Late persistence and deterministic extinction of “humid thermophilous plant taxa of East Asian affinity” (HUTEA) in southern Europe

https://doi.org/10.1016/j.palaeo.2015.08.015Get rights and content

Highlights

  • we examined the fossil record of extinct plant taxa in Europe persisting in East Asia;

  • we provided new data about the minimum mean annual temperature tolerated by living East Asian plants;

  • we showed that the "humid thermophilous plant taxa of East Asian affinity" (HUTEA) have an early Pleistocene record in southern Europe;

  • our fruit and seed data testify for a stepwise mass extinction of terrestrial plants in southern Europe from 4 to 0.5 Ma;

  • two main collective disappearance events coincide with well-known intervals of major climatic deterioration: 2.7-2.4 Ma and 0.9-0.8 Ma.

Abstract

Several terrestrial plant fossils found in the late Cenozoic of Europe belong to thermophilous genera or infrageneric taxa which do not grow in this continent today, and are usually called “exotic elements”. Within this large group we singled out three more precisely defined categories based on the hypothesis that the change of geographic distribution between the late Cenozoic and the present is the result of deterministic extinctions caused by climate change. Among the taxa shared by the modern East Asian and the Plio–Pleistocene European flora, the “humid thermophilous taxa of East Asian affinity” (HUTEA) represent the central category in our study. These were traditionally considered “Pliocene” elements in Europe. In our analysis of 13 reliably dated Italian assemblages the percentage of species belonging to the HUTEA category was found to be higher in Pliocene sites, and very low to null in Pleistocene ones. Also early Pleistocene assemblages across all of Europe did not contain any HUTEA, apart from Eucommia, and Symplocos sect. Lodhra in the refugial area of the Colchis.

Our analysis of fruit and seed assemblages in the San Lazzaro section (Umbria, central Italy), recently assigned to the early Pleistocene, provided contrasting evidence, which required a reconsideration of the stratigraphic and palaeontological context of another well known site in central Italy, Cava Toppetti II. Using vertebrate and continental mollusc biochronology the early Pleistocene age of this section was confirmed and its palaeontological records were compared with other assemblages in central Italy and Europe. We show that in central Italy at least three HUTEA species (Sinomenium cantalense, Symplocos casparyi, Toddalia rhenana) persisted after the Pliocene/Pleistocene boundary. We conclude that central-southern Italy offered a refugial niche that was warm and wet enough to assure the longer survival of some HUTEA, in contrast to central Europe.

Introduction

In the course of the stratigraphical and palaeontological study of the San Lazzaro section in central Italy (Fig. 1), recently assigned to the early Pleistocene (Baldanza et al., 2014), one of us (A.B.) found an endocarp of Sinomenium cantalense. The finding of this species, readily assignable to the humid thermophilous taxa of East Asian affinity, in an early Pleistocene section was the starting point for further collecting efforts to find evidence for the role of central Italy as a centre of refuge for such thermophilous taxa in the Plio–Pleistocene (Martinetto, 2001a). In this paper we adopt the definition of the Pliocene and Pleistocene of Gibbard et al. (2010), with the boundary fixed at 2.6 Ma, and we accept their indication for the chronologic boundaries of the four stages Zanclean, Piacenzian, Gelasian and Calabrian. Therefore, the terms middle Pliocene, late Pliocene and early Pleistocene used in previous works (among others, Ambrosetti et al., 1995a, Ambrosetti et al., 1995b, Abbazzi et al., 1997, Martinetto, 2001a) have a chronologic connotation which differs from that adopted here.

It is well known that many plant fossils found in the late Cenozoic of Europe belong to thermophilous genera or infrageneric taxa which do not grow in this continent today (Mai, 1989, Qian et al., 2006, Rodríguez-Sánchez and Arroyo, 2008). Such fossils are usually called “exotic elements” (Reid, 1920) and this concept corresponds more or less with “extinct plants” for the Plio–Pleistocene interval (Svenning, 2003). The climatic requirements are not considered in the definition of both exotic and extinct; however, several attempts have been made to assign the exotic (or extinct) elements to a few distinct plant groups that involve a climatic characterization and/or a phytogeographic aspect (Mai, 1989, Mai, 1991, Mai, 1995a, Grichuk, 1997, Grímsson et al., 2015). Examples of names which have been used include: “Palaeotropical flora/element”, “Arcto-Tertiary” or “Arctotertiary flora/element” (Engler, 1879–1882, Mai, 1989, Mai, 1991, Grímsson et al., 2015), “subtropical elements” (Mai, 1970, Zagwjin, 1990), “Mastixioideen” (Kirchheimer, 1957, Mai, 1964), “Boreotropical flora” (Wolfe, 1975), “Taxodiaceae group” (Bertoldi et al., 1994), “Tethyan plants (or Tethys flora)” (Szafer, 1961, Mai, 1989, Rodríguez-Sánchez and Arroyo, 2008), “Mega-mesothermic elements” (e.g. Popescu et al., 2010), and “humid subtropical elements” (Bertini and Martinetto, 2011). All these names leave some uncertainty as to what is included and what is excluded from the definition, firstly because the phytogeographic information, both past and present, is superimposed to, and variously interfingers with, the climatic one, and secondly because of the very difficult, not unambiguous, climatic characterization of the fossil-taxa (Kvaček, 2007, Grimm and Denk, 2012, Utescher et al., 2014). Also the modern reference models may be ambiguous, for example the qualitative term “subtropical” is used with very different temperature boundaries by Chinese (e.g. Hou, 1983) and Japanese authors (e.g. Kira, 1991).

The different extant distribution of plant taxa that grew together in the Cenozoic of Europe have often been given considerable relevance in the analysis of palaeofloras (see Reid and Reid, 1915, Szafer, 1961, Mai, 1964, Mai, 1989, Mai, 1995a). However, in our opinion most previous analyses and descriptions of the floral change in the Plio–Pleistocene of Europe suffered from the lack of precisely defined categories whose chronological analysis would adequately point out timing and entity of the large Plio–Pleistocene mass extinction (Tallis, 1991, Svenning, 2003). Additionally, the descriptions of Plio–Pleistocene floral changes mostly relied on pollen data (e.g. Tzedakis et al., 2006, Postigo-Mijarra et al., 2009, Magri, 2010, Orain et al., 2013), particularly in Italy (Bertini, 2010, Combourieu-Nebout et al., 2015). However, by combining pollen and carpological records (Bertini and Martinetto, 2011) it was noticed that pollen assemblages mainly reflect anemophilous plants, whilst they do not accurately represent the assemblages of “subtropical humid forest” type (sensu Hou, 1983, and Bertini and Martinetto, 2011), which are very rich in entomophilous plants and were present in southern Europe right at the time when major extinction events are hypothesized (Martinetto, 2001a, Bertini, 2010, Bertini and Martinetto, 2011, Biltekin et al., 2015, Combourieu-Nebout et al., 2015). As recently confirmed by Goring et al. (2013), taxa that are pollinated by insect or animal vectors (entomophilous or zoophilous, respectively), and species with limited dispersal ability are rarely recorded in fossil pollen records. Some works on modern fruit and seed assemblages (e.g. Thomasson, 1991, Vassio and Martinetto, 2012 and references therein) indicate a less biassed representation of plant diversity, in particular for several enthomophilous (e.g. Actinidia, Frangula, Paulownia, Rubus, Sambucus) and herbaceous plants (e.g. Ajuga, Cyperaceae, Hypericum, and Potamogeton). For these taxa, the plant elements that enter the fossil record and allow species-level identification are fruits and/or seeds. Thus, the works which exclude carpological data definitely underestimate past plant species diversity and the extent of Plio–Pleistocene plant extinctions, and the focus of this paper will be on fossil fruits and seeds.

The analysis of the San Lazzaro material led us to reconsider the bulk of information accumulated for the Italian late Cenozoic fruit and seed assemblages in the last 30 years (in particular: Gregor, 1990, Martinetto, 1994, Martinetto, 1995, Martinetto, 1999, Martinetto, 2001a, Martinetto, 2001b, Martinetto, 2009, Martinetto, in press, Bertoldi and Martinetto, 1995, Mai, 1995b, Basilici et al., 1997, Fischer and Butzmann, 2000, Ghiotto, 2010, Martinetto et al., 2007, Martinetto et al., 2015). Consequently, we felt the need to introduce precisely defined categories, which would permit us to better appreciate the chronological steps of the dramatic southern European floral change in the Plio–Pleistocene. One of the necessary operations was to combine in a clear manner the modern phytogeography and the climatic requirements of several taxa. Therefore, we focused on geographical and ecological characteristics of modern relatives of fossil taxa: partly shared geographic range, minimum thermic tolerance and moisture requirement. Since the geographic area where most of the “exotic” taxa of the European late Cenozoic are still living today is definitely East Asia (Tralau, 1963, Martinetto, 1998, Qian et al., 2006, Manchester et al., 2009), we considered it to be important for the definition of the new categories.

The taxonomic similarity between Neogene European floras and modern East Asian ones is rooted at least into the Miocene (Mai, 1989). As known from various studies at global and regional scales, Cenozoic climates were generally warmer and more humid than at present, and were characterized by shallow latitudinal gradients (Utescher et al., 2011 and references therein). Several authors (Bruch et al., 2011, Liu et al., 2011, Xing et al., 2012, Jacques et al., 2013) pointed out that the climate was wetter and warmer than the present one during the Miocene in both central Europe and China. Even central and northern Eurasian areas, such as Kazakhstan (Bruch and Zhilin, 2006) and Siberia (Popova et al., 2012), were wetter and warmer during the Miocene, despite the relatively higher seasonality and continentality.

This climatic situation was probably suitable for the formation of latitudinal vegetation belts with a similar floristic composition in both western and eastern Eurasia (Mai, 1989, Mai, 1991, Kovar-Eder et al., 2008), and strong floristic affinities with East Asia have also been encountered for North American floras (Liu and Jacques, 2010, Huang et al., 2014). Several authors explained that the modern East Asian woody flora is richer than the European (and North American) one (e.g., Kubitzki and Krutzsch, 1996, Manchester, 1999, Wen, 1999, Tiffney and Manchester, 2001, Wen et al., 2010) mainly due to a minor impact of extinctions, even if several woody species got extinct also in East Asia during the Plio–Pleistocene (Momohara, 2015).

Some close relatives of most European extinct species were already present in the warm temperate belt of East Asia before the Pliocene (e.g., Cathaya, Cephalotaxus, Craigia, Cryptomeria, Cyclocarya, Eucommia, Ginkgo, Glyptostrobus, Pseudolarix, Taiwania: Manchester et al., 2009) or possibly migrated there during the Pliocene (e.g., Hemiptelea, Rehderodendron: Manchester et al., 2009), and could survive the Pleistocene climatic crisis because of the presence of niches that were wet (atmospheric humidity) and warm enough, even in sites not related to rivers and swamps. Based on the concept of “physiological uniformitarianism” (Tiffney and Manchester, 2001) we can assume that the climatic tolerances of the living relatives of Neogene European taxa that survived in the humid and warm temperate to tropical areas of East Asia roughly correspond (maybe only in part) to those of the extinct European forms of the same genus, subgenus or section.

Svenning (2003) pointed out a deterministic effect in late Cenozoic plant extinctions and recognized three important groups of taxa for the analysis of the ancient European floras: 1) widespread taxa; 2) relictual taxa; 3) extinct taxa. In referring to extinct taxa, Svenning (2003) restricted his analysis to cool-temperate tree genera, but recently Eiserhardt et al. (2015) carried out an analysis on more thermophilous plants. Actually, several Plio–Pleistocene taxa occurring in Europe are more thermophilous than “cool-temperate” (Martinetto et al., 2015) so that we now consider it important to single out a new group of thermophilous taxa with a partly shared (as for eastern Asia) current distribution outside Europe and a common, definite climatic boundary. The thermophilous characterization of several European fossil-species is provided by the minimum Mean Annual Temperature (MAT) requirement of their modern relatives (Table 1).

Consequently, we define as “HUmid Thermophilous extinct European taxa of East Asian affinity”, in short HUTEA, those plant taxa which have well-documented fossil records in the late Cenozoic of Europe, which do not grow spontaneously in this continent and West Asia at present (unless as aliens), which do not tolerate a MAT below 8 °C and a Mean Annual Precipitation (MAP) below ca. 800–1000 mm/year, and which belong to genera or infrageneric taxa that presently grow in East Asia (Wang, 1961, Qian et al., 2006, Fang et al., 2009, Fang et al., 2011, Manchester et al., 2009, Grimm and Denk, 2012, Eiserhardt et al., 2015, Utescher and Mosbrugger, 2015).

We single out the 8 °C value of MAT because this is the boundary of the distribution of boreal (subarctic) and thermophilous (temperate) taxa in East Asia. The upper limit of fir and spruce forest and the lower limit of deciduous forest is 7.8 °C MAT in China (Fang and Yoda, 1989). Although the lower MAT limit of the thermophilous evergreen arboreal Fagaceae and Lauraceae (dominant tall trees of temperate broadleaved evergreen forests in East Asia) is between 9 and 12 °C (Hattori and Nakanishi, 1985, Fang and Yoda, 1989, Fang et al., 2011), we decided that adding 1 °C of tolerance would admit sporadic occurrences of thermophilous plants above the 9 °C MAT isotherm.

The focus on MAT for the definition of the HUTEA is justified by the large availability of data (Grimm and Denk, 2012, Utescher and Mosbrugger, 2015) for most of the plant genera documented by fossils in Europe, and by the determinant role of this parameter for plant extinction or survival in the late Cenozoic of Europe (Svenning, 2003, Eiserhardt et al., 2015). Conversely, we did not manage to gather precise values of minimum precipitation requirements for all the exotic Neogene plant taxa of Europe; nevertheless we consider important to include in the HUTEA definition a rule that excludes those plants which tolerate a low precipitation (below ca. 800–1000 mm/year). In fact it has been pointed out that the extinction of several Neogene taxa in Europe depended from a scarce tolerance not only of low temperature, but also of low precipitation (Svenning, 2003, Eiserhardt et al., 2015). The thermophilous genera that survived in southern Europe until the present time (e.g. Laurus, Olea) are mainly adapted to dry (Mediterranean) climate, whereas several thermophilous genera extinct in Europe are now growing in areas affected by the East Asian Monsoon that supplies higher precipitation to plants during the growing season. In East Asia the main evergreen forest formation, dominated by Fagaceae and Lauraceae, is called “lucidophyllous forest” and differs from the south European (Mediterranean) sclerophyllous forest formation by its less xeromorphic characteristics, such as larger shiny leaves, larger tree size and higher species diversity with many epiphytes and woody lianas (Kira, 1991).

We are aware that other parameters (e.g. Warmth Index, Coldness Index; Kira, 1991) could be more appropriate to define a category such as HUTEA. Nevertheless, the minimum MAT requirement is an important factor determining the possibility for a plant taxon to overcome a climatic bottleneck. The climatic characteristics of the refugia might have been decisive for the possibility of a plant species to survive (Magri, 2010, Gavin et al., 2014) and obviously it would have gone extinct if its minimal thermal or humidity requirements would no longer have been present in the last refugium. In this respect, groups of taxa with similar requirements may be expected to go extinct together (Tallis, 1991, Grichuk, 1997, Eiserhardt et al., 2015), given that the MATmin of the refugia created a bottleneck for all of the plants growing there. However, some extinctions have certainly been controlled by complex and multiple factors. For example it has been suggested that Cedrus (Su et al., 2013) and Sequoia (Zhang et al., 2015) disappeared from China because of seed ecological aspects, triggered by climate change.

Three examples, concerning genera which do not tolerate a MAT below 8 °C (Table 1), may be useful to support the above definition of HUTEA: Toddalia is assigned to the HUTEA because it is distributed in the tropical–warm temperate zone of East Asia and in Africa, but not in Europe and West Asia (Gregor, 1979). Symplocos sect. Lodhra is assigned to the HUTEA because it is distributed in the tropical–warm temperate zone of East Asia, but not in Europe and West Asia (Fritsch et al., 2015). Rehderodendron is assigned to the HUTEA because it is distributed only in the “subtropical” zone (sensu Hou, 1983) of East Asia.

The genera Cathaya and Pseudolarix meet all the requirements to be classified as HUTEA, but they are excluded for their present highly relictual distribution, which may provide an inaccurate representation of their past climatic requirements, similarly as for Tetraclinis (Kvaček, 2007). Even if the distribution of Amentotaxus is similarly relictual, we temporarily decided to consider it a HUTEA. Azolla is not considered a HUTEA because it is a water plant rather independent from atmospheric humidity.

According to the above definition and to the data (e.g., minimum thermic requirements: MATmin) reported in Table 1, the following HUTEA have so far been documented for the late Cenozoic of Italy (Martinetto, 1995, Martinetto, 1998, Martinetto, 1999, Martinetto, 2001a, Martinetto, 2001b, Follieri, 2010, Martinetto et al., 2015): Amentotaxus, Cinnamomum, Craigia, Cyclea, Cyclocarya, Ehretia, Engelhardia, Eucommia, Glyptostrobus, Mallotus, Meliosma subgen. Kingsboroughia, Paulownia, Rehderodendron, Sabia, Sargentodoxa, Saurauia, Sinomenium, Stemona, Symplocos sect. Lodhra, Taiwania, Ternstroemia, Tetrastigma, Toddalia, Trichosanthes, Turpinia and Wikstroemia.

Other taxa documented in the late Cenozoic of southern Europe have the correct geographic distribution nowadays to be considered HUTEA (i.e. embracing East Asia and excluding Europe and West Asia), but they are not considered, because the modern representatives do tolerate a MAT below 8 °C (e.g. Actinidia, Alangium, and Ampelopsis: Table 1). These taxa will be named CTEA (“Cool-Tolerant extinct European taxa of East Asian affinity”) in this paper and belong to the somehow ambiguous [changing on the basis of the extent of territory considered] category of the “exotic” taxa (Reid, 1920; see the more precisely defined “category E” in Martinetto, in press).

The HUTEA category already has a satisfactory climatic connotation, which we deem to be useful for an analysis of the climatic determinism in their extinction. Conversely, the CTEA category certainly contains a very heterogeneous mix of species with different climatic tolerances. In fact, Magnolia provides a good example of a cool-tolerant CTEA genus that contains several modern species (Grimm and Denk, 2012, Utescher and Mosbrugger, 2015), which are absolutely thermophilous and not cool-tolerant (tropical–subtropical). Similarly, a diversified climate tolerance has been also hypothesized for different European fossil-species (Mai, 1975). Given this situation, it is unsurprising that several CTEA would show a HUTEA-like extinction pattern. However, in this paper our attention has been focused on the species that show a delayed disappearance time in comparison to the HUTEA.

Finally, a few taxa which do not tolerate a MAT below 8 °C are not assigned to the HUTEA because of the modern geographic range: Coriaria, Datisca, Ficus, Laurus, Liquidambar, Morella, Ocotea, Olea, Platanus, Sideroxylon, Styrax, Tetraclinis and Visnea grow in southern Europe, North Africa (incl. Macaronesia) and/or West Asia. These taxa will be indicated as TEWA, Thermophilous European, West Asian and/or African elements, in this paper. Pterocarya, Parrotia and Zelkova are not assigned to the HUTEA nor to the CTEA or TEWA, because they grow in relict niches of south-eastern Europe and/or West Asia (southern shores of the Black Sea and Caspian Sea), commonly including sites with a MAT below 8 °C.

Finally, late Cenozoic south European taxa that today only survive in America are not many (Decodon, Dulichium, Leitneria, Proserpinaca, Sequoia, Taxodium) and will not be specifically dealt with in this paper.

It is apparent that the HUTEA and CTEA concepts have much to do with a change of geographic distribution between the Plio–Pleistocene and the present. The main aim of this work is to present new fossil data from Italy and an updated state-of-the-art regarding the timing of disappearance of HUTEA and CTEA species from Europe. Furthermore, we newly consider the possibility of deterministic extinctions (Svenning, 2003, Eiserhardt et al., 2015).

Section snippets

Geological setting

The post-Miocene, NW–SE oriented South Valdichiana Basin (Fig. 1), enclosed between the Meso-Cenozoic Rapolano-Mt. Cetona and Narnese-Amerina Apennine anticlines and bounded by extensional faults, occupies a wide area between south-eastern Tuscany and western Umbria, in central Italy. In the Pliocene–Pleistocene interval, the Narnese-Amerina ridge separated the mainly marine domain of South Valdichiana from the continental deposits of the Southern Tiberino Basin (Fig. 1, Fig. 2), whilst, during

Materials and methods

This work integrates the analysis of freshly collected material from the San Lazzaro section with the reinterpretation of the stratigraphic and palaeontological data from the sites Cava Toppetti II (Abbazzi et al., 1997, Argenti, 1999, Argenti, 2004, Martinetto, 2001a, Petronio et al., 2003, Sardella et al., 2003) and Dunarobba (Ciangherotti et al., 1998, Manganelli and Giusti, 2000, Manganelli et al., 2008, Martinetto et al., 2014).

In the San Lazzaro section, as well as in the neighbouring

The San Lazzaro section and its age constraints

The composite sedimentological and stratigraphic reconstruction proposed for the Fabro Scalo area integrates old observations (Baldanza et al., 2011, Baldanza et al., 2014, Bizzarri et al., 2015) and newly collected data. The general geological and sedimentological pattern, from the base to the top, is organized as follows (Fig. 3):

  • about 10 m (cropping out) of structureless, mollusc-rich clayey and silty sand (offshore transition deposits); the lowermost layers are covered by recent alluvial

Discussion

Depending on the concepts of “physiological uniformitarianism” (Tiffney and Manchester, 2001) and deterministic late Cenozoic plant extinctions in Europe (Svenning, 2003) we singled out three groups of plant fossil-species occurring in southern Europe: CTEA, HUTEA, TEWA. The CTEA and HUTEA include several species extinct in Europe and belonging to supraspecific plant taxa with a modern distribution in East Asia. The HUTEA are the descendants of the “exuberant laurophyllous flora” (Kubitzki and

Conclusions

New data on early Pleistocene fossil fruit and seed assemblages from Italy allowed us to detect several extinct taxa that commonly went unnoticed in pollen analyses. The combined analysis of Pliocene and early Pleistocene occurrence data provided a detailed picture of the reduction of plant diversity in southern Europe. The possible explanation of the causes of plant extinction requires an excursion into deeper times: Several Neogene plants were mainly adapted to grow in thermophilous mesic

Acknowledgements

We thank G. Basilici for useful information and discussions about the stratigraphy of the Tiberino Basin and for help provided in the field for the positioning of the carpological sample within his Cava Toppetti II section. Thanks to A. Bertini for very useful information on pollen assemblages and for suggestions that improved the whole manuscript, which also profited from the valuable revision carried out by two anonymous referees that we wish to thank. We also thank A. Bruch, T. Denk, G.

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