CHURA: Conserving Hyperendemic Udzungwa Restricted Amphibians

Posted by Elena Tonelli & Simon Valle

CHURA means frog in Swahili (Tanzania’s official language), and is also the acronym chosen for our project 'Conserving Hyperendemic Udzungwa Restricted Amphibians'.

The project focuses on the Udzungwa Scarp Forest Reserve (USFR; 200 km² ), a global biodiversity hotspot at the south-western end of the Eastern Arc Mountain (EAM) range, Tanzania. The great altitude range  (300–2068 m) and variety of vegetation types have contributed to an extraordinary number of strictly endemic species at the site. Four frog species (Kihansi spray toad Nectophrynoides asperginis, Poyntoni forest toad N. poyntoni, Wendy forest toad N. wendyae, and Kihanga reed frog Hyperolius kihangensis) are known only from specific sites on the scarp, and are regarded as ’hyper-endemics’. However, large portions of the forest remain unexplored and basic genetic and ecological data are lacking. 

The Kilombero Valley visible from the top of a waterfall around 1100 m (Photo E. Tonelli) 

Currently, we are refining amphibian inventories of the area, and examining species distribution, ecology and community dynamics throughout the USFR using ecological and molecular approaches. Given the occurrence of morphologically similar anuran species in the EAM range and that Eastern Arc herpetofauna shows distinctive changes in assemblages with small increases in altitude, genetic analysis is crucial to enable correct taxonomic classification, detection of potential sibling species and proper estimation of distributions. By adequately surveying the area and revising the conservation status of its amphibian species, my PhD project aims to support conservation management of this proposed Nature Reserve. 

Pitfall traps with drift fences 
(Photo E. Tonelli)

Three field seasons have been planned for the whole PhD project, each one lasting from November to March and coinciding with the short rains and the reproductive period, when amphibians’ detectability is higher. Field methods comprise pitfall traps with drift fences, night transects, day search with timed digging, opportunistic surveys, and audio recording. Since different species have different needs, all habitats are sampled, from closed canopy forest to open grasslands, from large rivers with waterfalls to shallow streams or ponds. The USFR is an exciting but demanding study area, with very steep, muddy paths connecting the Kilombero valley (about 200 m ) to the villages on the plateau at the top (about 2100 m). In many areas there are no paths at all, making movement slow.

In a previous study Menegon and Salvidio (2005), recorded 36 amphibian species in just five sites within USFR. We suspect this forest will surprise us again with some species still unknown to science and possibly a few more highly range-restricted amphibians.My team surveyed the historical sites of two hyper-endemics, with a rewarding outcome for the Kihanga reed frog H. kihangensis, which we found both in its historical site and in a new area over 7 km far from that previously known. This is potentially good news for the species, but it also suggests that some of the frogs we refer to as hyper-endemics are possibly more widespread in the scarp than first thought.

New sites have been discovered for the range restricted Kihanga reed frog (Photo E. Tonelli) 

This said, we weren’t as lucky with Poynton’s forest toad N. poyntoni, which we unsuccessfully tried to locate both in November and February. This is worrying since the species has not been recorded in its only known location in the past 10 years. We plan to survey the historical site again in the coming field season, hopefully with more encouraging results. Along with previously studied sites, three new sites at different altitudes were investigated. A total of 8 genera and 18 species were recorded, at least one of these species is new to science.

Callulina sp.,a new record for the USFR and possibly a new species (Photo E. Tonelli) 

 Table 1. Anuran species recorded along with altitudinal range.

    Recorded species                                                                             Altitude range m

    Afrixalus cf. uluguruensis                                                                     1650 - 1760

    Amietia angolensis                                                                                 1650 - 1740

    Arthroleptides yakusini                                                                          900 - 1200

    Arthroleptis affinis                                                                                  900 - 1760

    Arthroleptis reichei                                                                                 900 - 1760

    Arthroleptis stenodactylus                                                                    800 - 1760

   Arthroleptis xenodactyloides                                                                900 - 1760

   Callulina sp. (new record for USFR and possibly a new species)       1200

   Hyperolius kihangensis                                                                                1750

   Hyperolius minutissimus                                                                     1650 - 1740

   Hyperolius sp.                                                                                                1750

   Hyperolius substriatus                                                                          1750 - 1740

   L. cf. grandiceps                                                                                      1200  - 1760

   Leptopelis parkeri                                                                                         1650

   Leptopelis uluguruensis                                                                        900 - 1200

  Nectophrynoides sp. (new species)                                                          1650

  Nectophrynoides tornieri                                                                           1200

Molecular analysis on museum samples showed a remarkable genetic variety in the Scarp, especially within the genus Arthroleptis. We aim to disentangle the relationship between many cryptic sibling-species which occur in this forest using multiple genes.

Afrixalus cf. Uluguruensis (adult male, eggs and juvenile)

Next steps

In the two field seasons ahead I plan to survey 15 more sites, one of which will be the historical location of the hyper-endemic Wendy’s forest toad Nectoprhynoides wendyae at the south-western end of the reserve. Skin swabbing will be used to screen encountered individuals for Batrachochytrium dendrobatidis (Bd), a fungal pathogen which has been responsible for local amphibian extinction worldwide. 

John Lyakurva, a Tanzanian student from Dar es Salaam University will join the project next month. He will be trained in herpetological survey techniques to eventually lead one more team thereby covering a larger sampling area. Along with data on amphibians however, he will collect  data on reptile species occurrence and distribution in relation to altitude.

References

Menegon,  M.  and  Salvidio, S.  (2005)  Amphibians  and  reptiles  diversity  in  the  southern Udzungwa Scarp Forest Reserve, south-eastern Tanzania. In: Huber, B.A., B.J. Sinclair, K.-H.  Lampe  (eds).  African  biodiversity:  molecules,  organisms,  ecosystems.  Springer,  New York, pp 205–212.

Acknowledgements

Elena's work is done in collaboration with University of Basel and has been generously supported by
 

Reconstructing Atheris viper evolution in Africa

Posted by Michele Menegon and Stuart Marsden

A paper published recently in Molecular Phylogenetics & Evolution by Michele Menegon, PhD student in the group, Simon Loader and Sylvain Ursenbacher (University of Basel), William Branch (Nelson Mandela Metropolitan University), Tim Davenport (Wildlife Conservation Society), and Stu, reconstructs the evolutionary history of Atheris vipers across Africa.

 

The team analysed mitochondrial DNA to uncover phylogenetic relationships among Africa's wonderful Atheris viper species, including Matilda’s Horned Viper (Atheris matildae), a species recently discovered by Michele, Tim Davenport and Kim Howell (Menegon et al. 2011).

 

The recently discovered Matilda's Horned Viper Atheris matildae (Photo: Michele Menegon)

The study used molecular clock estimates to age taxa, and clades within ten of the genus’ 15  species. This was done to investigate whether the timing of the divergence within Atheris corresponds to specific geographic and climatic events. In other words, where did the forest-associated species we find today in the mountains of the EAM hotspot come from, and how does their current pattern of distribution and endemism across mountains fit with geological changes such as the formation of the Rift Valley, and climatic changes over the past 20 million years?

Africa's dry lowlands form barriers to dispersal in forest-associated reptiles and amphibians (Photo: Michele Menegon)

Analyses indicate that the early diversification of the genus probably took place in lowland Central/West Africa around 15-18 mya, potentially coinciding with the final phase of the existence of the ‘pan-African forest’ (a period when moist forest stretched right across the continent). The descendants from this first colonization from Central Africa to Eastern Africa are species currently confined to high mountains of Mozambique (A. mabuensis) and Kenya (A. desaixi). The presence of these species on distant mountain tops, with no known sister species from intervening mountains, may indicate that there have been many extinctions of species since the initial colonisation and divergence.

Atheris rungweensis (Photo: Michele Menegon)

More recently, between seven and nine million years, we highlighted divergences of extant species from the fragmented montane forests of the Albertine Rift, Southern Highlands and Eastern Arc Mountains. This phylogenetic pattern suggests a more recent colonization into these areas, delayed by around 7 million years from the first appearance of the genus in East Africa (A. nitschei and A. rungweensis in the Albertine Rift and A. ceratophora, A. matildae and A. barbouri in the Eastern Arc). 

Atheris nitschei (Photo: Michele Menegon)

A possible reason for this late colonization is the physical and climatic barrier of the Great Rift Valley. Such narrowing of dispersal routes might have promoted a ‘C-shaped’ dispersal route with a northern and a southern front – where species’ ‘relatedness’ tracks the species along these routes. Interestingly, despite the late colonization of the mountain ranges east of the Albertine Rift, a high proportion of current Atheris diversity occurs there, highlighting the likely role of mountains in promoting speciation and species accumulation.

The exquisite Uzungwe viper Atheris barbouri, considered one of the rarest snakes in the world (Photo: Silvia Ceppi)

 
Of the 15 recognised species, only one (A. squamigera) has a particularly wide distribution ranging from Nigeria in the west, across the Congolian forest belt to western Kenya in the east and Angola in the south (Phelps 2010). All other Atheris species have small known ranges. For example, A. desaixi is found in just two localities in the Kenyan highlands, A. mabuensis in two mountain blocks in Mozambique, A. acuminata is known for a single locality in Uganda and the newly described A. matildae in a single forest fragment in the Southern Highlands of Tanzania. Of course, these restricted-range vipers, like other herps of the Eastern Arc such as Nectophrynoides toads, will face intense battles to avoid extinction in the future. Michele’s PhD will further examine the protection offered to these herps across the region. 

Maintaining intact Afromontane forests holds the key to conserving restricted-range Atheris vipers (Photo:Michele Menegon)

References

Menegon M, Davenport TRB, Howell KM. (2011). Description of a new and critically endangered species of Atheris (Serpentes: Viperidae) from the Southern Highlands of Tanzania, with an overview of the country's tree viper fauna. Zootaxa 3120: 43-54. (Atheris matildae sp. nov.)

Menegon, M., Loader, S.P., Marsden, S.J. Branch, W., Davenport, T. & Ursenbacher, S. (2014). The genus Atheris (Serpentes: Viperidae) in East Africa: phylogeny and the role of rifting and paleoclimate in shaping the current pattern of species diversity. Molecular Phylogenetics & Evolution 79: 12-22.

Phelps, T. (2010). Old World Vipers, A Natural History of the Azemiopinae and Viperinae. Edition Chimaira, Frankfurt am Main, Germany, 558 pp.

Amphibian declines in Bale, Ethiopia

Posted by Michele Menegon

The creation of a new road in the Bale Mountains, Ethiopia, in the 1980s gave herpetologists a rare opportunity to study amphibians in the area. Michele, a PhD student in the research group, was part of a team which recently repeated Amphibian surveys first done in 1986. The team found some potentially very serious declines in amphibians from the area. Results have recently been published in the journal Oryx.

The Bale Mountains

The Bale Mountains lie in southern Ethiopia, east of the Rift Valley. The Mountains rise to nearly 4,400 m, and the extensive massif has a rich flora and fauna, including many unique, rare, spectacular and threatened taxa. Hillman (1986) considered the Mountains ‘a centre of faunal endemicity, probably with the highest rate of animal endemicity for a terrestrial habitat anywhere in the world’.

Ethiopian wolf (Canis simensis) one of the many endemics of the Bale Mountains (Photo: Paul Donald)

The highest part of the region, the Sanetti Plateau and associated peaks, comprises Afroalpine grasslands but to the south is the Harenna escarpment that drops from 3,200 to 2,000 m in just 8 km. A substantial area (c. 2,200 sq km) of the region is covered by the Bale Mountains National Park, established in 1971 but not yet formally gazetted by the Ethiopian government.

Forest alteration in Harenna Forest (Photo: M. Menegon)

Bale’s frogs and toads

Despite a long history of human habitation in the area, the Bale Mountains remained largely unexplored scientifically until the middle of the 20th century. W.H. Osgood, from the Chicago Field Museum,  collected some amphibians and reptiles in 1926–1927, and M.J. Largen and colleagues carried out extensive collections between 1971 and 1975. Early collecting expeditions were centred around Dinshu and the northern slopes below the Sanetti Plateau.

Around 15 amphibian species (all anurans) have been reported from the Bale Mountains, including 10 endemics (Largen, 2001; Largen & Spawls, 2010). The Bale Mountains National Park is an ‘Alliance for Zero Extinction’ site (http://www.zeroextinction.org), partly because of its threatened amphibians (Alliance for Zero Extinction, 2010). Given the Park’s importance for their conservation, we focus here on four monotypic frog genera: all endemic to Ethiopia and three endemic to the Bale Mountains.

Bale mountains moss frog (Balebreviceps hillmani)  (Photo: M. Menegon)

The survey and re-survey

In 1983, when a new road was constructed through the forest, it became possible to reach the Harenna Forest, on the southern side of the massif. Conscious of the conservation threat posed by the new road, the Ethiopian Wildlife Conservation Organization arranged an expedition with Addis Ababa University to conduct a preliminary survey of the Harenna Forest in August 1986. During a meeting in London a few years ago, Dr. Largen said that all the species discovered during the 1986 expedition were abundant, or very abundant, and that they often were seen, directly from the car, moving around the vegetation right by the side of the road.

In 2009, I was part of a team of five researchers, David Gower from the NHML, U.K. Simon Loader and Abebe Mengistu from University of Basel, Switzerland, and Rafael de Sa from University of Richmond, U.S.A. We spent around one month surveying frogs both in Bale Mountains and some of the western forests around the town of Bonga. This survey gave us the opportunity to re-survey frogs in the areas first surveyed in 1986. At that time, frogs were easy to find along the newly cut road – the surveyors could simply stop their car and collect many species of frogs right by the side of the road.

Altiphrynoides malcolmi:  a genus endemic to Bale Mountains (Photo: M. Menegon)

The results of our re-survey are presented in an Oryx paper. We present long-term quantitative data (individuals encountered per person hour of searching) for four monotypic frog genera endemic to an Afromontane region of exceptional importance, but growing conservation concern. These include one endemic to the Ethiopian highlands Altiphrynoides osgoodi and three endemic to the Bale Mountains: Altiphrynoides malcolmi; Balebreviceps hillmani; and Ericabatrachus baleensis; all collected during 15 field trips to the Bale Mountains between 1971 and 2009.

Only a single confirmed sighting of S. osgoodi has been made since 1995. The other three species have also declined, at least locally. E. baleensis appears to have been extirpated at its type locality and at the same site B. hillmani has declined. These declines may be associated with substantial habitat degradation caused by a growing local human population. Chytrid fungus was also found on several frog species in Bale, although no dead or moribund frogs have yet been encountered. These results mean there is an urgent need for more amphibian surveys in the Bale Mountains. Additionally, we argue that detrimental human exploitation must be halted immediately in at least some parts of the Harenna Forest if a local, and hence global, conservation crisis is to be averted.

Balebreviceps hillmani  (Photo: M. Menegon)

References

Alliance for Zero Extinction (2010) 2010 AZE Update. http://www.zeroextinction.org 

Gower, D.J., Aberra, R.K., Schwaller, S., Largen, M.J., Collen, B., Spawls, S., Menegon, M.,
Zimkus, B.M., De Sá, R., Mengistu, A., Gebresenbeta, F., Moore, R.D., Saber, S.A.  and Loader, S.P. (2013) Long-term data for endemic frog genera reveal potential conservation crisis in the Bale Mountains. Ethiopia. Oryx 47(1):56–59

Hillman, J. (1986) Bale Mountains National Park. Management Plan. Ethiopian Wildlife Conservation Organization, Addis Ababa, Ethiopia.

Largen, M.J. (2001) Catalogue of the amphibians of Ethiopia, including a key for their identification.Tropical Zoology, 14:307–402.

Largen, M.J. & Spawls, L. (2010) The Amphibians and Reptiles of Ethiopia and Eritrea. Chimaira, Frankfurt Am Main, Germany.

Can we make space for the Kipunji?

Posted by Claire Bracebridge and Stuart Marsden

Just published on-line at International Journal of Primatology:

The recently described kipunji Rungwecebus kipunji is endemic to two mountains in Tanzania. The species has a tiny extent of occurrence (42 sq km) and an estimated population of just over 1,000 individuals. Previous research in Rungwe (Bracebridge et al. 2011) found  that there is limited room for expansion of the range of kipunji within the forest – mainly because the areas of forest currently unoccupied are at higher altitudes which are unsuitable for the species. More suitable would be areas at lower altitude but these have unfortunately already been deforested to make way for agriculture. This paper examined Kipunji’s use of areas outside the forest and how such areas might be used in future conservation efforts. 

 

The recently discovered Kipunji is one of the World's Critically Endangered primates.

Land outside protected forest is dominated by subsistence agriculture with tiny patches of forest covering around 2% of the land within 10 km of the forest boundary. Kipunji rarely venture outside the forest block but do occasionally crop-raid people’s maize and, of course, people react to crop losses. The Bujingijila corridor (2.1 sq km) is a priority site for reforestation, particularly in the context of ongoing ‘Reducing Emissions from Deforestation and Forest Degradation (REDD+)’ activities. Reforesting Bujingijila could provide habitat for an additional 88 kipunji (an 8% increase in the population). Bujingijila has the additional benefit of reconnecting the Mt. Rungwe and Livingstone kipunji subpopulations.

References:

Bracebridge, C.E., Davenport, T.R.B. & Marsden, S.J. (2011) Can we extend the area of occupancy of the kipunji, a critically endangered African primate? Animal Conservation 14: 687-696

 

Claire’s PhD was funded by Wildlife Conservation Society – Tanzania