Zootaxa 3753 (5): 483–493 www.mapress.com /zootaxa / Copyright © 2014 Magnolia Press
Article
ISSN 1175-5326 (print edition)
ZOOTAXA
ISSN 1175-5334 (online edition)
http://dx.doi.org/10.11646/zootaxa.3753.5.6 http://zoobank.org/urn:lsid:zoobank.org:pub:93D3FEB4-3C66-4518-AA4A-67F2B091F46A
A new species of Choerophryne (Anura, Microhylidae) from the central cordillera of Papua New Guinea AMY IANNELLA1,2, STEPHEN RICHARDS1 & PAUL OLIVER3,4 1
South Australian Museum, Adelaide 5000, Australia School of Earth and Environmental Sciences, University of Adelaide, Adelaide, South Australia 5000, Australia 3 Department of Zoology, University of Melbourne, Melbourne, Victoria 3000, Australia 4 Museum Victoria, Melbourne, Victoria 3001, Australia 2
Abstract We describe a new species of very small microhylid frog in the genus Choerophryne from the upper Strickland River area, Western and Southern Highlands Provinces, Papua New Guinea. Choerophryne gracilirostris sp. nov. can be distinguished from congeners by the following combination of characters: small size (SUL 13.5–14.7 mm), moderately long and narrow snout, first finger without expanded disk and advertisement call consisting of 3–5 distinctly pulsed notes repeated in long sequences. Males in the type series were calling from within leaf litter in primary hill rainforest (213–1368 m a.s.l.). The new species is the third Choerophryne known from the southern side of New Guinea’s central cordillera. Measurements of a juvenile specimen (rare because most Choerophryne collected are calling males) demonstrate that the distinctive rostral projection of this genus exhibits pronounced positive allometry. Key words: frog, miniaturisation, Muller Range, rostral projection, systematics
Introduction Microhylids are the most species-rich radiation of frogs in New Guinea. Over 250 species are currently recognised, and this number is rapidly increasing (AmphibiaWeb 2013; Kraus and Allison 2009a; Papuan Herpetofauna 2013). Although Melanesian microhylids (all in the subfamily Asterophryinae) remain poorly studied they have attracted interest for the apparently repeated evolution of parental care of their direct-developing eggs (Bickford 2004; Köhler and Günther 2008). The existence of numerous lineages (many of them recently discovered) that have independently approached minimum size thresholds for terrestrial vertebrates has also attracted recent attention (Kraus 2010, 2011; Rittmeyer et al. 2012). The newly discovered genus Paedophryne is the most miniaturised lineage of Melanesian microhylids (and possibly of tetrapods (Kraus 2010, 2011; Rittmeyer et al. 2012)), but a number of other Melanesian microhylid genera also contain species with very small body sizes (e.g Kraus and Allison 2009a; Richards and Iskandar 2000; Kraus 2011). Perhaps the most notable of these is Choerophryne, a genus of nine recognised species of small to very small size (11.5–23.2 mm SVL) characterised by a unique extension of the nasal bones and the alary processes of the premaxillae, giving them a distinctively elongate snout. Despite this unique snout morphology a suite of morphological and molecular datasets indicates that Choerophryne is related to Albericus, a widespread genus of small to miniature blunt-snouted, largely arboreal microhylid frogs (Köhler and Günther 2008; Kraus and Allison 2001). Most recognised Choerophryne species (seven of nine) occur on the ranges and lowlands of the northern half of New Guinea and immediately adjacent islands, from Japen Island in the west to the Adelbert Mountains in the east (Günther 2008; Kraus and Allison 2001). Although a few species are widespread (Choerophryne rostellifer, C. proboscidea), most are currently known from a small number of localities, often at moderately high altitudes (>1000 m a.s.l.) in mountain ranges such as the Bewani and Torricelli Mountains (C. longirostris) or on the island of Japen (C. amomani) (Günther 2008; Kraus and Allison 2001) Accepted by M. Vences: 28 Nov. 2013; published: 9 Jan. 2014
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Choerophryne has only recently been documented from south of the central cordillera, with two very small species (IV>II>I, finger I less than half length of II, fingers II–IV with distinctly expanded discs up to 1.3 times width of penultimate phalanx, finger I without disk and with only faint circum-marginal groove; subarticular tubercles and webbing absent. Legs of moderate length (TL/SUL 0.40). Toes moderately long and wide, relative lengths IV>III>V>II>I, toe I approximately half length of II, all toes except I with terminal discs up to 1.4 times width of penultimate phalanx and with circum-marginal grooves; metatarsal tubercles and webbing absent. Disks on toes wider than those on fingers (F3/T4 0.78, Fig. 1).
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FIGURE 1. A) hand; and B) foot; of Choerophryne gracilirostris sp. nov. holotype (SAMA R67520) in the ventral aspect.
In preservative, ground colour of dorsum medium brown with dense dark-brown maculations, slightly denser anteriorly than posteriorly; dorsum dominated by a longitudinally oriented dark-brown hourglass mark, defined laterally by a pair of pale-tan dorso-lateral triangles extending from dorsal edge of the tympanum to the groin with medial tips approaching mid-dorsum, these pale-tan triangular patches with prominent but weakly defined darkbrown edging. Inguinal region with a pair of indistinct dark-brown lumbar ocelli with very small, distinct, pale cream medial spots. Vent bordered laterally and dorsally by an arc of dark-brown pigment. Exposed dorsal and lateral surfaces of limbs pale tan, extensively flecked and blotched with various shades of darker brown; darker pigmentation on limbs tending not to form distinct patterns, with the exception of some moderately distinct very dark-brown transverse bands at the midpoint of thigh, tibia and ankle. Dorsal surface of hands and feet pale buff with extensive pale-brown flecking. Venter pale buff with fine tan maculations coalescing on the throat, becoming scattered posteriorly and less dense around the vent and thighs, giving the throat an overall darker appearance than the belly and thighs; ventral surfaces of limbs buff, almost translucent, with scattered pale-tan flecks, palmar surfaces unpigmented; plantar surfaces largely unpigmented with light-tan speckling. Variation. Summary measurements for the type series are given in Table 1. The paratypes are of similar dimensions to the holotype, although all are slightly larger (SUL 13.7–14.7 mm vs. 13.5 mm). All specimens have a dorsal colouration including a longitudinally oriented dark-brown hourglass and paler-brown triangular lateral markings, and a pale-buff venter with extensive light-brown speckling. The paratypes have slightly paler dorsal colouration than the holotype (particularly SAMA R67519 and SAMA R67517); most also differ in having a distinct thin grey dorsal stripe extending from snout tip to urostyle tip (except SAMA R67518). The tympanic annulus is indistinct in all specimens, although a faint anterio-ventral ridge is sometimes apparent. A distinct palebuff medial stripe extends the full length of the venter on paratypes SAMA R67517 and SAMA R67514. The slope of the loreal region varies slightly among specimens, from slightly concave to nearly flat. Tuberculation in all paratypes is minimal and generally restricted to the flanks, a few low tubercles antero-lateral to the eyes are apparent in some specimens.
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TABLE 1. Summary of measurements (mm) for Choerophryne gracilirostris sp. nov. Reg#
R67520
PARATYPE PARATYPE PARATYPE PARATYPE PARATYPE PARATYPE R67515 R64986 R67516 R67517 R67519 R67514 R67518
Sex
Male
Male
Male
Male
Male
Male
Male
Juvenile
SUL
13.5
14.0
14.4
13.7
13.7
14.7
13.9
8.2
TL
5.4
5.5
5.3
5.4
5.2
5.6
5.4
3.3
F1D
0.2
0.2
0.2
0.3
0.3
0.2
0.3
0.1
F3D
0.5
0.5
0.4
0.4
0.5
0.5
0.5
0.2
T1D
0.4
0.4
0.4
0.3
0.4
0.4
0.4
0.1
T4D
0.6
0.5
0.6
0.8
0.7
0.8
0.8
0.4
HL
4.6
5.0
4.9
5.1
4.8
5.3
4.9
2.9
HW
4.7
5.1
5.3
5.0
4.6
5.3
4.8
3.1
SL
3.1
3.6
3.2
3.2
3.0
3.1
3.1
1.7
ED
1.3
1.4
1.5
1.5
1.5
1.5
1.6
1.1
OHG
1.2
1.1
1.1
1.0
0.9
0.9
1.0
0.5
END
2.1
3.2
2.2
2.0
1.9
2.2
1.9
1.1
IND
0.8
0.8
0.8
0.8
0.8
0.8
0.8
0.6
HOLOTYPE
The juvenile specimen (SAMA R67515) has the same dorsal and lateral colour pattern as adults, but the venter is much paler and almost entirely lacks flecks of light-brown pigmentation. The snout of the juvenile is also proportionally shorter than those of mature specimens, (SL/SUL 0.20 vs. an average of 0.23) while the eye diameter is proportionally larger (ED/SUL 0.13). Tibia length, head width and internarial distance are also relatively larger in the juvenile specimen. These data suggest that the elongated snout of this species undergoes positive allometric growth. Appearance in life. Photographs in life (Figure 2) of three specimens (SAMA R67516, R67519, R67520) taken at night, show a greater degree of contrast between light and dark brown dorsal and ventral areas than shown in preservative. The dorsal hourglass marking shows greater tonal variation than in preservative, sometimes including reddish-brown patches within the darker areas. Venter tinged grey on the throat grading to pink on the belly, with extensive fine reddish-brown maculations and scattered large pale grey-blue flecks (Figure 3), grey medial stripe more clearly visible than in preservative. Iris black with extensive small bronze flecks, pupil horizontal, encircled by a thin reddish-orange ring. Dorsal surfaces of torso and legs with numerous small tubercles of varying size that are less apparent in preservative. Advertisement call. Three full call sequences produced by SAMA R67520 at an air temperature of 25.5oC were recorded on 29 March 2008....... Calls are groups of 3–5 rather scratchy notes, sounding to the ear like: ‘crik..crik..crik..crik............crik..crik..crik..crik..’, repeated regularly, with each call separated from the next by 1.6–6.2 s (mean = 2.2; SD = 0.72; n = 50). However only three of 50 inter-call intervals are more than 2.5 s long, and with these outliers removed the range is reduced to 1.6–2.5 s (mean = 2.1; SD = 0.18; n = 47). The three call sequences last 36.5–55.8 s (n = 3) and contain 14–22 calls, each lasting 0.3–0.5 s (mean = 0.40; SD = 0.077, n = 53) and produced at a rate of 0.36–0.38/s (mean = 0.37; SD = 0.01). Each call contains 3–5 (mean = 4.2; SD = 0.6; n = 53) distinctly pulsed notes. Note repetition rate within calls is 7.2–13.3/s (mean = 8.9; SD = 0.8; n = 41) but only one of the 41 calls of sufficient quality for analysis has a note repetition rate of more than 10/s. Individual notes are 0.014–0.042 s long (mean = 0.028; SD = 0.005; n = 107) and contain 4–9 (mean = 5.6; SD = 1.0; n = 68) pulses. Pulse repetition rate within notes is 133–319 pulses/s (mean = 183.6; SD = 47.3, n = 68). Dominant frequency of the three calls is 4213–4519 Hz (mean = 4370; SD = 152.8; n = 3). A series of calls is illustrated in Figure 4. Etymology. The specific name gracilirostris is a feminine compound adjective, taken from the Latin “gracilis” meaning slender, in its combining form “gracili–”, and Latin “rostrum” meaning beak or snout, which in its adjectival combining form is “–rostris”.
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FIGURE 2. Choerophryne gracilirostris sp. nov. in life. A) Holotype SAMA R67520, B) Paratype SAMA R67516.
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FIGURE 3. Choerophryne gracilirostris sp. nov. in life, ventral view of SAMA R67516.
Natural history and distribution. C. gracilirostris is known from four locations in primary foothill and lower-montane rainforest on the southern side of the Central Cordillera at altitudes ranging from 213–1368 m; this is the widest altitudinal range known for a Choerophryne species. Males were primarily found calling during rain at night, from within leaf litter or rotting logs within 20 cm of the ground. No other Choerophryne species were found in sympatry with the new species; however Choerophryne burtoni is known from higher altitudes (1600 m a.s.l.) in the Muller Range (Kraus and Allison 2009b; Richards and Dahl 2009). Molecular differentiation. A DNA sequence of a fragment of the mitochondrial 16S rRNA gene of the new species, amplified using the primers 16SL3 and 16SAH from Vences et al. (2003) has been made available on Genbank (accession number KF561136). Comparisons to homologous data for C. amomani, C. arndatorum, C. microps and C. nigrescens (from Köhler and Günther 2008) using the Species Delimitation plugin for Geneious Pro 5.5.2 software revealed uncorrected sequence divergence from all taxa to be between 16.5–21.0%. These molecular data support the evolutionary distinctiveness of C. gracilirostris sp. nov from all other taxa, including the morphologically similar C. arndatorum (e.g. Vieites et. al. (2009) suggested a guideline of >3% uncorrected pairwise genetic divergence in 16S rRNA for identification of candidate species). TABLE 2. Comparison of diagnostic features of Choerophryne found on the central cordillera of New Guinea. Species
C. gracilirostris
C. rostellifer
C. burtoni
C. allisoni
SUL (mm)
13.5–14.7
14.0–15.6
12.1–13.6
11.5–11.6
TL/SUL
0.37–0.40
0.41–0.44
0.33–0.37
0.33
F3D/SUL
0.03–0.04
0.03–0.06
0.02–0.04
0.03
SL/SUL
0.21–0.26
0.19–0.22
0.17–0.21
0.15–0.21
OHG/SUL
0.06–0.09
0.08–0.10
0.03–0.06
0.04
IND/SUL
0.05–0.06
0.06–0.09
0.03–0.07
0.05-0.07
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FIGURE 4. Advertisement call of Choerophryne gracilirostris sp. nov. (SAMA R67520) recorded at a temperature of 25.5oC. A) Five consecutive calls from a longer sequence, showing waveform (top), spectrogram (bottom) and frequency distribution (left); B) Waveform (top) and spectrogram (bottom) of the third (middle) call illustrated in A, showing distinctly pulsed nature of the five notes.
Discussion Menzies and Tyler (1977) resurrected the genus Choerophryne from the synonymy of Cophixalus based on inspection of two specimens from Moiyokabip in the northernmost reaches of Western Province, Papua New Guinea, (1320 m a.s.l.). They briefly described these specimens and referred to them as “Choerophryne rostellifer”, the only recognized species in the genus at the time, but did not have access to call or molecular data. These specimens are the only records assigned to C. rostellifer from the southern side of the Central Cordillera. The range of Choerophryne gracilirostris sp. nov. (Figure 5) is closer (both in geography and altitude) to these southern “C. rostellifer” specimens than any populations of C. rostellifer from north of the range, and given the morphological similarity of these species it is possible that these “C. rostellifer” represent C. gracilirostris sp. nov.
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One of the two specimens (SAMA R15347) was examined during this study but the head had previously been removed for examination, precluding observations of the snout and internarial distance. Further work is required to confirm the identity of these specimens, but based on geography alone we consider it most likely that they represent Choerophryne gracilirostris sp. nov. or a closely allied form.
FIGURE 5. Map of New Guinea showing the type locality (solid circle) and other localities (open circles) of Choerophryne gracilirostris sp. nov. and specimens ascribed to Choerophryne rostellifer (triangle near Tabubil) by Menzies and Tyler (1977) that possibly also represent this species.
The rostral projection of Choerophryne comprises an extension of the nasal bones and the alary processes of the premaxillae and is unique amongst Melanesian microhylids. While the purpose of this structure (present in both sexes) is not known, in combination with the distinctly pointed urostyle this rostral projection gives members of the genus an unusual outline for a frog. We suggest that this plays some role in crypsis and masquerade (Skelhorn et al. 2010), helping the frogs to avoid identification as a recognizable prey item, especially against a background of leaf litter. The juvenile specimen of Choerophryne gracilirostris (SAMA R67515) has a proportionally shorter rostral projection than the adults, indicating that positive allometry is involved in the development of this character. Although C. gracilirostris sp. nov. is closest geographically to C. allisoni and C. burtoni, those species have relatively short snouts for the genus, and the new species’ distinctively elongated rostral projection is most similar to the geographically distant northern forms C. rostellifer and C. arndtorum. Further molecular studies of Choerophryne will be required to determine the affinities of the new species and to determine whether phenetic similarity or geographic proximity are the best predictor of its nearest relatives. Extensive surveys in the eastern half of New Guinea’s central cordillera have not detected additional populations of C. gracilirostris sp. nov., and it may be endemic to a small area on the southern side of the central ranges. A number of other potentially new species of Choerophryne from localities spanning New Guinea are under investigation, and further morphological and molecular studies will increase the known diversity in the genus. This work underlines the until-recently overlooked, but seemingly exceptional, diversity of miniaturised frog lineages present in New Guinea (Kraus 2010, 2011; Kraus & Allison 2009a; Rittmeyer et al. 2012).
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Acknowledgments Field work in Papua New Guinea was supported by Conservation International and ExxonMobil, and we are particularly grateful to Victoria Niesi of CI, and Steven Whisker and Luke Marodi of ExxonMobil for their assistance with this project. We are also grateful to Jim Robins of the PNG National Research Institute and Barnabas Wilmott and Fabian Taimbari of the PNG Department of Environment and Conservation for issuing relevant visas and export approvals. We thank the late Peter Blias for doing the CT scans, Ruth Williams and Adelaide Microscopy for CT scan advice and facilities and Mike Lee, Mark Hutchinson and Carolyn Kovach for extensive advice and support, and Fred Kraus for providing unpublished data. This work was supported by a grant to Paul Oliver, Mike Lee and Stephen Richards from the Australia Pacific Science Foundation.
Literature cited AmphibiaWeb (2013) AmphibiaWeb: Information on amphibian biology and conservation. Berkeley, California, Available from: http://amphibiaweb.org/ (accessed 25 February 2013) Bickford, D. (2004) Differential parental care behaviours of arboreal and terrestrial microhylid frogs from Papua New Guinea. Behavioural Ecology and Sociobiology, 55, 402–409. http://dx.doi.org/10.1007/s00265-003-0717-x Günther, R. (2008) Descriptions of four new species of Choerophryne (Anura, Microhylidae) from Papua Province, Indonesian New Guinea. Acta Zoologica Sinica, 54, 653–674. Köhler, F. & Günther, R. (2008) The radiation of microhylid frogs (Amphibia: Anura) on New guinea: A mitochondrial phylogeny reveals parallel evolution of morphological and life history traits and disproves the current morphology-based classification. Molecular Phylogenetics and Evolution, 47, 353–365. http://dx.doi.org/10.1016/j.ympev.2007.11.032 Kraus, F. (2010) New genus of diminutive microhylid frogs from Papua New Guinea. ZooKeys, 48, 39–59. http://dx.doi.org/10.3897/zookeys.48.446 Kraus, F. (2011) At the lower size limit for tetrapods, two new species of the miniaturised frog genus Paedophryne (Anura, Microhylidae). ZooKeys, 154, 71–88. http://dx.doi.org/10.3897/zookeys.154.1963 Kraus, F. & Allison, A. (2001) A review of the endemic New Guinea microhylid frog genus Choerophryne. Herpetologica, 57, 214–232. Kraus, F. & Allison, A. (2009a) New species of Cophixalus (Anura: Microhylidae) from Papua New Guinea. Zootaxa, 2128, 1–38. Kraus, F. & Allison, A. (2009b) New microhylid frogs from the Muller Range, Papua New guinea. ZooKeys, 26, 53–76. http://dx.doi.org/10.3897/zookeys.26.258 Menzies, J. & Tyler, M.J. (1977) The systematics and adaptations of some Papuan microhylid frogs which live underground. Journal of Zoology, 183, 431–464. http://dx.doi.org/10.1111/j.1469-7998.1977.tb04198.x Papuan Herpetofauna (2011) Checklist of the Amphibians and Reptiles of the Papuan Region. Bishop Museum Vertebrate Zoology, Honolulu, Available from: http://pbs.bishopmuseum.org/papuanherps/frogs.html/ (accessed 25 February 2013) Richards, S.J. & Burton, T.C. (2003) A new species of Choerophryne (Anura: Microhylidae) from Southern Highlands Province, Papua New Guinea. Transactions of the Royal Society of South Australia, 127, 47–51. Richards, S.J. & Dahl, C. (2009) Herpetofauna of the Strickland Basin and Muller Range, Papua New Guinea. In: Richards, S.J. & Gamui, B.G. (Eds), ‘Rapid Biological Assessments of the Nakanai Mountains and the Upper Strickland Basin.’ Surveying the Biodiversity of Papua New Guinea's Sublime Karst Environments. Conservation International, pp. 190–197. Richards, S.J., Dahl, C. & Hiaso, J. (2007) Another new species of Choerophryne (Anura: Microhylidae) from Southern Highlands Province, Papua new Guinea. Transactions of the Royal Society of South Australia, 131, 135–141. Richards, S.J. & Iskandar, D.T. (2000) A new minute Oreophryne (Anura: Microhylidae) from the mountains of Irian Jaya, Indonesia. Raffles Bulletin of Zoology. Singapore, 48, 257–262. Rittmeyer, E.N., Allison, A., Gründler, M.C., Thompson, D.K. & Austin, C.C. (2012) Ecological guild evolution and the discovery of the world's smallest vertebrate. PLoS ONE, 7. http://dx.doi.org/10.1371/journal.pone.0029797 Skelhorn, J., Rowland, H.M. & Ruxton, G.D. (2010) The evolution and ecology of masquerade. Biological Journal of the Linnean Society, 99, 1–8. http://dx.doi.org/10.1111/j.1095-8312.2009.01347.x Vences, M., Kosuch, J., Glaw, F., Bohme, W. & Veith, M. (2003) Molecular phylogeny of hyperoliid treefrogs: biogeographic origin of Malagasy and Seychellean taxa and re-analysis of familial paraphyly. Journal of Zoological Systematics and Evolutionary Research, 41, 205–215. http://dx.doi.org/10.1046/j.1439-0469.2003.00205.x
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Vieites, D., Wollenberg, K.C., Andreone, F., Köhler, J., Glaw, F. & Vences, M. (2009) Vast underestimation of Madagascar's biodiversity evidenced by an integrative amphibian inventory. Proceedings of the National Academy of Sciences, 106, 8267–8272. http://dx.doi.org/10.1073/pnas.0810821106
APPENDIX 1. Material examined. Specimens denoted by SJR field numbers are held at the South Australian Museum, pending repatriation to countries of origin or registration. Choerophryne allisoni SAMA R56075 (holotype), UPNG 9962 (paratype) Mt Sisa, Southern Highlands Province, PNG Choerophryne burtoni SAMA R62475 (holotype), SAMA R62476 (paratype), SJR 3295, SJR 3309 Moran, Southern Highlands Province, PNG; SAMA R65102 Sawetau, Western Province, PNG. Choerophryne longirostris SAMA R65929-32 Mt Menawa, West Sepik Province, PNG. Choerophryne nigrescens SJR 6052, SJR 6186 Marina Valen Village, Papua Province, Indonesia. Choerophryne proboscidea SAMA R60661-69 Wamangu, East Sepik Province, PNG Choerophryne rostellifer SAMA R60653-55, SAMA R60657, SAMA R60659-60 Utai, West Sepik Province, PNG Choerophryne ‘rostellifer’ SAMA R15347 Moiyokabip, Western Province, PNG
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Article
ISSN 1175-5326 (print edition)
ZOOTAXA
ISSN 1175-5334 (online edition)
http://dx.doi.org/10.11646/zootaxa.3753.5.6 http://zoobank.org/urn:lsid:zoobank.org:pub:93D3FEB4-3C66-4518-AA4A-67F2B091F46A
A new species of Choerophryne (Anura, Microhylidae) from the central cordillera of Papua New Guinea AMY IANNELLA1,2, STEPHEN RICHARDS1 & PAUL OLIVER3,4 1
South Australian Museum, Adelaide 5000, Australia School of Earth and Environmental Sciences, University of Adelaide, Adelaide, South Australia 5000, Australia 3 Department of Zoology, University of Melbourne, Melbourne, Victoria 3000, Australia 4 Museum Victoria, Melbourne, Victoria 3001, Australia 2
Abstract We describe a new species of very small microhylid frog in the genus Choerophryne from the upper Strickland River area, Western and Southern Highlands Provinces, Papua New Guinea. Choerophryne gracilirostris sp. nov. can be distinguished from congeners by the following combination of characters: small size (SUL 13.5–14.7 mm), moderately long and narrow snout, first finger without expanded disk and advertisement call consisting of 3–5 distinctly pulsed notes repeated in long sequences. Males in the type series were calling from within leaf litter in primary hill rainforest (213–1368 m a.s.l.). The new species is the third Choerophryne known from the southern side of New Guinea’s central cordillera. Measurements of a juvenile specimen (rare because most Choerophryne collected are calling males) demonstrate that the distinctive rostral projection of this genus exhibits pronounced positive allometry. Key words: frog, miniaturisation, Muller Range, rostral projection, systematics
Introduction Microhylids are the most species-rich radiation of frogs in New Guinea. Over 250 species are currently recognised, and this number is rapidly increasing (AmphibiaWeb 2013; Kraus and Allison 2009a; Papuan Herpetofauna 2013). Although Melanesian microhylids (all in the subfamily Asterophryinae) remain poorly studied they have attracted interest for the apparently repeated evolution of parental care of their direct-developing eggs (Bickford 2004; Köhler and Günther 2008). The existence of numerous lineages (many of them recently discovered) that have independently approached minimum size thresholds for terrestrial vertebrates has also attracted recent attention (Kraus 2010, 2011; Rittmeyer et al. 2012). The newly discovered genus Paedophryne is the most miniaturised lineage of Melanesian microhylids (and possibly of tetrapods (Kraus 2010, 2011; Rittmeyer et al. 2012)), but a number of other Melanesian microhylid genera also contain species with very small body sizes (e.g Kraus and Allison 2009a; Richards and Iskandar 2000; Kraus 2011). Perhaps the most notable of these is Choerophryne, a genus of nine recognised species of small to very small size (11.5–23.2 mm SVL) characterised by a unique extension of the nasal bones and the alary processes of the premaxillae, giving them a distinctively elongate snout. Despite this unique snout morphology a suite of morphological and molecular datasets indicates that Choerophryne is related to Albericus, a widespread genus of small to miniature blunt-snouted, largely arboreal microhylid frogs (Köhler and Günther 2008; Kraus and Allison 2001). Most recognised Choerophryne species (seven of nine) occur on the ranges and lowlands of the northern half of New Guinea and immediately adjacent islands, from Japen Island in the west to the Adelbert Mountains in the east (Günther 2008; Kraus and Allison 2001). Although a few species are widespread (Choerophryne rostellifer, C. proboscidea), most are currently known from a small number of localities, often at moderately high altitudes (>1000 m a.s.l.) in mountain ranges such as the Bewani and Torricelli Mountains (C. longirostris) or on the island of Japen (C. amomani) (Günther 2008; Kraus and Allison 2001) Accepted by M. Vences: 28 Nov. 2013; published: 9 Jan. 2014
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Choerophryne has only recently been documented from south of the central cordillera, with two very small species (IV>II>I, finger I less than half length of II, fingers II–IV with distinctly expanded discs up to 1.3 times width of penultimate phalanx, finger I without disk and with only faint circum-marginal groove; subarticular tubercles and webbing absent. Legs of moderate length (TL/SUL 0.40). Toes moderately long and wide, relative lengths IV>III>V>II>I, toe I approximately half length of II, all toes except I with terminal discs up to 1.4 times width of penultimate phalanx and with circum-marginal grooves; metatarsal tubercles and webbing absent. Disks on toes wider than those on fingers (F3/T4 0.78, Fig. 1).
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FIGURE 1. A) hand; and B) foot; of Choerophryne gracilirostris sp. nov. holotype (SAMA R67520) in the ventral aspect.
In preservative, ground colour of dorsum medium brown with dense dark-brown maculations, slightly denser anteriorly than posteriorly; dorsum dominated by a longitudinally oriented dark-brown hourglass mark, defined laterally by a pair of pale-tan dorso-lateral triangles extending from dorsal edge of the tympanum to the groin with medial tips approaching mid-dorsum, these pale-tan triangular patches with prominent but weakly defined darkbrown edging. Inguinal region with a pair of indistinct dark-brown lumbar ocelli with very small, distinct, pale cream medial spots. Vent bordered laterally and dorsally by an arc of dark-brown pigment. Exposed dorsal and lateral surfaces of limbs pale tan, extensively flecked and blotched with various shades of darker brown; darker pigmentation on limbs tending not to form distinct patterns, with the exception of some moderately distinct very dark-brown transverse bands at the midpoint of thigh, tibia and ankle. Dorsal surface of hands and feet pale buff with extensive pale-brown flecking. Venter pale buff with fine tan maculations coalescing on the throat, becoming scattered posteriorly and less dense around the vent and thighs, giving the throat an overall darker appearance than the belly and thighs; ventral surfaces of limbs buff, almost translucent, with scattered pale-tan flecks, palmar surfaces unpigmented; plantar surfaces largely unpigmented with light-tan speckling. Variation. Summary measurements for the type series are given in Table 1. The paratypes are of similar dimensions to the holotype, although all are slightly larger (SUL 13.7–14.7 mm vs. 13.5 mm). All specimens have a dorsal colouration including a longitudinally oriented dark-brown hourglass and paler-brown triangular lateral markings, and a pale-buff venter with extensive light-brown speckling. The paratypes have slightly paler dorsal colouration than the holotype (particularly SAMA R67519 and SAMA R67517); most also differ in having a distinct thin grey dorsal stripe extending from snout tip to urostyle tip (except SAMA R67518). The tympanic annulus is indistinct in all specimens, although a faint anterio-ventral ridge is sometimes apparent. A distinct palebuff medial stripe extends the full length of the venter on paratypes SAMA R67517 and SAMA R67514. The slope of the loreal region varies slightly among specimens, from slightly concave to nearly flat. Tuberculation in all paratypes is minimal and generally restricted to the flanks, a few low tubercles antero-lateral to the eyes are apparent in some specimens.
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TABLE 1. Summary of measurements (mm) for Choerophryne gracilirostris sp. nov. Reg#
R67520
PARATYPE PARATYPE PARATYPE PARATYPE PARATYPE PARATYPE R67515 R64986 R67516 R67517 R67519 R67514 R67518
Sex
Male
Male
Male
Male
Male
Male
Male
Juvenile
SUL
13.5
14.0
14.4
13.7
13.7
14.7
13.9
8.2
TL
5.4
5.5
5.3
5.4
5.2
5.6
5.4
3.3
F1D
0.2
0.2
0.2
0.3
0.3
0.2
0.3
0.1
F3D
0.5
0.5
0.4
0.4
0.5
0.5
0.5
0.2
T1D
0.4
0.4
0.4
0.3
0.4
0.4
0.4
0.1
T4D
0.6
0.5
0.6
0.8
0.7
0.8
0.8
0.4
HL
4.6
5.0
4.9
5.1
4.8
5.3
4.9
2.9
HW
4.7
5.1
5.3
5.0
4.6
5.3
4.8
3.1
SL
3.1
3.6
3.2
3.2
3.0
3.1
3.1
1.7
ED
1.3
1.4
1.5
1.5
1.5
1.5
1.6
1.1
OHG
1.2
1.1
1.1
1.0
0.9
0.9
1.0
0.5
END
2.1
3.2
2.2
2.0
1.9
2.2
1.9
1.1
IND
0.8
0.8
0.8
0.8
0.8
0.8
0.8
0.6
HOLOTYPE
The juvenile specimen (SAMA R67515) has the same dorsal and lateral colour pattern as adults, but the venter is much paler and almost entirely lacks flecks of light-brown pigmentation. The snout of the juvenile is also proportionally shorter than those of mature specimens, (SL/SUL 0.20 vs. an average of 0.23) while the eye diameter is proportionally larger (ED/SUL 0.13). Tibia length, head width and internarial distance are also relatively larger in the juvenile specimen. These data suggest that the elongated snout of this species undergoes positive allometric growth. Appearance in life. Photographs in life (Figure 2) of three specimens (SAMA R67516, R67519, R67520) taken at night, show a greater degree of contrast between light and dark brown dorsal and ventral areas than shown in preservative. The dorsal hourglass marking shows greater tonal variation than in preservative, sometimes including reddish-brown patches within the darker areas. Venter tinged grey on the throat grading to pink on the belly, with extensive fine reddish-brown maculations and scattered large pale grey-blue flecks (Figure 3), grey medial stripe more clearly visible than in preservative. Iris black with extensive small bronze flecks, pupil horizontal, encircled by a thin reddish-orange ring. Dorsal surfaces of torso and legs with numerous small tubercles of varying size that are less apparent in preservative. Advertisement call. Three full call sequences produced by SAMA R67520 at an air temperature of 25.5oC were recorded on 29 March 2008....... Calls are groups of 3–5 rather scratchy notes, sounding to the ear like: ‘crik..crik..crik..crik............crik..crik..crik..crik..’, repeated regularly, with each call separated from the next by 1.6–6.2 s (mean = 2.2; SD = 0.72; n = 50). However only three of 50 inter-call intervals are more than 2.5 s long, and with these outliers removed the range is reduced to 1.6–2.5 s (mean = 2.1; SD = 0.18; n = 47). The three call sequences last 36.5–55.8 s (n = 3) and contain 14–22 calls, each lasting 0.3–0.5 s (mean = 0.40; SD = 0.077, n = 53) and produced at a rate of 0.36–0.38/s (mean = 0.37; SD = 0.01). Each call contains 3–5 (mean = 4.2; SD = 0.6; n = 53) distinctly pulsed notes. Note repetition rate within calls is 7.2–13.3/s (mean = 8.9; SD = 0.8; n = 41) but only one of the 41 calls of sufficient quality for analysis has a note repetition rate of more than 10/s. Individual notes are 0.014–0.042 s long (mean = 0.028; SD = 0.005; n = 107) and contain 4–9 (mean = 5.6; SD = 1.0; n = 68) pulses. Pulse repetition rate within notes is 133–319 pulses/s (mean = 183.6; SD = 47.3, n = 68). Dominant frequency of the three calls is 4213–4519 Hz (mean = 4370; SD = 152.8; n = 3). A series of calls is illustrated in Figure 4. Etymology. The specific name gracilirostris is a feminine compound adjective, taken from the Latin “gracilis” meaning slender, in its combining form “gracili–”, and Latin “rostrum” meaning beak or snout, which in its adjectival combining form is “–rostris”.
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FIGURE 2. Choerophryne gracilirostris sp. nov. in life. A) Holotype SAMA R67520, B) Paratype SAMA R67516.
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FIGURE 3. Choerophryne gracilirostris sp. nov. in life, ventral view of SAMA R67516.
Natural history and distribution. C. gracilirostris is known from four locations in primary foothill and lower-montane rainforest on the southern side of the Central Cordillera at altitudes ranging from 213–1368 m; this is the widest altitudinal range known for a Choerophryne species. Males were primarily found calling during rain at night, from within leaf litter or rotting logs within 20 cm of the ground. No other Choerophryne species were found in sympatry with the new species; however Choerophryne burtoni is known from higher altitudes (1600 m a.s.l.) in the Muller Range (Kraus and Allison 2009b; Richards and Dahl 2009). Molecular differentiation. A DNA sequence of a fragment of the mitochondrial 16S rRNA gene of the new species, amplified using the primers 16SL3 and 16SAH from Vences et al. (2003) has been made available on Genbank (accession number KF561136). Comparisons to homologous data for C. amomani, C. arndatorum, C. microps and C. nigrescens (from Köhler and Günther 2008) using the Species Delimitation plugin for Geneious Pro 5.5.2 software revealed uncorrected sequence divergence from all taxa to be between 16.5–21.0%. These molecular data support the evolutionary distinctiveness of C. gracilirostris sp. nov from all other taxa, including the morphologically similar C. arndatorum (e.g. Vieites et. al. (2009) suggested a guideline of >3% uncorrected pairwise genetic divergence in 16S rRNA for identification of candidate species). TABLE 2. Comparison of diagnostic features of Choerophryne found on the central cordillera of New Guinea. Species
C. gracilirostris
C. rostellifer
C. burtoni
C. allisoni
SUL (mm)
13.5–14.7
14.0–15.6
12.1–13.6
11.5–11.6
TL/SUL
0.37–0.40
0.41–0.44
0.33–0.37
0.33
F3D/SUL
0.03–0.04
0.03–0.06
0.02–0.04
0.03
SL/SUL
0.21–0.26
0.19–0.22
0.17–0.21
0.15–0.21
OHG/SUL
0.06–0.09
0.08–0.10
0.03–0.06
0.04
IND/SUL
0.05–0.06
0.06–0.09
0.03–0.07
0.05-0.07
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FIGURE 4. Advertisement call of Choerophryne gracilirostris sp. nov. (SAMA R67520) recorded at a temperature of 25.5oC. A) Five consecutive calls from a longer sequence, showing waveform (top), spectrogram (bottom) and frequency distribution (left); B) Waveform (top) and spectrogram (bottom) of the third (middle) call illustrated in A, showing distinctly pulsed nature of the five notes.
Discussion Menzies and Tyler (1977) resurrected the genus Choerophryne from the synonymy of Cophixalus based on inspection of two specimens from Moiyokabip in the northernmost reaches of Western Province, Papua New Guinea, (1320 m a.s.l.). They briefly described these specimens and referred to them as “Choerophryne rostellifer”, the only recognized species in the genus at the time, but did not have access to call or molecular data. These specimens are the only records assigned to C. rostellifer from the southern side of the Central Cordillera. The range of Choerophryne gracilirostris sp. nov. (Figure 5) is closer (both in geography and altitude) to these southern “C. rostellifer” specimens than any populations of C. rostellifer from north of the range, and given the morphological similarity of these species it is possible that these “C. rostellifer” represent C. gracilirostris sp. nov.
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One of the two specimens (SAMA R15347) was examined during this study but the head had previously been removed for examination, precluding observations of the snout and internarial distance. Further work is required to confirm the identity of these specimens, but based on geography alone we consider it most likely that they represent Choerophryne gracilirostris sp. nov. or a closely allied form.
FIGURE 5. Map of New Guinea showing the type locality (solid circle) and other localities (open circles) of Choerophryne gracilirostris sp. nov. and specimens ascribed to Choerophryne rostellifer (triangle near Tabubil) by Menzies and Tyler (1977) that possibly also represent this species.
The rostral projection of Choerophryne comprises an extension of the nasal bones and the alary processes of the premaxillae and is unique amongst Melanesian microhylids. While the purpose of this structure (present in both sexes) is not known, in combination with the distinctly pointed urostyle this rostral projection gives members of the genus an unusual outline for a frog. We suggest that this plays some role in crypsis and masquerade (Skelhorn et al. 2010), helping the frogs to avoid identification as a recognizable prey item, especially against a background of leaf litter. The juvenile specimen of Choerophryne gracilirostris (SAMA R67515) has a proportionally shorter rostral projection than the adults, indicating that positive allometry is involved in the development of this character. Although C. gracilirostris sp. nov. is closest geographically to C. allisoni and C. burtoni, those species have relatively short snouts for the genus, and the new species’ distinctively elongated rostral projection is most similar to the geographically distant northern forms C. rostellifer and C. arndtorum. Further molecular studies of Choerophryne will be required to determine the affinities of the new species and to determine whether phenetic similarity or geographic proximity are the best predictor of its nearest relatives. Extensive surveys in the eastern half of New Guinea’s central cordillera have not detected additional populations of C. gracilirostris sp. nov., and it may be endemic to a small area on the southern side of the central ranges. A number of other potentially new species of Choerophryne from localities spanning New Guinea are under investigation, and further morphological and molecular studies will increase the known diversity in the genus. This work underlines the until-recently overlooked, but seemingly exceptional, diversity of miniaturised frog lineages present in New Guinea (Kraus 2010, 2011; Kraus & Allison 2009a; Rittmeyer et al. 2012).
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Acknowledgments Field work in Papua New Guinea was supported by Conservation International and ExxonMobil, and we are particularly grateful to Victoria Niesi of CI, and Steven Whisker and Luke Marodi of ExxonMobil for their assistance with this project. We are also grateful to Jim Robins of the PNG National Research Institute and Barnabas Wilmott and Fabian Taimbari of the PNG Department of Environment and Conservation for issuing relevant visas and export approvals. We thank the late Peter Blias for doing the CT scans, Ruth Williams and Adelaide Microscopy for CT scan advice and facilities and Mike Lee, Mark Hutchinson and Carolyn Kovach for extensive advice and support, and Fred Kraus for providing unpublished data. This work was supported by a grant to Paul Oliver, Mike Lee and Stephen Richards from the Australia Pacific Science Foundation.
Literature cited AmphibiaWeb (2013) AmphibiaWeb: Information on amphibian biology and conservation. Berkeley, California, Available from: http://amphibiaweb.org/ (accessed 25 February 2013) Bickford, D. (2004) Differential parental care behaviours of arboreal and terrestrial microhylid frogs from Papua New Guinea. Behavioural Ecology and Sociobiology, 55, 402–409. http://dx.doi.org/10.1007/s00265-003-0717-x Günther, R. (2008) Descriptions of four new species of Choerophryne (Anura, Microhylidae) from Papua Province, Indonesian New Guinea. Acta Zoologica Sinica, 54, 653–674. Köhler, F. & Günther, R. (2008) The radiation of microhylid frogs (Amphibia: Anura) on New guinea: A mitochondrial phylogeny reveals parallel evolution of morphological and life history traits and disproves the current morphology-based classification. Molecular Phylogenetics and Evolution, 47, 353–365. http://dx.doi.org/10.1016/j.ympev.2007.11.032 Kraus, F. (2010) New genus of diminutive microhylid frogs from Papua New Guinea. ZooKeys, 48, 39–59. http://dx.doi.org/10.3897/zookeys.48.446 Kraus, F. (2011) At the lower size limit for tetrapods, two new species of the miniaturised frog genus Paedophryne (Anura, Microhylidae). ZooKeys, 154, 71–88. http://dx.doi.org/10.3897/zookeys.154.1963 Kraus, F. & Allison, A. (2001) A review of the endemic New Guinea microhylid frog genus Choerophryne. Herpetologica, 57, 214–232. Kraus, F. & Allison, A. (2009a) New species of Cophixalus (Anura: Microhylidae) from Papua New Guinea. Zootaxa, 2128, 1–38. Kraus, F. & Allison, A. (2009b) New microhylid frogs from the Muller Range, Papua New guinea. ZooKeys, 26, 53–76. http://dx.doi.org/10.3897/zookeys.26.258 Menzies, J. & Tyler, M.J. (1977) The systematics and adaptations of some Papuan microhylid frogs which live underground. Journal of Zoology, 183, 431–464. http://dx.doi.org/10.1111/j.1469-7998.1977.tb04198.x Papuan Herpetofauna (2011) Checklist of the Amphibians and Reptiles of the Papuan Region. Bishop Museum Vertebrate Zoology, Honolulu, Available from: http://pbs.bishopmuseum.org/papuanherps/frogs.html/ (accessed 25 February 2013) Richards, S.J. & Burton, T.C. (2003) A new species of Choerophryne (Anura: Microhylidae) from Southern Highlands Province, Papua New Guinea. Transactions of the Royal Society of South Australia, 127, 47–51. Richards, S.J. & Dahl, C. (2009) Herpetofauna of the Strickland Basin and Muller Range, Papua New Guinea. In: Richards, S.J. & Gamui, B.G. (Eds), ‘Rapid Biological Assessments of the Nakanai Mountains and the Upper Strickland Basin.’ Surveying the Biodiversity of Papua New Guinea's Sublime Karst Environments. Conservation International, pp. 190–197. Richards, S.J., Dahl, C. & Hiaso, J. (2007) Another new species of Choerophryne (Anura: Microhylidae) from Southern Highlands Province, Papua new Guinea. Transactions of the Royal Society of South Australia, 131, 135–141. Richards, S.J. & Iskandar, D.T. (2000) A new minute Oreophryne (Anura: Microhylidae) from the mountains of Irian Jaya, Indonesia. Raffles Bulletin of Zoology. Singapore, 48, 257–262. Rittmeyer, E.N., Allison, A., Gründler, M.C., Thompson, D.K. & Austin, C.C. (2012) Ecological guild evolution and the discovery of the world's smallest vertebrate. PLoS ONE, 7. http://dx.doi.org/10.1371/journal.pone.0029797 Skelhorn, J., Rowland, H.M. & Ruxton, G.D. (2010) The evolution and ecology of masquerade. Biological Journal of the Linnean Society, 99, 1–8. http://dx.doi.org/10.1111/j.1095-8312.2009.01347.x Vences, M., Kosuch, J., Glaw, F., Bohme, W. & Veith, M. (2003) Molecular phylogeny of hyperoliid treefrogs: biogeographic origin of Malagasy and Seychellean taxa and re-analysis of familial paraphyly. Journal of Zoological Systematics and Evolutionary Research, 41, 205–215. http://dx.doi.org/10.1046/j.1439-0469.2003.00205.x
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Vieites, D., Wollenberg, K.C., Andreone, F., Köhler, J., Glaw, F. & Vences, M. (2009) Vast underestimation of Madagascar's biodiversity evidenced by an integrative amphibian inventory. Proceedings of the National Academy of Sciences, 106, 8267–8272. http://dx.doi.org/10.1073/pnas.0810821106
APPENDIX 1. Material examined. Specimens denoted by SJR field numbers are held at the South Australian Museum, pending repatriation to countries of origin or registration. Choerophryne allisoni SAMA R56075 (holotype), UPNG 9962 (paratype) Mt Sisa, Southern Highlands Province, PNG Choerophryne burtoni SAMA R62475 (holotype), SAMA R62476 (paratype), SJR 3295, SJR 3309 Moran, Southern Highlands Province, PNG; SAMA R65102 Sawetau, Western Province, PNG. Choerophryne longirostris SAMA R65929-32 Mt Menawa, West Sepik Province, PNG. Choerophryne nigrescens SJR 6052, SJR 6186 Marina Valen Village, Papua Province, Indonesia. Choerophryne proboscidea SAMA R60661-69 Wamangu, East Sepik Province, PNG Choerophryne rostellifer SAMA R60653-55, SAMA R60657, SAMA R60659-60 Utai, West Sepik Province, PNG Choerophryne ‘rostellifer’ SAMA R15347 Moiyokabip, Western Province, PNG
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