Revision of the Madagascan endemic Homollea (Rubiaceae-Pavetteae), with description of two new species

Homollea Arènes (Rubiaceae, subfamily Ixoroideae, tribe Pavetteae) is a genus of shrubs and small trees endemic to western and northern Madagascar. The genus comprises five species occurring in dry deciduous forest, often in limestone areas. The five species are narrow endemics and their conservation status is either Endangered (4 species) or Critically Endangered (1 species). Homollea is characterized by few-flowered, pseudo-axillary, pedunculate inflorescences, well-developed calyces with the lobes much longer than the tube, laterally flattened seeds with a shallow, elongated to linear hilum and entire endosperm, ovules arising from the upper margin of the placenta, and, pollen grains with supratectal elements in the shape of microgemmae. Until now, three species were known and their descriptions are amended. Two further species, H. furtiva De Block sp. nov. and H. septentrionalis De Block sp. nov., are described as new for science. The five species are dealt with in detail: descriptions, distribution maps, conservation assessments, illustrations, lists of exsiccatae and an identification key are given.


Introduction
Madagascar boasts an extremely rich and unusually diverse as well as a highly endemic flora. Endemicity is especially high at species level (> 80%), but much lower at genus level (19%) (Callmander et al. 2011). With ca 800 species (Govaerts et al. 2016) the Rubiaceae are the second largest family of flowering plants (after Orchidaceae) and comprise the second largest number of endemic species (again after Orchidaceae). Endemicity at species level is 92% (Callmander et al. 2011), which is higher than for the vascular flora as a whole. This is also the case for the rate of endemicity at genus level. At the time of writing (end 2016), 91 described Rubiaceae genera (Ferm et al. 2016;Govaerts et al. 2016) are present in Madagascar, of which 30 are endemic to the island and five further ones endemic to Madagascar and the Comoros (Govaerts et al. 2016;Ferm et al. 2016), which is equivalent to 33% and 38.5% of endemicity at genus level, respectively (vs 19% for the vascular flora as a whole). These rates are bound to become higher still as new genera continue to be described.
Unfortunately, Madagascar is not only known for great species richness and high endemicity, but also for the rapid destruction of its natural habitats. In 2007, Moat & Smith calculated that only 18% of primary vegetation remains in Madagascar, resulting in habitat loss for both plant and animal species and rendering them more vulnerable to extinction (Moat & Smith 2007). This is especially pertinent for the Rubiaceae since the family is still poorly known taxonomically and we run the risk of losing species before we have been able to formally describe them. An analysis of taxonomic effort (Davis et al. 2009) showed that, worldwide, the number of new Rubiaceae species described each year has not decreased markedly in recent years. For Madagascan Rubiaceae, recent years have in fact seen a spectacular increase in the description of new species. Since 2000, 125 new Rubiaceae species were described for Madagascar vs 28 species from 1980 till 1999 (data analysed in December 2016 from Govaerts et al. 2016 and from The International Plant Names Index (IPNI) 2012). Many of these newly described species are based on recently collected plant material, e.g., Coffea toshii A.P. Davis & Rakotonas. (Davis et al. 2010) and Ixora fuscovenosa De Block (De Block 2014), collected in 2006 and 2005 for the first time, respectively.
The tribe Pavetteae (subfamily Ixoroideae) accounts for ca 10% of the 800 Madagascan Rubiaceae species. Even though only 80 species occur on the island (vs ca 340 species in continental Africa and ca 240 in Asia), Madagascar is a centre of diversity for the tribe, because the Madagascan Pavetteae are very diverse in morphology and represent a high number of lineages, often with only a few species. The Madagascan Pavetteae are especially variable in fruit, seed and placentation characters, which usually are more conservative at tribal level. Many Madagascan Pavetteae species but also some genera are as yet undescribed. Currently, the Madagascan Pavetteae comprise the following genera: Coptosperma Hook.f. (= Enterospermum Hiern), Homollea Arènes, Paracephaelis Baill. (including Homolliella Arènes;De Block et al. 2015), Robbrechtia De Block, Schizenterospermum Homolle ex Arènes and Tarenna Gaertn. The Madagascan Pavetteae share the characters of the tribe: woody habit, entire stipules (but fimbriate in Rutidea DC.), terminal inflorescences (but rarely axillary, e.g., in the Afro-Madagascan Coptosperma supra-axillare (Hemsl.) Degreef ), contorted aestivation, stigmatic lobes fused over most of their length (but stigma bilobed in Robbrechtia De Block), drupaceous fruits, seeds with an adaxial excavation often surrounded by a thickened ring, endosperm entire or ruminate, exotestal cells parenchymatous or with thickenings along the outer tangential wall, 3-or 4-colporate tectate pollen grains and secondary pollen presentation.
The genus Homollea comprises shrubs and, more rarely, small trees up to 5 m tall from the dry deciduous forests of northern and western Madagascar. The majority of the species occur on limestone. Homollea is characterized by sheathing stipules, coriaceous or subcoriaceous leaves, few-flowered, pseudo-axillary, pedunculate inflorescences, well-developed calyces with the lobes much longer than the tube, laterally flattened seeds with a shallow, elongated to linear hilum and entire endosperm, ovules arising from the upper margin of the placenta, and, pollen grains with supratectal elements in the shape of microgemmae (De Block & Robbrecht 1998). Within the Pavetteae this combination of characters is only found in Homollea and two other Madagascar-centred genera Homolliella and Paracephaelis. Homollea and Homolliella were published at the same time by Arènes (1960), based on notes by Homolle, who had identified them as new but was unable to complete their publication. Paracephaelis had been described eighty years earlier as a monospecific genus (Baillon 1879).
In his unpublished manuscript on the Rubiaceae of Madagascar and the Comores, Capuron (1973) incorporated Homollea, Homolliella and Paracephaelis in the genus Tarenna. Within the modern concept of the tribe Pavetteae, Capuron recognized only two genera: Enterospermum (current name Coptosperma, see De Block et al. 2001), characterized by seeds with ruminate endosperm, and Tarenna, characterized by seeds with entire endosperm. Capuron was well aware of the great variation in seed structure and placentation in his genus Tarenna and recognized five sections, three of which concern species with laterally flattened seeds with shallow elongated hilum, i.e., Homollea, Homolliella and Paracephaelis. Recently, a first phylogenetic study of the tribe Pavetteae was published (De Block et al. 2015). Despite a largely unresolved phylogeny for the Afro-Madagascan clade due to low sequence divergence, Homollea was shown to be monophyletic, as was Paracephaelis after the inclusion of Homolliella. Homollea is easily distinguished from Paracephaelis (including Homolliella) by the pseudo-axillary, pedunculate and few-flowered inflorescences (vs terminal, (sub)sessile and usually multiflorous) and by the longer calyx lobes (4.5 -25 mm vs 1-4 mm long). De Block et al. (2015) also showed that Homollea and Paracephaelis do not belong to the same subclade as the Madagascan Tarenna. Therefore, these genera should not be included in Tarenna but deserve recognition at genus level.
The genus Homollea is undercollected, with less than fifty specimens for five species. This results in a certain degree of uncertainty regarding the descriptions, which are based on relatively few specimens. This is especially problematic for flower and fruit characters, since mature flowers and fruits are rare within the collected material.
As mentioned above, the Madagascan Pavetteae show great variation in their fruit and seed characters. While fruits are always fleshy, the endocarp is thin and crustaceous or thick and stony, the number of pyrenes either one or two, the number of seeds one to ca ten, the seed shape angular, spherical, hemispherical or laterally flattened, the hilum profound or shallow and round or elongated, the endosperm entire or ruminate and the exotesta cells parenchymatous or with thickenings along the outer tangential wall. While studying the fruits of Homollea, great variation was found in the structure of the endocarp. Thin, crustaceous pyrenes occur in certain species while others are characterized by stony pyrenes which open along preformed germination slits. Unique within the Pavetteae is the formation of dispersal units which consist of part of the pyrene wall and part of the septum. This paper is part of a series dealing with the Madagascan representatives of the Pavetteae (e.g., De Block et al. 2001;De Block 2003a, 2003b. The overall objective of this series is to clarify the generic delimitations and phylogenetic relationships within this group. Recent revisions of Madagascan Pavetteae are mostly inexistent and many species remain undescribed. In this context, this revision of Homollea summarizes and updates all known data on this genus endemic to Madagascar, and describes two new species.

Material and methods
All material cited was seen, except when stated otherwise. Herbarium specimens of the following institutions were studied: BR, G, K, MO, P, S, TAN, TEF and WAG; herbarium acronyms follow Index Herbariorum (Thiers continuously updated). Methods follow normal practice of herbarium taxonomy (Leenhouts 1968). Vegetative characters are described based on herbarium material, e.g., colour of leaf blades, leaf size, shapes of sections (e.g., of young shoots, petioles and peduncle); description and sizes of flowers and fruits cover the range of dried and alcohol-preserved material and their colours are given for living material. In the absence of flowers, certain characters such as size and shape of the ovary, the calyx tube and the calyx lobes have been scored on very young or aborted fruits. Flowering and fruiting periods are based on dates given on the labels of the herbarium material.
Terminology generally follows Robbrecht (1988): e.g., as opposed to the definitions in Beentje (2012), the 'calyx' is here considered to comprise the upper portion of the outermost floral whorl from where it becomes free from the hypanthium; 'calyx tube' is the fused basal part of this structure; 'calyx lobes' are the free sepals. However, leaf shape is described according to the terminology of simple symmetrical plane shapes (Anonymous 1962). Robbrecht (1988) does not detail terminology for bracts. In Homollea, as in many Pavetteae, the first order bracts (the pair of bracts supporting the entire inflorescence) are foliaceous. They are described here as consisting of stipular and foliar parts, i.e., the parts that are in the same position as the stipules and the leaves on a vegetative node, respectively. In Homollea the stipular parts form small sheaths, the foliar parts are actual blades with a short petiole.
Plant material studied is listed per province and per region, alphabetically per collector. Localities are cited as given by the collectors on the specimen labels, but regions have been added in order to reflect the new administrative division of the country. If no GPS coordinates were available, coordinates of localities were determined using the online Gazetteer to Malagasy Botanical Collecting Localities (Schatz et al. 2003). Additionally, 1:500.000 maps from the Malagasy Institut National de Géodésie et Cartographie were used. Distribution maps were drawn using Arcmap 9.2. The conservation status was assessed by applying the IUCN Red List Category criteria (IUCN 2001(IUCN , 2016 using GeoCAT (Geospatial Conservation Assessment tool; Bachman et al. 2011). In order to compensate for the inadequate level of sampling for the genus Homollea, cell size has been chosen at 3 × 3 km, rather than the 2 × 2 km cell size suggested by IUCN for most taxa (Callmander et al. 2007). The IUCN category Data Deficient (DD) was avoided since it tends to underestimate the number of threatened species (Callmander et al. 2005(Callmander et al. , 2007.

Description
Shrubs or small trees; vegetative and reproductive parts glabrous or pubescent (externally); young shoots quadrangular with concave sides or flattened and bisulcate (when dry). Leaves decussate, shortly petiolate; petioles canaliculate above; blades coriaceous or subcoriaceous; margin (somewhat) revolute when dry; domatia present or absent; venation brochidodromous; midrib somewhat impressed above (at the leaf base), raised below; secondary veins somewhat raised above, raised below; higher order veins somewhat raised above; stipules interpetiolar, sheathing, sheats keeled, basally fused into a cone (1-5 mm long) with upper free parts (1-5 mm long) triangular with acute tips or ovate with acuminate tips, adaxial surface glabrous but with a continuous row of large (1-1.5 mm long) colleters, sometimes interspaced with a few hairs, at the base. Inflorescences pseudo-axillary, pedunculate, cymose, compact, consisting of 1-12 flowers; peduncle, axes, pedicels and bracts green; peduncle 0.5 -13.5 cm long, quadrangular with concave sides or flattened and bisulcate (when dry); first order bracts with stipular parts consisting of small sheaths and foliar parts consisting of modified leaves; higher order bracts absent or strongly reduced; bracteoles absent. Flowers sessile or shortly pedicellate, 5-merous, hermaphrodite; calyx well developed, green; calyx tube 1-2.5 × 1.5 -2.5 mm; calyx lobes much longer than tube, linear to narrowly spathuliform; corolla narrowly tubular (1-1.5 mm wide) but widening in the upper 5 mm below the throat, white; corolla lobes contorted to the left in bud and spreading at anthesis; stamens sessile, inserted in the corolla tube somewhat below the level of the throat, included for 1-4 mm in the corolla tube at anthesis; anthers linear, basimedifixed, sagittate, with sterile apical appendix to ca 0.5 mm long; disc annular, fleshy, glabrous; ovary cupular, 1-2 × 1.5 -2 mm, bilocular; placentation axile; placentas peltate, attached at or somewhat below the middle of the septum, with 2 -7 ovules arising from the upper margin of the placenta; style and stigma white; style slender, glabrous; stigma partly exserted at anthesis, slender; stigmatic lobes fused over their entire length, papillae situated along the lines of fusion of the stigmatic lobes; secondary pollen presentation present. Fruits drupaceous, spherical or subspherical, usually somewhat wider than high (not including calyx), not exceeding 1 cm in diameter, glossy and often strongly wrinkled in dried state, with persistent calyx, colour unknown (indicated as green on collector labels, only once suggested to be yellow or orange at maturity); exocarp glabrous or pubescent; mesocarp with well-developed vascular bundles; endocarp forming 2 hemispherical or hemi-ovate pyrenes which remain joined adaxially, either thin and crustaceous and without opening mechanism, or stony and breaking up along 4 preformed germination slits, rarely with the formation of separate stony dispersal units each including a single seed; seeds 1-3 per pyrene, (1-)2 -6 per fruit, laterally compressed, reddish brown, hilar cavity shallow, elongated to linear; endosperm entire; embryo with foliaceous cotyledons; radicle inferior. Seed-coat thickened along the outer tangential wall and the upper parts of the radial walls; thickenings continuous but for a narrow ring-like intrusion from the cell lumen, visible in longitudinal section as two narrow canals running down from the outer edges of the cells; exotesta cells somewhat elongated around the hilum, but thickenings not taking part in the elongation; cell lumina filled with tannins (De Block 1997; see also Bridson & Robbrecht 1985: f. 8, depicted for Paracephaelis trichantha (Baker) De Block, as Tarenna trichantha (Baker) Bremek.)). Pollen grains 3-zonocolporate; exine microreticulate to perforate, microgemmae present.

Diagnosis
Resembling H. longiflora Arènes and H. leandrii Arènes because of the glabrous vegetative and reproductive parts, but differing from both species by the inflorescences with fewer flowers (1-3 vs 3-12); similar to H. longiflora because of the reddish brown shoots but differing from this species by the shape and size of the vegetative leaves (broadly obovate, broadly elliptic, or, rarely obovate, elliptic or ovate, 4-7 × 2.5-4 cm vs narrowly elliptic or narrowly ovate, (5.5 -)7-12 × (1.3 -)1.7-3(-4) cm) and the number of secondary veins on each side of the midrib (4 -6(-7) vs 7-12); similar to H. leandrii because of the calyx lobes which are sparsely ciliate at their bases and the shape of the blades of the first order bracts (broadly ovate or ovate with cordate to truncate base), but differing from this species by the reddish brown shoots (vs fawn or pale beige).

Etymology
The specific epithet comes from the Latin adjective furtivus (secret, clandestine). It refers to the fact that the species was only recently collected for the first time.

Distribution
Only known from Montagne des Français, a limestone massif close to Antsiranana in the Diana Region (Antsiranana Province) in North Madagascar (Fig. 6A).

Habitat and phenology
Lowland dry semideciduous or deciduous forest; on limestone. Fruiting: March.

Distribution
Known from the Melaky Region in western Madagascar (Mahajanga Province): only collected in the vicinity of Antsalova and Tsingy de Bemaraha (Fig. 6A).

IUCN status
Endangered: EN B1ab(i,ii,iii,iv,v) + 2ab (i,ii,iii,iv,v). The extent of occurrence (EOO) of H. leandrii is estimated to be 4,160 km 2 , and its area of occupancy (AOO) 63 km 2 using a cell width of 3 km.
Most of the specimens of this species were collected in the 1950s and 1960s. Only three specimens date from after the year 2003, two of these from inside the Tsingy de Bemaraha National Park, the third from Beanka forest. The species is present in two protected areas: the Tsingy de Bemaraha Strict Nature Reserve and the adjacent Tsingy de Bemaraha National Park, which have been protected since 1927. But, except for the inaccessible tsingy, the reserves are threatened by fires which are set each year in the dry season in order to favour the growth of young grass for the grazing of cattle (Nicoll & Langrand 1989;. Habitat loss as a result of bush fires is also a serious threat for H. leandrii outside the protected areas. Considering these threats and the fact that the species is distributed in only five locations, H. leandrii is assessed as Endangered (EN).

Notes
Only few specimens with mature flowers were collected.

Distribution
Known from Mahajanga Province in western Madagascar, centred in the Boeny Region with one collection from the Bongolava Region; mostly collected from the Ankarafantsika Reserve and surroundings (Fig. 6A).

Habitat and phenology
Lowland dry semideciduous or deciduous forest; on sandy soil, alt. 0 -200 m. Flowering: January -February, with peak in February; fruiting: March-May.

IUCN status
Endangered: EN B1ab(iii) + 2ab(iii). The extent of occurrence (EOO) of H. longiflora is estimated to be 1,209 km 2 and its area of occupancy (AOO) 36 km 2 using a cell width of 3 km. All collecting localities fall within the Ankarafantsika National Park and the Bongolava New Protected Area (created in 2006). The major threat for this species is habitat loss since both protected areas are under threat by logging for charcoal and timber, burning for grazing and slash-and-burn agriculture (Nicoll & Langrand 1989). The sandy soil, once denuded, erodes quickly and vegetations do not recover. The distribution of this species is insufficiently known since all but three of the 15 specimens available at this time are from the Ankarafantsika National Park (mostly from the Ampijoroa Forest station near Lake Ravelobe), an area easily accessible to collectors. Considering the threats, and the fact that the species is distributed in only three locations, H. longiflora is assessed as Endangered (EN).

Note
The holotype, Saboureau 7, bears a handwritten label by Saboureau. Duplicates are available at P and TAN (with similar handwritten labels), but are labelled as coll. ignot. 1857-RN.

Distribution
Known from the Boeny and Betsiboka Regions in western Madagascar (Mahajanga Province), collected from the surroundings of Mahajanga and Ambongo and from the Namoroka and Kasijy Reserves (Fig. 6B).

Habitat and phenology
Lowland dry semideciduous or deciduous forest, on sandy soil, from the upper level of the beach to limestone formations further inland, alt. 0-200 m. Flowering: November -January; fruiting: February -March.

IUCN status
Endangered: EN B2ab(iii). The extent of occurrence (EOO) of H. perrieri is estimated to be 10,176 km 2 , and its area of occupancy (AOO) 54 km 2 using a cell width of 3 km. Over a period of ca 175 years (first collection in 1841 by Pervillé) only seven specimens were collected: four specimens were collected before 1915, three between 1950 and 1975, the most recent specimen dates from the year 2000. The older specimens do not have detailed locality data, e.g., Majunga or Ambongo, which renders the assessment somewhat less reliable. The species occurs in five localities, three of which are in protected areas: Tsingy de Namoroka National Park, Kasijy Reserve and Mahavavy Kinkony New Protected area (created in 2015). The main threat to the species is decline of its habitat both inside and outside the protected areas as a result of logging for timber and charcoal, burning for grazing and slash-and-burn agriculture. Considering these threats, and the fact that the species occurs in only five locations, H. perrieri is assessed as endangered (EN).

Notes
In the protologue, Arènes (1960) described the flowers of H. perrieri as having a corolla tube of 11 mm long and corolla lobes of 5 mm long. Very few mature flowers are available for study (one on the isotype Perrier de la Bâthie 3633 and old, incomplete flowers in the envelopes on Morat 4700 and Perrier de la Bâthie 3504). None of these flowers show the measurements given by Arènes (1960). Their corolla tubes range between 15 and 20 mm and the corolla lobes between 8 and 10 mm long.

Etymology
The specific epithet refers to the distribution area of the species in the northernmost part of Madagascar.

Description
Shrub 1-2 m tall; vegetative and reproductive parts pubescent with trichomes (0.3 -)0.5 -1.5 mm long (the longest trichomes occurring on ovary and fruit); young shoots reddish brown, densely hispid; older shoots reddish brown, flaking, glabrous. Leaves with petioles 0.5 -1 cm long, densely hispid; blades elliptic, rarely ovate or obovate, 5-11 × 2.5 -5 cm, subcoriaceous or rarely coriaceous, drying greenish or brownish above, discolourous or somewhat paler below but sometimes young leaves drying blackish on both surfaces, moderately to densely hispid or villose or rarely ± glabrous with trichomes restricted to the veins above, densely hispid below; margins ciliate; apex acuminate, acumen 0.3 -0.8 cm long; base cuneate to obtuse or, more rarely, unequal; secondary nerves 5 -9 on each side of midrib; higher order veins sometimes dark or blackish brown in young leaves; domatia absent or inconspicuous; stipules 0.6 -1 cm long, at the base densely hispid and higher up sparsely to moderately villose or, more rarely, ± glabrous outside, margins ciliate, basal cone 2.5-5 mm long, free parts of sheaths 2.5 -5 mm long, triangular with acute tips or, more rarely, ovate with acuminate tips, acumen up to 2 mm long. Inflorescences 3-12-flowered, with peduncle, axes, pedicels and bracts densely hispid; peduncle 1-2(-4.5) cm long; first order axes up to 2 mm long; first order bracts consisting of 1-2 mm high triangular sheaths and blades sessile or subsessile, broadly ovate to ovate, 0.8 -3.5 × 0.5 -2.5 cm with cordate or truncate bases; higher order bracts usually absent, if present, then linear, up to 5 mm long; bracteoles absent. Flowers scented, sessile or subsessile; calyx tube 1-1.5 mm long, moderately to densely hispid outside, densely sericeous and without colleters inside; calyx lobes (9 -12 -)17-25 × 0.5 -0.8 mm, sparsely to moderately hispid outside, inside densely sericeous in the basal 5 mm, higher up pubescence identical to that on the outside, margins ciliate, tips acute; corolla tube 20 -27 mm long, sparsely to moderately hirsute and with up to 5 mm long longitudinal lines of appressed hairs below the sinuses of the corolla lobes outside, moderately villose in the upper half inside; corolla lobes 13 -18 × 2 mm, sparsely to moderately hirsute outside, sparsely to moderately sericeous at the base and glabrous higher up inside, margins ciliate, tips obtuse or acute; anthers 4.5 -5 mm long, mostly included in the corolla tube at anthesis (only ca 1 mm exserted), inserted ca 3 mm below the level of the throath; ovary ca 2 mm long, densely hispid; 4-6 ovules per locule; stigma exserted from corolla tube for 4 -5 mm at anthesis, receptive zone ca 14 mm long. Fruits ca 9 × 9 mm (persistent calyx not included), moderately to densely hispid; pyrene stony, breaking up into 4 valves along 4 preformed longitudinal germination slits (two along the lines of fusion of the two locules and two perpendicular to those); septum not stony; seeds ca 5 per fruit, ca 4.5 × 2.5-3 mm.

Distribution
Only known from the Diana and Sava Regions in northern Madagascar (Antsiranana Province; Fig. 6B).

IUCN status
Endangered: EN B1ab(iii) + 2ab(iii). The extent of occurrence (EOO) of H. septentrionalis sp. nov. is estimated to be 3,495 km 2 , and its area of occupancy (AOO) 54 km 2 using a cell width of 3 km. Seven of the eight known specimens are recent (collected after the year 2003) and are the result of the intensified collection effort made in this region mainly by the Conservatoire & Jardin Botaniques de la Ville de Genève. The species occurs in five localities, two of which fall within the Loky-Manambato New Protected Area (Daraina), created in 2005 and managed by a Madagascan non-governmental organization, Association Fanamby. The main threat to the species is loss of habitat as a result of subsistence farming, logging for timber and charcoal and fires. Furthermore, the region is also subject to traditional mining for gold (Rakotondravony 2009;Nusbaumer et al. 2010 (Fig. 6B).

Discussion
Many newly  Being narrow endemics, the five Homollea species are more vulnerable to extinction risk than widespread species (IUCN 2001). Because of their restricted distribution range (Area of Occupancy), their presence in five or less locations and a continuing decline in extent and/or quality of habitat, the IUCN assessment for H. leandrii, H. longiflora, H. perrieri and H. septentrionalis sp. nov. is Endangered. Homollea furtiva sp. nov., which is only present in one location in a protected area, is assessed as Critically Endangered.
All five Homollea species are represented in at least one protected area. Some of these protected areas, such as, e.g., Montagne des Français, Loky-Manambato and Bongolava, have only been recently created and lack strong protection. But all protected areas in Madagascar are in danger of encroachment by anthropogenic actions, such as tavy agriculture, fires to improve grazing land, logging for timber and charcoal, traditional mining, etc. (Nicoll & Langrand 1989;Hartley et al. 2007;Goodman et al. 2008;Draper 2010;Innes 2010). Protected areas have little financial means, few staff and resources and are unable to stop the encroachment (Nicoll & Langrand 1989;Hannah et al. 2008;Wingen 2011). Occurrence in protected areas therefore does not constitute a guarantee for low extinction risk.
All Homollea species occur in limestone areas or on calcareous soil. Homollea furtiva sp. nov., H. leandrii and H. perrieri occur in limestone massifs, Montagne des Français, Tsingy de Bemaraha, and, Tsingy de Namoroka and the Kasijy massif, respectively. Homollea longiflora and H. septentrionalis sp. nov. are linked with calcareous soils in the Ankarafantsika and the Loky-Manambato regions, respectively. Ankarafantsika lies on a calcareous plateau which is covered by sandy soil. Loky-Manambato is a mosaic of different habitats varying in elevation, climate, precipitation and soil types. Part of the region has calcareous soils (Nusbaumer et al. 2010;Lourenço & Goodman 2013). Du Puy & Moat (1998) stressed the influence of rock type on species distribution. The strongest correlation between rock type and species distribution is found for limestone: species on limestone are often restricted to this rock type, whereas widespread species may occur on a range of different rock types but are usually absent from limestone (Du Puy & Moat 1998). This correlation between limestone or calcareous soils and narrow endemism is also known outside Madagascar (Wong et al. 2002). Because of the presence of high numbers of narrow endemics, the limestone areas in Madagascar deserve additional collecting and stronger conservation efforts.
The genus Homollea shows great variation in the structure of the pyrenes. In all species, two pyrenes are present, their abaxial surface formed by the endocarp, which may be thin and crustaceous or thick and stony, and their adaxial surface formed by the septum, which may be membranous or stony. The two pyrenes, each comprising one to three seeds, enclose separate areas in the fruit, but remain joined to each other on their adaxial side. Thin crustaceous pyrenes without opening mechanism occur in H. longiflora (Fig. 3H) and H. furtiva sp. nov. The adaxial surface of the pyrenes (the septum) remains membranous and it is the fruit or the two joined pyrenes that function as dispersal unit. Stony pyrenes occur in the three other species of the genus. Here too, the two pyrenes remain joined on their adaxial side. They open easily along 4 preformed longitudinal germination slits, two along the lines of fusion of the two locules and two perpendicular to those ( Fig. 2F-G). In H. perrieri and H. septentrionalis sp. nov. the septum, forming the adaxial surface of the pyrenes, remains membranous. The two joined pyrenes break up into four valves along the preformed germination slits, freeing the seeds, which seem to act as dispersal units.
In H. leandrii a situation unique within the Pavetteae is found in that the dispersal units are formed by part of the pyrene, part of the septum and a single seed. The two joined stony pyrenes have the same four preformed germination slits as in H. perrieri and H. septentrionalis sp. nov. and open along these four slits. But instead of falling apart into four valves, each of the four pyrene parts remains connected to part of the stony septum. When the pyrenes break open each seed remains partly enclosed in a stony dispersal unit formed by part of the pyrene wall and part of the stony septum (Fig. 2H).
Further information is needed in order to better understand the different pyrene types and pyrene opening mechanisms in Homollea. Because of the fact that few collections with ripe fruits are available, it was not possible to perform many fruit dissections per species. The variation in pyrene type and pyrene opening mechanism are probably adaptations to the habitat in which Homollea species occur. But many of the Homollea specimens give little or no habitat data (especially historical collections) and, therefore, no hard conclusions can be drawn. It is possible that stony pyrenes and dispersal units are adaptations to prevent seed damage in the karst limestone areas. The presence of the opening mechanism could be a drought adaptation, allowing seeds to be freed rapidly after a period of rain.

by the Research Foundation -Flanders (FWO), the 'Stichting tot Bevordering van Wetenschappelijk
Onderzoek in Afrika' and the Percy Sladen Memorial Fund.