Distribution pattern and habitat preference for Lobelia species (Campanulaceae) in five countries of East Africa

Abstract East Africa is one of the centres of distribution and diversity for Lobelia L. (Campanulaceae, sub-family Lobelioideae). Lobelia habitats in East Africa have been facing habitat fragmentation and loss, which are recognised as a major threat to biodiversity. However, previous plant conservation studies in East Africa only focused on protected areas and ignored unprotected areas. Future conservation strategies of plants, such as Lobelia, will depend on knowledge of their distribution patterns and habitat preference in East Africa. To understand the distribution pattern and the habitat preference of Lobelia in five countries (Kenya, Uganda, Tanzania, Rwanda and Burundi) of East Africa, we conducted a literature review in the seven major vegetation regions (afro-alpine, afro-montane forest, drier savannah, grasslands, wetter savannah, Zambezian woodland and semi-desert and desert). We also employed meander and patterned searches, which allowed greater opportunities for recording Lobelia species. Our results showed that the genus is distributed in all of the seven regions of the five countries with 54 taxa. The afro-montane forest region, with 41 taxa, is the richest in species diversity, followed by the Zambezian woodland region with 18 taxa. The semi-desert and desert region has the lowest number with only four taxa. The afro-alpine region has 15 taxa, although the region is the smallest by area. The herbaceous type was found in all regions, while the giant type has a clear preference for the afro-alpine and afro-montane forest regions. Future conservation for Lobelia should consider its habitat preference by, for example, focusing on the afro-alpine and afro-montane forest regions. This study will facilitate the setting of future conservation strategies for Lobelia.

threats and habitat preferences. However, plant conservation studies in the EA only focused on protected areas and ignored unprotected areas (Eilu et al. 2007).
The distribution pattern of lobelias across different vegetations in the EA and the habitat preference remain unknown. As far as we know, lobelias are non-uniformly distributed in EA (Knox 1993;Kebede et al. 2007). For example, Lobelia telekii Schweinf. was only found on three mountains, Mt. Elgon, Aberdare Ranges and Mt. Kenya. Lobelia deckenii subsp. burtii (E.A.Bruce) Mabb., Lobelia burtii subsp. telmaticola E.B.Knox and Lobelia burtii subsp. meruensis E.B.Knox were only found in areas within the T2 region, specifically on Mt. Meru, Mt. Hanang and Mt. Loolmalassin in Tanzania (Thulin 1984). Lobelia aberdarica R.E.Fr. & T.C.E.Fr. inhabits the Cherangani Hills, Mau Ranges, Aberdare Ranges, Mt Elgon and Mt. Kenya. The upland afro-montane forest species Lobelia giberroa Hemsl. is widely spread within an altitude of 1200-3000 m in ten African countries including Kenya, Uganda, Tanzania, Sudan, Ethiopia, DR Congo, Rwanda, Burundi, Malawi and Zambia. The growth forms in this genus include annual or perennial herbs, shrubs or sub-shrub rosettes and small trees (Thulin 1984;Ruas et al. 2001). Amongst these growth forms, the most conspicuous are the branched inflorescence vs. unbranched inflorescence forms and giant vs. herbaceous forms (Fig. 1). Several studies have investigated the adaptation to afro-alpine environments, systematics and biogeography of lobelias (Knox and Palmer 1998;Kebede et al. 2007;Chen et al. 2016). For example, phylogeographic analyses indicated that L. giberroa could have migrated throughout different afro-mountains via the afro-montane forest bridge in previous interglacial periods (Kebede et al. 2007).
In this study, we reviewed previous literature and extracted data from our field survey. We aimed to identify the distribution pattern and habitat preference of Lobelia in five countries in the EA region (Fig. 1). This knowledge will facilitate the setting of future conservation strategies of the genus in EA.

Study area
This study covered five of the eight East African countries, i.e. within and amongst the early administrative divisions of Kenya (K1-7), Uganda (U1-4), Tanzania (T1-8), Rwanda and Burundi. The other three countries (Ethiopia, Somalia and South Sudan) in EA have limited data from both herbaria and the Flora of Tropical East Africa (FTEA) on the distribution of the lobelias. Therefore, they were not included in this study. The study area ranged from coastal regions to the alpine zones of high mountains with changes in the elevation gradient. To obtain a clear understanding of the Lobelia habitats and distribution patterns, seven vegetation regions (afro-alpine, afro-montane forest, drier savannah, grasslands, wetter savannah, Zambezian woodland and semi-desert and desert) were used ( Fig. 1; Kiage and Liu 2006). The vegetation regions in Rwanda and Burundi were not shown in the map of Fig. 1 (Kiage and Liu 2006). However, we recorded the distribution pattern of lobelias in the two countries by checking specimens and literature. Each lobelia in the two countries was assigned to the vegetation region, which is similar to the species' habitat(s).  Kiage and Liu (2006). Two pictures were used as examples of giant lobelias and herbaceous lobelias. The left picture is the giant Lobelia deckenii Hemsl. from Mt Kenya, while the right picture is the herbaceous Lobelia lindblomii Mildbr. from Mt Elgon (pictures by Ling-Yun Chen). (Thulin 1984), Knox and Pócs (1992) and Knox and Palmer (1998) were included in this study. The distribution and habitat for each species were explored using data from previous studies (Mabberley 1975;Thulin 1984;Knox and Pócs 1992;Agnew and Agnew 1994;Beentje et al. 1994;Knox and Palmer 1998;Knox et al. 2004;Zhou et al. 2017;Zhou et al. 2018), voucher specimens in the East African Herbarium of the National Museum of Kenya (NMK) and voucher specimens in the herbarium of Wuhan Botanical Garden (HIB) that had been collected from 2009 to 2019.

All lobelias described in the Flora of Tropical East Africa
To maximise recording lobelias in traversed habitats, meander and patterned searches (Lancaster 2000) were used. The meander search was employed on difficult terrains, such as in mountains, deep river valleys and rocky hills. On the other hand, the systematic transect was employed on flat grounds, such as grassland and shrublands. Lobelias were identified to species or subspecies level.

results
The lobelias in the seven regions of the five countries are represented by 54 taxa including herbs, shrubs and sub-shrubs (Table 1).
(1) Afro-alpine region. In this study, the afro-alpine region includes the sub-alpine ericaceous zone and the afro-alpine zone. The sub-alpine ericaceous zone ranges from about 3000 m to 3800 m (Wesche et al. 2000) and is dominated by Helichrysum Mill., Hypericum L. and Erica Boehm. The afro-alpine region extends to over 4900 m and is dominated by giant species of Dendrosenecio (Hauman ex Hedberg) B.Nord. and Lobelia. Recurring fires on the ericaceous belt created a buffer zone between the lower afroalpine and the upper afro-montane forest regions. This buffer zone was observed to provide regeneration habitats for the herbaceous species L. minutula, L. lindblomii and L. holstii (see Suppl. material 1: Table S1 for species details). (2) Afro-montane forest region. The afro-montane forest region currently occurs in anthropogenically-fragmented patches in East Africa and has an altitudinal range of 0-3000 m (Thulin 1984 (Thulin 1984). An interesting exception in this category is L. giberroa, which is widespread in Africa and has a distribution range that extends to about 3000 m (Table 1). This species inhabits a transition zone between the lowland and upland giant species. Interestingly, the lowland range of L. giberroa is found in understoreys of closed forest and riparian ecosystems, a similar habitat to its upland range. This provides insight into understanding the habitat preference of the species. The highlands of the afro-montane forest region extend from 1500 m to 3000 m. These forests have recently been highly fragmented. Jacq. spp. dominate the area. The region ranges from 10 m to 1000 m (or up to 1500 m in some habitats; Thulin 1984). Herbaceous lobelias are found in muddy ditches, river or marshy edges and seasonally-flooding grasslands. These species include L. fervens subsp. recurvata, L. goetzei, L. duriprati, L. inconspicua, L. flaccida subsp. granvikii, L. trullifolia subsp. minor, L. chireensis, L. holstii and L. welwitschii (Table 1). No giant lobelias were found in this region (see Suppl. material 1: Table  S3 for species details). (4) Grassland region. Grassland region is the most common habitat in the EA, and is dominated by alternating grasses with thorny bush-land and thicket. Although habitats in this region are different from others, some lobelias in this region are the same as in the areas of highland, wet and dry savannah and some even from the woodland. However, lobelias in this region are mostly restricted to the wet ground after rainfall (waterlogged grassland and seasonal river banks) and at the edges of wetlands in the marshy areas, streams and river banks, as well as tops of grass hills.  A-ar = Afro-alpine region, Amfr = Afro-montane forest region, Dsr = Drier savannah region, Gr = Grassland region, Wsr = Wetter savannah region, Zwr = Zambezian woodland region and S-ddr = Semi-desert and desert region. FTEA = Flora of Tropical East Africa, SR = Sight record, HS = Herbarium specimen, LR = Literature review; only if a species were not described in FTEA, literature was used to check the habitat and distribution.

Distribution patterns for lobelias in five countries of East Africa
We employed a map ( Fig. 1) with seven vegetation regions to cover the distribution of lobelias in Kenya, Uganda, Tanzania, Rwanda and Burundi (Kiage and Liu 2006). The seven regions are mainly dominated by stepped plateaus, flat land savannah, highlands, mountains and wetland ecosystems. The lobelias in the seven regions are represented by 47 species and seven subspecies including herbs, shrubs and sub-shrubs (Table 1). The most elevated habitat was inhabited by a giant species L. telekii on Mt. Kenya, while the lowest habitat was inhabited by herbaceous species, such as L. fervens and L. erinus. The altitudinal distribution of lobelias could have been shaped by their habitat preferences and by the adaptive evolution (Hedberg 1964;Chen et al. 2015). For example, L. telekii was confined to the afro-alpine belt characterised by an extreme climate with "summer every day and winter every night" (Hedberg 1964). The EA Mountains form altitudinal island-like habitats. Most of these mountains, which are known as sky-islands, are of volcanic origin (Hedberg 1969) and lie within the Latitudes 2°N and 4°S. The mountain vegetation is completely different from that of the surrounding lowland. For example, the savannah and the highland forest are different from those of the upper alpine in both species richness and growth habits (Tables 1, 2). Amongst the five sub-floras of EA, Tanzania with 38 taxa is the richest in lobelias followed by Kenya (21), Uganda (19), Burundi (9) and Rwanda (8) (Suppl. material 1: Tables S8-S12).

East African Mountains are a centre of endemism for giant lobelias
The East African Mountains embrace a wide range of altitudinal habitats and ecosystems, from surrounding environs at the foot of the mountains to the alpine zone (Zhou et al. 2018). The diversity and richness of lobelias can thus seem to be dependent on existing diverse habitats. In general, the diversity of giant lobelias varies greatly within habitats. The diversity is higher in the afro-montane forest region (13 taxa, Table 2), followed by the afro-alpine region (11 taxa). The giant lobelias demonstrated a clear preference for afro-montane forest and afro-alpine regions. On the other hand, the number of herbaceous lobelias is higher in the afro-montane forest (28 taxa) and Zambezian woodland regions (17 taxa). The herbaceous type demonstrates a clear preference for a habitat characterised by trees in both afro-montane forest and Zambezian woodland regions.
East African Mountain biomes were differentiated into two major categories, the mountains that reach the alpine (upland) and those without the alpine regions (lowlands and Eastern Arc Mountains). The upland giant lobelias, except L. petiolata, normally have a single aerial stem that is unbranched. The branched L. petiolata inhabits Nyungwe in Rwanda and extends its range to Kahuzi in DR Congo in very wet afro-montane forest region. These species have a clear preference for a wet forest habitat (Knox and Palmer 1998).
The Eastern Arc Mountains (lowlands) form the easternmost blocks of East Africa (Burgess et al. 2007). Although they do not extend to the afro-alpine region, their location creates a Massenerbung effect, therefore generating variable and unique habitats (Knox and Palmer 1998). The lowland biomes form habitats characterised by the branched lobelias (Knox and Palmer 1998). These species include L. undzungwensis, L. morogoroensis, L. stricklandiae, L. ritabeaniana, L. sancta, L. lukwangulensis and L. longisepala. The Arc Mountains have evolved their distinctive lobelias, which are different from those of the upland mountains. The Arc Mountain biome, therefore, is a hotspot for the East Africa branched lobelias. The regions inhabited by lobelias have moist and warm habitats somewhat differentiated from the regions occupied by the inland giant lobelias. The Arc Mountain giant lobelias demonstrated a clear preference for moist and warm conditions within the mountains along the East Africa Coast, which is known as one of the world's biodiversity hotspots (Stuart et al. 1990).
The Eastern Arc Mountains are separated from each other by lowland woodlands and savannah (Conte 2010). The Arc Mountain lobelias are distributed from open sites in seasonally-dry, semi-deciduous woodland (L. morogoroensis) to the sub-montane rainforests openings (L. longisepala) and also extend further to the cloud-forest summits (L. ritabeaniana, L. stricklandiae, L. undzungwensis, L. sancta and L. lukwangulensis (Table 1; Knox and Palmer 1998). Surprisingly, L. giberroa, which is found in the inland afro-montane forest, also grows on these Arc Mountains. Lobelia giberroa in the Arc Mountains occupies habitats with similar physiognomic characteristics and similar associated plant species found elsewhere in the highland afro-montane forests (Knox and Palmer 1998). The Eastern Arc and other East African mountains demonstrated an extraordinary pattern of lobelias' endemism and community preferences.

Major identified threats to afro-mountain lobelias' habitat and its lowlands environments
Land-use changes associated with deforestation and land degradation are major causes of biodiversity loss in East Africa (Maitima et al. 2009). Currently, the afro-montane forest is fragmented and remains isolated around the EA Mountains. Without the present anthropogenic activities, the afro-montane forest would probably have existed as a single connected habitat (Hedberg 1969). The habitat fragmentation threatens the distribution patterns of some native species, for example, L. giberroa (Kebede et al. 2007). Therefore, habitat loss and fragmentation could threaten the forest-dependent lobelias. For example, L. bambuseti has been reported as being under threat (Kipkoech et al. 2019).
Moreover, the afro-montane forest and its environment are also threatened by invasive plants (Obiri 2011;Hulme et al. 2013). Most of the mountains in the EA have become centres for ecotourism. To facilitate tourist activities, roads and paths within the mountain have been built. The invasive species could follow the roadsides to reach different altitudes (Pauchard et al. 2009). According to our observation, the disturbed roadsides created opportunities for disturbed habitat lobelias to dominate the roadsides. For example, L. holstii has expanded its range to almost 3900+ m on Mt. Kenya and dominated the roadsides in rocky disturbed places. Additionally, non-native tree species established in the forest plantation for timber production may pose a considerable threat (Pauchard et al. 2009) to native forest lobelias' ecosystems.
Mountain forests are major water towers, biodiversity hotspots, species evolution refugia, eco-tourism locations, sources of wild foods and centres of plant genetics (Viviroli and Weingartner 2008;Moelg et al. 2013;Kanui et al. 2016;Immerzeel et al. 2020). For example, they serve as a source of clean water for the drier lowlands, which are inhabited by lobelias, as observed in our extensive field survey. The afro-montane forest also provides places of cultural practices, such as religion for the native communities. Although lobelias are widely distributed in the seven vegetation regions, habitat loss is a challenge that calls for action. For example, the increasing human population has threatened the EA Mountain biomes. The habitat preference of lobelias' hotspots is also facing the risk of both anthropogenic and climate change (Chala et al. 2016). Habitat destruction and fragmentation are recognised as a major threat to biodiversity (Liao et al. 2013). Therefore, the afro-montane forest and its environs are especially in need of protection (Immerzeel et al. 2020).

Conclusions
Our results showed that lobelias are distributed in all of the seven vegetation regions in five countries of East Africa. The afro-montane forest region is the richest in species diversity, although it is not the largest by area. The herbaceous type has a preference for the lowland regions, while the giant type has a clear preference for the afro-alpine and afro-montane forest. Future conservation for the genus should consider the habitat preferences of lobelias.