The Ethiopian plateau comprises a mosaic of widely differing habitat types with extremely diverse relief and pronounced elevational zonation. These unique environmental conditions have encouraged intensive speciation processes, making the Ethiopian plateau a “mammal diversity hotspot”, i.e. a centre of diversification for numerous Ethiopian mammal taxa (Lavrenchenko et al. 2004, 2007, 2014). Ethiopia is characterised by a high degree of endemism, with 36 mammalian species presently considered endemic to the country (Bekele and Yalden 2013). This exceptional level of endemism is also emphasised by the existence of several endemic mammal genera; including Desmomys Thomas 1910, Stenocephalemys Frick 1914 and Nilopegamys Osgood 1928 among the rodents. Other phenotypically distinct forms previously placed in their own endemic monotypic genera (i.e. Muriculus and Megadendromus) have only recently been recognised as internal lineages of otherwise widespread African clades (Mus and Dendromus, respectively) (Meheretu et al. 2015, Lavrenchenko et al. 2017). Nevertheless, these species remain enigmatic Ethiopian endemics, especially as they are rarely recorded. Their highly distinct phenotype could serve as an example of such evolutionary cases where strong selective pressure within extreme Afroalpine habitats has resulted in accelerated morphological evolution, despite minimal genetic divergence.
The Ethiopian plateau, which covers much of the country, is divided into two parts by the Ethiopian Rift Valley (ERV), i.e. the Abyssinian massif (northwestern plateau) and the Harar massif (southeastern plateau) (Figure 1). The Arsi Mountains (AM), the northernmost mountain range on the Southeastern plateau, mainly comprise the Galama Ridge and the neighbouring Mount Chilalo (Figure 1). The first biological expeditions to Ethiopia, for a variety of reasons, started their work from the north of the country (Bekele and Yalden 2013). Consequently, the AM were the first southeastern montane massif encountered and early explorations described many new taxa, including such emblematic endemic Ethiopian species as the mountain nyala Tragelaphus buxtoni Lydekker 1910, based on type specimens collected from Mount Chilalo (Bekele and Yalden 2013). Likewise, it is unsurprising that descriptions of several endemic Ethiopian rodents (e.g. the Ethiopian narrow-headed rat Stenocephalemys albocaudata Frick, 1914, the African vlei rat Otomys helleri Frick 1914 and Blick’s Grass Rat Arvicanthis blicki Frick 1914) were also based on specimens collected from the AM (Frick 1914). Being much more extensive, the neighbouring Bale Mountains (BM) remained less accessible to investigators until a road was constructed across the Sanetti plateau in 1986. As a result, researchers have redirected their attention to the south (i.e. to the BM), with a high number of small mammal studies having been conducted there since the end of the 20th century. This has greatly contributed to the accumulation of data on Ethiopian small mammal taxonomy and genetic diversity (e.g. Yalden 1988, Corti et al. 1995, 1999, Lavrenchenko et al. 1997, Milishnikov et al. 2000). In contrast, knowledge on rodents of the AM has remained scanty, being based on sporadic faunistic surveys only (Kasso et al. 2010, Zerihun et al. 2012) with no preserved material. The results of these pilot investigations suggested the presence of such specialised Afroalpine dwellers as the black-clawed brush-furred rat Lophuromys melanonyx Petter, 1972 in the AM (Kasso et al. 2010); however, identification of this species has not been confirmed by genetic analysis. The occurrence of a further endemic Ethiopian species, the Ethiopian striped mouse Mus imberbis (Rüppell, 1842), was recently recorded based on a single individual (Meheretu et al. 2015). Both these findings strongly suggest the need for further detailed biological surveys within the AM.
The aim of this paper is to provide comprehensive information on the taxonomic diversity of AM rodents based on intensive long-term field sampling. Mitochondrial gene sequences for cytochrome b (CYTB) and four nuclear markers (DHCR24, GHR, IRBP, WLS-7; for selected taxa only) are also used to provide a basic genetic evaluation of the taxa sampled. Detailed phylogenetic analysis was not performed on each rodent group due to limited sampling and the associated drawbacks of using only maternally inherited mitochondrial DNA (mtDNA). Instead, mtDNA barcoding is used for species identification. Special attention is paid to the altitudinal distribution of particular species and to assessing the level of genetic divergence between individuals from the AM and their conspecifics from the neighbouring BM.
Materials and methods
Samples were collected at eight localities in the AM during three expeditions undertaken in 2012, 2015 and 2016 (Table 1, Figure 1). Terrestrial rodents were captured using approximately 50 Sherman’s live traps (23×9.5×8 cm) set up each night and baited with a mixture of sliced carrot and sunflower oil or wheat with peanut butter. Root-rats were caught using a range of hand made traps or with the assistance of local people. All specimens were weighed and the body and tail length, ear length and hind foot length (with and without claws) measured. Preliminary species identification, sex, reproductive condition and other informative details were also noted at the time of capture. Representative voucher specimens of each taxon were sacrificed by cervical dislocation and taken for further investigation. The dried skulls and prepared skins are now housed in the Zoological Museum of Moscow State University and the Zoological Natural History Museum of Addis Ababa University. Tissue samples of these specimens (muscle, liver, kidney and heart) were preserved in 96% alcohol and stored for genetic analysis. All remaining specimens were released where they were captured after taking a tissue sample (ear biopsy) for genotyping. We also installed three “Bushnell HD” camera traps (Bushnell Outdoor Products, USA) in order to observe the rodents’ behavioural and ecological peculiarities. All fieldwork complied with legal regulations in Ethiopia and sampling was undertaken with permission of the Ethiopian Wildlife Conservation Authority and the Oromia Forest and Wildlife Enterprise (see Acknowledgements).
DNA extraction was carried out using the phenol-chloroform method. Complete sequences of the CYTB gene (1140 bp) were amplified using the protocol described in Lavrenchenko and Verheyen (2006). Analysis of genetic relationships was performed for each genus, using available sequences from GenBank. In cases where conspecific populations from the AM and BM formed separate clades, the mean level of genetic divergence (uncorrected p-distance) was calculated using Mega 7.0 (Kumar et al. 2016). For precise species identification of Lophuromys specimens, bearing deeply divergent mtDNA haplotypes, four nuclear markers (DHCR24-7, GHR, IRBP and WLS-7) were sequenced using the primers and protocol described in Stanhope et al. (1992) and Rodríguez-Prieto et al. (2014). Reconstruction of the mitochondrial phylogeny of genus Lophuromys was inferred from a maximum likelihood framework using Treefinder (version of March, 2011. Munich, Germany) (Jobb 2011), with 1000 bootstrap replicates. Nuclear phylogeny of this group was obtained using Bayesian inference in MrBayes, v 3.2.6 (Ronquist and Huelsenbeck 2003), based on all species of the genus living in the AM (and the neighbouring BM) and other taxa that likely shared evolutionary history, i.e. L. simensis and L. menageshae (see Lavrenchenko et al. 2004). Traces of past hybridisation between two sympatric Stenocephalemys species (S. albocaudata and S. griseicauda Petter, 1972) were assessed using karyological analysis. Somatic metaphase plates for 20 specimens of these species were obtained from bone marrow preparations following the standard air-drying procedure (Ford and Hamerton 1956). Standard staining was carried out using 4% Giemsa (PanEco, Russia) in phosphate buffer at pH 7. Newly produced DNA sequences are available in GenBank under accession numbers MH297533-MH297581 (CYTB), MH325006-MH325019 (DHCR24-7), MH297493-MH297506 (GHR), MH297507-MH297519 (IRBP) and MH297520-MH297532 (WLS-7) (Supplementary Table S1).
Results and discussion
Overview of rodent trapping
Comments on particular taxa
Recently published African rodent distribution maps (Lavrenchenko 2013a, Monadjem et al. 2015) suggest that the AM should be inhabited by the short-tailed brush-furred rat L. brevicaudus Osgood, 1936 only, though there has also been a genetically unconfirmed record of Lophuromys melanonyx (Kasso et al. 2010). In our study, we recorded three brush-furred rat species in the AM. The first, L. melanonyx, an obligatory Afroalpine dweller (Yalden and Largen 1992), was recorded at high-densities in the Badda region (site 5) at the highest elevation sampled in the AM. Almost all animals were trapped during the day within colonies co-inhabited by A. blicki. Simultaneous use of the same burrow by both species was repeatedly recorded by the camera-traps (Figure 2). Similar external morphology, vocalisation and behaviour make this species pair an amazing example of convergent evolution in rodents adapted to extreme Afroalpine conditions. The second species, L. brevicaudus, is common in the ericaceous belt in the Ethiopian highlands, east of the ERV (Lavrenchenko 2013a). The species was abundant in the Shirka region (site 1), the western slope of Mount Chilalo (site 4) and in the Badda region (site 5). The third species, the Ethiopian forest brush-furred rat L. chrysopus Osgood, 1936, was trapped during a short survey of the montane forest near Assela (site 2). This species is typically a forest dweller of the southern Ethiopian highlands on both sides of the ERV (Lavrenchenko 2013b) and our records confirmed previous observations.
Analysis of Lophuromys melanonyx CYTB sequences revealed two distinct haplogroups. Hereafter, the previously known haplogroup of L. melanonyx is termed “Melanonyx-II” (=L. melanonyx sensu Lavrenchenko et al. 2004), while the second haplogroup, reported here for the first time, is termed “Melanonyx-I” (Figure 3). The mean p-distance between these two haplogroups was 6.54±0.011%. We then analysed variability at four nuclear markers in order to test whether individuals bearing particular mitochondrial haplogroups represented two distinct gene pools (=species). The concatenated tree suggested that L. melanonyx (AM) represents a single genetic species as no monophyletic groups (defined by mitochondrial haplogroups) were evident on the nuclear markers (Figure 4). The pattern observed is likely to be either a result of ancestral polymorphism or (more likely) mitochondrial introgression.
It is worth mentioning here that two distinct mitochondrial haplogroups were also found in another mountain species, L. simensis (Lavrenchenko et al. 2004). As one (termed “North II”) was very close to Lophuromys melanonyx (“Melanonyx-II”) and L. menageshae (Figure 3), Lavrenchenko et al. (2004, 2007) proposed ancient reticulate speciation processes, involving past hybridisation between the species. Our discovery of “Melanonyx-I” may well shed light on the evolutionary history of this complex. Phylogenetic analysis revealed strong support (by 97% bootstrap value) for a monophyletic clade consisting of three mitochondrial lineages belonging to three different species (L. melanonyx “Melanonyx-II”, L. menageshae and L. simensis “North II”). Mitochondrial sequences of L. melanonyx “Melanonyx-I” and L. simensis “North I” formed separate clades, differing from the composite clade by 6.74±0.011% and 6.83±0.012%, respectively. Based on these results, the following evolutionary scenario is proposed. “Melanonyx-I” and “North I” presumably represent the original species-specific mitochondrial haplotypes for L. melanonyx and L. simensis, respectively. The “Melanonyx-II” and “North II” mitochondrial haplogroups could have been introgressed into L. melanonyx and L. simensis through hybridisation with L. menageshae living at lower elevations in Central Ethiopia. While the distribution of the two high-elevation species (i.e. L. melanonyx, east of ERV, and L. simensis, west of ERV) is presently separated from that of L. menageshae (see distribution maps in Lavrenchenko et al. 2007), Pleistocene climatic fluctuations are likely to have repeatedly shifted the distribution of vegetation zones, along with their associated biota (Osmaston et al. 2005, Umer et al. 2007, Bryja et al. 2018).
For both L. brevicaudus and Lophuromys melanonyx (in the case of L. melanonyx, we only took the more widespread “Melanonyx-II” haplogroup), the negligible genetic distance between the AM and BM populations (Table 2) suggests a relatively recent split (late Pleistocene). In contrast, specimens of L. chrysopus captured in the AM displayed a more pronounced genetic distance from their BM conspecifics (Table 2). Topology of the reconstructed phylogenetic tree (without bootstrap support) suggests a closer relationship between L. chrysopus from the AM and conspecific populations from the Beletta and Sheko forests in the northwestern plateau (Figure 1) than with population from the geographically neighbouring BM (Figure 3). Hence, the evolutionary history of L. chrysopus was probably more complex and most likely involved two independent crossings of the ERV, though the hypothesis needs further testing.
The only genetically confirmed Arvicanthis species in the AM was A. blicki, which was only trapped at 3800 m a.s.l. in the Badda region (site 5). Molecular analysis indicated a low genetic difference between AM and BM A. blicki populations (Table 2). Two other Arvicanthis species reported by Kasso et al. (2010) from lower elevations in the AM (A. abyssinicus and A. dembeensis) still require genetic confirmation.
The phylogenetic position of Mus imberbis (until recently Muriculus imberbis; Meheretu et al. 2015) has long been unclear. Based on external features, such as the mid-dorsal black stripe, and morphological peculiarities of the skull, this species was previously placed in the separate Muriculus genus (Thomas, 1903); however, a recent study (Meheretu et al. 2015) using molecular data has shown that the species represents an ancient lineage of the African subgenus Nannomys within the genus Mus. During our survey, one individual of this extremely rare species was trapped in Erica bush on the western slopes of Mount Chilalo (site 4). Comparison with M. imberbis from the Shirka region (Meheretu et al. 2015) revealed an almost identical mitochondrial haplotype (p-distance=0.09). As these two specimens were captured in the northernmost and southernmost parts of the AM, one can assume that local populations of this species have low genetic diversity.
Another representative of the genus Mus, M. mahomet Rhoads, 1896, was trapped in the Shirka region (site 1) and on the western slope of Mount Chilalo at sites 3 and 4. Genetic analysis of the complete CYTB sequence revealed similar haplotypes in both AM and BM populations (Table 2).
The final Mus species, thought to inhabit montane forests in the AM, is undescribed yet M. sp. “Harenna” (sensu Bryja et al. 2014). Until now, this species has only been reported from the Harenna Forest on the southern slopes of the BM (Yalden 1988, Lavrenchenko 2000, Bryja et al. 2014). As we failed to collect this species in any habitat in the AM (including montane forest), despite intensive trapping efforts, it is likely that the species only lives in the BM Harenna Forest.
As shown by previous studies (e.g. Lavrenchenko and Verheyen 2006, Bryja et al. 2018), the BM are characterised by a well-developed elevational gradient of ecological conditions and clear separation between adjacent altitudinal belts, which are inhabited by different narrow-headed rat species of the genus Stenocephalemys. Specifically, Stenocephalemys albipes (Rüppell, 1842) occupies forest habitats at altitudes of 800 to 3100 m a.s.l., Stenocephalemys griseicauda is common in Erica bush and mountain meadow at approximately 3300 to 3700 m a.s.l. and Stenocephalemys albocaudata is restricted to the Afroalpine zone above 3700 m a.s.l. (Bryja et al. 2018). During our survey in the AM, we trapped all three Stenocephalemys species, though their spatial distribution was slightly different due to differences in altitudinal zonation (Table 2). In the Shirka region (site 1), we observed a local inversion of altitudinal belts, along with the species inhabiting them, i.e. S. griseicauda occupied hills covered with Erica bush, whereas S. albocaudata inhabited open swampy areas below these hills. On top of the Galama Ridge (3800 m a.s.l. and above) in the Badda region (site 5), a mosaic of both Ericaceous and Afroalpine habitats resulted in virtually sympatric populations of S. griseicauda and S. albocaudata, though the latter was more abundant. We performed chromosomal analysis in order to assess whether the sympatric occurrence of these generally parapatric sister species (see Bryja et al. 2018) was accompanied by ongoing hybridisation. As both species differ in the fundamental number of autosomal arms (NFa=62 in S. albocaudata and NFa=58 in S. griseicauda; Lavrenchenko et al. 1997, 1999), one would expect the karyotype of the putative hybrid to have an intermediate fundamental number. Though karyotyped 20 individuals of both species, including three intermediate between the two species colour variants, we failed to find evidence of hybridisation, all karyotyped individuals having typical NFa for the species, corresponding with their mtDNA genotypes (Bryja et al. 2018).
Stenocephalemys albipes was captured in forest habitats on both Mount Chilalo and the Galama ridge (sites 2, 3 and 6). A recent phylogenetic analysis of the genus Stenocephalemys revealed a clear phylogeographic structure for S. albipes (Bryja et al. 2018). As all three mitochondrial haplogroups identified from the Southeastern plateau were also found in S. albipes, inhabiting Mount Chilalo (i.e. ap_1a, ap_1b, ap_1d; sensu Bryja et al. 2018), the Mount Chilalo population clearly shows high genetic diversity. This can be explained in two ways: either the AM acts as a centre of S. albipes diversification, with a long-term refugium in the Southeastern plateau, or different lineages diversified through lineage sorting in other regions (e.g. the BM and Chercher Mts. in the Eastern Ethiopian Highlands; see Bryja et al. 2018) and came into secondary contact in the AM. In our study, genetic analysis showed that all three AM Stenocephalemys species shared most haplotypes with their conspecifics from the BM (Table 2).
Otomys helleri is commonly found in patches dominated by Alchemilla in both ericaceous and Afroalpine habitats. We captured this species in the Shirka region (site 1), on Mount Chilalo (site 4) and on top of the Galama ridge in the Badda region (site 5). Although the western slopes of Mount Chilalo are similar to the type locality of the Otomys yaldeni described from the BM (Taylor et al. 2011), we failed to trap this species, despite intensive trapping. Unless further sampling confirms the species in the AM and other mountains of the Southeastern plateau, the current distribution range of O. yaldeni appears to be restricted to the BM.
Until recently, Nikolaus’s African climbing mouse Dendromus nikolausi (Dieterlen and Rupp, 1978) was considered to be a representative of the distinct monotypic genus Megadendromus due to its larger size, relatively short tail and unique dental characters. However, molecular phylogenetic analysis of a single individual captured in the BM shows that this species is an internal lineage of the genus Dendromus (Lavrenchenko et al. 2017). During our field surveys, one additional individual of D. nikolausi was trapped on the western slope of the Galama ridge (site 7). This represents the sixth individual of this rare and poorly known species captured in almost 40 years since its first description. Molecular analysis of its CYTB sequence revealed a 2.39±0.005% p-distance between our individual and that captured in the BM.
A further Dendromus species was recorded in both the Shirka region (site 1) and on Mount Chilalo (sites 4 and 8), preliminary analysis suggesting that it is probably a new undescribed Dendromus species, differing genetically from other taxa (Lavrenchenko et al. 2017). It is worth mentioning that this species has also been caught at high altitudes (>3200 m a.s.l.) on the northwestern plateau near Debre Sina (Lavrenchenko et al. 2017). A genetic analysis has shown considerable genetic distance between Debre Sina and the AM specimens (5.19±0.007%). The species has also recently been collected at similar altitudes in the BM (Bryja et al. unpubl. data).
Although several sources still suggest at least past occurrence of the morphologically distinct giant root rat Tachyoryctes macrocephalus Rüppell, 1842 in the AM (Bekele and Yalden 2013), we found neither live individuals nor typical signs of their occurrence, i.e. the so-called mima mounds. Thus, after 3 years of field explorations in the AM, we conclude that the distribution range of this emblematic species on the southeastern plateau (and perhaps Ethiopia) is presently restricted to high elevations in the BM. We found a second representative of this genus, Tachyoryctes splendens Rüppell, 1835, during our survey in the Badda region (site 5) and on Mount Chilalo (sites 3 and 4). This taxon is characterised by an extremely high level of genetic diversity (Lavrenchenko et al. 2014), with up to four separate gene pools (=putative species) occurring parapatrically in Ethiopia (Šumbera et al. 2018). Genetic analysis of the CYTB sequences confirmed the existence of three distinct mitochondrial lineages in the AM, and two in the BM (all belonging to “spendens 4”, sensu Šumbera et al. 2018), with one being shared by the two mountain blocks. The level of genetic divergence (p-distance) between these four subclades ranged between 4.44 and 6.99% of CYTB gene nucleotide substitutions.
Comparison of rodent communities in the AM and BM
During our survey, 13 rodent species were documented from the AM, including such rare species as Mus imberbis and Dendromus nikolausi. Despite intensive trapping over 3 years, we failed to record three species known from the BM: Tachyoryctes macrocephalus, Otomys yaldeni and Mus sp. “Harenna”. Awaiting additional sampling from the AM, we hypothesise that distribution areas of the latter two species are currently restricted to the BM. The giant root-rat T. macrocephalus was described from the Northwest plateau, which suggests its wider distribution in Ethiopia in the past. However, all records since its description in 1842 derive from the BM, and it is very likely that the Afroalpine habitats of the BM remain the only refuge of its distribution.
Untill now there has been no reliable record of Mus imberbis in the territory of the BM. Type specimen as well as a majority of the captured specimens were collected from the Northwest plateau (Simien Mountains National Park). Findings of M. imberbis from the Southeast plateau are quite poor. Absence of this species in the BM may be explained in two ways. First, M. imberbis could have penetrated the AM from the northwestern plateau, though it appears not to have reached the BM. Second, Assefa and Zerihun (1980) have suggested that current knowledge of its distribution may reflect bias from using unsuitable trapping methods, rather than any real absence in the BM. In light of the high number of faunistic studies in the BM, it would appear that distribution of M. imberbis on the southeastern plateau is currently restricted to the AM only. The findings of this rare species in the AM is of particular interest and confirms this region as a target of biodiversity conservation.
A comparison of the genetic characteristics of rodents from the AM and the neighbouring BM indicated variable levels of genetic divergence for the different species (Table 2). Stenocephalemys spp. from both mountain blocks are virtually identical, for example, while populations of other groups (Lophuromys, Arvicanthis, Otomys, Dendromus and Tachyoryctes) in the AM and BM included both high and low divergence intraspecific mitochondrial lineages. Our data suggest a separation of AM and BM populations for a considerable period, during which particular lineages were sorted or accumulated mutations de novo. It is assumed that species with similar habitat preferences inhabiting the same altitude belt are likely to display similar genetic relationships between neighbouring montane ranges. Our own results, however, were rather equivocal. We found a significant level of genetic divergence between all three Lophuromys species from the AM and BM, whereas the three Stenocephalemys species had practically the same haplotypes in both mountain ranges. One explanation may be related to differences in dispersal potential between the two genera. We suggest that narrow-headed rats (Stenocephalemys) are more opportunistic taxa with a higher dispersal ability than the more specialised brush-furred rats (Lophuromys). It is possible, therefore, that gene flow between AM and BM Stenocephalemys was more intense during the last connection of suitable Afromontane habitats in the late Pleistocene.
Despite the establishment of a National Park in the AM in 2012, both Mount Chilalo and the Galama Ridge suffer from intense anthropogenic pressure. The remaining mosaic forests are threatened by intensive deforestation and agricultural ploughing. Montane habitats, unfit for agricultural purposes, suffer from burning during the dry season and overgrazing during the wet season. Our faunal survey revealed the exceptional importance of the AM as one of the main Ethiopian mammal diversity hotspots. Unless dramatic conservation management measures are put in place soon, the high level of mammal endemism in this region and the intense and irreversible anthropogenic impacts currently occurring to mountain ecosystems are likely to result in the permanent loss of unique Afromontane endemic species.
We are indebted to the Ethiopian Wildlife Conservation Authority (EWCA) and the Oromia Forest and Wildlife Enterprise (OFWE) for the permission to work in the Arsi Mountains National Park (permission no. EWCA Ref. No. 31/336/05, 20/03/2013; OFWE 06/02/2015, and OFWE 18/02/2016). We are grateful to the JERBE Coordinators Dr. Andrei Darkov (Joint Ethio-Russian Biological Expedition, Fourth Phase – JERBE IV) and Ato Woubishet Tefessa (Ethiopian Ministry of Science and Technology) for management of the expedition in the field and in Addis Ababa. We thank Dr. Elena Zemlemerova for help with genotyping. We are grateful to Dr. Kevin Roche for the help with English corrections. Financial support for this study was provided by the Russian Foundation for Basic Research, projects no. 15-04-03801-a and 18-04-00563-a (Funder Id: 10.13039/501100002261), and the Czech Science Foundation, project no. 18-17398S.
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The online version of this article offers supplementary material (https://doi.org/10.1515/mamm-2017-0135).