Research Article |
Corresponding author: Mark-Oliver Roedel ( mo.roedel@mfn-berlin.de ) Academic editor: Matthias Glaubrecht
© 2014 Mark-Oliver Roedel, Mike Emmrich, Johannes Penner, Andreas Schmitz, Michael Barej.
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:
Roedel M, Emmrich M, Penner J, Schmitz A, Barej M (2014) The taxonomic status of two West African Leptopelis species: L. macrotis Schiøtz, 1967 and L. spiritusnoctis Rödel, 2007 (Amphibia: Anura: Arthroleptidae). Zoosystematics and Evolution 90(1): 21-31. https://doi.org/10.3897/zse.90.7120
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We herein examine the taxonomic status of two West African forest-dwelling Leptopelis species. The small L. spiritusnoctis, described from the Upper Guinean forests of West Africa, was recently synonymized with L. aubryi, described from Gabon. The large L. macrotis, known from Ghana to Sierra Leone, was downgraded to a subspecies of L. millsoni, ranging from the Niger Delta to eastern Democratic Republic of Congo. These taxonomic decisions are in contrast to the general biogeographic pattern of African forest anurans and we consequently tested if the morphologically similar taxon pairs are indeed conspecifics by applying acoustic and molecular techniques. Both techniques confirmed that populations from West Africa differ significantly from their Central African morphological equivalents. Consequently, we herein resurrect L. spiritusnoctis as a valid species. The acoustic data indicate that L. aubryi may comprise a complex of cryptic species. We further advocate using the name L. macrotis for West African and L. millsoni for Central African populations of these larger arboreal frogs. However, we had neither genetic nor acoustic data from the type locality of L. millsoni available and could not clarify if these frogs belong to the more western or eastern taxon or even represent a Nigerian endemic. Thus, it is possible that West African populations need to be termed L. millsoni in the future. For populations east of the Cross River, Nigeria, the name L. guineensis would be available.
Advertisement calls, DNA-barcoding, biogeography, Central Africa, rainforest, taxonomy, treefrogs, West Africa
In many older and recent herpetological papers the term West Africa is used to describe a region, ranging approximately from Senegal in the northwest, along the western coast of the continent to Gabon, or even further south to northern Angola. However, recent investigations showed that the Upper and parts of the Lower Guinean forests, as defined based on plant distributions (see
Biogeographic subdivisions are even found within West Africa (
As detailed morphological descriptions of these species show, they are morphologically very similar to each other (
Life coloration and morphology in Leptopelis aubryi (a-c) and L. spiritusnoctis (d-h); a) L. aubryi, ZFMK 89562, call analyzed herein, and b) ZFMK 89560, call analyzed herein, both frogs from Big Massaka, Cameroon, large pictures color during night, inlet pictures color during daytime; c) L. aubryi (ZFMK 87728) from Nkoelon, Cameroon; d) L. spiritusnoctis (ZMB 79578) from Banambala, Guinea; e) L. spiritusnoctis (ZMB 79580) from Mt. Jideh, Liberia; f-h) L. spiritusnoctis (ZMB 79581-583) from Sapo National Park, Liberia.
Life coloration and morphology in Leptopelis macrotis (a-c) and L. millsoni (d); L. macrotis from a) Yomou, Guinea (ZMB 79585); b) Mt. Jideh, Liberia (ZMB 79587); c) Gola Rainforest National Park, Sierra Leone (type locality, not collected); d) L. millsoni from Nkoelon, Cameroon (ZFMK 87708).
Specimens of all four species have been collected by ourselves in various West African countries and Cameroon, respectively, or were obtained from the collections of the Zoologisches Forschungsmuseum Alexander Koenig, Bonn (ZFMK) and the Museum für Naturkunde, Berlin (ZMB; see
Origin, museum collection and GenBank accession numbers of the four West and Central African Leptopelis species compared herein.
Species | Catalogue | GenBank # | Locality | Country |
---|---|---|---|---|
L. aubryi | ZFMK 73157 | KF888326 | Barrage de Tchimbélé | Gabon |
L. aubryi | ZFMK 73236 | KF888327 | Fougamou | Gabon |
L. aubryi | ZFMK 75456 | KF888328 | N‘guéngué | Cameroon |
L. aubryi | ZFMK 87728 | KF888329 | Nkoelon | Cameroon |
L. aubryi | ZFMK 89560 | KF888330 | Big Massaka | Cameroon |
L. aubryi | ZFMK 89562 | KF888331 | Big Massaka | Cameroon |
L. spiritusnoctis | ZMB 79578 | KF888332 | near Banambala | Guinea |
L. spiritusnoctis | ZMB 79579 | KF888333 | near Gbanshue | Liberia |
L. spiritusnoctis | ZMB 79580 | KF888334 | Mt. Jideh | Liberia |
L. spiritusnoctis | ZMB 79581 | KF888335 | Sapo National Park | Liberia |
L. spiritusnoctis | ZMB 79582 | KF888336 | Sapo National Park | Liberia |
L. spiritusnoctis | ZMB 79583 | KF888337 | Sapo National Park | Liberia |
L. macrotis | ZMB 79584 | KF888338 | near Gpaole | Guinea |
L. macrotis | ZMB 79585 | KF888339 | near Yomou | Guinea |
L. macrotis | ZMB 79586 | KF888340 | Sapo National Park | Liberia |
L. macrotis | ZMB 79587 | KF888341 | Mt. Jideh | Liberia |
L. millsoni | ZFMK 87708 | KF888342 | Nkoelon | Cameroon |
We analyzed 454 and 522 base pairs (bp) of the mitochondrial 16S ribosomal RNA gene (
Acoustic data. Calls were either recorded by ourselves (various different recorders) and analyzed (44.1 kHz sample ratio, 16 bits resolution, FFT length = 256) with the software Soundruler 0.9.6 (
Molecular data. We analyzed 454 bp of the mitochondrial 16S ribosomal RNA gene for the L. macrotis / L. millsoni comparison and 522 bp for the L. spiritusnoctis / L. aubryi comparison. The uncorrected pairwise sequence divergence between L. aubryi (N = 6) and L. spiritusnoctis (N = 6) ranged from 5.74–6.56% (6.23 ± 0.22%; N = 36). The intraspecific variation in L. aubryi ranged from 0–2.12% (0.86 ± 0.94%; N = 15). The intraspecific variation in L. spiritusnoctis ranged from 0–0.62% (0.27 ± 0.23%; N = 15). The uncorrected pairwise sequence divergence between L. macrotis (N = 4) and L. millsoni (N = 1) ranged from 11.07–11.30% (mean ± sd: 11. 24 ± 0.12%; N = 4). The intraspecific variation in L. macrotis ranged from 0–0.22% (0.11 ± 0.12%; N = 6).
Acoustic data. For L. aubryi and L. spiritusnoctis we could analyze the “chuck” (
Oscillograms, audio spectrograms and power spectrograms of the “chuck” call of Leptopelis aubryi (ZFMK 89560) from Big Massaka, Cameroon (a) and Leptopelis spiritusnoctis from Taï National Park, Ivory Coast (b). This audio files are also available from the Tierstimmenarchiv at the Museum für Naturkunde, Berlin, through the following links: a) http://www.tierstimmenarchiv.de/recordings/Leptopelis_aubryi_DIG0174_01_short.mp3 (
Oscillograms, audio spectrograms and power spectrograms of the buzz calls of Leptopelis aubryi (ZFMK 89560) from Big Massaka, Cameroon (a) and of Leptopelis spiritusnoctis (two calls) from Taï National Park, Ivory Coast (b). This audio files are also available from the Tierstimmenarchiv at the Museum für Naturkunde, Berlin, through the following links: a) http://www.tierstimmenarchiv.de/recordings/Leptopelis_aubryi_DIG0174_03_short.mp3 (
Comparison of call characteristics of Leptopelis spiritusnoctis and calls assigned to L. aubryi (compare text). “Chucks” are interpreted as advertisement calls whereas “buzz” are regarded as territorial calls (compare
Species and call type | CD | minF | maxF | FR | DF | FF | sDF | eDF | CF | PC | PD | PI | Pps | Country | source |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
spiritusnoctis (chuck; N = 13) | 18.8 ± 4.2 | 2307.7 ± 46.3 | 3143.4 ± 80.5 | 835.5 ± 62.5 | 2726.4 ± 156.7 | 2726.4 ± 156.7 | 2786.1 ± 126.0 | 2660.2 ± 215.4 | (-)125.9 ± 119.8 | Ivory Coast | this paper | ||||
aubryi (chuck; N = 4) | 43.0 ± 8.0 | 1353.0 | 2019.0 | 1540.0 ± 321.0 | 2049.0 ± 461.0 | 162.0 ± 225.0 | 13.0 ± 2.0 | 281.0 ± 31.0 | Equatorial Guinea |
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aubryi (chuck; N = 22) | 10.0 ± 2.0 | 1512.3 ± 238.4 | 3771.2 ± 292.3 | 2259.1 ± 440.8 | 2984.6 ± 238.0 | 2984.6 ± 238.0 | 3004.2 ± 249.3 | 3009.8 ± 217.2 | 5.6 ± 159.8 | Cameroon | this paper | ||||
aubryi (chuck; N = 1) | 35.0 | 2547.0 | 3394.0 | 847.0 | 2842.0 | 2842.0 | 3015.0 | 173.0 | eastern Nigeria | A. Schiøtz | |||||
spiritusnoctis (buzz; N = 22) | 334.5 ± 122.5 | 2525.0 ± 114.0 | 3297.9 ± 86.5 | 773.0 ± 122.0 | 2996.9 ± 26.2 | 2996.9 ± 26.2 | 2799.5 ± 43.5 | 2998.9 ± 27.5 | 199.4 ± 50.6 | 15.2 ± 5.5 | 11.40 ± 3.43 | 12.69 ± 3.49 | 45.4 ± 1.1 | Ivory Coast | this paper |
aubryi (buzz; N = 3) | 51.0 – 105.0 | 2191.0 | 3562.0 | 1370.7 | 2906.3 | 2906.3 | 2719.0 | 2906.0 | 187.0 | 2.33 ± 0.58 | 3.97 ± 1.38 | 46.24 ± 2.22 | 0.03 ± 0.01 | Cameroon | this paper |
From L. macrotis we only know of one call type (
Oscillograms, audiospectrograms and power spectrograms of the advertisement call (“mmau”) of Leptopelis macrotis from Cavally Forest Reserve, Ivory Coast. This audio file is also available from the Tierstimmenarchiv at the Museum für Naturkunde, Berlin, through the following link http://www.tierstimmenarchiv.de/recordings/Leptopelis_macrotis_DIG0174_05_short.mp3 (
From L. millsoni we had no own recording available. The call of L. millsoni is described as a nasal “himp”, consisting of a single tonal long note (approximately 170 ms) with a high frequency range (
The overall morphological and presumed acoustic similarity between Leptopelis aubryi with L. spiritusnoctis and that of L. millsoni with L. macrotis (
Nevertheless, the Cross River in eastern Nigeria is not an all-or-nothing barrier, and a few Central African forest anurans indeed managed to occur further West reaching the Niger Delta or even beyond (e.g. Hymenochirus boettgeri, Amietophrynus camerunensis, Nectophryne afra, Conraua crassipes, Acanthixalus spinosus, Afrixalus paradorsalis;
Our molecular and acoustic data presented herein, clearly support the view that West and Central Africa comprise distinct anuran faunas, including the Leptopelis populations in question. The genetic distances between L. aubryi and L. spiritusnoctis in the studied 16S gene fragment (5.74–6.56%) and L. millsoni and L. macrotis (11.07–11.30%), respectively, by far exceed the values which are commonly assumed to indicate distinct species (3–5% in 16S; see
Taxonomic conclusions. Based on the molecular and acoustic data presented we conclude that synonymizing L. spiritusnoctis with L. aubryi was not justified and thus resurrect L. spiritusnoctis for the small forest-dwelling Leptopelis species in the Upper Guinean forest zone (see
The downgrading of L. macrotis as a subspecies of L. millsoni, as currently understood, was likewise erroneous. However, the situation is more complex. West and Central African populations clearly represent distinct species. Currently, we cannot decide to which species the name L. millsoni (type locality is the Niger delta, geographically a part of the western species assemblage) should be applied. Unfortunately, so far we do not have genetic samples from Nigeria. Thus, we do not know which species occurs in Nigeria and we cannot even exclude that southern Nigeria harbors taxa which are morphologically similar, but distinct on the basis of genetics and acoustics from those adjacent to the east and west (compare e.g.
We thank the various authorities from Cameroon, Ivory Coast, Guinea and Liberia for collection permits, and A. Schiøtz for making his call recordings available, through the sound library of the Cornell University. W. Böhme and D. Rödder (ZFMK) permitted tissue sampling from ZFMK vouchers. We thank Julia Barej for the permission to use her photos of life frogs. Jörn Köhler and Frank Glaw provided helpful critique.
Buzz call of Leptopelis aubryi (ZFMK 89560) from Big Massaka Cameroon
Data type: multimedia
Explanation note: This audio file is also available from the Tierstimmenarchiv at the Museum für Naturkunde, Berlin, through the following link: http://www.tierstimmenarchiv.de/recordings/Leptopelis_aubryi_DIG0174_03_short.mp3.
Chuck call of Leptopelis aubryi (ZFMK 89560) from Big Massaka, Cameroon
Data type: multimedia
Explanation note: This audio file is also available from the Tierstimmenarchiv at the Museum für Naturkunde, Berlin, through the following link: http://www.tierstimmenarchiv.de/recordings/Leptopelis_aubryi_DIG0174_01_short.mp3.
Advertisement call of Leptopelis macrotis from Cavally Forest Reserve, Ivory Coast
Data type: multimedia
Explanation note: This audio file is also available from the Tierstimmenarchiv at the Museum für Naturkunde, Berlin, through the following link: http://www.tierstimmenarchiv.de/recordings/Leptopelis_macrotis_DIG0174_05_short.mp3.
Two buzz calls of Leptopelis spiritusnoctis from Tai National Park, Ivory Coast
Data type: multimedia
Explanation note: This audio file is also available from the Tierstimmenarchiv at the Museum für Naturkunde, Berlin, through the following link: http://www.tierstimmenarchiv.de/recordings/Leptopelis_spiritusnoctis_DIG0174_04_short.mp3.
Chuck call of Leptopelis spiritusnoctis from Tai National Park, Ivory Coast
Data type: multimedia
Explanation note: This audio file is also available from the Tierstimmenarchiv at the Museum für Naturkunde, Berlin, through the following link: http://www.tierstimmenarchiv.de/recordings/Leptopelis_spiritusnoctis_DIG0174_02_short.mp3.