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Tadpole, Oophagy, Advertisement Call, and Geographic Distribution ofAparasphenodon arapapa Pimenta, Napoli and Haddad 2009 (Anura, Hylidae)Author(s): Ricardo Lourenço-de-Moraes , Amanda S. F. Lantyer-Silva , Luís F. Toledo , and Mirco SoléSource: Journal of Herpetology, 47(4):575-579. 2013.Published By: The Society for the Study of Amphibians and ReptilesDOI: http://dx.doi.org/10.1670/11-326URL: http://www.bioone.org/doi/full/10.1670/11-326

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Journal of Herpetology, Vol. 47, No. 4, 575–579, 2013Copyright 2013 Society for the Study of Amphibians and Reptiles

Tadpole, Oophagy, Advertisement Call, and Geographic Distribution ofAparasphenodon arapapa Pimenta, Napoli and Haddad 2009 (Anura, Hylidae)

RICARDO LOURENCO-DE-MORAES,1,2 AMANDA S. F. LANTYER-SILVA,1 LUIS F. TOLEDO,2,3AND MIRCO SOLE

4

1Graduate program in Ecology and Biodiversity Conservation, Universidade Estadual de Santa Cruz, Ilheus, Bahia, Brazil2Museum of Zoology ‘‘Prof. Adao Jose Cardoso,’’ Institute of Biology, Universidade Estadual de Campinas, Campinas, Sao Paulo, Brazil

4Department of Biological Sciences, Universidade Estadual de Santa Cruz, Ilheus, Bahia, Brazil

ABSTRACT.—The genus Aparasphenodon is poorly known. Of the four species, the larvae of only one have been described, and the

advertisement calls of all taxa remain unknown. Here, we describe the tadpole, adult coloration, and advertisement calls of Aparasphenodonarapapa. We also provide data that extend its known distribution 170 km to the south, from the type locality in Itubera to Una, Bahia, Brazil. Inaddition, we report larval morphology related to bromeligenous habitat specialization of tadpole and metamorph oophagy for the first time in

the genus. The advertisement call is composed of one multipulsed note with mean duration of 150 ms. Whether the observed oophagy is

obligatory or opportunistic remains unclear, suggesting that further studies are warranted. Our observations provide insight into the behavioraland morphological diversity in the genus Aparasphenodon, and may guide future studies of this unique group of anurans.

The genus Aparasphenodon Miranda-Ribeiro, 1920 is com-posed of four species (Aparasphenodon arapapa Pimenta, Napoliand Haddad, 2009, Aparasphenodon bokermanni Pombal, 1993,Aparasphenodon brunoi Miranda-Ribeiro, 1920, and Aparaspheno-don venezolanus Mertens, 1950) and is distributed from southernBrazil to northern South America (Frost, 2013). It is placedamong the casque-headed hylids, which all display phragmosis,a behavior in which the ossified head is used to obstruct burrowopenings, protecting the animal against predators (Smith et al.,2007; Toledo et al., 2011) and preventing desiccation (Andradeand Abe, 1997). The natural history of species in the genus ispoorly known, and tadpoles have been described only forAparasphenodon brunoi (Wogel et al., 2006).

The most recently described species in the genus is A. arapapa,which is found in ‘‘restinga’’ vegetation typical of sandy coastalplains (Pimenta et al., 2009). Only two specimens were availableat the time of description of this species (Pimenta et al., 2009):the holotype, an adult male from the municipality of Itubera,and the paratype from the municipality of Cairu (25 km north ofItubera), both in the southern state of Bahia, Brazil. During fieldexpeditions to the municipality of Una and Ilheus weencountered tadpoles and recently metamorphosed individualsof this species. Here we describe the tadpole and advertisementcall of A. arapapa, and report observations on the distributionand parental care of this species.

MATERIALS AND METHODS

Study Site.—Field studies were undertaken in two PrivateNatural Heritage Reserves (RPPN) in the Atlantic forest,southern Bahia: RPPN Nova Angelica, municipality of Una(158150S, 398040W, less than 100 m a.s.l.) and RPPN Boa Uniao,municipality of Ilheus (158040S, 398030W, less than 100 m a.s.l.).The Reserves are mainly a mosaic of secondary and primaryforests (Pardini, 2004).

Data Collection.—Two tadpoles were collected in a bromeliadwater tank, in the municipality of Una (15815 004.5"S,39804032.9"W, 79 m a.s.l.), Bahia, in February and March 2010.One tadpole at Gosner (1960) stage 41 was maintained in aterrarium until it completed metamorphosis, to confirm its

identity as A. arapapa; the second tadpole was collected atGosner stage 39. Another metamorphic frog was collected on 8December 2011 at the same locality and two tadpoles (stages 36and 40) were collected on 14 April 2012 in a bromeliad watertank in the municipality of Ilheus (15804029.6"S, 39803009.0"W, 95m a.s.l.). All specimens were preserved in 5% formalin. Wedescribe the tadpole following the terminology of Altig andMcDiarmid (1999). Measurements were made with digitalcalipers to the nearest 0.05 mm with the aid of a Zeissstereoscopic microscope. Calls of adult males were recordedon 9 March 2010 at 2230 hours, with a SONY WMD6Ct cassetterecorder equipped with an external microphone. Ambient airtemperature (measured with a digital thermo-hygrometer) atthe time of recording was 26.78C. The microphone waspositioned about 50 cm from the calling male. Calls weredigitized at 48.4 kHz with the use of the software Raven 1.4 Pro.The following acoustic parameters were analyzed: note dura-tion, interval between notes, maximum frequency, minimumfrequency, fundamental frequency, and dominant frequency.Sonograms were made with Fast Fourier Transform (FFT) andframe length of 512 samples, contrast 65% and brightness 85%.The terminology for the bioacoustic analyses follows Toledo andHaddad (2005).

Voucher specimens are deposited in the Zoological Collectionof Universidade Estadual de Santa Cruz (MZUESC 9097, 9098,10354), Zoology Museum ‘‘Prof. Adao Jose Cardoso,’’ Universi-dade Estadual de Campinas (ZUEC 16613, 16603, 16645, 16646).Call recordings are deposited in the Fonoteca NeotropicalJacques Vielliard, Universidade Estadual de Campinas (FNJV11896–12872).

RESULTS

Tadpole Description.—The description is based on threetadpoles at Gosner (1960) (Fig. 1) stages 39–40 (ZUEC 16603;MZUEC 10354). Mean total length 51.76 mm 6 2.92 (49.9–55.12mm); mean body length 17.87 mm 6 2.36 (15.25–19.85 mm).Body shape is elliptical (oval, with one end wider than theother) in dorsal and ventral view. Snout elliptical in lateral anddorsal view, truncate in dorsal view; mean internarial distance2.86 mm 6 0.39 (2.43–3.2 mm); eyes dorsolateral; mean eyediameter 1.71 mm 6 0.82 (0.84–2.47 mm), mean interorbitaldistance 3.98 mm 6 1.07 (2.90–5.03 mm). Spiracle single,

3Corresponding Author. E-mail: toledolf2@yahoo.comDOI: 10.1670/11-326

sinistral, located in the middle third of the body and below the

midline of the body, opening posteriorly. Vent tube single,

midventral, length 2.88 mm 6 0.93 (2.29–3.95 mm). Mean tail

length 33.89 mm 6 2.16 (31.40–35.27 mm); caudal musculature

with defined myotomes, mean tail height at proximal portion

2.66 mm 6 0.73(1.85–3.27 mm), mean maximum height 4.63

mm 6 0.61(4.10–5.30 mm); tail tip without terminal flagellum.

Dorsal and ventral fins symmetrical; dorsal fin originates at end

of body, straight, slight thinning at the end, with rounded point;

ventral fin slightly curved throughout its length; maximum

height in middle third of tail.

Oral disc (Fig. 1D) dorsal, mean length 4.28 mm 6 0.84 (3.79–

5.25 mm). Marginal papillae uniformly, simple, wide and short,

arranged as a single row around the oral disc with a superior

narrow gap; anterior labium with marginal papillae and wide

gap length 1.90 6 0.43 mm (1.45–2.30 mm) on the medium

region; labial tooth row formula (labial tooth row formula) is

2(2)/2(1–2). Upper jaw sheath forming U-shaped arc; lower-jaw

sheath V-shaped; upper and lower jaws black and keratinized

with thick serrations. Tooth row A-1 complete; A-2 row

interrupted medially by a wide gap; P-1 row interruption

medially by a wide gap (slightly less than A-2); scattered

denticles present between P-1 and P-2; P-2 row interrupted

medially by a wide gap (smaller than A-2, P-1, and P-2).

Body color in life light brown, darker in dorsal region and

lightening toward the base of tail; ventral surface translucent,

bluish (internal organs visible); tail light brown with small dark

spots at base; dorsal and ventral fins transparent with a dark line

at the margin; tail muscles light brown. Tibia and foot light brown.

Color in preservative body bluish; dorsal and ventral regions

lighter than coloration in life. Tail muscle beige. Ventral surface

FIG. 1. Tadpole Gosner’s stage 39 of Aparasphenodon arapapa (ZUEC 16603) in dorsal (A), lateral (B), and ventral (C) views, and mouthparts (D).

576 R. LOURENCO-DE-MORAES ET AL.

bluish, possibly because of pigment of underlying internalorgans partially visible through this translucent surface.

The tadpole of A. arapapa differs from that of A. brunoi (the onlyspecies of the genus for which a tadpole description has beenpublished, Wogel et al., 2006) by a labial tooth row formula of2(2)/6(1) in A. brunoi versus 2(2)/2(1–2) in A. arapapa; flagellumat the tail end absent in A. arapapa (present in A. brunoi); eyesarranged laterally in A. brunoi, dorsally in A. arapapa; upper lippapillae uniserial or biserial in A. brunoi, uniserial in A. arapapa;lower lip triserial in A. brunoi, uniserial in A. arapapa; oral discdorsal in A. arapapa, anteroventral in A. brunoi; smallest size instage 40 (A. arapapa 49.9 mm and A. brunoi 63.2 mm).

Natural History Notes.—The dorsal coloration of one juvenilewas bluish with one eye red and the other blue (Fig. 2A). Thewild-caught metamorphic specimen contained eggs in its gut(Fig. 2C,D) and the wild-caught juvenile had two red eyes.Other two juveniles observed in the field had two red eyes, anda third individual had two blue eyes.

We found an adult female and a tadpole stage 39 inside thecentral water tank of a bromeliad. On a second occasion, twotadpoles (stages 36 and 40) were found in the same bromeliadwith a male and a female perched in the bromeliad axil adjacentto the water tank. All tadpoles in the central water tank wereobserved to engage in air-gulping behavior (see Lannoo et al.,1987).

Advertisement Call.—Adult males (Fig. 2B) call from the watertank of terrestrial bromeliads that have accumulated water.Frogs were observed with the body half submerged and theirheads above the water surface. When disturbed, they sub-merged completely. The advertisement call (Fig. 3) wasanalyzed based on the recordings of nine calls of two males(ZUEC 16645, 16646). The call is composed of one multipulsed

FIG. 2. Newly metamorphosed juvenile of Aparasphenodon arapapa (A), adult male recorded (ZUEC 16645) (B), and metamorphic frog with eggs inthe stomach in lateral (C) and ventral (D) views.

FIG. 3. Audiospectrogram (above) and waveform (below) of oneadvertisement call of Aparasphenodon arapapa (ZUEC 16645) recorded inthe municipality of Una, Bahia, Brazil. Air temperature 26.78C.

NATURAL HISTORY NOTES OF APARASPHENODON ARAPAPA 577

note and has a mean duration of 150 6 20 ms (130–180 ms). The

mean maximum frequency was 2,122.42 6 212.90 Hz (1,874.70–

2,588.90 Hz), the mean minimum frequency of the call was

604.82 6 24.56 Hz (557.90–647.20 Hz). The dominant

(=fundamental) frequency was 1,481.52 6 36.30 Hz (1,464.30–

1,550.40 Hz). The mean intercall interval was 880 6 140 ms

(670–1,140 ms).

Distribution.—We found two populations of A. arapapa in

areas of Atlantic forest, in the municipalities of Ilheus

(15804029.6"S, 39803009.0"W, 95 m a.s.l.), and Una (15815004.5"S,

39804032.9"W, 79 m a.s.l.), southern Bahia. Therefore, our

findings extend the known distribution of A. arapapa 172 km

southern from the type locality in the municipality of Itubera

(Fig. 4).

FIG. 4. Distribution of Aparasphenodon arapapa in the vegetation map featuring the coastline of the state of Bahia, Brazil. Open circle corresponds tothe type locality (Itubera); closed circle corresponds to a previously known locality (Cairu); and triangles correspond to the new records frommunicipalities of Ilheus and Una.

578 R. LOURENCO-DE-MORAES ET AL.

DISCUSSION

We suspect that A. arapapa may exhibit parental care,including the presentation of unfertilized or fertilized eggs asa food source for developing larvae. This suspicion is based on1) the tadpole morphology, with mouth orientation similar toother oophagus species (LTRF 2/2 and tadpole Group I; seeLehtinen et al., 2004); 2) the presence of adults (female or maleand female) observed in the water tanks of bromeliads withdeveloping larvae, similar to other observations of parental carerelated to oophagy (Jungfer, 1996; Jungfer and Weygoldt, 1999);3) and eggs in the stomach of the metamorphic individual (Fig.2C,D). Laying trophic eggs for tadpoles and metamorphiclarvae is novel for the genus Aparasphenodon but has beenreported frequently for species within the Hylinae, Hylidaesubfamily, of the genera Osteocephalus (Jungfer and Weygoldt,1999), Osteopilus (Thompson, 1996), and Anotheca (Jungfer,1996). Anotheca is allocated in the tribe Hylini, whereas thegenera Osteopilus and Ostecephalus, together with Aparaspheno-don, are in the tribe Lophiohylini (Faivovich et al., 2005; Wiens etal., 2010). As this behavior is now reported for three out of theeight genera within the Lophiohylini, we suggest that thismonophyletic group presents an adequate model for studyingthe evolution of oophagy among anurans. Whether thisobserved oophagy is obligatory or opportunistic for A. arapaparemains unclear and may be target for future observational andexperimental studies.

Acknowledgments.—We thank M. D. P. Recchia for help withthe map production; A. Eduardo and P. Gouvea helped duringfield sampling; H. Hoffmann and J. W. Streicher commented onearlier versions of the manuscript; IESB (Instituto de EstudosSocio Ambientais do Sul da Bahia, RPPN Nova Angelica) andM. A. Castro (RPPN Boa Uniao) provided field support;Instituto Chico Mendes de Conservacao da Biodiversidade(ICMBio) provided the collecting permit (13708-1). RLM andASFLS are thankful to Coordenacao de Aperfeicoamento dePessoal de Nıvel Superior (CAPES) for scholarships. LFTappreciates a grant provided by Fundacao de Amparo aPesquisa do Estado de Sao Paulo (FAPESP: 2008/50325-5) anda scholarship (2008/52847-9). MS thanks Conselho Nacional deDesenvolvimento Cientıfico e Tecnologico for a scholarship(CNPq: 483412/2010-4).

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Accepted: 22 April 2013.

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