Fifty shades of red : Lost or threatened bryophytes in Africa

The bryoflora of sub-Saharan Africa and the East African islands is poorly known and recent taxonomic and floristic activity is minimal in comparison to other regions of the world (Diop et al. 2018; Hallingbäck & Hodgetts 2000; Magill 2010; O’Shea 2005; Wilding 2017). Recent, but still incomplete, floras and identification guides are available only for southern Africa (Magill 1981, 1987; Magill & Van Rooy 1998; Perold 1999), tropical Africa (De Sloover 2003), Kenya (ChuahPetiot 2003; Wilding et al. 2016), West Africa (Wigginton 2004) and Rwanda (Fischer 2013). However, a series of regional checklists with accepted names, synonyms, literature references and geographical distribution by country, of which the moss checklist of O’Shea (2006) and the liverwort and hornwort checklist of Wigginton (2018) are the most recent, provide a sound basis for research on the taxonomy, ecology and conservation of African bryophytes.


Introduction
The bryoflora of sub-Saharan Africa and the East African islands is poorly known and recent taxonomic and floristic activity is minimal in comparison to other regions of the world (Diop et al. 2018;Hallingbäck & Hodgetts 2000;Magill 2010;O'Shea 2005;Wilding 2017).Recent, but still incomplete, floras and identification guides are available only for southern Africa (Magill 1981(Magill , 1987;;Magill & Van Rooy 1998;Perold 1999), tropical Africa (De Sloover 2003), Kenya (Chuah-Petiot 2003;Wilding et al. 2016), West Africa (Wigginton 2004) and Rwanda (Fischer 2013).However, a series of regional checklists with accepted names, synonyms, literature references and geographical distribution by country, of which the moss checklist of O'Shea (2006) and the liverwort and hornwort checklist of Wigginton (2018) are the most recent, provide a sound basis for research on the taxonomy, ecology and conservation of African bryophytes.
The documentation of plant diversity and its urgent conservation are priority objectives of the Updated Global Strategy for Plant Conservation 2011-2020 (Convention on Biological Diversity [CBD] Secretariat 2017) and The Shenzhen Declaration on Plant Sciences (Crane et al. 2017).Several authors drew attention to the in general smaller and less spectacular, but to the same degree rare or threatened, bryophytes, especially in centres of bryophyte diversity, and emphasised the need for Red Lists (Hallingbäck & Tan 2010;Geffert et al. 2013;Longton & Hedderson 2000;Szabó & Pócs 2016).
The International Union for Conservation of Nature (IUCN) Red List Categories and Criteria provide an explicit framework for classifying species according to their extinction risk (IUCN 2012a).The IUCN Species Survival Commission (SSC) lists the expansion of geographic and taxonomic coverage of the IUCN Red Lists as its top priority (IUCN 2017b).The IUCN Red List of Threatened Species for bryophytes (IUCN 2017e;Tan et al. 2000) currently contains 102 species, including several from Africa.However, most of these assessments are more than 10 years old and thus in need of careful revision.There is currently no Red List for African bryophytes and the only regional Red List is the list of threatened liverwort and hornwort species compiled for the East African island of Réunion (Ah-Peng et al. 2012).
To rigorously assess the estimated 18 000 bryophyte species globally (Frey & Stech 2009), following IUCN methodology, which is now generally accepted and advocated by, for example, Vanderpoorten and Hallingbäck (2009:488), is an unsurmountable task given the current personnel and economic resources devoted to bryophyte conservation.Such an endeavour of IUCN red-listing is currently underway for the ca.1800 European bryophyte species (IUCN 2017c).To reinitiate red-listing activities on a global scale, the IUCN SSC Bryophyte Specialist Group has launched the so-called 'Top 10 Initiative' (IUCN 2017d; IUCN SSC 2016) to identify a minimum of 10 species at high risk of extinction from each continent and properly assign them to an IUCN Red List category (IUCN 2012a; IUCN Standards and Petition Subcommittee 2017).
It is generally accepted that centres of diversity and endemism, or so-called 'biodiversity hotspots', are priority areas for conserving biodiversity (Geffert et al. 2013;Marchese 2015).Conservation International, through the Critical Ecosystem Partnership Fund (CEPF) (2016a), recognises 36 global biodiversity hotspots.A biodiversity hotspot is characterised by high levels of vascular plant endemism (>1500 endemic species) and 30% or less of its original natural vegetation remaining (Conservation International 2017).Many of these are heavily threatened by habitat loss and other human activities (CEPF 2016a; Mittermeier et al. 2004).The hotspot system is used to assess global conservation priorities and to provide grants to non-governmental and private sector organisations through the CEPF (2016b; Conservation International 2017).
Eight of the global biodiversity hotspots are found in sub-Saharan Africa and the East African islands (Figure 1):   Recent analyses of bryophyte distributions at a global, continental or regional scale (Geffert et al. 2013;Tan & Pòcs 2000;Vanderpoorten & Hallingbäck 2009;Van Rooy & Phephu 2016;Von Konrat et al. 2008) indicate that African centres of bryophyte diversity and endemism partly coincide with the biodiversity hotspots defined on the basis of vascular plants.The most species-rich areas are Madagascar, especially the lowland forests along the east coast, the mountains of eastern Africa, the Afromontane and Cape Floristic regions of South Africa, and West Africa.
The aim of this paper is to highlight lost and threatened bryophytes in sub-Saharan Africa and the East African islands and to draw up a Top 10 list of bryophytes in Africa that are at highest risk of extinction.The Top 10 species will be subjected to a careful IUCN Red List assessment to be included in The IUCN Red List of Threatened Species, and they will be further evaluated (IUCN 2012b) to identify and design the most urgent conservation actions.We also test the hypothesis that most lost and threatened bryophytes on our list fall within the global biodiversity hotspots recognised by Conservation International (CEPF 2016a).

Research method and design
The area covered in this publication comprises sub-Saharan Africa, together with the Atlantic and Indian Ocean islands in the tropics (Figure 1).This corresponds to the area covered by the checklists of O'Shea (2006) and Wigginton (2018), except for the islands of Cape Verde, Ascension and St. Helena, which are excluded here.
Experts on the taxonomy, ecology and conservation of African bryophytes were invited to contribute to two initiatives, namely the 'Top 10 Initiative' by the IUCN SSC Bryophyte Specialist Group (IUCN SSC 2016) and the 'Search for Lost Species' initiative (Global Wildlife Conservation 2014).Global Wildlife Conservation approached IUCN Specialist Groups in 2014 to suggest candidate species for a proposal to search in the field for species that have gone unrecorded for years or decades (funding pendent).
Inspired by these two initiatives, a list of lost and threatened species (Online Appendix 1) was compiled based on the experts' and the first author's (J.v.R.) contributions.The following criteria were applied in the selection of species: • The species should be endemic to sub-Saharan Africa or the East African islands.In the Online Appendix 1, each species is presented at the hand of its taxonomy, geographical distribution, habitat (including substrate) and most likely threats.The current Red List status is indicated for those species that were previously assessed, either at the global or at regional scales.
However, not all of these Red List assignments follow IUCN methodology consequently, and some of the global Red List statuses are in need of revision.Family placement of the genera follows the classifications of Goffinet, Buck and Shaw (2009) and Frey and Stech (2009) for the mosses and Söderström et al. (2016) for the liverworts.Species author citations follow Söderström et al. (2016) for the liverworts and Missouri Botanical Gardens' TROPICOS database (Tropicos. org) for the mosses.
The 10 species that are at highest risk of extinction, and most likely to be categorised as 'critically endangered' when (re-) assessed using the latest IUCN Red List criteria (IUCN 2012a), were selected for the Top 10 list for Africa (Table 1).Monotypic genera and subgenera received priority and preference was given to species recognised and accepted in the latest world and African checklists of bryophytes

Results
We have identified a total of 50 species, representing 40 genera and 23 families of bryophytes, as lost and threatened in the area (Online Appendix 1).

Discussion
It is no coincidence that Lejeuneaceae is the liverwort family with the highest species number on the list of lost or threatened bryophytes in Africa as well as on the Top 10 list of bryophytes in Africa that are at highest risk of extinction.Not only is Lejeuneaceae the largest family of liverworts, but it contains more than 95% of all epiphyllous bryophytes (Gradstein 1994).The family displays high levels of diversity and endemism in moist tropical forests where they grow mainly on the bark of woody plants and on leaves at low and mid elevations (Gradstein 1992(Gradstein , 1994;;Pócs 1996;Von Konrat et al. 2008).Von Konrat et al. (2008:431) calculated that in Madagascar and some countries of central and West Africa, between 50% and almost 90% of the liverwort flora consist of Lejeuneaceae.
Recent researches in tropical forests indicate that ancient uncut stands of forest, with original phorophyte diversity and intact forest canopies, are important drivers for high epiphytic and epiphyllous bryophyte diversity (Benítez, Prieto & Aragón 2015;Malombe et al. 2016;Pócs & Tóthmérész 1997;Zartman 2003).The ongoing destruction, degradation and fragmentation of forests in the biodiversity hotspots of Africa (Aynekulu et al. 2016;CEPF 2016a;Gradstein 1992;Green & Sussman 1990;IUCN 2017a;Malombe 2007) therefore pose serious threats to epiphytic and epiphyllous bryophytes in general and species of Lejeuneaceae in particular.
The fact that 46 (92%) candidate species for the Top 10 list fall within six of the eight biodiversity hotspots in the region suggests that the African biodiversity hotspots designated on the basis of information from vascular plants may also represent hotspots for bryophytes.However, the concentration of lost or threatened species in the biodiversity hotspots may also be a consequence of collecting bias.Only two of the global biodiversity hotspots in Africa, the Coastal Forests of Eastern Africa and the Horn of Africa, are not represented on our list (Figure 1).Whilst these areas are under-explored (Hylander, Nemomissa & Hedenäs 2017;Wilding et al. 2016), lower bryophyte diversity in arid areas such as in the Horn of Africa hotspot may further contribute to this outcome.Many African regions, for example in Western Africa (Diop et al. 2018), are much less researched and thus still poorly understood in terms of plant diversity and threats to it.Thus, the detailed picture of the distribution of African bryophyte diversity is likely to change along with increasing knowledge and exploration, but we are confident that some overall patterns are recognisable based on this compilation.
The biodiversity hotspot with the highest number of lost or threatened species, as well as Top 10 species which are at highest risk of extinction in Africa, is Madagascar and the Indian Ocean Islands (Table 1, Figure 1).This hotspot is dominated by Madagascar, the fourth largest island globally, and includes the Seychelles (including Aldabra), the Comoros, Mauritius (including Rodrigues) and the French overseas departments of Réunion, Mayotte (one of the Comoros) and the volcanic Iles Esparses around Madagascar (Figure 1).The island of Madagascar, especially the eastern lowland rainforests, is known as a global centre of bryophyte diversity and endemism and the most speciesrich area of bryophytes in Africa (Geffert et al. 2013;Tan & Pócs 2000;Vanderpoorten & Hallingbäck 2009).It has also been identified as one of two major Lost Spots in Africa, countries where 'lost species', including a few mosses, are concentrated (Global Wildlife Conservation 2014).Agricultural activities, urbanisation, invasive alien species and deforestation have devastated and fragmented habitats, especially in the lowlands, throughout this hotspot (CEPF 2016a).At least one of the endemic bryophyte species from the Seychelles island of Mahé, Xylolejeunea muricella Xiao L.He et Grolle, may already be extinct (Online Appendix 1).
There is also concern about the recent marked increase in illegal logging in the remaining forests of Madagascar (Green & Sussman 1990;IUCN 2017a).
The second-highest number of lost or threatened species per biodiversity hotspot are found in the Eastern Afromontane hotspot (Figure 1).This hotspot is characterised by a series of montane islands and extensive plateaus along the eastern edge of Africa, from Ethiopia in the north to Zimbabwe in the south.It consists mainly of three ancient massifs: the Eastern Arc Mountains and Southern Rift, the Albertine Rift and the Ethiopian Highlands.Eastern Africa has also been suggested as one of the main centres of bryophyte diversity and endemism in Africa (Geffert et al. 2013;Von Konrat et al. 2008) and Tanzania is another major Lost Spot in the region for a variety of organisms (Global Wildlife Conservation 2014).Degradation and fragmentation of habitats and unsustainable exploitation of natural resources are the main threats in this hotspot (CEPF 2016a).This is caused by expanding agriculture, plantation forestry, logging, fires, invasive alien plants, mining, infrastructure development and gathering of firewood.
A substantial number amongst the lost or threatened bryophytes occur in the southwestern Cape, a region that contains the highest concentration of threatened vascular plants and plants of conservation concern in South Africa (Raimondo & Van Staden 2009).The Fynbos Biome of the Cape Floristic Region biodiversity hotspot is one of the most threatened biomes in southern Africa, classified as critically endangered (Driver et al. 2012).The southwestern Cape has been suggested as a global and regional centre of relatively high bryophyte species richness and endemism (Geffert et al. 2013;Tan & Pócs 2000).In an analysis of moss distributions in southern Africa, Van Rooy and Phephu (2016:29) recognised a Southwestern Cape Centre of Moss Diversity and found that the Cape Town-

Conclusions
This is the first compilation of bryophytes for sub-Saharan Africa and the East African islands that are most probably lost or threatened.Although it is not exhaustive, and many of the 'threat categories' reported herein are in need of revision and require to be scrutinised against the IUCN Red List criteria (IUCN 2012a), it represents a first approximation of the threats to bryophytes in Africa.
The species on the list of lost or threatened bryophytes served as candidates for the selection of the Top 10 species in Africa at high risk of extinction.Therefore, it is a crucial contribution towards the Top 10 Initiative of the IUCN Bryophyte Specialist Group (IUCN SSC 2015) and thus to the (global) IUCN Red List of Threatened Species (IUCN 2017e), as well as towards an assessment of the extinction risk of bryophytes on the African continent.Hence, it is a significant step towards meeting the targets of the Updated Global Strategy for Plant Conservation 2011-2020 (CBD Secretariat 2017) and priorities of The Shenzhen Declaration on Plant Sciences (Crane et al. 2017).
The vast majority of threatened species on our list, and all Top 10 species, are restricted to global biodiversity hotspots in Africa, areas of high endemism of vascular plants under severe threat of habitat loss (CEPF 2016a; Conservation International 2017).Investment in biodiversity conservation through the hotspots concept will therefore benefit threatened African bryophytes as well.
The Madagascar and Indian Ocean Islands biodiversity hotspot, which is also considered as a global centre of bryophyte diversity and endemism (Vanderpoorten & Hallingbäck 2009;Von Konrat et al. 2008), contains a particularly large number of threatened bryophytes.The recent increase in logging poses a serious threat to the remaining forest habitats on Madagascar and other Indian Ocean islands.The Eastern Afromontane and Cape Floristic Region biodiversity hotspots also stand out as hotspots of lost or threatened bryophytes in Africa.
The degradation and fragmentation of forests throughout sub-Saharan Africa and the East African islands have a visible impact on epiphytic bryophytes, epiphyllous liverworts of the family Lejeuneaceae in particular.Bryological exploration of Africa should be stepped up to increase our knowledge of species occurrences and threats and to facilitate the red-listing and the conservation of rare and threatened bryophytes.

Source:
Based on the Biodiversity hotspots map downloaded from http://www.cepf.net/where_we_work/Pages/map.aspx,figure licensed under the Creative Commons Attribution-Share Alike 4.0 International license (Author: Conservation International) km, kilometres.

FIGURE 1 :
FIGURE 1: The number of lost or threatened bryophytes in Africa and the East African islands (Top 10 candidates) in each of the eight Biodiversity hotspots recognised by Conservation International (CEPF 2016a).An additional four candidate species are only known from inland areas of southern Africa outside the Biodiversity hotspots (not shown on map).
• Known from a single or few localities with a narrow geographical distribution range.•The habitat should be threatened and declining or the known records date from previous centuries despite more recent collecting activity or searches in the area.

TABLE 1 :
O'Shea 2006;Söderström et al. 2016;Tropicos.org)ist of bryophytes in Africa that are at highest risk of extinction, compiled from the list of candidate species in the Online Appendix 1 where more details on the species' ecology and threats are provided.O'Shea 2006;Söderström et al. 2016;Tropicos.org)for which precise information on localities is available.
Xylolejeunea grolleana(Pócs)Xiao L.He et Grolle Lejeuneaceae Madagascar and Réunion Madagascar and the Indian Ocean Islands Xylolejeunea muricella Xiao L.He et Grolle Lejeuneaceae Endemic to the Seychelles Madagascar and the Indian Ocean Islands †, Biodiversity hotspots recognised by Conservation International through the CEPF (2016a).( Of these, 29 are endemic to mainland Africa, 19 to the East African islands and two are restricted to West Africa as well as islands off the coast. Table Mountain area is the most speciesrich in the region.The Cape Floristic Region is under increasing population pressure and much of the Fynbos and Renosterveld vegetation types of the lowlands have been destroyed or transformed by agriculture and urbanisation (CEPF 2016a; Rebelo et al. 2006; Von Hase et al. 2003).The lowland Renosterveld areas have been identified as top conservation priorities by the Cape Action Plan for the Environment (Von Hase et al. 2003).The remaining Fynbos is threatened by invasive alien species, the disruption of fire regimes, plantation forestry and fragmentation.