The Pteridaceae family diversity in Togo

Abstract Background The Pteridaceae family is the largest fern family in Togo by its specific and generic diversity. Like all other families of ferns in the country, Pteridaceae are poorly studied and has no identification key. The objective of this study is to perform a taxonomic revision and list establishment of this family of leptosporangiate ferns in the light of current available knowledge about the family. Pteridaceae was also assessed in terms of its diversity and conservation status, this was conducted through the recent field data and the existing herbaria specimens. The current study permits to confirm the presence of Pteris similis Kuhn. which brought the number of Pteridaceae to 17 in Togo. New information This study provides first local scientific information about the fern flora of Togo. It confirmed the presence of Pteris similis Kuhn. in Togo and brought the Pteridaceae family diversity to 17 species. A species identification key is provided for the easy identification of the Pteridaceae of Togo.

The Pteridaceae occupies aquatic and terrestrial environments. They are usually terrestrial, but sometimes aquatic, epilithic and epiphytic. However they abound in the humid tropics, the family includes several cosmopolitan species. They have a long or short rhizome, creeping, ascending, sub-erected or erected, and have splinters (more rarely hairs). They have a monomorphic limb, hemi-or rarely dimorphic, simple, pinnate, pedaled, sometimes decurrent; free and simple veins, or sometimes anastomosed, forming a network. The Sporangia are grouped in marginal or intra-marginal sori, without true indusium, often protected by the reflected margin of the lamina, or arranged along the vein. Each sporangia has a vertical and interrupted annulus, with a little or no visible receptacle.
The family is well present in Togo but few studies hitherto focused on it. The current data of the country's biodiversity (MERF 2009) shows a diversity represented almost in its entirety within the ecological zone 4 of Togo (the guineean forest zone of the country, according to Ern (1979) ecological classification of Togo) for all Monilophytes.

Study area
The study area is Togo. It is located in the Gulf of Guinea, and surface covers approximately 56 785 km . Its forest surface is counts among the least in the West African sub-region.
Three main types of climate are found in Togo. In the North, there is the tropical climate with variations increasingly wet, going to the South. The southern coastal area has a subequatorial climate. A transitional climate between these two types is found in the mountains of the south. Togo has varied soils. There are five main soil classes (Levêque 1979) which are: 1 / the tropical ferruginous soils, leached, indurated or waterlogged, 2 / slightly evolved alluvial soils or erosion intake, 3 / vertisols rich in swelling clay and mineral elements, 4 / ferralitic soils characterized by the persistence of iron and aluminum and other cations leaching (these are the best soils in the country), 5 / hydromorphic gley soils, clayey, poorly drained, encountered the edge of river mouths and some depressions. The relief consists essentially of two large plains separated by a strip of mountains which takes the country in scarf from the Southwest to the Northeast. The plains are mostly covered with savanna and patches of dry forest. The "Togo" Mounts are covered by dry forest in their northern part and rain forest in the southern part. This last part constitute the Togolese portion of the West African's rainforest and is the ecological zone 4 (Ern 1979). Indeed, Togo is divided into five ecological zones characterized by their climate, vegetation and soil type (Fig. 1).
There have been new harvest in the ecologic zone 4 of Togo in order to enrich the plant materials available for this study.

Materials
The study is based on new harvests from the ecological zone 4 (215 specimens) and specimens from herbaria of the University of Lomé (TOGO) (87 specimens) and the National Museum of Natural History in Paris (P) (122 specimens).

Methodology
New harvests were conducted along the banks of the natural ecosystem's streams in the study area along a topographic gradient. As many others authors, Moran (1995) works on the ecology of African ferns have indeed demonstrated fern's preference for mountainous rainforests and the banks of rivers.
Data from this new inventory is coupled with ecological and geographical data from previously performed harvests between 1973 and 1994 across the country and available in the RIHA data base (African Herbaria Computer Network) of the herbarium of Lomé. Togo ecological zones.
Ecological Zone 1: Refers to the Northern Plains. It enjoys a Sudanese climate characterized by an average of 6 to 7 months of drought. Rainfall varies from 800 to 1000 mm and water per year. The temperatures are between 17 and 39° C. The predominant vegetation is the Sudan savanna with few islands of dry forests and gallery forests. The soil is tropical ferruginous, sandy.Ecological Zone 2: It is covered with a mosaic of dry forests of mountain and forest galleries. The climate is Sudano-Guinean. The rainy season extends from April to October and the dry season is characterized by the presence of the Harmattan, a dry and cold wind. Rainfall is irregular and reaches 1200-1300 mm of water per year. The soils are thin and contain a high proportion of coarse elements. Ferruginous tropical soils are also present.Ecological Zone 3: It corresponds to the Guinean savannas of central area plains enjoying a tropical climate with a rainy season extends from May to October. Rainfall varies between 1200 and 1500 mm per year. The temperature is between 25 and 40° C. The soils are mainly ferruginous. Semi-deciduous forests are found in the southern part and dry forests in the northern part.Ecological Zone 4: This corresponds to the southern part of the Mount "Togo" and has a sub-equatorial climate of transition, characterized by a long rainy season from March to October with a small interruption in August or September. Rainfall varies between 1300 and 1600 mm per year. The vegetation is constitute of rainforests, on deep red lateritic soils.Ecological Zone 5: It is the South of the coastal plains area, with a sub-equatorial climate, characterized by a lack of rainfall in it's southern part. Rainfall varies from 800 mm at the coast up to 1200 mm per year at the northern limit of the zone. The vegetation is composed by a mosaic of savannah, farmland and dry forests (Kokou and Caballé 2000).
Each harvest consists of one or more photos of the whole plant in its habitat, a herbarium specimen represented by the whole plant (or a fragment then comprising parts of all organs) and a piece of lamina in silica gel (Gaudeul and Rouhan 2013) for future genetic studies. For epiphytic taxa, a fertile sample of the porophyte is also collected. The identification of new specimens was then performed thanks to the flora of Cameroon (Tardieu-Blot 1964) and Southern Africa (Roux 2001). The specimens are then identified and associated with specimens already available in herbaria of Paris and Lomé. The observed classification of the taxonomy is the one established by Christenhusz et al.  Distribution of Pteridaceae in Togo. Zones 1 to 5 indicated on the map correspond to the ecological zones of Togo as defined by Ern (1979).
The Pteridaceae family diversity in Togo (2011). The list of synonyms used comes from the online database of "The Plant List" (The Plant List 2015).
The morphological observations of all available specimens (new specimens and old herbarium collections) enabled the establishment of a list of morphological descriptors which have been added to the ecological characteristics of each species (Table 1). These descriptors are integrated in a knowledge base through the Xper² software.
Xper² is a free software for management, editing, and analysis of taxonomic knowledge bases (Ung et al. 2010).
All species identified as a result of the study and the identification of all available specimens were then associated with the states of the descriptors that characterize them. This same approach was also used by Corvez and Grand (2014) in order to identify better descriptors for ferns's taxonomy and systematics. The software has permit to classify the descriptors according to their ability to discriminate the different species identified and incorporated into the knowledge base. This discriminating power is given by the XPER index, provided by the software itself. This index has the advantage of not being a simple index of similarity or dissimilarity unlike indices of Jaccard or Sokal & Michener also provided by the software. It allows thanks to its calculation method to highlight the descriptors whose states allow better identification of concerned taxa. A descriptor is then more efficient if it exists in at least two exclusive modalities within the studied species group. The relevance of the descriptors is then given by their discriminating power. The best descriptors are those which have the highest index. The index of XPER range from 0 to 1. It is calculated by the ratio between the number of couples with no common values and the total number of couples. A descriptor with little or no discriminating power can however become very decisive when the state of the descriptor which conditioned its applicability is verified. All first order descriptors (not conditioned by the effectivity of any other descriptor) which have no discriminating power are then eliminated. This easily allowed to identify similarities and differences between species on one hand, and on the other hand between genera.
The different states of retained descriptors were used to create a dichotomous identification key of the Togolese Pteridaceae family species. For this purpose, the specimens were segregated into two groups according to their similarities and dissimilarities. Within each group, two groups are newly created and so on until the species rank. The key nodes are defined by the dissimilarities while the branches are defined by the similarities between species.
Geographic data were collected from herbarium specimen labels and new harvests sheets in order to edit a distribution map of the Pteridaceae family in Togo.

Nomenclature:
Acrostichum dichotomum Forssk., A. radiatum (Sw.) Poir, Acropteris radiata (Sw.) Link, Pteris radiata (Sw.) Bojer, Asplenium polydactylon Webb., A. radiatum Sw, Actiniopteris australis Sim., A. australis var. radiata (Sw.) C. Chr Notes: Small fern with an erect rhizome and fronds in clumps, with lanceolate scales toothed at their base, Actiniopteris radiata has a petiole of 5-15 cm long, sparsely scaly (Fig. 5a). The scales are marginate and reddish at the base. The lamina is flabellate, 2 a b to 4 cm long and 3-5 cm wide, semi-circular. It is divided into linear lobes, toothed at the top (Fig. 5b). The texture of the leaf is leathery. Actiniopteris radiata usually grows on rocks, cliff edges and rocky terrain, especially in dry forests.  Actiniopteris radiata a: General aspect of the fern b: Details of the lamina Notes: Adiantum incisum has a short and erect rhizome (Fig. 6a), with linear scales at the base, 4 to 5 mm long over 0.2 mm wide, blackish, with a narrow margin pale. The fronds, erect or drooping, are pinnate and are arranged in tufts. They are 10 to 40 cm long. The rachis and stem are dark brown. The lower half of the stem is densely hairy, and sometimes wears narrow pale brown scales. Pinnae, 0.7 to 2.3 cm long and 4-11 mm wide, become smaller and smaller at the top (Fig. 6b). They are alternate, oblong to obliquely triangular, slightly to deeply incised or lobed at the outer and lower margins, entire at the lower margin. The base is cuneiform or rarely rounded, generally, sparsely to densely covered with white or brown hairs (Fig. 6c). The sori are circular or oblong, 1 to 3.5 mm wide (Fig. 6d). Adiantum incisum usually grows on damp rocks and mountainsides in forest areas.  Notes: Adiantum lunulatum has a short rhizome, slightly erect or creeping, wearing dark brown scales of about 3 mm long. The fronds are arched and arranged in tufts (Fig. 7a). The petiole is black, shiny, hairless, 10 to over 15 cm long. The lamina is lanceolate, pinnate and has a herbaceous texture. The pinnae are alternate, longstalked, semi-elliptical, dimidiate (Fig. 7b). Their upper base is truncated. Their top margin is serrated on the sterile frond but slightly lobed on the fertile frond. The terminal pinnae is obtriangular (Fig. 7c). The sori are crescent shaped (Fig. 7d).

Adiantum incisum
Adiantum lunulatum grows almost everywhere, in the shade of trees, on various soils, with sufficient moisture.

Nomenclature:
Adiantum chevalieri Christ.  (Fig. 8a). The stem and rachis are purple-black and shiny, hairless. The pinnae are pale green, oblong or oblong-lanceolate, 1 to 2.2 cm long and 3-8 mm wide, oblique at the base; higher margins are lobed and serrated but not deeply incised. The lower margin is entire and glabrous. Each pinnae has 4-7 pairs of oblong-reniform sori, often 1 by a lobule (Fig. 8b). Notes: Adiantum vogelii is a fairly large fern with developed creeping rhizome, up to 70 cm long, bearing piliform black scales of 2 to 3 mm long (Fig. 9a). The fronds are between 20 and 60 cm long and are closely spaced. The petiole is blackish, channeled, 5 to 25 cm long, usually angular, hairy. The rachis, not winged, is shaggy. The lamina is bipinnate, deltoid-lanceolate and measures 10-15 cm for 8-10 cm wide. Pinnae and pinnules are alternate. The lamina is composed of 2 to 4 pairs of lateral pinnae similar to the terminal, short-stalked, linear, 8-10 cm long and 2-3 cm wide, with deltoid apex, shortly tapered. The pinnae are rhomboid-dimidiate, with upper base incised on about 1/3 of its width. The lobes are truncated and toothed. The ribs are single or bifurcated towards the lower 1/3. The sori are crescent shaped (Fig. 9b). Adiantum vogelii generally grows in forests, on fairly moist and rich soils.

Nomenclature:
Acrostichum siliquosum L., Pteris thalictroides (L.) Sw., P. siliquosum (L.) P. Beauv., P. cornuta P. Beauv., Ceratopteris gaudichaudii Brongn., C. cornuta (P. Beauv.) Lepr, C. siliquosa (L.) Copel, C. thalictroides Schelpe var. thalictroides, C. thalictroides var. Notes: Ceratopteris thalictroides is an annual aquatic fern, with dimorphic pale-green fronds, irregularly pinnate. Sterile fronds are wider than the fertile fronds. They have a thin texture and are traversed by anastomosing veins. The sterile fronds have a stem of 8 to 25 cm long, ovate to deltoid lamina, 20 to 40 cm long and 7-30 cm wide, pinnate, pinnatifid or 2-3-pinnatifid, with winding lobes. The terminal segments are triangular to lanceolate, hairless. The fertile fronds have a stem of more than 40 cm long, a limb of 24-50 cm long and 12-30 cm wide, 2-4-pinnate, with linear ultimate segments of more than 4 cm long for 1-2 mm wide, glabrous. The sporangia are located along the veins. They are protected by a marginal entire pseudo-indusium, membranous, formed by the reflected margin of the lamina, with 30-70 thickened cells (Fig. 10). Ceratopteris thalictroides usually grows in marshies and low flowing rivers. Notes: Doryopteris kirkii has a short rhizome, closely spaced fronds, wearing very thickened scales in the center and very thin at the edges (Fig. 11a, b). There is a dimorphism within fronds. The petiole of sterile fronds is black, 15 to 20 cm long, scaly at the extreme base, channeled. The sterile blade is 7 to 10 cm long as wide. It is deltoid, bipinnatifid, all pinnae are opposite and connected by a large wing. The lower pinnae are sickle-shaped, about 6-7 cm long, very developed basiscopically, divided down to costa in acute pinnules, also lobed. The texture of the leaf blade is subcoriaceous and its surface is glabrous. The fertile fronds have a slightly longer stalk than the sterile fronds, with the same shape, but more deeply lobed. The rachis and midrib are black and hairless. The sori are linear, marginal, interrupted and slightly covered by a pale and narrow lobe of the lamina, as a false indusium (Fig. 11c, d). The plant usually grows on rocks, cliffs, banks of rivers and roadsides in forest areas.

Haplopteris guineensis var. guineensis (Desv.) Crane
Nomenclature: Notes: Pellaea dura is a fern with erect rhizome, with fronds in clumps, from 19 to 60 (-100) cm long, with narrow scales, pale and colorless to light (Fig. 12a, bFig. 12a). The stipe is black, brown or purple, 5-39cm long, covered at the base with linear scales. The lamina is oblong to oblong-lanceolate, 15-58 cm long and 8-18 cm wide, pinnate. There are 6 to 21 pairs of lateral pinnae, oblong-lanceolate, oblong or oblong-oval, Pityrogramma calomelanos usually grows on rocks and roadsides, both in forests and more open environments.

Nomenclature:
Pteris spinulifera Schum.  Notes: The rhizome of Pteris burtonii is short, erect, covered with black scales, with pale margins, lanceolate to linear-lanceolate (3 to 4 mm long). The fronds are tufted, 0.3 to 1m long (Fig. 15a). The stem measures 10 to 38 cm long and is covered with scales at the base. The leaf blade is deltoid, lanceolate, 20-40 cm long and 15-40 cm wide, with a bud near the base of the terminal pinnae. Each frond has 1-5 pairs of simple pinnae, oblong-lanceolate, entire or slightly lobed, of 6 to 19 cm long and 1.4 to 4 cm wide. The two basal pinnae has a basiscopic spur. The pinnae are often pinnatifid, sometimes simple. Both types of fronds can coexist on the same plant. The terminal segment is deltoid-lanceolate, 3 to 6 (-9) cm long and about 1 cm wide, toothed at the apex. The ultimate pinnae segments are organized into 10-15 pairs, oblong. The basal basiscopic segment of lowest pinnae is longer. The stipe is slightly winged by decurrent leaf base. The ribs are anastomosed at the segments level. The sori are present on all the margin of the pinnae (simple as pinnatifid ones) without interruption in the sinus, but the apex of the ultimate segments is generally sterile and toothed, giving a U-shaped sori (Fig. 15b). Pteris burtonii usually grows on the banks of rivers, waterfalls, cliffs and wet roadsides in forest areas.

Nomenclature:
Pteris congoensis Christ., P. spinulifera sensu Tardieu.  Notes: Pteris togoensis is a terrestrial fern, with erect or shortly creeping rhizome. Fronds are scaly, in clumps, often reaching over 1m long (Fig. 17a, b). The petiole, 20 to 45 cm long, is reddish at the extreme base, stramineous above, canaliculate and smooth. The lamiina is bipinnatifid, 20 to 60 cm long; composed by 7-14 pairs of lateral pinnae. The lower pinnae are opposite, 4-5cm spaced, stalked, falcate, forming an angle of 80° with the rachis. The pinnae have a linear-oblong outline, divided almost to the rachis in 20-25 contiguous segments, oblong-obtuse, entire. The tip of the pinnae is linear, entire, of about 2 cm. The first pair of pinnae has a lower pinnatifid auricule. The upper pinnae are subopposite or alternate, sessile. The rachis is stramineous and glabrous. The lower side of lamina carries some yellow glands. The costa is smooth, with a spine on the upper side, at the insertion of the midrib of the lobe. The leaf blade has a sub-coriaceous texture. The ribs are free, usually bifurcated towards the middle. The sori do not reach the top of the lobe, nor the base of the sinus (Fig. 17c, d). Pteris togoensis grows almost everywhere in the forests, agro-forests, fallow land, roadsides and river banks.

Analysis
From all the studied specimens, 17 species have been identified, belonging to the Pteridaceae family. They are distributed into 9 genera which are themselves distributed into 4 subfamilies (Fig. 2). The Cryptogrammoideae subfamily is not present in the study area. The dominant genera are Pteris L. (5 species) and Adiantum L. (4 species). The subfamilies of Ceratopteridoideae, Cheilanthoideae and Vittarioideae are respectively represented by 2 genera. Furthermore, the Pteridoideae subfamily is represented by 3 genera (Fig. 2).
Pteris similis Kuhn was harvested in a riparian forest at Dikpéléou in Adélé region (ASM 0162). This collection confirms the presence of this undocumented species in Togo. The complete list of taxa, their synonyms and their distribution in Togo are indicated in the checklist. The geographic data on the family helped to map species distribution for the whole country (Fig. 3).
The recognition and distinction of taxa within the Pteridaceae species of Togo is based on their habitat, the shape and divisions of their limb, the organization of sporangia in sori, their shape and position. The nature and position of coverings, and exudates are also very decisive. However, the dimensions of the sporophyte are less crucial than the previous characters.

Discussion
Most of recorded species (14 species of 17 in total) are represented in the ecological zone 4. Some among them are unique to this area (Adiantum incisum, Doryopteris kirkii, Haplopteris guineensis var. guineensis, Pteris atrovirens, Pteris similis and Pteris tripartita).
On the other side, Actiniopteris radiata and Acrostichum aureum are respectively exclusive to the ecological zones 2 and 5. The entire chain of the mountains of Togo is rich: 16 species out of 17. This distribution shows the role played by biodiversity refuges such as mountains (Moran 1995), which are then comparable to islands. These results also confirm works of Aldasoro et al. (2004) on the biogeography of ferns in sub-Saharan Africa which show that ferns prefer mountainous and altitudinal areas.
Three families in the RIHA database of the herbarium of Lomé correspond to the current delimitation of the Pteridaceae (Christenhusz et al. 2011). These are the former families of "Adiantaceae", "Vittariaceae" and "Pteridaceae". They are now treated within a single taxon: the Pteridaceae family. About 84% (16 names on 19) of the species names in the RIHA database match the current delimitation of the Pteridaceae. However, two other species of the genus Nephrolepis are currently integrated within the Nephrolepidaceae (Hennequin et al. 2010 (1995), highlighting the close link which exists between the presence of mountain ranges, humidity, shade and diversity of ferns of an area. In Togo, rainforest of the ecological zone 4 constitute the ideal habitat for the development of Pteridaceae but unfortunately, reforestation efforts undertaken since 1908 goes mainly through the establishment of extensive plantations of teak (Tectona grandis), an exotic plant (MERF 2009). This gradual replacement of natural ecosystems by monoculture plantations pushed back the natural habitat of ferns in general and of Pteridaceae in particular. Indeed, from all the plantations covered, only Adiantum lunulatum could be harvested in young teak plantations, old plantations being devoid of all plant species.
The expansion of croplands is also a real threat to the Pteridaceae diversity. Indeed, with the expansion of agriculture added to the effect of bushfires at the detriment of the natural ecosystems (MERF 2011), Togo may lose much of its diversity, whereby the Pteris similis Kuhn is a species which distribution in Togo is not yet well known. Inadequacy of policies of reforestation with the conservation of the biodiversity, and the lack of specialists and systematic studies on some groups, including ferns, result in the abandonment of the systematic component in favor of a macro-ecological and especially economic components.
Similarly, the current prerogatives on the carbon stock promote species that store more carbon without necessarily referring to the local flora. Therefore, timber plantations like Tectona grandis, Eucalyptus spp., Gmelina arborea, Nauclea diderrichii and Senna siamea which are mostly exotic are encouraged (MERF 2009) for their ability to store more carbon and/or for their economic value. The impact of these exotic species on the biodiversity of natural developments which they replace is often minimized. At the pace where deforestation is increasing in Togo (20,000 hectares per year according to FAO 2011), the Pteridaceae might disappear at middle term from the local flora due to loss of habitat.

Conclusion
This study clarifies the nomenclature and systematic boundaries of the Pteridaceae in Togo. The Pteridaceae accounts for 20 % of the species diversity and 23.7% of the generic diversity of Monilophytes in Togo. It comprises a variety of 17 species included into 9 genera. Major genera are Pteris L. and Adiantum L. with respectively 5 and 4 species for each. Despite its relatively high diversity (the highest among ferns in Togo), the Pteridaceae are not distributed uniformly over the study area. Approximately 94.12 % of the species are confined in the ecological zone 4 which enjoys a tropical climate and is covered by a semi-deciduous evergreen forest. The zone is like a refuge for biodiversity. Few species are still subservient to the ecological zone 2 (Actiniopteris radiata) or 5 ( Acrostichum aureum).
This study is a basis for future valorization of the family. Considerations should be given to ex-situ conservation as well as restoration and conservation of some natural degraded areas to conserve the diversity of ferns and other Pteridaceae in Togo. Further studies extended to the whole West African sub-region would be needed for a better knowledge of the Pteridaceae.