Epipactis microphylla ( Ehrhart 1789: 42 ) Swartz (1800: 232)

Brullo, Salvatore, Brullo, Cristian, Cambria, Salvatore, Tavilla, Gianmarco, Pasta, Salvatore, Scuderi, Leonardo & Zimmitti, Angelo, 2021, A new subspecies of Epipactis microphylla (Orchidaceae; Epidendroideae) from Pantelleria Island (Sicily), Phytotaxa 512 (2), pp. 83-96 : 84-91

Epipactis microphylla ( Ehrhart 1789: 42) Swartz (1800: 232) . ( Fig. 1 )

Homotypic synonyms: Serapias microphylla Ehrhart (1789: 42) . Serapias latifolia (Linnaeus) Hudson var. microphylla (Ehrhart) Persoon (1807: 513) . Epipactis latifolia (Linnaeus) Allioni var. microphylla (Ehrhart) Condolle de (1815: 334). Epipactis latifolia (Linnaeeus) Allioni subsp. microphylla (Ehrhart) Bonnier & Layens (1894: 409) . Epipactis helleborine (Linnaeus)Crantz var. microphylla (Ehrhart) Reichenbach (1851: 141) . Limodorum microphyllum (Ehrhart) Kuntze (1891: 672) . Helleborine microphylla (Ehrhart) Schinz & Thell (1908: 589) . Amesia microphylla (Ehrhart) Nelson & Macbride (1913: 472) .

Heterotypic synonyms: Serapias latifolia (Linnaeus) Hudson var. parvifolia Persoon (1807: 512) . Epipactis latifolia (Linnaeus) Allioni subsp. parvifolia (Persoon) Richter (1890: 284) . Epipactis intermedia Schur (1866: 649) . Epipactis microphylla (Ehrhart) Swartz subsp. intermedia (Schur) Richter (1890: 283) .

Epipactis subsp. microphylla

Type:―Herb. Putterlick: 120. In Monte Deister, Serapias parvifolia Ehrh., Ehrhart s.n., (lectotype W 0028219!, designated by Hautzinger 1976: 41); isotypes: Herb. Smith: 120. In Monte Deister. Serapias parvifolia Ehrh. , scripsit Ehrhart (LINN-HS 1395.6.1!, LINN-HS 1395.6.2!, here designated); syntypes: Herb. Reichenbach: Herb. Orchid Nr. 12872: Serapias microphylla Ehrh. !, prope Hannover, Ehrhart, b. Berychio dedit ut F. Meyer (W 0067282! here designated); Serapias microphylla , H. (= Hannoverae), 1784, scripsit Ehrhart (GOET 008437! here designated); Serapias latifolia microphylla H. (= Hannoverae), 1780, scripsit Ehrhart (GOET 008435! here designated); Serapias microphylla Ehrh. = Epipactis microphylla Sw., Pyrmonti, Ehrhart (GOET 008436! here designated).

Perennial herbs with short rhizome and several roots renewed in spring. Stem (10) 15–55 cm tall, usually solitary, rarely two, erect, pale green to violaceous green, densely covered by grey and stellate hairs, with 1–3 basal sheaths. Cauline leaves 3–9, near sheathing, greyish-green to green, often tinged with violet, erect to spreading, well spaced, usually shorter than internode, lanceolate to ovate-lanceolate, the upper leaves bract like, parallelinerved, 2.5–5.0 × 0.5–1.5 (2.0) cm, laxly and more o less regularly crenulated at the margin, with 10–12 teeth per mm. Bracts linearlanceolate, acuminate, basal ones 14–20 × 2–4 mm, lower bract equal to the flower, upper ones shorter. Inflorescence lax, almost unilateral, 4–22 cm long, pubescent, with 4–30 flowers inserted on short hairy peduncles. Flowers bellshaped, facultatively autogamous, drooping to sub-horizontal, greenish white tinged with violet; sepals oblong-ovate, pointed, keeled, 7.0–9.0 × 3.0– 4.5 mm, pubescent on outer surface, usually green on inner surface, sometimes reddish; central one with 1(2) lateral nerves for the side not reaching the apex; lateral ones usually with only 1 lateral nerve on lower side; petals ovate-lanceolate, acute, pubescent on outer surface, keeled, with 1 nerve for side, 5–8 × 2–4 mm, whitish green to pink on inner surface, green tinged with violet on outer surface; hypochile cup-shaped, 3–4 mm, nectariferous, inside shiny dark green, sometimes tinged with violet, outside whitish to green; epichile cordiform, irregularly crenulated at the margin, whitish green to green, sometimes tinged with pink, 2.5–4.0 × 3.0–4.0 mm, terminating with a tip, occurrences at the base of two verrucose bosses, usually whitish, extending into a central perpendicular ridge. Anther triangular, rounded, 2.0 × 1.7–2.0 mm, greenish yellow; pollinia yellow, at first cohesive but then disintegrating and perhaps falling on the stigma; viscidium present. Ovary 6–8 mm long, more or less pyriform, ridged, densely hairy, green tinged with violet. Clinandrum present. Rostellum present. Stigma rectangular, subvertical, concave, lateral lobes present. Capsule 9–11 × 7–8 mm, patent or slightly pendulous, densely hairy. Seeds brownish, 1.0–1.2 × 0.2–0.3 mm.

Phenology: ―Flowering May–August, depending on the elevation.

Habitat and distribution: ―According to literature ( Crespo 2005, Delforge 2016, GIROS 2016, Grünanger 2017, AHO 2018), E. microphylla occurs at 50–1800 m throughout most central and southern European countries (including all large Mediterranean islands), extending eastward to the Crimea, Caucasus and Anatolia ( Fig. 2 ). It is completely absent from the southern Mediterranean, except for a restricted mountain locality of northern Algeria ( Bougaham et al. 2020). This species grows as scattered individual plants mainly in the shady undergrowth of deciduous mesic forests or sometimes in pinewoods and evergreen woodlands; it seldom occurs in forest edges or sunny positions. It prefers limestone substrates with humified soils at basic pH, only occasionally localized in siliceous environments and habitats with marked aridity.

Other specimens examined:— ITALY. Sicily: Bosco di Malabotta Nebrodi ( ME) , 16 Jul 1996, Brullo & Spampinato s.n. ( CAT) ; ibid., 17 Jul 2002, Brullo , Sciandrello & Stuto s.n. ( CAT) ; Quacella-Madonie , 17 Jun 1990, Spampinato s.n. ( CAT) ; Vallone Chiuso sopra le Favare di Isnello ( PA) , 2 Jun 1991, Brullo & Spampinato s.n. ( CAT) ; Vallone Chiuso , 25 Jul 1992, Brullo & Scelsi s.n. ( CAT) ; Piano Battaglia , 25 Jul 1992, Brullo & Scelsi s.n. ( CAT) ; ibid., 19 Jul 1996, Brullo , Guarino & Minissale s.n. ( CAT) ; Pizzo Carbonara ( Madonie ), 19 Jul 1996, Brullo , Guarino & Minissale s.n. ( CAT) ; ibid., 14 Jul 2001, Brullo , Giusso & Sciandrello s.n. ( CAT) ; ibid., Jul 2004, Brullo s.n. ( CAT) ; Fornazzo (lungo la statale per Linguaglossa ), 23 June 1990, Siracusa s.n. ( CAT) ; Nicolosi, Etna , 18 July 1991, Scelsi s.n. ( CAT) ; Etna , 17 June 1993, Brullo & Siracusa s.n. ( CAT) ; Etna, Mareneve quota 1000 m, 11 July 1996, Brullo & Siracusa s.n. ( CAT) ; Contrada Isola Ardito, Valle d’Anapo , 3 June 1991, Scelsi & Spampinato s.n. ( CAT) ; Liona ( S. Michele Ganzaria ), 17 May 2007, Guccione s.n. ( CAT) ; Calabria, Lungo strada riserva Basilicò ( Aspromonte ), 19 July 1985, Bartolo s.n. ( CAT) ; Valle Torrenti Listi (presso S. S. 83), 27 July 1991, Bartolo s.n. ( CAT) ; Riserva Basilicò ( Gambarie ), 17 July 1992, Bartolo & Pulvirenti s.n. ( CAT) ; Riserva Basilicò-Gambarie (strada per caserma forestale), 16 July 1994, Pulvirenti s.n. ( CAT) ; ibid., 18 July 1994, Bartolo, Milici & Pulvirenti s.n. ( CAT) ; Bosco di S. Maria, presso Serra S. Bruno , 18 July 1997, Bartolo, Brullo , Scelsi & Spampinato s.n. ( CAT) ; Sardinia, Strada per M. Tonneri, 9 June 2001, Bacchetta, Brullo , Casti & Giusso s.n. ( CAT) ; M. Tonneri rivoli, presso il nuraghe Ardasai , 8 June 2001, Bacchetta, Brullo , Casti & Giusso s.n. ( CAT) ; M. Tonneri (creste), 9 June 2001, Bacchetta, Brullo , Casti & Giusso s.n. ( CAT) ; Sa Duchessa ( CA) , 19 May 1998, Bartolo & Pulvirenti s.n. ( CAT) ; Sa Duchessa ( Domusnova ), 10 June 2001, Bacchetta, Brullo , Casti & Giusso s.n. ( CAT) ; Monte Albo , 5 June 2001, Bacchetta, Brullo , Casti & Giusso s.n. ( CAT) ; Monti di Oliena , 6 June 2001, Bacchetta, Brullo , Casti & Giusso s.n. ( CAT) ; Montarbu , 8 June 2001, Bacchetta, Brullo , Casti & Giusso s.n. ( CAT) ; Barraxutta, Bosco di Oriddi , 4 June 2002, Brullo & Giusso s.n. ( CAT) ; Tacco di Osiri, Nuoro , 5 June 2002, Brullo & Giusso s.n. ( CAT) ; Monte Novo S. Giovanni, 18 July 2004, Bacchetta & Brullo s.n. ( CAT) .

Epipactis subsp. cossyrensis Brullo , subspec. nov. (Figs 3,4)

Type:— ITALY. Sicily. Isola di Pantelleria , presso la cima di Montagna Grande, a circa 800 m, 36°46’51’’N, 12°00’15’’E, 18 Jun 2014, Brullo & Zimmitti s.n. (holotype: CAT) .

From the nominate subspecies, this new subspecies differs in having medium leaves usually ovate to ovatelanceolate 1.5–2.2 mm wide, with margin irregularly denticulate, sepals and petals dorsally glabrous, sometimes sparsely hairy, central sepal oblong-elliptical, lateral sepals with 1–2 nerves per side, petals ovate with 2 nerves per side, epichile widely cordiform, 5–6 mm wide, stigma with trilobed.

Perennial herbs, with short rhizome and several roots renewed in spring. Stem 25–50 cm tall, (1)2–5, erect, pale green to violaceous green, densely covered by grey and stellate hairs, with 1–2 basal sheaths. Cauline leaves 3–5(6), nearly sheathing, greyish green to green, tinged with violet mainly in the abaxial face, erect to spreading, well spaced, usually shorter than internode, the lower ones ovate to ovate-lanceolate, 3.0–6.0 × 1.5–2.2 cm, the upper leaves bract like, lanceolate, 2.0–4.0 × 0.4–0.7 cm, parallel veined, laxly and irregularly denticulate at the margin, with 14–15 teeth per mm. Bracts linear-lanceolate, acuminate, 5–30 × 2–6 mm, lower bract equal to flower, upper ones shorter. Inflorescence lax, bilateral, 7–27 cm long, pubescent, with 8–20 flowers inserted on hairy peduncles. Flowers bellshaped, facultatively autogamous, drooping to sub-horizontal, greenish white tinged with purple; sepals and petals glabrous or sometimes sparsely hairy on the outer surfaces, usually green on inner surface, sometimes reddish; central sepal oblong-elliptical, obtuse, keeled, 7.5–9.0 × 3.4–4.3 mm, with 1 nerve on each side not reaching the apex; lateral sepals ovate-lanceolate, obtuse, 8.0–9.0 × 4.0– 4.5 mm, with 1 nerve only on the lower side or with one short nerve also on the upper side; petals ovate, obtuse, keeled, with 2 nerves for each side, 6.5–7.0 × 4.0– 4.5 mm, whitish pink to purple on inner surface, whitish pink tinged with purple on outer face; hypochile cup-shaped, 3.2–3.4 mm, nectariferous, inside white-green, tinged with purple, outside whitish to greenish; epichile widely cordiform, irregularly crenulated at the margin, greenish white to whitish, sometimes tinged with pink, 3.5–4.0 × 5.0–6.0 mm, terminating in a tip, occurrences at the base of two verrucose bosses, usually whitish, extending into a central perpendicular ridge. Anther triangular, round, 2.0 × 1.4–1.6 mm, yellowish; pollinia yellow, at first cohesive but then disintegrating and perhpas falling on the stigma; viscidium present. Ovary 9–12 mm long, more or less pyriform, ridged, densely hairy, green tinged with violet. Clinandrum present. Rostellum present. Stigma rectangular, subvertical, concave, with welldeveloped lateral lobes, 3 per side. Capsule 12–15 mm long, pendulous, densely hairy. Seeds not seen.

Etymology:— In reference to Cossyra, the Latin name of Pantelleria Island (Sicily).

Phenology:— Flowering late May–June.

Habitat and distribution:— Epipactis microphylla subsp. cossyrensis ( Fig. 5 ) is a silicicolous species growing in the volcanic soils of Pantelleria Island near the top of Montagna Grande (836 m) under evergreen forests dominated by holm oak, Quercus ilex Linnaeus (1753: 995) , often mixed with maritime pine, Pinus pinaster Aiton (1789: 367) s.l. The top of the island benefits from mesic climatic conditions due to frequent fogs occurring all year and high water intake due to overnight dew accumulation. Pantelleria is geologically a volcanic island, with a subaerial eruptive history of more than 300 Ka ( Mahood & Hildreth 1986). This orchid is currently represented by a small population with a fluctuating annual number of flowering individuals, 780– 810 m.

Conservation status:— Based on personal field observations, this orchid is currently narrowly distributed (with EOO of ca. 0.002 km 2), where fewer than 50 mature individuals occur, for which AOO (area of occupancy) calculated with GeoCAT (Geospatial Conservation Assessment Tool, Bachman et al. 2011) is around 4 km 2. Therefore, according to IUCN (2020) criteria, this taxon should be classified as critically endagered (CR B2abiii). The main threats to this population are the fires that periodically affect local forest communities and anthropogenic disturbance (e.g. trampling, flower harvesting, road maintenance) due to the proximity of some individuals to a service road leading to the military buildings and antennae located on the top of the island.

Other specimens examined:— ITALY. Sicily: Isola di Pantelleria, margine del sentiero verso le antenne sulla vetta di Montagna Grande, circa 800 m s.l.m., 8 Jun 2005, Pasta & Scuderi s.n. ( CAT); ibid., Isola di Pantelleria , presso la cima di Montagna Grande a circa 800 m s.l.m., 11 Jun 2013, Brullo & Scuderi s.n. ( CAT) .

Notes:— According to Brullo et al. (1995), Pantelleria Island, in the Sicilian Channel (central Mediterranean) between Tunisia and Sicily, falls within the Cosirense district (Pelagian Domain). There are several endemics in this area, including Helicrysum errerae Tineo (1846: 27) , Limonium cosyrense ( Gussone 1832: 90) Kuntze (1891: 395) , L. secundirameum ( Lojacono 1907: 21) Brullo in Brullo et al. (1977: 20), L. parviflorum (Tineo ex Gussone, 1845 806) Pignatti (1971: 364), Serapias cossyrensis Baumann & Baumann (1999: 502) , Matthiola incana ( Linnaeus, 1753: 662) Aiton (1812: 119) subsp. pulchella ( Conti, 1900: 41) Greuter & Burdet (1983: 94) , Anthemis cossyrensis ( Gussone, 1844: 489) Gussone (1845: 870) , Senecio leucanthemifolius Poiret (1789: 238) subsp. cossyrensis ( Lojacono, 1903: 65) Brullo & Brullo (2009: 44) and Trifolium nigrescens Viviani subsp. dolychodon ( Sommier, 1907: 52) , Brullo, Brullo & Giusso (2011: 39).All these taxa, together with E. microphylla subsp. cossyrensis , suggest that several abiotic factors such as geographic isolation, volcanic substrata, habitat diversity and topography have favoured speciation mainly in those genera or species complexes where these are the most active. In fact, allopatric speciation, coinciding with vicariance, is due to the adaptation of geographically separate populations to local conditions. In the case of isolated allopatric peripheral populations, the most appropriate term, peripatric speciation, should be better applied to smaller isolated populations where gene exchange with the main population is unlikely ( Mayr 1954, 1992, Valtueña et al. 2017).

In addition to these taxa, which must be treated as neo-endemics ( Contandriopoulos 1962) bearing in mind the recent origin of the island, there are others absent in Sicily but found in North Africa and other Mediterranean territories, such as: Logfia lojaconoi ( Brullo, 1985: 8) Brullo & Brullo (2009: 43) , Carex illegitima Cesati in Friedrichsthal (1838: 271), Pimpinella lutea Desfontaines (1798: 265) , Limodorum trabutianum Battandier (1886: 297) , Brassica insularis Moris (1837: 168) , Cytisus rigidus ( Viviani 1824: 40) Cristofolini & Troia (2006: 741) , Bellium minutum ( Linnaeus 1763: 1250) Linnaeus (1771: 286) , Cyperus laevigatus Linnaeus (1771: 179) , Schoenoplectus litoralis (Schrader1806: 142) Palla (1888: 49) subsp. thermalis (Trabut in Battandier & Trabut, 1895: 99) Hopper in Saldanha & Nicolson (1976: 698), Andryala cossyrensis Gussone (1844: 407) , Genista asphalathoides Lamarck (1788: 680) , Ophrys scolopax Cavanilles (1793: 46) subsp. apiformis ( Desfontaines, 1799: 321) Maire & Weiller in Maire (1960: 260). These species highlight, apart from the geographical isolation of the island from Sicily, also the frequency of colonization from the Maghreb territories.

Taxonomic notes:— As concerns the taxonomic position of E. microphylla , it clearly belongs to sect. Epipactis (= Euepipactis), since it is characterized by a cup-shaped hypochile without lateral lobes and a fixed epichile ( Irmisch 1842), which is typified by E. helleborine . Within this section, Quentin (1993) recognized two new subsections, subsect. Atrorubensae, for which the type is E. atrorubens ( Hoffmann, 1804: 182) Besser (1809: 220) and subsect. Helleborine. Later, Peter (2002) recognized in Epipactis three sections, apart from the sect. Arthrochilium Irmisch , also the subsections proposed by Quentin (1993, 1995), but raising them to the rank of section, in the last he included E. atrorubens and E. microphylla . In contrast, Efimov (2004: 23) arranged both these species within a new series of the sect. Epipactis proposed as ser. Atrorubentae Nevski. More recently, Delforge (2016) recognized only two sections, sects. Arthrochilium and Epipactis (as Euepipactis), distinguishing several groups within each. In particular, in the last section he recognised the E. atrorubens group, in which he included, in addition to E. atrorubens and E. microphylla , also E. cardina Benito & Hermosilla (1998: 109) from southern Spain, E. kleinii Crespo, Lowe & Piera (2001: 854) from Spain, E. subclausa Robatsch (1988: 167) from Greece, E. spiridinovii Devillers-Terschuren & Devillers (1995: 87) from Bulgaria, and E. condensata Boissier ex Young (1970: 106) from the eastern Mediterranean-Caucasus. Besides, E. krymmontana Kreutz, Fateryga & Efimov in Fateryga et al. (2014: 24) from Crimea and southern Russia must be added. Morphologically, the species of this group share some diagnostic features such as an ovary with strongly villous pedicel and epichile with prominent wrinkled bosses, but significant features permit differentiation between them (Table. 1). As regards E. microphylla , the population from Pantelleria differs morphologically from the typical ones occurring in the rest of its distribution in some significant features of the number of stems, type of inflorescence, floral indumentum, shape and size of leaves and other floral features. These differences can be easily observed in the large orchid literature regarding E. microphylla , a species widespread in most of Europe ( Efimov 2004, Delforge 2016, AHO 2018, GBIF Secretariat 2021).

Figures

FIGURE 1. Epipactis microphylla subsp. microphylla. A. Habit. B. Flower frontal view. C. Flower lateral view. D. Central sepal. E. Petals. F. Lateral sepals. G. Labellum (hypochile and epichile). H. Gynostemium frontal view. I. Gynostemium lateral view. J. Leaf margin. Illustration by S. Brullo based on living material from Serra S. Bruno collected by G. Bartolo (CAT).

FIGURE 2. Geographical distribution of Epipactis microphylla subsp. microphylla (green area) and E. microphylla subsp. cossyrensis (red diamonds) based on herbarium materials and literature data (AHO 2018 and Bougaham et al. 2020, modified).

FIGURE 5. Phenological features of Epipactis microphylla subsp. cossyrensis. A–B. Habit in nature. C. Detail of inflorescence. D. Flower. (Photographs A, C by L. Scuderi, B, D by A. Zimmitti.)