguas (Spain) Sierra Parenchiza (Spain) Cabo de San Antonio (Spain) Gandía (Spain) Jara (Spain) Játiva (Spain) Monduber (Spain) Pego (Spain) thermo/semiarid thermo/semiarid thermo/semiarid thermo/semiarid thermo/dry thermo/dry thermo/dry thermo/subhumid thermo/subhumid thermo/subhumid thermo/subhumid thermo/subhumid thermo/subhumid Modern olive trees growing in riparian conditions Jorox (Spain) 28 29 Menzel (Tunisia) thermo/semiarid thermo/semiarid Plant associates Quercus coccifera, Q. ilex, Pistacia lentiscus Q. coccifera, P. lentiscus, Erica multiflora Q. coccifera, Q. ilex, P. lentiscus Q. ilex, Q. coccifera, J. oxycedrus Q. ilex, Q. coccifera, P. terebinthus Q. ilex, J. oxycedrus, P. terebinthus Q. ilex, Q. coccifera, P. terebinthus Q. ilex, Q. coccifera, P. terebinthus Q. ilex, Q. coccifera, P. terebinthus Q. ilex, J. oxycedrus, P. terebinthus Q. coccifera, Rosmarinus officinalis, E. multiflora Q. ilex, J. oxycedrus, P. terebinthus Q. ilex, Q. coccifera, J. oxycedrus Stipa tenacissima, Rhamnus lycioides, R. officinalis S. tenacissima, R. lycioides, R. officinalis S. tencissima, Pinus halepensis, R. lycioides S. tencissima, Pinus halepensis, Q. coccifera S. tencissima, Pinus halepensis, R. lycioides P. lentiscus, Chamaerops humilis, R. officinalis P. lentiscus, E. multiflora, Q. coccifera P. lentiscus, R. officinalis, E. multiflora P. lentiscus, C. humilis, R. officinalis P. lentiscus, C. humilis, R. officinalis P. lentiscus, C. humilis, R. officinalis P. lentiscus, Q. coccifera, P. halepenis Q. coccifera, P. lentiscus, R. officinalis Q. coccifera, P. lentiscus, R. officinalis Nerium oleander, Rubus ulmifolius, Q. coccifera N. oleander, Tamarix africana, Atriplex halimus N. oleander, T. africana, A. halimus thermo/semiarid Meknes (Morocco) 30 Note: see Table 1 for bioclimatic definitions. † Abbreviations are: meso, mesomediterranean; thermo, thermomediterranean. tures may have allowed Olea to adapt to different humidity levels, below 45° N. latitude. During the Last Glacial Maximum and possibly during other dry-glacial periods, wild olive trees would have survived in well protected areas, such as closed valleys and south-facing slopes. Riparian forests would have acted as ecological buffer zones maintaining a microclimate free from drastic temperature fluctuations. Riverbanks thus would have played a major role as refuge areas for Mediterranean taxa; olive trees could have grown alongside riparian taxa such as Salix, Populus, Alnus, and probably Nerium oleander, in warmer Mediterranean latitudes. By the end of the glacial episodes, these refuges would have facilitated the spread of olive into additional habitats. An initial rapid expansion of olive related to climatic warming (Terral and Mengüal 1999), could have been extended by human activities (Terral and Arnold-Simard 1996, Terral 2000). During the Holocene, olive trees retained their underlying riparian characteristics as shown by charcoal data from the Neolithic period, such as the sites of Buraca Grande, Cova de les Cendres and Giribaldi. NEW PERSPECTIVES ON THE ECOLOGY OF THE OLIVE TREE AND RELATIVES The evolution and distribution of Olea are closely linked to tectonic processes and climatic change. Recent phylogenetic studies support the hypothesis of an ancient segregation of the genus into two subgenera in Asia, Oceania and Africa. These studies also suggest an African origin for the O. europaea complex (Besnard et al., 2002b). As a result, we understand that the ancestral Miocene Eurasian Olea either had to decline or adapt to the Neogene environmental changes. By the Pliocene to Pleistocene transition, the Olea europaea complex might have assumed its current geographical November 2004 NOTES 3163 PLATE 1. Tranverse section of olive wood (Olea capensis L.; Cape of Good Hope, South Africa). Key to abbreviations: V, vessel section; PP, paratracheal parenchyma; R, biseriate ray; F, fiber. The thin section was prepared at the AMAP laboratory (Montpellier, France)and photographed by S. Ivorra (CBAE, Montpellier) range and genetic structure. Currently, Olea covers a broad ecological range from O. europaea subspecies well adapted to dryness, to species such as O. capensis and O. perrieri, able to grow under humid bioclimatic conditions (Fig. 3). In the northwestern Mediterranean areas, wild olive ultimately disappeared from riparian habitats, only surviving in dry and uncultivated locations apart from its cultivated descendants. At present, wild olive populations are sparse, owing mostly to human impact on FIG. 3. Predictive model of mean annual precipitation according to vascular conductivity ([vessel area/π]²/vessel density), based on wild olive trees (Olea europaea subsp. europaea) growing in typical modern ecological conditions. Data from (1) olive trees (O. e. subsp. europaea) growing in riparian conditions, (2) other Olea species and O. europaea subspecies, and (3) archaeological charcoal appear to be outside of the interpolation zone of the model. The positioning in the extrapolation zones may be explained by either the influence of climatic parameters (Olea species and Olea europaea subspecies) or edaphic conditions from archaeological charcoal. Abbreviations are: BG, Buraca Grande; CC, Cova de les Cendres; and GI, Giribaldi. 3164 NOTES the environment and shrinking primary plant communities (Lumaret and Ouazzani 2001). It has been assumed that the distribution of the cultivated olive tree coincides with that of the Mediterranean bioclimatic zone (Baldy 1990), which is characterized by hot and dry summers and humid winters. However, it now appears that the olive tree was capable of adapting to more diverse environmental conditions, particularly humidity, and more so than its present distribution might suggest. Consequently, the current distribution of olive should be interpreted not only in terms of Mediterranean climate, but also as a consequence of anthropogenic influence. We have demonstrated that ecophysiological interpretations from ancient fossil charcoal material from western Mediterranean can indicate a more complex history of this plant prior to being heavily influenced by cultivation and domestication. ACKNOWLEDGEMENTS We thank T. Aubry, J. Bernabeu, D. Binder, and H. Moura for permission to study the material from their archaeological sites. We are grateful to N. Chatti, L. Fabre and J.-C. Auffray, for their assistance during field work, and to N. Rowe and P. Vargas for extensive comments and discussion. We also thank S. Ivorra (CBAE, Montpellier) for her technical assistance. 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