A systematic compilation of endemic flora in Nigeria for conservation management

Acknowledgements: The author wishes to express appreciation to the staff of @One lab, Mathewson-IGT Knowledge Center, University of Nevada Reno for assistance with map designs. The brilliant suggestions and modifications of this manuscript by the reviewers and editors is also appreciated. Assistance from the staff of Herbarium unit, Forestry Research Institute of Nigeria, Ibadan, Nigeria is also appreciated. Abstract: Endemic species with limited geographical ranges are more susceptible to extinction than widely ranging species, and effective conservation management of endemic species requires detailed knowledge of their status and distribution. This study was conducted to assemble a comprehensive list of flora endemic to Nigeria. While earlier reports listed as many as 205 endemic plant species, only 91 species belonging to 44 families were found in this study, with Rubiaceae accounting for the highest number of species. The list contains 23 trees, 26 herbs, 22 shrubs, 14 epiphytic orchids and bryophytes, three vines and three ferns. The Oban Division of the Cross River National Park houses 41 endemic plants, while other notable locations for endemic flora include Eket, Naraguta, Degema, Idanre hills, Ukpon River Forest Reserve, Calabar and Anara Forest Reserve. Only 15 of the endemic plants are listed in the IUCN Red List of Threatened Species version 2013.2, ranging from Vulnerable to Critically Endangered.


INTRODUCTION
Naturalists and botanists have recognised the existence of rare and endemic species for centuries. The origin of the word "endemic" as it applied to the distribution of organisms is ascribed to De Candolle (1855). An endemic species is one that is restricted to a particular geographic area; the geographical area can be defined by political boundaries, such as country or department endemics, or by ecological boundaries (Gaston 1991;Beck et al. 2007;Young 2007). The degree of endemism for an area is often cited as a measure of the uniqueness of the flora, and consequently is important for prioritizing sites for conservation Brooks et al. 2002;Knapp 2002;Young et al. 2002). It should be noted that the confinement of endemic species to a single habitat renders them extremely vulnerable to environmental change. More than half of the endemic cichlid fishes in Lake Victoria have disappeared since the introduction of Nile perch, a voracious predator, as a game fish by Ugandan officials in the 1920s (Wilson 2010).
Endemism has attracted the attention of biologists and biogeographers since the 19 th century (López-Pujol, et al. 2011). Plant and animal endemism is the principal criterion for determination of hotspot status because endemic species are entirely dependent on a single area for their survival, and by virtue of their more restricted ranges, are often the most vulnerable . These species, confined to highly threatened ecosystems, will almost certainly be the first to be hit by extinction processes, and hence need rapid and effective conservation action (Heywood & Watson 1995). The 25 hotspots cover only 1.4% of the Earth's land surface, and account for 1,33,149 plant species (44% of all plant species worldwide) and 9,645 vertebrate species (35%) . More than ever before, conservationists have begun using data on the geography of biodiversity to set priorities for locating protected areas (Brooks et al. 2006).
Many of the world's hotspots for biodiversity are found in nations with tropical moist forests, but these nations also face profound socio-economic difficulties that cause widespread habitat loss and degradation. Given that endemism and extinction risk are closely coupled (IUCN 2001), actions to minimize global extinction need to focus on patterns in endemism and range-restricted species (Pimm et al. 1995;Pimm & Brooks 2000). The major issue with endemism is that most species are not scientifically described, and consequently little if anything is known about their ecology or geographical distributions (Pimm & Brooks 2000). Stuart et al. (2010) noted that only 3.9% of 2,82,000 known species have been are studied and evaluated for their conservation status (Stuart et al. 2010).
Rarity is central to tropical forest conservation (Kenfack et al. 2006). The African mainland has between 40,000 and 60,000 plant species (Beentje et al. 1994;Beentje 1996), of which approximately 35,000 are endemic. At least a sixth of the world's estimated 2,70,000 plant species (Groombridge & Jenkins 2002) are endemic to Africa, while five of the 20 global centres of plant diversity are located in Africa ( Barthlott et al. 2005). Yet for most African nations the number of endemic plant species is unknown or poorly estimated, and there is little research or conservation activities concerning them.
Brenan's 1978 report of plant diversity in Nigeria was based on his analysis of the geographical distribution of all species reported in previous publications (Hepper 1965;Morton 1972;Clayton & Hepper 1974) and the revised editions of Flora of West Tropical Africa (FWTA) (Hutchinson & Dalziel 1958, 1963, 1972. This figure of endemic species was further emphasized in the FEPA (1992) Nigerian biodiversity report. However, since many more species have been discovered after the last edition of the FWTA in 1972, some of the plants that were thought to be endemic to one country have been subsequently recorded from others. This study was carried out to review the current list of endemic species in Nigeria and compile an updated comprehensive list in order to highlight conservation priorities. 's (1978) account of endemism was based on analysis of Flora in Africa and other related studies. In this study identification of Nigerian endemic flora was done primarily via comprehensive secondary data mining of plant records in books, reliable internet resources and herbarium collections, performed between September 2012 and April 2014. The books used were Trees of Nigeria (Keay 1989); Nigerian Trees, volumes 1 and 2 (Keay & Onochie 1964a,b); second and revised edition of Flora of West Tropical Africa (FWTA), volume 1 (parts 1 and 2) (Hutchinson & Dalziel 1958), volume 2 (Hutchinson & Dalziel 1963), and volume 3 (parts 1 and 2) (Hutchinson & Dalziel 1972), and The Useful Plants of West Tropical Africa volumes 1-5 (Burkill 19851-5 (Burkill , 19941-5 (Burkill , 19951-5 (Burkill , 19971-5 (Burkill , 2000. There exists no nationwide plant    WWF and IUCN (1994) noted that floral inventory of the Cross River National Park is yet to be completed.

Possible evolutionary trends among endemic species
Rubiaceae was observed to have the highest number of species representatives in the endemic flora of Nigeria, as discovered in this study. Series of plant diversity studies carried out in various parts of Nigeria also show Rubiaceae to be one of the families with the highest number of species representatives (Ojo 2004;Soladoye et al. 2005;Borokini et al. 2010).
Rubiaceae was reported to be among the most diversified and largest of the families in the African rain forest (Robbercht 1996), and the family is identified as the fourth largest plant family globally, with 13,143 species, classified into 611 genera (Davis et al. 2009), more than 40 tribes, and three subfamilies (Goevarts et al. 2006). They occur on all continents (Goevarts et al. 2006), but most taxa are in tropical or subtropical areas (Bremer & Eriksson 2009). Endemism was reported to be generally high in Rubiaceae because many species have restricted distributions. Recording eight out of 11 endemic species of Rubiaceae in Cross River National Park (Oban Division) alone is of scientific interest, all of which are shrubs except for one vine. The same goes for endemic species in families such as Orchidaceae, Acanthaceae, Lecythidaceae and Annonaceae which are found in the same locations and having the same growth habit. It has been reported earlier that endemic species belonging to the same families sharing the same natural habitat must have originated from a single ancestral species (Wilson 2010). Similar situation of discovery of diversity (Brenan 1978).
As much as it is important to conserve endemic flora, it is equally important to accurately identify them in order to accord them conservation priorities. However, this study scrutinized the endemic flora in Nigeria and found only 91 to be true endemics in Nigeria, in contrast to 205 earlier reported by Brenan (1978). Likewise, Globulostylis and Psammetes, which were among the reported five endemic genera in Nigeria, have lost their endemic status. A total of 153 species thought to be endemic to Nigeria have been found in other countries (Table 2). Similar findings were reported in India, where 62 earlier reported endemic genera of angiosperms have been found in other countries, while some taxonomic changes to some genera have affected their status (Irwin & Narasimhan 2011). Furthermore, of the 147 earlier reported endemic genera in India (Nayar 1996), Irwin & Narasimhan (2011) concluded that only 49 genera are actually endemic.
This reduction in the number of endemic species in Nigeria may be due to the fact that recent taxonomic and herbarium records show that many have been found in other countries, especially neighbouring Cameroon. Brenan (1978) gave examples of such endemics such as Pennisetum dalzielli, Psychotria dalzielli, Allexis obanensis, Globulostylis talbotii, G. minor and Pohliella flabellata among others, which have been discovered in other countries, thus losing their endemic status in Nigeria (Table 2). In addition, changes in plant adaptability and physiology, gradual spread and increased dispersal capacity, human disturbance, new pests and diseases and new consumers could make some plants cross their natural distribution range to other political boundaries and thus lose their natural endemic status in Nigeria.
As taxonomic records are being improved, some of the endemic species "imperfectly known" in the Flora of West Tropical Africa (FWTA) are being properly described, given binomial names and their geographical distribution determined. For example, Coccinia sp C of FWTA has been properly named as C.  Lowe & Soladoye (1990). Some of the imperfectly known endemic species in FWTA are in over 500 endemic haplochromine cichlid fish species in Lake Victoria, originating from a single ancestral species was reported by Meyer (1993).
In the same vein, eight endemic species of Orchidaceae were identified in this study. Orchidaceae is the largest plant family on earth, having an estimated 25,000 species, grouped into 850 genera, with over 70% being epiphytes (Gravendeel et al. 2004). Seger back (1983) described 104 species of orchids for Nigeria, but Jayeola (1991) otherwise encountered over 400 species for Nigeria. The African continent harbours around 2,400 orchid species (Madison 1977). The high numbers of representative species of these two families-Rubiaceae and Orchidaceae-indicate a high diversity of these families in Nigerian flora, and therefore, there is the need for thorough studies on the phylogenetic relationship among these species.
Factors that could be responsible for their evolution include development of adaptive features to climate change that occurred thousands of years ago, changes in flowering time, dispersal capacity and some of them may be sun-loving or shade tolerant, with preference for altitudes. Furthermore, it is scientifically accepted that geographical barriers could isolate populations of a single species, leading to allopatric speciation (Templeton 1981;Slatkin 1987;Coyne 1992;Palumbi 1994). The tropical rainforests are a big candidate for any form of speciation-allopatry, parapatry, peripatry, sympatry and ecological. This is because high diversification rate and biogeographic history of tropical environments, abundance of geographical barriers (e.g., mountains, rivers, hills and deep valleys), new niche evolution, species survival in mountainous refugia during the pleistocene age, biotic interactions among species (such as predation, association and competition), spatial heterogeneity, higher metabolic rate, rapid accumulation of genetic incompatibilities and other intrinsic and extrinsic isolating mechanisms could lead to speciation that gave rise to the present species richness and endemism in the present tropical regions (Mittelbach et al. 2007;Schemske et al. 2009;. Genetic bottlenecks, behavioural isolation and the effects of landscape and metapopulation processes have been demonstrated and reported for several plants and animals, including Lahontan Cutthroat Trout Fish in Nevada and California, United States of America (Neville et al. 2006;Peacock & Dochtermann 2012).

Mountain Biodiversity
The present study shows that nine of the geographical locations of these endemic flora are hills and mountains, harbouring 57 species out of the entire 91 endemic flora, indicating that 62.6% of the endemic species are found in mountainous regions. Literatures have shown that a large fraction of the world's most precious gene pools are preserved in mountains, while nearly half of the world's biodiversity hotspots are concentrated on mountains (Spehn et al. 2010), with tropical montane forests noted for their high levels of species endemism and diversity (Gentry 1992(Gentry , 1993Kapos et al. 2000;Schmitt et al. 2010). In addition, from Ethiopia to the Cape (South Africa), mountains contain several centres of endemism for birds, mammals, and plants (Fjeldså & Lovett 1997;de Klerk et al. 2002;Goodman & Benstead 2003;Jetz et al. 2004). All these indicate that mountains are centres of biodiversity and endemism, and this should therefore encourage intensive ecological studies on the plant diversity of hills, mountains and inselbergs that spread across Nigeria, for which research information are currently lacking. In addition to this, 32 out of the entire 55 locations are within tropical rainforest ecoregions. The concentration of most of the endemic plants in tropical rainforests in Nigeria is supported by previous findings by Myers et al. (2000), McNeely et al. (1990) and Mittermeier et al. (2000) among others.

Biodiversity of the Nigerian-Cameroon forest complex
The ecological importance and the significance of the biodiversity of the Cameroon-Nigerian forest complex cannot be overemphasised. And recording 66 (72.5%) species out of 91 endemic species in southern Nigeria (Cross River, Akwa Ibom and Rivers states) is another confirmation of not only the global significance of its biodiversity, but also of the species richness of endemic flora in the region. The Korup National Park shares boundaries with Nigeria's Cross River National Park (Oban Division), while the Okwango division of the Cross River National Park borders the Takamanda Forest Reserve in Cameroon, forming an extensive trans-boundary corridor of biodiversity complex (Fig. 4). This forest ecoregion is a part of the Guineo-Congolian regional centre of endemism (White 1983). Among the taxa that exhibit particularly high levels of species richness and endemism in this trans-boundary ecoregion are primates (Eeley & Lawes 1999;Oates et al. 2004;Sarmiento & Oates 2000;Hilton-Taylor 2000), mammals (AECCG 1991;Happold 1994), amphibians (Lawson 1993;Schiøtz 1999;Kamdem-Toham et al. 2003;Conservation International 2007), birds (Collar & Stuart 1988;Stattersfield et al. 1998), butterflies (Larsen 1997), dragonflies (Vick 1999), fish (Reid 1989), mammals (Burgess et al. 2000), and vascular plants (Cable & Cheek 1998). The biogeographical barriers of the Sanaga River in Cameroon and the Cross River in Nigeria define the mainland boundaries of this ecoregion. These rivers are particularly important geographical barriers for primates, Red-eared Guenon Cercopithecus erythrotis and amphibians, such as Dizangue Reed Frog Hyperolius bopeleti. However, they are significant to global conservation because they are only found within a restricted ecosystem shared between the two countries. In Cameroon's Korup National Park, 1700 species of vascular plants have been recorded, as many as 5% of which are narrow endemics (Davis et al. 1994). These support the need for a stronger framework for transboundary management of biodiversity.

Coexistence of endemic plants and animals
Cross River National Park is the peak of Nigeria's biodiversity, being the largest tract of the remaining and surviving primary rainforest in Nigeria. About 78% of primate diversity finds home in the protected areas; while it harbours another 30 species of nonprimate mammals, including the African Forest Elephant Loxodonta cyclotis, Hippopotamus Hippopotamus amphibious, Forest Buffalo Syncerus cafer nanu, Giant Otter Shrew Potomagale veloxl (Stuart et al. 1990). Over 30% of Nigeria's 860-bird species are found in the Park, including the endangered Red-headed Rock Picathartes oreas, the rare Green Ibis Bostrychia olivacea, the Violetbacked Flycatcher Hyloita violacea, and the Black Guinea Gowl Agalacea niger, Bannerman's Weaver, Whitethroated Babbler, Bat Hawk, Cassin's Hawk-eagle, Greythroated Rail, Olive Long-tailed Cuckoo, Bare-cheeked Trogon, Lyre-tailed Honeyguide, Green-backed Bulbul, Grey-throated Flycatcher and Rachel's Malimbe (Manu & Imong 2006). Eniang & Ijeomah (2011) reported 56 species of snake in the Oban division while 28 snake species were reported for the Okwango division (Eniang et al. 2002) of the Cross River National Park. Larsen (1997) estimated about 950 butterfly species in the Oban division, of which the Cross River National Park officials reported that two are endemic and another two-Tetrahanis okwangwo and T. oboti-are new to science. Furthermore, the Park officials reported that two new frog species were identified, namely Didynamipus sjooesteati and Nyctibates corrugatus, which are new records for Nigeria. The floral diversity of the National Park was reported to be 1,568 species from 523 genera in 98 families. These include 1,303 flowering plants, 141 lichens and 56 moss species.
These information strongly support high mutual  Knops et al. (1999) and Haddad et al. (2001) among others. Species endemism richness, as described by Kier et al. (2009) is the mutual coexistence of endemic flora and fauna in the same geographical area; this was observed in Hawaiian Islands where over 10,000 known endemic insects, 100 endemic birds and about 1,000 endemic flowering plants were reported (Wagner et al. 1990(Wagner et al. , 2005Wilson 2010 Brooks et al. 2002).

Threats to the endemic species
These results present some troubling news with respect to the reported hotspots of this Nigerian endemic flora. For instance, some endemic plants noted to be located in Lagos and Calabar have been completely overtaken by urbanization. Several forest reserves in Nigeria are being de-reserved and concessions given to timber companies for logging, and replacing them with monocultural plantations of exotic trees such as Tectona grandis, Gmelina arborea and Eucalyptus camaldulensis. Furthermore, the indigenous people around around these forest reserves clear significant sections for farming, as well as hunting for wild animals. The presence of those endemic species in those locations and their population status should be investigated. Eket is a big town in Akwa Ibom State in the southern region of Nigeria, housing eight endemic plants in addition to high biodiversity in the region; but is plagued by problems such as oil spillage and gas flaring from commercial oil exploration and acid rain (Nduka et al. 2008;IUCN 2013). These threats have been identified as a major threat to the endemic plants, some of which are already assessed by the IUCN Red List of Threatened species (IUCN 2013). Collins (1990) and Mittermeier et al. (2000) reported that the West African Guinean forest is the worst damaged of the 25 global hotspots which, due to logging and clearance, have destroyed at least 85% of the rainforests. All these probably support the report that 20 plants are extinct in Nigeria (FEPA 1992). Worse still, a recent survey conducted on the plant collections of all botanic gardens in Nigeria shows that none of these endemic species is being conserved ex situ, as a back-up to these endemics in their natural habitats (see BGCI Garden Search Database for Nigerian botanic gardens <http://www.bgci.org/garden_search.php>). In addition, database search on JSTOR and ISI Web of Science produced very few published research works on any of the endemic plants, indicating a very wide research and knowledge gap on these endemic species, let alone their conservation in Nigeria. For example, in order to ensure effective conservation of threatened species, population viability analysis (PVA) should be conducted to predict their survial in the future.
Therefore, there is the need for intensive conservation of the remaining endemic flora in Nigeria. It is important to note that since timber resources in free public lands have been exhausted in Nigeria, pressure is on timber resources in protected areas, through illegal logging and indiscriminate allocation of forest concessions and de-reservation of forest reserves and other in situ conservation sites. It is safe to say that in situ conservation sites in Nigeria have been heavily disturbed, though efforts are being increased to protect the remaining tracts, especially in Southern Nigeria. Ecological restoration, through re-vegetation of disturbed areas should be done, using indigenous tree species. Community Forestry should be adopted and introduced in the forest reserves and national parks, as a way of combating illegal activities and enhancing participatory forest management.
In addition, existing policies governing the management of these protected areas need to be critically reviewed so as to increase transparency in decision making and reducing corruption. Intensive taxonomic and phylogenetic studies, vegetation surveys and biogeographical research should be conducted on the Nigerian flora; in situ conservation efforts have to be supported by adequate ex situ conservation measures.