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Systematics of Treefrogs of the Hypsiboas Calcaratus and Hypsiboas Fasciatus Species Complex (Anura, Hylidae) With the Description of Four New Species

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Systematics of Treefrogs of the Hypsiboas Calcaratus and Hypsiboas Fasciatus Species Complex (Anura, Hylidae) With the Description of Four New Species

Marcel A Caminer et al. Zookeys.

Abstract

We review the systematics of the Hypsiboas calcaratus species complex, a group of widely distributed Amazonian hylid frogs. A comprehensive analysis of genetic, morphological, and bioacoustic datasets uncovered the existence of eleven candidate species, six of which are confirmed. Two of them correspond to Hypsiboas fasciatus and Hypsiboas calcaratus and the remaining four are new species that we describe here. Hypsiboas fasciatus sensu stricto has a geographic range restricted to the eastern Andean foothills of southern Ecuador while Hypsiboas calcaratus sensu stricto has a wide distribution in the Amazon basin. Hypsiboas almendarizae sp. n. occurs at elevations between 500 and 1950 m in central and northern Ecuador; the other new species (H. maculateralis sp. n., H. alfaroi sp. n., and H. tetete sp. n.) occur at elevations below 500 m in Amazonian Ecuador and Peru. The new species differ from H. calcaratus and H. fasciatus in morphology, advertisement calls, and mitochondrial and nuclear DNA sequences. Five candidate species from the Guianan region, Peru, and Bolivia are left as unconfirmed. Examination of the type material of Hyla steinbachi, from Bolivia, shows that it is not conspecific with H. fasciatus and thus is removed from its synonymy.

Keywords: Advertisement call; conservation status; cryptic diversity; morphology; new species.

Figures

Figure 1.
Figure 1.
Maximum likelihood phylogram depicting relationships within Hypsiboas. The phylogram was derived from analysis of 2400 bp of mitochondrial DNA (gene fragments 12S, 16S, COI). Museum catalog number and locality are shown for each sample. Bootstrap values are shown above the branches and Bayesian posterior probabilities are shown below; missing values indicate values below 50 (bootstrap) or 0.5 (posterior probability). Outgroup species (Hypsiboas lanciformis, Hypsiboas pellucens andHypsiboas rubracylus) are not shown. Abbreviations are: ARG Argentina, BO Bolivia, EC Ecuador, FG French Guiana, GUY Guyana, PE Peru, SU Suriname.
Figure 1.
Figure 1.
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Figure 2.
Figure 2.
Maximum likelihood phylogram depicting relationships within Hypsiboas. The phylogram was derived from analysis of 1272 bp of nuclear DNA (gene fragments RAG-1 and POMC). Museum catalog number and locality are shown for each sample. Bootstrap values are shown above the branches and Bayesian posterior probabilities are shown below; values below 50 (bootstrap) or 0.5 (posterior probability) are not shown. Colors refer to clades identified using mtDNA (see Figure 1).
Figure 3.
Figure 3.
Dorsolateral (top), ventral (left), and dorsal (right) views of the holotype of Hypsiboas fasciatus (BMNH 58.4.25.22).
Figure 4.
Figure 4.
Dorsolateral views of adult females of A Hypsiboas fasciatus, QCAZ 48611, SVL = 51.79 mm B Hypsiboas almendarizae, QCAZ 32638, SVL = 51.26 mm C Hypsiboas calcaratus, QCAZ 24282, SVL = 51.26 mm D Hypsiboas maculateralis, QCAZ 43825, SVL = 55.31 mm E Hypsiboas alfaroi, QCAZ 43252, SVL = 45.37 mm.
Figure 5.
Figure 5.
Adult Hypsiboas fasciatus showing variation in dorsal and ventral coloration of preserved specimens. From left to right, first and second rows: QCAZ 24866, 26497, 41575 (females); third and fourth rows: QCAZ 18271, 41488, 41576, 48584 (males). See Appendix for locality data. All specimens are shown at the same scale.
Figure 6.
Figure 6.
Adult Hypsiboas almendarizae showing variation in dorsal and ventral coloration of preserved specimens. From left to right, first and second rows: QCAZ 32638, 32645 (females), 24392 (male); third and fourth rows: QCAZ 39647, 39650, 24394 (males). See Appendix for locality data. All specimens are shown at the same scale.
Figure 7.
Figure 7.
Principal components from analysis of six size-corrected morphological variables for A 34 females and B 136 males of Hypsiboas. See Table 8 for character loadings on each component.
Figure 8.
Figure 8.
Dorsolateral views of adult males of A Hypsiboas fasciatus, QCAZ 48584, SVL = 33.77 mm B Hypsiboas almendarizae, QCAZ 39649, SVL = 36.54 mm C Hypsiboas calcaratus, QCAZ 43256, SVL = 40.07 mm D Hypsiboas maculateralis, QCAZ 40082, SVL = 36.16 mm E Hypsiboas alfaroi, QCAZ 43260, SVL = 30.35 mm F Hypsiboas tetete, QCAZ 40081, SVL = 31.15 mm.
Figure 9.
Figure 9.
Adult Hypsiboas calcaratus showing variation in dorsal and ventral coloration of preserved specimens. From left to right, first and second rows: QCAZ 44422, 44530 (females), 14957 (male); third and fourth rows: QCAZ 43259, 40085, 43256 (males). See Appendix for locality data. All specimens are shown at the same scale.
Figure 10.
Figure 10.
Holotype of Hyla leptoscelis (BM 1947.2.23.10). Above: dorsolateral view; below: ventral (left) and dorsal (right) views.
Figure 11.
Figure 11.
Syntype of Hyla steinbachi (BM 1947.2.13.61). Above: dorsal (left) and ventral (right) views; below: lateral view of head and ventral view of left hand.
Figure 12.
Figure 12.
Calls of the Hypsiboas calcaratus species complex. A–B Hypsiboas fasciatus (QCAZ 48585) from La Pradera, Provincia Morona Santiago C–D Hypsiboas almendarizae (QCAZ 39650) from Limón, Provincia Morona Santiago E–F Hypsiboas calcaratus (QCAZ 40085) from Tena, Provincia Napo. A, C, E are oscilograms and B, D, F spectrograms.
Figure 13.
Figure 13.
Calls of the Hypsiboas calcaratus species complex. A–B Hypsiboas maculateralis (QCAZ 40082) from Comunidad Santa Rosa, Provincia Napo C–D Hypsiboas alfaroi (QCAZ 43260) from Estación Científica Yasuní PUCE, Provincia Orellana E–H Hypsiboas tetete (QCAZ 40081) from Comunidad Santa Rosa, Provincia Napo. A, C, E, G are oscilograms and B, D, F, H spectrograms.
Figure 14.
Figure 14.
Variation in color of the iris of A Hypsiboas fasciatus (QCAZ 47051), and B Hypsiboas almendarizae (QCAZ 42055). Calcar in C Hypsiboas almendarizae (QCAZ 39639) and D Hypsiboas calcaratus (QCAZ 40055). Note that the calcar in Hypsiboas almendarizae is large and conical while in Hypsiboas calcaratus is large and triangular. Dorsolateral views of the holotypes of E Hypsiboas almendarizae, adult male (QCAZ 39650), SVL = 36.72 mm F Hypsiboas maculateralis, adult male (QCAZ 40082), SVL = 36.16 mm; and G Hypsiboas tetete, adult male (QCAZ 40081), SVL = 31.15 mm.
Figure 15.
Figure 15.
Distribution of species of the Hypsiboas calcaratus complex. Localities are based on museum specimens from Museo de Historia Natural Gustavo Orcés of Escuela Politécnica Nacional, Museo de Zoología of Pontificia Universidad Católica del Ecuador, Natural History Museum University of Kansas, and Smithsonian Institution National Museum of Natural History.
Figure 16.
Figure 16.
Adult Hypsiboas maculateralis showing variation in dorsal and ventral coloration of preserved specimens. From left to right, first and second rows: QCAZ 43825, 44531, 44651, 28004, 28401 (females); third and fourth rows: QCAZ 40082 (holotype), 43897, 44020–21, 44184 (males). See Appendix for locality data. All specimens are shown at the same scale.
Figure 17.
Figure 17.
Distribution of Hypsiboas calcaratus and Hypsiboas maculateralis. Localities are based on museum specimens from Museo de Historia Natural Gustavo Orcés of Escuela Politécnica Nacional, Museo de Zoología of Pontificia Universidad Católica del Ecuador, Natural History Museum University of Kansas, and Smithsonian Institution National Museum of Natural History.
Figure 18.
Figure 18.
Adult Hypsiboas alfaroi showing variation in dorsal and ventral coloration of preserved specimens. From left to right, first and second rows: QCAZ 28272, 28398, 44180 (females); third and fourth rows: QCAZ 43262 (holotype), 43263, 43826 (males). See Appendix for locality data. All specimens are shown at the same scale.
Figure 19.
Figure 19.
Adult Hypsiboas tetete showing variation in dorsal and ventral coloration of preserved specimens. From left to right, first and second rows: QCAZ 48095–96 (females), 40060 (male); third and fourth rows: QCAZ 40079, 40081 (holotype), 48094 (males). See Appendix for locality data. All specimens are shown at the same scale.
Figure 20.
Figure 20.
Axes I and II from Principal Components Analysis based on five acoustic variables from the advertisement calls of Hypsiboas fasciatus (5 males), Hypsiboas almendarizae (5), Hypsiboas calcaratus (7), Hypsiboas maculateralis (1), Hypsiboas alfaroi (4), and Hypsiboas tetete (4). See Table 9 for character loadings on each component.

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