Research Article |
Corresponding author: Werner Conradie ( werner@bayworld.co.za ) Academic editor: Peter Bartsch
© 2016 Werner Conradie, Gabriela Bittencourt-Silva, Hanlie M. Engelbrecht, Simon P. Loader, Michele Menegon, Cristóvão Nanvonamuquitxo, Michael Scott, Krystal A. Tolley.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Conradie W, Bittencourt-Silva GB, Engelbrecht HM, Loader SP, Menegon M, Nanvonamuquitxo C, Scott M, Tolley KA (2016) Exploration into the hidden world of Mozambique’s sky island forests: new discoveries of reptiles and amphibians. Zoosystematics and Evolution 92(2): 163-180. https://doi.org/10.3897/zse.92.9948
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We carried out a survey of reptiles and amphibians within Afromontane forest and woodland slopes of three inselbergs in northern Mozambique (Mount Mabu, Mount Namuli, and Mount Ribáuè). A total of 56 species (22 amphibians and 34 reptiles) were recorded during the current survey. Our findings substantially increase the number of herpetofaunal species recorded from these mountains (Mount Ribáuè 59%, Mount Mabu 37%, and Mount Namuli 11% of the total species), including one new country record and several putative new species. An updated checklist of the herpetofauna of these mountains is presented.
Amphibia , Reptilia , conservation, diversity, new species
Northern Mozambique (north of the Zambezi River and south of the Rovuma River) is biologically one of the most poorly known areas in Africa (see
The topography of northern Mozambique is characterised by isolated mountains (‘inselbergs’), mainly in the west closer to Mt. Mulanje in Malawi, where the highest peaks are found, but also by chains of smaller inselbergs extending eastwards towards the coast. These montane isolates form an important link between the better studied Eastern Arc Mountains (EAM) and the East African Coastal Forest (EACF).
Findings from previous surveys suggest the Mozambican montane sky island forests contain high levels of biodiversity, particularly in terms of single site endemics (e.g.
Through targeted fieldwork, we explored three poorly known montane isolates (Mts. Mabu, Namuli, and Ribáuè), to document their herpetofaunal diversity. We conducted intensive surveys on these mountains across several habitats and over an altitudinal gradient searching for amphibians and reptiles. Although some herpetological surveys have been done recently on Mt. Namuli (
The study area comprises of two mountain blocks in the Zambezia province and one in the Nampula province in northern Mozambique (Fig.
Map of localities surveyed in northern Mozambique. Black triangles indicate the mountains sampled during this study and grey triangles show other areas previously sampled in northern Mozambique and southern Malawi. Numbers indicate the following localities: (1) Mt. Chiperone, (2) Mt. Mulanje, (3) Mt. Inago, (4) Serra Jeci, (5) Serra Mecula.
Mountain | Locality | Province | Latitude | Longitude | Elevation (m) |
---|---|---|---|---|---|
Mabu | River Camp | Zambezia | -16.281528 | 36.443778 | 429 |
Forest Base Camp | Zambezia | -16.286222 | 36.400056 | 987 | |
Summit Camp | Zambezia | -16.296817 | 36.392433 | 1609 | |
Namuli | Pese dome | Zambezia | -15.386420 | 37.033520 | 1892 |
Ukalini dome | Zambezia | -15.369367 | 37.061417 | 1616 | |
Muretha Plateau | Zambezia | -15.387194 | 37.044611 | 1892 | |
Satellite Camp | Zambezia | -15.397972 | 37.019778 | 1633 | |
M’pàluwé | Oasis Water Camp | Nampula | -14.915220 | 38.316450 | 588 |
Miombo area | Nampula | -14.902583 | 38.323306 | 714 | |
Summit area | Nampula | -14.889306 | 38.316139 | 1366 |
For both Mt. Mabu (Fig.
In northern Mozambique, the average temperature in the warmest months (December-February) varies between 20–25 ºC, and in the cooler months between 15–20 ºC. The wet season lasts from November-April when the average rainfall per month is 150–300 mm (
We conducted herpetofaunal surveys in the study area, between 15 November and 4 December 2014, using a combination of visual encounter survey and standard drift fences with pitfalls (each trap array consisted of 3 × 10 m long and 50 cm high fences positioned in a Y-shape with four pitfall traps at the ends and middle, and two one-way funnels per fence – only employed at Mts. Mabu and Namuli). Diurnal searches were done by actively looking for specific microhabitats including underneath rocks and logs. Nocturnal surveys were carried out with the use of headlamps or flashlights. Specimens were captured by hand, hook stick, noosing or net (e.g. tadpoles), and euthanized, according to ethically approved methods (
Specimens were identified using field guides (
A total of 27 amphibian species representing 10 families and 14 genera (Table
Updated species lists for amphibians based on historical records as well as data from the current surveys. Parentheses in the totals given denote the number of new species recorded during the current surveys. Literature records are indicated with L and new records with N.
ORDER/Family | Species | Mount Mabu | Mount Namuli | Mount M’pàluwé |
---|---|---|---|---|
ANURA | ||||
Arthroleptidae | Arthroleptis francei | L,N | L,N | |
Arthroleptis stenodactylus | L,N | N | L,N | |
Arthroleptis xenodactyloides | L,N | L | L,N | |
Leptopelis broadleyi | L,N | |||
Leptopelis flavomaculatus | L,N | N | ||
Brevicipitidae | Breviceps mossambicus | L,N | N | |
Bufonidae | Sclerophrys gutturalis | L,N | ||
Sclerophrys pusilla | L,N | L | N | |
Hyperoliidae | Afrixalus brachycnemis | L,N | L | N |
Afrixalus fornasini | N | |||
Hyperolius nasutus complex | L | |||
Hyperolius marmoratus albofasciatus | L,N | |||
Hyperolius spinigularis | L | |||
Hyperolius substriatus | L,N | L,N | ||
Phrynobatrachidae | Phrynobatrachus natalensis | L | ||
Phrynobatrachus acridoides | L,N | |||
Phrynobatrachus mababiensis | L | L,N | ||
Pipidae | Xenopus laevis | N | ||
Ptychadenidae | Ptychadena anchietae | L,N | ||
Ptychadena taenioscelis | N | |||
Ptychadena guibei | L | |||
Ptychadena cf. porossisima | L,N | |||
Pyxicephalidae | Amietia quecketti | N | L,N | L,N |
Nothophryne cf. broadleyi | L,N | L,N | ||
Strongylopus fuelleborni | N | L,N | ||
Rhacophoridae | Chiromantis xerampelina | L | ||
GYMNOPHIONA | ||||
Scolecomorphidae | Scolecomorphus kirkii | N | L | |
12 (5) | 18 (2) | 15 (4) |
Updated species lists for reptiles based on historical records as well as data from the current surveys. Parentheses in the totals given denote the number of new species recorded during the current surveys. Literature records are indicated with L and new records with N.
ORDER/Family | Species | Mount Mabu | Mount Namuli | Mount M’pàluwé |
CHELONIA | ||||
Testudinidae | Kinixys belliana | L | ||
SQUAMATA | ||||
Agamidae | Agama kirkii | L,N | N | |
Agama mossambica | L | L | ||
Chamaeleonidae | Chamaeleo dilepis | L,N | ||
Nadzikambia baylissi | L,N | N | ||
Rhampholeon tilburyi | L,N | |||
Rhampholeon maspictus | L,N | |||
Rhampholeon sp. | N | |||
Trioceros melleri | L | |||
Cordylidae | Platysaurus maculatus | L,N | ||
Gekkonidae | Chondrodactylus turneri | N | ||
Hemidactylus mabouia | N | L | ||
Hemidactylus platycephalus | L | N | ||
Lygodactylus grotei | N | |||
Lygodactylus regulus | L,N | |||
Lygodactylus cf. rex | N | |||
Lygodactylus sp. | N | |||
Lacertidae | Holaspis laevis | N | ||
Scincidae | Melanoseps cf. ater | L,N | L | |
Mochlus afer | L | |||
Panaspis wahlbergi | L | |||
Trachylepis boulengeri | N | |||
Trachylepis maculilabris | N | |||
Trachylepis margaritifer | L | L | N | |
Trachylepis striata | L,N | |||
Trachylepis varia | L,N | L,N | N | |
Colubridae | Dispholidus typus | N | L,N | |
Dipsadoboa cf. shrevei shrevei | L,N | N | ||
Philothamnus angolensis | L,N | |||
Philothamnus cf. carinatus | L | |||
Philothamnus hoplogaster | N | N | ||
Thelotornis mossambicanus | N | L | N | |
Elapidae | Naja melanoleuca | L,N | L | |
Naja mossambica | N | |||
Lamprophiidae | Boaedon capensis | L | N | |
Duberria shirana | N | |||
Gonionotophis capensis | N | |||
Lycophidion acutirostre | L | |||
Psammophis orientalis | N | |||
Psammophylax variabilis | L,N | |||
Natricidae | Natriciteres sylvatica | L | L | |
Viperidae | Atheris mabuensis | L | L | |
Bitis arietans | L | N | ||
Bitis gabonica | L | L | ||
Causus defilippi | L | |||
23 (8) | 27 (3) | 17 (15) |
During the current survey we recorded four species of reptiles endemic to Mozambique (Nadzikambia baylissi, Rhampholeon maspictus, Rhampholeon tilburyi, and Lygodactylus regulus), and four putative new species of Nothophryne (
Mt. Mabu (
Specimens were collected from moist leaf litter in closed-canopy forest (Fig.
A selection of amphibians from northern Mozambique inselbergs. A – Arthroleptis francei (Mt. Namuli,
Mt. Mabu (
Found in both dry transitional miombo woodland and montane forest (Fig.
Mt. Mabu (
In Mt. Mabu it was common on the forest floor, and at Mt. M’pàluwé it was found in moist leaf litter at lower elevations (Fig.
Mt. M’pàluwé (
Sub-adult male specimen was collected from mid-elevation slopes while calling from low vegetation. This species is part of the L. argenteus group. Some authors regard this as a valid species (
Mt. Mabu (
Common along streams at both Mt. Mabu and Mt. Namuli. In most cases, the males of this species are much smaller and have a uniform lime-green dorsum with yellow spots. All the males have well developed pectoral glands. Females are much larger with dull brown dorsum with scattered green spots or patterns.
Mt. Namuli (
Both specimens are males, based on the presence of a very dark throat and small size. The specimen from Mt. M’pàluwé was collected at night in a shamba at mid-elevation (ca. 1000 m).
Mt. Namuli (
One adult female collected from Muretha Plateau at night. No red infusions on the thighs or side of the body were observed, but the well-elevated parotid glands exclude it from being S. pusilla.
Mt. Mabu (
Specimens were found calling along low-elevation streams at dusk.
Mt. Mabu (
Adult male was collected during the day sitting on a leaf in an open area at lower slopes of Mt. Mabu. Two females were collected sheltering in sugarcane fronds at the base of Mt. M’pàluwé. Species identification was based on the absence of dorsal patterning and transverse tibial bands (
Mt. Mabu (
Three females were collected along a low-elevation forest stream. One female (
Mt. Namuli (
Found to be abundant on the grassland of the Muretha Plateau at Mt. Namuli. Males were found calling from very low vegetation close to water level. Adult males and females exhibit the same dorsal pattern indicating no sexual dichromatism. The H. marmoratus group consists of many regional colour patterns and this population conforms to that of H. marmoratus albofasciatus (
Mt. Mabu (
Found in abundance at low, mid (ca. 920 m asl) and high elevations along forested streams at both Mts. Mabu and Namuli. All material showed typical adult coloration, similar to that reported by
Mt. M’pàluwé (
Found moving near stagnant pools at a low-elevation (544 m asl) streams. Species identification was based on extensive webbing and swollen toe tips.
Mt. M’pàluwé (
Specimens were found in dry leaf litter at low elevation, and two individuals were collected in the same microhabitat as Nothophryne cf. broadleyi (in water seepage over rocks).
Mt. Mabu (
One specimen was collected from a low-elevation stream below an old hydroelectricity dam.
Mt. M’pàluwé (
Was found on dry leaf litter at low elevation.
Mt. Namuli (
Collected from grassland on Muretha Plateau. This specimen is tentatively identified as Ptychadena cf. porosissima using the key provided in
Mt. M’pàluwé (
Found on dry leaf litter at low slopes of Mt. M’pàluwé. Identification was based on the key provided in
Mt. Mabu (
Mt. Namuli (
Specimens were collected both during the day and at night from rocky outcrops in water seepages (Fig.
Mt. Mabu (
Part of the Strongylopus faciatus group that has seen two newly described species in recent years (
Mt. Mabu (
A single specimen was found under a log in the closed canopy forest of Mt. Mabu after 36 hours of heavy rain (Fig.
Mt. Namuli (
Collected at the lower slopes on the rocky outcrops of both Mt. Namuli and Mt. M’pàluwé. Both males brightly coloured, while females are dull in overall colouration.
Mt. Namuli (
One specimen collected in Gurúè town. This record was omitted from our final checklist of the inselbergs, as it was collected from the low lying town (see Results and Discussion).
Mt. Namuli (
One specimen donated by a local, presumably obtained from near the village just below the Muretha Plateau.
Mt. Mabu (
Collected from canopy forest, in Afromontane forest above 600 m asl. Historically, Nadzikambia was considered a monotypic genus endemic to Mt. Mulanje (
A selection of reptiles from northern Mozambique inselbergs. A – Nadzikambia baylissi (Mt. Namuli,
Mt. Namuli (
This newly described species of pygmy chameleon was collected from Mt. Namuli at both the Ukalini forest and the forest patches on the Muretha Plateau (Fig.
Mt. Mabu (
Specimens were found in Afromontane forest above 1900 m asl. This species is restricted to Mt. Mabu.
Mt. M’pàluwé (
This is the first record of a pygmy chameleon from Mt. Ribuáuè insolates forests (Fig.
Mt. M’pàluwé (
Collected from the lower slopes of Mt. M’pàluwé where they were found in abundance running on rocky slopes. Previously, collected from Mt. M’pàluwé [=Ribáuè] by
Mt. M’pàluwé (
Collected at night on rock surface at lower slopes.
Mt. Mabu (
Collected at Mt. Mabu from rock surface and under tree bark in low to mid-elevation. At Mt. M’pàluwé specimens were collected in sympatry with H. platycephalus on derelict buildings of the Oasis Water Camp.
Mt. M’pàluwé (
Collected from derelict buildings and mango trees around the Oasis Water Camp.
Mt. Mabu (
Collected at the base of a tree in dry miombo woodland.
Mt. Namuli (
Recently described gecko related to the larger L. rex from Mt. Mulanje (see
Mt. Mabu (
Specimens were collected from tree trunks in transitional miombo at lower slopes (Fig.
Mt. M’pàluwé (
One individual collected from a tree trunk in a newly cleared shamba at the top of Mt. M’pàluwé at night. Specimen from Mt. M’pàluwé differs from L. cf. rex from Mt. Mabu, and L. regulus from Mt Namuli in that they lack the conspicuous ocellus above the shoulder. It closely resembles L. angularis in general throat markings and that the mental is entire and not split with shallow lateral slits as in the L. rex group.
Mt. Mabu (
Found on tree trunks in transitional miombo woodland at lower slopes (Fig.
Mt. Mabu (
Mt. M’pàluwé (
Only one specimen was collected in dry bamboo leaves from the eastern slopes of Mt. M’pàluwé. This species is known from only a handful of records from northern Mozambique, e.g. Niassa (Branch et al. 2005), and Marrupula (
Mt. Mabu (
One adult female was collected from a transition woodland. Branch et al. (2005) were the first to record this species from northern Mozambique and indicate, based on material used from coastal northern Mozambique (
Mt. M’pàluwé (
Two adult females were collected from the Oasis Water Camp running among outbuildings and on rocky slopes.
Mt. Namuli (
Specimen was collected from the lower slopes of Mt. Namuli running on granite rocky outcrops. Common and widespread species in southern Africa, but only recorded from Niassa (Branch et al. 2005), Namuli and Lichinga (
Mt. Mabu (
Specimens from Mts. Mabu and M’pàluwé represent the plain tan brown dorsum coloration with dark-edged white lateral line and uniform beige ventrum, while the montane grassland population of the Murteha Plateau of Mt. Namuli have the dorsum greenish with five finely striped white lines, and ventrally a bluish darker colouration.
Mt. M’pàluwé (
Juvenile dislodged by a Southern Shrike (Lanius sp.) from the branches of a mango tree at the Oasis Water Camp. This specimen can be assigned to the northern race D. typus viridis (Smith, 1828).
Mt. Mabu (
Specimens collected from forest floor or in low growing trees along streams (Fig.
Mt. Namuli (
One specimen collected from mid-elevation forested stream, swimming across the stream at the base of the two Namuli granite domes when disturbed.
Mt. Mabu (
Specimen collected from Mt. Mabu has 10 black spots anterior on the dorsum, while the Mt. M’pàluwé specimen has uniform lime-green colouration. The Mt. Mabu specimen was collected from an overhanging tree along a well vegetated low-elevation stream at night, while the Mt. M’pàluwé was collected around a water tank at the Oasis Water Camp.
Mt. Mabu (
At Mt. Mabu one specimen was collected from closed-canopy forest while the other was collected in transitional miombo woodland. A male and female specimen donated by a local presumably obtained from near Ribáuè town. The juvenile collected from closed-canopy forest had a juvenile Rhampholeon maspictus in its stomach.
Mt. M’pàluwé (
Collected at night on the lower slopes near the shambas.
Mt. M’pàluwé (
A female specimen donated by a local, presumably obtained from near Ribáuè town. We follow
Mt. Namuli (
Collected in a funnel trap situated in montane grassland of the Muretha Plateau (Fig.
Mt. Mabu (
Two specimens were collected on the same night (15 November 2014) from the same locality near a stream at the base of Mt. Mabu. It is possible that the male was following the female, as they were collected minutes apart.
Mt. M’pàluwé (
One specimen collected at night, one meter from the ground in a low growing shrub in transitional miombo.
Mt. Namuli (
Collected in montane grassland on the Muretha Plateau (Fig.
Mt. M’pàluwé (
One specimen collected at night on the path near the shambas.
We have found eight putative new species through field identification, added additional species known from northern inselbergs (13 species to Mt. Mabu, five species to Mt. Namuli, and 19 species to Mt. M’pàluwé), and one new country record. Additional analyses are necessary, including barcoding and phylogenetic analyses, to determine whether these mountains are exceptionally high in species richness. We now know there are at least 30-40 species of reptiles and amphibians on each of these sky islands, many of which are montane endemics. Although the state of knowledge is growing for Mt. Mabu and Mt. Namuli and can be considered to be relatively well sampled, it is clear that Mt. Ribáuè isolates requires more work given the brevity of our survey. In addition, several other sky islands in the area have received little or no attention in terms of the herpetofaunal survey (e.g. Mt. Inago and Mt. Chiperone).
The present collection is essentially a preliminary assessment of amphibian and reptile diversity in the region and does not account for seasonal variation in activity of herpetofauna. Future surveys that are more comprehensive in space and over time should considerably increase our understanding of the regional diversity, endemism, and richness of these inselbergs. Although the state of biodiversity knowledge has grown for Mts. Mabu and Namuli, there is an urgent need for a clear understanding of the nature of threats, and mitigation measures that will directly improve protection of habitat. At Mt. Ribàué additional surveys are imperative, given the comparatively limited exploration on that mountain coupled with the apparent high rate of forest clearing. Overall, the sky islands of Mozambique clearly require additional surveys to quantify species richness and endemism for a broad range of taxonomic groups. Ultimately, a better understanding of the threats to biodiversity will allow for prioritisation of conservation interventions.
We thank the Natural History Museum of Maputo who endorsed and provided permits to carry out this work, National Geographic Society Committee for Research and Exploration (CRE 9281-13), the South African National Biodiversity Institute, and the National Research Foundation of South Africa (Grant #92776) for providing funding and logistical support for the 2014 survey, and Khangela Safaris for camp logistics in 2014. We also thank Bill Branch and Harith Farooq for their support for this survey, and the Swiss-African Kick-Start Funding, the Freiwillige Akademische Gesellschaft and the University of Basel for funding contributions to SPL and GBBS. We thank the two reviewers and editor whose comments improved the quality of this paper.