Callmander, M. W., I. Luino, S. Da-Giau, C. Rakotovao & L. Gautier (2014). A synoptic revision of the Malagasy endemic genus Socratina Balle (Loranthaceae). Candollea 69: 65–73. In English, English and French abstracts.
The hemiparasitic endemic genus Socratina Balle (Loranthaceae) is revised for Madagascar. Three species are recognized, including a new one, Socratina phillipsoniana Callm. & Luino. The vegetative and floral morphology of the new species is distinctive; in particular the conspicuous longitudinal villous fringe of long dendritic trichomes on the outer surface of its corolla along each suture of the lobes that contrasts with the shorter floccose indument that covers the rest of the outer corolla surface. All three known species are provided with preliminary risk assessments based on the IUCN Red List Categories and Criteria. A key to the genus is presented and a discussion of the morphological affinities of each species is also provided.
Introduction
The endemic Malagasy genus Socratina Balle (Loranthaceae) is distinguished from Bakerella Tiegh., the only other genus of Loranthaceae occurring in Madagascar, based on the presence of an indument at least on young parts (vs. glabrous in Bakerella) and its long recurved filaments at anthesis (vs. short, straight) (Balle, 1964a). Socratina was placed in the subtribe Tapinanthinae Nickrent & Vidal-Russell along with 14 African and Arabian genera (Nickrent & al., 2010). Among these genera, Socratina is unique in the presence of an indument of straight appressed trichomes on the inner surface of the corolla-lobes (Balle, 1964b; Polhill & Wiens, 1998). It nevertheless has strong morphological affinities with both Taxillus Tiegh. and Vanwykia Wiens, and with the latter, an eastern and south-eastern African genus, it shares styles with peculiar pluricellular ramified trichomes (Polhill & Wiens, 1998). This character is absent in Taxillus, a predominantly south-east Asian genus of c. 35 species with a single species in East Africa, T. wiensii Pohl. (Polhill & Wiens, 1999). Vanwykia was revealed to be sister to Socratina in a recent molecular phylogenetic study and consequently a “dispersal event to Madagascar from a common ancestor with Socratina could be implied“ (Vidall-Russel & Nickrent, 2008: 1026; see also Buerki & al., 2013).
Previous treatments of Socratina recognised two well-defined species: Socratina bemarivensis (Lecomte) Balle and S. keraudreniana Balle. They are localized respectively in the south-western dry bush and in the dry deciduous forests of the northern part of Madagascar (Fig. 1). A recent review of material of the genus Socratina for the “Catalogue of the Vascular plants of Madagascar“ (Madagascar Catalogue, 2014) revealed a collection from the limestone region of Bemaraha (Jongkind & al. 3548) that did not match either of the currently known species. Subsequently, further collections of this undescribed species have been made at sites on a similar substrate in the Beanka area, about 100 km to the north of Bemaraha. The Beanka forests have recently been the subject of intensive biodiversity inventories and a recently published monograph on the biodiversity of this interesting area (Goodman & al., 2013), including a checklist of vascular plant species (Gautier & al., 2013). These inventories lead to the discovery of new species in different groups including one bird, several invertebrates [see Goodman & Gautier (2013) for a review] and plants (Letsara & al., 2012; Callmander & al., 2013; Gautier & Deroin, 2013).
In the present article, we provide a synoptic revision of Socratina and describe a new species endemic to western Madagascar, S. phillipsoniana Callm. & Luino. All three known species are provided with preliminary risk assessments based on the IUCN Red List Categories and Criteria (IUCN, 2012). Calculations of the Area of Occupancy (AOO), Extent of Occurrence (EOO) and number of subpopulations were based on the methods presented in Callmander & al. (2007). A key to discriminate the three currently known species in the genus is presented and a discussion of the morphological affinities of each species is also provided.
Key to the endemic Malagasy genus Socratina
1. Flowers buds c. 1–2 mm in diam. just prior to anthesis; corolla tube covered by a sparse indument; splitting distally between each of the five lobes at anthesis S. keraudreniana
1a. Flowers buds c. 4–6 mm in diam. just prior to anthesis; corolla tube covered by a dense indument, splitting mostly unilaterally at anthesis 2
2. Mature leaves and petiole covered by a russet indument; corolla with a dense uniform external indument S. bemarivensis
2a. Mature leaves and petiole glabrescent; corolla with two different external indument types: a uniform, relatively sparse indument over the entire surface, and with conspicuous villous fringe of long trichomes on the outer surface of its corolla longitudinal along each suture S. phillipsoniana
Systematics
Socratina Balle in Adansonia ser. 2, 4: 135. 1964.
Typus: Socratina bemarivensis (Lecomte) Balle
Socratina bemarivensis (Lecomte) Balle in Adansonia ser. 2, 4: 135. 1964.
Lectotypus (designed by Balle, 1964b: 135) : MADAGASCAR. Prov. Mahajanga: Bois de la Haute Bemarivo, [16°06′S 47°44′E], XI.1918, fl., Perrier de la Bâthie 10646 (P [P00573453]!; isolecto-: P [P0573454, P0573455]!).
Conservation status. — With an EOO of 2,336 km², and an AOO of 27 km² and three subpopulations, none situated within the protected area network, S. bemarivensis is assigned a preliminary status of “Vulnerable“ [VU B1ab(i)+2ab(i)] following IUCN Red List Categories and Criteria (IUCN, 2012).
Notes. — Socratina bemarivensis was originally described in Loranthus Jacq. by Lecomte (1923) following the very broad generic concept of Engler & Krause (1935), a genus that is now circumscribed as mostly restricted to temperate or mountain forest from Europe to south-est Asia (Barlow, 1997). Henri Perrier de la Bâthie, who collected both syntypes wrote on the label of one of them (Perrier de la Bâthie 10652), that the flowers open at maturity with only one longitudinal split along the entire length of the corolla lobes (see Balle, 1964b: 137). Anthesis of S. bemarivensis is very different to that of Socratina keraudreniana where the corolla divides into five lobes in the distal part (Fig. 2). Several other characters of the morphology of its leaves and flowers allow to differentiate those two species: limb sub-orbicular to largely ovate, 0.8–4.8 cm in width in S. bemarivensis (vs. oblanceolate to obovate, 0.3–0.8 cm in S. keraudreniana); corolla broad, covered with long (2–2.5 mm) trichomes forming dense indument (vs. corolla slender covered by short (1–1.5 mm) trichomes forming a sparse indument) (Fig. 2).
Perrier de la Bâthie noted several hosts for Socratina bemarivensis: Acacia sp. and Dalbergia sp. (Leguminosae), Eugenia sp. (Myrtaceae) and Vernonia sp. (Asteraceae) (Balle, 1964b). Most Loranthaceae species seem to have a wide range of hosts (Polhill & Wiens, 1998) but some species have also very restricted hosts such as Taxillus wiensii known only to grow on Cynometra webberi Baker f. (Leguminosae) (Polhill & Wiens, 1998). Further studies are needed in Madagascar to determine if the genus Socratina has host specificity as this information is recorded on very few collections (see also comments under S. keraudreniana).
Additional material examined. — MADAGASCAR. Prov. Antsi ranana: Ambilobe, Ambakirano, Behefaka, Anjahana, forêt d'Ampivanana, 9 km au S de Behefaka, 13°21′12″S 49°09′11″E, 276 m, 6.V.2005, fl. & fr., Ratovoson 105 (CNARP, MO, P [P06714072], TAN). Prov. Mahajanga: Bord de l'Anovilava, affluent du Bemarivo (Boïna), [16°09′S 47°51′E], VI.1906, fl., Perrier de la Bâthie 10642 (P [P05447659, P05447668, P05447669] [syntypes]!)
Fig. 1.
— Map showing the distribution of Socratina bemarivensis (Lecomte) Balle (stars), S. keraudreniana Balle (squares) and S. phillipsoniana Callm. & Luino (circles) in Madagascar, plotted on the map of phytogeographical domains sensu Humbert (1955).
Socratina keraudreniana Balle in Adansonia ser. 2, 4: 135. 1964.
Typus: MADAGASCAR. Prov. Toliara: Gorges du Fiherenana, entre Beanty et Anjamala, [22°57′S 44°19′E], 30–300 m, I.1947, fl., Humbert 19902 (holo-: P [P05447658]!; iso-: [P05447656, P05447657, P05447660, P05447661]!).
Conservation status. — With an EOO of 34,514 Km², and an AOO of 108 km² and nine subpopulations, two of which are within the protected area network (Beza Mahafaly and Tsimanampetsotsa) and one occurs in a proposed protected area which currently benefits from only temporary protection (Mikea Forest), S. keraudreniana is assigned a preliminary status of Least Concern (LC) following IUCN Red List Categories and Criteria (IUCN, 2012).
Notes. — Socratina keraudreniana is unique in the genus in having the corolla tube not splitting unilaterally at anthesis but rather divided into five lobes in the distal part only, thus the tube is much longer than the corolla lobes (Balle, 1964a; Fig. 2A). The species is known from the south-western part of Madagascar in dry deciduous forests and xerophyte scrub, sometimes on limestone. Despite being a rather widely collected species, only two different hosts have been documented: Grewia sp. (Malvaceae) (Du Puy & al. 699) and Mimosa delicatula Baill. (Leguminosae) (Phillipson 2595).
Additional material examined. — MADAGASCAR. Prov. Toliara: Ampanihy vers la Linta, 24°53′S 44°23′E, I.1999, fl., Allorge 2304 (P [P00156506]); 30 km de Tuléar, [23°16′S 44°00′E], II.1962, fr., Bosser 15660 (MO, P [P05447665, P05447666], TAN); ca. 2 km N of Itampolo on route to Lavavolo, 10 m, 24°39′S 43°58′E, 8.II.1990, fl., Du Puy & al. 630 (K, P [P00075257], TAN); Forest of Mikea c. 3 km N of Beroroha, 60 m, 22°52′54″S 43°33′25″E, 8.II.1990, fl., Du Puy, Labat & Comtet 699 (K, P [P016795], TAN); Env. Lac Tsimanampetsotsa (SO), 30 m, [24°07′30″S 43°47′00″E], 24.XI.1960, fl., Leandri & Saboureau 4023 (P [P05447651, P05447654]); Env. Lac Tsimanampetsotsa (SO), 30 m, [24°07′30″S 43°47′00″E], 24.XI.1960, fl., Leandri & Saboureau 4034 (P [P05447652]); 40 km au env. de Tuléar, 300 m, [23°10′S 44°04′E], II.1962, fl., Keraudren 1368 (P [P05447662]) ; Fiherena, [22°57′30″S 44°19′00″E], 8.XII.1967, fl., Koechlin 10 (P [P05447663]); Beza Mahafaly RS, 160 m, 23°40′S 44°36′E, 19.XI.1987, fl., Phillipson 2595 (MO, P [P05447653], TAN); Betaimboraky, 120 m, 22°44′12″S 43°31′17″E, 11.XI.1998, fl., Rakotomalaza & Messmer 1816 (G, MO, P [P0544 7655]); Forêt de Mikea, axe Belo-Ankilimihavotse, 0–50 m, 22°05′S 43°22′E, 30.I.2000, fl., Ranaivojaona & al. 280 (MO, P [P05447543], TAN) ; Makay, forêt Akolitsika, 238 m, 21°40′04″S 44°59′45″E, 22.I.2011, buds, Razakamalala 6136 (MO, P, TAN).
Socratina phillipsoniana Callm. & Luino, spec. nova (Fig. 2, 3, 4).
Typus:MADAGASCAR. Prov. Mahajanga: Beanka, partie N, 18°07′05″S 44°27′04″E, 174 m, 23.VII.2013, fl. & fr., Luino & Ranaivoarisoa 63 (holo-: G [G00341307]!; iso-: K [K000865017]!, MO!, P [P00853035]!, TEF!).
Haec species a congeneris foliis glabrescentibus, alabastro apice fusiformi atque corolla extus secus quamque suturam loborum conspicue longitudinaliter fimbriata trichomatibus villosis dendriticis longis praeut indumento floccoso breviore corollam extus ceterum obtegente distinguitur.
Hemi-parasitic shrub, 0.5–1 m in diam., young fertile and sterile parts covered by a white floccose indument; twigs c. 0-7-1 mm long. Leaves alternate on young shoots, becoming clustered on twigs; petiole 1–6 mm, sometimes sub-sessile; lamina papery-coriaceous, obovate to oblanceolate, rounded at apex, cuneate or attenuate at base; (10-)15–25(-45) × 10–15(-20) mm, tomentose at first, soon becoming glabrescent, triplinerved, attenuate at the base. Inflorescence an umbel, developing at nodes, sessile, 2–5-flowered. Bracts c. 2.5 mm long, boat-shaped, apex rounded, soon glabrescent except for margins and apex that remain covered with longer reddish brown persistent trichomes. Receptacle c. 3 × 2 mm, covered with a dense white indument. Calyx short, c. 1 mm long, green, soon glabrescent, with 5 scarcely differentiated teeth. Corolla 5-merous, 35–50 mm long; the outer surface covered with a dense white shorter floccose indument, composed of dendritic trichomes up to 0.8 mm long, the ramifications forming a series of closely whorled layers; and with a conspicuous longitudinal villous fringe along each suture, composed of slender elongated dendritic trichomes up to 1.5 mm long with a few irregular proximal ramifications and only a few distal whorled ones. Buds sub-conic, with a fusiform apex in the upper 1/3 distal part; tube splitting unilaterally between 2 lobes at anthesis, sometimes slightly splitting between the other lobes distally; lobes c. 20 × 1.5 mm, broadly linear-spatulate in the proximal part, apiculate in the last 7–10 mm distal part. Stamens coiled, arising at or just above the base of the corolla lobes; anthers 2.5 mm long, rolled; filaments 4 mm long, puberulent, dark purple. Style 40 mm in length, pale green, covered with long white trichomes except in the distal 4 mm, filiform. Stigma obovoid to globular, c. 0.5 mm in diam. Fruit a red berry “in vivo”, pale orange when dried, covered with a sparse indument, obovoid, c. 12–14 × 7–9 mm.
Etymology. — The species is named in honour of our colleague Peter Phillipson who obtained funds and arranged the first field mission to Beanka in 2009 and contributed to the floristic checklist recently published on the region (Gautier & al., 2013). Peter has collected over 3000 plants in Madagascar, especially in the dry south-western region where he first collected in 1987. He has a wide knowledge on many plant groups on the Island and participates actively in the milestone “Catalogue of the Vascular plants of Madagascar” project (Madagascar Catalogue, 2014).
Distribution and ecology. — Socratina phillipsoniana is only known from the limestone region of Bemaraha and Beanka in western Madagascar (Fig. 1).
Conservation status. — With an EOO of 557 km2, and an AOO of 27 km2 and three subpopulations, one of which occurring in the protected area network (Bemaraha) and the other two in a projected protected area and already holding a temporary status (Beanka), S. phillipsoniana is assigned a preliminary status of Vulnerable (VU D2) following IUCN Red List Categories and Criteria (IUCN, 2012).
Notes. — Socratina phillipsoniana is similar to S. bemarivensis in having a corolla tube splitting unilaterally at anthesis. It can however easily be recognized when flowering by the conspicuous longitudinal villous fringe of long dendritic trichomes on the outer surface of its corolla along each suture in addition to a uniform floccose indument over the entire surface (vs. uniform indument in S. bemarivensis) and the fusiform shape of the bud apex (vs. rounded in S. bemarivensis) (Fig. 3, 4). When sterile S. phillipsoniana differs from S. bemarivensis by its glabrescent leaves whereas the latter species has leaves covered by a russet indumentum (Fig. 2).
Paratypi. —MADAGASCAR. Prov. Mahajanga: Beanka, partie S, Andoloposa, 18°00′27″S 44°30′10″E, 287 m, 20.III.2012, fr., Hanitrarivo, Bolliger & Rakotozafy 343 (BR, G [G00376797], K, MO, P, TEF) ; Tsingy de Bemaraha, S of the river Manambolo, 19°09′S 44°49′E, 50 m, 15.XII.1996, Jongkind, Andriantiana & Razanatsoa 3548 (G [G00404128], P [P05096712], MO, WAG) ; Beanka, partie N, 18°07′09″S 44°27′02″E, 165 m, 23.VII.2013, fl. & fr., Luino & Ranaivoarisoa 60 (BR, G [G00341313], K, MO, P, TEF).
Fig. 2.
— Living plants. A. Socratina keraudreniana Balle; B. S. bemarivensis (Lecomte) Balle; C. S. phillipsoniana Callm. & Luino.
[Photos: A: J. Bosser; B: F. Ratovoson; C: I. Luino]
Fig. 3.
— Socratina phillipsoniana Callm. & Luino. A. Fertile branch with flowers and fruit; B. Apex of open flower; C. Bud apex showing the fringe of trichomes along the sutures; D. Calyx and bract.
[Luino & Ranaivoarisoa 63, G] [Drawings: S. Da-Giau]
Fig. 4.
— Trichomes. A–D: Socratina phillipsoniana Callm. & Luino; E–G: S. bemarivensis (Lecomte) Balle; H–J: S. keraudreniana Balle.
A, E, H. Trichomes from the outer surface of the corolla tube: side view; B, F, I. Trichomes from the outer surface of the corolla tube: cross section; C, G, J. Trichome from the inner surface of the corolla tube: side view; D: Trichome from villous fringe of the corolla tube: side view.
[A–D: Luino & Ranaivoarisoa 63, G; E–G: Ratovoson 105, P; H–K: Rakotomalaza & Messmer 1816, G]
[Drawings: S. Da-Giau]
Acknowledgements
The authors thank their collaborators of the Département de Biologie et Ecologie Végétales de l'Université, the Parc Botanique et Zoologique of Tsimbazaza, the Missouri Botanical Garden, the Vahatra association in Antananarivo and the Conservatoire et Jardin botaniques de la Ville de Genève. We are especially grateful to Roy Gereau for preparing the Latin diagnoses and the late Jean Bosser and Fidy Ratovoson for providing the photos. Financial support was provided to MWC & CR by the National Geographic Society (Exploration Grant # 8699-09) and the Andrew W. Mellon Foundation; to IL & LG by grants from the Vontobel Foundation; and to IL by a scholarship of the Ernst and Lucie Schmidheiny Foundation. We thank Pete Phillipson for improving an earlier version of this manuscript and Steve Goodman, Pete Lowry, Pierre-André Loizeau and Louis Nusbaumer for support, interest and help in our research.
