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Treasurer: Stéphane GROSJEAN (Paris, France).

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AILRTTES

INTERNATIONAL JOURNAL OF BATRACHOLOGY

Volume 23, N° 3-4

Alytes, 2006, 23 (3-4): 81-95.

(Microhylidae: Scaphiophryninae)

and Mantella expectata

(Mantellidae: Mantellinae)

The tadpoles of Scaphiophryne gottlebei

from Isalo Massif, south-central Madagascar

Corresponding author <£andreone@libero.it>

Vincenzo MERCURIO & Franco ANDREONE!

Museo Regionale di Scienze Naturali, Via G. Giolitti 36,

10123 Torino, Italy

The tadpoles of the microhylid Scaphiophryne gottlebei and of the

mantellid Mantella expectata from the Isalo Massif (south-central Mada-

gascar) are described and compared with already known tadpoles belonging

to the same genera. The tadpole of $. gottlebei is peculiar in having the oral

unique feeding habits and a peculiar associated behaviour. During ch the dav it

stays close to the bottom and often burrows half of the body into the sand

with the tail obliquely upwards; in this position it ingests organic material

from among the substrate particles. During night time the tadpole leaves the

bottom and swims throughout the water column. Since this tadpole cannot

be included in any of the currently known ecomorphological categories we

create a new category for this species, the “psammonektonic" tadpole.

Mantella expectata was often found in the same environments, although it

appears to prefer more open habitats. In some cases, tadpoles of both

species were found together, although M. expectata usually prefers small

and temporary streams for reproduction. The mantella tadpoles were also

found in quite open savannah areas. The tadpole morphology agrees in

general with that of other mantellas, mainly of the M. betsileo group, and is

of the generalized ranoid type.

Bibliothèque Cen

TVR

trale Muséum

séürée 7 MNIHN, Paris

82 ALYTES 23 (3-4)

INTRODUCTION

Given the very high number of known species of amphibians in Madagascar (more than

220 according to ANDREONE & LUISELLI, 2003, ANDREONE et al., 2005, and subsequent

updates), it is not surprising that for most of them the tadpole morphology and general larval

ecology are not yet known. Nevertheless, it is clear that the knowledge of the tadpoles is a

crucial step in the assessment of conservation priorities, as it allows understanding the

ecological requirements of the species in its whole and not only during the adult stage.

Besides, the analysis of anuran larvae may help in the clarification of enigmatic phylogenetic

positions that are hardly to be unveiled by studying only the adult characters. Finally, it is

interesting to understand how the adaptation to peculiar and local ecological conditions is

reflected in the larval ecology.

The conservation status of all the Malagasy amphibians was recently evaluated during

the Global Amphibian Assessment (ANDREONE et al., 2005), which led to the identification of

nine critically endangered species. Since the majority of these species (five of the genus

Mantella and Scaphiophryne gottlebei) are (or have been until recently) important items in the

pet trade, and therefore quite regularly kept in captivity (ANDREONE & LUISELLI, 2003), it is

surprising that the larval morphology is known for only one species, Mantella aurantiaca

(ARNOULT, 1965; VENCES et al., 1999).

Thus, a series of surveys was recently carried out aimed at unveiling distribution and life

history traits of these species. This was the case for Scaphiophryne gottlebei Busse & Bôhme,

1992 and Mantella expectata Busse & Bôühme, 1992, which are limited in distribution to the

sandstone Isalo Massif, south-central Madagascar (GLAW & VENCES, 1994). Incidentally

both these species were described upon specimens imported for the trade, and until recently

little was known about their life history traits (BUSSE & BÔHME, 1992; GLaAw & VENCES, 1994).

During an inventory in the Isalo Massif we had the opportunity to find the tadpoles of these

species, for which we provide here descriptions.

Since the tadpole of the enigmatic genus Scaphiophryne was stated to be intermediate

between the microhylid and ranid forms (WAssERSUG, 1984), we also took the opportunity to

compare the S. gorrlebeïs tadpole with those of other allied species. Its peculiar behaviour

and habits led us to create a new ecomorphological category, discussed in detail below. Since

both species turned out to be syntopic, we also provide information on their larval ecology.

MATERIAL AND METHODS

Tadpoles were captured with a handnet during day and night inspections of the pools

and other water bodies present in the wet canyons (and nearby areas) of the Isalo Massif,

south-central Madagascar (Fianarantosa Province). They were maintained alive in small

aquaria and fed with fish food. This allowed us to obtain a complete development series and

to confirm their natural history traits via observations in a controlled environment. Preserved

tadpoles are now housed in the Museo Regionale di Scienze Naturali, Torino (MRSN; see

Appendix).

Source : MNHN, Paris

MERCURIO & ANDREONE 83

For S. gotilebei, the species identification was based on rearing the tadpoles until

metamorphosis and on comparing the mitochondrial DNA of larvae (voucher specimen

MRSN A2618) and of adults. For DNA study, we used standard extraction methods. A

fragment of the mitochondrial 165 rRNA gene was amplified using the primers 16Sa-L and

16Sb-H of PALUMBI et al. (1991). Sequences were validated and aligned with the software

Sequence Navigator (Applied Biosystems), and deposited in Genbank (accession numbers of

newly obtained sequences from the tadpole: DQ078784). For Mantella expectata, the tad-

poles were collected in a temporary pool and were reared until metamorphosis.

Tadpoles were photographed at different stages. A small number was euthanized by

immersion in chlorobutanol, and successively fixed in 4% formalin for morphological

measurements. À few individuals were fixed and preserved in 90 % ethanol for genetical

analyses. The remnant part was released at the capture site.

Terminology of measurements follows ALTIG & MCDIARMID (1999), whereas the labial

tooth formula is given according to ALTIG (1970). Measurements were made at 0.01 mm

under stereoscope, and are respectively based on 10 specimens at GOsNER’s (1960) stages 25-44

for S. gottlebei, and on 20 specimens at stages 25-37 for M. expectata. Mean values and

standard deviations are given in the descriptions (see tab. 1-2). We measured the following

physicochemical parameters at two sites: pH (with Extech Extik PH100), conductivity

(Extech Extick EC400) and oxygen (Extech D0407510).

RESULTS

TADPOLES’ DESCRIPTIONS

Scaphiophryne gottlebei Busse & Bühme, 1992 (fig. 1-3)

The tadpole of this species exhibits a mosaic of different ecomorphological traits

(McDrarmi & ALTIG, 1999), and we propose for it a new ecomorphological category (see

Discussion).

The body is stout and elliptical, flattened below, ovoid above. The snout is trapezoidal in

dorsal view. The eyes are medium-sized, positioned dorso-laterally. The external nares are

located dorsally, closer to eyes than to snout tip. They are visible and positioned in a slight

light-coloured furrow. In tadpoles at advanced development stages (from 25 to 38), the narial

apertures are apparently not open; they become clearly open at stage 41.

Tail fins are rather high. The dorsal fin is parallel to tail musculature, the ventral fin is

higher than the dorsal, with its maximum height at about two-thirds of tail length. The dorsal

fin originates at the tail-body junction and the ventral fin at the postero-ventral end of the

body.

The spiracle is latero-ventral with a posterior opening. The inner wall of spiracle is

absent. The vent tube is medial, ventrally directed, with a medial aperture.

Source : MNHN, Paris

84 ALYTES 23 (3-4)

Table 1. — Measurements (at 0.1 mm) of 10 tadpoles of Scaphiophryne gotlebei. GS, Gosner stage, n,

number of specimens; TL, total length; TAL, tail length; BL, body length; BW, body width; E, eye

diameter; IOD, inter-orbital distance, TMW, tail muscle width; TMH, tail muscle height, MTH,

maximum tail height. Values are given as mean + standard deviation. See the Appendix for locality

references.

GS| ” TL TAL BL BW E 10D TMW TMH MTH

25 12.7 + 1.9/25.3 + 0.4114.6 + 5.1] 4.8 + 1.1 10.2#+01|25+41.1|10+00!|1.7+02|46+16

26 143 26.1 11.8 48 02 30 12 2.0 45

27|1 21.0 37.0 15.5 18.0 03 5.0 12 30 7.0

3311 235 40.8 173 10.0 04 57 20 35 8.0

3411 25.0 41.5 16.5 8.5 03 60 13 3.1 82

38|1 29.1 482 19.1 11.0 16 80 2.6 5.0 _-

41 25.7 + 3.2|41.3 4 3.2/160+0.0|9.3+04|04+01|53+04|18+04|36+04|70+1.3

4411 13.6 26.6 13.0 6.0 0.4 37 12 2.1 23

Table 2. - Measurements (at 0.1 mm) of 20 tadpoles of Maniella expectata. GS, Gosner stage, n, number of

specimens; TL, total length; TAL, tail length; BL, body length; BW, body width, E, eye diameter;

IOD, inter-orbital distance, TMW, tail muscle width, TMH, tail muscle height, MTH, maximum tail

height. Values are given as mean + standard deviation. See the Appendix for locality references

GS| # TL TAL BL BW BE 10D TMW TMH MTH

25 15.6+34194+21|62+1.3| 40409 | 0.5+0.1 |1.340.3/09+03| 11403 |[26+06

26 19.74 0.1/12.4 + 1.8] 7.3 40.5 |3.6+03|06+0.1|1.2402|109+01|11+03|24+03

27 18.8+49|11.0+4.2|7.8+0.7|384+02|07+0.1|13+01|11+02|114#+02|25+02

28 20.0 12.0 80 40 07 15 09 1.1 13

35 25.1 148 103 57 09 15 17 17 40

37 28.6 178 10.8 62 LI L8 18 2.6 46

The oral disc is roundish, not emarginated, with marginal and submarginal papillae tidily

arranged all over the disc. The papillae are conical with rounded tips, sometimes with

brownish pigment except at tips. Labial teeth are absent. Jaw sheaths are well developed. The

inferior part of the lower jaw sheath is partially pigmented.

In life, the tadpoles are light greyish-brownish at night, shading to black during day, with

sparse dark melanophores, denser in the dorsal and lateral posterior part of the body. A

diamond-shaped translucent area is present between the eyes. Tail fins are transparent with a

darker pigmented border on external edges, broader in the posterior end of ventral fin. Above

the darker border, the tail is lightly scattered with dark spots. In preservative, the specimens

become darker but maintain the natural pattern. Tadpoles near metamorphosis begin to

acquire the adult pattern. Tadpoles in formalin kept the overall natural colour pattern,

whereas tadpole in ethanol showed a general shrinkage and loss of colour. Metamorphosing

toadlets are 10-15 mm long, with an overall coloration (white, red and black) similar to that of

the adults, although apparently less contrasted.

Source : MNHN, Paris

MERCURIO & ANDREONE 85

Fig. 1. - Lateral view of a tadpole of Scaphiophryne gottlebei. MRSN A4961, Gosner stage 38 (total

length 29.1 mm), from Zahavola, Isalo Massif.

Fig. 2. - Oral disc of Scaphiophrvne gorrlebei (based upon MRSN A2618) at Gosner stage 38

Source : MNHN, Paris

ALYTES 23 (3-4)

2. 3. Tadpole of Scaphiophryne gortlebei half-buried in the sand, a typical position assumed during the

day.

Source : MNHN, Paris

MERCURIO & ANDREONE 87

Observations in captivity and in nature confirmed that during the day the tadpoles stay

close to the bottom and often burrow within the bottom’s substrate with half the body

embedded in the sand and mud and with the tail projecting obliquely upwards at an angle of

about 30-45°. In this position, the tadpoles ingest particles of the substratum. At night they

leave the bottom and swim throughout the water column, often reaching the surface where

they ingest air.

Mantella expectata Busse & Bôhme, 1992 (fig. 4-5)

These tadpoles are of the benthic type (MCDIARMID & ALTIG, 1999).

The body is elliptical in lateral view and ovoid in dorsal view. The snout is dorsally

rounded, whereas in lateral view it slopes gently to the oral region and then turns strongly.

External nares are located dorso-laterally, almost half way from eyes to snout tip. The eyes are

small and directed dorsally.

Tail fins are low and of about equal height, the dorsal fin being lower than the ventral at

the level of the vent tube. The dorsal fin originates near the tail-body junction, and the ventral

fin at the posterior ventral end of the body. The maximum tail height is at the middle of the

tail. The tail tip is rounded with the tail muscle almost reaching the end of the tail.

The spiracle is sinistral with a mid-lateral opening directed posteriorly. The inner wall of

the spiracle is present and free from the body. The vent tube is parallel with the ventral margin

of the fin, tubular in shape and displaced dextrally, with a medial aperture.

The oral disc is antero-ventral, elliptical, emarginated, with a uniserial row of marginal

papillae in the lower labium and on the lateral side of the upper labium. Few submarginal

papillae are present in the lateral portions of the upper labium. The papillae are conical, with

rounded tips, unpigmented and translucent. The labial tooth row formula is 5(2-5)/3(1). The

upper jaw sheath is flat on its large medial part with a median concavity, the lower jaw sheath

is V-shaped: both are finely serrated and entirely pigmented in black.

In life, these tadpoles are uniformly brownish and speckled with sparse melanophores,

denser in the dorsal and lateral posterior part of the body. Tail fins are mainly transparent,

slightly scattered with dark spots, especially the dorsal fin. In preservative, the specimens

maintained the natural colour pattern.

The morphology of Mantella expectata tadpoles is similar to that of other mantellas of

the M. betsileo group, being of a generalized ranoid type. Tadpoles close to metamorphosis

begin to acquire the coloration typical of most of Mantella species: the back is brownish-

yellowish, and the flanks blackish. At metamorphosis the froglets measure about 10 mm.

HABITAT DESCRIPTION

The sandstone Isalo Massif is located within the Central Ecoregion (ANONYMOUS, 2003).

At the closest town, Ranohira, the mean monthly temperature is 25.1° C, with an absolute

minimum of 3.4° C (June): precipitation is concentrated in the rainy season from late October

to February (ANONYMOUS, 1999).

Source : MNHN, Paris

88 ALYTES 23 (3-4)

Fig. 4. — Lateral view of a tadpole of Mantella expectata. MRSN A3435, Gosner stage 37 (total length

28.5 mm) from Zahavola 1, Isalo Massif.

3, sant

im innnnses SEE

age 37

Source : MNHN, Paris

MERCURIO & ANDREONE 89

To provide indications about the ecological preferences in adults and tadpoles of S.

gottlebei and M. expectata, it is necessary to give an overall description of the Isalo Massif in

terms of habitat availability.

The three main habitat types recognised within the Isalo Massif are related to the

peculiar topography: (1) the savannahs, (2) open valleys, and (3) narrow canyons.

(1) The savannahs are subject to repeated fires and are covered with extensive meadows

with scattered trees and isolated forest parcels. The night-day temperature difference is high,

and the humidity is usually very low. Aquatic habitats are represented by temporary pools

(often used for cattle), streams and rivers. The temporary rivers are filled by seasonal rains,

and are dry for most of the year. A few permanent or semi-permanent rivers are present and

may be accompanied by gallery forests. At these habitats we found species which breed in

temporary waters (e.g., Boophis occidentalis, Laliostoma labrosum, Ptychadena mascarenien-

sis, Scaphiophryne brevis and Dyscophus insularis).

(2) The open valleys are usually crossed by permanent or semi-permanent torrents with

quite wide water beds, cascades and pools, and gallery forests of various sizes. We found frog

species that usually need permanent water to breed, such as Mantidactylus cf. femoralis,

Boophis goudoti and also Boophis occidentalis.

(3) The rocky and montane part is crossed by canyons of various lengths, widths and

depths, and with a variable water presence. Some canyons are very narrow with a sandy bed

delimited by vertical rock walls. The habitat is dark and sometimes quite similar to a cave, with

a rather low and constant temperature (19-22°C) and high humidity (about 100 %). Within

these close canyons, vegetation is absent (due to scarcity of light) or limited to a few isolated

trees. Typical species of this habitat are Scaphiophryne gottlebei, Mantidactylus corvus and

Mantella eXpectata.

The canyons can be ideally divided in four tracts, although not all of them are always

present: (a) savannah tract, with absent to low walls (0.5-1.5 m high), grass vegetation,

sandstone soil substratum with cobbles, small pools (0.1-0.2 m deep) with little or no

water, exposed to sunlight and subject to strong evaporation: (b) initial tract with medium-

high walls (1.5-5.0 m), if present high arboreal or shrub-like vegetation in the floodwater

bed, thin sandstone substratum with cobbles or isolated stones, and deep water-filled pools

(0.5-1,5 m), sometimes exposed to sunlight: (ce) gully tract, with high to very high vertical walls

(5.0 m and more), no vegetation, thin sandstone soil or rocky substratum, very deep water-

filled pools (1.5 m and more), generally no sunlight exposure (in some cases this tract may

have a cave-like aspect): (d) terminal tract, with high to very high vertical or concave walls

directly in contact with the watershed, possibly temporary waterfalls, absent or scarce

flood-water bed vegetation, water-filled pools of different depths, temporarily exposed to

sunlight.

Adults of S. gorrlebei were usually found within the canyons, where they burrow in the

sandy substrate or hide in cavities in the walls. In rare cases we found them outside the

canyons. As a consequence, the tadpoles were usually found in temporary pools excavated by

running water in the rocks within the narrow canyons, gully and terminal tracts (fig. 6). In

some cases, especially after heavy rainfalls, tadpoles were found in the initial tract. In

December 2004, we found tadpoles that had likely hatched at the beginning of October: after

Source : MNHN, Paris

Fig. 6.

ALYTES 23 (3-4)

Habitat of Scaphiophryne gottlebeï at Malaso, Isalo Massif. Gully tract of the canyon. with deep

and semi-permanent water pool.

Source : MNHN, Paris

MERCURIO & ANDREONE 91

more than two months, they were still without hind legs. For this reason, we suspect that

metamorphosis in this species takes 2-3 months, according to the local climatic conditions.

Adult individuals of M. expectata were found in open areas along the small streams quite

exposed to the sun. We usually did not observe the mantellas within the real canyons, although

in some occasions they were seen at the initial tract. The tadpoles were found in the small

pools in open areas, only rarely within the canyons. Tadpoles of M. expectata Were generally

found in the savannah and initial tract of canyons, quite exposed to the sunlight, although in

some cases they could be present in the other tracts (fig. 7). M. expectata breeds and completes

its larval development in about 1-2 months.

We also measured the chemical water parameters at two of the studied sites: (1)

“Zahavola 2” (presence of S. gortlebei tadpoles): water temperature 24°C, pH 5.23, conduc-

tivity 10.04 uS/cm, O, 8.8 mg/l; (2) “Zahavola 3” (presence of M. expectata tadpoles), water

temperature 26.6°C, pH 7.25, conductivity 8.07 uS /em, O, 2.7 mg/l.

DISCUSSION

The discovery and description of the tadpole of Scaphiophryne gottlebei allows us to

make some preliminary comparisons with the general morphology of tadpoles of other

species belonging to the genus Scaphiophryne. At present only the tadpoles of S. calcarata and

of the recently described S. menabensis are sufficiently known (BLOMMERS-SCHLÔSSER, 1975;

BLOMMERS-SCHLÔSSER & BLANC, 1991; GLos et al., 2005).

Concerning S. calcarata, the line drawing and the written description of the tadpoles

suggested that they were nektonic. The text also indicated that their beak was not keratinised.

As stressed in WASsERsUG’s (1984) study of the internal anatomy, this statement was wrong,

since these mouthparts are keratinised. Apart from this, the description of this tadpole does

not differ much from what we report for S. gortlebei. Both species have a terminal mouth

surrounded by dermal papillae. Possible differences concern the lack of the extended flap on

the lower lip and the narial position, which appears nearer to the tip of the snout in S.

calcarata and nearer to the eye in S. gortlebei.

The tadpole of Scaphiophryne gottlebei differs from that of S. menabensis by body shape,

by narial distances (nearer to the eye vs. same distance to snout tip and to eye). Similarities are

shared in the morphology of the oral dise with unpigmented jaw sheaths and marginal conical

papillae, and on the displacement of the spiracle (GLOS et al., 200$).

The tadpoles of Scaphiophryne gottlebei also show unique feeding habits and an asso-

ciated particular swimming behaviour. During the day they usually stay close to the bottom

and burrow within the substrate, propelled by intermittent movements of tail and body, with

half the body dug into the sand and with the tail obliquely upwards (at an angle of 35-40°). In

this half-buried position they ingest particles from the mud and sand substratum. In fact, in all

collected tadpoles the intestine was completely filled with detritus. During night time the

tadpoles leave the bottom and swim throughout the water column while apparently filtering

suspended particles. As far as known the only other tadpoles that show somewhat similar

habits belong to the microhylid Orophrvne robusta. This tadpole is a passive filter-feeder in a

Source : MNHN, Paris

ALYTES 23 (3-4)

Habitat of Manrella expectata at Lola, Isalo Massif. IL is represented by à temporary stream at

the beginning of the initial tract of the typical montane canyons

Source : MNHN, Paris

MERCURIO & ANDREONE 93

full fossorial habitat with related unique morphological features (WAsSERSUG & PYBURN,

1987).

The odd feeding habits make it hard to place the S. gortlebei tadpole in the ecomorpho-

logical categories of MCDIARMIG & ALTIG (1999). If forced into this classification, it should

be considered as intermediate between “suspension feeder type 2” and “suspension rasper”

and between “benthic” and “psammonic”. For this reason we coined the name “psammonek-

tonic” for a new ecomorphological category. This category describes a tadpole with kerati-

nised mouthparts and papillae, ventro-lateral spiracle, dorso-lateral eyes, feeding partially by

filtering suspended particles within the water column and by direct ingestion of substratum

through active burrowing, and active day and night.

Four other Scaphiophryne species (S. brevis, S. sp. from Andringitra [formerly attributed

to S. madagascariensis], S. madagascariensis from Ankaratra, and S. marmorata from Anda-

sibe area) were cursorily described by GLAW & VENCES (1994), VENCES et al. (2002) and BiGG1

(2002), but none of these data allows any detailed comparison. Anyhow, from the observa-

tions and photographs in these publications, we presume that the tadpoles of these species are

similar to that of S. gortlebei in having: (1) a ventro-lateral spiracle, (2) keratinized jaw sheaths,

(3) an absence of teeth, (4) dorso-lateral eyes, (5) a general robust body shape, and (6)

suspension and/or macrophagous feeding habits. Furthermore, these tadpoles are also tran-

sitional between benthic and nektonic morphotypes and feed on small particles. The general

morphological similarity is also confirmed by the photograph of S. madagascariensis from

Ankaratra (VENCES et al., 2002), that shows a tadpole very similar to that of S. gorrlebei herein

described.

Of the above mentioned characters, the presence in S. madagascariensis of keratinised

jaw sheaths, described by GLAW & VENCES (1994), has been recently confirmed by Haas

(2003). Maybe, as observed also in the tadpole description of S. calcarata, the presence of

unpigmented but keratinised jaw sheaths lead previous authors to mistake as they assumed

that keratinized tissue has to be black.

A more detailed comparative analysis of the Scaphiophryne tadpoles is much needed

because the scaphiophrynines have so far been alternatively included in the Ranidae, Micro-

hylidae or Hyperoliidae families (WasseRSUG, 1984) or even in a separate family (DUBOIS,

1992). The type 2 larva of ORTON (1953, 1957) was generally considered diagnostic of the

Microhylidae, but indeed larvae of scaphiophrynines and many other microhylids remain

unknown. As shown by BLOMMERS-SCHLÜSSER"s and WASSERSUG’s works, now confirmed by

the description of the S. gortlebei tadpole, the tadpole groups after ORTON often appear

inadequate to provide clear phylogenetic information. Furthermore, the inclusion the genus

Paradoxophyla within the Scaphiophryninae should be re-investigated, as this genus has a

sed filtering tadpole (ANDREONE et al., 2006). So far, the information available does not

provide an unequivocal indication.

Finally, tadpoles of the genus Mantella are less crucial in determining phylogenetic

allocation because they belong to the typical ranoiïd morph. Moreover, the genus Mantella

appears very homogeneous in terms of morphology and ecology. The only detailed data were

reported for M. aurantiaca by ARNOULT (1965) and later summarised by BLOMMERS-

SCHLÔSSER & BLANC (1991). Indeed, both species share a labial tooth row formula of

5(2-5)/3(1) and have an emarginated oral dise with papillae on the lower labium. Papillae in M.

Source : MNHN, Paris

94 ALYTES 23 (3-4)

expectata are displaced in a uniserial row whereas in M. aurantiaca they are apparently

biserial. In contrast, M. laevigata differs in having a reduced labial formula of 3(2-3)/3 or

4(2-3)/3(1-3) and a stronger and more notched horny beak (GLAW & VENCES, 1994). Further

comparisons with other species are not possible because of lack of information.

ACKNOWLEDGMENTS

This work was supported by the Nando Peretti Foundation, the National Amphibian Conservation

Center, the Declining Amphibian Population Task Force / IUCN (Seed Grants and Rapid Response

Fund), the Madagascar Fauna Group, Conservation International, Gondwana Conservation and

Research, and the Wildlife Conservation Society. Thanks are also due to the Malagasy authorities for

collection and export permits. G. Aprea, F. Mattioli, J. E. Randrianirina and T. J. Razafñndrabe assisted

in the field. M. Vences helped with the genetic species identification in the framework of a project founded

by the Volkswagen Foundation and with critical comments on an earlier draft of this paper. We are also

much grateful to R. Altigand A. Dubois, who were so patient to read, correct and comment several earlier

drafts of this manuscript, and to R. J. Wassersug for crucial bibliography.

LITERATURE CITED

ANONYMOUS [Projet ZICOMAJ, 1999. — Les zones d'importance pour la conservation des oiseaux à

Madagascar. Projet ZICOMA.

ANONYMOUS [Association Nationale pour la Gestion des Aires Protegées], 2003. — Plan de gestion du

réseau national des aires protégées de Madagascar. Revised version. Antananarivo, Madagascar,

ANGAP & Ministère de l'Environnement.

AuriG, R., 1970. — À key to the tadpoles of the continental Unites States and Canada. Herpetologica, 26:

180-207.

ALr16, R. & MCDIARMID, R. W,, 1999. - Body plan: development and morphology. Jn: R. W. MCDIARMID

& R. ALTIG (ed.), Tadpoles: the biology of anuran larvae, Chicago Univ. Press: 24-51.

ANDREONE, F., CADLE, J. E., GLAW, F., NUSSBAUM, R. A., RAXWORTHY, C. J., VALLAN, D. & VENCES, M.

2005. - Species review of amphibian extinction risks in Madagascar: conclusions from the Global

Amphibian Assessment. Conserv. Biol., 19 (6): 1790-1802.

ANDREONE, F. & LUISELLI, L., 2003. - Conservation priorities and potential threats influencing the

hyper-diverse amphibians of Madagascar. 1. J. Zool., 70: 53-63

ANDREONE, F., APREA, G., ODIERNA, G. & VENCES, M., 2006, - À new narrow-mouthed frog of the genus

Paradoxophyla (Microhylidae: Scaphiophryninae) from Masoala rainforest, northeastern Mada-

gascar, Acta herp., 1: 15-27.

ARNOULT, J., 1965.- Contribution a l'étude des Batraciens de Madag:

Mantella aurantiaca Mocquard, 1900. Bull. Mus. natn. Hist. nai

BiGGi, E., 2002, — Marmo in terrario. Allevamento e riproduzione di Scaphiophryne marmorata. Aqua-

rium, 5: 60:

BLOMMERS-SCH , R. M. À. 1975. - Observations on the larval development of some Malagasy

frogs, with notes on their ecology and biology (Anura: Dyscophinae, Scaphiophryne and Cophy-

linac). Beaufortia, 24: 7-26.

BLOMMERS-SCH , R. M. À. & BLANC, C. P, 1991. - Amphibiens (première partie). Faune de

Madagascar, 75 (1): 1-380.

E, K. & BôHME, W., 199:

Mantellinae) and Scaphiophryne (Microhylida

gascar. Rev. fr. Aquariol., 19 (1-2): 57-64.

Bus Two remarkable frog discoveries of the genera Mantella (Ranidae

aphiophryninae) from the west coast of Mada-

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MERCURIO & ANDREONE 95

GLaw, FE & VENCES, M., 1994. — 4 field guide to the amphibians and reptiles of Madagascar. 2“ edition,

including mammals and freshvater fish. Kôln, Vences & Glaw Verlag: 1-480.

GLos, J., GLAW, F. & VENCES, M., 2005. — À new species of Scaphiophryne from western Madagascar.

Copeia, 2008 (2): 252-261.

Gosner, K. L., 1960. — A simplified table for staging anuran embryos and larvae with notes on

identification. Herpetologica, 16: 183-190.

Haas, A., 2003. — Phylogeny of frogs as inferred from primarily larval characters (Amphibia: Anura).

Cladisties, 19: 23-89.

McDiarmiD, R. W. & ALTIG, R., 1999. - Materials and techniques. fr: R. W. MCDiarMiD & R. ALTIG

(ed.), Tadpoles: the biology of amuran larvae, Chicago Univ. Press:

Ortow, G. L., 1953. - The systematics of vertebrate larvae. Syst. Zool., 2: 63-75.

1957. - The bearing of larval evolution on some problems in frog classification. Syst. Zool., 6: 79-86.

PALUMBI, S. R., MARTIN, À., ROMANO, $., MCMILLAN, W. O., Sricr, L. & GRAROwSKI, G., 1991. — The

simple fool's guide to PCR, Version 2.0. Privately published document compiled by S. Palumbi,

Dept. Zoology. Honolulu Univ.

Vencrs, M. GLAW, F. & BÔHME, W. 1999. — A review of the genus Mantella (Anura, Ranidae,

Mantellinae): taxonomy, distribution and conservation of Malagasy poison frogs. Alytes, 17 (1-2):

VENCES, M., APREA, G., CAPRIGLIONE, T., ANDREONE, F. & ODIERNA, G., 2002. - Ancient tetraploidy and

slow molecular evolution in Seaphiophryne: ecological correlates of speciation mode in Malagasy

relict amphibians. Chrom. Res. 6.

WassERSUG, R. J., 1984. — The Pseudohemisus tadpole: a morphological link between microhylid (Orton

type 2) and ranoïd (Orton type 4) larvae. Herpetologica, 40: 138-149.

WassersuG, R. J. & PyaurN, WF, 1987. — The biology of the Pe-ret’ toad, Orophryne robusta

(Microhylidae), with special consideration of its fossorial larva and systematic relationships. Zool.

J. Linnean Soc., 91: 137-169.

“

Corresponding editor: Alain DUBOIs.

APPENDIX

LIST OF EXAMINED SPECIMENS

All the collecting sites are within Ranobhira Fivondrononana, Fianarantsoa Faritany,

Madagascar. An asterisk (*) indicates ethanol fixed specimens.

Scaphiophryne gottlebei Busse & Bôhme, 1992: MRSN A2618 (n= 1) and A2619* (n=1),

Isalo Massif, Parc National de l’Isalo, Vallée du Petit Nazareth, 22°32.9/’S, 45°21.72'E,

890 m, leg. V. Mercurio, 2.11.2004; MRSN A49%61 (7 = 3), Isalo Massif, Parc National

de l’Isalo, Marojana River, 22°27.43'S, 45°22.40'E, 867 m, leg. V. Mercurio, 15.X1.2004;

MRSN A4962 (n = 6), Isalo Massif, Zahavola 2, 22°37.38'S, 45°21.52°N, 825 m, leg. F.

Andreone, F. Mattioli & V. Mercurio, 20.X1.2004.

Mantella expectata Busse & Bôhme, 1992: MRSN A3432 (n = 22) and MRSN A3433

(1 = 23), Isalo Massif, Andranomena, 45°18.86'E, 22°45.71'S, 786 m, leg. F. Andreone, V.

Mercurio & J. E. Randrianirina, 28.1.2004; MRSN A3434, (n = 2), Isalo Massif, Parc

National de l’Isalo, Zahavola 3, 45°21.48"E, 22°37.5L'S, 835 m, leg V. Mercurio, 2.11.2004;

MRSN A3435 (n = 2), Isalo Massif, Pare National de l'Isalo, Andohasahenina, 45°17.28'E,

22°49.79'S, 630-680 m, leg. F. Andreone, G. Aprea, V. Mercurio & J. E. Randrianirina,

15.1.2004.

Source : MNHN, Paris

Alytes, 2006, 23 (3-4): 96-102.

Description of the tadpole

of the Malagasy treefrog

Boophis andohahela

Meike THOMAS*, Liliane RAHARIVOLOLONIAINA**,

Frank GLAW*** & Miguel VENCES****

* Department of Genetics, University of Cologne, Zülpicher Strasse 47, 50674 Kôln, Germany

<meike.thomas@uni-koeln.de>

** Département de Biologie Animale, Université d'Antananarivo,

Antananarivo 101, Madagascar

##* Zoologische Staatssammlung, Münchhausenstr. 21, 81247 München, Germany

###* Institute for Biodiversity and Ecosystem Dynamics, Zoological Museum,

University of Amsterdam, Mauritskade 61, PO Box 94766, 1090 GT Amsterdam, The Netherlands !

We describe the larval stages of the Malagasy treefrog Boophis ando-

hahela, based on specimens identified by their DNA sequences. The

tadpoles were collected in a stream pool under a waterfall and were

dwelling on submerged rocks. They show a rather distinctly flattened and

convex body shape. Their oral disk structure and labial tooth row formula

(2:4+4/1+1:2) is similar to those of other representatives of the Boophis

luteus species group.

INTRODUCTION

The genus Boophis Tschudi, 1838 contains a radiation of treefrogs which belongs to the

endemic family Mantellidae from Madagascar and the Comoro island of Mayotte (VENCES

et al., 2003). The genus currently contains about 48 species (GLAW & VENCES, 2003), but

new taxa are continuously being discovered, and many species have been already identified

and await formal description (VALLAN et al., 2003). Frogs of this genus are arboreal, with

typical treefrog habitus: enlarged finger dises, broad and anteriorly rounded head, large eyes

and no dorsolateral ridge (GLAW et al., 2001). According to BLOMMERS-SCHLÔSSER & BLANC

(1991) and GLaw & VENCES (1994), seven phenetic species groups are distinguished in the

genus.

Within Boophis, two major clusters can be distinguished depending on the site of

reproduction: the pond breeders of the Boophis tephracomystax group appear to be charac-

terized by ancestral states of several characters (VENCES et al., 2002) but they were grouped as

roup in a more recent analysis (VENCES et al., 2003). It is clear, however, that

a homophyletie

: Zoological Institute, Technical University of Braunschweig, Spielmannstr. 8, 38106

Germany

1. Current add

Braunschwei:

Source : MNHN, Paris

THoMas et al 97

the species-rich assemblage of brook-breeders is a homophyletic, probably monophyletic

group (RICHARDS et al., 2000; VENCES et al., 2002, 2003).

One of the species assemblages in this lotic lineage is the Boophis luteus group that

contains a number of morphologically extremely similar, medium-sized green-coloured

treefrogs. The number of species in this group has climbed up from one (BLOMMERS-

SCHLÔSSER & BLANC, 1991) to 12 (GLaAw & VENCES, 2002). Larval stages are known for only

three of these, Boophis luteus (Boulenger, 1882), Boophis ankaratra Andreone, 1993 and

Boophis jaegeri Glaw & Vences, 1992 (BLOMMERS-SCHLÔSSER, 1979; GLAW & VENCES, 1994).

We here describe the tadpole of one further species of the B. luteus group, Boophis andohahela

Andreone, Nincheri & Piazza, 1995.

MATERIAL AND METHODS

Specimens were collected in January 2003 in Ranomafana National Park, Fianarantsoa

Province, southeastern Madagascar, from a brook in the rainforest. The habitat was a pool

underneath a waterfall (ca. 847 m above sea level; 21°15.77S, 47°24.78'E), which dropped

down about five meters along rocks. The pool was very deep (more than 2 metres) and had a

diameter of at least seven metres. Specimens were attached to the submerged rocks in the pool

and were found on rocks in quiet water areas as well as on rocks positioned in strong current.

Collected specimens were anesthetized and killed in a solution of highly concentrated

chlorobutanol. The dead tadpoles were assigned to morphotype categories using a stereomi-

croscope. From one specimen of each of these categories a piece of tail was taken as a DNA

tissue sample. Subsequently all tadpoles were preserved in 4 % buffered formalin. Adult and

larval voucher specimens were deposited in the herpetological collections of the Université

d’Antananarivo, Département de Biologie Animale (UADBA), Zoologische Staatssam-

mlung München (ZSM) and the Zoological Museum Amsterdam (ZMA).

Species identification was based on DNA sequences. We amplified a fragment of about

500 bp of the mitochondrial 165 rRNA gene of each tadpole sample, using primers and

protocols described in THOMAS et al. (2005), and compared it with homologous sequences of

adult specimens. DNA sequences were deposited in Genbank (accession numbers AY863216-

AY863217 for the two tadpole DNA vouchers, and AY848447-AY 848448 and AY 848456 for

three comparative adult specimens).

Drawings and descriptions are based on the DNA voucher, and other representative

specimens of the same series were used to supplement structures missing because of tissue

sampling. In order to assess morphological variability, measurements were taken from six

specimens of the series g dial calipers: values were taken to the nearest 0.1 mm. AIl

tadpoles were staged according to GOsnER (1960). Terminology is based on ALTIG &

MCDiarMiD (1999) with some modifications. Body length is estimated by measuring the

distance from the tip of the snout to the body terminus, which is the junction of the posterior

body wall with the tail axis (ALTIG & MCDIARMID, 1999). Tail length is defined as the distance

from the body terminus to the absolute tip of the tail (ALTIG & MCDiaRMID, 1999). Total

length is the sum of body length and tail length. Body width is measured at the widest point

Source : MNHN, Paris

98 ALYTES 23 (3-4)

of the “head” right behind the eyes, not in the intestinal part. Eye diameter is the maximum

width of the orbit. Interorbital distance is measured between the centres of the pupils;

internarial distance is measured between the centres of the nares. The distance between tip of

snout and naris is taken to the centre of the naris. Distance between naris and eye is measured

from the centre of naris to the anterior edge of the eye. Distance between tip of snout and

spiraculum is also taken up to the centre of the spiracular aperture. Tail muscle height is first

measured vertically from the junction of the body wall with the ventral margin of the tail

muscle and secondly measured at midtail. Tail height including fins and caudal musculature is

taken at its maximal vertical extent. Dorsal fin origin is defined relatively to the tail body

junction. The formula of labial tooth rows follows Dugois (1995). The mouthparts include

upper tooth rows (UTR) and lower tooth rows (LTR).

RESULTS

Boophis andohahela was described from Andohahela National Park in south-eastern

Madagascar (ANDREONE et al., 1995). Our surveys of south-eastern rainforests yielded, in

2003 and 2004, several specimens that agreed with this species in general morphology and

coloration: (1) at Ambatolahy forest next to Ranomafana National Park, 21°14.632'S,

47°25.57YE, 915 m a.s.I. (specimens ZMA 20017-20018 and 20304, collected in February

2004); (2) close to the first locality, between Vohiparara and the entrance of Ranomafana

National Park, no coordinates taken (specimens ZSM 665.2003, collected on 17 January

2003); (3) at Vevembe forest, close to Vondrozo, 22°47.686'S, 47°11.228'E, 581 m a.sil

(specimens ZMA 20019 and 20125-20126, and UADBA 24292, collected on 10 February

2004). Specimens from Vevembe were observed calling, their advertisement calls fully corre-

sponding to those of topotypical specimens as described by ANDREONE et al. (1995). DNA

from three of these adult specimens was sequenced, the two sequences from the Ranomafana

region (specimens ZMA 20018 and ZSM 665.2003) resulting fully identical, the one from

Vevembe (ZMA 20125) having 6 substitutions compared to those from Ranomafana (1.2 %

pairwise sequence divergence).

Two tadpole series from Ranomafana with the field numbers FG/MV 2002.1802 (cata

logued a M 667.2004) and FG/MV 2002.1803 (catalogued ZSM 668.2004) had sequences

fully identical with the adult sequences from Ranomafana, and their sequences strongly

differed from all other frog species studied in this region. In terms of DNA barcoding we

therefore consider these tadpoles to be reliably identified. We based the following description

on a subset of the specimens from one of these series (ZSM 667.2004). Specimens from the

second series agreed in general morphological features.

Larvae of B. andohahela are exotrophic and benthic tadpoles of ORTON"s (1953) type IV.

The coloration shows irregular pattern of dark areas on a light ground. The intestinal spiral

is clearly visible through the abdominal wall. In life, most of the observed specimens showed

a yellow coloration on the tail: the fins were almost without pigmentation, just a yellow

glimmer was visible.

We selected the DNA voucher of the series ZSM 668.2004 and five additional tadpoles of

s, Of representative size and stage, and in good state of preservation, for the

this same ser

Source : MNHN, Paris

THoMas et al 99

EE ra

(}

Eve HA

1 mm

Fig. 1. Drawings of a tadpole of Boophis andohahela from the series ZSM 667.2004 . On top (A) the

specimen is shown in dorsal view with its relatively large eyes, in lateral view (B) the very low body

shape is visible: the oral apparatus (C) shows the dense row of marginal papillae with its large

medial gap in the upper labium and its small gap in the lower labium

description. The DNA voucher specimen had a part of the tail removed for DNA extraction.

All specimens were in stage 25. Detailed morphometric data of the specimens are given in tab.

1. The larvae of B. andohahela have a total length of 21.84 + 0.76 mm (mean + standard

deviation). They show an oval to more of less rhombic body shape in dorsal view (fig. IA) and

the body width is about 58 % of body length. The snout is flatly rounded, and the upper

Source : MNHN, Paris

100 ALYTES 23 (3-4)

Table 1. — Morphometric measurements (mm) of six tadpole specimens of Boophis andohahela

(series ZSM 667.204, all in stage 25) collected in Ranomafana National Park.

Character n Mean sindard Minimum | Maximum

deviation

Body length 6 8.03 0.66 73 8.9

Tail length 5 13.98 0.58 13.5 14.9

Total length 5 21.84 0.76 20.8 22.6

Body width 6 4.66 0.52 43 57

Eye diameter 6 1.20 O1 11 14

Interorbital distance 6 3.02 0.19 2.9 34

Internarial distance 6 137 0.05 13 14

Distance snout-naris 6 125 0.12 1.0 13

Distance naris-eye 6 1.78 0.12 16 1.9

Distance snout-spiraculum | 6 4.82 0.38 43 54

Tail musele height 1 6 2.60 0.09 2.5 21

Tail muscle height 2 6 2.05 0.08 2.0 22

Fin height 6 3.30 028 28 36

mouthpart is anterior. The eyes are relatively large (diameter about 15 % of body length).

They are positioned dorsally and directed dorsolaterally. In ventral view the eyes are not

visible. The internarial distance is about 45 % of the interorbital distance. The rounded naris

is moderate in size, directed dorsally and positioned closer to the snout than to the eyes. In

lateral view (fig. 1B), the body shape is very depressed and in some specimens shows an

extreme concave shape ventrally. The snout is rounded. The spiracle is sinistral and #%!" of the

tube are attached to the body wall; it is positioned laterally (closer to venter than to dorsum)

and oriented posterodorsally. The spiracular opening is oval and situated slightly below the

level of the apex of myotomes of tail musculature. The tail musculature is strong, of almost

uniform height until the midtail; in the distal half of the tail the musculature is gradually

tapering and almost reaches the tail tip. The fins are moderate. The dorsal fin originates near

the dorsal tail body junction, but really expands just after one fourth of the tail length. Like

the ventral fin, the dorsal fin has a concave shape. The point of maximun fin height is located

in the third fourth of the tail. The anal tube is short, tubular and medial with a lateral

displacement to the right, the opening is directed posterolaterally.

The oral apparatus (fig. 1C) is generalized. Itis positioned ventrally and there is no lateral

emargination present. The upper labium shows a large medial papillae gap. The rest of the

oral disc is bordered by a dense row of marginal papillae, except a small part in the middle of

the lower labium. Submarginal papillae are present in the lateral parts and cover almost the

whole lower labium, just a small area in the middle being free of submarginal papillae. The

labial tooth row formula is 2:4+4/1+1:2. In the upper labium, the tooth rows become

continuously shorter from UTR, to UTR,. UTR; is the first row that touches the beak. LTR,

has a short medial gap. The jaw sheaths are slightly serrated: the coloration is white with black

pigmentation. On the upper labium the beak has a wide opened reversed U-shape, whereas the

lower beak is a compact element with a slight V-shaped grooving.

Source : MNHN, Paris

THOMAS et al 101

DISCUSSION

DNA barcoding has proven to be a valuable tool to assign larval stages to adult species,

especially in cases were rearing would be very time-consuming (HEBERT et al., 2004; THOMAS

et al., 2005). In the case study reported here, we have even used this method first to assess the

conspecificity of adult specimens from several localities, and in a second step to verify tadpole

identification. In Boophis andohahela, as in other species of the B. luteus group, the original

green colour quickly fades to yellow and later to white, with the slight species-specific

chromatic characters totally vanishing. Even living frogs have few diagnostic characters, and

the most distinct one (light dorsolateral lines on the anterior part of the body) can also be

found in other species. Hence, the only adult specimens in our collection that could be reliably

identified using traditional methods were those from Vevembe, because here we could collect

them while emitting their diagnostic advertisement calls (described by ANDREONE et al., 1995).

These differ clearly from those of all other representatives of the B. luteus group, except

B. jaegeri (see GLAW & VENCES, 2002) which strongly differs genetically. Adult specimens

collected at Ranomafana were assigned to B. andohahela because of agreement in live

coloration and low genetic differences to a specimen from Vevembe. In turn, tadpoles from

Ranomafana were identical in their DNA sequence to adults from this region. Altogether five

DNA sequences of B. andohahela (two tadpoles and three adults) were available, and the

differences among these were much lower than to all other species of Boophis, confirming the

validity of molecular taxonomy to identify larval stages of tropical anurans.

According to BLOMMERS-SCHLÔSSER (1979) and GLAW & VENCES (1994), the tadpoles

assigned to B. luteus and B. jaegeri are characterized by the following morphologies: labial

tooth formula 1:5+5/3 or 1:4+4/3 with a large number of papillae, gap in papillae on the upper

labium and median gap on the lower labium; body not conspicuously flattened in B. luteus,

slightly flattened in B. jaegeri. Hence, the general oral morphology of B. andohahela agrees

relatively well with its close relatives. Its rather flattened, almost concave ventral body shape

might be an adaptation to adhesion to submerged rocks in strong currents and reminds

tadpoles of B. ankaratra (as briefly described in GLAW & VENCES, 1994) and of representatives

of other species groups: Boophis majori (Boulenger, 1896) (Boophis majori group), Boophis

erythrodactylus (Guibé, 1953) and Boophis mandraka Blommers-Schlôsser, 1979 (Boophis

rappiodes group). This indicates that several characters of the tadpole morphology in Boophis

have undergone extensive parallel evolution in similar habitats. Deciphering the pathways and

ecological correlates of the recurrent adaptations to more or less extreme lotic conditions

must await a better knowledge on the phylogeny of these frogs, and the descriptions of the

larval stages of more species.

ACKNOWLEDGEMENTS

We are grateful to M. Puente, D. R. Vieites and W. Vôrde Zum Sieve Vôrding for their help in the

field. Special thanks are due 10 D. Tautz (Cologne) who made it possible 10 obtain the DNA sequences in

his lab, Permits for collection and export of specimens were kindly issued by the Ministère des Eaux et

Source : MNHN, Paris

102 ALYTES 23 (3-4)

Forêts of Madagascar. This work was carried out in the framework of a cooperation accord among the

Département de Biologie Animale, Université d'Antananarivo, the Association Nationale pour la

Gestion des Aires Protégées (ANGAP) and the Zoologische Staatssammlung München, and supported

by grants of the Volkswagen Foundation and the Deutscher Akademischer Austauschdienst.

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& R. ALTIG (ed.), Tadpoles: the biology of anuran larvae, Chicago, University of Chicago Press:

24-51.

ANDREONE, F,, NINCHERI, R. & PIAZZA, R., 1995. - Un nouveau Boophis vert (Ranidae: Rhacophorinae)

des fôrets pluviales du Sud de Madagascar, Rev. fr: Aquariol., 21: 121-127

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(Rhacophoridae). Bijdr. Dierkunde, 49 (2): 261-312.

BLOMMERS-SCHLÔSSER, R. M. A. & BLANC, C. P. 1991. — Amphibiens (première partie). Faune de

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Dusors, A., 1995. — Keratodont formulae in anuran tadpoles: proposals for a standardization. J. 2001.

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GLaw, FE, VENCES, M. ANDREONE, E & VALLAN, D., 2001. — Revision of the Boophis majori group

(Amphibia: Mantellidae) from Madgascar, with description of five new species. Zoul. J linn, Soc.,

133: 495-520.

Goswer, K.L., 1960. - A simplified table for staging anuran embryos and larvae with notes on identifi-

cation. Herpetologica, 16: 183-190.

HegerT, P. D. N., PENTON, E. H., BURNS, JL. M. JANZEN, D. H. & HaLLwWACHS, W, 2004. — Ten species in

one: DNA barcoding s cryptic species in the neotropical skipper butterfly Astrapres fulgera-

tor. Proc. natl. Acad. S A, 101: 14812-14817.

Orron, G, L., 1953. - The systematics of vertebrate larvae. Sysr. Zoo. 2: 63-75.

RicHarDs, M. C., NUSSBAUM, R. A. & RaxWORTHY, C. J., 2000. - Phylogenetic relationships within the

madagascan boophids and mantellids as elucidated by mitochondrial ribosomal genes. African J

THOMAS, M. RAHARIVOLOLONIAINA, L., GLAW, F, VENCES, M. & VIEITES, D. R., 2005. - Montane

tadpoles in Madagascar: molecular identification and description of the larval stages of Manti-

dactylus elegans, M. madecassus and Boophis laurenti from the Andringitra Massif. Copeia, 2005:

174-183.

VaLLAN, D., VENCES, M. & GLAW, E, 2003. - Tivo new species of the Boophis mandraka complex (Anura,

Mantellidae) from the Andasibe region in eastern Madagascar. Amphibia-Reptilia, 24: 305-319.

Vexcrs, M., ANDREONE, F, GLAW, F, KosucH, J, MEVER, À., SCHABFER, H.-C. & VerrH, M., 2002. —

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Corresponding editor: Stéphane GROSIEAN.

Source : MNHN, Paris

Alytes, 2005, 23 (3-4): 103-122. 103

Description of advertisement calls

of six species

of the genus Chaparana (Ranidae)

from Nepal and India

Stéphane GROSIEAN & Alain DuBoIs

Reptiles et Amphibiens, USM 602 Taxonomie & Collections,

Département Systématique & Evolution, Muséum national d'Histoire naturelle,

25 rue Cuvier, 75005 Paris, France

<sgrosjea@mnhn.fr>, <adubois@mnhn.fr>

The advertisement calls of six species of the genus Chaparana (sub-

genus Paa) are described in details, those of two of them (Chaparana

minica and Chaparana vicina) for the first time. For each species various

temporal and frequency parameters are given. Each call is illustrated by an

oscillogram, a spectrogram and a spectrum. The general characteristics of

these peculiar calls are discussed as adaptations to a noisy torrent environ

ment. The calls and modes of life of these frogs are consistent with their

taxonomy based on morphological and molecular characters.

INTRODUCTION

This paper is devoted to the description of the advertisement calls of six species of the

subgenus Paa of the genus Chaparana Bourret, 1939, as redefined by OuLer & DuBois (2006).

This genus of the ranid tribe Paini (DuBois, 1992; OuLer & DUBoIs, 2006) includes 26 species

distributed in South and Southeast Asia (Pakistan, India, Nepal, western China through

Myanmar, Thailand, Laos, Cambodia and Vietnam) (DuBois, 1976; FRosT, 1985; 1999).

The species of the genus Chaparana are torrent-living species. The males of these species

usually call at night from the bed of the torrent, very often hidden under stones and rocks or

below the bank, more rarely sitting in the water in more open places of the torrent bed

(Dumois, 1976, 1977b). They are distributed along the torrent which avoids interactions

between them (Dugois, 1977b). The loud and continual background noise of the running

water as well as their calling sites triggered the frogs to develop an adve

to this environment, a type of call seldom encountered in the other species of Ranidae, except

for those living in the same kind of habitats, such as Amolops (DuBois, 19774). The calls of

some of the species described hereafter have already been briefly described by Dugois (1977b).

We decided to redescribe them to provide parameters which were not measured at that time

and to give standard descriptions of calls which can be used for comparison in future studies.

sement call adapted

Source : MNHN, Paris

104 ALYTES 23 (3-4)

The calls of six species of Chaparana ( Paa) were recorded during field work in Nepal and

India by the second author in 1972, 1973 and 1977 (tab. 1). However, the distributions of these

species are larger: Chaparana (Paa) rostandi lives in Nepal only, Chaparana (Paa) vicina

oceurs in India and Pakistan, Chaparana ( Paa) minica in India and Nepal, and Chaparana

(Paa) blanfordii, Chaparana ( Paa) liebigii and Chaparana ( Paa) polunini are found in Nepal

and China (Dugois, 1976, 1980, 2000; Frosr, 1985). They are all mountain species which

oceur mostly at high altitudes.

MATERIAL AND METHODS

Recordings (tab. 1) were made using either a Uher Report 4000 or a Sony TCDM-S tape

recorders, and Scotch magnetic 215 and TDK SA-X90 tapes. Oscillograms, spectrograms and

spectrums were prepared with the software tool Canary 1.2 from the Cornell Laboratory of

Ornithology (CHARIF et al., 1995). The sampling rate used to convert the signals to digital

format was 22.254 Hz with 16-bit precision. A filter bandwidths of 349.70 Hz and frame

length of 512 points were used for both spectrogram and spectrum analyses.

The following measurements were taken from the oscillogram: duration of calls (dc),

duration of notes (dn) and intervals between notes (din), number of notes per call (nn) and

note rate (number of notes per second, nns). Frequency measurements were made from the

spectrum of a few notes within the signals. The frequency values given (in text and tab. 2) are

the means of the values of the same frequency band of those notes. The visible frequency

bands are noted f1b to f5b (when possible) from the fundamental frequency to the highest

harmonie.

The recording of the call of C. vicina was interfered by a significant background noise. So

we used the software Signalyse 3.10 which proves to be more efficient to filter signals:

frequencies below 300 Hz and above 500 Hz were cut off, oscillograms and spectrogram were

built with Canary 1.2. The call of €. minica was recorded with deficient batteries in the tape

recorder. So one can hear an important speed difference when the tape is played with a Uher

in good condition. The tape was re-recorded using the human voice on the tape as an

indication for the adequate speed (original speed 17.6 cm/s instead of 19.0 cm/s, that is to say

—7.5% of the normal speed). Therefore there is a probable (slight) error on the measurements

of the parameters for time and frequency. The latter should be considered with caution and

rounded off (the margin of error could not be estimated). However it seemed useful to publish

a description of this call as data concerning this species are rare.

Al the specimens are deposited in the collection of the Muséum National d'Histoire

Naturelle of Paris (MNHN).

Except for C. vicina, no males whose calls are studied here could be caught, so it is

impossible to give a voucher number for each animal. Snout-vent lengths were estimated by

averaging the snout-vent lengths of males caught in the same population as the singer

(Dusois, pers. obs.). The MNHN collection numbers of the individuals taken into consider-

ation for calculation of the means are the following: (1) €. blanfordii: 1975.1056-1058; (2)

C. liebigii: 1975.1093, 1975.1097-1098, 1975.1102, 1975.1105-1107, 1975.1109-1112; (3)

Source : MNHN, Paris

Table 1. List of the species studied with information on the place and date of recording, Air T°: air temperature; Water T°: water temperature.

Species Date and hour of recording Country Locality Coordinates | Altitude | Air T° |Water T° 2

(Chaparana (Paa) blanfordii (Boulenger, 1882)| 05.05.1973: 19h25-22h00 Nepal Lam Pokhari |27°06°N,87°59°E] 2910 m No data No data £

Chaparana (Pau liebigii (Günther, 1860) 25.06.1973: 20h30 Nepal Ghat 2TASN,8643E) 2510m | 150°C | 14.5°C ë

Chaparana (Pau) minica (Dubois, 1975) 03.08.1977:22h50 | India (Himachal Pradesh) Katrain |32°08"N,77°09"E) 1530m | 21.0°C | 240°C &

Chaparana (Paa) polunini (Smith, 1951) 23.06.1973: 20h20 Nepal Thammu [2749 86%4/E) 3360m | 12.5°C | 11.5C el

Chaparana (Pa) rostandi (Dubois, 1974) 21.08.1972: 23h00 Nepal Kalopani |28938°N,83936E) 2540m | 160°C | No data ë

04.09.1972 Û 4 ” b 145C | 11.5C a

31.08.1972: 20h4t + Kutsab Terna Tal |28°46°N, 83°43°E) 2890 m 16.5°C 19.0°C

Chaparana (Pau) vicina (Stoliezka, 1872) 10.07.1977 India (Jammu & Kashmir) | __ Patnitop __|33°02°N, 75°20°E/2050-2060 m| 19°C | No data

Source : MNHN, Paris

106 ALYTES 23 (3-4)

Fig. 1. Chaparana ( Paa) blanfordii (Boulenger, 1882): female MNHN 1975.1056, Chauki (East Nepal),

15 July 1973

C._ minica: 1989.2057-2058, 1989.2060, 1989.2062, 1989.2064-2067, 1989.2069-2070,

1989.2072, 1989.2075, 1989.2077-2083; (4) C. polunini: 1975.1441-1446, 1975.1457-1458; (5)

€. rostandi (Kalopani): 1975.959, 1975.962-964; C. rostandi (Kutsab Terna Tal): 1973.310,

1973.320-321; (6) C. vicina: 1985.1047.

Dates and times of recordings are provided in tab. 1, together with the data on temper-

ature (air and water) when available.

RES

JLTS

CuaparaNa (Pas) 8LaNrorDu (Boulenger, 1882)

Chaparana blanfordii (fig. 1) was recorded during the rainy season in a humid forest rich

in small torrents, where calls could be heard all around both during day and night. The call

was recorded at night in a small torrent running under trees. The males were calling from the

bed of the forest torrent hidden between rocks, so not directly from the ground. Several males

were calling widely spaced in this torrent.

The call of this species (fig. 2, tab. 2) is short, high-pitched and repetitive. It consists

in continuous series of 15-17 short amplitude modulated notes with two lobes (0.026 s

Source : MNHN, Paris

Table 2. - Characteristies of the advertisement call of Chaparana (Paa) blanfordii and Chaparana (Paa) liebigii from Nepal, Chaparana (Paa) minica

from India, Chaparana (Paa) polunini, Chaparana (Paa) rostandi and Chaparana (Paa) vicina from Nepal. Only one male was recorded for

each species except for P. rostandi whose calls of three different males were recorded.

SVL, male snout-vent length; de, duration of sequences from first to last note; dic, duration of silent intervals between two consecutive

sequences; dn, duration of notes; din, duration of silent intervals between two consecutive notes; nn, number of notes per call; nns, number of

notes per second: fib, frequence of the band i. Snout-vent lengths are expressed in mm, time measurements in seconds and frequencies in Hz.

Value are given as: mean + standard deviation, minimum-maximum, number of measurements.

Species

Chaparana blanfordii

{Lam Pokhari)

Chaparana liebigii

(Ghat)

Chaparana minica

(Katrain)

Chaparana polunini

CThammu)

Chaparana rostandi

(Kalopani)

Chaparana rostandi

Kutsab Terna Tal)

Chaparana vicina

(Patnitop)

MNHN 1985.1047

SVL de dic dn din nn nns flb 2b f3b f4b f5b

3.96 + 0.44 0.025 + 0.009 | 0.236 + 0.019! 16.0+ 1.4 | 4.1+0.1 | 1529+ 37 |3076+ 102! 4631 + 87

3.65-4.27 _ 0.010-0.044 15-17 4.0-4.1 1469-1548 | 2860-3194 | 4487-4741 _ _

3 2 32 8 7 8 Q

70.1 + 9,7 |2.26 + 0.02 0.021 + 0.003 | 0.130 + 0.032 730 + 52 8

56.4-89.5 | 2.25-2.28 _ 0.016-0.026 | 0.097-0.254 15-16 686-784 _ = à £

31 29 2 9 >

0.087 + 0.017 | 0.207 + 0.061 | 13.54 3.0 | 3.540.2 | 1134443 | 2274 + 78 |3430 + 116|4497 4 116]5639+ 116 é

à 0.044-0.127 | 0. -0.466 10-19 1097-1215 | 2136-2410 | 3252-3625 | 4310-4643 | 5486-5780

8 72 6 20 20 17 10 9 8

0.019 + 0.007 | 0.093 + 0.25 | 10.340.6 | 9.8+0.4 | 164240 | 32744 11 | 4954445 E

_ 0.003-0.030 | 0.073-0.210 10-11 3260-3284 | 4902-4995 _ _ a

31 28 8 4 6

0.055 + 0.006 | 0.216 + 0.029 1593 + 10413138 + 247 | 4686 + 326

æ 0.046-0.061 | 0.186-0.255 1371-1646 | 2645-3272 | 4056-4918 _ _

7 5 7 7 6

SL7ESS 0.054 + 0.012 | 0.144 + 0.016 1949 + 16513923 + 3786178 + 117

46.0-58.7 _ 0.029-0.068 | 0.127-0.177 1646-2077 | 3194-4212 | 6034-6289 =. _

4 Z il # LL à L 6

49.8 + 1.0 0.6 0.059 + 0.005 012 1641 + 120]3262 + 232 |4883 + 332

49.0-50.9 _ 0.055-0.065 -0.145 1469-1724 | 2919-3429 | 4389-5074 2 Æ

3 4 4 4 4

0.1215.06 + 1.62 | 0.056 + 0.021 | 0 .023| 6.3+1.0 10 350 700

047-088 | 3.50-7.74 | 0.015-0.108 | 0.001-0.091 5-8 “ . ns

10 6 69 45 11

Source : MNHN, Paris

108 ALYTES 23 (3-4)

s 00 10 20 30 40 50

Les

-60

-80

r T T T T T

Fe 0 2 4 6 8 10

Fig, 2. — À sequence of the advertisement call of Chaparana ( Paa) blanfordit (Boulenger, 1882), Lam

Pokhari (East Nepal), 5 May 1973: (a) spectrogram: (b) oscillogram: (c) spectrum of a note in the

middle of the call.

in average) whose intensity increases until half or towards the end of the call, and then

decreases in the same way. The average call duration is 4.0 s. The note repetition rate is quite

slow (four notes per second). The intensity of each note decreases from its start to its end.

Each note consists of two lobes, the first one with a large amplitude, the second one with a

small one. The dominant frequency corresponds to the first frequency band and it is about

1529 Hz.

Cuaparana ( Paa) LiegiGi (Günther, 1860)

The recordings of Chaparana liebigii were made at night in the Dudh Kosi river bed. The

male (fig. 3) could not be caught: it was calling hidden down between blocks close to water in

this rather large torrent. The females were often seen close to the males, hidden in cavities

between rocks.

Source : MNHN, Paris

GROSIEAN & DUBOIS 109

Fig. 3. — Chaparana (Paa) liebigüi (Günther, 1860) male at night in its calling site under rock in the

torrent's bed, Ghat (Center-East Nepal), 25 June 1973

Fig. 4. — A sequence of the advertisement call of Chaparana { Pau) liebigii (Günther, 1860), Ghat

(Center-East Nepal), 25 June 1973, air temperature 15.0°C, water temperature 14.5°C: (a) spec-

trogram: (b) oscillogram. Note the important background noise due to the torrent

Source : MNHN, Paris

110 ALYTES 23 (3-4)

Fig. 5.— Chaparana ( Paa) minica (Dubois, 1975): male MNHN 1989.2065, Katrain (Himachal Pradesh,

India), 4 August 1977.

The call of this species (fig. 4, tab. 2) is a more or less regular succession of 15-16 short

notes. It has the same structure as the call of C. blanfordii and bout 2.26 seconds. The

note repetition rate is about 6.8 notes per second and the duration between two successive

notes averages 0.134 s. The first note of the call is emitted with higher intensity than the

following ones, and the duration of the interval between this note and the next one is longer

than the interval between the other notes of the sequence. Because of the loud background

noise, only the dominant frequency was measured (about 730 Hz).

CHapaRaNA ( Paa) minica (Dubois, 1975)

Chaparana minica (fig. 5) was recorded at night near a small stream where the males were

calling, on the ground, in a basin filled with water. Among the six species studied in this paper,

this is the only species in which two or three males were observed singing in a chorus.

Because of the problem encountered during recording (see Materials and methods), the

values given here in text are rounded off, whereas the values in tab. 2 are reported as measured.

The call of this species (fig. 6, tab. 2) consists of long (3. sequences, separated by

intervals of about ten seconds, and composed of numerous notes (10-19). By its general aspect

this call is quite similar to that of C. lichigii. Generally, the call of € minica begins by one or

Source : MNHN, Paris

GROSJEAN & DuBoIs 111

es Ne RE EE QE 0 PE à

“en 5 7 FA r” FA P"

-40

-60 A

A nn

eo) W A \ na Ag AN

dB L T TE T- T

kHz 0 2 4 6 8

Fig. 6. — À sequence of the advertisement call of Chaparana ( Pau) minica (Dubois, 1975), Katrain

(Himachal Pradesh, India), 3 August 1977, air temperature 21.0°C, water temperature 24.0°C: (a)

spectrogram: (b) oscillogram; (c) spectrum of a note in the middle of the call.

two notes shorter and greater in amplitude than the following ones. During the sequence the

duration of notes incre: (without variation in amplitude), as well as the duration of

intervals between notes (this is not an artifact due to problems in the tape speed, as the same

values are found in all recorded sequences). The signal stops usually with one or two notes

emitted after an interval lasting in average 0.5 s (range 0.4-0.6), i.e., longer than the previous

ones. The value of this unusual interval was excluded from the calculation of the mean

interval between notes (din) (tab. 2). The amplitude of the notes reach

beginning then decreases gradually. Each note is composed of two parts, the first one,

rounded, covering about the first quarter of the total length of the note, the second one,

s its maximum at its

elongate, reaching its maximum amplitude shortly after its beginning, then decreasing slowly

An amplitude modulation, and a rising frequency modulation of about 300 Hz, are present at

the beginning of each note. Up to nine frequency bands are visible in the spectrogram.

Tivo frequency bands are more intense than the others: the second frequency band at

about 2300 Hz corresponding to the dominant frequency, and the sixth band lying at about

6800 Hz

Source : MNHN, Paris

112 ALYTES 23 (3-4)

+ es 2 NRA CE n

Fig. 7. Chaparana ( Paa) polunini (Smith, 1951): male MNHN.1975.1454, Tesinga (Center-East Nepal),

21 June 1973.

CHapaRANa ( Pa4) PoLunINI (Smith, 1951)

Calls of Chaparana polunini (fig. 7) were heard in the afternoon, at 16h30, under a mossy

block with water dripping, along a small steep torrent. The calls started again at 19h00 and

were recorded at 20h20.

The call of this species (fig. 8, tab. 2) is structurally similar to that of C. hlanfordii, i.e.,

with an increase of intensity of notes until middle of sequence, followed by a decrease in the

same way. Ît is composed of 10-11 short notes (about 0.020 s) separated by intervals of about

0.1 ach note consists of two parts, the former with a great amplitude and a rapid rise and

fall, and the latter with a small amplitude. The dominant frequency corresponds to the first

frequency band and is about 1642 Hz. The second harmonic band is ill-defined. The dominant

frequency of the third call (emitted by the same individual) is about 200 Hz lower and no

sible.

harmonie bands are

Crraparana ( Pa4) roSrANDI (Dubois, 1974)

Chaparana rostandi was first recorded on 21 August 1972 near Kalopani in the large bed

of the Kali Gandaki river. The males (fig. 9) were calling in smaller streams running under the

Source : MNHN, Paris

GROSJEAN & DUBoIS 113

.s < pr ce 9e be pa 10

ms pr = de he de de

-50

-60

\ c

-70

0 \ N\

F ù ù — 7

ci kHz 0 2 4 6 8

Fig. 8. A sequence of the advertisement call of Chaparana (Pa) polunini (Smith, 1951), Thammu

(Center-East Nepal), 23 June 1973, air temperature 12.5°C, water temperature 11.5°C: (a) spec-

trogram: (b) oscillogram: (c) spectrum of a note in the middle of the call.

grassy bank of the river or in puddles under the banks left after decrease of the river level. The

male recorded was hidden by grass and bush covering the banks. On 4 September 1972, in the

same locality, a single male was calling and was recorded during night.

C. rostandi Was recorded again on 31 August 1972 near the lake Kutsab Terna Tal

(type-locality of the species) at night. The males were calling in the water, under leaves and

moss of the bank of the lake covered by vegetation, just below a small forest. Some males

called on this bank but none was calling on or under the opposite bank lacking vegetation.

The males were spaced out from each other. Other males called sporadically in the puddles,

little streams and on the shore of the lake but their calls were not synchronized.

The call of this species (fig. 10, tab. 2) is very short (shorter than or equal to 1 second) and

composed of only a few whistled notes (from 3 to 6). The average note repetition rate is 5.7

notes per second. The duration of notes is less than 0.06 s and the intervals between them are

of moderate length (from 0.12 to 0.26 s). This call presents à remarkable peculiarity: the last

Source : MNHN, Paris

114 ALYTES 23 (3-4)

Fig. 9. — Chaparana ( Paa) rostandi (Dubois, 1974): male MNHN 1975.0964, Kalopani (Northwest

Nepal), 22 August 1972

note of each call has a very notable different tone (there are differences from 100 to more than

400 Hz between the dominant frequency of the last note and that of the others). Furthermore,

this note is generally shorter and more damped than the previous ones. Its dominant

frequency corresponds to the first frequency band and is about 1745 Hz.

CHapaRaNa ( Pa4) vicina (Stoliczka, 1872)

The sequences of the advertisement call of Chaparana vicina (fig. 11) analyzed were

emitted by a single male, hidden under a block in a torrent.

The call of this species (fig. 12, tab. 2) is composed of short sequences (0.65 s) emitted

irregularly and separated by intervals of about 5 s. Each sequence consists of a series of 5-8

notes (mean length of note 0.056 s) separated by intervals of 0.05 s on the average. The

structure of the notes is similar to that of the notes of C. hlanfordii. The notes are composed

of two bodies linked to each other. Their amplitude increases in the course of the sequence

and then decreases very quickly in the last or two last notes. The dominant frequency is about

700 Hz and corresponds to the second band of the spectrogram. The fundamental frequency

{or the first band) lies at about 350 Hz.

Source : MNHN, Paris

GROSJEAN & DUBOIS 115

ms 200 +00 600 60 1000

cr - : +

ms 200 ns 600 50 1900

-60

-80 A

æ. * T T r T

kHz O0 2 4 6 8

Fig. 10. — A sequence of the advertisement call of Chaparana ( Pa) rostandi (Dubois, 1974), Kalopani

(Northwest Nepal), 4 September 1972, air temperature 14.0-14.5°C, water temperature 11.5°C: (a)

spectrogram: (b) oscillogram: (c) spectrum of a note in the middle of the call. Note a fluctuation of

the background noise during the call

DISCUSSION

According to their general aspect, the signals of C. blanfordii and C. liebigit are close to

each other, the signal of €. polunini appears to be similar to that of €. vicina, Whereas those of

C. rostandi and C. minica are particular. The calls of the two former species can be distin-

guished mainly by the values of the frequency bands. The advertisement calls of € polunini

and C vicina share only a relatively high note rate (10 notes per second). The call of C. minica

is particular by the fact that the amplitude of notes does not increase in the first part of

sequence and does not decrease in the second half: only the two first notes have a greater

amplitude than the others, whereas all the following ones have the same amplitude. The

parameters of the calls of several individuals of C. rostandi recorded in two different

populations show an important variation that covers the values found in other species. For

instance the silent interval between the notes of a sequence varies from 130 to 250 ms and

overlaps the values of C. blanfordii and C. liebigii. It is probable that a larger sampling of the

Source : MNHN, Paris

116 ALYTES 23 (3-4)

11. — Chaparana (Paa) vicina (Stoliczka, 1872): male, Manali (Himachal Pradesh, India), 26 July

1977.

other species taken throughout their distribution area would also show a greater variation of

each parameter.

Among these species, two are almost sibling species: C. liebigii and C. vicina (DUBOIS,

1976, 1980). Except for the male secondary sex characters, their morphologies are very

similar, but their advertisement calls are quite different. The call of the former species is longer

and composed of more notes than that of the latter species (more than two seconds with about

15 notes in C. liebigit in comparison to only half a second with 5-8 notes in C. vicina).

Differences in notes duration (dn) and interval duration between notes (din) also exist

between these two species, but an extended sample of calls could show an interspecific overlap

for these parameters. Finally, there is a difference in the frequency. as C. vicina has a frequency

band below the dominant frequency. Then, even if the two species have an identical dominant

frequency, the call of €. vicina sounds lower-pitched.

Comparing the bands of dominant frequency of each species, we can notice that

€. liebigit and €. vicina have a very low dominant frequency and C. minica a high dominant

Source : MNHN, Paris

GROSJEAN & DUBOIS 117

5 00 10 20 30 0 s0 €

-50

-60

-70

-80

dŒ

T T T T

ke 0 2 4 é 8

hmir, India), 10 July 1977, air temperature 19°C: (a) spectrogram: (b) oscillogram:

(Jammu & Ka

frequency, whereas the three other species cover the same frequency band, i.e., about 1300 Hz

to 1850 Hz. This frequency band is surely the best suited to the ecological conditions of these

species (see below). Among these three latter species, only C. polunini and C. rostandi are

sympatric in a small area. Therefore other factors must allow the discrimination of the

advertisement calls by the females. The frequency of sound is not the only efficient parameter.

The duration and shape of the call, the durations between the sequences and other parameters

can play a part in the recognition of the specific signal too (PAILLETTE, 1971). The call of C.

rostandi is markedly different from the other two calls. It has few whistle notes and the last

note of each sequence is lower than the previous ones (from 100 Hz to 400 Hz lower pitched

than the others). The first note is quite short, the notes in the middle of the call are the loudest

and the last one is of lower intensity. The differences between the calls of C. blanfordii and C.

Source : MNHN, Paris

118 ALYTES 23 (3-4)

polunini, which are not sympatric species although both present in Nepal and China (DuBois,

1979; Fer, 1999), are less pronounced.

Little information is available about the advertisement calls of species belonging to the

other genera of the tribe Paini as redefined by OHLER & DuBois (2006). The advertisement call

Of Quasipaa spinosa (David, 1875) was briefly described as follows by PoPE (1931): “(...)trilled

base notes, a sound rivaling in volume and depth that of any frog I have ever heard. Another

note is often emitted but it is a weak monosyllable and reminds one of the sound of a hammer

brought down upon a small but long pipe filled with water”. The call of Quasipaa exilispinosa

(Liu & Hu, 1975) was briefly described from observations in captivity (VorrEL, 2000). It

consists in a long series of notes (up to 30), each note lasting about 0.1 s. The value of the

dominant frequency has not been specified though the area where frequencies are the most

pronounced spreads from 320 to 1920 Hz. The advertisement call of a species of another

genus, Gynandropaa bourreti (Dubois, 1987), was heard during a field course (GROSIEAN, pers.

obs.). It consists in a series of pulse groups of equal intensity, lasting in total less than ten

seconds. The genus Chaparana (or at least its subgenus Paa) seems to differ from the other

genera by an advertisement call rather homogeneous in its gross features.

The species of the ranid tribe Paini are torrent-living species. Their calls are very different

from those of other ranid species living in other habitats (Dugois, 1977a-b; Dugois &

MARTENS, 1984; SUEUR, 1995) and share the same general characteristics. They are character-

ized by an important particularity: the notes are emitted with a low rate and in more or less

long series (from 3 to 19 notes in the calls studied here) separated by relatively long intervals

(from 3.5 seconds to one and a half minutes). The notes are very short (from less than 0.010

to 0.127 second) and are separated by short silent intervals (from juxtaposition of notes to

0.466 second). In spite of the weak intensity of calls, these features unquestionably allow a

better distinction and localization among the noise of strong streams. This discrimination is

likely to work mostly at the beginning and end of sequences.

The main characteristics of these calls have already been discussed (DuBois, 1977a-b;

Dugois & MARTENS, 1984). Three major characteristics are common to these calls: (1) the

calls are composed of short sequences of notes separated by long periods of silence; (2) the

notes are pure, short, and have narrow frequency bands; (3) the notes are rhythmically

separated within the sequences.

The calls of torrent-living species belonging to different anuran genera, such as the

Oriental Leptobrachella (DRING, 19834), Leptolalax (MATSUI, 1997), Ansonia (DRING, 1983b;

INGER & DRING, 1988) and Amolops (MATSUI et al., 1993), present the same kind of temporal

features. However, differences with the calls of Chaparana species also exist, especially in

frequency features. Indeed the high dominant frequency of these torrent-living species

spreads out on a large frequency band, whereas the calls of Chaparana exhibit a low dominant

frequency limited to a narrow frequency band. This is found also in some Bolivian torrent-

living frog traditionally referred to the genus Hyla (MARQUEZ et al., 1993), and placed in the

genus Hypsiboas by FAIVoviICH et al. (2005). The concentration of energy in a very narrow

frequency band, generally the lowest frequency, would provide a greater amplitude to the call

and thus favour the propagation of the pure notes over a greater distance, and the signal

reception may be more efficient against a background of wide band noise (CHApPuIS, 1971;

MorToN, 1975). However, the calls of the Chaparana remain of weak intensity and a single

Source : MNHN, Paris

GROSIEAN & DUBoIS 119

AL LH! D LI A HAE JU

fn fe

Fig. 13. — Diagram showing the succession of the calls of two males of Chaparana (Paa) polunini

(Smith, 1951) calling close to each other at Thammu (Center-East Nepal), 23 June 1973. Each

vertical line indicates the beginning of a sequence of call. The time scale is arbitrary, based on the

recorder counter, The breaks on the horizontal line indicate stops in the recording (after Dunots,

1977b).

rock in the torrent interposed between the observer and the calling frog may be a sufficient

obstacle to prevent the frog's call from being heard. The adult males of this genus are

distributed along the torrents so that often only the call of a single male can be heard at once

by a human observer. The localization of the male is helped in part by the slight binaural

discrimination at beginnings and ruptures in the sound emission (MARLER, 1967; FENG et al.,

1976; GRiBENSKI, 1977; DuBois & MARTENS, 1984; SUEUR, 1995), fast rise and fall times, short

durations and moderate repetition rates (LITTLEJOHN, 1977). As a result, the calls of these

frogs stand out well on the continuous background noise of the torrent (DuBois, 1977a-b;

DuBois & MARTENS, 1984).

The other characteristics found in the Chaparana calls, such as a low dominant fre-

quency, a prominent harmonic content and a rapid rise and fall of each note, are shared by

some fossorial microhylid frogs’ calls from New Guinea (MENZIES & TYLER, 1977) as well as

by Australian and Chilean leptodactylid burrowing frogs (LITTLEJOHN & MAIN, 1959; PEN-

GILLEY, 1971; FORMAS, 1985; PENNA & SoLis, 1999). These frogs exhibit a dominant frequency

lower than 3200 Hz which suits well with the resonance of the burrow and so amplifies the

efficiency of the call (BAILEY & ROBERTS, 1981). Other anurans that call hidden from within

the ground, such as species belonging to the genera Alytes or Tomodactylus (DiXON, 1957;

MARQUEZ & BosCH, 1995), also share tonal calls with the Chaparana species. When the

torrents are not in spate, the Chaparana call hidden under the rocks. This calling site can be

compared to the burrows and subterranean habitats of fossorial frogs. Their notes present a

dominant frequency band comprised between 700 and about 2000 Hz (excluding the value of

C. minica). In all the species studied here, except for C. minica and C. vicina, the dominant

frequency is the fundamental too. The call of C. minica, species less rheophilous than the

others, which calls from the side of the stream, has a higher dominant frequency.

In most anuran species, during calling period the males synchronize their calls just as if

they answered each other. Some species arrange their calls in chorus. This is the case in the

European species of the genus Hyla, particularly in the well-studied Hyla meridionalis

(PAILLETTE, 1970, 1976). On the contrary, the males of Chaparana studied above, except in C.

minica, do not answer each other. DUELLMAN (1967) defined different categories of calling

behaviour in the light of the social organization of frogs, and named the latter calling

behaviour “individual”. This behaviour was observed in the field in C. polunini (DuBois,

Source : MNHN, Paris

120 ALYTES 23 (3-4)

1977b) and C. rostandi, and in playback experiments in C. blanfordii. À diagram showing the

succession of the call sequences of two males of C. polunini that were calling close to each

other illustrates this phenomenon (fig. 13). Territorial calls, frequent in paddy-field species

and sometimes in forest species (DuBois, 1977a), do not seem to exist in the species of this

genus. In standard conditions, the males are distributed far from each other, so that only the

call of one individual can be heard at once by a human observer. The calls of different males

may interfere when the torrents are high, so that the usual shelters of the frogs are flooded.

The advertisement calls can have a territorial function so that when a male hears the call of

another male he could move away until not hearing it anymore. This function of call has also

been assumed in the Papuan microhylids (MENZIES & TYLER, 1977).

The call of €. minica has the highest dominant frequency of all of the calls analyzed until

now, and numerous harmonics. Furthermore, in this species (but also in C. vicina), the

dominant frequency corresponds to the second frequency band (to the first band in the other

four species). These differences with the calls of the other species could be due to the slightly

different mode of life of this species. C. minica inhabits rather quiet small streams rather than

violent torrents and does not call hidden under rocks but on the side of the stream, in puddles.

This may explain why the energy of call is not concentrated on a narrow frequency band but

spread over a wide range. Furthermore the shape of the advertisement call shows more

similarities to the calls of the species inhabiting open areas and some typical features of calls

adapted to torrents, such as short duration of notes or variation of amplitude of notes during

the call, are not present. Another striking difference to other members of the genus reviewed

here is the presence of a chorus like in species living in open areas. So €. minica has a habitat

and a calling behaviour slightly different from those of the other species considered in

this paper. However its call still possesses several features adapted to communication in

torrents.

As suggested by DuBois (1977b), the strong similarities which exist between the calls of

the species studied here more probably express the phylogenetic relationships of these species

rather than an evolutive convergence. The constraint imposed by the habitat was presumably

the predominant factor responsible for the elaboration of such call features which then were

conserved through speciation. A study on American bufonids and hylids (COCROFT & RYAN,

1995) showed that several call parameters can be conserved through repeated speciation

events within a homophyletic group.

RÉSUMÉ

Les chants de six espèces du genre Chaparana (sous-genre Paa) sont décrits, deux

d’entre-eux (Chaparana minica et Chaparana vicina) pour la première fois. Pour chacune des

espèces, de nombreux paramètres de durée et de fréquence sont donnés. Chaque chant est

illustré par un oscillogramme, un sonagramme et un spectre. Les caractéristiques générales de

ces chants particuliers sont considérées comme des adaptations à un environnement torren-

ticole. Les chants et modes de vie de ces grenouilles concordent avec les taxons définis par des

caractères morphologiques et moléculaires.

Source : MNHN, Paris

GROSIEAN & DUBOIS 121

ACKNOWLEDGMENTS

We thank Renaud Boistel and Jean-Marc Fontaine (Paris) for their valuable help in the treatment of

bad quality recordings, and Evanina de Morcillo y Makow (Jersey) for the stylistic revision.

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Corresponding editor: Franco ANDREO

Source : MNHN, Paris

Alytes, 2006, 23 (3-4): 123-132. 123

Hyla reinwardtii Schlegel, 1840

as a nomen protectum

Annemarie OHLER & Alain DUBOIS

Reptiles & Amphibiens, USM 602 Taxonomie & Collections,

Département Systématique & Evolution, Muséum national d'Histoire naturelle,

25 rue Cuvier, Case postale 30, 75005 Paris, France

<ohler@mnhn.fr, adubois@mnhn.fr>

Following article 23.9.1 of the International Code of Zoological

Nomenclature, the nomen Rhacophorus moschatus Kuhl & Van Hasselt,

1822 should be considered a nomen oblitum and the nomen Hyla

reinwardtii Schlegel, 1840, its junior subjective synonym, should be

treated as the valid nomen of the Reinwardt’s Gliding Frog. In order to

demonstrate the large acceptance of the nomen Rhacophorus reinwardtii,

we provide a list of references using this nomen as valid. À lectotype is

designated for Hyla reinwardtii Schlegel, 1840 and its description and

figure are provided.

South-east Asia is one of the hot-spot areas of amphibian biodiversity (STUART et al.,

2004). Many groups of frogs of this region have not been revised recently, and in those which

were so many new species were described (e.g.: VEITH et al., 2001: BROWN & GUTTMAN, 2002:

OHLER, 2003). As many old scientific names or nomina (DUBOIs, 2000) are “sleeping” in the

synonymies of many species, in order to link new results of research to previous knowledge,

reliable nomenclatural work should be done prior to naming new taxa.

We have shown on several occasions how useful the Principle of Priority is for automatic

determination of the valid nomen of a taxon in case of synonymy (DuBois & OHLER, 1995,

1997, 1999, 2000; Dugois, 1995, 1998: OnLer & DUBoIs, 1999; Bossuyr & DUBoIs, 2001). We

expressed our disagreement with some of the decisions of the International Commission on

Zoological Nomenclature giving precedence to a nomen that had been used only in a few more

publication than a senior synonym, although in some of these cases “usage” of the protected

nomen had been limited to specialised taxonomic publications (DUBoIs, 2005a-c). We always

strongly insisted and continue to insist that such cases should not be concerned by reversal of

only tend to weaken the legislative value and strength of the Code in the

eyes of zoologists and thus contribute to spreading arbitrary and chaos in zoological

nomenclature. Nevertheless there are cases when such an act is a reasonable one. In theedition

of the Code currently in force (ANONYMOUS, 1999), Article 23.9 gives rules for reversal of

precedence in such cases.

precedence as they

Dusois (1982, 1989) pointed to some problems in relation to the genus-group nomen

Rhacophorus Kuhl and Van Hasselt, 1822 and the species-group nomina Rhacophorus mos-

Source : MNHN, Paris

124 ALYTES 23 (3-4)

chatus Kuhl & Van Hasselt, 1822 and /yla reinwardtii Schlegel, 1840. When creating the

genus-group nomen Rhacophorus for large tree-frogs from Java, KuHL & VAN HASSELT

(1822a) referred two specific nomina to this genus. The first nomen, Rhacophorus reinwardtii,

was not accompanied by any description, definition or indication, and consequently must be

considered a nomen nudum (Dugois, 1989). This specific nomen became only available in the

work of SCHLEGEL (1840) who figured this tree-frog species as Hyla reimvardtii. The second

specific nomen proposed by KUHL & VAN HASsEeLT (18224), Rhacophorus moschatus, was

accompanied by a very short indication (‘“dewijl zij eenen sterken Bisamreuk zeer ver

verspreidt”, i.e., “because it spreads a strong musky scent very far”) which is sufficient to

make the nomen moschatus nomenclaturally available as of KuHL & VAN HASsELT (1822a).

This nomen being the only available specific epithet associated with the generic nomen

Rhacophorus in the original description of the genus, Rhacophorus moschatus Kuhl & Van

Hasselt, 1822 is the type-species by monotypy of Rhacophorus Kuhl & Van Hasselt, 1822

Dusois, 1989).

The status of the species group nomina Rhacophorus moschatus Kuhl & Van Hasselt,

1822 and Hyla reinwardtii Schlegel, 1840 remains to be dealt with. BRONGERSMA (1942) gave

arguments to support the opinion that Rhacophorus moschatus was proposed for a juvenile of

the species known as Rhacophorus reinwardtii. If this is true, the two species-group nomina are

synonymous, and the valid nomen should be the senior one. But the junior synonym, Æyla

reinwardtü, has been widely used in the combination Rhacophorus reinwardtii, and, to our

knowledge, Rhacophorus moschatus has never been used as a valid nomen. Application of the

Principle of Priority would lead to disturbance of a usage established for almost 200 years,

including in popular and non-specialised taxonomic literature. The case was submitted to the

International Commission on Zoological Nomenclature 20 years ago (Dugois, 1989: 101),

but despite the rare clarity of the case this application was never published in the Bulletin of

Zoological Nomenclature and no vote was ever organised on this question (DuBois, 1989).

Working on a list of synonymy of Oriental amphibians we reconsidered this case under the

new edition of the Code. This text shows an important novelty regarding the rules regulating

change of precedence between synonymous nomina. The way this rule is formulated (espe-

cially mentioning “valid” rather than “available” nomina) is highly open to criticism (DuBois,

1999, 2005b-c), and changes in this writing should be considered in the future. Nevertheless,

in the present case, this rule allows to establish the valid nomen of the species at stake without

having any more to wait for an improbable vote of the Commission.

Article 23.9.1 gives the conditions when prevailing usage must be maintained: “the senior

synonym or homonym has not been used as a valid name after 1899” (Article 23.9.1.1); and

“the junior synonym or homonym has been used for a particular taxon, as its presumed valid

name, in at least 25 works, published by at least 10 authors in the immediately preceding 50

years and encompassing a span of not less than 10 years” (Article 2. ). In order to apply

Article 23.9.1, an author must cite the two nomina together and state explicitly that the junior

nomen is valid and that the action is taken in accordance with this Article. In particular it must

be stated that Article 23.9.1.1 applies and that conditions of Article 23.9.1.2 are met.

Considering the usage of the nomina Rhacophorus moschatus and Hyla reimvardtii, the

conditions of Article 23.9 are clearly met for both nomina. The nomen Rhacophorus moscha-

tus has never been used as valid nomen for these tree-frogs: all authors who mentioned this

Source : MNHN, Paris

OuLer & DUBoIs 125

nomen considered it as invalid (DUBoIs, 1982, 1989; Frost, 1985; ZHAO & ADLER, 1993). On

the other hand, Hyla reinwardtii (as Rhacophorus reinwardtii) has been used largely, in

particular in faunal lists, field guides, books on amphibian biology and general zoology. This

species is well-known also by non-specialists, as it is one of those that have a particular mode

of aerial locomotion, gliding in the canopy of primary forests. A list of 25 publications, by 25

independent authors (sensu DuBois, 2005c), citing the nomen Rhacophorus reinwardtii, is

provided in Appendix 1. Among hundreds, these references were chosen in order to represent

a great variety of countries and of works, to corroborate large acceptance.

Having met conditions given in Article 23.9 of the Code, the nomen F/yla reinwardtii has

precedence over Rhacophorus moschatus. This action only considers precedence but not

availability in the case where synonymy of both nomina should be questioned. As a matter of

fact, some authors (VAN KAMPEN, 1923: 254; Au, 1931: 148; WoLr, 1936: 187) suggested that

R. moschatus might be the species later called Æyla margaritifera Schlegel, 1844, and also Hyla

javanus Boettger, 1893. In such a case the nomen Rhacophorus moschatus Would remain

available for possible “resurrection”, as is explicitly stated in Article 23.9.2. Stabilisation of

the status of this nomen would require designation of a neotype, as the original syntypes are

lost (BRONGERSMA, 1942).

In the publication where the nomen Hyla reinwardtii was made nomenclaturally avail-

able, SCHLEGEL (1840) provided figures of three specimens, thus pointing to morphological

and color variation in this group. CHAN-ARD et al. (1999) also documented this variation, as

they showed a photo of a specimen which they only tentatively recognized as being a member

of R. reimvardtii. Should this variation reflect specific differentiation, the nomen Rhacophorus

moschatus could possibly be available for one of the taxa. A modern revision of the species

groupusing etho-ecological, genetic and molecular characters might redefine species limits. In

this perspective, it is important to stabilise the nomenclatural status of the nomen Hyla

reimvardtii Schlegel, 1840. As the nomen is available from the Abbildungen, only the specimens

originally illustrated in the latter are syntypes. These specimens are still extant and kept in the

collections of the Nationaal Natuurhistorisch Museum (formerly Rijksmuseum van Natuur-

lijke Historie), Leiden, Netherlands (RMNH). Plate 30 of SCHLEGEL (1840) shows three

specimens: figures 1 and 2 correspond to RMNH 6517.A, figure 3 to RMNH 3899 and figure

4 seems to be painted on the model of RMNH 1970.A. Only these three specimens are

syntypes of this nominal species, and not the two additional specimens in the Leiden Museum

listed by FRosr (1985: 547) as syntypes (RMNH 1870.B and 6517.B). We hereby designate the

specimen RMNH 6517.A as lectotype. This choice is justified as only this specimen in

SCHLEGEL'S plate (1840) clearly corresponds to the current concept of the species. This

specimen is from Java, so there is a type-locality indication. We provide below in Appendix 2

a description and a photograph (fig. 1) of this specimen.

For the time being, the synonymy of Rhacophorus reimvardti is as follows:

Rhacophorus reinwardtii (Schlegel, 1840)

[Reinwardt's Flying Frog, Green Flying Frog, Black-webbed Treefrog]

Rhacophorus moschatus Kuhl & Van Hasselt Nomen oblitum. - Onomato-

phore: syntypes unknown. — Type-locality: near Rosanelen forest, region of Gunung

Source : MNHN, Paris

126 ALYTES 23 (3-4)

Pangerango (106°57°E, 06°46’S), near Bogor [Buitenzorg], Java, Indonesia. - Synonymy:

BRONGERSMA (1942: 345). - Comments: BRONGERSMA (1942) considered the specimen of

figure 4 in SCHLEGEL (1840) as one of the syntypes of this nominal species. This specimen

closely resembles in color pattern RMNH 1970.A, which cannot be a syntype as it has

not been collected by Kuhl but by S. Müller in Sumatra, according to the RMNH

catalogue.

“Rhacophorus reimvardtii” Kuhl & Van Hasselt, 18224: 104. - Nomen nudum.

“Rhacophorus rheinwardtif® Kuhl & Van Hasselt, 1822b: 476. - Nomen nudum.

“Hypsiboas reinwardtit” Wagler, 1830: 200. - Nomen nudum.

Hyla reimvardtii Schlegel, 1840: 105. —- Nomen protectum. - Onomatophore: lectotype, by

present designation (see Appendix 2 below), RMNH 6517.A, adult female. - Type-

locality: Java, Indonesia.

Rhacophorus reinwardtii: DUMÉRIL & BIBRON, 1841: 532.

Polypedates reimwardtii: SEDLECKI, 1909: 704.

Rhacophorus reimvardti: VAN KAMPEN, 1910: 43.

R{hacophorus] (R[hacophorus]) reimvardtii: Au, 1931: xü, 60, 171.

Rhacophorus ( Rhacophorus) reinwardtii: DuBois, 1987: 77.

? Rhacophorus reinwardti var. lateralis Werner, 1900: 495 [nec Rhacophorus lateralis Boulen-

ger, 1883: 162]. - Onomatophore: holotype, Naturhistorisches Museum, Basel, Switzer-

land (NHMB) 1192, adult female (FORCART 1946: 132). - Type-locality: Batu Bara, Laut

Tador, Sumatra, Indonesia. - Synonymy: WoLr (1936: 213).

RÉSUMÉ

En raison de l’article 23.9.1 du Code International de Nomenclature Zoologique, le nomen

Rhacophorus moschatus Kuhl & Van Hasselt, 1822 doit être considéré comme un nomen

oblitum et le nomen Hyla reinwardtit Schlegel, 1840, son synonyme subjectif plus récent,

comme le nomen valide de la Rainette parachute de Reinwardt. Une liste de références de

travaux dans lesquels le nomen Rhacophorus reinvardtii est employé comme nomen valide

permet de démontrer l'importante utilisation de ce nomen. Un lectotype est désigné pour ce

nomen et sa description et figure sont données.

ZUSAMMENFASSUNG

Aufgrund des Artikels 23.9.1 des /nternational Code of Zoological Nomenclature sollte

der Name Rhacophorus moschatus Kuhl & Van Hasselt, 1822 als nomen oblitum betrachtet

werden und der Name Hyla reimvardtii Schlegel, 1840, sein jüngeres subjektives Synonym,

sollte der valide Name des Reinwardtschen Flugfrosches sein. Eine Liste von Werl in

denen der Name Rhacophorus reinwardtii als valider Name gebraucht wird, soll die breite

Anerkennung des Namens bezeugen. Ein Lectotypus für diesen Names wird designiert und

seine Beschreibung und Abbildung werden gegeben.

Source : MNHN, Paris

OnLER & DUBOIS 127

ACKNOWLEDGEMENTS

We acknowledge Michèle Lenoir and her staff for facilitating access 10 the historical collection of the

Bibliothèque Centrale du Muséum (Paris). We are grateful to Franco Andreone and Victoire Koyamba

for their help in bibliographic research.

LITERATURE CITED

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BorrrGer, O., 1893. - Neue Reptilien und Batrachier aus West Java. Zool. Anz., 16: 334-340.

BOssuvr, F. & Dusois, A., 2001. — À review of the frog genus Philautus Gistel, 1848 (Amphibia, Anura,

Ranidae, Rhacophorinae). Zeylanica, 6 (1): 1-112.

BouLENGER, G, À., 1883. — Description of new species of Reptiles and Batrachians in the British

Museum. Ann. Mag, nat. Hist., (5), 12: 161-167.

BRoNGERSMA, L. D., 1942. - On two Rhacophorus species mentioned by Kuhl and Van Hasselt. Arch.

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BROWN, R. M. & Gurrman, S. L., 2002. - Phylogenetic systematics of the Rana signata complex of

Philippine and Bornean stream frogs: reconsideration of Huxley's modification of Wallace’s Line

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CHan-arD, T., GROSSMANN, W., GUPRECHT, À. & SCHULZ, K.-D., 1999. — Amphibians and Reptiles of

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261-280.

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1989. — Hyla reinwardtit Schleyel, 1840 (?) (Amphibia, Anura}: proposed conservation. Alytes, 7:

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1999. - Editorial. Aves, 17 (1-2): 1-2

2000. - Synonymies and related lists in zoology: general propos

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20054. — Les règles de la nomenclature familiale en zoologie. /n: À. Dusois, O. PoxcY, V. MALÉCOT

& N. Lier (ed.), Comment nommer les taxons de rang supérieur en =oologie et en botanique?,

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Comment nommer les taxons de rang supérieur en zoologie et en botanique? Bi ma, 23: 73-96.

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--- 1997. — Early scientific names of Amphibia Anura. I. Introduction. Bull. Mus. natn. Hist. nat.,

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nee 1999. - Asian and Oriental toads of the Bufo melanostictus, Bufo scaber and Bufo stejnegeri groups

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types. J South Asian nat. Hist., 4 (2): 133-180.

—— 2000. -Systematics of Fejervarya limnocharis (Gravenhorst, 1829) (Amphibia, Anura, Ranidae) and

related species. 1. Nomenclatural status and type-specimens of the nominal species Rana limno-

charis Gravenhorst, 1829. A/ytes, 18 (1-2): 15-50.

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Tome 8. Paris, Roret: i-vii + 1-792.

ForcarT, L., 1946. - Katalog der Typusexemplare in der Amphibiensammlung des Naturhistorischen

Museums zu Basel. Verh. naturf. Ges. Basel, 57: 118-142.

FRosT, D. R. (ed.), 1985. — Amphibian species of the world. Lawrence, Allen Press & Assoc. Syst. Coll.:

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KUHL, H. & Van HasseLr, J. C., 18224. — Uittriksels uit brieven van de Heeren Kuhl en Van Hasselt, aan

de Heeren C. J. Temmnick, Th. Van Swinderen en W. De Haan. Algemeene Konst-en Letter-Bode,

7: 99-104.

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Swinderen zu Groningen. {sis von Oken, 1822: 472-476.

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tion of two new species. Alpes, 21 (1-2): 23-44.

OHLER, A. & DELORME, M., 2006. — Well known does not mean well studied: morphological and

molecular support for existence of sibling species in the Javanese gliding frog Rhacophorus

reinwardtit (Amphibia, Anura). Comptes rendus Biologies, 329: 86-97.

Ouer, A. & Durots, A., 1999. - The identity of Elachyglossa gyldenstolpei Andersson, 1916 (Amphibia,

Ranidae), with comments on some aspects of statistical support to taxonomy. Zoologica scripta, 28

(3-4): 269-279.

SCHLEGEL, H., 1840. — Abbildungen neuer oder unvollständig bekannter Amphibien. Düsseldorf, Arnz and

Comp. Atlas: pl. 21-30.

SiEpLECKI, M., 1909. - Zur Kenntniss des javanischen Flugfrosches. Biol. Centralbl., 29: 704-714 +

715-737,2 pl.

STUART, S. N., CHANSON, J. S., Cox, N. A., YOUNG, B. E., RODRIGUES, A. S$. L., FISCHMAN, D. L. &

WALLER, R. W., 2004. — Status and trends of amphibian declines and extinctions worldwide.

Science, 306: 1783-1786.

EN, P. N., 1910. - Beitrag zur Kenntniss der Ampibienslarven des Indischen Archipels.

Natuurkd. Tijd: Nederl. Indie, 69: 25-48.

923. The Amphibia of the Indo-Australian archipelago. Leiden, Brill: i-xii + 1-304.

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(Gravenhorst, 1829) (Amphibia, Anura, Ranidae) and related species. 2. Morphological and

molecular variation in frogs from the Greater Sunda Islands (Sumatra, Java, Bornco) with the

definition of two species. Alvres, 19 (1): 5-28

, J, 1830. — Narürliches System der Amphibien, mit vorangehender Classification der Säugethiere

und Vôgel. München, Stuttgart & Tübingen, Cotta: i-vi + 1-354

Were, F. 1900. - Reptilien und Batrachier aus Sumatra. Zoo!. Jahrb., Jena, Abt. Syst. 13: 479-508, pl.

Wor, S., 1936. Revision der Untergattung Rhacophorus (ausschliesslich der Madagaskar-Formen).

Bull. Raffles Mus., 12: 137-217.

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pl 1-48 + 1.

Source : MNHN, Paris

OnLer & DUBoIS 129

APPENDIX |

List OF 25 REFERENCES OF GENERAL WORKS USING THE NAME RHACOPHORUS REINWARDTII

Q) BERRY, P. Y., 1975. The amphibian fauna of Peninsular Malaysia. Kuala Lumpur, Tropical Press: i-x

+1-130.

(2) CHAN-ARD, T., GROSSMANN, W., GUPRECHT, A. & SCHULZ, K.-D., 1999. — Amphibians and Reptiles

of Peninsular Thailand. An illustrated checklist. Wuerelen, Germany, Bushmaster Publications:

1-240.

(3) CocHRAN, D. 1965. - Les Amphibiens vivants du monde. Paris, Hachette: 1-211.

(4) Fe, L., (ed.), 1999.— Arlas of amphibians of China. Zhengzhou, Henan Publishing House of Science

and Technology: 1-432. [In Chinese].

(5) Frost, D. R., (ed.), 1985. Amphibian species of the world. Lawrence, Allen Press & Assoc. Syst.

Coll. [i-iv] + iv + 1-732.

(6) Hazubay, T. & ADLER, K., 2002. — The new encyclopedia of Reptiles and Amphibians. Oxford,

Oxford University Press:1-240.

(7) HorriCHTER, R., (ed.), 1998. - Amphibien: Evolution, Anatomie, Physiologie, Okologie, Verbreitung,

Verhalten, Bedrohung und Gefährdung. Augsburg, Naturbuch Verlag: 1-264.

(8) INGER, R. F. & STUEBBING, R. B., 1997. — À field guide to the frogs of Bornco. Kota Kinabalu &

Sabah, Natural History Publications & Science and Technology Unit: i-ix + 1-207.

(9) IskANDAR, D. T., 1998.— The Amphibians of Java and Bali. LIPT, The field guide series: i-xix + 1-117,

26 pl.

(10) KHONSUE, W. & THIRAKUPT, K., 2001. — A checklist of the Amphibians in Thailand. Nat. Hist. J.

Chulalongkorn Univ., 1: 69-82.

(11) LaNZA, B., (ed.), 1982. — Dizionario del Regno Animale. Milano, Arnoldo Mondadori Editore:

1-706.

(12) La, S. S., 1970. — The morphology, systematics, and evolution of the Old World treefrogs

(Rhacophoridae and Hyperoliidae). Fieldiana: Zool., 57: i-vii + 1-145.

(13) Liu, C.-C. & Hu, S.-C., 1961. - The tailless amphibians of China. Beïjing, Science Press: [i-ii] + i-xvi

+ 1-364, pl. 1-6 + 1-28. [In Chinese].

(14) MANTHEY, U. & GROSSMANN, W.. 1997. — Amphibien and Reptilien Südostasiens. Münster: 1-512.

(15) MarrisoN, C., 1987. - Frogs and toads of the world. New York & Sidney, Planford Press, Poole:

1-191.

(16) MERTENS, R., 1959. — La vie des Amphibiens et des Reptiles. Paris, Horizon de France: 1-206.

(7) NurTPHUND, W., 2001. - Amphibians of Thailand. Amarin Printing & Publishing, Thailand: 1-192.

{ln English and Thai]

F.J., RICHTER, K. & JACOB, U., 1984. - Lexikon der Terraristik und Herpetologie. Leipzig,

Landbuch Verlag:1-465.

(19) ORLO, N. L., LArHROP, A. MurPHY, R. W. & CC, H. T. 2001. - Frogs of the family Rhacopho-

ridae (Anura: Amphibia) in the northern Hoang Lien Mountains (Mount Fan Si Pan, Sa Pa

District, Lao Cai Province), Vietnam. Russian Journal of Herpetology, 8: 17-44.

(20) SokoLov, V.E.. (ed.), 1988. Dictionary of animal names in five languages. Amphibians and Reptiles.

Moscow, Russky Yazyk Publishers:1-554. [In Russian].

(1) TILLIER, 1999. — Dictionnaire du règne animal. Paris, Larousse:1-509.

(22) VaNNI ologia dei vertebrati. Torino, UTET: 1-685.

(23) YAN 1991. — The Amphibia fauna of Yunnan. Kunming, China Forestry Publishing

-259. [In Chinese].

(24) Znao, E.-M., 1999. - Distribution patterns of amphibians in temperate Eastern Asia. /n: W. E.

DUELLMAN (ed.), Patterns of distribution of amphibians: a global perspective, Baltimore, John

Hopkins University Press: 421-443.

(25) Zur, T., 2002. — Die Amphibien und Reptilien eines Tieflandfeuchtwald-Schutzgebietes in Viet-

nam, Münster, Natur- und Tier-Verlag: 1-342

(8)

Source : MNHN, Paris

130 ALYTES 23 (3-4)

Fig. 1.- Lectotype of Hyla reinwardtit Schlegel, 1840, RMNH 6517.A, in dorsal view.

APPENDIX 2

DESCRIPTION OF LECTOTYPE OF HYLA REINWARDTII

To facilitate comparisons, the format of this description is the same as in our other recent

descriptions of Oriental Amphibia, especially of the genus Rhacophorus (OHLER & DELORME,

2006). Measurements were taken in mm. They are designated by the following abbreviations:

SVL: snout vent length. Head: HW: head width; HL: head length (from back of mandible to

tip of snout); MN: distance from back of mandible to nostril, MFE: distance from back of

mandible to front of eye; MBE: distance from back of mandible to back of eye; IFE: distance

between front of eyes; IBE: distance between back of eyes: IN: internarial space; EN: distance

from front of eye to nostril; EL: eye length; SN: distance from nostril to tip of snout; SL:

distance from front of eye to tip of snout; TYD: greatest tympanum diameter; TYE: distance

from tympanum to back of eye; IUE: minimum distance between upper eyelids; UEW:

maximum width of inter upper eyelid. Forearm: HAL: hand length (from base of outer

palmar tubercle to tip of toe); FLL: forelimb length (from elbow to base of outer tubercle);

TEL: third finger length (from base of first subarticular tubercle); pal-pa4: width of pads of

finger I to IV: wal-walV: width of fingers I to IV; Hindlimb: FL: femur length (from vent to

Source : MNHN, Paris

OuLer & DuBois 131

knee); TL: tibia length; FOL: foot length (from base of inner metatarsal tubercle to tip of toe);

FTL: fourth toe length (from base of first subarticular tubercle to tip of toe); ppl-ppV: width

of pads of toes I to V: wpl to wpV: width of toes I to V; IMT: length of inner metatarsal

tubercle; ITL: inner toe length. Webbing: MTTF: distance from distal edge of metatarsal

tubercle to maximum incurvation of web between third and fourth toe; TFTF: distance from

maximum incurvation of web between third and fourth toe to tip of fourth toe; MTFF:

distance from distal edge of metatarsal tubercle to maximum incurvation of web between

fourth and fifth toe; FFTF: distance from maximum incurvation of web between fourth and

fifth toe to tip of fourth toe).

Lectotype of Hyla reinwardtii Schlegel, 1840, by present designation, RMNH 6517.A,

adult female (fig. 1). Poor preservation, specimen stuffed and dried.

(A) Size and general aspect. (1) Specimen of moderate size (SVL 69.3 mm), body rather

robust.

(B) Head. (2) Head moderate, as long (HL 23.4 mm) as wide (HW 23.3 mm; MN

19.5 mm; MFE 15.7 mm; MBE 8.4 mm), flat. (3) Snout rounded, not protruding; its length

(SL 10.53 mm) longer than horizontal diameter of eye (EL 9.47 mm). (4) Canthus rostralis

rounded, loreal region convex; obtuse in cross section. (5) Interorbital space convex, larger

QUE 6.84 mm) than upper eyelid (UEW 5.26 mm) as large as internarial distance (IN

6.79 mm); distance between front of eyes (IFE 14.1 mm) about two thirds of distance between

back of eyes (IBE 21.9 mm). (6) Nostrils rounded, without flap of skin; as close to tip of snout

(NS 5.93 mm) as to eye (EN 5.66 mm). (7) Pupil indistinct. (8) Tympanum (TYD 5.53 mm),

distinct, oval, oblique; tympanum-eye distance (TYE 0.92 mm) one fifth its diameter. (9)

Pineal ocellus absent. (10) Vomerine ridges not observed. (11) Tongue not observed. Tooth-

like projection on maxilla absent.

(HAL 22.1 mm), not enlarged. (13) Fingers I and IT rather long, thin; fingers IT and IV long

and thin (TFL 12.4 mm). (14) Relative length, shortest to longest: 1 <II < IV <IIL. (15) Tips

of fingers I to IV rounded, enlarged; circum-ventral dises on fingers I to IV, very wide

compared to finger width (pal 2.92 mm, wal 1.56 mm; pall 3.76 mm, wall 1.94 mm; palll

4.15 mm, wall 2.59 mm; palV 4.41 mm, walV 2.40 mm). (16) Fingers with webbing: 12-1

I 0 — O III 0 — O IV. (17) Subarticular tubercles present, poorly distinct, rounded, single:

proximal tubercle of fingers III and IV small and flat. (18) Prepollex oval, very prominent;

palmar tubercle indistinct.

(D) Hindlimbs. (19) Shank six times longer (TL 32.8 mm) than wide (TW 5.3 mm),

shorter than thigh (FL 35.5 mm) but as long as distance from base of internal metatarsal

tubercle to tip of toe IV (FOL 33.0 mm). (20) Toes long, thin, toe IV (FTL 17.9 mm) longer

than third of distance from base of tarsus to tip of toe IV (TFOL 48.2 mm). (21) Relative

length of toes, shortest to longest: 1 < IT < V < III < IV. (22) Tips of toes rounded, enlarged,

circum-ventral grooves on toes I to V (ppl 2.40 mm, pwl 1.30 mm; ppll 2.27 mm, pwll

1.62 mm; ppIll 2.98 mm, pwlll 1.94 mm; pplV 3.50 mm, pwIV 1.94 mm: ppV 2.98 mm, pwV

1.94 mm). (23) Webbing complete: 10-0100 110-01V 0-0 V(MTTF 23.1 mm; MTFF

25.5 mm; FTFT 7.8 mm; FFTF 13.4 mm). (24) Dermal fringe along toe V from tip of toe

along toe, continuing on tarsus to heel, well developed. (25) Subarticular tubercles present,

distinct, rounded, simple, all present. (26) Inner metatarsal tubercle short, distinct, its length

Source : MNHN, Paris

132 ALYTES 23 (3-4)

(IMT 2.50 mm) 4.1 times in length of toe I (ITL 10.26 mm). (27) Tarsal fold absent. (28) Outer

metatarsal tubercle, supernumerary tubercles and tarsal tubercle absent.

(E) Skin. (29) Dorsal and lateral parts of head and body smooth, flanks with small

glandular warts getting larger ventrally. (30) Dermal folds on forearm, heel, tarsus, metatar-

sus and vent; latero-dorsal folds absent; “Fejervaryan” line absent; lateral line system absent;

supra-tympanic fold absent; cephalic ridges absent; co-ossified skin absent. (31) Dorsal parts

of limbs smooth. (32) Ventral parts of head, body and limbs: throat and chest smooth; belly

and thigh covered with treefrog belly skin. (33) Macroglands absent.

(F) Coloration in alcohol. (34) Dorsal and lateral parts of head and body: dorsal parts of

head and body and upper part of flank creamy white; lower part of flank brown with whitish

spots corresponding to glandular warts; loreal region, upper lip, tympanic region and

tympanum creamy white. (35) Dorsal parts of limbs creamy white; posterior part of thigh

brown. (36) Ventral parts of head, body and limbs: throat, margin of throat and chest white;

belly and thigh brown with white spots corresponding to glandular warts; webbing between

toes I and IT creamy white; other toes dark brown with whitish longitudinal bands.

(G) Secondary sexual characters. Not observed.

Corresponding editor: Miguel VENCES.

Source : MNHN, Paris

Alytes, 2006, 23 (3-4): 133-143. 133

The suburban common frog

(Rana temporaria) population

in the eastern Helsinki suburb, Finland

Antti HAAPANEN

Helsinki, Finland

kolumbus.fi>

Huhtasuontie 7, 00

<antti.haapanen

The common frog population in the eastern Helsinki suburb was

estimated in 1999-2002 by counting the numbers of egg clumps in spaun-

ing sites. The study area covered 1590 ha. The frogs were found in various

types of green areas such as woodlands, agricultural land and various types

of parks. These areas covered 40 % of the whole study area. The population

was 786 + 262 spawning female frogs. The population size increased

during the study period. The population density was 1.3 females/ha in

green areas. Spawning sites were small dikes, ponds, brooks and their

wider parts with still water. Small and shallow dikes and ponds are

vulnerable to overfilling and other negative changes. It was found that some

new sites were made as a by-product of city works. The amount of spawning

habitats seemed to be the density dependent limiting factor controlling the

common frog population.

INTRODUCTION

It has been repeatedly reported that frog populations are especially sensitive to various

types of pollution and habitat destruction. AÏl species are not, however, as sensitive. Several

healthy populations have been monitored lon h to verify this (e.g.. MEYER et al., 1998)

It has been stated that the common frog is less sensitive to urbanisation than many other

species (KUZMIN, 1994) and seems to survive in urban conditions (HITCHINGS & BEEBEE,

1997)

eno!

Frog population studies such as catching and recatching are time-consuming. HAAPANEN

(1982) has developed for northern habitats a counting procedure which gives quite exact

numbers of spawning female common fr The same type of method to estimate the

population and to observe the annual variation of a frog population in a long term has been

used e.g. by KUTENKOV & PANARIN (1995). Although males and subadults are ignored, the

spawning females are the essential part of the population.

and to

The aim of this study is to count the number of breeding female common frog

describe the habitats in suburban conditions in the boreal zone.

Source : MNHN, Paris

134 ALYTES 23 (3-4)

STUDY AREA AND METHODS

The common frog populations were surveyed in the eastern part of Helsinki (60°12°N,

25°08'E, 0-25 m above sea level). The study area covers about 1590 ha, which is 8.5 % of the

whole area of Helsinki (fig. 1). The area consists of apartment house sectors, small house

blocks, industrial areas, and various kinds of traffic lines and green areas (forest, park and

meadow in fig. 1). The local industry does not pollute air or waters. The acid rain load has

been cut down by 60 % from the situation in the late 1970°s (KULMALA et al., 1998). In the late

1980's several lichen species have reinvaded the region showing the enhanced air quality. One

apartment house block has been constructed on an old dumping place in the 1970's. In the late

1990's it was found to pollute the soil and small dikes below. According to the information

from the City of Helsinki, this pollution is limited to the nearby dikes and does not reach the

study area itself.

The constructed areas outside the green areas cannot be regarded significant as a

common frog habitat because of high density of traffic lines, the blocking effect of houses on

the migration and only minimal green areas. Therefore those areas have not been included in

this study as a common frog habitat.

The study area was sparsely inhabited, in some places like countryside, until the 1960°s.

The rapid urbanisation took place in the 1960’s and 1970’, including four-lane road and

underground railway constructions. The present green areas appear in the city general plan

mostly as parks, outdoor recreation areas and as a university farm. The green areas have been

more or less the same during the last 25-30 years. Altogether there are 633 ha green areas,

which were divided into 24 sub-areas. These are isolated from each other in most cases by

streets, four-lane highways or house blocks.

The green areas are most extensive in the western part of the study area in the university

farm, where they form 50 % of all green areas. The green areas altogether cover 40 % of the

whole study area but only 25 % east of the university farm (fig. 1).

These green areas were classified into five different habitat types as follows: (1) broad

leaved woodlands with rich natural field layer vegetation, later called woodlands: (2) wood-

; (3) areas covered partly with woodlands and partly well-managed short-cut lawns,

pen areas below; (4) agricultural areas; and (5) barren rocky pine woods. The

rocky barren woodlands are mostly 20-25 m above sea level, often with fairly steep slopes. The

other habitat types are found mostly in lowlands.

There are three brook watershed areas in the study area (fig. 1). The total length of

brooks in the study area is 11 km. These brooks have been canalised in earlier times. Parts of

them have been restored in recent years. In addition there are small ponds and dikes. Some of

the dikes date back to old farming which has ceased decades ago. The few pH measurements

in these brooks show that water is lose to neutral during the spawning season. The observed

pH values are 6.5-7.3 and the water quality in general was good in surveys made by the City

of Helsinki (JALAVA, 1987; KETOLA, 1998).

The dikes are very small. The amount of water may be only some cubic metres and most

of them are dry later in the summer. Only a small proportion of them have water plants. The

Source : MNHN, Paris

HAAPANEN 135

Fig. 1. The study area in the eastern part of the City of Helsinki. X-marked areas show the green areas,

where spawning frogs were found. Constructed areas, motorways and other main roads isolate

these from each other. Two crosses seem not to be in green areas, but this is not the case. These green

areas are either in the corner of an industrial area or above the subway where natural vegetation

with a pond has survived. The green areas are not connected to rural areas. The index map shows

the brook systems with flowing directions one on the western border, one in the middle and one on

the eastern side of the study area.

small ponds are bigger, from 100 to 1000 m?, 20-60 cm deep. Many of them are permanent

water bodies. Brooks and their wider parts are permanently wet at least in normal years. Only

such parts of brooks are used by frogs where there is still water during the spawning season.

These brooks are small, 0.5-2 m wide and 20-50 em deep. Measurements of the flow from one

brook were 1.5-1280 1/s, with an average of 35 1/s (KETOLA, 1998). During spawning the flood

is mostly over but the flow is apparently above the average.

The study area is connected to the Baltic Sea. The brackish waters are not used as

breeding habitat (HAAPANEN, 1982), although the salt content is hardly noticeable. Moreover

it varies greatly (0-0.5 %), depending on the amount of fresh water and winds.

The spawning sites are of four different types: dikes, small ponds, brooks with still water

and the wider parts of brooks with still water.

The counts were made over four years (1999-2002). The year 2002 was exceptionally dry.

The amount of rain from early April to mid-June was only 72 mm or 56 % of the long term

average. The other years were wet or close to the normal.

Source : MNHN, Paris

136 ALYTES 23 (3-4)

Spawning pattern

15"

12:

€

£2

€ 5

s IH

1 2 3 4 5 6 LP 9 10 11 12 13 14 15 16 17 18 19

Date

Fig. 2. - The spawning pattern of the common frogs in 2002. The columns show the percentage of egg

clumps laid each day (7 = 192). The spawning started April 14 and to0k 19 days.

The census of the common frog population is based on the counting of egg clump masses

during the breeding season. One female lays only one egg clump per season (SAVAGE, 1961).

The census followed the procedure proposed by HAAPANEN (1982). This method was devel-

oped further, as follows. It is impossible to make the census when all the clumps have to be

surveyed at once, as the development starts immediately after laying and accumulations of

dozens of egg clumps can occur. However, each day the newly appeared egg clumps can be

distinguished and counted in these egg clump groups (HAAPANEN, 1982). In 2001 and 2002 a

certain number of breeding sites were surveyed daily from the early beginning of breeding

until no new egg clumps were seen. So it was possible to see which percentage of the total egg

clump numbers had been laid each day of the census period (fig. 2).

The spawning sites surveyed daily made a fairly representative sample of the total

spawning female population as they formed 10 and 19 % of the total census in 2001 and 2002,

respectively. The census in other spawning sites was made approximately after 10 days from

Source : MNHN, Paris

HAAPANEN 137

the start of egg laying or somewhat later and the numbers were corrected using the correction

figure based on the results in areas followed daily (fig. 2). In 1999 and 2000 only one census

was made with no additional counting as the method would require (HAAPANEN, 1982). In

those two years the figures were corrected based on the results in 2001 and 2002, and by

HAAPANEN (1982).

Although the author knows the area very well each year some new breeding sites were

found. Especially in 1999 and 2000 the sites were not fully covered. However, most sites were

checked each year. The sites surveyed every year (7 = 52) covered 57 % of the egg clumps

found in 2002. The size of the female spawning population and its annual variation were

estimated based on the census figures from the sites surveyed each year 1999-2002.

The results of this study are compared with those obtained in part of this population in

1973-1977 (HAAPANEN, 1982).

RESULTS

SIZE OF THE FEMALE POPULATION

In 1999-2002 there were in average 786 + 262 (mean and standard deviation) spawning

females in the area. The amount of the spawning frog females increased during the whole

study period and especially from 1999 to 2000 (fig. 3).

In the university farm the spawning female frog numbers were 81 + 44 in 1999-2002,

versus 58 + 43 in 1973-1977 (HAAPANEN, 1982). The difference is not, however, significant (P

= 0.45, r test).

SUB-AREAS

The spawning sites were found from about 0 to 12.5 m above sea level, but not in brackish

waters.

During these four years 91 spawning sites were found on 18 green sub-areas (size 1-

125 ha). They covered 70 % of all green areas.

Only one spawning site was found in the small house block in a dike connecting two

woodlands. In six green areas no spawning sites were seen. During the study period two

sub-areas were lost as spawning area and one additional was found.

The numbers of female frogs varied greatly in these sub-areas. The average number of

spawning females in 2002 was 63 + 70/sub-area (range 3-248). The two sub-areas with 3 and

248 female frogs are located on both sides of a four-lane highway. This big difference in frog

numbers was observed in all four years.

Source : MNHN, Paris

138 ALYTES 23 (3-4)

Population growth

1200-

1000-

600:

400

200:

1999 2000 2001 2002

!! population

Fig. 3. The growth of the spawning female common frog population in 1999-2002 in the study area in

eastern Helsinki. The figures are the sums found in different sub areas.

There is a strong correlation between the number of egg clumps found in a sub-area and

the number of breeding sites (Pearson r = 0.87). So the amount of spawning sites accounts for

76% (r? = 0.76) of the total variation in the numbers of spawning females between the

sub-areas. In contrast, there is only a very low correlation (r = 0.29) between the numbers of

egg clumps and the size (ha) of the sub-areas. The size of the sub-area accounts for only 8

of the numbers of the spawning females.

POPULATION DENSITY IN TERRESTRIAL HABITATS

No frogs were seen to spawn on rocky pine woodland areas although the latter are

extensive in the study area and include some ponds. These pine woodlands account 30 % of

those green areas where no breeding common frogs were found.

The highest population densities (9.1 and 7.0 female frogs/ha) were found in woodland

parks and in woodlands, respectively. In semi-open areas and agricultural land, the densities

were much lower (tab. 1). There are only two agricultural areas and these are grouped in tab.

1 with the semi-open areas. In agricultural land there were only 0.8 females/ha.

The spawning female frog density for the whole green area was 1.3/ha and in the whole

study area it was 0.5/ha.

Source : MNHN, Paris

HAAPANEN 139

The spawning site density was so high (tab. 1) that the frogs could easily reach these sites

in any type of habitat and vice versa.

SPAWNING SITES

The most common spawning site in the study area was the small dikes (tab. 2). One half

of all egg clumps were laid in these dikes. AI] together the egg clumps were distributed within

different spawning habitat types as these habitat types were used (tab. 3). The average number

of egg clumps per site was almost the same (tab. 3).

Only 17 of the spawning sites were used in every four years. In such areas the egg clump

numbers were, however, high in each year (average 31 + 27) and there is highly significant

difference (P <0.001, r test), with the average number of egg clumps (6 + 6) in sites used only

once or twice but not in following years. From 31 to 58 % of sites were empty. The lowest

number of unused sites was found in 2002 when the population density was highest. The

population increase did not cause the continuous increase of egg clump numbers per spawn-

ing site. The population increase was seen in the increase of the number of used spawning sites

(tab. 4). In any spawning site the egg clump numbers varied considerably from year to year.

As the spawning sites are very small water bodies, they may easily become totally dry. A

high proportion of all breeding sites became dry in early June 2002 when the metamorphosis

of larvae had not yet taken place (tab. 5). There were no significant differences between the

desiccation of dikes and ponds. AIl the brooks stayed watered. Some days after the inventory

it rained so much that it is quite probable that the larvae in all remaining sites were able to

metamorphose.

SPAWNING PATTERN AND START OF SPAWNING

The spawning started just after the average day temperature reached above 5°C. The

spawning took 19 days in 2002. Most egg clumps were laid during the first days of spawning:

half of egg clumps was laid already on the fifth day of spawning (fig. 2), and after ten days

80 % of all egg clumps has been laid, both in 2001 and 2002.

DISCUSSION

POPULATION SIZE AND DENSITY

The present common frog population is most probably the continuation of the former

rural population. Taking into account the low survival rate in this species (50 % according to

GiBons et al.. 1984: 40 % according to LOMAN, 1984), the populations of the study area have

lived several generations in the present situation of urbanisation.

The spawning sites of the study area are ideal for egg clump counting and the procedure

developed gives quite exact figures of spawning female numbers.

Source : MNHN, Paris

140 ALYTES 23 (3-4)

Table 1. - Density of spawning females (female frogs/ha) and of spawning sites (sites/10 ha) in

2002 in different habitat types. Semi-open areas cover agricultural areas with woodlands,

100. x, mean; s, standard deviation.

Woodlands Woodland parks Semi-open areas

Population density (x + s) 7+3.8 9.1+1.6 2.142.1

Number of areas 7 2 9

Spawning site density 68 96 1

Table 2. — Distribution of spawning sites (7 — 91) between different habitat types and destruction

and construction of sites in 1999-2002.

Distribution % Destruction n Construction 7

Dikes 51 3 0

Ponds 38 il 1

Brooks 7 0 0

Wider parts of brooks 4 0 1

Total 100 4 2)

Table 3. - Distribution of spawning sites (n = 63) and of egg clumps (7 = 1007) in 2002 within

spawning habitat types, and mean numbers of egg clumps per site. x, mean; s, standard

deviation.

Wider parts of

Dikes Ponds Brooks |" broks

Distribution of sites (%) 54 32 9 4

Distribution of egg clumps (%) si 35 9 5

Number of egg clumps (x s) 15415 184 19 14421 n+il

The frog population density of the study area is much lower than that (50-530 adults/ha)

found by LoMaAN (1984) in southern Sweden or that (64-80 adults/ha) found by PASANEN et al.

(1993) in eastern Finland. Taking into account that, in these Finnish data, there were only

20 % females, the density figures in woodlands and woodland parks were of the same order of

magnitude. The biased sex ratio in northern conditions may be caused by the slower develop-

ment of the females (LOMAN, 1976: GIBBONS et al., 1984).

Source : MNHN, Paris

HAAPANEN 141

Table 4. - Spawning in the 52 sites in 1999-2000, mean and median of egg clump numbers per site.

x, mean; $, Standard deviation.

1999 2000 2001 2002

Percentage used as a spawning site (%) 44 42 50 69

Number of egg clumps/site (x + s) 11411 | 20+24 | 21+26 | 16+20

Number of egg clumps/site (median) 26 43 43 39

Table 5. - Results of the spawning site inventory on 5-10 June 2002. The figures show the sites

which still were watered. Total number of sites surveyed: n = 58.

Dikes Ponds Brooks Total

n(%) n(%) n (%) n (%)

Watered sites 15 (52) 14 (70) 9 (100) 38 (52)

Egg clumps in watered sites | 274 (57) 174 (50) 44 (100) 579 (60)

The results show that the common frog has for generations inhabited areas which seem to

be quite fragmented and isolated, though frogs disappeared from one sub-area because the

spawning sites were filled and the dikes were canalised.

SEPPÂ & LAURILA (1999) estimated that, in the conditions of the Baltic Sea small islands,

32 or more breeding females per island would result in an effective population. In my study

area, 35 % of the populations in sub-areas were below this limit.

Vos & CHARDON (1998) found that the most decisive factor on the occurrence of the

moor frog was the quality of habitat, not the degree of isolation. The data of this study show

that small populations can survive at least several decades even close to highways in spite of

the traffic mortality and the isolation.

Anuran population sizes vary because of variation in the size of annual cohorts (RYSER,

1986). This is quite evident in the case of small populations which are dependent on a small

amount of spawning sites (see e.g. HAAPANEN, 1982). Here there were 91 different spawning

sites available. This clearly levelled the annual population variations. Also in the present data

the amount of spawning females in any spawning site varied considerably from year to year.

CONSERVATION REMARKS

In the study area the destruction of the habitat has not been a big problem during the

study period (tab. 2). On the other hand some new sites were constructed. All the wider parts

of brooks are a result of the restoration of a former canalized brook. The future succession of

the vegetation will probably enhance these sites further.

The slow filling up of shallow dikes and ponds is à natural phenomenon which can

destroy a great part of spawning sites in coming years. The city will be informed on the

importance of the small water bodies as a frog habitat. The general plan provides certain

protection of the summer habitat. Still the fragmentation of the population and especially the

possible habitat loss make the future of the populations uncertain.

Source : MNHN, Paris

142 ALYTES 23 (3-4)

LIMITING FACTORS

This study allows to discuss whether the spawning habitat can be the density dependent

factor limiting the common frog populations in these circumstances.

The summer range of these frogs can be measured as it is isolated from the surrounding

by buildings and wide traffic lines. The frogs can easily reach the whole available terrestrial

habitat as the distance to the spawning sites is not more than 500 m (see also tab. 1).

It was observed that the amount of spawning sites accounted for 76 % of the total

variation in the population density. The size of the terrestrial habitat was only of secondary

importance. It was also found that the amount of egg clumps per spawning site did not

increase with the increase of the total number of egg clumps. Instead, with the increasing

population, the number of spawning sites increased. The frogs apparently started to use the

sites of secondary quality. So the number of spawning sites will be the ultimate limiting factor

in situations when other factors, e.g. climatic conditions, have not caused the local decline of

the population.

RÉSUMÉ

L'étude porte sur la population de grenouilles rousses de la banlieue est de Helsinki,

capitale de la Finlande (60°12°N, 25°08'E). La zone étudiée en 1999-2002 couvre 1.590

hectares, soit 8,5 % de la superficie totale de la ville. Elle a été urbanisée surtout dans les

années soixante et soixante-dix, et sa population de grenouilles provient sans doute des

grenouilles qui y vivaient avant cette période. Les grenouilles occupent les espaces verts de la

zone. Ceux-ci couvrent un quart de la zone et se divisent en cinq catégories: (1) forêts de

feuillus; (2) parcs boisés; (3) parcs à moitié ouverts avec pelouses entretenues; (4) terres

arables; et (5) bois de pins sur terrain rocheux. Dans la catégorie 5 il n°y avait pas de

grenouilles. Les espaces verts des quatre premières catégories sont divisés par des maisons, des

rues et une route à quatre voies en 24 secteurs, dont 18 avaient des grenouilles au moins

pendant une des années d'étude. Les masses d'œufs dans ces 18 secteurs ont été comptées dix

jours après le début du frai ou un peu plus tard. Le résultat obtenu a été corrigé par le nombre

de masses dans le secteur où l'on a pu suivre le frai jour par jour (fig. 1). Les frayères étaient

des petits fossés, étangs, ruisseaux ou parties stagnantes des cours d'eau (tab. 2). La taille

moyenne annuelle de la population de grenouilles en frai a été estimée à 786 (+ 262) femelles

dans la zone entière, et le nombre d'animaux a augmenté d'année en année (fig. 2). Dans les

18 secteurs où il y avait des grenouilles, leur densité moyenne était de 1,3 femelles par hectare.

Celle-ci était la plus grande dans les habitats boisés (tab. 1). Une corrélation significative (r =

0,87) a été constatée entre le nombre de femelles en frai par secteur et le nombre de frayères. La

taille du secteur n'est corrélée qu'avec 7 % du nombre total des femelles en frai. L'accroisse-

ment du nombre de frayères utilisées est allé de pair avec l'accroissement de la population de

grenouilles, mais le nombre de masses d'œufs par frayère a augmenté moins vite. La conclu-

sion est que c’est le nombre de frayères qui limite la taille de la population des grenouilles.

Quand la population croît, une partie des femelles est obligée de choisir des frayères subop-

timales.

Source : MNHN, Paris

HAAPANEN 143

ACKNOWLEDGEMENTS

Mr. Kerkko Hakulinen translated the French summary. My wife, Mrs. Marja-Leena Haapanen,

MD. PhD, has helped in various ways of the treatment of the data. I thank the referees and editors for

their comments 10 improve the text. The City of Helsinki has provided the map of the study area.

LITERATURE CITED

GiBBONS, M. M. & MCCARTHY, T.K., 1984. - Growth, maturation and survival of frogs Rana temporaria

L. Holarctic Ecology, 7: 419-427.

, A., 1982. - Breeding of the common frog (Rana temporaria L.). Ann. Zool. Fennici, 19: 75-79.

, S. P. & BEEBEE, T. J. K., 1997. - Genetic substructuring as a result of barriers to gene flow in

urban Rana temporaria (common frog) populations: implications for biodiversity conservation.

Heredity, 79: 117-127.

JALAVA, H., 1987. [The brooks of Helsinki]. Helsingin kaupungin ympäristénsuojelulautakunta julkaisu,

5: 1-92. [In Finnish].

KETOLA, T., 1998. — [The quality of water and the transport of material in Mellunkylä brook, Eastern

Helsinki]. Helsingin kaupungin ympäristôkeskuksen julkaisuja, 7: 1-46. [In Finnish].

KULMALA, A., LEINONEN, L., RUOHO-AIROLA, T., SALMI, T. & WALDÉN, J., 1998. — Air quality trends in

Finland. Helsinki, Finnish Meteorological Institute, Air Quality Measurements: 1-91.

KUTENKOV, A. P. & PANARIN, À. E., 1995. - Ecology and status of populations of the common frog (Rana

temporaria) and the moor frog (Rana arvalis) in Northwestern Russia with notes on their distribu-

tion in Fennoscandia. /n: S. L. KUZMIN, C. K. Dopp, Jr. & M. M. PIKULIK (ed.), Amphibian

population in Commonwealth of Independent States — Current status and declines, Moscow, Pensoft

Publ.: 64-70.

KUzMIN, $. L., 1994. - The problem of declining amphibian populations in the Commonwealth of

Independent States and adjacent territories. Alytes, 12 (3): 123-134.

LoMaN, J., 1976. - Fluctuations between years in density of Rana arvalis and Rana temporaria. Norw: J.

Zool., 24: 232-233.

== 1984, — Density and survival of Rana arvalis and Rana temporaria. Alytes, 3: 125-134.

Meyer, À. H., SCHMIDT, B. R. & GROSSENBACHER, K., 1998. - Analysis of three amphibian population

with quarter-century long time-series. Proc. r Soc. London, (B), 265: 522-528.

,S.. OLKINUORA, P. & SORIONEN, J., 1993. - Summertime population density of Rana temporaria

in a Finnish coniferous forest. Alytes, 11: 155-163.

SAVAGE, R. M. 1961. - The ecology and life history of the common frog (Rana temporaria temporaria )

London: 1-221.

Sri, P. & LAURILA, A., 1999. - Genetic structure of island populations of the anurans Rana temporaria

and Bufo bufo. Heredity, 82: 309-317.

Vos, C.C. & CHaRDON, J. P., 1998. - Effects of habitat fragmentation

pattern of the moor frog, Rana arvalis. J. appl. Ecol., 35: 44

PASAN

nd road density on the distribution

Corresponding editors: Thierry Lo & Alain Durois.

Source : MNHN, Paris

Alytes, 2006, 23 (3-4): 144-149.

A preliminary biotelemetric study

of a feral invasive Xenopus laevis

population in France

Christophe EGGERT* & Antoine FOUQUET**

* Laboratory of Alpine Ecology, UMR CNRS 5553, CISM, University of Savoie,

73376 Le Bourget du Lac, France

<eggert@univ-savoie.fr>

** Le Buisson Garroux, 79100 Mauzé-Thouarsais, France

The invasive African clawed frog (Xenopus laevis) is currently spread-

ing over a large area in western France. In order to investigate the

population expansion processes we studied the feasibility of implanted

transmitters use. Seven frogs were radiotracked during the winter period.

Even in this cold period of the year, individual movements were observed in

the natural water network, and also in the flooded terrestrial surrounding

area. These areas play a key role in the invasive process. During the study,

freezing and predation by the polecat (Mustela putorius) seemed to be the

major adult mortality factors.

INTRODUCTION

Introduction of non-native organisms into the wild for economic, sport, aesthetic

reasons, or accidentally, are very common processes occurring at a growing rate since the last

century. If in many cases non-native organisms may be harmless in their new environment, in

other cases they prone to escape human control and could become invasive (WILLIAMSON,

1996). Like many animal groups, amphibians have also been the subjects of the invasive

process. The African clawed frog, Xenopus laevis, is one of the known invasive frog species,

currently established in many non-native area, principally in California, Arizona and north

Mexico since the sixties (CRAYON, in press), and in Chile and south Wales since the seventies

EASEY & TINSLEY, 1998; Logos et al., 1999; Loos & MEASEY, 2002). Many other more or

ss isolated populations have also been noticed, including on Ascension Island in the south

Atlantic Ocean since 1944 (TINSLEY & McCoip, 1996; CRAYON, in press). Quite recently feral

African clawed frogs have been discovered in western central France (FOUQUET, 2001) and are

suspected to have become established since the eighties. It may be the largest known European

population since its known range was about more than 100 square kilometers in 2003, which

is likely to be largely underestimated and quickly increasing (FOUQUET & MEAsEY, 2006).

According to climatic conditions, French feral X. luevis suffer almost the same conditions

as in south Wales, which have been described as ill-suited to this southern African species

Source : MNHN, Paris

EGGERT & FOUQUET 145

(MEasey & TINSLEY, 1998). The south Wales populations have been intensively studied

regarding their demographic parameters and feeding habits (MEASEY & TINSLEY, 1998;

MEASEY, 1998, 2001), and they seem to occur only within a limited area (MEASEY & TINSLEY,

1998). A skeletochronological investigation shows that successful recruitment infrequently

occurs (MEASEY & TINSLEY, 1998; MEASEY, 2001), potentially limiting X. laevis spread.

Therefore, the dispersal success of X. Jaevis in the French countryside calls for some explana-

tion. Surprisingly, the African clawed frog, despite being a standard for developmental,

physiological or molecular laboratory studies, remains poorly known regarding its population

ecology, even in its native habitats (MEASEY, 2004). The goals of this study are (1) to test the

use of implantable transmitters to track clawed frogs in the wild, and then (2) to observe frogs’

movement and winter mortality during cold wet season in the area inhabited in France.

MATERIAL AND METHODS

STUDY AREA

We chose one of the numerous colonized ponds of the current frog’s distribution,

according to the following criteria: permanent pond, resembling many other colonized ponds

and surrounded by à maximum diversity of landscapes, not situated in the border of the

occupied area, not holding a high density of African clawed frogs. The chosen pond was

located near Vibreuil (46°59°N, 00°19'E), in the middle of an extensive pasture, surrounded by

typical traditional hedges, including small groves, wooded hedges and ditches (fig. 1), and also

ploughed fields. The pond, shaped with strong sloping banks except on one side, serves as

watering place for some cattle. Its depth was about 200 cm maximum during the study. It was

free of fish, contained very little vegetation, and during the study few other amphibian species

were caught (Zriturus cristatus, T. helveticus). The pond was supplied with water by small

ditches collecting rainwater from the nearby pasture area, but also sometimes by overflow

from the same continuous small ditches which are connected further up to a larger water

network. The pond was connected to the water network only during the wet seasons, i.e.,

probably only a few months each year.

SAMPLING OF CLAWED FROGS AND TELEMETRIC PROCEEDINGS

African clawed frogs were caught using funnel traps baited with pieces of meat (FOUQUET

& MEasEY, 2005) from November 2002 to February 2003. Traps were set for one or two

consecutive nights in the water. Then frogs were brought to the lab for transmitters implan-

tation. They were sexed, weighed and measured with a calliper to the nearest millimeter.

According to the implantation method described by EGGERT (2002), frogs were anaesthetized

and transmitters (Sirtrack, Single Stage Transmitters) were placed through a small incision in

the body cavity. The abdominal muscles and skin layers were then sutured together in two

separate layers. The animals were kept for a few days in aquarium to verify full recovery before

releasing in the exact place of capture. Animals were located about once a week, sometimes

Source : MNHN, Paris

146 ALYTES 23 (3-4)

‘Field road

tractor path

Fig, 1. - Situation plan of the studied area of feral clawed frogs in France.

less during very cold weather conditions. They were located with at least half a meter

accuracy. When death of a frog was suspected in the water, we tried to catch it with a landing

net.

RESULTS

Seven frogs (4 males and 3 females) were caught in the pond and then tracked during

winter (tab. 1).

Most of the frogs’ movements were limited to the pond, but sometimes frogs went out of

it. Thus 19.6 % of the frog locations were situated in surrounding dishes and 21.6 % in

temporary puddles. Only one individual (female 696) did not leave the pond but after 8 days

the transmitter was found alone and damaged some meters out of the pond in the pasture. In

the same way a male (male 555) was predated after a two weeks trip in the small ditches

upstream from the pond. In both cases we assume that the western polecat (Mustela putorius)

was the predator (polecat faeces were found very close to the still working transmitters). Two

males were tracked until transmitter signals were lost for unknown reasons, but in both cases

polecat action is suspected. One was lost just after releasing, while the other (male 1036; see

fig. 2) was tracked for two months. Two dead individuals were found in the pond, close to its

border, without any evident cause of death. One (male 059) had shown a constant movement

activity (but mainly in the pond) during the 3 weeks of tracking, whereas the other (female

436) was found dead only one week after release. In both cases post-operative problems

cannot be excluded, even if posterior autopsies have not revealed any apparent injuries, except

a slight inflammation in the region of the incision.

Source : MNHN, Paris

EGGERT & FOUQUET 147

Table 1. - Some data on radiotracked feral clawed frogs in France (November 2002-February

2003).

Sex/code Size mm| Massg | Date of capture | Last control Cause of loss

Male 059 69 45.0 17 November | 14 December Death

Male 555 68 47.0 16 November | 01 December Predated

Male 696 71 42.7 09 February | 20 February Unknown

Male 1036 74 46.7 13 December 16 February Unknown

Female 436 89 85.7 23 November | 14 December Death

Female 398 94 99.1 23 November 16 February Dead frozen

Female 696 99 114.1 23 November | 14 December Predated

The first two weeks of December were cold (but without freezing), whereas the two last

were milder (a temperature up to 10°C during the day was observed). January was very cold,

with most of the night temperatures below 0°C, like in mid-February. Soil and water became

colder during January, freezing during the first week of February. At that moment, all wetland

habitats were covered with 10 centimeters of ice. One individual (female 398) which moved

about 80 meters from the pond (fig. 2), moved overland through pasture, crossing a wooded

hedge then was located in a puddle 20 centimeters deep. It died in early February by freezing.

DISCUSSION

IMPLANTATION PROCEDURE

As laboratory kept frogs often perform an overhead kicking movement with their clawed

feet, it was necessary to sew up the suture using a large amount of skin. Moreover it was not

possible to keep clawed frogs for a long time in dry conditions, so that healing was consid-

erably longer than in terrestrial amphibians (pers. obs.). Stitches of one female break just after

sewing up and therefore we sewed them again with a larger suture, with a larger recovering of

the two facing skin parts. We suggest using absorbable gut for the muscle layer and nylon

suture for the skin closure. Also broad-spectrum antibiotics to prevent infections in the wild

could be tested. Likewise avoiding cold water temperatures during healing process may

increase healing rate (COLBERG et al., 1997).

CLAWED FROGS MOVEMENTS

In spite of the rather cold weather conditions during the course of our study, clawed

frogs’ movements were not limited to the pond. Trips in the connected small dishes, with lower

Source : MNHN, Paris

148 ALYTES 23 (3-4)

Fig. 2. - Example of clawed frogs movement in the study site during the tracking period (see text). The

other tracked frogs did not move further than these.

water level (maximum about 40 cm), were observed, as well as overland movements. There-

fore, during winter, clawed frogs could be found not only together in ponds or rivers, but also

alone or in small numbers in small temporary puddles unconnected with permanent or

temporary streams. The use of such temporary water places, that are numerous in this

agricultural region, should clearly be considered in any planned eradication program. More-

over, clawed frogs are able to move even in quite cold weather conditions. By marking

individuals during several years in the UK, MEasEy & TiNsLEY (1998) observed that less than

36 % of the frogs were moving between capture sites, mainly over few hundred meters, with a

maximum of two kilometers along a river valley. Overland movements could occur through

woodland with dense undergrowth, over metalled roads and also across rivers. In our study,

leaving the pond was associated with high risk of mortality by contact with predators or by

freezing in a temporary water surface (also several young X. laevis have been found dead in a

shallow pond after a cold period; pers. obs.). Nevertheless, the relationship between animals

with implantable transmitters and predation probability remains to be studied. Severe winters

have been proposed as a major factor affecting clawed frog introduction success in European

area (FRAZER, 1964). Freezing or suffocation underneath ice layer have long been reported for

European amphibians (e.g. Rana temporaria in DE LA FONTAINE, 1881). It was obviously a

cause of X. laevis mortality in France but clearly does not prevent its invasion.

LITERATURE CITED

CoL8eRG M. E., DENARDO D. F., ROJEK N. A. & MILLER J. W., 1997. - Surgical procedure for radio

transmitter implantation into aquatic, larval salamanders. Herpetological Review, 28 (2): 77-78.

Source : MNHN, Paris

EGGERT & FOUQUET 149

CRaYON, I. I, in press. - Species account: Xenopus laevis. In: M. 1. LANNOO (ed.), Status and conservation

of US Amphibians, Volume 2, Berkeley, University of California Press.

De LA FONTAINE, 1881. — Effets des grands froids de l'hiver 1879 à 1880, en particulier sur les règnes

végétal et animal. Publications de l'Institut royal grand-ducal de Luxembourg, 28: 63-92.

Ecerr, C., 2002. - Use of fluorescent pigments and implantable transmitiers to track a fossorial toad

(Pelobates fuscus). Herpetological Journal, 12: 69-14.

Fouqurr, À. 2001. - Des clandestins aquatiques. Zamenis, 6: 10-11.

FouQuer, À. & Mrasey, G J., 2006. - Plotting the course of an African clawed frog invasion in western

France. Animal Biology, in press.

Frazr, J. FE. D., 1964. - Introduced species of Amphibians and Reptiles in mainland Britain. British

Journal of Herpetology, 3 (6): 145-150.

Logos, G., Carran, P. & Lorrz, M., 1999. - Antecedentes de la ecologia tréfica del sapo africano

Xenopus laevis en la zona central de Chile. Boletin del Museo nacional de Historia natural, Chile, 48:

7-18.

Lomos, G. & Massy, G. J,, 2002. - Impact of invasive populations of Xenopus laevis (Daudin) in Chile.

‘Herpetological Journal, 12: 163-168.

Measey, G. J., 1998. — Diet of feral Yenopus laevis in south Wales, UK. Journal of Zoology, 246: 287-298.

_—— 2001. - Growth and ageing of feral Xenopus laevis (Daudin) in south Wales, UK. Journal of Zoology,

254: 547-555.

ee 2004. - Species account: Xenopus laevis (Daudin 1802). In: L. R. MINTER, M. BURGER, J. A.

HaRkisoN, P. J. BisuoP & H. BRaaCK (ed.), Atlas and red data book of the frogs of South Africa,

Lesotho and Swaziland, Washington DC, Smithsonian Institution Press: 266-267.

Measey, G. J. & TINSLEY, R. C., 1998. - Feral Xenopus laevis in South Wales, Herpetological Journal, 8:

23-27.

Tixsuey, R. C. & McCop, M. JL, 1996. - Feral populations of Xenopus outside Africa. In: R. C. TINSLEY

&H. R. KomeL (ed.), The biology of Xenopus, Oxford, Oxford University Press: 81-94.

WILLIAMSON, M, 1996. — Biological invasions. London, Chapman & Hall: 1-256.

Corresponding editor: Alain PAGANO.

Source : MNHN, Paris

Alytes, 2006, 23 (3-4): 150-151. Book review

Laurenti revisited

Günter GOLLMANN

Universität Wien, Department für Evolutionsbiologie,

Althanstr. 14, 1090 Wien, Austria

<guenter.gollmann@univie.ac.at>

Josephus Nicolaus LAURENTI, 1768. — Specimen medicum, exhibens synopsin Reptilium emendatam cum

experimentis crea venena et antidota Reptilium Austriacorum. Facsimile reprint with an English

translation by Sergius L. Kuzmin. Laurenti Verlag, Supplement der Zeitschrift für Feldherpetologie, 7,

2005: 1-247. ISBN 3-933066-24-7.

Reprinting old volumes in zoology has gained some popularity in recent times. In many cases,

beautiful illustrations provided the main attraction of such an enterprise, So why should anybody be

interested in what ADLER (1989) called an “’unimposing little book” with just five black-and-white plates

of illustrations?

Laurentis treatise contains two parts, a systematic overview of the “Reptilia” (including amphib-

ians) and a natural history of Austrian “reptiles”, with some detailed descriptions and remarkable

observations on natural history, including eighty-nine carefully detailed experiments on the venoms of à

number of species. Viewed from a local patriotic viewpoint, this book opens the chronicle of herpetolog-

ical research in Austria (which was a large empire at that time) (TIEDEMANN, 2001). Its main interest for a

wider audience is based on the many genus and species names first proposed here, making it an important

resource for taxonomy and nomenclature even today. Much of its scientific content, especially the

toxicological work, is clearly outdated and will be read mainly for curiosity or historical interest.

Nevertheless, I found — both in the descriptive and in the experimental sections — many statements,

discussions and stories that stimulate reflections on the state and development of science then and now.

The book starts with two prefaces, by Burkhard Thiesmeier and Wolfgang Bôhme, and an introduc-

tion by Sergius Kuzmin. Then Laurenti's treatise is presented, the on the right hand pages, with

the English translation on the opposite pages, followed by the illustrations. Finally, the t or provides

a few comments, a list of books of the authors mentioned by Laurenti, a list of valid scientific names for

species mentioned by Laurenti, and references for main sources of information.

Sergius Kuzmin has undertaken the difficult task of translating the text from one foreign language

into another, One can find flaws and minor mistakes in the translation if one looks for them, but by and

large Kuzmin has succeeded remarkably well in providing a readable and correct English version of

Laurenti's work. The treatment of geographic terms, both Latin and German ones, is slightly inconsistent

as sometimes a modern spelling is given (e.g. “Wieden” for “Widen”, “Dauphine” for “Delphinatu”)

whereas in other an outdated spelling is directly taken into the English text (e.g. “Nusdorfl” or

“Smolandia”). The location “In alpe Etscher” n Etschero monte” (type locality for Triturus

alpestris) is repeatedly rendered as “Escher mountain” though the name of this mountain is Otscher

(RotEK et al., 2003, gave the incorrect spelling Otscher).

The publisher is to be commended for making available this important classical work to a wider

audience.

Source : MNHN, Paris

GOLLMANN 151

LITERATURE CITED

Aoer, K., 1989. — Herpetologists of the past. In: K. ADLER (ed.), Contributions to the history of

herpetology, Saint Louis, Society for the Study of Amphibians and Reptiles: 5-141.

Roërk, Z., JOLY, P. & GROSSENBACHER, K., 2003. - Triturus alpestris (Laurenti, 1768). Bergmolch. /n: K.

GROSSENBACHER & B. THIESMEIER (ed.), Handbuch der Reptilien und Amphibien Europas, Schwanz

lurche I1A, Wiebelsheim, AULA-Verlag: 607-656. :

TIEDEMANN, E, 2001. - Chronik der herpetofaunistischen Erforschung Osterreichs. In: A. CABFLA, H.

GRILLITSCH & F. TIEDEMANN, Atlas zur Verbreitung und Okologie der Amphibien und Reptilien in

Ôsterreich, Wien, Umweltbundesamt: 13-42.

Corresponding editor: Annemarie OHLER.

Source : MNHN, Paris

152 ALYTES 23 (3-4)

LE SEUL OUVRAGE CONSACRÉ

À LA FAUNE HERPÉTOLOGIQUE,

TERRESTRE ET D'EAU DOUCE,

DE L'ARCHIPEL DE LA GUADELOUPE

6 Anoures 21 Lézards

5 Tortues 7 Serpents

Histoire naturelle des Amphibiens et

Reptiles terrestres de l’archipel Guadeloupéen

Guadeloupe, Saint-Martin, Saint-Barthélery

Michel BREUIL

PAR MICHEL BREUIL

PROFESSEUR AGRÉGÉ

340 pages format A4 — 250 illustrations en couleurs

Prix de vente : 46 € (+ port)

Règlement à l’ordre de l'AALRAM, Laboratoire des Reptiles & Amphibiens,

MNHN, 25 rue Cuvier 75005 PARIS

Source : MNHN, Paris

AIN7TTES

International Journal of Batrachology

published by ISSCA

EDITORIAL BOARD

Chief Editor: Alain Durois (Laboratoire des Reptiles et Amphibiens, Muséum national d'Histoire naturelle,

25 rue Cuvier, 75005 Paris, France; <adubois@mnhn.fr>).

Deputy Editor. Franco ANDREONE (Museo Regionale di Scienze Naturali, Via G. Giolitti 36, 10123 Torino, Italy;

<fandreone@libero.it>).

Alytes Editorial Board: Lauren E. BrowN (Normal, USA); Heinz GriLLrrscH (Wien, Austria); Stéphane

GROSIEAN (Paris, France); W. Ronald HEyER (Washington, USA); Esteban O. LAVILLA (Tucumän, Argen-

tina): Thierry LoDÉ (Angers, France); Masafumi MATSUI (Kyoto, Japan); Alain PAGANO (Angers, France),

John C. PoyToN (London, England); Miguel VENCES (Braunschweig, Germany).

Amphibia Mundi Editorial Board: Alain Dupois, Chief Editor (Paris, France); Ronald I. CRoMBIE (San

Francisco, USA); Stéphane GROSIEAN (Paris, France); W. Ronald HEyer (Washington, USA); JIANG

Jianping (Chengdu, China); Esteban O. LAVILLA (Tucumän, Argentina); Jean-Claude RAGE (Paris,

France). David B. Wake (Berkeley, USA).

Technical Editorial Team (Paris, France): Alain Durots (texts); Roger BoUR (tables); Annemarie OHLeR (figures).

Book Review Editor: Annemarie OHLER (Paris, France).

SHORT GUIDE FOR AUTHORS

(for more detailed Instructions to 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 to 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,

acknowiedgements, 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; GRAF & POLLS PELAZ, 1989; INGER

et al., 1974). References in the Literature Cited section should be presented as follows:

BouRRET, R., 1942. — Les batraciens de l'Indochine. Hanoï, Institut Océanographique de l’Indochine: i-x + 1-547,

Graf, J-D. 8 PoLLS PaLaz, M. 1989. Evolutionary genetics of the Rana seule complex, In:R. M. DAwLEt

& I. P. BoGaRT (ed.), Evolution and ecology of unisexual vertebrates, Albany, The New York State Museum:

289-302.

ixceR, R-F. Von, H. K.& Voris, H. H, 1974. = Genetic variation and population ecology of some Southeast

Asian frogs of the genera Bufo and Rana. Biochem. Genet,

Manuscripts should be submitted in triplicate either to Alain Dumois (address above) if dealing with

mphibian morphology, anatomy, systematies, biogeography, evolution, genetics, anomalies or developmental

bi logy, 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. Accep-

tance for publication will be decided by the editors following review by at least two referees.

If possible, after acceptance, a copy of the final manuscript sent by e-mail or on a floppy disk (3 % or 5 4)

should be sent to the Chief Editor. 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 to 7.0); (2)less

preferably, formated DOS (ASCII) or DOS-formated MS Word for the Macintosh (on a 3 14 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 is charged. For each published paper, a free pdf or 25 free reprints are offered by ISSCA

to the author(s). Additional reprints may be purchased.

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 Pdblication: Alain DuBoïs.

Numéro de Commission Paritaire: 64851.

Source : MNHN, Paris:

Alytes, 2006, 23 (3-4): 81-152.

Contents

Vincenzo MERCURIO & Franco ANDREONE

The tadpoles of Scaphiophryne gottlebei (Microhylidae: Scaphiophryninae)

and Mantella expectata (Mantellidae: Mantellinae)

from Isalo Massif, south-central Madagascar. ............................ 81-95

Meike THoMas, Liliane RAHARIVOLOLONIAINA, Frank GLAW & Miguel VENCES

Description of the tadpole of the Malagasy treefrog

BOODhIS ORACLE EEE EEE REC ERRESE R AE CE CRE EE 96-102

Stéphane GROSIEAN & Alain DuBois

Description of advertisement calls of six species

of the genus Chaparana (Ranidae) from Nepal and India .. 103-122

Annemarie OHLER & Alain DuBois L

Hyla reinwardtii Schlegel, 1840

AS A NOMENIPTOECTU A Re D en rase ne 123-132

Antti HAAPANEN

The suburban common frog (Rana temporaria) population

in the eastern Helsinki suburb, Finland ................................ 133-143

Christophe EGGERT & Antoine FOUQUET

A preliminary biotelemetric study

of a feral invasive Xenopus laevis population in France. .…................ 144-149

BOOK REVIEW

Günter GOLLMANN

TO Ce PA nn Bee OO CET PRE EU 0 En 150-151

ANNOUNCEMENT

Amphibiens et Reptiles de Guadeloupe... 152

Alytes is printed on acid-free paper.

Alytes is indexed in Biosis, Cambridge Scientific Abstracts, Current Awareness in Biological

Sciences, Pascal, Referativny Zhurnal and The Zoological Record.

Imprimerie F Paillart, Abbeville, France.

Dépôt légal: 1° trimestre 2006.

Source : MNHN, Paris: