Uvariopsis dicaprio (Annonaceae) a new tree species with notes on its pollination biology, and the Critically Endangered narrowly endemic plant species of the Ebo Forest, Cameroon

Key to the species of Uvariopsis (and Dennettia) in Cameroon

• 1. - Crushed leaves emitting a strong citrus scentU. citrata

• - Crushed leaves without citrus scent2

• 2. - Leaf blades 7.2 – 15.5( – 18) cm long; pedicel 0 – 7( – 9) mm long3

• - Leaf blades (11.1 – )16.3 – 38( – 61.5) cm long, pedicel (3 – )8 – 60( – 450)mm long 6

• 3. - Flowers cauliflorous, pedicel 0 – 2 mm longU. sessiliflora

• - Flowers ramiflorous, pedicel (0 – 2)3 – 11 mm long, sometimes cauliflorous4

• 4. - Flowers bisexual, petals 3 ( – 4)Dennettia tripetala

• - Flowers unisexual, petals 45

• 5. - Young branches glabrous or very sparsely pubescent, petals freeU. congensis

• - Young branches densely to sparsely pubescent, petals basally fused U. zenkeri

• 6. - Petals basally fused7

• - Petals free10

• 7. - Petals 3U. congolana

• - Petals 48

• 8. - Flower buds globose, monocarps verrucoseU. pedunculosa

• - Flower buds conical to pyramidal, monocarps smooth9

• 9. - Sepals 5 – 10 mm long, flowers completely covering base of trunk, generally occurring above 800 m a.s.l.U. submontana

• - Sepals 2 – 4 mm long, flowers partially covering base of trunk, generally occurring below 800 m a.s.l.U. korupensis

• 10. - Flowering pedicels 3 – 8 mm long11

• - Flowering pedicels 10 – 160 mm long12

• 11. - Petals linear, 25 – 45 mm long, more than 6 times longer than wideU. bakeriana

• - Petals elliptic to ovate, 10 – 14 mm long, less than 6 times longer than wideU. etugiana

• 12. - Flower buds globoseU. dioica

• - Flower buds conical or narrowly ovoid to pyramidal13

• 13. - Stems and petioles tomentose, lateral nerves 8 – 13 on each side of the midrib; flowers wine brownU. solheidii

• - Stems and petioles glabrous; lateral nerves 5 – 8( – 9) on each side of the midrib; flowers green-yellowU. dicaprio

Uvariopsis dicaprio Cheek & Gosline sp. nov. Type: Cameroon, Littoral Region, Yabassi, Ebo Forest, 4° 20′ 44″ N, 10° 24′ 33″ E, 849 m alt. Dicam Trail 2000 m from Bekob camp, male fl. 25 March 2008, MacKinnon 51 (holotype K001381842; isotypes MO, YA).

Syn. Uvariopsis ebo nom. nud. (Gosline et al., 2021: 5).

Diagnosis. Similar to Uvariopsis solheidii (De Wild.) Robyns & Ghesq., differing in the stem, petioles and abaxial midrib glabrous (versus tomentose); number of secondary nerves on each side of the midrib 5–8 (versus 8–13); petals yellow-green, (14–) 16 × (5.5–) 9 mm (versus wine brown, 7–10 × 2.5–5 mm).

Cauliflorous, probably monoecious understorey tree 3–4 m tall. Trunk terete, lacking flutes or prop roots, 1.8–2.5 cm diameter at 1.5 m above the ground, bark smooth, dark-brown, with sparse, longitudinal lines of white lenticels (Fig. 1), the crown sparsely branched (Fig. 2). Leafy stems with 3–4 leaves per season’s growth, terete, internodes (1.2–) 1.5–2.8 (–4.3) cm long, 0.15–0.2 cm diam., pale yellow-green, later orangish brown, glabrous. Axillary buds dome-shaped 0.5–0.75 × 1 mm, bud-scales numerous, linear, spreading, densely hairy, hairs simple, appressed, c. 0.5 mm long, colourless or red brown. Leaves distichous, with punctations (minute translucent glands in the interior of the blade), lacking scent when crushed (collection metadata, MacKinnon 51), blades oblanceolate 17.7–20.2 (–23) × (6.4–) 7–7.9 cm, acumen narrowly triangular (0.5–) 1–1.3 cm long, base broadly acute with convex edges, minutely cordate, blade mounted above petiole, margins undulate-sinuous (live & dried), midrib impressed on adaxial surface, inconspicuous, below a groove; on abaxial surface subcylindrical, 1–1.2 mm diam., conspicuous; secondary veins 5–8 (–9) on each side of the midrib, brochidodromous, arising at c. 50° from the midrib, initially straight, then curving in the outer third, uniting with the secondary nerve above to form a looping inframarginal nerve, attaining 3–4 mm from the margin; intersecondary nerves sometimes present, tertiary nerves raised, conspicuous, forming a reticulum with cells 4–5 mm long, quaternary nerves inconspicuous; glabrous (except in bud when densely orange-brown hairy, hairs c. 0.1 mm long). Petiole stout, shallowly canaliculate, c. 4 (–5) mm long, 1.9–2.1 mm diam., narrowing at base and apex, adaxial groove shallow, c. 0.5 mm wide, glabrous. Female inflorescences unknown. Male inflorescences cauliflorous, scattered along the trunk from near ground level to the top of the trunk 2.5–3 m above the ground, each 1–7-flowered (Figs. 1 & 2). Peduncles patent, c. 2 × 2 mm, pale brown, glabrous, bearing sub-umbellate, radiating, 1-flowered partial-peduncles. Partial-peduncles 0.5–2 × 0.9–1.2 mm, terminating in 1–2 bracts subtending a pedicel. Bracts oblong-elliptic, 1.5 × 0.5–0.6 mm, apex acute, outer surface about 50% covered in appressed white hairs c. 0.15–0.2 mm long, inner surface glabrous. Male flowers. Pedicels 1.8–2.5 cm long, 0.1 cm diam., articulated with the partial-peduncle, with (0–) 1 (–2) scattered, bracteoles in the proximal few mm. Bracteoles similar to the bracts, ovate-oblong, shortly sheathing, (1–) 1.25 × 1 mm, outer surface with sparse scattered simple appressed translucent hairs 0.05–0.2 mm long, buds narrowly ovoid to pyramidal, c.16 × 11 mm. Sepals 2, opposite, drying pale brown, reflexed, semi-orbicular, 1–1.5 × 2.1–2.5 mm, glabrous. Petals 4, uniseriate, free, thinly leathery, pale, glossy, yellow-green when live (Fig. 1), drying black, lanceolate-oblong, (14–) 16 × (5.5–) 9 mm, not fleshy but c. 0.25–0.3 mm thick, apex rounded, base rounded, outer surface sparsely and inconspicuously hairy, hairs 7–9 per mm² (5% of surface covered), simple, translucent, appressed, c. 0.1 mm long, apices rounded. Inner surface of petals smooth, non-tuberculate, with a shallow elliptic-oblong excavation c. 8 × 5 mm, the margin of the excavation raised, the apex with a ridge extending along the midline to the petal apex, glabrous apart from a few scattered erect, minute white hairs 0.05 mm long at the excavation apex. Staminal dome 3.5–4 mm long, 3.5–4 mm diam., consisting of stamens and a receptacular torus. Stamens shortly cylindrical-angular, c. 0.5 × 0.1 (–0.2) mm, connective with two lateral extrorse longitudinal anther cells, each exceeding the connective. Apical connective appendage absent. Female flowers, fruit and seed unknown. Figs. 1–3.

DISTRIBUTION. Cameroon (Fig. 4) endemic to the Ebo Forest of the Littoral Region on present evidence.

HABITAT. Uvariopsis dicaprio is so far only known from lower submontane forest (850 m elev.). below the elevation for the upper montane forest indicator species Podocarpus latifolius (Thunb.) R.Br. ex Mirb. The geology is ancient, highly weathered basement complex, with some ferralitic areas in foothill areas which are inland, c. 100 km from the coast. Altitude varies from c. 200 m to 1,200 m elevation. The wet season (successive months with cumulative rainfall >100 mm) falls between March and November and is colder than the dry season. Average annual rainfall at Bekob measured 2010–2016 is 2,336 mm (E. Abwe, 2018 Ebo Forest Research Programme, Cameroon, personal communication, Abwe & Morgan, 2008; Cheek et al., 2018a).

CONSERVATION STATUS. Uvariopsis dicaprio is currently known from a single specimen with all male flowers at a single location inside the mid-eastern part of the Ebo Forest (Fig. 4). Less than 50 mature individuals have been observed (B. Morgan, 2021, personal communication), despite the species being highly conspicuous in flower (Fig. 1) and situated on a major footpath close to a research camp used by many biologists over the last 15 years.

Since 2006, botanical surveys have been mounted almost annually, at different seasons, over many parts of the formerly proposed National Park of Ebo. About 2,500 botanical herbarium specimens have been collected, but this species has not yet been seen elsewhere in the c. 2,000 km² of the Ebo Forest. However, the area outside the two research camps, especially the western edge, has not been fully surveyed for plants. While it is likely that the species will be found at additional sites within the Ebo Forest, there is no doubt that it is genuinely range-restricted as are some other species of Uvariopsis in Cameroon (see “Introduction”). Botanical surveys and other plant studies for conservation management in forest areas north, west and east of Ebo resulting in tens of thousands of specimens being collected and identified have failed to find any additional specimens of this species (Cheek et al., 1996; Cable & Cheek, 1998; Cheek, Onana & Pollard, 2000; Maisels, Cheek & Wild, 2000, Harvey et al., 2004; Cheek et al., 2004; Cheek, Harvey & Onana, 2010; Harvey, Tchiengue & Cheek, 2010; Cheek, Harvey & Onana, 2011).

The area of occupation of Uvariopsis dicaprio is estimated as 4 km² using the IUCN preferred cell-size. The extent of occurrence is the same. In February 2020 it was discovered that moves were in place to convert the forest into two logging concessions (e.g. https://www.globalwildlife.org/blog/ebo-forest-a-stronghold-for-cameroons-wildlife/ and https://blog.resourceshark.com/cameroon-approves-logging-concession-that-will-destroy-ebo-forest-gorilla-habitat/ both accessed 12 April 2021). Such logging would result in timber extraction that would open up the canopy and remove the intact habitat in which Uvariopsis dicaprio is found. Additionally, slash and burn agriculture often follows logging trails and would negatively impact the population of this species. Fortunately the logging concession was suspended in August 2020 due to representations to the President of Cameroon on the global importance of the biodiversity of Ebo (https://www.businesswire.com/news/home/20200817005135/en/Relief-in-the-Forest-Cameroonian-Government-Backtracks-on-the-Ebo-Forest accessed 12 April 2021). However, the forest habitat of this species remains unprotected and threats of logging and conversion of the habitat to plantations remain, and mining is also a threat. Uvariopsis dicaprio is therefore here assessed as Critically Endangered, CR B1+2ab(iii), D.

PHENOLOGY. Flowering has been observed in late March and early April (B. Morgan, 2021, personal communication).

ETYMOLOGY. This threatened and spectacular tree is named for the American actor and conservationist Leonardo DiCaprio, who, through several months in 2020, lobbied extensively on social media (e.g. https://www.instagram.com/p/B_0LSAhFRue/?hl=en; https://twitter.com/leodicaprio/status/1257729388314943490?lang=en both accessed 12 April 2021) to draw attention to threats for the numerous rare Ebo species from the logging concession that had been announced at Ebo earlier that year. The concession was cancelled in August 2020, surely partly due to his efforts.

VERNACULAR NAMES & USES. None are known.

NOTES. The distal half of the petals and the margins of the proximal half are flat, wing-like and held against each other (applanate) in bud. In section therefore, the distal part of the corolla will appear cross-shaped (see Fig. 1). This seems to be an extreme form of the petal structure and pyramidal flower bud shape seen in the probably closely related Cameroonian species Uvariopsis korupenis and U. submontana (see results, above). Uvariopsis dicaprio is further distinct from all other species of the genus in that a distinct peduncle is present that bears several branches (partial-peduncles) each of which bears and is articulated with a single pedicel (Fig. 3). Other cauliflorous species of Uvariopsis have few to many-flowered fasciculate inflorescences, a peduncle not being observed, the pedicels arising directly from a perennial woody burr. In non-cauliflorous species of Uvariopsis the inflorescences consist of a single, axillary flower.

It was first intended to name Uvariopsis dicaprio as U. ebo and this name was used in the bioRxiv pre-print (Gosline et al., 2021: 5). However, such pre-prints have no standing as publications for nomenclatural purposes according to the Code (Turland et al., 2018) because they not intended by the authors as the final publication. Therefore Uvariopsis ebo is classed as a nominum nudum.

Pollination biology in Uvariopsis and Uvariopsis dicaprio

Unusual and distinctive features of Uvariopsis dicaprio within the genus include the colour, shape and texture of the corolla. Bright, glossy, pale yellow-green petals are otherwise unknown in a genus where the petals are otherwise dull shades of pink to purple and brown. Unlike in all other species of the genus known, the petals are not thick and fleshy but thinly leathery. The centre of the proximal half of each petal is concave before anthesis, forming a globose chamber for the staminal dome with the other three petals (Fig. 1). On the inner surface of the petal, the concave area is demarcated by an inverted U-shaped, distinct, raised, broad ridge which seems to be the point of contact with those of the other sepals, sealing the chamber. Such a structure has not been reported or observed in other species of the genus.

A striking feature of Uvariopsis dicaprio is the presentation and colour of the flowers. Of the 14 species of the genus in Cameroon, 11 are cauliflorous. All of these except U. dicaprio have petals which are shades of pink, red, purple to brown. Cauliflorous Uvariopsis species present their flowers more or less perpendicular to the trunk; the flowers of U. dicaprio are pendant and with the corolla opening only slightly (see “Results”), and facing the ground (Fig. 1). All species of Uvariopsis other than U. bisexualis Verdc. are monoecious. The majority of Annonaceae species are protogynous hermaphrodites, most often beetle pollinated, some exhibiting thermogenesis (Gottsberger, 2012). In the monoecious U. bakeriana (Hutch. & Dalziel) Robyns & Ghesq. and U. congolana (De Wild.) R.E.Fr. the female flowers mature before the male (Gottsberger, Meinke & Porembski, 2011), and our evidence for U. dicaprio suggests the same sequence. In U. submontana, U. korupensis, U. congolana, U. dioica, and U. pedunculosa, the male flowers are higher on the trunk, with the female flowers clustered towards the base of the trunk. In U. dioica and U. korupensis the female pedicels are generally less than 10 cm long and in U. korupensis the fleshy fruits mature in dense concentrations at the base of the trunk where they can attract ground-dwelling animals.

In Uvariopsis congolana, (Diels) Robyns & Ghesq. and U. pedunculosa (Diels) Robyns & Ghesq. the female globular flowers are born on slender pedicels to c. 50 cm long embedded in the leaf litter. This habit is also exhibited by Isolona cauliflora Verdc. Gottsberger, Meinke & Porembski (2011) studied the visitors to U. pedunculosa (identified as U. congolana) and concluded that pollination likely was by small litter-flies (not beetles). “It is suspected that this predominantly sapromyiophilous species has a pollination system mimicking fungi and/or carcass, and that the pollinating flies normally live on fungi and/or carcass.” They also conclude that U. bakeriana is pollinated by dung-flies. Mertens et al. (2018) studied U. dioica and found minimal visitation by Lepidoptera but more by nocturnal crickets and cockroaches. In all three species of Uvariopsis where pollination studies have been done, the researchers have described the pollinators as scarce and unpredictable, and thermogenesis has not been observed.

In this context, it seems likely that U. dicaprio has found a different pollinator from its sister taxa. The bright pale yellow-green flowers suggest nocturnal pollinators. The similarly glossy, yellow-green flowers of the Asian, widely cultivated ylang-ylang, Cananga odorata (Lam.) Hook.f. & Thomson are pollinated by nocturnal moths and small beetles (Parrotta, 2014). We speculate that the flowers of Uvariopsis dicaprio, unique in the genus, may also be adaptated for moth pollination, otherwise unrecorded in indigenous African Annonacaeae (Gottsberger, 2012). Concerted field monitoring to observe pollinators is needed during the flowering season of Uvariopsis dicaprio to test this hypothesis.

The centre of diversity of Uvariopsis

With the recognition in this paper of Uvariopsis dicaprio, 20 species are now accepted in Uvariopsis (see introduction). The highest species diversity for any country is found in Cameroon, now with 14 species, and with six of these nationally endemic. However, the biogeographic area with highest species diversity is the much smaller area of the Cross-Sanaga Interval which includes 12 species, of which five are globally endemic including Uvariopsis dicaprio. The Cross-Sanaga Interval appears to be the main centre of diversity of Uvariopsis. Numerous other plant genera have their centre of diversity in the interval (Cheek et al., 2001) and some are endemic to it, e.g. Medusandra Brenan (Peridiscaceae formerly Medusandraceae, Breteler, Bakker & Jongkind (2015), Soltis et al. (2007)). The fleshy orange-red fruits of Uvariopsis are consumed by primates, which are thought to disperse their seeds (Dominy & Duncan, 2005). The high level of endemism of Uvariopsis species to the Cross-Sanaga River Interval may therefore be linked to the high number of primate species that are also endemic to the interval, bounded by the rivers Cross and Sanaga that represent barriers to primates. Ten species of primate are confined to the Interval (Kingdon, 2015).

The range of Uvariopsis dicaprio and other endemic species in the Ebo Forest area

Abwe & Morgan (2008) and Cheek et al. (2018a) give overviews of habitats, species and the importance for conservation of the highly threatened Ebo Forest to which Uvariopsis dicaprio is restricted on current evidence. Sixty-eight globally threatened plant species are currently listed from Ebo on the IUCN Red List website (https://www.iucnredlist.org/ accessed 12 April 2021) and the number is set to rise rapidly as more of Cameroon’s rare species are assessed for their conservation status as part of the Cameroon TIPAs programme. The discovery of a new species to science at the Ebo Forest is not unusual. Numerous new plant species have been published from Ebo in recent years. Examples of other species that, like Uvariopsis dicaprio, appear to be strictly endemic to the Ebo area on current evidence are presented in Table 2.

With the exception of Crateranthus cameroonensis Cheek & Prance which is widespread over a large part of eastern Ebo, each of the eight species listed have on current evidence, a single small discreet range of no more than 8 km² (usually far smaller) within the Ebo Forest area (see the references cited in Table 2). These species are not concentrated together in one or several spots but are scattered from the far West to the East of the forest, none of the species, apart from the Crateranthus, sympatric with any of the others.

Further species described from Ebo have proved not to be endemic but to have also been found further west, in the Cameroon Highlands, particularly at Mt Kupe and the Bakossi Mts (Cheek et al., 2004). Examples are Gilbertiodendron ebo Burgt & Mackinder, Myrianthus fosi Cheek (Harvey, Tchiengue & Cheek, 2010), Salacia nigra Cheek (Gosline, Cheek & Kami, 2014) and Talbotiella ebo Mackinder & Wieringa (Mackinder, Wieringa & Burgt, 2010).

Additionally, several species initially thought endemic to Mt Kupe and the Bakossi Mts and adjoining areas in the Cameroon Highlands have subsequently been found at Ebo, e.g. Coffea montekupensis Stoffelen et al. (1997), Costus kupensis Maas & H. Maas (Kamer et al., 2016), Deinbollia oreophila Cheek & Etuge (2009), Microcos magnifica Cheek (2017), and Uvariopsis submontana Kenfack et al. (2003). It is considered likely that additional Kupe species may yet be found at Ebo such as Brachystephanus kupeensis Champluvier & Darbyshire (2009), and Impatiens frithii Cheek & Csiba (2002) since new discoveries are still frequently being made in the Ebo Forest. Therefore, it is possible that Uvariopsis dicaprio might yet also be found in the Cameroon highlands, e.g., at Mt Kupe. However, this is thought to be only a relatively small possibility given the high level of survey effort at Mt Kupe: if it occurred there, it is highly likely that it would have been recorded already since it is so spectacular when in flower that it would be difficult to overlook.