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AIRNTTES

INTERNATIONAL JOURNAL OF BATRACHOLOGY

February 2011 Volume 27, N° 3

Alytes, 2011, 27 (3): 73-84.

Age profile in nine Mantella poison frogs

from Madagascar,

as revealed by skeletochronological analyses

Franco ANDREONE*, Cristina GIACOMA**, Fabio M. GUARINO ***,

Vincenzo MERCURIO **** & Giulia TESSA*

* Museo Regionale di Scienze Natural,

Via G. Giolitti, 36, 10123 Torino, Italy

<franco.andreone(@regione.piemonte.it>

** Dipartimento di Biologia Animale e dell Uomo,

Università degli Studi di Torino,

Via A. Albertina, 13,

10123 Torino, Italy

<cristina.giacoma@unito.it>

*** Università degli Studi di Napoli,

Dipartimento di Biologia Strutturale e Funzionale,

Via Cintia, 80126 Napoli, Italy

<fabio.guarino@unina.it>

**#** Museum für Naturkunde,

Leibniz-Institut für Evolutions- und Biodiversitätsforschung

an der Humboldt-Universität zu Berlin,

Invalidenstrafe 43,

10115 Berlin, Germany

<vincenzomercurio@gmx.de>

Skeletochronology has been successfully used to age temperate amphi-

bians, enabling comparisons of longevity and the age at sexual maturity. To

date, however, there have been few similar studies conducted using this

technique in tropical amphibians. Here we present data on age structure

and age at maturity for nine species of Malagasy Mantella frogs: M. baroni,

M. bernhardi, M. sp. aff. expectata, M. cowani, M. crocea, M. laevigata,

M. nigricans, M. pulchra and M. viridis. The genus Mantella includes

some of the most threatened frog species in Madagascar, and also some of

the most requested species for the international pet trade. The lack of basic

information on the life history of these species in the wild is hindering the

development of sustainable collection models. We analysed museum speci-

mens and bone samples of free g individuals collected during several

surveys in western and eastern Madagascar. AIl investigated species showed

a comparatively short longevity (0-4 LAGs) and sexual maturity was reached

on the 1° or the 2°“ year of life.

LOGTGGEC

INTRODUCTION

The island of Madagascar is one of the most extraordinary amphibian hot-spots in the

World: there are reliable estimated to be as many as 465 species, and many new taxa are being

Source : MNHN, Paris

74 ALYTES 27 (3)

described at a very rapid rate (ANDREONE et al., 2008; VIEITES et al., 2009). Even though major

progress has been made in describing the diversity of the Malagasy amphibian fauna, much

still remains to be understood about the ecology and life history traits of most species, and

about the practical implications for conservation.

One of the best known frogs of Madagascar are those belonging to the genus Mantella,

the Malagasy poison frogs. Currently, 16 species have been already described, and a few others

still wait for a formal description (GLAW & VENCES, 2007). Their fame is due mainly to their

bright aposematic colouration, their diurnal behaviour and the relative facility to keep them

in captivity (at least for some species), that make them among the most sought after frogs for

the international pet-trade (ANDREONE et al., 2006; GLAW & VENCES, 2007). So far, it is

commonly accepted that many Mantella species are threatened because of a combination of

narrow distribution, increasing deforestation and habitat degradation and intensive collec-

tion (ANDREONE et al., 20054). The most recent conservation assessment (ANDREONE et al.,

2008; ANONYMOUS, 2009) highlighted three species (M. aurantiaca, M. cowani and M.

milotympanum) as “Critically Endangered”, and four as “Endangered” (M. bernhardi, M.

crocea, M. expectata and M. viridis).

Whether the pet-trade could be a primary cause of conservation concern and

population/species decrease for amphibians is still matter of controversy and is worth of a

more in-depth investigations in the future. The impact of collection from the wild on most

Mantella species is still poorly understood and information on the breeding biology of species

is badly needed. The whole genus Mantella is now listed on CITES II (ANDREONE et al., 20054,

2006), and the trade is managed through a system of annual quotas (TEssA et al., 2009). In

terms of commercial exploitation, a review carried by RABEMANANJARA et al. (2008b) reported

a total of about 230,000 individuals exported from Madagascar between 1994 and 2003.

Although this number is quite low when compared to around two million Hymenochirus and

1.6 million Cynops orientalis referred to the importation trade for the USA in 1998-2002

(SCHLAEPFER et al., 2005), it still represents a considerable portion of traded amphibians,

capable of generating important economic benefits.

Seen all these aspects, it is our conviction that a special attention should be paid to

gathering life history data for most Mantella species, in order to assess a better comprehension

of the threats affecting the species. Population estimates, fecundity and age structure are

among the most important factors to be taken into consideration, and could help in drawing

the conservation profiles of the traded species.

Despite the commercial interest in the genus, there is little information on Mantella life

history traits in the wild (VENCES et al., 1999). Scattered information on longevity of

Malagasy frogs (especially mantellas and other traded species) are available from observa-

tions from captive individuals published in herpetoculturist papers and books (e.g., STANIS-

ZEWSKI, 2001), or as web-literature (CAREY & JUDGE, 2000). So far, the value in terms of

conservation utilisation of these data is highly questionable. First of all because they are often

reported in à non systematic way, then because the husbandry conditions are usually very

different from what is the reality in nature. For this reason we do not consider these data as

indicative of the real maximum longevity of a species.

A robust method used to assess longevity is skeletochronology (CASTANET, 1975). It has

been widely used for individual age determination (ANDREONE et al., 2002, 2005b; GUARINO et

Source : MNHN, Paris

ANDREONE et al. 75

al., 1998, 2008; Tessa et al., 2007; KUMBAR & PANCHARATNA, 2001). Here we report skeleto-

chronological data of nine Mantella species which significantly add to information already

available (GUARINO et al., 2008), and verify the congruence between maximum longevity and

age at sexual maturity.

MATERIAL AND METHODS

We analysed bone samples of the following Mantella species: M. baroni (15 males and

9 females; data from GUARINO et al., 2008); M. bernhardi (20 males and 12 females); M. sp. aff.

expectata (9 males and 6 females); M. cowani (14 males and 12 females; data from GUARINO et

al., 2008); M. crocea (13 males and 1 female); M. laevigata (5 males and 5 females);

M. nigricans (5 males and 5 females); M. pulchra (13 males, 12 females); and M. viridis

(20 males and 20 females). À complete list of the analysed specimens and their provenance is

given in tab. 1 and in app. 1. The individuals from the Isalo population, attributed to

M. betsileo by CROTTINI et al. (2008), are here considered as a still undescribed species,

M. sp. aff. expectata “South”, according to GLAW & VENCES (2007). The individuals attri-

buted to M. crocea populations (according to GLAW & VENCES 2007) were considered as M.

cf. milotympanum by Bora et al. (2008).

Frogs were sampled during the rainy season (October-March), when they are active and

show breeding habits. They were localized by sight and by acoustic emissions of males. Once

captured, they were sexed (males are usually smaller than females and often show femoral

glands, or have differential chromatic characters; see JovaNovIc et al., 2006), and measured

for snout-vent length (SVL, at the nearest 0.1 mm). For one species, M. bernhardi, the study

was partly conducted on phalanges taken from wild (non-captured) individuals and partly

from preserved specimens. In such a case, the third toe of each captured individual was eut in

the field, put in 90 % ethanol and then processed for skeletochronology and genetical analysis.

After toe-clipping, the specimens were released at the site of capture or conserved as museum

voucher specimens. For all the other species, the phalanx was taken directly from preserved

voucher specimens, now part of the herpetological collections of Museo Regionale di Scienze

Naturali, Torino, Italy (MRSN), and Parc Botanique et Zoologique de Tsimabazaza, Anta-

nanarivo, Madagascar (PBZT).

In M. bernhardi, we analysed separately individuals of two different populations which

differed for habitat conditions: the first one from a rather intact rainforest site (Mangevo)

within the Parc National de Ranomafana, and the second one from a heavily deforested site

(Ambohimandrozo) next to the presumed species’ type locality (RABEMANANJARA et al., 2005;

VIEITES et al., 2006).

The skeletochronological method followed the protocol used for other Malagasy amphi-

bians (GUARINO et al., 2008). Phalanges were decalcified in 3% nitric acid for 1 hour,

sectioned at 12 4m and stained in Ehrli haematoxylin for about 15 minutes. Finally, two

researchers observed independently the sections and counted the LAGs, using a light micros-

cope. In individuals sampled at the beginning of the rainy season (just after the latency

period), the last LAG is positioned close (sometimes coincident) to the external edge of the

Source : MNHN, Paris

76 ALYTES 27 (3)

Table 1. Data on provenance of samples of species of the genus Mantella analysed by

skeletochronology.

Snaci , " i P Peri

Species Sites Coordinates | Altitude Habitat proies

Mantella baroni Antoetra 203090 à | — 1400 |Montane fragmented rainforest| 1-112003

Mantella bernhardi Ambohimandrozo | 2122843: S | _ 600 | Secondary altered rainforest 1112004

Mantella bernhardi Mangevo = 500 Rainforest 11.204

Mantella cowani Antoetra PP aS p | = 1400 | Montane fragmented rainforest| 1:112003

Mantella paf. expectata Isalo Pan | 800 Savannah, dry forest XI-XI1.2004

Mantella crocea Ficrenana | 1634305 | 010 Rainforest XI12003

Mantella lacvigata Masoala Ron D | 615 Rainforest XI-XIL.1998-1999

Mantella migricans Masoala SOS |-S61s Rainforest XI-XII.1998-1999

Mantella pulchra Fierenana PE S | -910 Rainforest 1.1999

Maniella viridis Antongombato | 19523055 | -120 | Secondary forests, dry forest 12005

bone section because the maximal growth season has not yet started. In such cases we

considered the external border of the section as a LAG itself.

Then, in order to estimate age at sexual maturity, we followed the criterion of LAG

rapprochement as proposed by KLEINEBERG & SMIRINA (1969) and widely used by other

authors (e.g., FRANCILLON-VIEILLOT et al., 1990; LÉCLAIR et al., 2005; TsioRA & KYRIA-

KOUPOLOU-SKLAVOUNOU, 2002). Therefore, the first decreasing interval between LAGs, which

is supposed to indicate the attainment of sexual maturity, was identified for each section.

All numerical data were analyzed by Student's #-test. À probability level of P < 0.05 was

considered as significant. We compared the values (mean + standard deviation) of SVL,

maximum LAG number and number of LAGs at the sexual maturity for males and females

whose samples were greater than five individuals.

RESULTS

At a qualitative analysis the bone sections of all the studied species were similar and

composed of two concentric layers, which corresponded to the endosteal (the innermost) and

periosteal (the outermost) bone (Fig. 1). In the periosteal bone, we noticed contrasted

haematoxynophilic lines that were considered as reliable LAGs. In some individuals, similar

Source : MNHN, Paris

ANDREONE et al. HUE

380um

Fig. 1. — Histological section in the analysed Mantella species. Arrows indicate the lines of arrested

growth (LAGs). A: M. bernhardi, MRSN A3112, female with 2 LAGs, SVL =

af. expectata, MRSN A5234, male with 2 LA( VL=21.1 mm; C: M. laer À 53

male with 2 LAGs, SVL = 24.8 mm; D: M. pulchra, MRSN A3060, female with 2 LAGs,

SVL = 26.1 mm; E: M. viridis, MRSN A5082, female with 2 LAGs, SVL = 32.0 mm; F: M. viridis,

MRSN AS112, male with 1 LAGs, SVL = 25.1 mm. Abbreviations: endosteal bone; Mc,

medullar cavity; MI, metamorphosis line; Pb, periosteal bone.

Source : MNHN, Paris

78 ALYTES 27 (3)

lines were also visible in endosteal bone and thus corresponded to the periosteal LAGs.

Although a reversal line (the boundary between periosteal and endosteal bone) was not

always easy to detect, we assumed that the bone erosion did not delete any LAGs, assuming

the short longevity of these frogs. In addition, in 47.5 % of the specimens we detected the

presence of the metamorphosis line, a line visible near the reversal line occurring at the

passage from tadpoles to metamorphosed froglets.

AIl the species were small bodied (SVL 13-33 mm) and showed a comparatively short

life span (0-4 LAGs). Females were significantly larger than males, excepting for the

M. bernhardi population from Ambohimandrozo. In six species the mean LAG values were

higher in females than in males, but these differences were significant only for M. cowani.

Males and females reached sexual maturity the first or, less frequently, the second year, in all

the species (mean + SD = 1.37 + 0.31 years). The only exception was observed for

M. laevigata, in which the sexual maturity was attained at the second year in nine of the

10 individuals; in this species the longevity was two years, and thus sexual maturity coincided

with the life expectancy. In all the species except for M. pulchra, males reached sexual maturity

earlier than females, but the only species in which this difference was significant were M. aff.

expectata and M. viridis.

DISCUSSION

The data here presented represent the most exhaustive contribution on skeletochrono-

logy applied to a single tropical amphibian genus. Moreover, as stressed before, most of the

analysed Mantella specimens came from series held in collections of natural history museums.

So far, we advocate the importance of using preserved museum vouchers as a long-term

source of biological data, and this is not only useful, but also relevant in conservation terms,

since it maximises the amount of information that can be obtained from zoological collec-

tions (TESSA et al., 2009).

Our data also confirm that skeletochronology is reliable and successful for tropical

amphibians, despite of their provenience and ecology. All the studied species showed evident

LAGs, thus indicating that they observed a period of growth and a period of inactivity and

latency, as this was witnessed by the differential bone deposition and different chromophily in

bone sections. Although we cannot provide definitive conclusions about the life history of the

species because of the small sampled numbers, we noticed that all of the analysed frogs had a

short life span, and this could be put in relation with their small body size. Skeletochronol-

ogical studies on anurans utilizing both sexes show that in most species there is a positive

correlation between body size and age both in males and females (RYSsER, 1988; ESTEBAN et al.,

1996, 1999). Moreover, there is often a wide size overlap among age classes even if body length

and age are positively correlated.

Our results for nine Mantella species are consistent with longevity patterns observed in

other amphibians of Madagascar, such as Boehmantis microtympanum (GUARINO et al.,

1998), Dyscophus antongilii (TESSA et al., 2007) and Boophis tsilomaro (ANDREONE et al.,

2002). These species are much larger than mantellas, all exceeding 80 mm (with a body size

Source : MNHN, Paris

ANDREONE et al. 79

record in D. antongili of 110 mm), and reach a maximum age of 11 years (in B. microtympa-

num and B. tsilomaro). In the Mantella species, the body miniaturisation, which is associated

to mirmecophagy, diurnal activity, and poison segregation at skin level (see VENCES et al.,

1998), is a limit for their maximum life expectancy that does not exceed four years in the wild.

In six species, males had a shorter longevity than females, but this difference was

significant only for M. cowani. This population comes from a high plateau site at around

1400 m a.s.1. (GUARINO et al., 2008) In particular, males of this species showed short mean

longevity, with 1.2 + 0.2 LAGs, while females had 2.2 + 0.2 LAGs. So far, we assume that

females can effectively live more than males, and reach a larger body size, as shown in tab. 2.

‘We do not have sound explanations for such a difference, but we may hypothesise that females

carry out a much more hidden life, and thus are less subject to predation, this leading to a

differential mortality between the sexes.

We also presented information about the age at sexual maturity from skeletochronology.

This was reached quite early (< 1-2 years) in all the examined species, except for M. laevigata.

This arboreal species (GLAW & VENCES, 2007) showed a different age profile, with sexual

maturity reached at two years in all the examined individuals. Unfortunately, our sample was

too small to draw such a significant explanatory hypothesis, but, probably, in this species the

majority of the individuals reproduce after two years of age and possibly die just after. Most

likely, the delay in reaching sexual maturity could allow to get a larger size that can be useful

in males for the male-male fights over defended resources necessary for reproductive success

and in females for maternal care (HEYING, 2001). More studies are needed on this species to

understand whether this difference is constant and which could actually be the advantages for

both sexes.

In general, males reach sexual maturity earlier than or at the same age as females, but the

only significant differences were found in M. sp. aff. expectata (1.2 + 0.1 versus 1.3 + 0.2

LAGs) and in M. viridis (1.0 + 0.0 versus 1.1 + 0.1 LAGs). Notably, these are the only two

species from open grassland habitats, with accentuated seasonality (TEssA et al., 2009).

In several anuran species, the sexes reach sexual maturity at the same age (ESTEBAN et al.,

2004), whereas in others females reach sexual maturity later than males (CHERRY & FRAN-

CILLON, 1992). These data may be explained by the fact that females start breeding when they

reach a minimum body size to maximize clutch mass (CHERRY & FRANCILLON, 1992; ESTEBAN

et al., 1996). On the other hand, in anuran females delayed maturity often means a larger body

size and higher fecundity (Gi8Bons & MCCARTHY, 1984), and sexual selection for larger body

size in females occurs when it represents an important determinant of female reproductive

success.

The age profile can also provide information on the conservation status of the studied

species, as witnessed by the two studied M. bernhardi populations, which showed a different

LAG number profile. The individuals from Mangevo, which is a rather intact rainforest,

showed a comparatively larger body size and a longer life than those from the increasingly

deforested site of Ambohimandrozo (SVL: males: 1 = 1.88, P < 0.05; females: 1 = 4.44,

P <0.05; LAGs: males: { = 1.05, P < 0.05; females: 1 = 2.03, P > 0.05). Instability of habitat

quality and the intense degradation following anthropogenic may be invoked as a cause to

decrease population viability.

Source : MNHN, Paris

ALYTES 27 (3)

Table 2. - Data on body size (SVL in mm), longevity (LAG numbers) and age at sexual maturity (given as

LAG numbers, largely corresponding to years) in the analysed species. Values are provided as mean

4 standard deviation. The numbers between round brackets refer to the number of analysed

specimens, whereas the values between square brackets are the extreme range values; 1, Students

value; asterisked values are significantly different for P < 0.05 (*) or for P < 0.01 (**).

Maximum | LAGs at

Species Sex SvL ’ numberof | 4 sexual ’

LAGs maturity

Males (15) 1.64 0.2 1.405

fantella be en [13] [1-2]

Mantella baroni er 348: Sao 1.07 14405 0.09

“0 110

[a LS + 0.6 13 + 0.

Mantella bernhardi Mass (10) ; 1-31 , {21

(Mangevo) Females (2) 25407 po À

re 10400

Mantella bernharaï Mass (10) 071205 | 4 pa il Mr

(Ambohimandroz0) Eagles (10) | 2204 12 ‘ é 11403 À

FU [181-218] [1-2]

Mass (14) 25.74 1.7 10404

Mantella cowani 6.29%% 7.86%* ï ss 3 2.01

Females (12) (1-2)

1240.

Males (13) 2

Mantella crocea dé à : - (ral ;

Female (1) ps Pl]

ea 20.94 1.5 1240.

Mantella sp af Mes 187233) | 4 53e 026 [1-21 236

dis Females (6) 24.04 1.0 d 13402 2.36

123.0-25.3] [1-2]

242405 20400

Mantella k es 12372481 | a gjes 0.99 1

lantella lacvigata Re État 0 20260 0.00

12]

12401

Mantella nigric Pere 1241-2601 | 4 gg 13 [1-2]

lantella nigricans Mère en RE TE 0.00

IS 126.5-28.3] [1-2]

Males (13) 20.6 2.1 164 0.1

-2

Mantella pulchra 3.63** 0.73 1 pal 2 1.07

Females (12 5402

Females (12) | 313.282 fi

Males (20) 25.942.1 1.0 + 0.0

Mantella viridis 842 18! , w l y |aore

Females (20) U21

Our final consideration goes to the advantage of putting together a series of integrative

data for conservation purposes. In particular, for the genus Mantella, the data on age

structure, longevity and age at sexual maturity here presented represent a crucial complement

to those on fecundity, distribution and population consistency (e.g., RABEMAMANJARA et al.,

2008a; TEssa et al., 2009). AIT these parameters could be usefully utilised to test extinction

probability of species and populations 4

sociated to the different threat causes using popula-

tion viability analyses. In particular, by comparing the survival probability of threatened

Source : MNHN, Paris

ANDREONE et al. 81

species in relation to different pet-trade collection pressures may provide indications about the

sampling limit for national and international trade. On the occasion of future works,

longevity data should be integrated with data on the type and the state of the habitat, and the

fragmentation and the density of each harvested population, so to implement tailored

conservation programs.

ACKNOWLEDGEMENTS

We are indebted to the Parc Botanique et Zoologique de Tsimbazaza and the Direction des Eaux et

Forêts for permissions to visit the protected areas and for collecting the preserved animals. The fieldwork

was financially supported by DAPTF, Amphibian Specialist Group, Acquario di Genova, Madagascar

Fauna Group, Nando Peretti Foundation, Gondwana Conservation and Research, Van Thienhoven

Foundation, and Wildcare Institute. Thanks to two anonymous referees for their useful comments.

LITERATURE CITED

ANONYMOUS [IUCN], 2009. - JUCN Red list of threatened species. Version 2009.2. <http//www.

iucnredlist.org>.

ANDREONE, F., CADLE, J. E., COX, N., GLAW, F., NUSSBAUM, R. A., RAXWORTHY, C. J., STUART, S. N

VALLAN, D. & VENCES, M., 20054. — Species review of amphibian extinction risks in Madagascar:

ions from the Global Amphibian Assessment. Conservation Biology, 19: 1790-1802.

CARPENTER, À. [., Cox, N., DU PREEZ, L., FREEMAN, K., FURRER, S., GARCIA, G., GLAW,

LOS, J., KNOX, D., KÔHLER, J., MENDELSON IT, J. R., MERCURIO, V., MITTERMEIER, R. A.,

Moorë, R. D., RABIBISOA, N. H. C., RANDRIAMAHAZO, H., RANDRIANASOLO, H., RASOAMAMPIO-

NONA RAMINOSOA, N., RAVOAHANGIMALALA RAMILUAONA, O., RAXWORTHY, C. J., VALLAN, D.,

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Corresponding editor: Stéphane GROSIEAN.

APPENDIX |

LIST OF MANTELLA SPECIMENS USED FOR SKELETOCHROLOGICAL ANALYSIS

Abbreviations: MRSN, specimens housed in the Museo Regionale di Scienze Naturali, Torino:

PBZT, specimens housed in the Parc Botanique et Zoologique de Tsimbazaza, Antananarivo; Prov.,

Province; AA, surroundings of Antongombato and Montagne des Français; 1M, Isalo Massif: MP,

Masoala Peninsula.

Mantella bernhardi Vences, Glaw, Peyrieras, Bôhme & Busse, 1994. - 7 unnumbered phalanges

collected from wild individuals (Mangevo, Fianarantsoa Prov., 8.11.2004); MRSN A3112-3116 (Man-

gevo, Fianarantsoa Prov., 8.11.2004); MRSN A3042, 12 phalanges, PBZT (two unlabelled specimens,

Ambohimandrozo, Fianarantsoa Prov., 15.11.2004).

Mantella sp. aff. expectata Busse & Bôhme, 1992. - MRSN A5232-5233, A5325 (Antoha, IM,

Fianarantsoa Prov., 3.X11.2004); MRSN A5223, A5225, A5228-5229, A5231, A5234-5236, A5238

(Tsitorina, IM, Fianarantsoa Prov., 3.X11.2004); MRSN A5237, A5239 (Kazofoty, IM, Fianarantsoa

Prov., 2.XI1.2004); MRSN A5230 (Sakavato, IM, Fianarantsoa Prov., 6.X11.2004).

Mantella crocea Pintak & Bôhme, 1990. - PBZT unlabelled, likely Fierenana, Toamasina Prov.

Mantella laevigata Methuen & Hewitt, 1913. - MRSN A4475 (Antsarahan'Ambararato, MP,

Antsiranana Prov., 4.XI1.1999); MRSN A4533, A3000 (Andasin'i Governera, MP, Antsiranana Prov.,

6.XI1.1998); MRSN A4531-4532 (Andasin'i Governera, MP, Antsiranana Prov., 7.XI1.1998); MRSN

A3001-3002 (Andasin’i Governera, MP, Antsiranana Prov., 9.XI1.1998), MRSN A2999 (Bchanjada, MP,

Antsiranana Prov., 22.X1.1999); MRSN A4505-4506 (Menamalona, MP, Antsiranana Prov.,

11.XI1.1999).

Mantella nigricans Guibé, 1978. - MRSN A4457 (Andasin'i Governera, MP, Antsiranana Prov.,

5.XI1.1998); MRSN A4467 (Ambatoledama, MP, Antsiranana Prov., 17.X1.1998); MRSN A4454

(Ambatoledama, MP, Antsiranana Prov., 16.X1.1998); MRSN A4508 (Antsarahan’Ambararato, MP,

Source : MNHN, Paris

84 ALYTES 27 (3)

Antsiranana Prov., 30.1X.1999); MRSN A4472 (Antsarahan’Ambararato, MP, Antsiranana Prov.,

29.X1.1999); MRSN A4456 (Behanjada, MP, Antsiranana Prov., 17.X1.1998); MRSN A4480 (Menama-

lona, MP, Antsiranana Prov., 11.X11.1999); MRSN A4481 (Menamalona, MP, Antsiranana Prov.,

15.XI1.1999); MRSN A4482 (Menamalona, MP, Antsiranana Prov., 11.XI1.1999); MRSN A4503

(Menamalona, MP, Antsiranana Prov., 15.XI1.1999).

Mantella pulchra Parker, 1925. - PBZT unlabelled, Fierenana, Toamasina Prov.; MRSN A3060-

3062 (Corridor bethween Moramanga and Zahamena, Tamatave Prov., 10.1.1999); MRSN A2753, 2754

(An'Ala, Tamatave Prov., 1.111.2003), MRSN A59(2-4) (An'Ala, Tamatave Prov., 4.1.1992); MRSN

A4487, A4489 (Andasibe surroundings, Tamatave Prov., 1.1.1995).

Mantella viridis Pintak & Bôhme, 1988. - MRSN A5055, A5073, A5077 (Ambovomany, AA,

Antsiranana Prov., 15.1.2005); MRSN AS102, A5112 (Ambodimanga, AA, Antsiranana Prov.,

17.1.2005); MRSN A5064, A5070, A5076, A5094 (Andamanga, AA, Antsiranana Prov., 4.1.2005);

MRSN A5075, A5080-5081, A5095, A5097, A5106 (Andronotsimety Ambiney River, AA, Antsiranana

Prov., 8.1.2005);, MRSN A5095, A5117 (Andohenimangoko, AA, Antsiranana Prov., 15.1.2005); MRSN

A5056 (Anketrabe, AA, Antsiranana Prov., 6.1.2005); MRSN A5066 (Anosiravo, AA, Antsiranana

Prov., 24.1.2005); MRSN A5088 (Antonboko, AA, Antsiranana Prov., 6.1.2005); MRSN A5054, A5096

(Anjanaharibe, AA, Antsiranana Prov., 8.1.2005); MRSN A5050, A5052, A5067 (Antonboko, AA,

Antsiranana Prov., 21.1.2005); MRSN A5115 (La Mere Rouge, AA, Antsiranana Prov., 7.1.2005);

MRSN A5113-5114, A5124, A5127 (Maleja, AA, Antsiranana Prov., 7.1.2005); MRSN A5063, AS121

(Mabhatsinjo, AA, Antsiranana Prov., 17.1.2005); MRSN A5107 (Porchuite, AA, Antsiranana Prov.,

8.1.2005); MRSN A5060 (Tsimanankaratre, AA, Antsiranana Prov., 8.1.2005); MRSN A5082 (Tegnan

Antshampano, AA, Antsiranana Prov., 8.1.2005); MRSN AS5100 (Tsimanankaratre, AA, Antsiranana

Prov., 8.1.2005).

OISSCA 2011

Source : MNHN, Paris

Alytes, 2011, 27 (3): 85-115. 85

Tadpole morphology and

table of developmental stages

of Polypedates teraiensis (Dubois, 1987)

Paramita CHAKRAVARTY*, Sabitry BORDOLOI*, Stéphane GROSIEAN**,

Annemarie OHLER** & Aparajita BORKOTOKI***

* Resource Management and Environment Division.

Institute of Advanced Study in Science and Technology,

Paschim Boragaon, Guwahati 781035, Assam, India

<paramitachakravarty@gmail.com>: <sabitrybordoloi@rediffimail.com>

** Reptiles et Amphibiens, UMR 7205 OSEB,

Département de Systématique et Evolution, Muséum national d'Histoire naturelle,

25 rue Cuvier, CP 30, 75005 Paris, France

<sgrosjea@mnhn.fr>; <ohler@mnhn.fr>

***_ Department of Zoology, Gauhati University, Jhalukbari, Guwahati 781014, Assam, India

<a_borkotoki@yahoo.com>

Breeding specimens of Polypedates teraiensis are commonly seen

during monsoon among vegetation near lentic water bodies in Assam,

northeastern India. Early life history stages, the normal development, is

described and illustrated based on Gosner’s (1960) 46 developmental

stages. The morphology and the buccal features of a stage 38 tadpole are

described in detail and illustrated. At ambient temperature (26°C to 32°C),

completion of the entire development from ovum fertilization up to emer-

gence of the froglet took 58 days (1392 hours). À comparison with larvae of

congeneric species is provided, including a discussion on the advantages of

their embryonic development in a foam nest.

INTRODUCTION

Polypedates leucomystax (Gravenhorst, 1829) has long been thought to be a very widely

distributed species. Modern methods, such as bioacoustics and molecular techniques, allowed

recognizing cryptic species (e.g., MaTsuI et al., 1986; Nains et al., 1998). Taxonomic

revisions of this species complex remain to be done in various parts of its range. They will

likely result in description of new species (BROWN et al., 2010). This complex has not been

well-studied in northeastern India where at least six species are currently recognized: Polype-

dates assamensis Mathew & Sen, 2009; Polypedates maculatus (Gray, 1830); Polypedates

megacephalus Hallowell, 1861; Polypedates subansiriensis Mathew & Sen, 2009; Polypedates

taeniatus (Boulenger, 1906); and Polypedates teraiensis (Dubois, 1987). The status of Polype-

dates maculatus himalayensis (Annandale, 1912), which is either considered synonym of

P. maculatus, P. leucomystax or P. teraiensis (FRosT, 2010 [http://research.amnh.org/vz/

Source : MNHN, Paris

86 ALYTES 27 (3)

herpetology/amphibia/; accessed on 24“ April 2010)]), a subspecies of P maculatus (ANNAN-

DALE, 1912; Dugois, 1987), or a valid species (AHMED et al., 2009; MATHEW & SEN, 2009)

remains to be solved. Adults of P teraiensis are morphologically closer to Polypedates mutus

(Smith, 1940) than to P leucomystax (Dusois & OHLER, pers. comm.). Adults of P teraiensis

and P mutus are large, have co-ossified skulls, have always longitudinal stripes on their backs,

and large spots on back of thighs. However, P teraiensis has vocal sacs whereas they are

absent in P mutus (DuBois, 1987; DuBois & OHLER, pers. comm.). Additional characters of

adult morphology are particularly needed to understand this difficult group. Tadpole mor-

phology and development is one of the most important life history traits that could add

important information to our knowledge of this genus. Among the species of Polypedates

occurring in northeastern India, only the larvae of P maculatus and P. megacephalus have

been previously described (MOHANTY-HEIMADI & DUTTA, 1988; CHou & Lin, 1997).

Normal tables of development are very useful for studies of comparative development as

well as for a variety of experimental and descriptive studies on any species. Normal develop-

mental tables are available for the following Indians anurans: (1) Dicroglossidae: Hoplobatra-

chus tigerinus (Daudin, 1802) (KHAN, 1969; AGARWAL & Niazi, 1977), Fejervar ya “limnocha-

ris (Gravenhorst, 1829)” (Roy & KHARE, 1978) and Euphlyctis cyanophlyctis (Schneider,

1799) (KumaR, 1982); (2) Hylidae: Hyla annectans (Jerdon, 1870) (Ao & BoRDOLOI, 2001).

Partial developmental tables are available for the following Indian Rhacophoridae: P “leu-

comystax"” (KIYASETUO & KHARE, 1986), P maculatus (MCCANN, 1932; MOHANTY-HEJMADI

& Durra, 1988) and Rhacophorus malabaricus Jerdon, 1870 (SEKAR, 1990). Some develop-

mental data were provided for the dicroglossid Sphaerotheca bre (Schneider, 1799) and

the microhylid Uperodon systoma (Schneider, 1799) (MoHANTY-HEsmaDI et al., 19794-b).

Herein, we describe and illustrate the embryological and larval development of Polype-

dates teraiensis throughout the 46 stages of GosnEr’s (1960) standard table. Furthermore we

describe the morphology and buccal anatomy of a stage 38 tadpole. Completion of the whole

development from ova fertilization to froglets took 58 days (1392 hours) at a room tempera-

ture ranging from 26°C to 32°C.

MATERIAL AND METHODS

Amplecting adults of Polypedates teraiensis were collected at various dates between

2" February 2002 and 17" August 2006 at different sites of Guwahati city (Assam state,

northeastern India). Amplecting pairs were subsequently transferred to glass aquaria (60 x 45

* 45 cm, with 20 em of water and sloping sand on one side) where they laid eggs in a foam nest

within 12 hours. Our data are based on five clutches, laid by five different pairs, that were kept

until the end of metamorphosis. The eggs were reared under laboratory conditions and the

entire development was recorded. Each clutch was reared in a separate aquarium, the number

of individuals decreasing subsequently as larval samples were taken and fixed for description

of the developmental process and as voucher for the developmental table. Tadpoles were fed

plankton and algae (mostly Spirogyra ssp.) from natural habitat. Specimens were preserved in

8 % formaldehyde solution and stored in the herpetological collection at the Museum of the

Source : MNHN, Paris

CHAKRAVARTY et al. 87

Institute of Advanced Study in Science and Technology of Guwahati, under collection

numbers IASST.AT.731-IASST.AT.1170. Staging follows Gosner (1960). Sampling was

repeated for three successive years and the average data are presented herein. Only stages 16

and 19 were not collected. Morphological terminology follows ALTIG & MCDIARMID (1999)

and Keratodont Row Formula (KRF) follows Dugois (1995). Measurements were taken on

preserved specimens. The stage 38 tadpole description is provided separately. The measure-

ments, done with the help of a dial vernier calliper, are given to the nearest 0.1 mm.

Morphological landmarks follow ALTIG & MCDiarMiD (1999: 26, fig. 3.1.) and GROSIEAN

(2006) except for FLL, HH, HL, HLL, SE, SpE and SpN. Study of the buccopharyngeal

anatomy was done with a Scanning Electron Microscope (SEM) model No. JSM-6360 at the

North Eastern Hill University (NEHU), Shillong (India). The terminology of buccal struc-

tures follows WAssERSUG (1976).

ABBREVIATIONS

BH, maximum body height; BW, maximum body width; ED, maximum eye diameter;

FLL, forelimb length; HH, maximum head height; HL, head length (from tip of snout to

posterior margin of eye); HLL, hind-limb length (from insertion of limb to tip of 4!" toe);

IOD), interorbital distance (distance between the centres of the pupils); KRF, keratodont row

a; MTH, maximum tail height; NP, nare-pupil distance (from centre of nare to centre

of pupil); NN, internarial distance; ODW, oral disc width; SE, snout-eye distance (from tip of

snout to anterior edge of eye); SN, snout-nare distance; SPE, spiracle-eye distance (from

opening of spiracle to centre of pupil); SpN, spiracle-nare distance (from opening of spiracle

to centre of nare); SSp, distance from tip of snout to opening of spiracle; SVL, snout-vent

length; TAL, tail length; TL, total length.

RESULTS

NATURAL HISTORY AND PHYSICO-CHEMICAL ANALYSIS OF TADPOLE HABITAT

Polypedates teraiensis begins to breed early in the year. It breeds sporadically after the

first few rains of the rainy season, usually in the month of March. Normally, the frogs produce

foam nests that are attached to vegetation above shallow temporary waters. However, foam

nests have been observed on logs or walls of human habitations far from water; these foam

nests were desiccated or decayed. Foam nests or tadpoles were never found in running water.

The following physico-chemical characteristics were noted. In the present study the value of

dissolved oxygen was between 3.3 and 7.4 mg/l and that of free CO, was between 1.7 and

6.2 mg/l; total alkalinity was between 51 and 84 mg/l and total hardness was between 20 and

59 mg/1. The values of dissolved oxygen and free carbon dioxide are highly variable as they are

greatly influenced by the decomposition process.

Source : MNHN, Paris

88 ALYTES 27 (3)

DEVELOPMENTAL TABLE

The clutch size of the five nests was 67, 114, 127, 120 and 75 eggs (x = 100.6 + 27.6). The

eggs were uniformly white in colour. Eggs on the outermost surface of the foam nest

sometimes did not develop and turned pale yellow due to desiccation.

Stages 1 to 19 were completed within the foam nest. The embryos hatch at stage 20 and

stay within the nest until stage 22 when they drop down in water to complete metamorphosis.

The characteristics of each stage are presented below.

1. Gosner Stage I (fig 1)

Age.-0h.

Diameter. — 2.0-2.2 mm.

Characters. - Fertilized egg, spherical in shape. Egg uniformly white in colour.

2. Gosner Stage 2

Age. -0 h 50.

Diameter. — 2.0-2.2 mm.

Characters. - One cell stage, just before the start of cleavage.

3. Gosner Stage 3 (fig. 2)

Age.-2h25.

Diameter. — 2.0-2.2 mm.

Characters. — Two cells stage. Start of cleavage: the meridian cleavage furrow originates

at the animal pole and proceeds to the vegetal pole, dividing the egg completely into two equal

blastomeres.

4. Gosner Stage 4 (fig. 3)

Age.—-3h 10.

Diameter. — 2.0-2.2 mm.

Characters. — Four cells stage. The second meridian furrow, which starts at the animal

pole, extends to the vegetal pole at a right angle to the first.

5. Gosner Stage 5 (fig. 4)

Age.-3h 55.

Diameter. — 2.0-2.2 mm.

Characters. - Eight cells stage. The third cleavage is horizontal, slightly above the

equator, forming eight blastomeres, four smaller micromeres in the animal pole and four

bigger macromeres in the vegetal pole.

6. Gosner Stage 6 (fig. 5)

Age. -4h 35.

Diameter. — 2.0-2.2 mm.

Characters. — 16 cells stage. The cleavage furrow is vertical. First the micromeres

are divided into eight cells, resulting in twelve cells in total (eight micromeres and four

Source : MNHN, Paris

CHAKRAVARTY et al. 89

Fig. 1. - Gosner Stage 1 Fig. 2. - Gosner Stage 3 Fig. 3.- Gosner Stage 4

Fig. 4. — Gosner Stage 5. Fig. 5. - Gosner Stage 6. Fig. 6. - Gosner Stage 7.

Fig. 7. Gosner Stage 8. Fig. 8. — Gosner Stage 9 Fig. 9. - Gosner Stage 11

Fig. 10.- Gosner Stage 13 Fig. 11.- Gosner Stage 14 Fig. 12. - Gosner Stage 17.

Fig. 1 to 12. - Developmental stages 1-17 (GosNER, 1960) of the embryo of Polypedates teraiensis.

Source : MNHN, Paris

90 ALYTES 27 (3)

macromeres). This is followed by the division of the four macromeres as the cleavage furrow

reaches the vegetal pole, resulting in 16 cells.

7. Gosner Stage 7 (fig 6)

Age.-5h35.

Diameter. — 2.0-2.2 mm

Characters. — 32 cells stage. The latitudinal cleavage furrows of the micromeres and

macromeres result in the formation of 16 micromeres and 16 macromeres.

8. Gosner Stage 8 (fig. 7)

Age.-8h.

Diameter. — 2.0-2.2 mm.

Characters. - Morula stage. Cell proliferation increases the embryo to more than 64 small

blastomeres. The surface of the animal pole resembles a cluster of beads.

9. Gosner Stage 9 (fig. 8)

Age. 9 h 56.

Diameter. — 2.0-2.2 mm.

Characters. — Blastula stage. The blastomeres are minute in size and the surface of the egg

appears granular.

10. Gosner Stage 10

Age.-16h.

Diameter. — 2.0-2.2 mm.

Characters. — Early gastrula stage. The dorsal lip of the blastopore has formed and is

crescent-shaped. The zone of the vegetal hemisphere is reduced due to migration (epiboly) of

the micromeres towards the vegetal pole.

11. Gosner Stage 11 (fig 9)

Age.-19h.

Diameter. — 2.0-2.2 mm.

Characters. - Mid: rula stage. The epibolic migration of micromeres over the vegetal

pole reduces the exposed area of macromeres, which is surrounded by the lateral lips of the

semicircular or horse shoe shaped blastopore.

12. Gosner Stage 12

Age.-21h.

Total length. - 2.0-2.3 mm.

Characters. — Late gastrula stage. The blastopore, initially ventral, becomes the posterior

pole of the antero-posterior axis.

13. Gosner Stage 13 (fig 10)

Age. -24h.

Total length. - 2.0-2.3 mm.

Source : MNHN, Paris

CHAKRAVARTY et al. 91

Characters. — The embryo is slightly elongated. A ridge is observed on one side. The

protruding plug of yolk cells gradually disappears and the neural plate develops as a tubular

area along the dorsal surface.

14. Gosner Stage 14 (fig 11)

Age. -36h.

Total length. — 2.0-2.4 mm.

Characters. - Embryo elongate, slightly oval. Neural fold present: elevation of two lateral

ridges separated by the neural groove.

15. Gosner Stage 15

Age.- 56h.

Total length. — 2.0-2.6 mm.

Characters. —- Embryo oval in shape. Period of active ciliary rotation, during which the

neural groove narrows and the folds approach each other.

16. Gosner Stage 17 (fig. 12)

Age.-62h.

Total length. — 2.2-2.8 mm.

Characters. - Appearance of tail bud at the posterior tip of the embryo which is wider

than long.

17. Gosner Stage 18 (fig 13)

Age.-71h.

Total length. 2.9-3.1 mm.

Characters. - Head region well defined with optic and gill plates bulges. Body elongated,

tail bud elongate and rolled up around the body. This stage is recognized by the initiation of

muscle contraction.

18. Gosner Stage 20 (fig. 14)

Age. -104h.

Total length. —4.7-5.3 mm.

Characters. —- The embryos hatch but the larvae remain within the nest. Large yolk

reserve. Tail prominent, slightly curved ventrally. Gills distinct.

19. Gosner Stage 21 (fig. 15)

Age.-118h.

Total length. — 6.8-7.7 mm.

Characters. — Tail fins opaque. The yolk reserve is quite large and elongated. Eyes

distinct, cornea transparent. Gills developing. Very light pigmentation on the dorsal side but

not around the eyes.

Source : MNHN, Paris

92 ALYTES 27 (3)

mé

Fig. 13.- Gosner Stage 18. Fig. 14. - Gosner Stage 20. Fig. 15.- Gosner Stage 21.

Fig. 16.- Gosner Stage 22. Fig. 17. - Gosner S

Fig. 18. - Gosner Stage 24.

Fig. 19. - Gosner Stage 25. Fig. 20. - Gosner Stage 26. Fig. 21. - Gosner Stage 27.

Fig. 22. - Gosner Stage 28. — Gosner Stage 31.

Fig. 2 Fig. 24, - Gosner Stage 32.

Fig. 13 10 24. - Developmental stages 18-32 (GosnR, 1960) of the tadpole of Polypedates teraiensis.

Source : MNHN, Paris

CHAKRAVARTY et al. 93

20. Gosner Stage 22 (fig. 16)

Age. - 140 h.

Total length. — 7.0-7.7 mm.

Characters. — The tadpole drops in water. The tail fins are transparent and blood

circulation within them begins. The yolk reserve is quite large and elongated. Eyes distinct.

Gills very well developed. Light pigmentation on the dorsal side but not around the eyes.

Upper and lower labial fringes develop, but without papillae.

21. Gosner Stage 23 (fig. 17)

Age.-162h.

Total length. — 8.2-10.4 mm.

Characters. — Yolk still visible but reduced. Stomach region less bulging. Developing

operculum, with gills projecting below it. Papillae start developing on the upper and lower

labial fringes. Darker pigmentation on dorsal side. Pigmentation extended up to the end part

of the tail but gradually becoming lesser. No pigmentation around the eyes. Vent closed.

22. Gosner Stage 24 (fig. 18)

Age.—179h.

Total length. — 10.6-10.9 mm.

Characters. -Yolk still present. Gills reduced. Operculum closed on the right side, gills on

the left side distinct. Upper and lower jaw sheaths are developing. A faint row of upper

keratodonts develops, the future uppermost row Al. Tail tip pointed. Dark pigmentation on

the dorsal side, lighter on tail. Pigmentation on the ventral side just above the yolk plug and

in the region of the mouth.

23. Gosner Stage 25 (fig. 19)

Age. 197h.

Total length. — 11.4-12.9 mm.

Characters. - Gills disappeared, operculum closed. A faint line corresponding to the

opening of the spiracle can be seen. Upper and lower jaw sheaths developed. Serrations of the

jaw sheaths not distinct. KRF 1:1+1/1+1:2. Digestive tract with three loops. Dorsal side

darkly pigmented, lighter on the ventral side and on the end of the tail.

24. Gosner Stage 26 (fig. 20)

Age. —312h (13 days).

Total length. - 20.6-23.1 mm.

Length of hind-limb. — 0.17-0.23 mm.

Characters. — Hind-limb bud visible, its length is half of its diameter. Definitive KRF

1:3+3/1+1:2 reached. Pigmentation all over the dorsal side except around the eyes.

Source : MNHN, Paris

94 ALYTES 27 (3)

25. Gosner Stage 27 (fig. 21)

Age. — 360 h (15 days).

Total length. — 17.8-27.3 mm.

Length of hind-limb. — 0.32-0.47 mm

Characters. - The length of the hind-limb bud is equal to its diameter. Tail muscle well

developed. Oral papillae well developed and slightly pigmented. Dark pigmentation on the

dorsal side with a dark transversal band in the centre of the dorsal side.

26. Gosner Stage 28 (fig. 22)

Age. -432h (18 days).

Total length. — 20.6-23.1 mm.

Length of hind-limb. — 0.71-0.89 mm.

Characters. - Limb bud elongated, equal or longer than its diameter, its distal end slightly

conical. Keratodonts distinct. Pigmentation on the ventral side just above the intestinal coil.

27. Gosner Stage 29

Age. — 456 h (19 days).

Total length. — 20.6-28.8 mm.

Length of hind-limb. — 0.71-1.18 mm.

Characters. — Length of limb equals to one and half times its diameter. Distal end of limb

bud conical. Pigmentation on the ventral side extending near the mouth.

28. Gosner Stage 30

Age. — 468 h (19.5 days).

Total length. -23.1-30.1 mm.

Length of hind-limb. — 0.7-1.90 mm.

Characters. - Length of limb bud equals to twice its diameter. Distal half of conical limb

bud bends slightly ventrally. Digestive tract with four loops.

29. Gosner Stage 31 (fig. 23)

Age. - 480 h (20 days).

Total length. — 28.4-31.7 mm.

Length of hind-limb. — 1.5-1.8 mm.

Characters. — Hind-limbs paddle shaped. Pigmentation lesser compared to the earlier

stages but concentrated.

30. Gosner Stage 32 (fig. 24)

Age. — 642 h (26 days).

Total length. — 26.1-30.5 mm.

Length of hind-limb. — 1.5-1.8 mm.

Characters. — The edge of the foot paddle becomes indented on the dorsal side, which

marks the development of the 4!" and 5!” toes.

Source : MNHN, Paris

CHAKRAVARTY et al. 95

31. Gosner Stage 33

Age. - 672 h (28 days).

Total length. — 29.6- 33.0 mm.

Length of hind-limb. — 1.5-2.4 mm.

Characters. — The edge of the foot paddle becomes indented behind the prominence of

4% toe, which marks the 3", 4 and 5" toes. Pigmentation much lesser.

32. Gosner Stage 34 (fig. 25)

Age. — 720 h (30 days).

Total length. — 31.2-35.6 mm.

Length of hind-limb. — 1.5-3.9 mm.

Characters. - The edge of the foot paddle becomes indented, on the ventral side, behind

the prominence of 3 toe, which marks the prominence of 2%, 3", 4" and 5" toes.

Pigmentation darker than in the previous stage.

33. Gosner Stage 35 (fig. 26)

Age. — 768 h (32 days).

Total length. — 33.3-38.7 mm.

Length of hind-limb. — 1.8-3.9 mm.

Characters. - The edge of the foot paddile is indented behind the 2" toe, demarcating the

prominence of the 1“ toe. AII the five toes are separated from each other. Digestive tract with

five loops. Pigmentation negligible on the ventral side. Pigmentation uniform on the dorsal

side with a distinct longitudinal dark line in the middle.

34. Gosner Stage 36

Age. — 864 h (35 days).

Total length. — 34.9-40.6 mm.

Length of hind-limb. — 2.12-5.0 mm.

Characters. - Margin of the 5!" toe web directed towards the tip of the 2"! toe. Knee joint

formed.

35. Gosner Stage 37 (fig. 27)

Age. — 936 h (39 days).

Total length. - 42.4-45.2 mm.

Length of hind-limb. — 7.4-9.9 mm.

Characters. - The margin of the 5" toe web is directed towards the tip of the 1" toe.

Toe tips rounded. Webbing of feet distinct between 1“ and 2° toes as well as between 2"! and

3" toes. Dark pigmentation on the dorsal side and on the tail region, fins pigmented.

Source : MNHN, Paris

96 ALYTES 27 (3)

Fig. 25. - Gosner Stage 4. Fig. 26. - Gosner Stage 35.

Fig. 28. - Gosner Stage 38.

Fig. 29. - Gosner Stage 40. Fig, 30. - Gosner Stage 41.

Fig. 25 to 30. - Developmental stages 34-41 (Gosner, 1960) of the tadpole of Polypedates teraiensis.

Source : MNHN, Paris

CHAKRAVARTY et al. 97

36. Gosner Stage 38 (fig. 28)

Age. — 1008 h (42 days).

Total length. — 39.3-45.5 mm.

Length of hind-limb. — 7.0-9.8 mm.

Characters. - The margin of the 5" toe web is directed towards the prehallux. The toe tips

are rounded with slight pigmentation on the limbs. Pigmentation appears on the 3", 4!" and

5" toes along the foot. Webbing of feet distinct between all toes. Foot-knee joint well

developed. Appearance of metatarsal tubercle as a small outgrowth.

37. Gosner Stage 39

Age. — 1056 h (44 days).

Total length. — 43.0-45.6 mm.

Length of hind-limb. — 7.9-9.81 mm.

Characters. — Subarticular tubercles appear on the inner surface of the toes as light

patches. The inner metatarsal tubercle becomes a small oval outgrowth. Toe tips rounded with

slight pigmentation. Developing forelimbs visible below the skin but not distinct. Digestive

tract with six loops. Fins pigmented.

38. Gosner Stage 40 (fig. 29)

Age. — 1104 h (46 days).

Total length. —42.6-50.0 mm.

Length of hind-limb. — 8.02-10.5 mm.

Characters. — Toe tips are rounded. Subarticular tubercles are clearly elevated. Vent tube

not yet reduced. AIl rows of keratodont present and distinct. Some of the keratodont rows are

very faint due to loss of individual keratodonts. Muscles on the dorsal side are well built.

Pigmentation lighter.

39. Gosner Stage 41 (fig 30)

Age. — 1128 h (47 days).

Total length. — 42.6-49.5 mm.

Length of hind-limb. — 10.8-15.2 mm.

Characters. — Vent tube reduced. Only a narrow strip remains over and in between bases

of the thighs still attached with ventral fin distally. Skin over the forelimbs transparent.

Tubercles on the hind-limbs distinct with pigmentation. KRF 1:2+2/1+1:2. AI the kerato-

dont rows faint due to shedding of individual keratodonts. Oral papillae remain intact.

Digestive tract with five loops. Uniform pigmentation on the dorsal side.

40. Gosner Stage 42 (fig. 31)

Age. — 1176 h (49 days).

Total length. - 47.3-51.6 mm.

Length of hind-limb. — 26.38-27.6 mm.

Characters. — The forelimbs emerge. Usually the right emerges first, followed by the left

after a few hours, and the fingers have rounded tips. The webbing of the forelimbs is

Source : MNHN, Paris

98 ALYTES 27 (3)

Fig. 31. - Gosner Stage 42. Fig. 32. - Gosner Stage 43.

Fig. 33. - Gosner Stage 44.

Fig. 34. - Gosner Stage 45.

Fig, 31 to 34. - Developmental stages 42-45 (Goser, 1960) of the tapdole of Polypedates teraiensis.

Source : MNHN, Paris

CHAKRAVARTY et al. 99

rudimentary, but as in the adult stage. The vent tube disappeared completely, leaving the vent

aperture free below. The tail darkens and becomes shorter. Kerotodont rows and jaw sheaths

are lost. Resorption of the labial fringe begins, however angular papillae still remain as a small

tuft on both corners of the mouth, which starts widening. The angle of the mouth is in level

with the nostril.

41. Gosner Stage 43 (fig. 32)

Age. — 1224 h (51 days).

Total length. - 20.6-23.1 mm.

Length of hind-limb. — 18.8-26.8 mm.

Characters. - Mouth opening widens. The angle of the mouth reaches a point midway

between nostril and the anterior margin of eye. Eyes slightly protruding. The dorsal and

ventral fins disappear and the tail becomes shorter. Digestive tract with four loops. The

pigmentation is uniform.

42. Gosner Stage 44 (fig. 33)

Age. — 1248 h (52 days).

Total length. — 17.6-18.6 mm.

Length of hind-limb. — 20.4-23.1 mm.

Characters. — Eyes protruding. The widening angle of mouth reaches the level of the

middle of eye. The dorsal and ventral fins completely disappeared. The tail becomes much

shorter.

43. Gosner Stage 45 (fig. 34)

Age. — 1320 h (55 days).

Total length. — 14.9-15.8 mm.

Length of hind-limb. — 20.6-23.1 mm.

Characters. —- The angle of the mouth reaches the posterior margin of the eye. The tail is

reabsorbed to a small triangular stub which is dark in color.

44. Gosner Stage 46

Age. — 1392 h (58 days).

Total length. — 15.6-17.4 mm.

Characters. - The tail stub disappeared completely. It is a metamorphosed froglet.

Conclusion

The total time for the completion of development was 58 days (1392 h). The most

important developmental steps are summarized in table 1. Measurements of stages 22-46 are

presented in tables 2-4.

Source : MNHN, Paris

100 ALYTES 27 (3)

Table 1. - Significant developmental stages of Polypedates teraiensis

No. Stage Characteristics Age

ll 1 Fertilized egg Oh

2 3 Two cell stage 2h25

3 10 Blastula 16h

4 12 Gastrula 21h

5 14 Appearance of neural fold 36h

6 17 Appearance of tail bud 6h

7 20 Hatching 104 h (4.3 days)

8 21 Distinct external gills 118h (4.9 days)

9 25 Appearance of spiracle 197 h (8 days)

10 26 Appearance of hind-limb bud 312h (13 days)

il 35 Distinct five digits 768 h (32 days)

12 38 Appearance of metatarsal tubercle 1008 h (42 days)

13 42 Emergence of both forelimbs 1176 h (49 days)

14 46 Metamorphosed frog 1392 h (58 days)

DESCRIPTION OF TADPOLES AT STAGE 38

External morphology. — Stage 38 tadpoles (n = 10, collection numbers IASST.AT.1081-

IASST.AT.1090; fig. 28) were studied in detail.

Tadpoles of moderate size (TL 39.3-45.5 mm; SVL 13.8-14.8 mm), generalized exotro-

phic tadpoles of ORTON’s (1953) type IV, lentic: benthic (ALTIG & JOHNSTON, 1989).

In dorsal view body elliptical, widest at the middle of the intestinal coil; head oval with

a blunt snout. In profile, body roughly ovoid. Eyes of medium size (about 2.0 mm), bulging,

positioned and directed almost laterally; interocular distance large (6.0-6.9 mm). Eyes

placed closer to the spiracle (3.2-3.6 mm) than to the snout (4.3-4.8 mm). Pineal ocellus

present, lying before the anterior edge of the eyes. Nares small, rimmed and closely spaced;

internarial distance small (1.5-1.8 mm). Nares placed nearer to snout (1.6-1.9 mm) than to

eyes (2.3-3.5 mm).

Spiracle sinistral, of moderate size (about 1.8 mm), rectangular shaped, flat, entirely

attached to body wall, ventrolateral in position, closer to vent tube opening than to snout,

oriented posterodorsally. Dorsal body musculature distinct. There are 5/2 intestinal loops.

Very short and dextral vent tube, ring-like, not attached to ventral fin, directed posterolate-

rally, opening dextral. Glands absent. Lateral line system not observed, lacrymal canals

present from stage 36 (at stage 35 a faint pigmentation is present along the canal, but the latter

is not yet visible).

Source : MNHN, Paris

CHAKRAVARTY et al. 101

Fig. 35. - Picture of the oral disc of a stage 38 tadpole of Polypedates teraiensis stained with methylene

blue (TL 44.2 mm, collection number IASST.AT.1088).

Tail length (25.9-31.8 mm) with delicate fins. Dorsal and ventral fins of nearly equal size,

high (about 1/3 higher than maximum body height; MTH 7.8-9.7 mm), slightly convex, upper

fin extending onto upper body (on a distance of about 1.9 mm). Tail tip greatly narrowing

near tip, tip pointed.

Oral disc (fig. 35) of moderate size (ODW 2.8-2.9 mm), subterminal/anteroventral

positioned and oriented anteroventrally, emarginated. One row of marginal papillae largely

interrupted on the upper labium, and only very shortly in the centre of the lower labium. A

row of submarginal papillae on the lower labium (also interrupted in the middle) and at the

angle of the mouth. Papillae rounded. Jaw sheaths serrated, upper jaw sheath a large arch with

a weak median convexity, lower jaw sheath V-shaped. KRF 1:3+3/1+1:2. First row of the

upper labium continuous whereas the 2", 3! and 4‘ rows are interrupted. Innermost row of

lower labium very slightly interrupted whereas the two other rows are continuous. This

tadpole is overall herbivore. However zooplankton was also found during the gut content

analysis, but as the number is very low it is considered as a chance entry.

Life coloration. — The larvae are light brown with dark brown pigments. Ventral side light

gray and transparent. A light point on the tip of the snout. Caudal muscle light brown, lighter

that abdomen; fins transparent immaculate. In preservative, the colors fade and the ground

color became beige, the ventral side creamy white.

Source : MNHN, Paris

102 ALYTES 27 (3)

Fig. 36. - Buccal floor of a stage 38 tadpole of Polypedates teraiensis (WASST.AT. 1082). BFA, buccal floor

arena; BP, buccal pocket; TA, tongue anlage; VV, ventral velum.

Buccopharyngeal anatomy. - Buccal floor (fig. 36). — Prelingual arena narrow with a pair of

large infralabial papillae with their anterior edge pustulated. Tongue anlage rounded with two

pairs of lingual papillae pustular on tip, the two median slightly longer than the lateral ones.

Buccal floor arena wide, defined by about 9-10 moderately-sized papillae on each side; surface

of floor arena with 20-25 pustules. Buccal pockets nearly oval, closer to the tongue anlage

than to the ventral velum. Ventral velum continuous with spicular support and 10 projections,

the median six closer together; medial notch present; secretory pits present on the velum.

Branchial baskets exposed with three gill chambers on each side.

Source : MNHN, Paris

CHAKRAVARTY et al. 103

Fig. 37. - Buccal roof of a stage 38 tadpole of Polypedates teraiensis (IASST.AT.1082) DV, dorsal velum;

MR, median ridge: PA, postnarial arena; PLR, posterolateral ridge: PR, prenarial arena.

Buccal roof (fig. 37). — Prenarial arena slightly rectangular and concave with a semicir-

cular pustular prenarial ridge. Prenarial papillae present, rising in the middle of the anterior

narial wall; a few pustulations present on the anterior narial wall. Choanae slightly postero-

medially oriented, almost oval. Narial valve smooth, elevated. Two pairs of transversely

oriented postnarial papillae on the same transversal plane, the higher pair small and pustular

at tip, the lowest pair long and pustular on most part. Median ridge low, with irregular small

papillae on its free edge; at least two small papillae in the postnarial arena. Lateral ridge

papillae triangular elongate, transversely oriented, bearing a few papillae on their anterior

edge. Buccal roof arena defined by only three buccal roof arena papillae on each side, oriented

slightly anteromedially, the medial one being the largest and having pustulated tip, the most

anterior less pustular, the posteriormost smooth; buccal roof arena with about 35-40 small

Source : MNHN, Paris

104

ALYTES 27 (3)

Table 2. - Morphometric measurements of tadpoles of Polypedates teraiensis in stages 22 to 34.

Mean + standard deviation and range of 10 measured individuals per stage. See text for

abbreviations.

TL SVL SSp TAL MTH HLL

Stage 22 754023 380 | — 4.164 0.195 - -

7.0-7.7 3.45-3.86 3.85-4.58

Stage 23 9.14 0.84 3.310.197 - 5.54 0.42 - -

8.2-10.4 2.90-3.60 5.062

Stage 24 | 10.840.105 | 3.65+0.237 - 7040.13 - -

10.6-10.9 3.38-420

Stage 25 12.2 + 0.403 4.14 + 0.140 - me x

114-129 3.88-4.28

Stage 26 | 19.340.781 7.0 4 0.46 - 4.3 + 0.49 - 0.19 + 0.03

20.6-23.1 7.5-8.7 45-48 0.17-0.23

Stage 27 | 22.14 3.68 83413 - 4.9 + 0.68 - 0.40 + 0.05

17.8-27.3 6.7-9.8 3.9-5.9 0.32-0.47

Stage 28 | 22.140.986 804041 - 4740.14 - 0.78 + 0.08

20.6-23.1 7.5-8.7 4.5-4.8 0.71-0.89

Stage 29 | 25.143.32 9.14 1.2 5.774#0454 | 17.042.12 5.60 # 1.06 0.99 + 0.19

20.6-28.8 7.5-10.6 5.20-6.18 144-193 4.48-6.62 0.71-1.18

Stage 30 | 28.141,94 | 10.540.690 | 56340359 | 1854148 | 57440126 | 1.11+0.148

23.1-30.1 9.5-11.8 5.20-6.23 14.6-19.7 5.56-5.98 071-118

Stage 31 30.2 + 0.970 11.0 + 0.644 6.48 + 0.168 19.9 + 0.543 6.534 0.214 1.68 + 0.103

284-317 97-118 6.14-6.78 19.2-20.7 5.94-6.68 1.48-1.77

Stage 32 | 28.741,56 | 10.440.094 | 6.01 40.174 1894124 | 61340213 | 1.6840.103

26.1-30.5 10.3-10.5 5.80-6.22 17.2-20.8 5.84-6.39 1.48-1.77

Stage33 | 3074130 | 10.740441 | 64340530 | 20440659 | 6214+0.211 | 1.774 0.262

104-114 5.98-7.30 19.7-21.1 5.96-6.49 1.48-2.40

Stage 34 11.940.867 | 7.374 0.364 67140379 | 221+0.648

31.2-35.6 11.0-13.3 6.42-7.80 6.48-7.40 1.50-3.86

pustulations, more concentrated in the middle and fewer in the posterior region. Posterolate-

ral ridge low and present laterally. Glandular zone present and continuous across the buccal

roof, of about five secretory pits large, size of secretory pits decreasing anteroposteriorly.

Dorsal velum pustular, interrupted medially.

DISCUSSION

Northeastern India contains a rich assemblage of anuran species and is considered a

biodiversity hotspot (MYERs et al., 2000). Nevertheless, only a few studies on the annual

breeding cycles of the amphibian in this region have been carried out. Some of them concern

Fejervarya “limnocharis” and Euphlyctis cyanophlyctis from Shillong by Roy & KHARE (1978)

and KUMAR (1982) respectively, Humerana humeralis (Boulenger, 1887) and Hylarana lepto

Source : MNHN, Paris

CHAKRAVARTY et al.

105

Table 3. — Morphometrie measurements of tadpoles of Polypedates teraiensis in stages 35 to 40.

Mean # standard deviation and range of 10 measured individuals per stage. See text for

abbreviations.

Stage 35 Stage 36 Stage 37 Stage 38 Stage 39 Stage 40

TL 3594162 | 3874167 | 43840910 | 4364206 | 44940622 | 4714220

33.3-38.7 34.9-40.6 42.4-45.2 39.3-45.5 43.5-45.6 42.6-50.0

SVL | 12740954 | 13.440.789 | 14940313 | 14540292 | 14.740.168 | 15.240.993

110-144 123-145 144155 13.8-14.8 144-149 13.6-16.7

BW 5.99 + 0.526 7.04 + 0.791 8.44 + 0.248 8.54 + 0.587 8.74 + 0.385 8.87 + 0.148

5.20-6.90 5.00-7.90 8.20-9.01 7.66-8.93 8.20-9.45 8.65-9.00

HL | 63140492 | 60840788 | 64340052 | 62140619 | 64040458 | 64840141

5.60-7.20 4.80-7.20 633-648 5.01-6.84 5.20-6.84 6.30-6.74

10D 6.00 + 0.200 6.24 + 0.658 6.57 + 0.207 6.48 + 0.260 6.49 + 0.139 6.60 + 0.165

5.76-6.40 5.08-6.90 6.34-6.92 6.02-6.94 6.24-6.66 6.42-7.00

NN 1.64 + 0.140 1.63 + 0.135 1.73 + 0.036 1.73 + 0.096 1.74 + 0.034 1.75 4 0.030

1.50-1.90 1.42-1.90 1.68-1.80 1.50-1.82 1.68-1.78 1.69-1.80

NPE 2.35 + 0.102 2.57 + 0.220 3.23 + 0.034 3.00 + 0.390 341+0.191 3.46 + 0.075

.50 2.20-2.94 3.18-3.26 .54 2.09-3.55 3.36-3.55

ODW | 24240.145 | 26540133 | 28140026 | 28440037 | 27840.105 | 28740153

223-260 2.50-2.80 2.18-2.86 2.18-2.88 2.66-2.88 2.64-3.14

SSp 7.48 + 0.209 7.63 + 0.447 8.65 + 0.063 8.57 + 0.261 8.62 + 0.143 8.73 + 0.289

7.18-7.80 6.96-8.44 8.58-8.79 8.00-8.94 8.40-8.86 8.43-9.48

SN | 13240071 | 15340206 | 18220038 | 17040101 | 17620084 | 1.770058

1.40 124-182 1.79-1.89 1.60-1.89 1.60-1.86 162-181

SE 3.55 + 0.142 3.98 + 0.478 448 + 0.133 4.57 # 0.123 4.59 + 0.087 4.65 + 0.227

3.31-3.72 3.48-4.80 4.32-4.64 4.30-4.75 4.50-4.75 4.50-5.24

SpE | 35340167 | 32940624 | 35040042 | 3.4940.142 | 33940209 | 3.140440

3.30-3.80 2.04-3.80 340-3.54 3:20-3.62 2.14-3.62 2.98-4.76

SpN 7.16+ 0.257 7.22 4 0.299 7.59 + 0.055 7.51 4 0.294 7.714 0.139 7.79 + 0.167

6.80-7.50 6.80-7.80 7.44-7.64 7.10-7.87 7.46-7.87 7.46-8.08

TAL 24.141,15 25.9 + 1.30 29.5 + 0.609 29.94 1.87 30.24 1.95 31.94 1.40

22.2-26.3 23.5-27.2 28.5-30.2 25.9-31.8 29.9-34.2

MTH | 75540775 | 77840703 | 76040.245 | 91420626 | 91940463 | 91340464

648-8.66 7.10-9.18 7.12-7.82 7.84-9.73 8.30-9.92 8.68-10.17

HLL 2.86 + 0.641 338+ 0.718 9.45 + 0.421 8.75 & 1.20 9.24 + 0.776

1.82-3.86 2.12-4.12 8.69-9.96 7.00-9.80 7.90-9.81

Source : MNHN, Paris

106

ALYTES 27 (3)

Table 4. - Morphometric measurements of tadpoles of Polypedates teraiensis in stages 41 to 45.

Mean + standard deviation and range of 10 measured individuals per stage. See text for

abbreviations.

Stage 41 Stage 42 Stage 43 age 44 Stage 45

F TL 46.4 2 2.65 49.6 + 1.10 22.34 0.852 18.2 4 0.362 15.14 0.417

426-495 473-516 20.6-23.1 17.6-18.6 14.6-15.7

SvL 15.0 + 1.02 18.6 + 0.474 14.4 4 0.821 15.04 0.435 -

13.6-15.8 17.9-19.4 12.7-15.2 144-155

BW 8.63 # 0.179 8.59 + 0.273 5.70 4 0.050 4.56 + 0.070 6.114 0.097

838-893 7.88-8.81 5.59-5.76 4.50-4.69 6.02-6.22

BH 7.64 4 0.286 7.64 + 0.302 4225 + 0.049 4.21 + 0.022 6.564 0.051

7.00-7.98 738-798 419-432 418- 642-662

HL 6.56 4 0.122 6.58 4 0.207 5.68 + 0.347 5.22 + 0.153 5.35 4 0.180

642-6.75 6.10-6.77 5.02-5.88 5.10-5.60 5.10-5.60

HH 5.98 + 0.298 5:93 4 0.345 5.58 4 0.069 43740172 6.20 4 0.104

520-622 520-622 5.50-5.67 4.06-4.58 6.02-6.34

10D 6.56 + 0.145 6.54 + 0.093 4.82 4 0.050 5.13 + 0.009 5.814 0.036

6.42-6.90 6.38-6.62 4.75-4.88 5.12-5.14 5.78-5.85

NN 1.74 4 0.036 1784 0.163 2.1440.051 2.67 4 0.008 2.41 4 0.086

1.69-1.80 1.69-2.24 2.10-2.20 2.66-2.68 232-248

ED 2.004 0 2.65 # 0.031 2.00 40

2.00 2.64-2.66 2.00

NP 3444 0.135 343 4 0.063 2.084 0.018 1.46 à 0.004 23240031

3.10-3.55 336-355 2.06-2.12 145-1.46 2.30-2.40

ODW | 46240.179 6.65 4 0.008 7.05 + 0.055 7.584 0.013 6.63 4 0.039

423-482 6.64-6.66 7.00-7.12 7.56-7.59 6.60-6.70

SN 180 + 0.025 2.03 # 0.015 1:59 4 0.033 1.55 4 0.013 1.75 4 0.024

176-183 2.02-2.06 1.54-1.62 1.54-1.58 1.69-1.78

SE 4514 0.123 4514 0.138 3.27 & 0.006 343 4 0.052 2.144 0.110

442-469 415-469 326-328 336-347 2.64-2.95

TAL 3154 1.57 31.0 4 0.695 784021 3540.05 -

29.3-33.6 300-322 76-82 34-36

MTH 8.76 4 0.710 8.72 4 0.460 2794016 2.87 4 0.009

6.86-9.44 7.48-8.99 264-296 2.86-2.88

HLL 9.23 & 0.742 26.74 0.415 20.84 3.15 2134 1.08 41.04

8.02-9.80 263-276 188-268 20.3-23.1 20.6-23.1

FLL - 8.374 0.105 7.11 4 0.408 7.45 à 0.095 7.60 + 0.147

820-852 6.66-7.67 7.40-7.86

Source : MNHN, Paris

CHAKRAVARTY et al. 107

glossa (Cope, 1868) in Assam (BORTAMULI et al., 2010), and Polypedates “leucomystax” and

Hyla annectans in Nagaland (Kiyaseruo & KHARE, 1986 and AO & BoRDOLOI, 2001,

respectively). Furthermore Ao et al. (2006) provided basic information for Rana khare

(Kiyasetuo & Khare, 1986).

There are several reports on the development and metamorphosis as well as on the

staging tables of Rhacophoridae species: Polypedates “leucomystax” (ViLLADOLID & DEL

RosaRIO, 1930; ALCALA, 1962; KIYASETUO & KHARE, 1986); Polypedates maculatus

(MCCANN, 1932; MOHANTY-HEIMADI & DUTTA, 1988; GirisH & SAIDAPUR, 1999; DUTTA et

al., 2001); Rhacophorus arboreus (Okada & Kawano, 1924) (IwasAwWA & KAWASAKI, 1979);

Rhacophorus malabaricus (SEKAR, 1990); and Rhacophorus pardalis (ALCALA, 1962).

This paper describes the morphology and development of P teraiensis. It was found that

Polypedates teraiensis completed its development and metamorphosis in 58 days and hatching

took place after four days at an ambient temperature of 26-32°C. Most of the data on

developmental time concerned P. “leucomystax” from different locations throughout the

range of this complex of species. KIYASETUO & KHARE (1986) studied development of

P. “leucomystax” from Nagaland (although these individuals likely belonged to the

P. mutuslteraiensis species group; DuBois, 1987; Ao et al., 2003). The complete development

took 57-58 days at room temperature of 15 (night) to 24°C (day). This developmental time

was very close to our results despite the cooler temperature. The tadpoles allocated to

P leucomystax from Peninsular Malaysia hatched four days after laying at the stages 20-22

and began to metamorphose about seven weeks after hatching at air temperature of 24-34°C

(VoRKkeE, 1983). These data also agree with our results but, as the author did not refer to precise

stages, comparisons are limited. SHERIDAN (2008) reported a larval life (post hatching) of 42

days and a size at metamorphosis of 19.4 mm for specimens of P leucomystax from Sakaerat

(northeastern Thailand). Although the developmental time is still close to our results, the

metamorphosed froglet of P leucomystax is bigger than those in our study. However, reared

tadpoles are often smaller than wild ones (e.g., MOHANTY-HEIMADI & DuTrA, 1979). The

complete development of Polypedates leucomystax from Negros Island (Philippines) took

70-100 days in laboratory rearing conditions at water temperature 24-30°C (ALCALA, 1962).

The hatchling and exit of the nest occurred at stage 20, as in P teraiensis, and the imagos

reached a size of 16.2-20.2 mm. Polypedates maculatus, the common Indian tree frog,

completes development and metamorphosis in 55 days, 30-35°C room temperature, at

Bhubaneswar, Orissa (MOHANTY-HEIMADI & DUTTA, 1988). As in the latter species, tadpoles

dropped from the nest 4-5 days after deposition and pigmentation appeared after tadpoles

left the foam nest (MOHANTY-HEIMADI & DUTTA, 1988). Under natural conditions, embryos

of P maculatus from South India completed embryonic development in nine days and

hatched at stage 23; the total timing from day of oviposition to completed metamorphosis was

60 days. Species of the genus Rhacophorus (a close relative to Polypedates: e.g., GROSIEAN et

al., 2008; Li et al., 2009; YU et al., 2009) also produce foam nests. Rhacophorus malabaricus

completes metamorphosis in 68 days at room temperature 28-35°C (SEKAR, 1990), R.

arboreus in 44 days at 22°C (Iwasawa & KAWASAKI, 1979) and R. pardalis in 60-100 days at

water temperature of 24-30°C (ALCALA, 1962). Although these data are close to our results for

P teraiensis, the various species show interspecific variation. To evaluate this variation, more

data on intra-specific variation should be collected.

Source : MNHN, Paris

108 ALYTES 27 (3)

Metamorphosis (i.e., stages 42-46, from emergence of forelimbs until completion of

metamorphosis) lasts 9 days in P teraiensis. This is longer than the few available data on the

duration of metamorphosis in other species. DOWNIE et al. (2004) who studied timing of

metamorphosis in 14 taxonomically and ecologically diverse species from Trinidad plus

Xenopus laevis (Daudin, 1802) reported metamorphosis ranging from 2.0 to 7.3 days at room

temperature of 25.0-28.5°C. Among the factors that could influence metamorphosis dura-

tion, these authors discussed three that could partially explain this long duration in P

teraiensis tadpoles: (1) relative large size of the prometamorphic tadpoles (more tissue has to

be re-modeled); (2) low number of predators present in new-filled temporary water bodies (the

Polypedates foam nests are sometimes built before depressions are filled by rain; GROSIEAN,

pers. obs.); and (3) metamorphosing Polypedates are able to leave water in earlier stages of

metamorphosis and climb and hide within vegetation, thus avoiding aquatic and most of

terrestrial predators. However, these are potential explanations that need further testing

because, as emphasized by DowniE et al. (2004), the natural history of froglets is well

under-studied. Furthermore, few data are available in the Rhacophoridae to compare with

our results: P maculatus and R. arboreus undergo metamorphosis in five days (IWASAWA &

KAWASAKI, 1979; MOHANTY-HEIMADI & DuTTA, 1988), whereas SEKAR (1990) reported a

metamorphosis duration of 12 days in R. malabaricus. The metamorphosis of the Philippine

populations of P leucomystax is reported to last about two weeks (VILLADOLID & DEL

RosaRIO, 1930), though these data are far from being precise.

The clutch size for P teraiensis consists of about 100 eggs. This size is much less

than that given in most of the published data for P maculatus (210-719 eggs per clutch;

MOHANTY-HEJMADI & DUTTA, 1988; GirisH & SAIDAPUR, 1999) and P. “leucomystax”

(100-900 eggs per clutch; VILLADOLID & DEL ROSARIO, 1930; YORKE, 1983; SHERIDAN,

2008). This low number could be due to reproduction in captivity and data from wild

caught clutches must be obtained before considering this clutch size as characteristic of the

species.

The eggs of P teraiensis measure 2.0-2.2 mm in diameter. This is slightly larger than eggs

of P “leucomystax” from Sakaerat, northeastern Thailand (average 1.81 mm: SHERIDAN,

2008), P “leucomystax” from Nagaland (1.73-1.75 mm: KivASETUO & KHARE, 1986), and P

leucomystax from Philippine (1.7-2.0 mm: ALCALA, 1962; 1.0-1.5 mm: VILLADOLID & DEL

RosaRIO, 1930). In Polypedates maculatus, eggs are also smaller than those of P teraiensis

(1.25-1.50 mm: MCCANN, 1932; MoHANTY-HEImADI & DUTTA, 1988; DANIEL & SEKAR, 1989)

and those of P megacephalus (1.8-2.0 mm: Liu, 1950). On the contrary, eggs of species of the

genus Rhacophorus are bigger than those of P teraiensis (2.76 mm in R. malabaricus: SEKAR,

1990; 2.5 mm in R. maximus Günther, 1859: MCCANN, 1932; and 3.0 mm in R. arboreus and

R. pardalis: ALCALA, 1962; IwAsAWA & KAWASAKI, 1979).

Polypedates teraiensis breeds in rain-fed pools that are sporadically filled by rain and then

dry at different speeds. In such an unpredictable habitat, desiccation is arguably the single

most important environmental factor affecting larval survivorship, and species that breed in

such ponds have evolved several traits that allow su sful development. One of these traits

is a high rate of larval development, as observed in this study. This rapid rate of development

in Polypedates teraiensis may be advantageous, as it allows the larvae to metamorphose

quickly and escape de: tion, but also reducing exposure to aquatic predators and diseases

Source : MNHN, Paris

CHAKRAVARTY et al. 109

as reported in other frog species (NEWMAN, 1988; DENVER et al., 1998; PARRIS & BAUD, 2004).

The tadpoles of small temporary ponds have been reported to spend more time in feeding and

develop faster than tadpoles from large permanent ponds, where the larvae spend more time

hiding from predators and develop more slowly (PELTZER & LAIMANOVICH, 2004). Environ-

mental factors also can regulate amphibian metamorphosis. Amphibian larvae respond to

alterations in these factors through high level of plasticity in the developmental phenotypes

(STEARNS, 1989; PFENNIG, 1990, 1992). Such plasticity may involve changes in the rate of

developmental transition, adopting alternative morphologies and so on (NEWMAN, 1992;

MCcCoLLUM & VAN BUSKIRK, 1996).

The present study reports that foam nest is essential for the development of this

rhacophorid species. When eggs were removed from the foam nest before hatching, the

embryo did not develop further. In P maculatus, tentatives of rearing just hatched tadpoles

before they naturally go out of the foam nest also failed (MOHANTY-HEIMADI & DUTTA, 1988)

indicating that a period of development inside the foam nest after hatching is necessary.

It thus seems that such a minimum period of development in the nest is a pre-requisite

for embryonic development in Polypedates. The foam nest has been suggested to protect

the eggs and embryos from predators and desiccation (HEYER, 1969; DoWNIE, 1988,

1993). Also protection from thermal damage was suggested as white foam reflects heat

(GorzZULA, 1977).

The embryonic development takes place between stages 1 and 19. The first cleavage starts

at stage 3 and divides the egg completely into two equal blastomeres. The formation of blastula

takes 16 hours and occurs at stage 10. The next significant stage is the 12‘° when the gastrula is

formed. The neural fold appears at stage 14 and the tail-bud appears at stage 17. The form of the

tail as observed in the stages 18-20, i.e., first rolled up against the yolk then very fine and almost

straight, is more similar to endotrophic tadpoles (e.g., in Arthroleptis poecilonotus Peters, 1863:

LAMOTTE & PERRET, 1963; Nimbaphrynoides occidentalis (Angel, 1943): LAMOTTE & XAVIER,

1972; or Nectophrynoides tornieri (Roux, 1906): ORTON, 1949 than to exotrophic ones. The

embryonic development continues up to stage 19 and finally the embryo hatches at stage 20

Within the nest. The whole embryonic development takes place within the foam nest. The

young tadpole in stage 21 stays within the nest and drops in water at stage 22.

The newly hatched larvae are very delicate, have a large yolk sac and external gills. At

stage 21, the cornea becomes transparent but the tail fins are still opaque. The tail fins become

quite transparent at stage 22 and blood circulation within them begins. The external gills

slowly get reduced and finally are completely covered with the completion of the development

of the operculum at stage 25. At this point a faint line corresponding of the spiracle opening

can be seen.

The differentiation of the oral disc and keratodont rows begin at stage 23; by stage 25 the

keratodont rows are quite distinct. On the upper labium there is one uninterrupted and one

interrupted row of keratodonts whereas on the lower labium all three rows are already

present, the third one being small in size. By stage 26, the larval KRF 1:3+3/1+1:2is attained.

This remains up to stage 39. Subsequently, the keratodonts start shedding and by stage 40

there are one uninterrupted row (but half the size of the original one) and two interrupted

rows of keratodonts on the upper labium. On the lower labium three rows still remain but are

very faint due to shedding of individual keratodonts. At stage 41, there is one interrupted row

Source : MNHN, Paris

110 ALYTES 27 (3)

on the upper labium and two uninterrupted rows on the lower labium, all very faint. With the

emergence of the forelimbs at stage 42, the jaw sheaths and the keratodonts have completely

disappeared. These results corroborate previous findings and are in agreement with develop-

mental pathway of tadpoles with a KRF higher than 2/3 (GROSIEAN, 2006, and literature cited

therein). The sequence of keratodont rows appearance is of a “proximal” type on each labium

after the 2/3 formula is attained, a pattern common to the stream dweller tadpoles of Ranidae

and Megophryidae (type E of ALTIG & JOHNSTON, 1989: fig. 5: 91). The marginal papillae of

P. teraiensis appear at stage 23 that is earlier than usually in other species, whereas the

formation of keratodonts and jaw sheaths is slightly delayed (THIBAUDEAU & ALTIG, 1988).

The opening of the mouth widens gradually from stage 42, and by stage 44 the angle of the

mouth reaches the level of the middle of the eye. Feeding activity generally stops after stage 42

and the larvae undergo fasting during the period of intestinal remodeling.

A very faint pigmentation is visible at stage 22 on the dorsal side and the larvae are

fully pigmented by stage 38. In P maculatus, the pigmentation is also reported to appear

after the embryo escaped the foam nest at stage 22 (MOHANTY-HEIMADI & DUTrA, 1988).

The toe web starts developing at stage 37, then is present between all toes at stage 38 as in

the adult state. During the next stages, it develops conjointly with toes but its relative

expanse does not change. During this time the toe tips also become rounded, the subarticular

tubercles appear at stage 40 and gradually develop. At stage 41, the skin covering the forelimbs

becomes transparent and they finally emerge at stage 42. The toes of the forelimbs have

rudimentary web.

Many of the morphological variations of buccopharyngeal (buccal filters) and oral

(papillae, keratodonts) features are correlated with the mode of feeding (e.g., carnivorous,

suspension feeding, scraping; ALTIG & JOHNSTON, 1989; ORTON, 1953; WASSERSUG & HEYER,

1983). The oral apparatus of a typical exotrophic pond tadpole includes an oral disc

composed of an upper labium with free lateral edges and two keratodont rows, a larger lower

labium with free marginal edges and three keratodont rows, unmodified jaw sheaths, a wide

dorsal gap in the marginal papillae and submarginal papillae laterally and ventrolaterally

(CANNATELLA, 1999). The structures of the oral apparatus of P. teraiensis were found to be

similar with this description except that the upper labium bears more than two keratodont

rows. This species is generally herbivore but a few specimens of zooplankton were also

observed during the gut content analysis (here considered as a chance entry).

The tadpoles of all Polypedates species have an ovoid body (i.e., BW/BH about 100 %),

lateral eyes, and a flagellum at the tip of the tail. They are all globally very similar (for the

species from Borneo, not discussed here except for P leucomystax, see INGER, 1966, 1985).

Comparison of the tadpole of P teraiensis with other Polypedates tadpole species is extremely

difficult, primarily because of the lack of accuracy in specific assignation of the described

tadpoles (most of them assigned to P leucomystax: FLOWER, 1896, 1899; SmrrH, 1917; VAN

KAMPEN, 1923; ViLLADOLID & DEL ROSARIO, 1930; Porz, 1931; Liu, 1940, 1950; ALCALA &

BROWN, 1956; INGER, 1956; ALCALA, 1962), and because of too succinct descriptions.

The descriptions of FLOWER (1896, 1899), SmrrH (1917), INGER (1956), ALCALA &

BROWN (1956) and ALCALA (1962) can be assigned to Polypedates leucomystax as these

samples are from north Borneo (Sabah), Thailand, Malay Peninsula, Singapore, and Philip-

pines. However, two different KRF are commonly found in Thailand, i.e., 1:4+4/1+1:2 and

Source : MNHN, Paris

CHAKRAVARTY et al. 111

Table 5. - Summary of two morphological characteristics among described tadpoles in the genus

Polypedates including different populations of P. “leucomystax”. KRF, Keratodont Row

Formula.

KRF Lien pointon References

the snout

P. leucomystax 1:44) Absent? INGER, 1956

{north Borneo) (S+SYI+1:2

P. leucomystax 1:3+3 or Present ALCALA & BROWN, 1956;

(Philippines) 1343/1412 ALCALA, 1962

P. leucomystax 13433 Present FLOWER, 1896; SMITH, 1917

(Malay Peninsula, Singapore)

P. leucomystax 1447112 Present FLOWER, 1899; SMirit, 1917

{mainland Thailand, Bangkok)

P. maculatus (India) 13433 Absent MOHANTY-HEMADI & DUTTA, 1988

P. maculatus himalayensis 1:43) Absent ANNANDALE, 1912; GROSIEAN, 2004

(India, Nepal) (+4y1+1:2

23#3/1#1:2

P. megacephalus 13433 Present Por, 1931; LIU, 1940, 1950:

(China, Vietnam) 1643) Chou & LIN, 1997; GROSIEAN, 2004

GH4yI+12

P. mutus (Vienam) 14+4/1+12 GROSIEAN, 2004

P. teraiensis 1343/1412 | This study

1:3+3/3, the latter form being found only in Malay Peninsula. The specimens of Bangkok

show a light yellow point on the tip of the snout (FLOWER, 1899). The populations of the

Philippines have a KRF 1:3+3/3 or 1:3+3/1+1:2 and bear a white dot on the tip of the snout

(ALCALA & BROWN, 1956; ALCALA, 1962) wheras those of north Borneo have a KRF

1:(4+4)-(5+5)/1+1:2 (INGER, 1956). Substantial differences in KRF are observed among

these geographical populations of P leucomystax. Recent biogeographical and demographi-

cal investigation of these populations (BROWN et al., 2010) showed shaliow genetic divergence

among them although four clades were recognized. The first one comprised the northern

Sunda Region (including Malay Peninsula, North Borneo and South Philippines), the

second one comprised the southern Sunda Region, the third the North Philippines and the

fourth Sulawesi. However the observed differences in KRF can also be due to ontological

differences.

PorE (1931) recognized a form from Hainan (as P {. leucomystax) and a form from

mainland China (as P !. megacephalus) though clear differences are not evident (from his own

statement). Furthermore, he found no differences between the two tadpole forms; we consider

these samples to represent larvae of P megacephalus. The KRF is 1:3+3/3. Tadpoles from

West China (Sichuan) have a KRF 1:3+3/1+1:2, more rarely of 1:4+4/1+1:2 (Liu, 1940,

1950). Tadpoles collected from Sa Pa, Vietnam and described as Polypedates gr. leucomystax

in GROSIEAN (2004), here tentatively assigned to P. megacephalus, have a KRF 1:4+4/1+

Finally, CHou & Lin (1997) described the external morphology and the buccal features of

tadpoles from Taiwan with a KRF 1:(3+3)-(4+4)/1+1:2. Though not noticed by Pope (1931),

Source : MNHN, Paris

112 ALYTES 27 (3)

a creamy (LIU, 1940, 1950), ivory (CHou & Li, 1997) or white (GROSIEAN, 2004) dot on the

tip of the snout of the tadpole is present in this species.

The KRF of the tadpole of P maculatus is 1:3+3/3 (MOHANTY-HEJMADI & DUTTA,

1988). The subspecies P. maculatus himalayensis shows two KRF 1:(3+3)-(4+4)/1+1:2 (the

most common) or 2:3+3/1+1:2 which is unique among known species (ANNANDALE, 1912;

GROSIEAN, 2004). The size of this tadpole is greater than the others and it is brown colored

(even after 40 years in preservative), whereas other species turn clear gray very rapidly.

Polypedates mutus has a KRF 1:4+4/1+1:2 and a clear dot on the snout (GROSIEAN,

2004). Its keratodont formula is distinct from that of P teraiensis, thus corroborating the

separation of the two species which are morphologically very close. So, although adults can be

distinguished by the presence/absence of vocal sacs, the two species can also be distinguished

With larval characters, emphasizing the importance of knowing larval stages, especially on the

ground of integrative taxonomy.

Itis important to note that the contrast between the clear dot and the darker surrounding

coloration fades in preservative and it could have escaped the attention of some describers.

A summary of these comparisons is provided in table 5.

LITERATURE CITED

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Rana tigrina Daud. (Ranidae, Anura, Amphibia). Proc. nat. Acad. Sci., India B, 47: 79-92, 4 pl.

AHMED, M. F., Das, A. & DUTrA, K., 2009. — Amphibians and Reptiles of Northeast India. A

photographie guide. Guwahati, Aaranyak: i-xiv + 1-170.

ALCALA, À. C., 1962. - Breeding behavior and early development of frogs of Negros, Philippine Islands.

Copeia, 1962: 679-726.

ALCALA, À. C. & Brown, W. C., 1956. — Early life history of two Philippine frogs with notes on

deposition of eggs. Herpetologica, 12: 241-246.

ALTIG, R. & JOHNSTON, G. F., 1989. — Guilds of anuran larvae: relationships among developmental

modes, morphologies and habitats. Herp. Monogr., 3: 81-109.

ALTIG, R. & MCDiarMiD, R. W., 1999. - Body plan. Development and morphology. /n: R. W. MCDiar-

Mi & R. ALTIG (ed.), Tadpoles: the biology of anuran larvae, Chicago, University of Chicago Press:

24-51.

ANNANDALE, N., 1912. - Zoological results of the Abor Expedition 1911-1912. [. Batrachia. Rec. ind.

Mus., 8: 7-36, pl. 2-4.

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©ISSCA 2011

Source : MNHN, Paris

Alytes, 2011, 27 (3): 116. Announcement

Bionomina

{international Journal of Biological Nomenclature and Terminology)

Should we write Hexapoda or Insecta, Testudines or Chelonii, systematics or taxonomy, character or

attribute, monophyletic or holophyletic, rank or category? What is the origin and meaning of the terms

gene, induction, species, hybrid, hybridogenesis, klepton, relacter, fitness, exaptation, natural selection,

genetic pollution, holism, teleology?

Science does not consist only in “facts” and data, but also in theories, hypotheses and concepts. An

unambiguous and efficient communication between scientists, and between them and society as a whole,

requires the use of well defined terms, understood in the same way by all. Many scientific errors, debates

and polemics take their roots in misunderstandings that result from the use of a vague terminology or in

an approximate or erroneous nomenclature. In this domain, “common sense” is rarely a good guide, as

was aptly stressed by Bertrand Russell in 1953:

“No one wants to alter the language of common sense, any more than we wish to give up talking of the sun

rising and setting. But astronomers find a different language better, and I contend that a different language is

better inphilosophy. (..) Iconclude that common sense, whether correct or incorrect in theuseof words, doesnot

know in the least what words are. 1 wish 1 could believe that this conclusion would render it speechless.”

So far, no journal in the world was devoted specifically to the questions posed by scientific language,

particularly in the domain of biology. This will be the purpose of Bionomina, published, simultancously

online and in paper version, in New Zealand by Magnolia Press (publisher of Zooraxa, Phytotaxa,

Zoosymposia and Molluscan Research). This journal will deal with all questions related to the “languages

of biology” in a transversal and pluridisciplinary approach, touching biology, epistemology, linguistics,

translation, history of sciences, sociology and philosophy. The journal can be accessed by the link:

<htip/wwwmapress.com/bionomina/>.

Editorial Board

Chief Editor: Alain Dubois (P: France).

Deput, Alessandro Minelli (Padova, Italy).

Managing Editor: Zhi-Qiang Zhang (Auckland, New Zealand).

Other members of the Editorial Board: Erna Aescht (Linz, Austria); Richard Bateman (Richmond, UK);

Brent Berlin (Athens, USA); Yann Bertrand (Huddinge, Sweden); Olivier Béthoux (Black Moun-

tain, Australia); Roger Bour (Paris, France); Ingo Brigandt (Edmonton, Canada); Michel Chauvet

(Montpellier, France); Frédéric Chérot (Gembloux, Belgium); Benoît Dayrat (Merced, USA); Mark

Epstein (Ewing, USA); Philippe Grandcolas (Paris, France); Werner Greuter (Berlin, Germany);

Thierry Hoquet (Nanterre France); Julio Mario Hoyos (Bogota, Columbia); Nikita Kluge (Saint-

Petersburg, Russia); Michel Laurin (Paris, France); Valéry Malécot (Angers, France); Rolf Rutis-

hauser (Zürich, Switzerland); Gerhard Scholtz (Berlin, Germany); Marc van Regenmortel (Stras-

bourg, France); Lars Vogt (Bonn, Germany); Zhong Shengxian (Chengdu, China).

Contents of volume 1 (December 2010)

Alain Dubois. — Bionomina, a forum for the dis

biology.

Jens H. Kuhn & Victoria Wahl-Jensen. - Being obsessive-compulsive about terminology and nomencla-

ture is not a vice, but a virtue.

Nikita Julievich Kluge. - Circumscriptional names of higher taxa in Hexapoda.

Roger Bour. - Constant Duméril's Zoologie Analytique was published in 1805.

Thiery Hoquet. - Why terms matter to biological theories: the term “origin” as used by Darwin.

ion of nomenclatural and terminological issues in

Contents of volume 2 (February 2011)

Alain Dubois. - The /nternational Code of Zoological Nomenclature must be drastically improved before

itis too late.

Source : MNHN, Paris

AINTES

International Journal of Batrachology

published by ISSCA

EDITORIAL BOARD

Chief Editor: Stephane GRostr:N (Reptiles et Amphibiens, UMR 7205 OSEB, Département de S;

Evolution, Muséum national d'Histoire naturelle, CP 30, 25 rue Cuvier 75005 Paris, France:

<sgrosjea@mnhn.fr>).

Deputy Editor: Franco ANDREONE (Museo Regionale di Scienze Naturali, Via G. Giolitti 36, 10123 Torino, Italy:

<fandreone@libero.it>).

Alytes Editorial Board: Ariadne ANGULO (Toronto, Canada): David C. BLACKBURN (Kansas, USA): Lauren E.

BROWN (Normal, USA): Angus I. CarëNTIER (Norwich, UK): Ignacio DE LA RIVA (Madrid, Spain):

Rafael O. be S4 (Richmond, USA); Alain Dunois (Paris, France): W. Ronald HeyeR (Washington, USA):

Rafael MaRQUEZ (Madrid, Spain): Masafumi Matsut (Kyoto, Japan); Annemarie OHLER (Paris, France):

Mark-Oliver Rôbez. (Berlin, Germany): Miguel VENCES (Braunschweig, Germany).

Amphibia Mundi Editorial Board: Alain Dunois, Chief Editor (Paris, France) Ronald 1. CROMBIE (San

Francisco, USA): Stéphane GROSIEAN (Paris, France): W. Ronald Heyer (Washington, USA): HANG

Jianping (Chengdu, China): Esteban O. LaviLLA (Tucumän, Argentina): Jean-Claude RAGE (Paris,

France); David B. Wak (Berkeley, USA).

Technical Editorial Team (Paris, France): Alain Dumois (texts): Roger BoUR (tables): Annemarie OHLER (figures).

Book Review Editor: Annemarie OuLER (Paris, France).

SHORT GUIDE FOR AUTHORS

(for more detailed /nstructions 10 Authors, see Alytes, 1997, 14: 175-200)

Alytes publishes original papers in English, French or Spanish, in any discipline dealing with amphibians.

Beside articles and notes reporting results of original research, consideration is given for publication 10 synthetic

review articles, book reviews, comments and replies, and to papers based upon original high quality illustrations

(such as colour or black and white photographs), showing beautiful or rare species, interesting behaviours, etc.

The title should be followed by the name(s) and address(es) of the author(s). The text should be typewritten

or printed double-spaced on one side of the paper. The manuscript should be organized as follows: English

abstract, introduction, material and methods, results, discussion, conclusion, French or Spanish abstract,

acknowledgements, literature cited, appendix.

Figures and tables should be mentioned in the text as follows: fig. 4 or tab. 4. Figures should not exceed 16

X 24 em. The size of the lettering should ensure its legibility after reduction. The legends of figures and tables

should be assembled on a separate sheet. Each figure should be numbered using a pencil.

References in the text are to be written in capital letters (BOURRET, 1942; GRar & POLLS PELAZ, 1989: INGER

et al., 1974). References in the Literature Cited section should be presented as follows:

M.. 1989. - Evolutionary genetics of the Rana esculenta complex. fn: R. M. DAWLEY

lution and ecology of unisexual vertebrates. Albany, The New York State Museum:

ariation and population ecology of some Southeast

Asian frogs of the genera Bufo and Rana. Biochem. Gener., V2: 121-145.

Manuscripts should be submitted either as attached document by e-mail, or in paper form by mail but then

t te, cither 10 Stéphane GROSIFAN (address above) if dealing with amphibian morphology. anatomy,

systematics, biogeography, evolution, genetics, genetics, anomalies or developmental biology, or to Franco

ANDREONE (address above) if dealing with amphibian population genetics, ecology, ethology. life history or

conservation biology, including declining amphibian populations or pathology. Acceptance for publication will

be decided by the editors following review by at least two referees.

After acceptance, a copy of the final manuscript should be sent to the Chief Editor, either as attachment by

e-mail, or by mail on a floppy disk (3 % or 5 4). We welcome the following formats of text processing: (1)

preferably, MS Word (1.1 to 6.0, DOS or Windows), WordPerfect (4.1 to 5.1, DOS or Windows) or WordStar (3.3

10 7.0); (2) less preferably, formated DOS (ASCII) or DOS-formated MS Word for the Macintosh (on a 3 4 high

density 1.44 Mo floppy disk only).

Page charges are requested only from authors having institutional support for this purpose. The publication

of colour photographs rged. For each published paper, a free pdf or 25 free reprints are offered by ISSCA

10 the author(s). Additional reprints may be purchased.

Vs,

Published with the support of AALRAM

(Association des Amis du Laboratoire des Reptiles et Amphibiens

du Muséum National d'Histoire Naturelle, Paris, France).

Directeur de la Publication: Alain DUBOIS.

Numéro de Commission Paritaire: 64851.