Salvia ceratophylloides Ard. (Lamiaceae): A Rare Endemic Species of Calabria (Southern Italy)

Salvia ceratophylloides Ard. is a very precious narrow endemism of Southern Italy. It grows in the suburban surroundings of Reggio Calabria, on coastal strip hilly ridges between 250 and 450 m a.s.l. At the beginning of 1900, it was present in several localities, as evidenced by literature, where it was already very rare. Afterward, despite the research carried out by various botanists, the species was no longer found, due to its disappearing in the places mentioned in literature result-ing from the intense environmental transformations suffered by the territory. Therefore, the species since 1997 was included in the “Red Book of the flora of Italy” among the extinct species. The successive research carried out in 2008 made it possible to ascertain new localities at about 10 km of distance from those reported in the literature. The actual population consists of about 1000 individuals, and according to IUNC criteria, the conservation status is critically endangered (CR). The threats to survival and spread of the species are different, but above all, it is the habitat destruction due to urbanization to threaten this species.


Introduction
The genus Salvia has a cosmopolitan distribution and is probably the richest in species of the Lamiaceae family. Many species have considerable economic importance for medicinal, food, or ornamental uses. The authors that have dealt with this genus estimate that it contains between 900 and 1000 species [1,2]. The Mediterranean and Western Asia, with about 240 species, are one of the diversity centers of the genus Salvia [2]. The Italian flora includes 20 species of the genus Salvia [3] among which Salvia ceratophylloides Ard., is a rare endemism of a small hilly area close to the city of Reggio Calabria in Southern Italy (Figure 1).
Until 2008, Salvia ceratophylloides was considered "extinct in the wild" (EW) by the "Red regional lists of Italian plants" [4], by the "Atlas of endangered species" of Italian flora [5], and by authors who have studied the genus Salvia in Italy [6]. The intense urbanization of the areas surrounding the city of Reggio Calabria has led to profound changes in the landscape with the reduction, degradation, and disappearance of natural habitats. All this caused the extinction of the species from the places where it was collected until the beginning of 1900 by various authors [7].
Field surveys carried out in the last decade have, however, allowed us to verify the presence of the species in other localities and to define its taxonomic and ecological characteristics as well as the conservation status [8].
Salvia ceratophylloides currently occurs in small and isolated populations, which are expected to face extinction mainly due to the habitat destruction.
We present a study on the distribution, taxonomy, and conservation status of S. ceratophylloides, aimed at identifying the criteria for the management and conservation of this rare species of Italian flora.

Materials and methods
We define the distribution of Salvia ceratophylloides by several ways such as analysis of herbarium collections, literature data, and through a deep field investigation carried out from 2010 until 2018. To map the distribution, all sites of species were geo-referenced in the field and the coordinates archived in a geographical information system (GIS).
The morphological traits were measured on 10 herbarium specimens with a stereomicroscope. The specimens are kept at the "Mediterranea" University of Reggio Calabria Herbarium (REGGIO). To assess population size and the habitat, several surveys were carried out on the S. ceratophylloides biotope. Conservation status was assessed according to the IUCN Red List criteria [9], which is actually the more widely used in the world to assess extinction risk. The nomenclature of the species is according to [10].

Historical vicissitudes
The first news on this species dates back to the pre-Linnaean period and is due to Cupani [11], a Franciscan monk, an expert on Sicilian flora, who in his monumental work "Panphyton siculum" published the iconography and description of many species of Sicilian flora. The work published posthumously by the publisher Endemic Species 4 in 1713 [12] contains an iconography (t 186) clearly referable to Salvia ceratophylloides (Figure 2) that Cupani describes with the phrase "Sclarea verbenae petalis purpurates florae." Cupani described many species in his book that he collected spontaneously in Sicily, but also non-native, grown at the botanical garden of Misilmeri in Sicily, of which he was the curator [13]. This has created confusion in Sicilian botanists who for a long time have attributed this species also to the Sicilian flora [14].
Arduino for the description used plants grown at the Botanical Garden of Padua, obtained from seeds that received from a friend from Sicily as he says "Ex seminibus e Sicilia ab amico delatis, et in horto hoc nostro satis quinque anni sab hinc nata est." Also for this reason, Sicily was considered for a long time the place of origin of this species, although no one has ever collected samples in the wild. Arduino attributed to this sage the epithet "ceratophylloides" to highlight the similarity that in his opinion, this species has with Salvia ceratophylla L., a species distributed in the Irano-Turanian region absent in Italy (from the Greek εἷδος eidos appearance, resemblance). Arduino describes the species as: "Salvia ceratophylla sed luxuriantis similis; forte diversa ac distincta").
Arduino deposited the type specimens used for the species description, in its herbarium of Vicenza, which unfortunately was destroyed during the Second World War. He sent some herbarium samples to Linnaeus in 1763, still preserved at the Linnaean herbarium at London. The sample sent and inserted by Linnaeus in his herbarium No. 42.55 (Figure 4) shows the name of the species and connected to a list attached to some exsiccata sent by Arduino to Linnaeus. Lacaita [7] organized the taxonomic framework of Salvia ceratophylloides, clarifying the real place of origin of the species. He pointed out that the species has never been found spontaneously in Sicily and that the few specimens present in various herbaria are all coming from southern Calabria or from crops obtained by seeds always coming from these localities.
Lacaita [16] found that the samples named by Linnaeus as Salvia ceratophylla L. and by subsequent authors as S. ceratophylloides L. are, in fact, to be attributed to Salvia ceratophylloides Ard. Therefore, S. ceratophylloides L. is a synonym of S. ceratophylloides Ard., which has a nomenclatural priority. Until the beginning of 1900, Salvia ceratophylloides was collected by various botanists [7,17,18] from some locations around Reggio Calabria: Gallico Superiore, Terreti, Straorino, Ortì, Vito Superiore, Pietrastorta, even then the species was very rare [7]. In the following decades, the species was not found again despite the research carried out by various botanists, as the profound environmental transformations due to the urban expansion of the city of Reggio Calabria determined the destruction of the habitat and disappearance of the species. In 1997, the species was considered extinct and included in the "Red Book of the flora of Italy" as extinct species (EX) [4][5][6]19]. Field research started in 2008, however, allowed to discover some small new populations of S. ceratophylloides around Reggio Calabria (Puzzi, Cataforio) [20]. Later were found other small populations in places hardly accessible, always in the surroundings of Reggio Calabria [21].

Morphological trait
Salvia ceratophylloides (Figures 1, 3 and 4) is a perennial herbaceous plant (scapose hemicryptophyte), densely pubescent for both glandular and simple patent hairs. The plant is 30-90 cm tall, has upright or ascending stems, normally lignified and much ramified at the base. The leaves are pinnate-partite, with toothed lobes, the basal of 10-12 × 4-6 cm, and the cauline of 3-4 × 1-2 cm. The leaf blade, wrinkled on both sides, is glandular and pubescent, more evident on the lower one. The inflorescences are very showy, 20-30 cm long, normally ramified at the base, and are made up of 5-6 verticillaster each with 4-6 flowers. The calyx, 8-10 × 3-5 mm, is zygomorphic, ferruginous, and covered with numerous sessile or pedicel glandular hairs. The bilabiate corolla, violet, 15-25 mm long (three times the calyx) has an upper lip strongly folded to the cap on the stamens pubescent-glandular on the outside. The two stamens are 10 mm long and the style 20-30 mm long, protrudes over 10 mm from the upper lip and has a deeply bifurcated purple-colored stigma at the extremity. The fruit is a peculiar schizocarp: a microbasarium made up of four dark brown, spherical to ovoidal mericarps; each mericarp, 2-3 mm long, has a thickened margin.
Salvia ceratophylloides has a main flowering period in spring from April to June and a second flowering period in autumn from October to November. The fruiting occurs after some flowering weeks.
It is a strongly aromatic plant, rich in essential oils [22], and of future potential economic interest. The composition of volatile substances produced by glandular hairs suggests that these substances are involved in chemical defense against insects.

Taxonomic remark
The taxonomic rank of S. ceratophylloides is controversial. Hedge [23] considers it a synonym of Salvia pratensis subsp. pratensis, instead the greater number of the authors indicate it as a good species [19,24]. The species is reported with different taxonomic classification in the Italian floras: Fiori & Paoletti [25] reported S. ceratophylloides as a variety of S. pratensis, Tenore [17] and Pignatti [3], considering it as an autonomous species. The most recent checklists of the Italian flora [10] and the authors who dealt with the taxonomy of the Salvia genus in Italy [6]  Salvia ceratophylloides belongs to Subgenus Sclarea (Moench) Benth., Section Plethiosphace Benth., characterized by a campanulate calyx, above two furrowed, concave, with three conniving teeth and corolla with a crescent-shaped upper lip and compressed. It is a part to the group of S. pratensis present in Italy with: S. pratensis L. subsp. pratensis, S. pratensis L. subsp. saccardina (Pamp.) Poldini, S. haematodes L., S. virgata Jacq., and S. ceratophylloides Ard. [3]. S. ceratophylloides is well distinguished from the other sages species of the Salvia pratensis group, above all for the pinnate-partite leaf with toothed lobes. Table 1 shows the main morphological differences between the species of Salvia pratensis group in Italy.
The type of Salvia ceratophylloides was lost because the Arduino herbarium was destroyed during the Second World War. Del Carratore et al. [26] carried out the lectotyping of S. ceratophylloides Ard. Among all the samples, present in the various legally recognized herbarium, they are indicated as the lectotype of Salvia ceratophylloides, the specimen that Arduino sent to Linnaeus stored in the Linnaean Herbarium of London at N° 42.55 (Figure 4).

Habitat
Salvia ceratophylloides grows near Reggio Calabria, on the hills of the western side of the Aspromonte facing the Strait of Messina (Southern Italy), at altitudes between 250 and 400 m a.s.l. especially on the cooler slopes with the north or northwest exposition. The geology of the area is characterized by layers of loose sand alternating with benches of soft calcarenites of Pliocene origin. The soils have a sandy texture with a basic pH and fall into the group Calcaric Cambisols [27].

Distribution and abundance of the population
The field researches conducted in 2008-2010 allowed discovering four small new populations of S. ceratophylloides around Reggio Calabria (Puzzi, Cataforio). Each population consisted of a few dozen individuals, for a total census of 100 mature individuals [20,31]. After looking everywhere, in recent years, other eight small populations of S. ceratophylloides in places hardly accessible were found, always in the surroundings of Reggio Calabria (Figure 6). The total area occupied by the 12 sites is about 4200 m 2 . In these sites, the plants are distributed as follows: 601 breeding without flowers or fruits, 22 flowering individuals, 3 fruiting individuals, 216 seedlings, 259 juvenile individuals nonbreeding, and 17 dead individuals. For a total of about 1100 individuals [21]. The distribution of plants in the fragmented subpopulations is very irregular in relation to the quality of the habitat. In some sites, the number of plants is more abundant, with about 250 individuals; in other sites, the individuals do not exceed 3 units.

Conservation status
As a consequence of population disappearance from the historical places where Salvia ceratophylloides was collected at the beginning of the 1900s, it was considered extinct globally (EX) [4,5]. In 2010, after the discovery of some sites, an assessment was made from Crisafulli et al. [20], and according to the IUCN criteria, the species was ascribed to the "critically endangered" risk categories (CR). Research carried out more recently by Laface et al. [21] ascertained an increasing population size in number of breeding adults and in the area of occupied populations. Nevertheless, the new assessment, using the IUCN criteria B, C, and D, confirmed the status of "critically endangered" species. So, S. ceratophylloides is seriously threatened, facing an immediate high risk of extinction.
S. ceratophylloides has a naturally small population and therefore susceptible to damaging influences. The remarkable fragmentation of the habitat, also due to the environmental transformations caused mainly by various anthropic activities, is the major conservation problem.
According to EIONET classification [32], the threats that influence the survival of this sage can be codified as follows: F01: conversion from other land uses to housing, settlement or recreational areas (excluding drainage and modification of coastline, estuary, and coastal conditions); A02: conversion from one type of agricultural land use to another (excluding drainage and burning); A03: conversion from mixed farming and agroforestry systems to specialized (e.g., single crop) production; A15: tillage practices (e.g., plowing) in agriculture; A16: other soil management practices in agriculture; A17: harvesting of crops and cutting of croplands; B01: conversion to forest from other land uses, or afforestation (excluding drainage); C01: extraction of minerals (e.g., rock, metal ores, gravel, sand, shell); A11: burning for agriculture; A13: burning for forestry; I02: other invasive alien species (other than species of Union concern); and L06: interspecific faunal and floral relations (competition, predation, parasitism, pathogens). The latter threat, due to insects that feed on fruits and flowering stems, is particularly serious and strongly compromises the reproductive capacity of the species.
Salvia ceratophylloides currently is not safeguarded in situ from protected areas or from Sites of Community Importance (SCI) according to Directive CEE 43/92. The ex situ conservation is carried out in the Messina Botanical Garden "Pietro Castelli," where it is successfully reproduced by seed and where currently there are about thirty individuals. Some environmental organization proposed the inclusion of S. ceratophylloides in the lists to the laws of the Calabria Region on the autochthonous flora protection (L.R. n.30 of 26/11/2001; L.R. n.47 of 07/12/2009) [33]. Researchers from the Department of Agriculture of the Mediterranean University of Reggio Calabria have initiated, on its own initiative, monitoring and research on the biological conservation of this rare sage [21].

Conclusion
Endemic species have a high conservation priority, as they are exclusive to a geographically restricted and limited territory. Being often rare and ecologically infrequent, any unfavorable change can cause their rapid extinction [34]. The exclusive endemisms deserve the conservation priority since the disappearance of the local populations caused the complete extinction of these species. Considering the regional responsibility for the conservation of species [35] and that S. ceratophylloides is one of the most endangered rare endemic plants, this species should be the subject of specific in situ and ex situ conservation actions.
The involvement of local authorities (Calabria region and metropolitan city of Reggio Calabria), responsible for the conservation of natural resources and the environment, is essential to take concrete actions aimed at the conservation of this species.
To protect populations of this species and preserve them over time, the establishment of microreserves, following the example applied in Spain [36], could be a good solution for the in situ conservation of this rare sage. These are small protected areas created in order to ensure the future study and monitoring of the endangered endemic flora plants, which can be entrusted to environmentalist associations or to the landowner.