Research Article |
Corresponding author: David R. Vieites ( vieites@mncn.csic.es ) Academic editor: Angelica Crottini
© 2020 David R. Vieites, Sandra Nieto-Román, Marcos Peso Fernández, Javier H. Santos-Santos.
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:
Vieites DR, Nieto-Román S, Peso Fernández M, Santos-Santos JH (2020) Hidden in plain sight: a new frog species of the genus Blommersia from the oceanic island of Mayotte, Comoros archipelago. ZooKeys 994: 149-166. https://doi.org/10.3897/zookeys.994.57012
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The amphibian fauna of the western Indian ocean volcanic island of Mayotte is currently constituted by two species belonging to two genera of the anuran family Mantellidae: Blommersia transmarina and Boophis nauticus. These were recently described after intense fieldwork on the herpetofauna of the island. We here describe a third new species of frog from Mayotte, based on morphological and molecular data, that occurs in sympatry with the others and was utterly unnoticed until now. Genetic analyses of the16S rRNA gene, including all described and several undescribed species of the genus Blommersia from Madagascar and Mayotte, confirms that the new species is the sister species of Blommersia transmarina. Both species show apparent morphological differences as well as different life histories, ecology and genetics that confirm Blommersia nataliae sp. nov. as a new species. We propose an IUCN Red List status of Critically Endangered for B. nataliae sp. nov.
Amphibia, Anura, Blommersia nataliae sp. nov., Comoros archipelago, Mantellidae, Mayotte
The Mantellidae is a hyperdiverse family of frogs mostly endemic to Madagascar (
The genus Blommersia comprises eleven described frog species and constitutes a monophyletic radiation with at least six undescribed, genetically divergent lineages that may warrant species status, suggesting that the genus is likely more diverse than currently known (
In this context, the known species present on Mayotte offer an exciting opportunity to study the morphological and life history evolution of species that have evolved in isolation without the presence of other congeners for the last 5 or 6 million years. Blommersia transmarina evolved into a bigger body size than any other Blommersia from Madagascar, likely having undergone a process of moderate gigantism compared to the rest of Blommersia species (
Individuals of Blommersia transmarina were located by tracking their calls during regular searches to localize calling males, as well as by visiting different types of water bodies and forests in Mayotte. Although this species calls during the night, the newly discovered one is much more secretive in terms of calling as no calls were ever heard in breeding places during reproduction. Individuals of the new species were found first on the forest ground mixed with B. transmarina, and later we discovered their breeding places where reproduction could be observed.
Individuals were euthanized using chlorobutanol, fixed in 90% ethanol, and preserved in 70% ethanol. Tissue samples were taken in the field and preserved in 99% ethanol or RNAlater for molecular studies. Preserved specimens are deposited at the Museo Nacional de Ciencias Naturales (
Morphological measurements were taken by D. Vieites, using a Vernier caliper, to the nearest 0.1 mm (Table
Measurements of Blommersia nataliae sp. nov. and B. transmarina for comparison. See methods for abbreviations. The holotype of B. nataliae sp. nov. is shown in bold letters.
Species | Locality | Field number |
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Sex | SVL | HW | HL | TD | ED | END | NSD | NND | FORL | HAL | HIL | FOTL | FOL | TIBL | FGL | FGW | FGD | RHL |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
B. nataliae sp. nov. | Mont M’Sapere | DRV6854 | MNCN50447 | F | 19.6 | 7.4 | 7.2 | 1.7 | 2.9 | 2 | 1.6 | 2.7 | 14 | 5.5 | 36 | 16 | 10 | 11 | 3 | |||
Mont M’Sapere | DRV6855 | MNCN50448 | F | 19.8 | 7.7 | 8.1 | 1.9 | 2.9 | 2 | 1.7 | 2.9 | 15 | 6 | 37 | 16 | 11 | 11 | 3 | ||||
Mont M’Sapere | DRV6869 | MNCN50449 | F | 20.0 | 8.1 | 8.6 | 1.6 | 2.6 | 2 | 2 | 2.8 | 14 | 6 | 37 | 16 | 10 | 12 | 4 | ||||
Mont M’Sapere | DRV6868 | MNCN50450 | F | 22.0 | 7 | 8.8 | 1.4 | 2.9 | 1.8 | 1.6 | 2.8 | 14 | 5.8 | 38 | 17 | 11 | 12 | 3 | ||||
Mont M’Sapere | DRV6808 | MNCN50451 | F | 23.0 | 7.3 | 8.7 | 1.5 | 2.4 | 2.1 | 1.8 | 2.9 | 15 | 6.2 | 38 | 18 | 12 | 12 | 4 | ||||
Mont M’Sapere | DRV6862 | MNCN50452 | M | 17.9 | 5.9 | 7 | 1.4 | 2.5 | 1.7 | 1.3 | 2.6 | 11 | 5 | 33 | 14 | 8.8 | 10 | 2 | 1.2 | 2.6 | 5 | |
Mont M’Sapere | DRV6857 | MNCN50453 | M | 18.4 | 6.9 | 7.5 | 1.6 | 2.6 | 1.9 | 1.4 | 2.4 | 13 | 5.4 | 31 | 14 | 8.5 | 9.9 | 2.4 | 1.3 | 3 | ||
Mont M’Sapere | DRV6861 | MNCN50454 | M | 18.4 | 7.3 | 7.8 | 1.7 | 2.3 | 2 | 1.6 | 2.5 | 14 | 5.6 | 35 | 16 | 10 | 11 | 2.6 | 1.2 | 5 | ||
Mont M’Sapere | DRV6859 | MNCN50455 | M | 18.5 | 6.5 | 7.1 | 1.5 | 2.2 | 1.8 | 1.2 | 2.2 | 14 | 5.7 | 35 | 16 | 10 | 11 | 2 | 1.1 | 5 | ||
Mont M’Sapere | DRV6867 | MNCN50456 | M | 18.6 | 6.3 | 7.5 | 1.5 | 2.8 | 2 | 1.4 | 2.4 | 14 | 5.4 | 33 | 15 | 9.7 | 10 | 3 | 1.8 | 2.3 | 3 | |
Mont M’Sapere | DRV6863 | MNCN50457 | M | 19.0 | 6.6 | 7.7 | 1.9 | 2.7 | 2.2 | 1.5 | 2.4 | 14 | 5.8 | 38 | 17 | 11 | 11 | 2.6 | 1.1 | 5 | ||
Mont M’Sapere | DRV6860 | MNCN50458 | M | 20.5 | 6.8 | 7.4 | 1.5 | 2.9 | 1.9 | 1.5 | 2.6 | 13 | 5.5 | 37 | 17 | 9.9 | 12 | 2.7 | 1.1 | 2.7 | 4 | |
B. transmarina | Mont Choungi | DRV6835 | MNCN50430 | F | 29.3 | 11 | 12 | 2.4 | 4 | 2.8 | 1.9 | 3.7 | 21 | 8.8 | 61 | 26 | 17 | 18 | 7 | |||
Mont Combani | DRV6848 | MNCN50431 | F | 26.0 | 9.1 | 10 | 2.4 | 3.5 | 2.7 | 1.9 | 3.3 | 20 | 7.8 | 52 | 22 | 14 | 16 | 7 | ||||
Mont Combani | DRV6805 | MNCN50432 | F | 29.1 | 10 | 12 | 2.1 | 4.1 | 2.5 | 2 | 3.2 | 22 | 8.9 | 56 | 25 | 17 | 17 | 7 | ||||
Mont M’Sapere | DRV6813 | MNCN50433 | F | 30.4 | 11 | 13 | 2.8 | 4.3 | 2.9 | 2 | 3.6 | 23 | 9.9 | 60 | 26 | 18 | 19 | 7 | ||||
Mont Bénara | DRV6831 | MNCN50434 | M | 25.5 | 9.8 | 9 | 2.6 | 3.6 | 2.5 | 1.8 | 3 | 21 | 8.2 | 48 | 22 | 14 | 15 | 4.6 | 1.7 | 7 | ||
Mont Bénara | DRV6832 | MNCN50435 | M | 25.5 | 8.5 | 9.8 | 2.4 | 3.1 | 2.5 | 1.6 | 2.9 | 20 | 8.6 | 50.9 | 22 | 14 | 15 | 4.5 | 1.6 | 1.5 | 7 | |
Mont Bénara | DRV6833 | MNCN50436 | M | 27.5 | 9.1 | 10 | 2.1 | 3.4 | 2.7 | 1.8 | 3 | 19 | 8.1 | 53 | 23 | 15 | 16 | 4.9 | 1.7 | 7 | ||
Mont Bénara | DRV6841 | MNCN50437 | M | 24.6 | 8.7 | 11 | 2.3 | 3.7 | 2.5 | 2.2 | 3.1 | 20 | 8.1 | 49 | 21 | 15 | 15 | 4.8 | 1.6 | 1 | 7 | |
Mont Bénara | DRV6838 | MNCN50438 | M | 25.5 | 8.8 | 9.3 | 2.8 | 3.2 | 2.6 | 1.9 | 3 | 17 | 7.5 | 49 | 23 | 15 | 14 | 5 | 1.6 | 7 | ||
Mont Bénara | DRV6836 | MNCN50439 | M | 26.0 | 9.3 | 9.9 | 2.5 | 3.6 | 2.6 | 1.7 | 3 | 17 | 7.6 | 45 | 22 | 14 | 15 | 5.6 | 1.7 | 1.6 | 7 | |
Mont Combani | DRV6852 | MNCN50440 | M | 24.5 | 8.4 | 9.7 | 2.1 | 3.4 | 2.2 | 1.4 | 3 | 16 | 6.4 | 47 | 21 | 13 | 15 | 3.8 | 1.5 | 7 | ||
Mont Combani | DRV6819 | MNCN50441 | M | 25.0 | 8.4 | 10 | 2.7 | 3.4 | 2.2 | 1.7 | 3.2 | 18 | 7.4 | 44 | 20 | 13 | 14 | 4.4 | 2 | 7 | ||
Mont Combani | DRV6818 | MNCN50442 | M | 26.0 | 8.8 | 9.4 | 2.4 | 3.5 | 2.8 | 1.7 | 3 | 19 | 7.8 | 49 | 24 | 14 | 15 | 4.6 | 1.7 | 7 | ||
Mont Combani | DRV6806 | MNCN50443 | M | 26.5 | 8.7 | 9.2 | 2.2 | 3.7 | 2.6 | 1.9 | 3.3 | 15 | 7.8 | 51 | 23 | 15 | 15 | 5.7 | 1.8 | 1 | 7 | |
Mont Combani | DRV6849 | MNCN50444 | M | 27.0 | 9.4 | 12 | 2.4 | 3.9 | 2.5 | 2 | 3.6 | 18 | 8.6 | 46 | 23 | 16 | 15 | 4.5 | 1.6 | 1.6 | 7 | |
Mont Combani | DRV6850 | MNCN50445 | M | 27.0 | 9.4 | 10 | 2.4 | 3.4 | 2.5 | 1.9 | 3.4 | 18 | 8.3 | 44 | 24 | 16 | 16 | 4.8 | 1.6 | 7 | ||
Mont M’Sapere | DRV6807 | MNCN50446 | M | 29.0 | 9.7 | 11 | 2.4 | 3.9 | 2.5 | 2.2 | 3.5 | 20 | 8.5 | 50 | 22 | 14 | 16 | 5.3 | 2 | 1.1 | 7 |
DNA was extracted, and a fragment of 489bp of the mitochondrial 16S rRNA gene was amplified using primers 16S-AL and 16S-BH (see
For phylogenetic analysis, we assembled a dataset of sequences for all Blommersia species available in GenBank that cover all described and several undescribed candidate species (
The recovered phylogenetic relationships between Blommersia species are shown in Fig.
The two Blommersia lineages from Mayotte differ from each other, and from other Blommersia species, by several morphological traits: (1) the shape, position, and size of the femoral glands (Figs
Following an integrative taxonomic approach, morphological, genetic, life history, and biogeographic data support recognizing the newly discovered lineage on Mayotte as a new species under the evolutionary and biological species criteria. We therefore scientifically describe and name it here, providing a detailed description of adult morphology, intraspecific variation, and the first data on its life history and ecology.
An adult male, left thigh muscle removed for genetic analyses. Original field number: “DRV6867, David R. Vieites collection”. Museo Nacional de Ciencias Naturales catalog number: MNCN50456. Collected in a degraded forest with giant bamboo, in forest leaf litter at the Mont M’Sapere, island of Mayotte (French Overseas Department), Comoros archipelago, -12.7656°S, 45.1852°E 500 m a.s.l. the 25th November 2012 by D. Vieites and M. Peso Fernández.
Females DRV6808 (MNCN50451), DRV6854 (MNCN50447), DRV6855 (MNCN50448), DRV6868 (MNCN50450), DRV6869 (MNCN50449); males DRV6857 (MNCN50453), DRV6859 (MNCN50455), DRV6860 (MNCN50458), DRV6861 (MNCN50454), DRV6862 (MNCN50452), DRV6863 (MNCN50457), collected at the type locality at the Mont M’Sapere in 2012 by D. Vieites and M. Peso Fernández.
Noun in the genitive case. D. Vieites and S. Nieto dedicate this species to their daughter Natalia Vieites Nieto, who has a birthmark resembling the beautiful conspicuous round moon-like brown spot characteristic of the species.
Assigned to the genus Blommersia in the family Mantellidae and subfamily Mantellinae by a combination of (1) presence of femoral glands and absence of nuptial pads in males, (2) presence of intercalary elements between ultimate and penultimate phalanges of fingers and toes (verified by external examination and microCT scanning), (3) presence of a single subgular vocal sac in males, (4) small size (adult SVL < 30 mm), and (5) molecular data.
Within the genus Blommersia, B. nataliae sp. nov. is characterized by the following unique suite of morphological characters: (1) small adult body size (SVL 18–23 mm), (2) round femoral glands that are distantly separated in males, (3) inconspicuous vomerine teeth, (4) ovoid tongue, (5) tibiotarsal articulation reaching between the eye and the nostril when adpressed along the body. Furthermore, the new species is differentiated from all other species of Blommersia by a significant molecular genetic differentiation (≥ 4.3% uncorrected pairwise-distance in 16S).
Blommersia nataliae sp. nov. can be distinguished from all other described Blommersia species except B. wittei and B. transmarina by the presence of vomerine teeth (vs. absence) and having separated metatarsalia (vs. unseparated).
Blommersia nataliae sp. nov. can be distinguished from its syntopic sister taxon B. transmarina by its rounded, distantly separated femoral glands (versus oblong, less separated glands; Figs
Scatterplot of relative femoral gland length (FGL/SVL ratio) and the relative distance between the inner edges of the femoral glands (FGD/SVL) in the two new species from Mayotte and their sister taxon Blommersia wittei from Madagascar. Measurements are based on Table
Description of the holotype (Fig.
Coloration of the Holotype (Fig.
The measurements of the holotype and paratypes are provided in Table
The species was found on the ground and in its breeding places: cut bamboo trunks filled with water (Fig.
Initially found on the slopes of Mont M’Sapere only where there is still forest present and giant bamboos, between 235 m a.s.l. and 409 m a.s.l. (2012, 2014, and 2019). In the 2014 expedition, we also found the new species at Mont Bénara (12.8712°S, 45.15614°E, 317 m a.s.l.) in a forested place with fewer bamboo stands available, but few specimens. It is possible that the species breeds in other microhabitats (e.g., tree holes) as in the places where it occurs at Mont Bénara there are not many bamboo stands available, but this hypothesis needs to be confirmed. After several trips and visits around the whole entire main island of Mayotte and surrounding islets, with very intense fieldwork, we have not found it anywhere else, and the habitat appears to be degraded for the species.
The new species is only known from two localities and seems restricted to mountain areas where the forest is still present with giant bamboo stands. The area of occupancy is estimated to be less than 10 km2 from the elevation range where it was observed (235 to 409 m a.sl.) and the remaining forest available at the Reserve Forestière de Majimbini (Mont M’Sapere) and the Reserve Forèstiere du Mont Benara (
For a long time, the Mantellidae was considered an endemic family of frogs to Madagascar, where it is highly diverse, with more than 220 species described so far. The presence of two amphibian mantellid species in Mayotte, a Boophis and a former Mantidactylus (now Blommersia), was known for a relatively long time (
Oceanic islands offer unique opportunities to study the evolution of ecological and morphological characters as new colonizers have few competitors and empty niches to exploit. In many cases, this leads to island radiations that show a wide range of ecological and morphological adaptations in small territories (e.g.,
From the external morphological point of view, and comparing with their sister taxon Blommersia wittei from Madagascar (Table
The different events of ecological and morphological release in Comoran species lead to their morphological divergence with an adult morphological pattern in B. nataliae sp. nov. that resembles other Blommersia from Madagascar that evolved towards miniaturization, whereas B. transmarina occupies the morphological space of other larger genera present in Madagascar (e.g., Mantidactylus or Gephyromantis). This offers a unique opportunity to explore the mechanisms of their morphological evolution in isolation.
In this study, we have followed an integrative taxonomic approach by incorporating morphological, genetic, and life history data, which supports the species status of this new taxon. Despite the effort to register mating calls from the new species, we never heard it in the field or in captivity, even when observing reproduction in front of us. This contrasts with B. transmarina, in which males are very active, calling at night everywhere, even at close distance. Hence, we could not include calls in the analyses, and the call of this species still needs to be determined.
The observed genetic divergence between Mayotte’s two Blommersia species is above the values observed between other mantellid sister species (
Two other significant threats can also affect the conservation of the Comoran herpetofauna apart from habitat degradation. Warming of the western Indian Ocean is becoming more intense, with a higher likelihood of extreme climatic events (
In contrast, B. transmarina is present in the typical Blommersia habitats: swamps, ponds, little brooks, roadside channels, and even water deposits, fountains, or buckets, occurring in both forest habitats as well as in very degraded areas. The breeding season can extend throughout the year as long as there is rain, as we observed clutches in spring, fall, and winter, although the main reproductive activity coincides with the rainy season. In captivity, they can reproduce all year round. The males of B. transmarina are very active in breeding grounds, calling from leaves, shrubs, low branches of trees or rocks, sometimes with frenetic activity. They even were even found calling in fountains of hotels during the night, so the potential impact of climate change may be less intense for this species. The introduction of the chytrid fungus, which so far has not been reported in Mayotte, could easily drive the three amphibian species known on the island to extinction as well.
We are grateful to Nina Bernard, Isaac Pozo and Thijs van den Burg for their help in the field, and to M. Vences and F. Glaw for previous discussions about the origin and diversification of these frogs. We thank the Guillaume Decalf and the DEAL of Mayotte for authorizing our research at Mayotte. We want to thank Frank Glaw, Mark Scherz and Franco Andreone for reviewing this manuscript. The Spanish Ministry of Science and Innovation supported this work with grants CGL2009-10198, CGL2013-40924-P, and CGL2017-89898-R (AEI/FEDER, UE) to DRV.
Data descriptor for Blommmersia nataliae sp. nov.
Data type: COL