The montane trees of the Cameroon Highlands, West-Central Africa, with Deinbollia onanae sp. nov. (Sapindaceae), a new primate-dispersed, Endangered species

Taxonomic treatment

Deinbollia sp. 2 (Fig. 1), because it has leaves of flowering branches less than 1 m long, only sparsely hairy on the lower surface, leaflets more than 15 cm long and sepals adaxially glabrous, flower buds very sparsely hairy and less than 5 mm diam., borne on a branched inflorescence 10–30 cm long, keys out in the Flore du Cameroun treatment of Deinbollia (Fouilloy & Hallé, 1973) to a couplet leading to D. grandifolia Hook.f. and D. maxima Gilg. However, it differs from these two species in having (2–)8–11-jugate leaves (not 4–7-jugate), and in other characters shown in Table 1. In its Nigerian location our species has been referred to as D. pinnata (Abiem et al., 2020). Deinbollia pinnata Schum. & Thonn. is a common lowland West African species that occurs from Guinea to Nigeria, it differs in being densely hairy, so that the lower surface of the leaflets are softly hairy to the touch due to dense, patent, translucent hairs, and it is usually a small shrub of disturbed habitats, with an unbranched, raceme-like inflorescence that is pendulous in fruit, with hairy fruits 12–13 mm wide (see https://commons.wikimedia.org/wiki/File:Deinbollia_pinnata_MS6765.jpg; Keay, 1958: 714–715). In contrast, Deinbollia sp. 2 has only a very few, sparse, red, subappressed hairs along the midrib and secondary nerves, is a tree of intact high elevation forest, the inflorescence is erect, with numerous long branches bearing glabrous fruits 20 mm or more wide (see description below). Additional characters separating Deinbollia sp. 2 from Deinbollia pinnata are included in Table 1.

The affinities of Deinbollia sp. 2 may be with the recently described D. oreophila since this species also occurs at altitude in the Cameroon Highlands and both species share numerous raised lenticels and also leaflets with high length: breadth ratios and with high numbers of secondary nerves. Both species share an unusual structure which is also seen in Deinbollia pinnata: the adaxial surface of the leaf rhachis is not rounded as in the other West African species, but flattened, the margins slightly raised forming acute angles with the sides, with a distinct, raised midline (Cheek & Etuge, 2009a: Fig. 1C). In fact, at two locations, Mt Kupe and Bali Ngemba, the two species D. oreophila and Deinbollia sp. 2 are sympatric and their altitudinal ranges can overlap (Cheek et al., 2004; Harvey et al., 2004). However, without DNA studies, convergent evolution cannot be ruled out. As the only two species of the genus to grow at altitude in the Cameroon Highlands, there is a possibility that they might be confused with each other. The two species can be separated using the morphological characters presented in Table 2.

Similar to but differing from Deinbollia oreophila Cheek in the length of leaves of flowering stems (14–)60–70 cm (versus 25–63 cm), number of leaflets per leaf (4–)16–23 (versus (4–)6–8(–10)), width of leaflets (2.1–)2.5–4 cm (versus (3–)5.5–9(–10.2) cm, number of secondary nerves on each side of midrib (15–)17–18, (versus (7–)9–14(–17); stems with lenticels brown, concolorous and inconspicuous, (versus discolorous, bright white and conspicuous), ovary bilocular (versus trilocular).Typus: Cameroon, Mt Oku and the Ijim Ridge, Aboh to Tum, 2400 m alt., fl. 22 Nov. 1996, Etuge 3600 (holotype K000337729! Fig. 2, isotypes MO!, WAG0336084!, WAG0336083!, YA0057050!);

Monoecious tree or treelet (4–)5–15 m tall, trunk 14.5–40 cm diameter at 1.3 m from the ground, lacking exudate or scent when wounded, sparingly branched, nearly glabrous, apart from the inflorescence. Stems of flowering branches terete (0.8–)1–1.5 cm diameter, solid (not hollow), second internode below apical inflorescence 2–2.5 cm long, outer epidermis pale grey-brown, contrasting with the darker brown bases of the adjoining petiolar pulvini, lenticels dense, raised, elliptic, 0.6–1.1 mm long, concolorous, inconspicuous, glabrescent, hairs sparse to dense, dark brown, cylindric 0.1–0.5 mm long.

Leaves alternate, pinnately compound, (14–)60–70 cm long; leaflets (4–)16–23 per leaf on flowering stems, leaflets 10–14 per leaf on leaves of juvenile trees. Petiole (4–)9.5–20.8 cm long, terete, c. four mm diameter at midpoint, drying pale yellow; basal pulvini dark brown; rhachis (4.5–)32–44 cm long, (2–)8–11-jugate on flowering stems, 5–7-jugate on non-flowering stems of juvenile trees, the upper surface of the distal half flattened with two thin lateral wings and with a central dark hairy rounded central ridge, the rest of the rhachis glabrescent with sparse inconspicuous hairs (de Wilde 4555), or with sparse dark brown appressed hairs (Cable 3386). Leaflets mostly oblong (6.6–)14–19.5 × (2.1–)2.5–4 cm, (but leaflets of sterile branches to 6.5 cm wide), acumen c. 1 cm long, base broadly acute, slightly asymmetric, (basalmost leaflets lanceolate and about half the length of the other leaflets) lateral nerves and midrib yellow, raised above and below, convex, (15–)17–18 on each side of the midrib, nearly brochidodromous, the lateral nerve apices forming a weak irregular submarginal nerve, stronger branches uniting with the secondary nerve above, intersecondary nerves strong, parallel to the secondaries, tertiary and quaternary nerves reticulate raised yellow and conspicuous, on both surfaces, contrasting with the pale grey-green areolae (except in Cable 3386(K) where they are concolorous and so inconspicuous above, possibly an artefact of poor drying); upper surface glabrous, lower surface with inconspicuous, minute, cylindrical, subappressed glossy dark-brown hairs c. 0.25 mm long, distributed very sparsely along the midrib and secondary nerves, absent from mature leaves of non-flowering specimens (e.g., Cheek 8709) but then the same hair type present on axillary buds and young leaves; petiolules yellow, 2–5 mm long, glabrous.

Inflorescence a 80–120-flowered, loose, terminal panicle 25 × 10 cm; auxiliary inflorescences sometimes present in the axils of the distal 1–4 leaves (Cheek 13625); peduncle of terminal inflorescences 0–2 cm long; rhachis internodes (1–)2–3 cm long, shortest in the distal portion; first order bracts caducous; indumentum brown hairy; primary branches 10–20 per inflorescence, 2–8 cm long, each bearing (1–)2–5 partial-inflorescences; partial-peduncles 0–5 mm long, apex with a cluster of 3–5 bracteoles; bracteoles subulate to narrowly lanceolate, 2–3 mm long, apex narrowly acute, partial-inflorescences (1–)3-flowered in glomerules, pedicels erect, terete, 3–4 × 1.5 mm (female), 4–5 × 1 mm (male), sparsely puberulent, hairs 0.1–0.5 mm long.

Flowers white, scent not recorded, flower buds c. four mm diam., open flowers c. 6 × 7 mm. Calyx with sepals 5(–6), orbicular to broadly ovate, concave, green colour, 4–5 × 3.5–4.5 mm apex obtuse. Corolla apex slightly exserted from calyx, petals rhombic or spatulate. Male flowers (Fig. 1C). Petals 5(–6), white, rhombic c. 5 × 3 mm, apex obtuse-acute, base cuneate, margins densely ciliate, hairs 0.3 mm long, outer surface glabrous, inner surface glabrous in distal half, proximal half compressed funneliform with ventral appendage adnate at margins, retuse (notched) for 0.5 mm at midline, adaxial surface moderately densely hairy, hairs c. 0.3 mm long. Extra-staminal disc torus-like, glabrous, irregular, outer wall convex, lacking constrictions or teeth with c. 15 poorly defined lobes, 2.5–3 mm wide, c. 0.8 mm high. Stamens c. 15, erect, slightly exserted by 1–2 mm at anthesis, c. 5–6.5 mm long; filament 4–5 mm long, straight, densely puberulent the entire length (Fig. 1D); anthers yellow, ovate-ellipsoid, 1–1.3 mm long. Ovary (vestigial, Fig. 1E) bilobed, c. 1 × 1.5 mm densely appressed hairy, hairs c. 0.5 mm; style 0.7 mm long, glabrous.

Female flowers (Fig. 1G), with sepals and petals as the male flowers, but petals c. 6 × 2.6–2.9 mm, usually detaching with a stamen attached, probably due to interlocking hairs (see Fig. 1J), proximal two-thirds claw-like, c. 0.7 mm wide, margin sparsely and irregularly ciliate; ventral appendage with apex deeply bilobed, lobes c. 1 mm × 1 mm; disc as in male flower. Stamens c. 10 (see Fig. 1I), included at anthesis, filament c. 2.5 mm long, proximal half to quarter glabrous, distal part densely hairy; anther as male flowers but indehiscent; ovary bilobed (see Fig. 1H), 3.2  × 5 mm, indumentum as male flower, style c. 5 mm long, apical 1 mm, curved, surface papillate-minutely puberulent, apex subcapitate. Infructescence, of same dimensions as inflorescence, erect. Fruit colour recorded as nearly black when ripe, tasting sweet-sour (Elisha Barde, see uses below), and not coloured yellow when ripe (as in other species of the genus), mericarps 1 or 2, transversely ellipsoid, c.1.8 × 2.1 × 1.2 cm (hydrated), the surface leathery, shallowly and finely muricated, glabrous, mesocarp spongy and juicy, 1-seeded. Seed ellipsoid, c. 1.8 × 1.1 × 0.8 cm, testa thin, parchment like, endosperm absent, cotyledons fleshy.

Phenology: flowering in November-December; fruiting in February and April, immature fruit recorded in December and June.

Local name and uses: none are reported in Cameroon but in Ngel Nyaki, Nigeria, Elisha Emmanuel Barde of the Nigeria Montane Forest Project (pers. comm. to M. Cheek Dec. 2020), states that Nyeberehi (Fulfude) is the general name for all Deinbollia species while Jellahi (Fulfude) is a specific name for Deinbollia onanae in Ngel Nyaki where Fulfude speakers (Fulanis) use the bark of this species as medicine for themselves, to treat stomach aches as well as an anti-helminthic. It is not used for treating cattle. The fruits are reported to taste sour-sweet by Mr Barde. The species is also known as Pabba (Ndolla language).

Etymology: The specific epithet of Deinbollia onanae means ‘of Onana’ commemorating Dr Jean-Michel Onana, currently Senior Lecturer in Botany at the University of Yaoundé I, Cameroon, champion of plant conservation in Cameroon, specialist in Sapindales (Burseraceae, author of Flore du Cameroun Burseraceae (Onana, 2017), co-chair of the IUCN Central African Red List Authority for Plants, former Head of the National Herbarium of Cameroon (2005–2016), co-author of the Red Data Book of the Plants of Cameroon (Onana & Cheek, 2011) and the Taxonomic Checklist of the Vascular Plants of Cameroon (Onana, 2011). He led field teams of YA staff working with those of K that resulted in the collection of several of the specimens of this species and personally collected this species in the field (Onana 1600, K, YA).

Distribution & ecology: known only from the Cameroon Highlands of Cameroon (one location in the adjoining Mambilla Plateau, Nigeria) Fig. 3. Upper submontane & montane evergreen forest, sometimes in gallery forest; (1200–)2,050–2,200 m alt.

Additional specimens: CAMEROON. South West Region, Mt Kupe, near main summit, immature fr., 26 June 1996, Cable 3386 (K000197863!, YA!); North West Region.

Bali Ngemba Forest Reserve, fr. April 2002, Onana 1600 (K!); Mt Oku and the Ijim Ridge: above Laikom, st. 21 Nov..1996, Cheek 8709 (K000337728! YA!); Dom, Kinjinjang Rock, st. 25 Sept. 2006, Cheek 13436 (K000580433!; YA!); ibid. Forest Patch 1, fl. buds, 27 Sept. 2006, Cheek 13625 (K000580434!, MO!,US!, YA!); ibid., Javelong Forest, st. 29 April 2005, Pollard 1400 (K000580432!; YA!); Adamaoua Region, c. 120 km E of Ngaoundéré, 15 km NE of Belel, falls in Koudini River, alt. ± 1200 m, fl. 4 Dec. 1964, W.J.J.O. & J.J.F.E. de Wilde, B.E.E. de Wilde-Duyfjes 4555 (K000593309!; K000593310!, WAG1269760!, YA). NIGERIA. Taraba State, Mambilla Plateau, Ngel Nyaki Forest Reserve, near camp, fr. 2 Dec. 2003, H.M. Chapman 481 (FHI, K!); ibid. female fl. 4 Dec. 2002, H.M. Chapman 484 (FHI, K!).

Notes: Deinbollia onanae first came to our attention in 2000 when completing the “Plants of Kilum-Ijim” (Cheek, Onana & Pollard, 2000). Two specimens of Deinbollia matched no other and were named Deinbollia cf. pinnata (Cheek, Onana & Pollard, 2000). In subsequent surveys this taxon was more explicitly referred to as a new species: Deinbollia sp. 2 (Harvey et al., 2004; Cheek et al., 2004; Cheek, Corcoran & Horwath, 2009). However, the earliest known collection was made in 1964 (W.J.J.O. & J.J.F.E. de Wilde, de Wilde-Duyfjes 4555(K)).

This species is remarkable for the very large number of pairs of unusually long and slender leaflets (Fig. 4), and for the comparatively large size of the individuals which often attain 10–15 m in height (Fig. 4), among the largest trees known in the genus. However, at Ngel Nyaki trees can begin flowering at only 2.5 m in height (E. Barde pers. comm. to Cheek Jan. 2020)

Conservation: Deinbollia onanae is rare at each of its six known locations so far as is known, although at Ngel Nyaki this is difficult to establish due to potential confusion with Deinbollia oreophila. Despite many thousands of herbarium specimens being collected at Kilum-Ijim, at Mt Kupe and the Bakossi Mts, at Ngel Nyaki and at Bali Ngemba (Cheek, Onana & Pollard, 2000; Cheek et al., 2004; Harvey et al., 2004) only two specimens of this species at two sites, were made at each of the first three locations and only one at the third location. Surveys at other sites with suitable habitat in the Cameroon Highlands and elsewhere, e.g at Mt Cameroon and at the Lebialem Highlands, failed to find this species (Cheek et al., 1996; Cable & Cheek, 1998; Harvey, Tchiengue & Cheek, 2010; Cheek, Harvey & Onana, 2011). However, at Dom, where a targetted search for this species was made by the first author, three specimens were made, each representing single, isolated trees Cheek, Harvey & Onana (2010). No more individuals than these were found. At Adamaoua Region, Cameroon it has only been collected once, and only a single tree was then noted (W.J.J.O. & J.J.F.E. de Wilde, B.E.E. de Wilde-Duyfjes 4555(K)). None of these locations is formally protected for nature conservation. Tree cutting for timber and habitat clearance for agriculture has long been known to be a threat at all but the last of these locations (references cited above). The range of the species is large: extent of occurrence was calculated as 50,525 km² using GeoCAT. However, severe habitat fragmentation has resulted over many hundreds of years, forest patches being now distant from each other by tens of kilometres, isolated in oceans of cultivation and secondary fire-maintained grassland making the possibility of primate-mediated dispersal from one forest area to another now extremely unlikely. Ecological evidence from Ngel Nyaki is that while Deinbollia regenerates in that forest patch, its primate dispersers do not, or seldom cross to other forest patches (Dutton & Chapman, 2015, see discussion below). We assess the area of occupancy of Deinbollia onanae as 34 km² using the IUCN preferred 4 km² cell size. Therefore, we assess this species as Endangered, EN B2ab(iii) using the IUCN (2012) standard. We suggest that this species be included in forest restoration plantings within its natural range to partly reverse its move to extinction. However, the large (c. one cm diam.), thin-walled seeds are probably recalcitrant, so not suitable for conventional seed-banking, and should not be allowed to be dried before sowing since this can be expected to kill them. Experience at Ngel Nyaki (Matthesius, Chapman & Kelly, 2011) shows that it is possible to raise hundreds of seedlings in nurseries and to establish them in natural forest.

Montane Forest Trees of the Cameroon Highlands

The Cameroon Highlands extend through four tropical African countries. Beginning in the south on the volcano island of Bioko (Equatorial Guinea) they continue on the mainland with the Mount Cameroon active volcano, heading NNE along a major fault, forming the ridges, plateaux and isolated peaks of the Bakossi Mts and Mt Kupe, Muanenguba, Bamboutos Mts, the Lebialem and Bamenda Highlands, Mt Oku, Tchabal Mbabo, then heading eastwards and forming the lower and drier Adamaoua Highlands which extend into the Central African Republic. Two westward extending arms from the central section in Cameroon extend into Nigeria, forming the Obudu and Mambilla Plateaux. The altitudinal division between montane and submontane forest is well-marked in the Cameroon Highlands. Most species of montane tree only occur above the 2000 m contour and not below it (Table 3), while tree species from the submontane forest belt rarely exceed the 2000 m contour (Cheek et al., 1996; Cheek, Onana & Pollard, 2000; Cheek et al., 2004; Thomas & Cheek, 1992), although some species of tree, like Deinbollia onanae can occur on either side of the 2,000 m contour. Since most of the Cameroon Highlands do not ascend above 2,000 m alt., montane forest is not ubiquitous along their length. Moreover, even where altitude is sufficient to support it and where it formerly occurred, montane forest has seen massive clearance for agriculture, and has been totally lost at the Bamboutos Mountains of West Region Cameroon (Ngoufou, 1992). Indeed, the Bamenda Highlands of Cameroon, long since cleared of their montane forest, are now known in Cameroon as “The grasslands” because they are blanketed in secondary grassland, perpetuated by fire. It has been estimated that as much as 96.5% of the original montane forest of the Bamenda Highlands has been lost (Cheek et al., 2020, 49–50). The tallest mountain in the range, Mt Cameroon (4,040 m), despite its height and lack of human activity above 2,000 m alt., has surprisingly little forest above this contour due to the free-draining nature of its predominantly volcanic cinder substrate (Thomas & Cheek, 1992; Cheek et al., 1996; Cable & Cheek, 1998). The single largest block of montane forest that survives by far in the Cameroon Highlands is that at Mt Oku and the Ijim Ridge (Kilum-Ijim) where about 70 km² has been estimated to survive and to have a measure of protection. Here it extends from the 2,000 m contour to the summit at 3,011 m alt. (Cheek, Onana & Pollard, 2000: 20). Elsewhere in the Cameroon Highlands, such as at Mt Kupe, Muanenguba, Bali-Ngemba, Ngel Nyaki and Dom, surviving patches of montane forest consists of only a few hectares, although an area of 40 km² of forest has been recorded at Dutsin Dodo and Gangirwal mountain within the Gashaka Gumti National Park of Nigeria (H.M. Chapman, pers. obs., 2000).

The tree species diversity of the montane forest of the Cameroon Highlands is low (28 species, based on herbarium specimens, see Table 3) compared with submontane forest which has hundreds of species, and also in great contrast, montane forest contains few Cameroon Highland endemic tree species (only seven: 25% of the total, see Table 3). The majority of the canopy contains even fewer species. It was estimated that just ten species made up 90% of the montane forest canopy at Mt Oku and the Ijim Ridge, three of which are endemics (Cheek, Onana & Pollard, 2000: 20). The majority of montane tree species of the Cameroon Highlands are widespread in montane forest in Africa (Afromontane) occurring also east of the Congo Basin in the rift mountains of East Africa and several, such as Ilex mitis, extend north to Ethiopia and south to South Africa. The East African montane forest is more species-diverse, and only a subset of its species extend west to the Cameroon Highlands, and an even smaller subset, just seven species, extend even further west from the Cameroon Highlands, to the Guinea Highlands (Couch et al., 2019: 54).

The high altitudinal range of Deinbollia onanae is unrivalled west of the Congo basin by any other species of the genus. Elsewhere in Africa it is matched only by Deinbollia kilimandscharica Taub., of mountains from Ethiopia to Malawi, reported to achieve 2,250 m elevation in Tanzania (Davies & Verdcourt, 1998). Most species of the genus in tropical Africa are lowland forest shrubs, in the Cameroon Highlands only Deinbollia oreophila also occurs regularly at altitude over 800 m, and is largely confined to the submontane forest band being recorded from (880–)1,000–1,900(–2,050) m altitude where it is often relatively frequent (Cheek & Etuge, 2009a). We postulate based on their shared morphological characters that these two may be sister species (see results above) that have segregated between two adjacent altitudinally based vegetation types in a similar way to certain clades of bird species in the Cameroon Highlands such as the Turaco (Njabo & Sorenson, 2009). This hypothesis needs testing. It would most readily done by a comprehensive species-level molecular phylogenomic study of Deinbollia as has been achieved in several other genera, such as Nepenthes L.f. (Murphy et al., 2020).

The fruits of Deinbollia onanae are similar to those of other species of the genus, i.e., fleshy, indehiscent and large-seeded, suggesting that the now intermittent distribution of this species, along a line c. 570 km along peaks of the Cameroon Highland line, was likely due to dispersal in the gut by animals. Chimpanzees (Pan troglodytes ellioti) and putty-nose monkeys (Cercopithecus nictitans) are known to disperse the species at one location however these species do not cross from one forest patch to another, especially when as now these patches can be separated by tens of kilometres of secondary grassland. Formerly the range of Deinbollia onanae may have once been more continuous along the mountain range than today, but it was likely greatly reduced when forest was cleared for agriculture as reported above.