Vallonea or Aegilops Oaks, a Short Review

Introduction

Oaks are a common and taxonomically diverse yet dominant element of many of the Northern Hemispheric forests and woodlands. The Near East is one of the major centers of speciation of the genus, presenting most old and new evolutionary lines (Zohary 1961 and 1973;  Denk and Grimm 2010; Hubert et al. 2014).

Their diversity has long attracted taxonomists and plant biogeographers (Linneaus 1753; Koch 1849; Kotschy 1862; Candolle 1864; Boissier 1879; Wenzig 1886; Camus 1938-39; Schwarz 1936; Zohary 1961; Menitsky 1972).The approach of each one towards the genus and its morphological complexity reflected the changing historical and technical context of their work. The result is often a plethora of names (Djavanchir-Khoie 1967) that confuse and hide important special aspects.

This applies in particular when it comes to the taxonomic categorization (species, superspecific ranks) of the different regional assemblages of oak species. The assemblage of the oaks known as the "vallonea oaks" or "aegilops oaks" from the Eastern Mediterranean and the Levant is a good case example.

The vallonea oaks

Currently most researchers recognize two or three species within this assemblage: Quercus brantii Lindl., Q. ithaburensis Decne., and Q. macrolepis Kotschy, with the latter sometimes treated as a subspecies of Q.ithaburensis (e.g., Med-Checklist of Greuter, Burdet and Long (1986)).

Recent molecular studies (Denk and Grimm 2010; Hipp et al. 2015; further unpublished data by A. Hipp, M. Simeone and coworkers) added new information regarding the vallonea oaks and their evolutionary significance.

Illustration from Monographie du genre Quercus by Aimée Camus: Quercus aegilops subsp. vallonea Kotschy and subsp. ithaburensis Decne.(click on image to enlarge)

The fact that the group has as its center of biodiversity in the lands of the Fertile Crescent, an area that is one of the major centers of human evolution – adds weight to this aspect.

The three species: (Q. brantii, Q.ithaburensis, and Q. macrolepis) differ in their morphological features from each other and from others, and by their very limited East Mediterranean and more widespread Near Eastern (Browizc 1978) occurrence and ecology (Dufor–Dror et al. 2004). They form a very distinct and clear, isolated, natural group – confirmed by nuclear sequence and phylogenomic data (Denk and Grimm 2010, see also Hipp et al. 2015) – within the Quercus Group Cerris, which has a much wider distribution, from East Asia to North Africa (according Denk and Grimm 2010).

All vallonea oaks share nine common features:

  1. The leaves of all the species in the group are relatively thick, coriaceous, almost xeromorphous, but large, densely tomentose (at least beneath) and often semi deciduous, persisting till the new growth flush or the distinctly whitish secondary summer flush.
  2. The blade forms are distinctly ovate, rarely lyrate, with large acuminate lobes and an aristate-mucronate, or even serrulate bristly margin.
  3. Secondary leaf veins are parallel, mostly lacking intercalaries.
  4. The acorns are large, among the largest in the genus, ripening biannually, inserted into a cup of large, thick, and distinct scales.
  5. The cupules are sessile or on a thick peduncle up to 5 mm long. The scales are large, broad, ligulate, loose,
    Quercus brantii leaves, from a specimen at Harold Hillier Gardens - © Jan de Langhe

    and reflexed, or rhomboidal, and tightly appressed.

  6. The three species recognized here are distinctly allopatric, native to semiarid habitats in the Fertile Crescent. They mostly grow into wide, low branching trees that form single-species-dominated communities of open, park-like woodlands.
  7. All species are deciduous, xero-thermophylic and limited to low elevations, mostly on limestone- or basalt-derived alkaline soils in Southwestern Asia or the Eastern Mediterranean countries, rare or lacking on the Mediterranean Islands.
  8.  Acorns of all species have high content of nutritionally valuable materials; and the cupules are rich in tannins.
  9. All were domesticated early by local populations for human consumption and hog feeding, tanning, and tool making, with profound implications for their modern distribution.

A short history

Theodor Kotschy, who travelled extensively in the Near East during the first half of the 19th century and collected many oaks, was the author of the names of most species from this group. The specimens he collected

Illustration of Quercus vallonea by Carl Horegschj from Kotschy's Die Eichen Europa's und des Orient's

are now deposited in herbaria across Europe where I was able to check them. Kotschy also comments in great detail on their affinities with other species. He was the one who coined the term "vallonea" for one of the species known in the trade of his time for tanning and black dye production. In his monumental treatise on oaks (Kotschy 1862) he described 40 species, among them 18 new ones. He "named" many more species from within this group among his many herbarium sheets that he sent to the major European herbaria and his sponsors.

Candolle (1864) in his comprehensive treatment of the genus as a whole, recognized most of the species published by Kotschy, but placed them in one large group, Section Lepidobalanus Endl., that included both deciduous and evergreen, as well as pubescent and glabrous species from all over Eurasia.

Boissier (1879) moved some of the deciduous species of Candolle’s Section Lepidobalanus group into subgenus Cerris Oerst., without distinguishing between them and the glabrous species like Q. libani Oliv. or Q. look Kotschy. The only species Boissier retained from among the earlier published ones (Kotschy 1862) in the vallonea group were Q. ehrenbergii Kotschy and Q. aegilops L., to which he added Q. look, Q.brantii, and Q. persica Jaub et Spach. The species Q. macrolepis, Q. ithaburensis, Q. pyramy Kotschy, Q. ungeri Kotschy, and Q. vallonea Kotschy were all regarded by Boissier as equivalent to forms of Q. aegilops.

Schwarz (1936) emended Reichenberg’s (1832) delimitation of this assemblage of three species (macrolepis, brantii, and ithaburensis) as the section Aegilops. However his separation of the Mount Tabor oak as evergreen

Quercus macrolepis Kotschy - Photo: © Michael Avishai

(Series Suberiformes) from the two others as deciduous (Series Vallonea) is mistaken: all three are deciduous.

Zohary (1961) followed the sectional delimitation of Schwarz.

Menitsky (1972 and 1984, in Russian; and in the 2005 English translation) treats the vallonea oaks as part of the Section Cerris in his Subsection Cerris (Dumort) Guerke. While he grants Q. aegilops the status of typus for the parallel Subsection Aegilops (Reichenb.) Menits., he includes among the species of the Subsection both the Far Eastern Q. acutissima Carruth. and Q. variabilis Blume as well as the Middle Eastern Q. libani, Q. trojana Webb, Q. brantii, and Q. aegilops.

In Q. aegilops he includes, as the first of two subspecies, subsp. aegilops (the vallonea oaks: Q. vallonea, Q. ehrenbergii, Q. macrolepis, and Q. graeca Kotschy) and as the second, subsp. ithaburensis Decne.: Q. goedelii Kotschy, Q. pyrami Kotschy, Q. ungeri Kotschy, and (as a hybrid with Q.libani) Q. look.

Vallonea oaks in the light of modern research

The lack of a personal familiarity with the situation in the field and the great morphological variability of the group resulted in much confusion regarding the status granted to many of the taxa and their putative synonymy.

Quercus ithaburensis Decne. - Photo: © Michael Avishai

The lack of a clear taxonomic framework further confused later researchers with similar experience studying the group (e.g., Mouterde 1966). Mouterde determined samples (checked by me with many others at herbaria in Geneva, Paris, and Kew[1]) from Lebanon as hybrids, although they represented distinct species. Ecology and climatic conditions are a main aspect regarding the distribution of the species in the same area. Dufour-Dror and Ertas (2004) show that the climatic niches of Q. macrolepis and Q. ithaburensis differ profoundly. However, Strid (2016) referred to Quercus macrolepis as a subspecies of Q. ithaburensis.

The results of recent phylogenetic molecular studies also shed new light on the group and their evolutionary position. Q. macrolepis and Q. brantii share unique sequence variants of the nuclear-encoded 5S rDNA intergenic spacer differentiating them from other members of the Group Cerris in western Eurasia (Denk and Grimm 2010). Newest phylogenomic data (single-nucleotide polymorphism data) obtained using next-generation sequencing, recognized a clade within the Group Cerris comprising the three vallonea oaks (Hubert et al. 2014; Hipp et al. 2015). Further analyses using a larger sample of individuals and additional plastid data are on the way (A. Hipp, M. Simeone, pers. comm. 2016).

Assessment of the genetic diversity (Schiller 2016) of populations of Q. ithaburensis in Israel also indicates a differentiation of this species according to geo-climatic conditions and to the intervention of man in the distribution of the species in Israel.

Finally, the discontinuous range of the three species on land and sea (they are of cultivated origin or missing from the smaller Central Mediterranean islands and the island of Cyprus (Meikle 1985), and are quite rare on

Illustration from Monographie du genre Quercus by Aimée Camus: Quercus aegilops subsp. brantii Lindl., subsp. pyrami Kotschy, subsp. ungeri Kotschy and subsp. look Kotschy.

Crete (Strid and Tan 1997; Strid 2016)) in the region and their distinctive ecology, holds the key to one of the most interesting stories in the evolution of oaks: their dispersal and domestication by early man in the Fertile Crescent.

The world in which we live changes continually, reshaping the distribution of plants. When tectonic events in Greenland brought about an extensive glaciation (Steinberger et al. 2015), the once very rich warm temperate flora (Grímsson et al. 2015) was eliminated. The last oaks (probably white oaks) vanished from the northern North Atlantic about 8-9 million years ago (Denk et al. 2010).

In the Near East, the once continuous mid-latitude belt of oak species along the newly forming Paratethys (including the putative ancestors of Ilex and Cerris oaks) from East Asia to Europe and North Africa, was interrupted by a series of orogenies related to the northward movement of the African and Indian Plates, from the early Eocene onwards, eventually leading to substantial drying of large parts of (central) Eurasia. The last vast central Eurasian inland sea, the remnant of the West Siberian Seaway, was eliminated (Akhmetiev and Beniamovski 2009; Akhmetiev et al. 2012) and its former area turned into the Central and Southwest Asian desert biome area. The once continuous mid-latitude, more or less humid forest belt vanished, opening a wide gap between the warm temperate Cerris and Ilex oaks of the southern foothills of the Himalayas and their relatives of the Near East, Southern Europe, and North Africa.

But on the coastal and inland areas, affected by the relatively warm Mediterranean winter rainfall belt, some of the surviving Cerris oaks were apparently able to re-radiate and evolve into a new oak assemblage.

The westernmost occurrence of Q. macrolepis in the province of Puglia is most probably due to the introduction by Greek settlers. Their absence from the native floras of the large, more ancient Mediterranean Islands like Sicily (Pignatti 1982) or Cyprus (Meikle 1985), where other species of oaks are quite common, is well

Herbarium specimen collected by E. Psarides in 1852 as Quercus aegilops L. var. portugalussa Halácsy, revised by O. Schwarz as Q. macrolepis in 1935.

documented. Even on Crete, where Q. macrolepis was originally described by Kotschy, this species is limited to a relatively small area on the fertile plains south of Rethymion (Zohary and Orshan 1966; Zohary 1973), or rare (Strid 2016). Here it was most probably introduced by man together with olive, fig, and other crops. Stands recorded by Zohary and Orshan occur from sea level to 700 m under ecological conditions similar to those of the Q. ithaburensis community in Israel.

However the climatic preferences of Q. macrolepis and Q. ithaburensis differ and under the selective pressure of the relatively modern semi-arid niches they occupy, the vallonea-aegilops assemblage started to evolve from refugia after the end of the Miocene and once the Pleistocene glaciations started to retreat. In Israel the existence of deciduous woodlands of Q. ithaburensis on basalts of relatively recent origin (Avishai 1966; Browicz 1978) can perhaps also indicate the short, very recent time span under which this distinctly novel vallonea group dispersed and evolved.

The novel insights into the significance of acorns as food of early man (Kremer, 2015; Schiller 1916) give the evolution of the group an additional twist: dispersal and domestication by early man. The fact that this aspect was not appreciated correctly in the past is no doubt related to the insufficient understanding of the early effects of human societies on forests and woodlands (see also Pervolotsky and Haimov 1992). While considerable work has been directed towards the domestication of the modern crop plants, the materials of ancient pre-agriculture, the lower Paleolithic hunting and gathering cultures, like the Natufian Culture are getting serious attention only recently. The relatively large acorns of the vallonea-aegilops species assemblage native to the lands of the Fertile Crescent are an excellent example. Tumuli and cairns on the Golan Heights, built to improve tree fertility by Calcolithic cultures (Kaplan 2005), point in this direction. The easily roasted and consumed almonds, walnuts, and pistachios replaced them in many parts of the Near East. But Bedouins, to this day, in some areas still mark, preserve, and protect high-yielding trees (Eliav 1985). These oaks could have an important function as a transitional nutritional element that is easy to collect, store, and transport. But because of the advantages of more modern crops, acorns disappeared from this stage, giving way to the more efficient settled stage's cereals and legumes that replaced them later in the human diet.

The species of the vallonea assemblage are well adjusted to the rapidly changing and fluctuating climate of the postglacial era. The pattern of their dispersal confirms very well the migratory pattern of early human societies from 40,000 years BP. What was correct for the species of Subgenus Quercus (Kremer, 2015) would also most likely be so for this assemblage of large-sized acorns – perhaps even earlier and more so!

Evidence for acorn consumption is not lacking (Deforce et al.2009; Lerch 2005; Dubreuil and Nadel 2015). If hydrocyanic acid was not an obstacle to the domestication of almonds, tannic acid was not one for oaks, but the ease of grafting was. That was the reason that oaks were soon overtaken by the more modern, better-yielding fruit, cereal, and pulse crops.

The absence of these species from the diet of populations of the much later settled islands also proves this point.

Man left his imprint on the morphology, distribution, and evolution of the vallonea oaks.

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[1] Conservatoire et Jardin botaniques de la Ville de Genève ; Muséum national d'histoire naturelle, Paris ; Royal Botanic Gardens Kew