Saxicolella Engl. ( Engler 1926: 356 )

Cheek, Martin, Molmou, Denise, Magassouba, Sekou & Ghogue, Jean-Paul, 2022, Taxonomic revision of Saxicolella (Podostemaceae), African waterfall plants highly threatened by Hydro-Electric projects, Kew Bulletin 77 (2), pp. 403-433 : 405-410

Saxicolella Engl. ( Engler 1926: 356) ,

non J.B. Hall (1971: 122); non Ameka et al. (2002).

Type species: Sapicolella nana Engl.

Pohliella sensu Taylor quoad P. flabellata ( Taylor 1952: 52) . Heterotypic synonym.

Rheophytic herbs. Roots ribbon-like and/or disc-like, crustose, highly dorsiventrally flattened, to at least five times as wide as thick, adhering to the substrate by root hairs on the ventral surface, rootcaps and haptera absent. Shoots erect, minute and supporting sessile leaf rosettes, the stem then not visible, then arising from the margins of the radiating ribbon-like part of the root or, ( S. futa ) the sinuses of the bifurcations of the ribbon-like root OR up to several cm long, unbranched or branched, arising from either the centre of the disc-like crustose part of the root. Leaves with spiral phyllotaxy, bases sheathing where known, with one or a pair of acute basal stipules in leaves subtending spathellae (stipules absent in S. futa and often in proximal leaves on a stem of other species), blades filiform or flattened, usually entire, rarely bifurcate (or trifurcate) in S. flabellata and S. nana respectively, blades reduced or rudimentary in S. deniseae and S. marginalis or absent in S. futa . Flowers single, terminal on shoots, rarely in clusters on main stem ( S. angola , S. flabellata ). Spathellae ellipsoid, sessile, rarely globose ( S. ijim ), apex often with mucro. Flowers erect in intact spathellum, held completely partly within the opened spathellum at anthesis except in S. nana and S. sp. A. Pedicel accrescent in fruit. Tepals 2, filiform rarely spatulate (sometimes spatulate in S. ijim ), flanking the stamen. Stamen single, exceeding ovary, thecae often divergent. Pollen in dyads. Gynophore present (except S. sp. Aand S. ijim ). Ovary unilocular, ellipsoid, not laterally compressed, isolobous, erect, 6 or 8- ribbed in fruit, ovules numerous around a columnar axil placenta, septum not detected. Stigmas 2, botuliform to filiform or complanate. Fruit dehiscing into two equal, persistent valves. Seeds ellipsoid, mucilaginous.

Discovery

The first published and type species of Sapicolella , S. nana , was collected in Kamerun, then a German colony, now Cameroon, in January 1913 by the renowned botanist Mildbraed ( Engler 1926). In 1922 Gossweiler in Angola first collected material of the species published in this paper as S. angola Cheek. Keay , collecting in eastern Nigeria in 1938 and 1950, made the specimens that became the basis of S. flabellata (G.Taylor) C.Cusset (originally published as Pohliella ), and S. marginalis (G.Taylor) C.Cusset ex Cheek (originally published as the monotypic Butumia ). In 1998 the first author collected in Cameroon and misidentified as Ledermaniella cf musciformis the species published in this paper as S. ijim Cheek. Then , in Guinea-Conakry in Jan. 2018 he collected the material of the species named here as S. futa Cheek sp. nov., together with the second author. The second and third authors then went on in Feb. 2018 to collect the species described as S. deniseae Cheek sp. nov. Sapicolella sp. Aonly came to our attention as this paper was being concluded in mid- 2021, thanks to photos via GBIF.org of recent collections by the LBV-MO botanical team.

The new species published in this paper are unlikely to be the last added to the genus. It is expected that botanical survey of the many rapids and waterfalls of Africa that have never been inspected for Podostemaceae will produce additional species new to science if this can be done before they are modified by the hydro-electric projects which are likely to result in their extinction.

Morphology

While species of several other genera of African Podostemaceae have been investigated in detail for their morphology and anatomy in such studies as Moline et al. (2007) and Thiv et al. (2009), this has not been the case for any of the species of the genus Sapicolella Engl. as delimited here (the Ghanaian species previously referred to as Sapicolella have been transferred to Pohliella , see Cheek 2020). None of the species appear to have been investigated anatomically, nor has their micromorphology been investigated under the electron microscope. The overview present- ed here is partly based on the protologues of the species already published by Engler (1926) & Taylor (1952), but mainly from the observations of the authors of the four new species described below.

Root. The root (thallus) is either crustose and/or with several, ± broadly ribbon-like arms radiating from a central crustose area (rarely absent/not detected e.g. Sapicolella futa ). It is usually several times wider than thick, and is closely appressed to the substrate of smooth rock to which is firmly fastened by numerous short root hairs. A faint raised ridge running along the midline of the rootribbon of S. futa suggests that as in Inversodicraea ( Cheek et al. 2017b) , a single, central vascular bundle is present. Photosynthesis seems to be mainly performed by the ribbon-like roots since these make up most of the surface area of the plants, in fact>90% of the area in almost all species. Root-caps have not been reported nor observed, but are in any case not usual in those Podostemaceae genera with crustose and broad ribbon-like roots. Nor are haptera, also known as hold-fasts, present. Roots are neither recorded nor preserved in the available material of S. angola , and are incompletely known in S. nana and S. flabellata . The ribbon-like roots of individuals appear to radiate out from the central point of establishment, presumably where a seed has germinated and established. In contrast, in S. nana the radial growth appears to be “crustose”, that is, not in the form of distinct separate ribbon-like structures, but a solid mass which extends outwards more or less evenly along the circumference, with only slight lobing at the margins.

In most species, e.g. Sapicolella deniseae , and S. marginalis , the root is intermediate: it has both a central crustose part several centimetres in diameter, but also the margins are well-developed into radiating ribbon-roots. In S. futa the central crustose part if developed at all, must be small and only a short-lived stage which is lost by fruiting time (if it is developed in the first place), leaving the radiating roots disconnect- ed from each other at the centre.

In most species the ribbon-like, radiating roots rarely ( Sapicolella deniseae , S. marginalis and S. ijim ) branch, when they bifurcate into two equal branches. However, in S. futa the branching is frequent and regular and the roots form a distinctive pattern. In fact, each species of Sapicolella can be identified by the architecture and grossmorphology of its root alone (where known), although this can be difficult to convey in words.

Shoots. The origins of the shoots from the roots and their development, follows one of three patterns:

1. the shoots arise only from the central, more or less disc-like, crustose part of the root, and not from the radiating ribbon-like roots. The shoots form visible stems with measurable internodes. Sapicolella nana , S. flabellata , S. ijim and, possibly, (root unknown but visible stems present) S. angola .

2. The shoots arise only from the margins of the radiating, ribbon-like roots. The shoots are sessile, not forming visible stems but supporting an inconspicuous rosette of reduced leaves and a terminal spathellum. Sapicolella marginalis , S. deniseae , S. sp. A

2. The shoots arise only from the synusiae of the bifurcations of the radiating, ribbon-like roots. As in 2, the shoots are sessile, not forming visible stems. Sapicolella futa .

These three shoot position patterns appear to have value in supporting generic delimitation in Asian podostemoids ( Koi et al. 2012: 375), pattern 1=”D” (dorsal surface of root)”; pattern 2=”P ( Paracladopus - type)”; pattern 2=”C (Cladopus -type)”; ( Koi et al. 2012).

The shoot patterns appear to correlate with the three root patterns (see Roots, above). The taxonomic significance is discussed below.

In those species where visible stems are developed, they are erect, terete, and in those species where they exceed more than 5 mm long, sparingly branched. In Sapicolella ijim , the stems are robust and free-standing at anthesis. This species was found in the spray zone of a waterfall (Cheek pers. obs.) and is not supported by water as appears to be the case of the more laxly stemmed S. flabellata which has the longest (21 cm) stems in the genus, described as flowing in the protologue ( Taylor 1952).

Leaves. The phyllotaxy is consistently spiral. The leaves are best developed in the species with pattern 1 shoot position, where visible stems are developed. The largest leaves are those of Sapicolella flabellata which are flabellate (dorsiventrally flattened with radiating lobes) and up to 2 cm long, 2 cm wide. Each leaf bifurcates or trifurcates up to four times, the ultimate segments are capillary. The base is sheathing. Stipules are inconspicuous.

Leaves in Sapicolella angola are poorly preserved, smaller, but otherwise similar, with fewer bifurcations and with stipules conspicuous. In S. nana the leaves are filiform-capillary and trifurcate, while those of S. ijim are unbranched and laterally compressed.

In pattern 2 species, Sapicolella marginalis and S. deniseae , whilst the shoots are reduced and visible stems are not formed, the leaves appear reduced to the sheathing, stipulate base with only a rudimentary blade, while in S. sp. A, the linear blade is as long as the flower

In pattern 2 Sapicolella futa , the leaves are reduced further, to inconspicuous, minute 0.2 mm long concave sheaths with stipules and blade not developed.

Leaves of the type usual in African podostemoids are absent — that is, those which are filiform, terete and bifurcate repeatedly in the distal half, and which are shed before anthesis.

Inflorescences. In all species flowers occur singly at the apex of shoots except in Sapicolella flabellata and S. angola where they are in terminal clusters. The developing spathellae are protected by the subtending leaves in the earliest stages. In fact, the leaves appear to function primarily as protective bracts in most of the remaining species of the genus. The spathellum varies from globose ( S. ijim ) to narrowly ellipsoid, sometimes with a small apiculus. It lacks a distinct stipe.

The flower is erect and held within the opened spathellum at anthesis. Generally, only the styles and anthers are exserted from the ruptured spathellum but sometimes all or part of the ovary is projected from the spathellum. However, in Sapicolella nana and S. sp. A. the ovary can be projected on a naked pedicel as long as itself. Ashort pedicel, two filiform (rarely spatulate) tepals that flank the single stamen, and a short gynophore are present (absent in Sapicolella sp. A ), all concealed within the ruptured spathellum at anthesis. The anther-thecae often face away from each other (latrorse). Pollen is dyad (where available for study).

The ovary is either ellipsoid, e.g. Sapicolella ijim , S. futa , S. marginalis , or narrowly ellipsoid ( S. flabellata , S. deniseae , S. nana , S. angola , S. sp. A). In the fruit there are eight longitudinal ribs extending from base to apex ( S. flabellata , S. marginalis , S. deniseae ) or the commissural ribs are not developed, when only 6 ribs are developed ( S. angola , S. nana , S. futa , S.ijim ).

The two stigmas are filiform or narrowly botuliform ( Sapicolella nana , S. sp. A, S. angola , S. flabellata , S. deniseae ) or they are complanate (flat) and about as broad as long ( S. futa , S. marginalis , S. ijim ).

The free-central axile placenta in the unilocular ovary is either narrowly spindle-shaped e.g. Sapicolella angola , S. nana , S. futa or broadly so, occupying about half the radius of the locular cavity in S. ijim . The seeds are all ellipsoid, completely covering the placenta, where known.

The fruit, as the ovary, is fully erect, and isolobous (the two valves are equal). The fruit is carried further out of the spathellum remains by the extension of the pedicel post-anthesis. The two valves dehisce but usually persist in the fruit. The seeds are mucilaginous where known as usual in the family.

DISTRIBUTION. Tropical West Africa: Guinea, Nigeria, Cameroon, Gabon and Angola.

Eight species. Sapicolella species are restricted to Africa and extend from the Guinea Highlands of Guinea-Conakry in west Africa (newly recorded here) to Angola (newly reported here) in western southcentral Africa. They are not recorded from the Congo basin, nor eastern Africa.

The geographic range of the genera Talbotiella Baker f., (Leguminosae, nine species of evergreen tree) recently also extended to Guinea ( van der Burgt et al. 2018), is similar to that of Sapicolella although that genus does not extend to Angola ( Mackinder et al. 2010). Mischogyne Exell ( Annonaceae trees, five species, Gosline et al. 2019) also has a similar distribution but has an outlying species in Tanzania and one in DRC. The highest species diversity of Sapicolella is the Cross-Sanaga River interval of eastern Nigeria-western Cameroon which has three of the eight species: S. marginalis , S. flabellata , and S. ijim . The Cross-Sanaga River interval area contains the highest species and generic diversity of flowering plants per degree square in Tropical Africa according to several studies (Barthlott et al. 1996; Dagallier et al. 2020) possibly in part because it corresponds with the Cameroon Highlands ( Cheek et al. 2001). Many of the species and some genera (e.g. Medusandra Brenan ( Peridiscaceae , Breteler et al. 2015; Soltis et al. 2007) are both endemic and threatened. Sapicolella species are known only from the five countries mentioned but are likely to be found in intervening areas such as Sierra Leone, Liberia, Ivory Coast and Congo- Brazzaville. Of the eight known species, four are point endemics.

HABITAT. Sapicolella only grows, as with most Podostemaceae , in sites with seasonally or permanently, fast-flowing, well aerated, silt-free fresh water. They are always associated with waterfalls and rapids. Unusually among African Podostemaceae genera, about half the known species of Sapicolella occur mainly in the 700 – 1300 m altitudinal range, when other genera are predominantly restricted to lowland elevations. However, S. nana , S. flabellata , S. deniseae and S. sp. Aall occur in the (100 –) 300 – 700 m altitudinal band. The species of the genus appear to avoid coastal areas. Although Cameroon has the highest species diversity of both Sapicolella and Podostemaceae in Africa, Sapicolella is absent from the most species-diverse Podostemaceae site (which has 10 species) the Lobé Falls near Kribi, at the coast in the lowland evergreen forest belt ( Cheek et al. 2017b). However, all but one of the eight species of Sapicolella co-occur at least once with one or several other species of Podostemaceae (see individual species accounts). The exceptions is S. ijim , which is was not observed to occur with other Podostemaceae , possibly because of its unusual ecological niche. Sapicolella ijim is unique in the genus in that it flowers in the sprayzone of a waterfall, and it is not immersed in water immediately before flowering as is usual in other species. However, Ledermanniella prasina J.J.Schenck & D.W.Thomas of the Korup has the same ecology ( Schenk & Thomas 2003) and L. letouzeyi C.Cusset of the Bakossi Mts can also occur in the spray-zone of waterfalls although not exclusively as does Sapicolella ijim ( Cheek et al. 2003) .

Pollination & Hybridisation

Although we suspect that pollination is by flying insects such as bees, as reported in other African podostemoids ( Cheek et al. 2017b), no floral visitors have been reported or observed thus far for any Sapicolella species. Hybridisation, reported for the first time in African Podostemaceae in Cheek et al. (2017b) is not known in Sapicolella . Since none of the species is sympatric, this is not unexpected.

Habitat partitioning

In those four species of Sapicolella that co-occur at sites with other Podostemaceae species, it has not been possible to study habitat partitioning except for Sapicolella futa at one site in Guinea:

Case study: Salaa Falls, Futa Djalon, Guinea-Conakry At this site four species of Podostemaceae occur in close proximity some tens of metres downstream from the main tourist falls. At one point, all four can be found within a 1 m by 1 m square. When observed by MC and DM in Jan. 2018, midway through the dry season, Stonesia heterospathella G.Taylor was in fullflower, having been exposed by the slowly falling water in recent weeks, while Ledermanniella guineense C.Cusset , growing deeper in the water than any other species, was just beginning to flower. Highest up the gradually sloping flat rock surfaces were colonies of Tristicha trifaria Spreng. , long dead. Sapicolella futa , also long dead, grew on the rock surface 20 – 100 cm above the level of the water surface, in a band below the Tristicha and above the Stonesia , plants of the two species intermingling at the interfaces. This same zonation, with Tristicha (above) and Stonesia (below) the Sapicolella futa was also seen just above the main Kambadga Falls near Pita, where Sapicolella futa was much rarer. Sapicolella futa appears to grow or compete better in slightly deeper water, than the Tristicha , and needs a shorter growing season (a shorter period underwater) than both the Stonesia and Ledermanniella .

Conservation status

The principal threats to Sapicolella species apply to Podostemoideae species as a whole, especially in Africa. Because they are restricted to habitats with clean, non-turbid, aerated water, with a rock substrate, degradation of any these environmental factors pose threats. Given that so many Podostemaceae species, including Sapicolella , are restricted to only one or two locations, they are especially at risk. Athreat at even one location is likely to pose a high extinction risk for any Sapicolella present. All of the species are provisionally assessed as either Endangered or Critically Endangered using the IUCN 2012 standard.

Turbidity & eutrophication threats

Turbidity in the water, indicating that silt is present, can reduce establishment of seedlings ( Philbrick & Novelo 1995). It can also reduce photosynthesis during the main growth period, when plants are under water in the wet season ( Cheek et al. 2015).

Algal growth can blanket Podostemaceae plants at some sites and reduce their ability to photosynthesise. Such growth appears to be associated with nutrient addition to rivers from human populations that may use water courses for processing crops, cleaning, and removal of waste-products. Sapicolella futa (this paper) appears to be threatened in this way.

Hydroelectric Power Project threats

The greatest threats of global extinction for species of Podostemaceae such as those of the genus Sapicolella are from hydroelectric projects which have been growing rapidly in number in recent years as a source of cheap, greener energy in Africa. They are attractive

to investors and governments being seen as sustainable and a good alternative to hydrocarbon-sourced energy. While hydroelectric projects have many environmental benefits compared with alternative options, all too often they threaten Podostemaceae species with extinction, and there are now many documented cases of local and global extinctions of Podostemaceae species resulting from such projects ( Cheek et al. 2015; Cheek et al. 2017b; Couch et al. 2019).

Dams for hydro-electricity generation are construct- ed just above rapids or falls so as to benefit from the vertical drop in water levels (the “head”) at these sites. The construction of the dams may directly impact upon the falls and the species that they contain. More usually dams negatively affect populations of Podostemaceae through changes in water flow by four different threats:

1) Reduction of water flowing over falls at the dam site;

2) Impounding of water by the dam creates a large reservoir of motionless, non-aerated water in which Podostemaceae cannot survive;

2) Disruption downstream of natural seasonal fluctuations in flow;

3) Cascade hydro projects which destroy all Podostemaceae habitat along the length of a river.

These four threats are expanded in detail in Cheek et al. (2017b).

Cascade systems are steadily being developed in the Cuanza of Angola, where two of the four global locations of Sapicolella angola are thought to have been lost even before the species is formally named (see that species), in the Ogooué of Gabon which will threaten S. sp. A (see that species), and also in the Konkouré of Guinea which may already have destroyed the only known global population of S. deniseae .

Difficulties with EIAs for Podostemaceae

It is extremely rare that competent Environmental Impact studies (EIA) are requested and conducted in advance of planning for such hydro projects in our experience. If EIA studies are conducted, they usually do not take into account the possible presence of Podostemaceae at these sites: many botanists mistake these flowering plants for mosses or algae (groups of plants usually regarded as non-threatened) and do not collect samples for identification so that dam construction goes ahead in ignorance of the presence of these often highly threatened species. Even if such studies have been done in advance, and samples collected from which Podostemaceae can be identified, two further obstacles exist 1) many Podostemaceae have out-of-date Red List assessments which often misrepresent the species as being of low or unthreatened status when they may be highly threatened and 2) most Podostemaceae species remain without a Red List assessment. Unless species can be shown to have a published Red List assessment of EN or CR on iucnredlist.org, or an extent of occurrence of <50,000 km 2, they are generally not considered to merit concerted conservation action in projects by the International Finance Corporation of the World Bank Group that often supports finance of such projects ( IFC 2019).

PHENOLOGY. Species of the genus generally flower as water levels drop after the rainy season, exposing the plants that have developed underwater in previous months, and triggering flowering, and seed set, and if the plants become dried out, death. Sapicolella futa is thought to complete its life-cycle in 6 months or less (see that species), but other species, such as S. ijim , may prove to be perennial if they are kept moist by waterfall spray throughout the dry season.

ETYMOLOGY. The name Sapicolella is compounded of saxicole, meaning ‘dweller on rock’ and — ella a diminuitive. The whole signifies “little dweller on rock”. However, almost all Podostemaceae always grow on a rock substrate, and many are diminuitive.

VERNACULAR NAMES. None have been recorded. Generally, e.g. in Guinea, local communities do not have terms for different species of the genus at a location, but one term, treating the family as one entity (Cheek pers. obs, Guinea 2018, 2019).

Infrageneric classification. Thespeciesfallintothreegroups strongly supported by root and shoot type and pattern, and by leaf characters. It can be argued that the three groups of species within Sapicolella sensu stricto could each be recognised as separate genera since in Asia, the same grouping characters (shoot position) have been found useful for this purpose ( Koi et al. 2012, see above under shoots). Moreover, this argument is strengthened by the correlation of root characteristics with these same groups (see above), but with no correlated floral or fruit characters. However, weare reluctant to increase the numberof genera if there is an alternative option. Therefore, we have optedto recognise these three groups at subgeneric rather than generic level. Should molecular phylogenetic work support generic recognition (e.g., by long branches with high support values), consideration might then be given to elevate these subgenera to generic level. This would necessitate resurrection of the generic name Butumia G.Taylor (here adopted as a subgeneric name) and elevating the subgeneric name Kinkonia (proposed below for the eccentric Sapicolella futa species of the Futa) to genericlevel. However, it is possiblethat these groupings are the result of convergence and have no phylogenetic value.

Sapicolella sensu stricto, sampled from Cameroonian material, is embedded within and near the base of the major clade of African podostemoids and is sister to all other African genera apart from Inversodicraea R.E.Fr. and Monandriella Engl. ( Koi et al. 2012). The sister relationship of Sapicolella and Monandriella shown by Koi et al. (2012) was foreshadowed by Engler who in

his global treatment of Podostemaceae placed these two genera consecutively ( Engler 1920: 29).

Identification Key to the species of Saxicolella

1. Floweringshoots (0.9 –) 3 – 10 (– 21) cmlong… ........................................... 2

1. Flowering shoots sessile or <0.5 cm long................................................. 3

2. Flowering shoots to 21 cm long; leaves dorsiventrally flattened, flabellate, bifurcating three times. Nigeria ... ......... ......... ........ ......... .......... ........ ...... 1. S. flabellata

2. Flowering shoots to 7 cm long; leaves if flabellate, bifurcating only once. Cameroon and Angola....... 2

2. Flowering shoots (1 –) 3 – 7 cm long, each with 3 – 6 spur branches; flowers single, terminating the short shoots. Cameroon ............................................................. 2. S. ijim

2. Floweringshoots 0.9 – 1.5 cmlong, unbranched; flowersinterminalcluster. Angola ......... 3. S. angola

3. Roots 0.2 – 0.5 (– 0.8) mm wide, bifurcating at intervals of 1.5 – 2.2 mm; shoots with spathellae single at the sinuses of bifurcations. Guinea.................................................. 7. S. futa

3. Roots 1.8 – 3 mm (or more) wide, not, or rarely, bifurcating; shoots with spathellae closely spaced in centre of crustoserootsoratedgeof ribbon-likerootsbutneveratthebifurcations ........................ 5

5. Shoots several, stems distinctly visible, clustered in centre of the disc-shaped crustose root; distal leaves 1.5 – 6 mm long, divided 1.5 mm from the base into (2 –) 2 (– 3) filiform segments; Cameroon...... 4. S. nana

5. Shoots without stems distinctly visible, in rows along the margins of the ribbon-like roots; distal leaves entire, not filiform....................................................................... 6

6. Leaves linear, flattened, exceeding the flower in length; pedicel at anthesis fully exposed, as long as ovary; ovarysessile (gynophore absent). Gabon ........................................... 8. S. sp. A

6. Leaves triangular or scale-like, far-shorter than the flower; pedicel at anthesis concealed inside the spathellum, far shorter than ovary; gynophore present................................................ 7

7. Shoots with 5 – 7 ± isomorphic subulate leaves, which lack a large concave orbicular or elliptic basal part; leaves exceeding the ovary in length; stigmas complanate. W Cameroon and SE Nigeria......... 5. S. marginalis

7. Shoots with 2 heteromorphic leaves, composed mainly of a concave orbicular or elliptic basal part; leaves all far shorter than the ovary; stigmas botuliform. Guinea................................. 6. S. deniseae