Advances in Zoology

Advances in Zoology / 2014 / Article

Research Article | Open Access

Volume 2014 |Article ID 563165 | https://doi.org/10.1155/2014/563165

André Pansonato, Jessica Rhaiza Mudrek, Fernanda Simioni, Itamar Alves Martins, Christine Strüssmann, "Geographical Variation in Morphological and Bioacoustic Traits of Pseudopaludicola mystacalis (Cope, 1887) and a Reassessment of the Taxonomic Status of Pseudopaludicola serrana Toledo, 2010 (Anura: Leptodactylidae: Leiuperinae)", Advances in Zoology, vol. 2014, Article ID 563165, 13 pages, 2014. https://doi.org/10.1155/2014/563165

Geographical Variation in Morphological and Bioacoustic Traits of Pseudopaludicola mystacalis (Cope, 1887) and a Reassessment of the Taxonomic Status of Pseudopaludicola serrana Toledo, 2010 (Anura: Leptodactylidae: Leiuperinae)

Academic Editor: Ariovaldo A. Giaretta
Received04 Apr 2014
Revised11 Jun 2014
Accepted04 Jul 2014
Published12 Aug 2014

Abstract

Comparisons of advertisement calls of anurans can be used to determine intra- and interspecific differences or affinities. Described from midwestern Brazil, Pseudopaludicola mystacalis is widely distributed and abundant in major open Brazilian ecosystems. However, researchers frequently fail to determine the true taxonomic status of some of these populations and attribute them to unidentified or misidentified species. Herein, we employ morphological and bioacoustic data to reassess the distribution range and to evaluate intraspecific variation in P. mystacalis based on specimens from fifteen localities and seven Brazilian states. We also reassess the distribution and taxonomic status of Pseudopaludicola serrana, herein considered as a junior synonym of P. murundu based on morphology, bioacoustics, and molecular data.

1. Introduction

Advertisement calls are important for mate recognition in anurans and hence contribute to premating isolation among sympatric species [1]. Comparison of advertisement calls can be used to determine differences and affinities among different anuran species and so to determine taxonomic identity and phylogenetic relationships [2, 3]. Such comparisons may be especially useful for situations in which the taxonomic identity of a species is uncertain or contested involving synonymies, redescriptions, and species resurrections. Indeed, in the absence of consistent morphological characters for interspecific distinctiveness, advertisement calls have proven to be of great help in revealing and supporting hypotheses of putative new species of Pseudopaludicola [49].

Described from midwestern Brazil (Chapada dos Guimarães, Mato Grosso), Pseudopaludicola mystacalis is widely distributed and abundant in open environments along South American “diagonal of open formations” [8]. However, some populations along the species’ range are not recognized as belonging to this taxon, being rather attributed to other taxonomic entities, such as Pseudopaludicola aff. falcipes, Pseudopaludicola aff. mystacalis, and Pseudopaludicola sp. [1014]. Therefore, an integrative taxonomic revision is needed to clarify the distribution range and variation in this species [9].

In spite of great morphological similarity among most of the 18 species of Pseudopaludicola currently recognized, three of them are readily distinguished from the others by having longer hindlimbs [46, 8, 9]: Pseudopaludicola saltica (Cope, 1887), Pseudopaludicola murundu Toledo, Siqueira, Duarte, Veiga-Menoncello, Recco-Pimentel, and Haddad, 2010, and Pseudopaludicola serrana Toledo, 2010. Advertisement calls of all three species are similarly composed of series of notes with nonconcatenated pulses [8, 1517] and they all share chromosomes [16, 18] comprising a monophyletic clade [19]. However, the results of a recent molecular phylogenetic analysis suggested that P. serrana is a junior synonym of P. murundu [19].

Objectives of the present article are (1) to provide and to discuss the intraspecific variation in morphological and bioacoustic traits of P. mystacalis along its distribution range in Brazil; (2) to reassess the taxonomic status of P. serrana, based on the reinterpretation of the literature data and on the examination of new materials (specimens and calls), freshly obtained at the type-locality and/or its vicinities of P. serrana and related species.

2. Material and Methods

Examined specimens of P. mystacalis, P. murundu, P. saltica, and P. serrana (Appendices A and B) are deposited in the following collections: “Coleção Zoológica de Vertebrados, Universidade Federal de Mato Grosso” (UFMT, Cuiabá, Mato Grosso, Brazil), “Coleção Herpetológica da Universidade Federal do Ceará” (UFC, Fortaleza, Ceará), “Fonoteca Neotropical Jacques Vielliard” (FNJV, Campinas, São Paulo), and “Museu de Ciências Naturais” (MCNAM, Belo Horizonte, Minas Gerais). Material deposited at UFMT was collected with permission of the “Instituto Chico Mendes de Conservação da Biodiversidade” (ICMBIO 27231-1).

Since the available diagnoses for P. serrana and P. murundu do not allow clearly distinguishing specimens from these two species, new material from additional localities was putatively associated with each of them based solely on the positioning of collecting and/or recording sites: populations from easternmost localities in Minas Gerais were considered to represent P. serrana and populations from westernmost localities in Minas Gerais (and those from the state of São Paulo) were considered to represent P. murundu.

The measurements of 218 adult specimens (Tables 1 and 2) of P. murundu (6 males; 1 female), P. mystacalis (101 males; 37 females), P. saltica (39 males; 3 females; original data in Pansonato et al. [8]), and P. serrana (22 males; 6 females) were taken with a digital caliper to the nearest 0.1 mm. Measurements for hand length (HAL), tibia length (TL), tarsus length (TAL), and foot length (FL) followed Heyer et al. [20]. Measurements for snout-vent length (SVL), head length (HL), head width (HW), interorbital distance (IOD), eye diameter (ED), eye-nostril distance (END), internarial distance (IND), and thigh length (THL) followed Duellman [21].


Mato GrossoSão PauloGoiásPará
MalesFemalesMalesFemalesMalesFemalesMales
()()()()()()()

SVL
(10.9–16.3)(14.3–18.1)(13–14.9)(14.3–16)(11.7–16.5)(14.6–17)(14.6–16.6)
HL
(4.4–6.5)(5.2–7.5)(4.6–5.9)(5.1–6.0)(4.7–6.1)(5.0–6.3)(5.3–5.9)
HW
(3.7–6.7)(5.0–6.8)(4.3–5.1)(4.6–5.8)(4.3–6.4)(4.9–5.9)(4.5–5.3)
IOD
(0.7–1.6)(0.8–1.7)(1.0–1.4)(1.1–1.4)(1.0–1.7)(1.2–1.8)(1.1–1.5)
ED
(1.0–1.9)(1.3–2.3)(1.1–1.7)(1.3–1.9)(1.2–1.7)(1.4–1.8)(1.6–1.8)
END
(0.7–1.8)(1.1–2.1)(1.0–1.2)(1.1–1.8)(0.9–1.5)(1.1–1.4)(1.1–1.4)
IND
(0.8–1.7)(1.0–1.9)(1.1–1.5)(1.3–1.5)(1.1–1.7)(1.2–1.7)(1.2–1.4)
HAL
(3.1–4.4)(3.2–6.3)(3.5–4.3)(3.8–4.8)(3.4–4.4)(3.8–4.5)(3.6–4.1)
THL
(5.1–7.3)(6.4–9.4)(5.6–6.9)(5.3–7.1)(5.6–7.3)(7.1–7.7)(6.6–7.2)
TL
(5.9–8.2)(7.2–9.8)(6.7–7.6)(7.1–7.8)(6.4–8.0)(7.5–8.1)(7.2–7.6)
TAL
(3.1–4.6)(3.1–5.2)(3.5–4.5)(3.9–4.6)(3.2–4.5)(4.0–4.8)(3.4–4.2)
FL
(6.3–9.2)(7.9–10.6)(7.3–8.4)(7.6–8.9)(6.9–8.2)(7.8–9.2)(7.6–8.8)


Pseudopaludicola  serrana Pseudopaludicola  murundu
TopotypesAdditional localitiesTopotypes
MalesFemalesMalesFemalesMalesFemales
()()()()()()

SVL17.717.3
(14.6–17.5)(12.6–16.7)(15.9–18.5)(15.2–16.9)
HL6.86.8
(6.2–7.3)(4.8–6.9)(6.3–7.1)(5.6–6.7)
HW6.65.9
(5.7–6.3)(4.7–6.1)(5.9–6.7)(5.3–5.8)
IOD1.81.5
(1.3–1.6)(1.2–1.6)(1.5–1.7)(1.3–1.5)
ED1.71.9
(1.5–1.7)(1.3–1.7)(1.5–1.7)(1.4–1.8)
END1.61.6
(1.5–1.7)(1.3–1.7)(1.4–1.6)(1.4–1.6)
IND1.81.6
(1.3–1.7)(1.2–1.7)(1.5–1.7)(1.4–1.7)
HAL4.94.9
(4.3–4.6)(3.4–4.6)(4.3–4.7)(4.2–4.6)
THL10.29.5
(8.5–9.3)(6.8–9.4)(8.7–10.1)(8.6–9.3)
TL12.712.3
(10.6–11.3)(8.9–11.5)(10.9–12.2)(10.8–11.6)
TAL5.86.3
(5.1–5.7)(4.2–5.5)(5.0–6.1)(5.4–5.6)
FL11.111.4
(9.5–10.3)(7.4–10.4)(9.5–10.6)(9.9–10.9)

Vocalizations of specimens of P. murundu, P. mystacalis, P. saltica, and P. serrana were recorded by André Pansonato with a professional digital recorder Marantz PMD 660 equipped with a Yoga EM-9600 external directional microphone. Digital recordings were sampled at 44.1 kHz sampling rate and 16 bit resolution and saved in uncompressed wave files. Spectrograms were edited using Raven Pro 1.3 software with the following configuration: for P. mystacalis, brightness 75%; contrast 80%; DFT size 512 samples; 3 dB filter bandwidth 112 Hz; time grid overlap 50%; for P. murundu, P. saltica, and P. serrana, brightness 70%; contrast 80%; DFT size 512 samples; 3 dB filter bandwidth 124 Hz; time grid overlap 50%.

We analyzed 1894 notes (Tables 3 and 4): 503 from P. murundu, 444 notes from P. mystacalis, 577 from P. saltica, and 370 from P. serrana. The following temporal variables were measured from the waveform: number of pulses per note; note and pulse duration (ms); internote and interpulse interval (ms). Note that repetition rate was calculated in notes per minute. Dominant frequency (note peak frequency; Hz) was obtained from the spectrogram. Terminology for bioacoustic variables follows Magalhães et al. [7], Pansonato et al. [8], and Heyer et al. [20]. Vocalizations are archived in the “Banco de Registros Bioacústicos” and housed at the “Laboratório de Herpetologia do Instituto de Biociências da Universidade Federal de Mato Grosso” (LH, Cuiabá, Mato Grosso).


Locality—StateAir tempNote duration (ms)Internote interval (ms)Pulses per notePulse duration (ms)Dominant frequency (Hz)Notes/min
(mean)

Poconé—MT ()25.6°C (30–50) (60–100) (14–18)
(1-2)
(4522–4909.6)511.1
N.S. Livramento—MT ()25.2°C (40–50) (50–200) (14–19)
(1-2)
(4737.3–4909.6)506.4
C. Guimarães—MT ()26.3°C (30–50) (40–100) (14–17)
(1-2)
(4651.2–5254.1)576.9
Cuiabá—MT ()26°C (30–50) (60–100) (12–16)
(1–3)
(4651.2–4909.6)443.3
Cuiabá—MT ()26°C (30–50) (50–200) (13–18)
(1-2)
(4478.9–4995.7)524.3
Cáceres—MT ()26°C (40–50) (50–70) (14–18)
(1-2)
(4737.3–4995.7)538.9
Balsas—MA ()26.5°C
(37–45)
(70–90) (14–18)
(1-2)
(4780.4–5340.2)513.7
Icém—SP ()23°C (50–60) (100–150) (14–20)
(1-2)
(4737.3–4974.2)363.3
Itapipoca—CE () (40–50) (70–130) (14–18)
(1-2)
(4780.4–5211)420.7
Taíba—CE () (40–50) (60–70)16±1.1 (13–18)2±0.5  
(1–3)
4795.2±85.2 (4694.2–4952.6)535.3
Brejo do Buriti—PI ()27°C (45–50) (60–140) (18–20)2 (4823.4–4909.6)429.6
Primavera—PA ()25.5°C (40–50) (70–100)18±1.2 (16–20)2±0.5  
(1-2)
5040.6±45.6 (4921.9–5109.4)463.7
Uruaçu—GO ()24.5°C50±2  
(40–50)
60±5  
(50–80)
16±1.2 (14–18)
(1-2)
(4500–4968.8)543.5
Mean ± SD (30–60) (40–200) (12–20)
(1–3)
(4478.9–5340.2)490.1±61.1 (363.3–576.9)


Species
(voucher record)
Note duration (ms)Internote interval (ms)Pulse duration (ms)Interpulses interval (ms)Dominant frequency (Hz)Pulses/noteNotes/minMunicipality/state

P. murundu
(LH 676)
(58–105) (69–141) (4–12) (7–40) (5168–5857) (2–5) (314.5–370.4)Rio Claro/SP
P. murundu
(LH 677)
(49–114) (70–140) (9–17) (6–39) (5254.1–5857) (2-3) (295.6–341.9)Rio Claro/SP
P. murundu
(LH 678)
(33–104) (89–137) (5–17) (8–46) (5340.2–5900.1) (2–4) (292.6–326.4)Rio Claro/SP
P. murundu
(FNJV 12976)
(56–103) (79–247) (5–14) (10–29) (5168–6201.6) (3-4)280.3Rio Claro/SP
P. murundu
(FNJV 4575)
(54–105) (97–193) (5–16) (5–50) (4875–5812.5) (2–5) (218.2–369.1)São Roque de Minas/MG
P. murundu
(FNJV 4576)
(77–143) (129–194) (8–18) (10–54) (5250–5625) (2–4) (189.3–266.6)Poços de Caldas/MG
P. serrana
(LH 673)
(65–131) (131–224) (8–18) (6–32) (5168–5814) (3–5) (206.1–225.8)Brumadinho/MG
P. serrana
(LH 674)
(49–117) (184–288) (6–17) (5–41) (5168–5512.5).4 (2–4)1 (170.9–187.7)Brumadinho/MG
P. serrana
(LH 675)
(49–99) (81–197) (7–16) (5–33)5857 (3-4) (228.2–272.7)São João Del Rei/MG
P. serrana
(FNJV 12879)
(47–72) (63–101) (4–14) (4–16) (5512.5–5857) (3-4) (361.4–476.2)São João Del Rei/MG
P. serrana
(FNJV 12880)
(26–97) (75–166) (1–9) (4–33) (5512.5–6029.3) (2–5) (251.1–517.2)São João Del Rei/MG
P. saltica
(13A-01)
(48–86) (75–170) (5–13) (5–55)4 (4608.1–4952.6) (2-3) (342.4–406.2)Chapada dos Guimarães/MT
P. saltica
(42A-06)
(46–70)1 (90–137) (4–11) (5–30) (4823.4–4952.6) (3-4) (298.5–441.2)Pontes e Lacerda/MT
P. saltica
(42A-07)
(48–87) (144–224) (4–19) (30–46) (4005.2–4952.6) (2-3) (213.5–283)Pontes e Lacerda/MT
P. saltica
(LH 12)
(63–95) (80–172) (4–9) (3–49) (4866.5–5512.5) (3–5) (229.9–394.7)Porto Estrela/MT
P. saltica
(LH 13)
(85–106) (99–158) (3–7) (2–56) (5081.8–5297.2) (5–6) (230.8–314.1)Porto Estrela/MT
P. saltica
(LH 14)
(70–92) (107–210) (4–44) (4–10) (4651.2–4995.7) (2-3) (206.2–338.9)Porto Estrela/MT
P. saltica
(LH 16)
(64–118) (93–162) (6–18) (3–56) (4306.6–5340.2) (3–5) (226.4–335.2)Porto Estrela/MT
P. saltica
(LH 17)
(33–122)