Diagnosis and systematic position

The genus Gymnocarpos Forssk. is diagnosable against all the other European Caryophyllaceae with stipulate leaves (Walters 1993) by its terete, fleshy leaves and, more specifically, by showing: (1) opposite leaves (unlike Corrigiola L. and Telephium L.); (2) fruit without inflated peduncle (unlike Pteranthus Forssk.); (3) gynoecium trimerous, i.e. ovary tricarpellate and style trifid (unlike Herniaria L., Illecebrum L. and Paronychia Mill.); (4) sepals entire (unlike Loeflingia L.); (5) flowers apetalous (unlike Polycarpon L., Spergula L. and Spergularia (Pers.) J. Presl & C. Presl); and (6) stipules laminar, non-setaceous and fruits indehiscent, 1-seeded (unlike Ortegia L.).

Within its genus, Gymnocarpos sclerocephalus is unique for its annual habit and for the tightly clustered, partly connate in-florescences and infructescences (Fig. 1). It shares with the shrubby G. decander Forssk. the terete leaf-like bracts, so different from the large, scarious, Paronychia-like bracts of the rest of the genus.

Owing to its morphological distinctiveness, the species has often been classified in its own genus, Sclerocephalus Boiss., under the replacement name S. arabicus Boiss. (see, e.g., Chaudhri 1968; Petrusson & Thulin 1996), and as such it is still considered by Marhold (2011). However, molecular phylogenetics has been conclusive in showing that this species is deeply nested within Gymnocarpos (Oxelman & al. 2002; Jia & al. 2016).

According to the tribal system of Harbaugh & al. (2010), the most suitable suprageneric category for all these species is the tribe Paronychieae (the clade Gymnocarpos + Herniaria + Paronychia).

Ecological interpretation of diagnostic features

The above-mentioned generic and specific distinctive traits can be interpreted as the consequences of the ecological filtering imposed by an increasing aridity on more conventional Paronychia-like ancestors (Jia & al. 2016). The narrow, terete leaves and fleshy, green stems are easily cooled by wind to safe levels when stomata are closed under full sun and no transpiration takes place, their circular section also increasing the volume available to store rainwater and to diffuse the heat gained by radiation in the sun-exposed surface. In terms of water savings and survival, these two effects in combination more than compensate for the loss of specific leaf area. Similarly, the characteristic white hairs of the sepals (Fig. 1B, C) are likely to reflect sunlight and reduce thermal stress in the reproductive organs. Moreover, the mucronate apex of the leaves seems a way to facilitate morning dew to form falling droplets that the roots can absorb.

The tightly clustered infructescences and the apically spiny sepals suggest an efficient dispersal by epizoochory (Bittrich 1993: 214), explaining the particularly large geographical range of the species compared to other members of the genus and making still more plausible the full autochthony of the Spanish population. In can also be argued that seeds are protected within the spiny, dry heads and released only in response to rain (when the plant is more likely to complete its short cycle), in which case these unique infructescences can be interpreted as a mechanism of serotiny.

Fig. 1.

Gymnocarpos sclerocephalus – A, B: two individuals found in the rambla of Lanujar; note the heterogeneous, stony nature of the soil; C: close-up of the inflorescence; note the tightly clustered flowers, spiny bracts and sepals, and white hairs covering the sepals. – A–C: Spain, Almería, 17 Mar 2018, photographed by F. Le Driant.

Anything but an outlier

Gymnocarpos sclerocephalus was known to occur in a large area across the North African and Eastern Asian arid regions, from the Cape Verde archipelago to southern Iran (Fig. 3), and now must be added to the list of genera and species distributed mainly if not only in the Saharo-Arabian region and with their only European populations in the arid areas of southeastern Spain: Ammochloa palaestina Boiss., Anabasis articulata (Forssk.) Moq., Commicarpus plumbagineus (Cav.) Standl., Enneapogon persicus Boiss., Forsskaolea tenacissima, Hammada articulata (Moq.) O. Bolòs & Vigo, Ifloga spicata (Forssk.) Sch. Bip., Koelpinia linearis Pallas, Leysera leyseroides (Desf.) Maire and Notoceras bicorne.

Fig. 3.

Map created by combining the fragmentary or imprecise distributional information provided by the Global Biodiversity Information Facility ( https://www.gbif.org/) and the Catalogue of Life ( https://www.catalogueoflife.org/) with the general map in Jia & al. (2016). The red dot indicates the Spanish localities presented here.

The list grows substantially if mostly Saharo-Arabian xerophytic genera or even species well represented in southeastern Spain but with a few colonies in other European regions, mainly on Mediterranean islands, are taken into account: Androcymbium Willd. (with A. gramineum (Cav.) J. F. Macbr. in Spain and northwestern Africa and A. rechingeri Greuter in Crete and Libya); Apteranthes europaea (Guss.) Plowes (SE Spain and Sicily and across North Africa and the Near East); Cistanche Hoffamnns. & Link (with C. phelypaea (L.) Cout. along western Spanish and Portuguese Atlantic coasts and C. lutea (Desf.) Hoffmanns. & Link in southeastern Spain and across Saharo-Arabian areas); Cynomorium coccineum (southern Portugal, Ibiza, southern Corsica, Sardinia, Sicily, Basilicata, Malta and across arid regions of North Africa and Asia); Lasiopogon muscoides (Desf.) DC. (widespread in the deserts of southern Africa and across the whole arid belt of North Africa and southwestern Asia, from the Canary Islands to the Indus river, it reaches not only southeastern but also central Spain); Launaea Cass. (with up to 14 species across arid regions of Africa and the Near East, of which L. arborescens, L. lanifera Pau and L. nu-dicaulis (L.) Hook. f. occur also in southeastern Spain, L. fragilis (Asso) Pau and L. pumila (Cav.) Kuntze are more widespread across eastern Spain, the former occurring also in Sicily, and a 15^th species, L. cervicornis (Boiss.) Font Quer & Rothm., is endemic to the Balearic Islands); Periploca angustifolia Labill. (SE Spain, Sicily, islands south of Crete and across North Africa); Pteranthus dichotomus (southeastern Spain, Cyprus, Malta and across North Africa and southwestern Asia); and Volutaria Cass. (with ten species: two endemic to Morocco, two endemic to the Canary Islands and six widespread across North Africa, three of which occur also in Europe: V. crupinoides (Desf.) Maire in central Portugal, V. muricata (L.) Maire in southern Spain and V. tubuliflora (Murb.) Sennen in southern Spain and Sicily).

There are still quite a few species which, despite belonging to genera widespread in Europe, also have a wide Saharo-Arabian range and their only European localities in southeastern Spain: Achillea santolinoides Lag., Argyrolobium uniflorum (Decne.) Jaub. & Spach, Filago desertorum Pomel, Pallenis hierichuntica (Michon) Greuter, Plantago notata Lag., P. ovata Forssk. and Senecio flavus (Decne.) Sch. Bip.

So what explains the existence of such a contingent of desert flora in this corner of Spain, surrounded by areas with physiognomically and to a great extent also taxonomically standard Mediterranean flora?

Geology, climate and history collude to sculpt a unique landscape

The idiosyncratic summer drought of the Mediterranean belt, imposed by the northward expansion of the Azores High, is enhanced in these areas by the strong rain shadow of the Baetic mountains, whose highest massif, the Sierra Nevada (up to 3479 m a.s.l.), towers above the western edge of the Tabernas basin. The arrival of any substantial moisture from the Atlantic is hampered throughout the year, and total annual precipitation becomes very modest (around 200 mm on average, but below 100 mm in the drier years), evapotranspiration exceeding it by about fourfold. Precipitation is furthermore very irregular and unpredictable, much coming in short, heavy storms that physically erode the sparsely vegetated soils (Lázaro & al. 2004). Erosion disproportionately aggravates the water stress for plants and back-feeds the aridity of the region by reducing the capacity of soils to store water through the long sunny periods – this area receives the highest mean global daily radiation of continental Spain, above 5.3 kWh m^-2 day^-1 (Sancho & al. 2012).

A long history of aridity, dating back to the emersion of the Tabernas basin in the Pliocene (Alonso-Zarza & al. 2002), affects vegetation not only directly but also indirectly, insofar as it has contributed to generate and preserve unleached in the landscape large amounts of soluble evaporites with severe effects on plant development, both physical, as a result of superficial crusts and a too-strong adsorption of soil water, and chemical, because the abundance of certain ions hinders the absorption of essential nutrients and reduces the osmotic potential of soil water, further hampering its absorption by plants (Merlo & al. 2011; Moore & al. 2014; Escudero & al. 2015). In fact, Shmida (1985: 58–64) explored the strong links between desert and coastal flora as a consequence of the common effect of high ionic concentration in the edaphic solution.

However, it is possible that the striking desertic appearance nowadays predominant in this area is partly the result of human influence, and that a virtually continuous shrubland of sclerophyllous woody plants (syntaxonomically referable to the alliance Asparago albi-Rhamnion oleoidis) originally covered a substantial part of these slopes (Carrión & al. 2010). But such scrub revealed itself very fragile and was unable to recover fast enough from human destruction by fire and axe, spurred not only by pasturing but by the exploitation of esparto (Macro-chloa tenacissima (L.) Kunth) and by the demand for charcoal for smelting the products of ancient mining, all of which led to massive desertification and expanded the suitable habitat for all this strongly xerophytic flora, most likely restricted in the ancestral pre-Neolithic landscape to spots particularly dry for edaphic or topographic reasons (especially gypsum outcrops and saline marls; Mota & al. 2004).

Last but not least, the strong Föhn effect under nearly any wind regime and the low altitude and latitude of these arid regions of southeastern Spain, by almost eliminating frosts and by intensifying evaporation through consistently higher temperatures, strengthen their similarities with North African and Arabian deserts compared to other more northern or higher arid areas of Spain (Ebro, Tajo and Baza-Guadix basins). In these conditions, the flora of true warm deserts not only survives but thrives at the expense of both Eumediterranean and less thermophilous, xerophytic Irano-Turanian species. Data gathered in the period 1990–2004 at the Experimental Station of “El Cautivo” (Solé-Benet & al. 2008), 1.5 km to the east and some 60 m higher than the site of Gymnocarpos sclerocephalus, suffice to establish the exceptionality of this climate: 18.74°C of annual average temperature (45.5°C of absolute maximum, –1.5°C of absolute minimum, 34.5°C of average maximum in July) and average annual precipitation of 243 mm (115 mm in the driest year, and an average of less than 1 mm in July).

According to Shmida's (1985: 23) definitions, this area qualifies as a semidesert (annual precipitation below 400 mm but above 150 mm, figures conceived for regions with predominant winter rains). Such a label accurately conveys the striking physiognomic and floristic singularity of these southeastern Spanish areas, justifying the straightforward recognition of a distinct phytogeographic province (Murciano-Almeriense province) which, despite its remarkable similarities with Saharo-Arabian territories, is neatly included in the Mediterranean Region and, more precisely, in the West Mediterranean Subregion for its floristic background, for the nature of its connections with bordering provinces and for the fact that the most strongly subarid sectors are local and depend on topographic rather than on macroclimatic causes (Rivas Martínez & al. 2014).

Biogeography of the species: truly new to Europe?

Shmida (1985: 57) listed Sclerocephalus as one of the genera endemic to his “Sahara+Arabia” desert region, one out of many biogeographical proposals to reunite the continuous arid belt of Africa and southwestern Asia. Other systems (Rivas Martínez & al. 2017: 20) are less synthetic and distinguish, for instance, a Mediterranean northern Sahara from a tropical one. Gymnocarpos sclerocephalus occurs in both, as well as in other African and Asian regions considered to be bioclimatically and biogeographically different. Therefore, we prefer to use the less formal, more general term of “Saharo-Arabian” to summarize the large area occupied by the species.

In strict political terms, the genus and the species are new neither to Spain nor to Europe, since Gymnocarpos sclerocephalus is known at least from the Canary Island of Fuerteventura (Scholtz & Palacios 2015: 81, 87, 189), and its close relative G. decander from the islands of Fuerteventura, La Gomera, Gran Canaria, Lanzarote and Tenerife. But from a biogeographic perspective, is it clear that the Canary Islands are not part of Europe? It is indeed, because even admitting that the traditional idea of a “Macaronesian region” as opposed to the Mediterranean world is ill-founded, the occurrence of a number of palaeoendemic taxa and the outstanding concentration of taxa connected with eastern Africa as part of the so-called Rand Flora (Pokorny & al. 2015) put the Canary Islands considerably aside even from the otherwise marginally Mediterranean and by definition African adjacent Moroccan coasts. Therefore, Rivas Martínez & al. (2017), although including the Canary Islands in the Mediterranean Region, recognized them (with Madeira) as a separate subregion, the same rank assigned to the Maghreb Mediterranean, the Mediterranean Desertic Sahara and the West Mediterranean (significantly dubbed “Mediterranean Europe” and to which our population of G. sclerocephalus, as explained above, belongs).

As a more informal, pragmatic argument, the Canary Islands were excluded from the main initiatives to compile the floristic knowledge about the continent (Flora europaea, Atlas florae europaeae) and even about the whole Mediterranean Region (Med-Checklist). Only recently were they considered by the more comprehensive Euro+Med PlantBase (Euro+Med 2006+), as well as, most likely for purely normative convenience, by the European Red List of vascular plants (Bilz & al. 2011). More conclusively, Brummitt (2001: 37, 109) explicitly considered the Canary Islands as part of Africa.