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AILVTES

INTERNATIONAL JOURNAL OF BATRACHOLOGY

December 2002 Volume 20, N° 1-2

Alytes, 2002, 20 (1-2): 1-12.

The tadpole of Ptvchadena aequiplicata

(Werner, 1898) with the description

of a new reproductive mode for the genus

(Amphibia, Anura, Ranidae)

Mark-Oliver RôDEL* **, Daniel KRÂTZ* & Raffael ERNST*

* Theodor-Boveri-Institute (Biocenter of the University),

Department of Animal Ecology and Tropical Biology (Zoology I),

Am Hubland, 97074 Würzburg, Germany

** University of Mainz, Institute of Zoology,

Saarstrasse 21, 55099 Mainz, Germany

<roedel@biozentrum.uni-wuerzburg.de>

We describe the tadpole of Ptychadena aequiplicata (Werner, 1898)

based on specimens from Taï National Park, Ivory Coast. Compared to other

tadpoles of the genus it is unique by its bicoloured body, posterior part

lighter than anterior one. Ptychadena aequiplicata is restricted to closed

forest habitats. lt has a reproductive behaviour unique to the genus.

Clutches of numerous females were communally deposited on the forest

floor, between leaves and small plants. Spawning sites were always situated

at the edges of dried up ponds. Pre-hatching time was variable. Tadpoles

still hatched two weeks after oviposition. In some specimens development

continued in the large eggs up to Gosner stage 28. Developmental time from

hatching to metamorphosis was less than two weeks. We regard this

developmental mode as an adaptation to the surprisingly high desiccation

risks of the forest ponds in Taï National Park.

INTRODUCTION

Piychadena aequiplicata (Werner, 1898) is widespread in West and Central Africa (tab. 1).

In its whole range it inhabits exclusively fo habitats (GUIBÉ & LAMOTTE, 1958; LAMOTTE,

1966; AMIET, 1974, 1975; LARGEN & DoWseTT-LEMAIRE, 1991), mainly primary rain forest

(RivA, 1994; BôHME, 1994). While tadpole descriptions (GUIBÉ & LAMOTTE, 1958; LAMOTTE &

Zu8er-VOGELI, 1953; LAMOTTE et al., 1958, 1959; LAMOTTE & PERRET, 1961: RôDEL, 20004)

and biological data (BARBAULT & TREFAUT RODRIGUES, 1978; RÔDEL, 20004) of many other

Source : MNHN, Paris

2 ALYTES 20 (1-2)

Table 1. - Knowmn distribution of Ptychadena aequiplicata.

BOHME, 1994

GUIBÉ & LAMOTTE, 1957, 1958; SCHIOTZ, 1968; EUZET et al., 1969

EUZET et al., 1969; LAMOTTE, 1967; RÔDEL, 2000; this paper

ScHorz, 1964a

SCHIGTZ, 1963

PERRET, 1966; AMIET, 1974, 1975; LAWSON, 1993; FRETEY & BLANC, 2000

Central African Republic |FRETEY & BLANC, 2000

Republic of Congo FRETEY & BLANC, 2000

Congo LARGEN & DOWSETT-LEMAIRE, 1991; FRETEY & BLANC, 2000

Equatorial Guinea Riva, 1994; FRETEY & BLANC, 2000

Gaboon FRETEY & BLANC, 2000

West African Prychadena species are available, nearly nothing is know about the biology of

this common forest frog. Its voice was made known by ScHioTz (19644) and AMtEr (1974). In

all Ptychadena species where reproduction is known, spawn is deposited as a surface layer in

stagnant waters of variable size (WAGER, 1986; RôDEL, 2000a). In Taï National Park (TNP),

Ivory Coast, we were able to identify P aequiplicata tadpoles in 1999. Those tadpoles have

been collected in forest ponds and raised to metamorphosis to assure species affiliation.

However, other details of the frog's reproductive biology, especially spawning sites and

clutches, remained unknown. In 2000 we found P aequiplicata clutches deposited terrestrially

at the edges of dried up forest ponds.

MATERIALS AND METHODS

STUDY AREA AND FIELD DATA

The TNP is the largest protected area of rain forest in West Africa. Our main investiga-

tion area was located 23 km southeast of the small town of Taï and comprises about 30 km?

of primary and secondary rain forest around the Station de Recherche en Ecologie Tropicale

(SRET,; 5°50°N, 7°20°W). Between 1991 and 1999, mean annual precipitation at the SRET

was 1,854 mm (sd 249; range 1,424-2,194 mm: R. Noë, pers. comm.). Most precipitation

occurred from April to July and from September to November. The first dry period lasted

from December to February, normally a second one occurred in August. The mean annual

temperature was about 25°C. More detailed descriptions of the TNP are provided by

GUILLAUMET (1967) and RiEZEBOS et al. (1994).

Data were collected irregularly in different parts of the forest, and regularly along 10

transects, 600 m in length. Six transects have been set up in primary and four in secondary

forest. Data collection and transect conception were described in more detail in RÔDEL

(2000b) and RÔDEL et al. (in press a).

Source : MNHN, Paris

RÔDEL, KRÂTZ & ERNST 3;

PRESERVATION AND DESCRIPTIVE METHODS

Frogs were sacrificed in a chlorbutole solution and preserved in 4 % formaldehyde or

70% ethanol. Later on all adults were transferred into ethanol. Larvae of different

stages were preserved in 4 % formaldehyde. Measurements were taken with a dial calliper

(& 0.1 mm) or a measuring ocular in a dissecting microscope (+ 0.1 mm; Zeiss Stemi SV 6).

We measured body length (BL), body width (BW, measured at the plane of the eyes), tail

length (TL), fin height (TF), height of tail axis (TA) and body height (BH). Measures are

given in mean values with standard deviation. Nomenclature of morphological features

follows VAN Dux (1966), ALTIG & JOHNSTON (1989) and ALTIG & MCDIARMID (1999). The

labial tooth row formula is according to DuBois (1995). Staging of tadpoles was according to

Goser (1960). The tadpole description is a summary of all specimens from Gosner stages

27-38. The description of the coloration is based on living tadpoles. Drawings were done with

the aid of a camera lucida. Voucher specimens are deposited in the collection of the

Staatliches Museum für Naturkunde Stuttgart (SMNS 9774.1-6, 2 males, 4 females; 9775.1-

15, tadpoles; 9776.1-73, tadpoles).

REARING

Tadpoles were reared in plastic aquaria (PT2 Firma Hoch, 25 X 15 cm, 16 cm water

depth), filled with rain water and fed ad libitum with commercial fish food (TetraMin").

Water was changed every day. As development in nature seems to be much faster (see below),

we don't give any developmental time tables. Species affiliation was assured by tadpoles

captured in forest ponds and partly raised to metamorphosis in 1999 (SMNS 9775.1-15).

RESULTS

TADPOLE DESCRIPTION

Body ovoid in dorsal view (fig. 1b); in lateral view slightly pointed (fig. la); body length

1.70 + 0.08 (x = 51) times body width (measured at the plane of the eyes): body length

0.61 + 0.05 (n = 51) tail length; eyes laterally; nostrils dorsolaterally, closer to snout tip than

to anterior corner of the eyes; tail straight, if extrapolated, axis of tail passing through eyes:

fin height nearly equal to body height (0.80 + 0.08, n = 51); dorsal fin originating anterior to

tail-body junction; dorsal and ventral fin nearly parallel to tail axis; tail tip rounded:

small oral disc anteroventral, bordered by two to three rows of papillae with large rostral

gap, caudal with few larger papillae; many additional papillae grouped in oral angles; jaw

sheaths massive and serrated; upper jaw sheath evenly broad U-shaped; lower jaw sheath

V-shaped; labial tooth row formula of tadpoles, older than stage 28, 1:2+2/2 or 1:2+2/1+1:1

(fig. 2; formulae of all stages are summarized in tab. 2); spiracle sinistral, visible dorsally;

Source : MNHN, Paris

4 ALYTES 20 (1-2)

Fig. 1. Lateral (a) and dorsal (b) view of a Prychadena aequiplicata tadpole (stage 33) from Taï National

Park, Ivory Coast. Scale bar: 10 mm

Fig. 2. - Oral disc of the specimen illustrated in fig. 1. Scale bar: | mm

Source : MNHN, Paris

RÔDEL, KRÂTZ & ERNST 5

Table 2. — Labial tooth row formulae of Piychadena aequiplicata tadpoles, sample size in parentheses.

Stage afer GOSNER (1960).

Stage Labial tooth row formule Stage Labial tooth row formulae

20 Not present (1) 31 1242/1451 (3); 1224272 (3)

2 Not present (1) 32 1:242/1#1:1 (4)

24 1H (1); 11/1451 (4) 33 1:2+2/2 (2)

25 11H11 (6); 1:1#1/1#1:1 (3) 34 122+2/1#1:1 (3)

27 1:1#1/2 (1); 1224222 (1) 35 12#2/1#1:1 (1)

28 11412 (4) 11H/1#H:1 (8); 36 1:2+2/1#1:1 (6)

1:242/1#1:1 (3); 1:2+2/2 (6) 37 1:2+2/1#1:1 (7)

29 1:2+2/2 (3) 38 1242/4131 (1)

vent opening medially, positioned basicaudally. Further measurements are summarized in

tab. 3.

In life the tadpoles are bicoloured. The anterior part of the body is dark beige to brown,

the posterior part is light brown to yellow. The tail axis becomes lighter towards the tail tip.

The fin is transparent. The venter is slightly lighter than the back.

BIOLOGY

In P. aequiplicata sexes differ considerably in size. Mean size in females was 48.3 mm

(range 39-64, n = 8), in males mean SVL was 39.5 mm (range 36-43, n = 6). Two dissected

females (SMNS 9774.5-6; 58 and 54 mm SVL) bore 457 and 478 ovarian eggs, respectively.

The eggs had a diameter of about one mm, and black and white poles.

Male’s choruses were regularly heard after heavy rainfall throughout the whole rainy

season. Calling males were always concealed between leaves or roots, several meters apart

from filled or dried up forest ponds. Calling activity was mainly during night, rarely during

day. Adults were registered in swampy areas, as well as in relatively dry parts of the forest

without open water. Compared to other leaf-litter frogs, P. aequiplicata Was not very abun-

dant. We found 0.15 P aequiplicata per transect hour in primary forest (289 h). During 93

transect hours in secondary forest we found only one P aequiplicata. Tadpoles were conti-

nuously encountered throughout the rainy season. We found them only in stagnant forest

ponds within primary rain forest. Juveniles were registered between end of June and begin-

ning of November. They measured 14.8 + 2.8 mm SVL (11-20 mm, n = 31).

At2 p.m. on September 8", we heard a large chorus at a dry pond after rainfall (site 1).

While approaching the spot, about 50 P aequiplicata jumped away (J. Fahr, pers. comm.). On

September 15‘, we discovered more than 2000 eggs at this site. The eggs were deposited on the

ground between the stalks of herbs. The eggs were congregated on two areas, measuring

1.5 m° and 2 m°, respectively. On September 18‘, we found similar spawning sites at four other

Source : MNHN, Paris

6 ALYTES 20 (1-2)

Table 3. - Ptychadena aequiplicata tadpole measurements (mean + standard deviation). Only tadpoles for

which all measurements were available were taken into consideration. For abbreviations see

Materials and methods. Stage after GOSNER (1960).

——

Stage BL BH BW TL TF TA |BL+TL|BL/BW

20 | 1 | 26 13 13 F 36 14 05 62 20

22 | 2 |26+01/12+01| 1340 |36+02|14+01| 0540 |61+03|20+01

24 | 5 |34:03/154+02|20+03| 5641 |18403|08+03|904+13|17+01

25 | 9 |32402|1.5402|194+02|52+04|17403|0.8+04|8440.6|17+01

27 | 2 |43406|19+03|27+05|50+30|23403|104+01193428|16+01

28 |16|50209/21+03|314206|80412|28406|1140.1 [130220] 17401

29 | 3 |65402|304+02|40202/1034203/3.7402| 13401 169203) 16+0

31 | 6 |88+10/37+07|53+07|149420| 49408 | 1940.3 |23.74+29| 16401

32 | 4 |89408|37+01|53402|143208|47403|20+0.1 [232416] 17401

33 | 2 [92401|394+01|55401/157406| 4740 |214+01 248405] 1740

34 | 3 [92405|38+03|57203|1474+09|47407|21+01|2394+07| 1640

35 [1] 93 41 54 15.0 49 29 243 17

36 | 6 |99404/404+03|58404/167+11|5.1404|22+02 |266+1.5| 17401

37 | 7 f01+05/43+03|62+03|172417|49405|22402|272221| 16401

38 |1| 110 49 63 17.0 52 22 [280 17

forest ponds. These sites comprised several hundreds to thousand eggs, spread between leaf

litter, restricted to a few square meters at the very border of the ponds. AII five ponds were

dried up at that time. Egg size was between 3.5 and 6 mm. At all but one site, all eggs were of

the same stage. Four of the five ponds remained water filled only in the high rainy season

between August and November (Rôdel, unpubl.). AIl spawning sites were located such that

eggs only came in contact to open water after the ponds reached their maximum possible

water capacity.

We assume that the eggs (4-5 mm) we discovered at site 1 were deposited on or shortly

after September 8". On September 16‘, we flooded 100 eggs of these eggs with water. At

that time the original pond was also water-filled. Within 5 min, 95 tadpoles, stage 25,

hatched. None of these tadpoles possessed external gills, but all still had large yolk sacks.

However, they immediately started feeding on the provided fish food. The remaining five

tadpoles were still alive but apparently not able to hatch. We regularly preserved tadpoles

of this series (SMNS 9776.1-73). On September 25!", the tadpoles reached stages 37-38 and

had a body length of 10-11 mm. At that time, P aequiplicata tadpoles in the forest pond had

nearly twice the size of the ad libitum fed captive ones, and were about to metamorphose. In

nature, time from hatching to metamorphosis seemed to last about two weeks. We kept

another 106 eggs of the same site until September 23". Development of these eggs continued

until stage 28 (fig. 3). The diameter of the eggs increased slightly during development (tab. 4).

After flooding the 106 eggs with water, 38 larvae (stage 28) hatched within 40 minutes. After

90 minutes, only six tadpoles remained within the jelly capsules, obviously not able to hatch.

Hatching success therewith equalled those eggs that were flooded a week before. Presuming

that these eggs were deposited the 8‘ or shortly after that date, they survived within eggs for

two weeks.

Source : MNHN, Paris

RÔDEL, KRÂTZ & ERNST 7

Fig. 3. - Lateral (a), ventral (b) and dorsal (c) view of egg stages of Prychadena aequiplicata: (a) and (b)

show individuals of stage 23, (c) figures a stage 25 tadpole. Scale bar: 1 mm.

Source : MNHN, Paris

8 ALYTES 20 (1-2)

Table 4. - Stage of pre-hatching Phychadena aequiplicata and respective egg sizes.

Stage n Egg diameter Stage n Egg diameter

20 2 447 24 2 48

21 8 4.2-5.1 25 2 5.5-5.7

22 3 4.4-5.1 27 2 5

23 2 5-53

On September 18‘, we collected much smaller eggs (3.5 mm) from a second site. We

flooded 28 of these a day later. After 8 hours, only three tadpoles had hatched, all with

external gills and large volk sacks. After 24 hours, 13 tadpoles remained in the eggs, still alive.

During the next 8 hours only four others managed to hatch.

We were able to monitor eggs at one site in the forest for one week. During that time it

seemed that almost none of the eggs had disappeared, despite the fact that numerous ants,

including driver ants (Dorylus sp.), were regularly encountered at that spot. We never detected

any P aequiplicata eggs that were covered with fungi.

DISCUSSION

With the exception of its habitat preferences (e.g., AMIET, 1975; LARGEN & DOWSETT-

LEMAIRE, 1991), its voice (ScHiOTZ, 1964b; Amir, 1974) and the size dimorphism in male and

female P aequiplicata (PERRET, 1966), nearly nothing was known about the biology of this

widespread West and Central African forest frog. Prychadena aequiplicata tadpoles differ

from other West African Prychadena larvae by their bicoloured body, anterior part darker

than posterior one. Other species have a more or less uniform beige or brown body (LAMOTTE

& ZuBer-VOGELI, 1953; GUIBÉ & LAMOTTE, 1958; LAMOTTE et al., 1958, 1959; LAMOTTE &

PERRET, 1961: RÔDEL, 20004). Another distinctive feature was the presence of three labial

tooth rows in the upper lip in tadpoles more advanced than stage 28. Only a few individuals of

P oxyrhynchus and P. mascareniensis tadpoles are also known to possess three tooth rows in

the upper lip (tab. 5).

While the free-swimming tadpoles fit the general characterisation of tadpoles of that

genus (ALTIG & MCDiaRMID, 1999), being exotroph, lentic and benthic, clutch deposition

clearly does not. AIl other known Prychadena species deposit their eggs in a single layer as a

surface film (WAGER, 1986; RÔDEL, 20004). P aequiplicata deposit its eggs on the forest floor

at the border of dried up forest ponds. These eggs are larger than other Prychadena eggs

(compare with RôDEL, 20004). Consequently, P aequiplicata females seem to produce smaller

clutches (tab. 6).

Our experiments showed that P aequiplicata is very variable in respect to hatching time,

lasting from a few days to more than two weeks. This strategy is very similar to that of a

Source : MNHN, Paris

RÔDEL, KRÂTZ & ERNST 9

Table 5. — Labial tooth row formulae (LTRE) of Piychadena tadpoles.

LTRF Piychadena species (source)

V/1H:1 |schubotzi (RODEL, 2000a)

172 |schubotzi (RODEL, 2000a); bibroni (GuiBé & LAMOTTE, 1958; LAMOTTE & PERRET, 1961);

submascareniensis (LAMOTTE et al, 1958); trinodis (LAMOTTE et al., 1958); fournieri

(LAMOTTE et al., 1958; RÔDEL, 20004)

1242 | schubotzi (RÔDEL, 2000a)

1:1#1/1 |bibroni (RÔDEL, 2000a); submascareniensis (LAMOTTE ct al., 1958)

1:1#1/2 |pumilio (LAMOTTE et al., 1959); longirostris (RÔDEL, 20004); oxyrhynchus (GUIBÉ &

LAMOTTE, 1958; WAGER, 1986, LAMBIRIS, 1988; RÔDEL, 2000a); trinodis (LAMOTTE et al.,

1958; RÔDEL, 20004); mascareniensis (PERRET, 1966)

2/2 |oxyrhynchus (LAMBIRIS, 1988, 1989)

1:1#1/3 |oxyrhynchus (LAMOTTE & ZUBER-VOGELI, 1953)

1:2+2/2 |oxyrhynchus (GUIBÉ & LAMOTTE, 1958); mascareniensis (PERRET, 1966)

Table 6. - Egg numbers of West African Ptychadena species.

Species Egg numbers Source

P. aequiplicata 457-478 |This paper

P. bibroni 800-1500 RÔDEL, 20004

P. bibroni 1333+643 | BARBAULT & TREFAUT RODRIGUEZ, 1978; BARBAULT, 1984

P. schubotzi 500-1000 RÔDEL, 20004

P. schubotzi 2011+851 |BARBAULT, 1984

P. oxyrhynchus 3476+ 1542 |BARBAULT & TREFAUT RODRIGUEZ, 1978; BARBAULT, 1984

P. mascareniensis 1079 BARBAULT, 1984

savannah frog, Hemisus marmoratus, who has to cope with rather unpredictable environmen-

tal conditions (RÜDEL et al., 1995; KaminsKY et al., 1999). Forest ponds in TNP dry up

surprisingly often, even during the rainy season (Rôdel, unpubl. data). This high desiccation

risk is due to the sandy soil in most parts of the forest. A variable time until hatching, in

combination with the selection of spawning sites that assure that eggs or tadpoles come only

into contact with water after ponds have completely filled, presumably offers tadpoles enough

time to finish metamorphosis. When development continues within the eggs, tadpoles may

additionally profit in competition with other tadpoles by their head start and towards smaller

predators by their increased size (compare with RôDEL, 1998).

According to STEWART (1967), another larger African ranid, Rana fasciata fuelleborni,

deposits its eggs terrestrially. Single eggs or small groups are attached underneath overhang-

Source : MNHN, Paris

10 ALYTES 20 (1-2)

ing mats of sedges, other dense vegetation or on moist earth about 2.5 cm above water.

Hatched tadpoles drop into water. A large number of West African forest frogs also deposit

their eggs outside of water, e.g. various Hyperolius sp., all Afrixalus sp., Chiromantis rufescens

and all Leptopelis sp. (ScHiorz, 1999; own data). In Hyperolius, Afrixalus and Chiromantis,

tadpoles are often washed into the ponds even after small rains that might not provide

sufficient water to assure metamorphosis. Depositing clutches terrestrially at the border of

potential ponds might minimize the risk of hatching too early. However, at these sites

predation risk might be higher than in arboreal clutches that are often protected by plant parts

(Afrixalus) or foam (Chiromantis; but compare with RÔDEL et al, in press b). In contrast to

this assumption we never observed that P aequiplicata eggs were eaten, even when driver ants

were present, nor did we ever observe eggs covered with fungi. It might therefore be interesting

to assay the egg capsules with respect to their chemical components.

ACKNOWLEDGMENTS

MOR was supported by a post-doctoral scholarship from the German Academic Exchange Service

(DAAD). Analyzing and publication of the data was part of the BIOLOG-program of the German

Ministry of Education and Science (BMBF; Project WO8 BIOTA-West, 01 LC0017). TROPENBOS-

Côte d'Ivoire helped with transportation and various administrative services. Lodging facilities in TNP

were provided by the “Centre de Recherche en Ecologie” and the “Projet Autonome pour la Conservation

du Parc National de Taï (PACPNT)”. The “PACPNT” and the “Tai Monkey Project” provided logistic

support. Research permission was given by the “Ministère de l'Enseignement Supérieur et de la Recher-

che Scientifique” of the Republic of Ivory Coast. The access permit to TNP was issued by the “Ministère

de la Construction et de l'Environnement”. G. G. Gbamlin and C.Y. Ouoro were of invaluable help

during field work. J.-L. Amiet made valuable comments on a previous draft of the manuscrit. These

supports are gratefully acknowledged.

LITERATURE CITED

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modes, morphologies and habitats. Herp. Mon, 3: 81-109

ALriG, R. & MCDiaRMID, R. W., 1999. — Diversity: familial and generic characterizations. /n: R. W.

McDiarmin & R. ALTIG (ed.), Tadpoles: the biology of anuran larvae, Chicago, Illinois, Univ.

Chicago Press: 295-337,

AMIE, JL-L., 1974. — Voix d° amphibiens camerounais. IV. Raninae: genres Piychadena, Hildebrandtia et

Yaoundé, 0: 33-107.

BaRBAULT, R., 1984. — Stratégies de reproduction et démographie de quelques Amphibiens Anoures

tropicaux. Oikos, 43: 77-87.

BaRBAULT, R. & TREFAUT RODRIGUES, M., 1978. - Observations sur la reproduction et la dynamique des

populations de quelques anoures tropicaux. I. Prychadena maccarthyensis et Prychadena oxyrhyn-

chus. Ter! 32: 441-

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Source : MNHN, Paris

Alytes, 2002, 20 (1-2): 1

Description of a new torrent frog

in the genus Arthroleptides

from Tanzania (Amphibia, Anura, Ranidae)

Alan CHANNING*, David C. MoyER** & Kim M. HOWELL***

* Zoology Department, University of the Western Cape,

Private Bag X17, Bellville 7535, South Africa

<achanning@uwc.ac.za>

** Wildlife Conservation Society, PO. Box 936, Iringa, Tanzania

<wes@wes.or.12>

*#* Department of Zoology & Marine Biology, University of Dar es Salaam,

PO. Box 35064, Dar es Salaam, Tanzania

<khowell@twiga.com>

A new torrent frog in the genus Arthroleptides is described from the

Udzungwa and Uluguru mountains in Tanzania. It is distinguished from the

previously known species, A. dutoiti and A. martiensseni, by its large size,

non-thickened supratympanic ridge, and more extensive webbing. À key to

the three species in this endemic East African genus is presented.

INTRODUCTION

The series of block-faulted highlands forming a chain on the eastern side of Tanzania are

known collectively as the Eastern Arc Mountains (LOVETT, 1990). Major montane elements

from south to north are the Udzungwas, Rubehos, Ukagurus, Ngurus, Ulugurus, East and

West Usambaras, South and North Pares, and Taita Hills (fig. 1). The Eastern Arc Mountains

are very old, consisting of basement crystalline rocks that were thrust up during the formation

of the East African rift system (Grirrrrus, 1993). It is believed that they have been biologi-

cally stable for long periods of time, during which many new species have evolved (LOVETT,

1993; FreLpsÀ & LoveTT, 1997). There is evidence that forest cover may have been in existence,

continuous

, for some 30 million years.

Forests on the Eastern Arc mountains are recognized for their diversity of plants and

animals, and represent centers of high endemism in all groups of organisms studied (KING-

DON, 1989; LOvETT, 1990).

A large proportion of the amphibians found in the forests of the Eastern Arc mountains

isendemic. NIEDEN (1911) described a large torrent frog from the research station at Amani in

Source : MNHN, Paris

14 ALYTES 20 (1-2)

KENYA

Area

see

Ngorongoro Kilimanjaro

MeruQ Ci de Tic Hils

North Pare

Mbulu

South Pare

(O)

Eastern Arc Hanang

mountains

Forested

volcanic mts.

Other forested

mountains

0 100

West Usambara (

5 Pemba

Zanzibar

East Usambara —

Northern Nguru 4

(Nguu) *

É*guru

Ukaguru

Rubeho

(Usagara)

4 Uluguru

« Malundwe

Kipengere

ne à

[

el zaMBA) \| Livingstone

34° 36°

[TANZANIA

t Mahenge

Makambako Gap

Fig. 1. Map showing the mountains comprising the Eastern Arc in Tanzania. Arthroleptides yakusini n.

sp. is known from the Udzungwa and Uluguru mountains, and A. martiensseni is known from the

West and East Usambaras and the Ngurus.

the East Usambaras. It was similar in many respects to the leaf litter frogs Arthroleptis Smith

1849, and the West African Perropedetes Reichenow, 1874. Nieden proposed the genus

Arthroleptides for this frog. He named the species Arthroleptides martiensseni, after one of the

collectors, the German military commander in Tanga. The type specimen of this species

collected at Amani, and although the specimen presented by Martienssen to the Berlin

Zoological Museum had no definite locality, Nieden assumed it was also from the Usambaras.

This frog was distinguishable from all others in the area by the presence of large bifid dises on

the fingers and toes. C. A. Du Toit discovered a second species of Arthroleptides on Mt Elgon

Source : MNHN, Paris

CHANNING, MOYER & HOWELL 15

in 1934, that LOVERIDGE subsequently (1935) named Arthroleptides dutoiti. It was distin-

guished from 4. martiensseni by the dark ventral coloration with pale spots, smaller size, and

eyes that protruded beyond the jaw when viewed from below.

À. dutoitiis only known from Mt Elgon, an extinct volcano on the border between Kenya

and Uganda. 4. martiensseni has been recorded from the East Usambaras, the Ngurus, the

Uluguru Mountains, and the Udzungwa Mountains in Tanzania, but fieldwork in Tanzania

during 1999-2001 showed that torrent frogs from the Udzungwa and Uluguru mountain

ranges were consistently separable from Arthroleptides martiensseni in the Usambaras. This

southern form is here described as a new species.

Characters previously used to distinguish the species are reviewed, and a key is provided.

KLEMENS (1998) described the extent of male secondary sexual characters in Arthroleptides

based on a specimen from the Udzungwa Mountains. The specimen illustrated in that paper

is selected as the type for the new species.

MATERIALS AND METHODS

Animals were collected in the field during 1999-2001, and photographed before being

preserved. Comparative material was obtained from the collections in the Zoology and

Marine Biology Department at the University of Dar es Salaam in Tanzania (UDSM and

KMH numbers), the American Museum of Natural History (New York), the California

Academy of Sciences (San Francisco), the Museum of Comparative Zoology at Harvard, and

the Museo Tridentino di Scienze Naturali (Trento, Italy). Material with AC field numbers will

be deposited in the American Museum of Natural History, specimens with RdS field numbers

will be deposited in the National Museum in Washington, and specimens with ES field

numbers will be deposited in the California Academy of Sciences in San Francisco. Specimens

examined included tadpoles, juveniles, and large adults. The material examined is listed in

app. 1, and includes 48 Arthroleptides n. sp. and two batches of Arthroleptides n. sp. tadpoles,

19 4. martiensseni and two batches of 4. martiensseni tadpoles, and five 4. dutoiti. This genus

is not well represented in collections.

The measurements taken, in millimeters, include: snout length, measured from anterior

corner of eye to tip of snout; horizontal diameter of eye; horizontal tyÿmpanum diameter;

distance from tympanum to snout tip; maximum jaw width; snout-vent length; distance

between anterior corners of eyes; length of third finger to include the palmar tubercle; length

of fourth toe to include the metatarsal tubercle; length of tibia measured with the leg bent;

width of forearm. The measurements were compared as ratios of tympanum-

snout/tympanum, snout-vent length/tympanum, width of disc of fourth toe/tympanum, jaw

width/snout-vent length, tympanum/distance between anterior corners of eyes,

tympanum/eye, snout-vent length/distance between anterior corners of eyes, tibia/snout-vent

length, snout-vent length/third finger, snout-vent length/ fourth toe, snout-vent length/eye,

forearm width/eye, and jaw/tympanum. Webbing forms a thin margin along the toes, and

traditional webbing formulae (e.g8. SAVAGE & HEYER 1997) based on measures of phalanges

free of web are not useful. However, the amount of webbing measured from the notch

Source : MNHN, Paris

16 ALYTES 20 (1-2)

between the toes (“main web”) against the position of the proximal subarticular tubercle

shows fixed differences between the species. The main webbing between the toes was measured

against the proximal subarticular tubercles of the relevant toes. The main webbing of the

fourth toe was measured on the inner and outer side.

Observations of breeding biology, including advertisement call, egg deposition sites and

tadpole development were made for the new species at Kihansi in the Udzungwa mountains.

Calls were recorded in the forest at 600 m in the Kihansi Gorge on the Udzungwa escarpment,

using a Sony MZ-R70 recorder and an omnidirectional microphone placed at waist level in a

bush near the calling individuals. A long cable permitted the observer to record the calls from

five meters away. Calls were analysed using CANARY 1.2.4 (Cornell Laboratory of Ornithol-

ogy, 1998) running on a Macintosh G4 or iBook. The tadpoles of the new species were

compared to À. martiensseni tadpoles from the East Usambaras, and described using the

approach of ALTIG & MCDIARMID (1999).

Arthroleptides yakusini n. sp.

Holotype. - À male, collected on 8 December 1995 along the Njokomoni river, Udzungwa

Mountains National Park, Tanzania, 07°4857"S, 36°51°15°E, by M. W. Klemens. The

specimen, AMNH A.151342, is housed in the American Museum of Natural History.

Paratypes. - Three specimens collected at the same time and place as the holotype, a male

AMNH A.151343 and two females A.151341 and A.151344.

Other material. — Specimens assigned to this species are listed in app. 1.

Diagnosis. — A large frog, exceeding 70 mm SVL in exceptional males, and 54 mm or over in

13 of 14 adults examined. The new species is distinguished from Arthroleptides dutoiti by its

larger size, over 35 mm SVL in mature males (less than 25 mm in 4. dutoiti males), webbing

more extensive, with the main web reaching or passing the proximal subarticular tubercle on

both sides of the fourth toe (never reaching in À. dutoiti) (P < 0.0001, Mann-Whitney U test).

The posterior edge of the supratympanic ridge is never thickened (always thickened in 4.

dutoiti).

The new species is distinguished from 4. martiensseni by more extensive webbing (P <

0.0001, Mann-Whitney U test) with the main web always reaching or passing the proximal

subarticular tubercle of the fourth toe (only reaching in one specimen of 20 examined in 4.

martiensseni, falling far short in the other specimens).

Description of the holotype. - Comparative measurements of the holotype and the three

paratypes are presented in tab. 1. The holotype is a male with well-developed secondary sexual

characters, 73 mm SVL (fig. 2). The head is broad, with the maximum jaw width (32.0) 44 %

of the SVL. The eyes are not visible from below. The nostrils, situated near the front of the

snout, open 45° postero-laterally. The tympanum (6.6) is dark, round, ringed with small

. snout to tympanum distance is 22.9. The horizontal diameter of the tympanum

is slightly less than half the distance between the anterior corners of the eyes (13.5). The

tympanic papilla is black, protruding from the upper half of the tympanum. The supratym-

panic ridge obscures the upper posterior margin of the tympanum. This ridge is nearly

Source : MNHN, Paris

CHANNING, MoYER & HOWELL 17

Fig. 2. Holotype of Arthroleptides yakusini, AMNH A.151342. Snout-vent length is 73 mm. Redrawn

after KLEMENS (1998).

straight when viewed from the side, and is illustrated in KLEMENS (1998). The basal portion of

the ridge is not thickened.

The forearm (10.7) is wider than the diameter of the eye (7.8). The terminal disks of the

fingers and toes are large, bifid, with a pair of dorsal scutes. The width of the disk on the third

finger is 50 % of the width of the tympanum (fig. 3). The third finger is 20.4 measured to the

base of the palmar tubercle. The palmar, metatarsal and subarticular tubercles are well

developed. The tibia (43.7) is 59 % of the SVL, and the fourth toe (38.9) is 53 % of the SVL

(fig. 4). No femoral glands are present.

Webbing extends in a distinct margin along the toes. The main web reaches the middle of

the proximal subarticular tubercle of the first toe, the distal edge of the proximal subarticular

tubercle of the second toe, and the lower inner edge of the proximal subarticular tubercle of

the third toe, passing beyond the outer edge. The main webbing passes the proximal subarti-

cular tubercle of the fourth toe on the inside, and reaches it on the outside. Main webbing

reaches the middle subarticular tubercle of the fifth toe.

The dorsum and upper limbs are gray-brown with darker mottling. The back of thethigh

is speckled with white on a dark background. The throat is dark with pale speckling, while the

chest and belly have a paler background with white speckles. The underside of the limbs is

pale. The dorsal skin is granular, with small white-tipped warts on the side of the head. The

upper and lower jaws are edged with minute dark-tipped spines.

Source : MNHN, Paris

18 ALYTES 20 (1-2)

Fig. 3. - Right hand (ventral view) of A. yakusini AMNH A.151342. Scale line: 10 mm.

The paratypes are similar but with none of the secondary sexual characters. See tab. 1 for

comparative measurements.

The type and paratypes have encysted parasites in the skin, probably mites. These are also

present in sympatric 4frana and Phrynobatrachus spp. in material collected at the same time.

Other material examined. — The mean, range and standard deviation are given for the

ratios investigated in tab. 2. The jaws are wide, varying between 40 and 45 % of the SVL in À.

vakusini. The tympanum is exceptionally large in males displaying secondary sexual charac-

ters, with a dimension equal to nearly half the distance between the anterior corners of the

eyes, but considerably less in smaller males and females, where the tympanum may be as small

as 20 % of the distance between the anterior corners of the eyes. In large males showing spines

on the chin and throat, and a ring of spines around the tympanum, the forearms are also

hypertrophied, with the forearm width sometimes reaching up to 150 % the diameter of the

eye. In animals not displaying secondary sexual characters, the forearm thickness is less than

eye diameter, and may be as little as half eye diameter. The mean tibia/SVL proportion is 60 %

in the three species, with no relationship with size or sex. The main web of 4. martiensseni

never passes the subarticular tubercle of the fourth toe on either side. In only one specimen

examined, a 19.8 mm SVL juvenile from the East Usambaras, did the main web just reach the

proximal edge of the subarticular tubercle of the fourth toe, and just pass the subarticular

tubercle of the third toe. In contrast, the main web of 31 of 34 4. yakusini examined passed

Source : MNHN, Paris

CHANNING, MOYER & HOWELL 19

Fig. 4. Right foot (ventral view) of A. yakusini AMNH A.151342 on the left and A. martiensseni CAS

168625 on the right. Scale lines: 10 mm.

the subarticular tubercle of the third toe, and reached or passed the subarticular tubercle of

the fourth toe (P < 0.0001, Mann-Whitney U test). The proportions of the web and

subarticular tubercles are such that there is nearly twice as much webbing in À. yakusini as in

A. martiensseni. The digital discs vary by age and presumably by sex and reproductive status.

Figure 5 illustrates the variation in the disces of the fourth toe in some specimens. The relative

size of the disc, for example when compared to tympanum size, would not be useful in this

genus. Work is in progress to investigate this variation. The body proportions investigated

(tab. 2) show slight differences between males and females, but no significant differences

between the three species.

The differences in the amount of webbing between A. yakusini and À. martiensseni are

consistent in all specimens examined and represent an absolutely distinct character with no

overlap in variation between the species.

In life, many individuals show an orange-reddish band through the upper part of the eye.

The dorsal color pattern is a remarkably good camouflage against leaf litter on the forest

floor. Smaller animals are nearly invisible against a wet log, for example, with only the pale

digital scutes showing. Some smaller animals have distinct transverse banding on the back.

Source : MNHN, Paris

20 ALYTES 20 (1-2)

Table 1.- Comparative measurements of the holotype and paratypes of Arthroleptides yakusini.

Status Holotype Paratype Paratype Paratype

AMNH number A.151342 | A151341 | A151343 | A.151344

Sex Male Female Male Female

SVL 73 57 55 56

Eye 78 72 62 7.1

Tympanum 66 31 45 35

Tympanum-snout tip 229 19.5 17.6 18.7

Jaw width 320 23.6 228 24.0

Anterior cyes 13.5 122 10.8 114

Length 3 finger 204 16.9 163 173

Forearm width 10.7 40 55 47

Length 4" toe 38.9 32.0 284 30.8

Tibia 437 343 342 372

Main inner web toe 4: proximal tubercle Passes Passes Passes Reaches

Main outer web toe 4: proximal tubercle Reaches Reaches Passes Reaches

Table 2. - Mean, range and standard deviation for the ratios examined in specimens of

Arthroleptides yakusini. The overall mean is based on males, females and juveniles.

Males

Mean (range) s,

Females

Mean (range) s, m

Ratio Overall

mean

Tympanum-snout / tympanum 5.64

Snout-vent length /tympanum | 16.59

Jaw width / snout-vent length 0.43

Tympanum / anterior eyes 031

Tympanum / eye diameter 048

Snout-vent length / anterior eyes | 4.92

Tibia / snout-vent length 0.63

Snout-vent length / third finger 3.50

Snout-vent length / fourth toe 1.86

Snout-vent length / eye 7.70

Forearm /eye 0.68

Jaw width / tympanum 7.05

4.36 (3.81-5.62) 0.84, 7

13.11 (10.80-17.08) 2.53, 7

0.43 (0.40-0.45) 0.02, 7

0.39 (0.27-0.49) 0.08, 7

0.73 (0.73-0.85) 0.06, 4

5.01 (4.37-5.63) 0.43, 7

0.65 (0.60-0.68) 0.03, 7

3.29 (3.14-3.58) 0.17, 7

1.77 (1.61-1.93) 0.10, 7

9.07(8.85-9.36) 0.34, 3

0.95 (0.89-1.37) 0.23, 4

5.67 (4.85-7.25) 1.00, 7

5.64 (4.86-6.29) 0.47, 6

16.63 (16.00-18.48) 0.96, 6

0.43 (0.41-0.44) 0.01, 6

0.31 (0.25-0.32) 0.02, 6

0.48 (0.43-0.56) 0.05, 5

4.92 (4.70-5.19) 0.18, 6

0.63 (0.59-0.69) 0.04, 6

3.50 (3.24-3.56) 0.12, 6

1.86 (1.72-2.01) 0.10, 6

7.71 (7.68-8.99) 0.52, 5

0.68 (0.56-0.94) 0.17, 5

7.06 (6.62-7.61) 0.39, 6

Source : MNHN, Paris

CHANNING, MOYER & HOWELL 21

Fig 5. Comparison of the dises of the fourth toe of À. pakusini AMNH A.151342 (left), À. martiensseni

CAS 168625 (middle) and 4. yakusini KMH 21534 (right). Similar variation was found within all

populations examined

Male secondary sexual characters. — KLEMENS (1998) discussed the development of male

secondary sexual characters in Arthroleptides. These are shared by its assumed sister group,

Petropedetes, in West Africa. The characters include a soft tympanic papilla, spines on the

chin and throat, enlarged forearms and a ring of spines around the tympanum. Unlike most

frogs in the area, it appears that the males are larger than the females. Males collected out of

season, smaller males and females show none of these characters (KLEMENS, 1998). The

relationship between Petropedetes and Arthroleptides is under investigation. NARINS et al.

(2001) investigated the function of the tympanic papilla in Petropedetes parkeri.

Advertisement call. - Males call after the start of the short rains in November. Calling takes

place after dark, from the forest floor, although males may climb on to rocks or fallen tree

trunks to call. The call is a series of short “wauks” repeated at long intervals of up to 25

seconds. A total of 39 calls from five individuals was analysed. Calls consist of 4 to 8 pulses

{mode 6) produced in 30.6 to 81.2 ms (x 60.9 ms, s 9.1, n 39). The resulting pulse rate varies

from 73.2 to 106.5/s (x from 1.2 to 1.4

kHz (x 1.3 kHz, s 0.04, n 39). A sound spectrogram of a typical call is illustrated in fig. 6.

Eges. — The following descriptions are based on observations made in January 2001 at

Kihansi. The dark eggs are deposited either in small groups of four or five, or in large mas

of about 200. The eggs are always attached to sloping or vertical rock faces that are covered by

a film of water. Near the base of the Kihansi falls the rocks were wet from drifting spray, while

ses

Source : MNHN, Paris

22 ALYTES 20 (1-2)

2.54

2.04 Î

1.57 | |

1.04 }

0.s-

HE ns 0 30 100 150 200

Fig, 6. - Sound spectrogram of a typical advertisement call of Arthroleptides yakusini, Kihansi Gorge,

Udzungwa mountains, Tanzania. 24°C, 28 January 2001.

other rocks in dryer situations were wet from natural drainage from higher ground. Each egg

is 2 mm in diameter, in a 4 mm capsule. The eggs are camouflaged against the dark reflective

surface.

Tadpoles. - Tadpoles at various stages were collected over a period of three months from the

Udzungwa escarpment. They are similar in body proportions and mouthparts to the tadpoles

of Arthroleptides martiensseni (DREWES et al., 1989, whose descriptive approach is followed

here for comparison).

This description is based on a tadpole of stage 37 (AC 2452) collected in the Kihansi

Gorge in the Udzungwa Mountains, Tanzania. The individual (fig. 7) has a total length of

27.4. Its other measurements and major features are: body length 8.7, tail length 18.7, body

height 6.0 from snout 3.1, body width 6.0 from snout 4.7, tail muscle height at base 1.5,

greatest dorsal fin height 10.0 from tail tip. The ventral fin is absent. Interorbital distance 2.3

internarial distance 1.4, snout to anterior edge of nares 0.8, snout to anterior corner of eye

1.9, snout to spiracle 5.2, posterior edge of naris to anterior corner of eye 1.0, naris diameter

0.13, eye diameter 1.3, pupil diameter 0.6 and width of oral disc 2.2. Oral disc without

anterior oral papillae (fig. 8), vent medial, eyes protruding dorsally, sinister spiracle, with a

labial tooth formula 3(1-3)/3(1).

Fig. 7. A 27.4 mm tadpole of Arthroleptides vakusini from Kihansi, Udzungwa Mountains, Tanzania.

AC 2452.

Source : MNHN, Paris

CHANNING, MOYER & HOWELL 23

Fig. 8. - Oral disc of the tadpole of 4. yakusini AC 2452.

The labial tooth rows have about 52 teeth/mm. The upper jaw sheath is strongly curved,

resembling the beak of a parrot. The lower jaw sheath is acutely curved, fitting inside the

upper sheath when the jaws close. The posterior edge of the oral disc has a double row of

marginal papillae, becoming single towards the angle of the jaw. The papillae are short and

rounded.

The oral disc is closed in preserved specimens, similar to the illustration in DREWES et al.

(1989). The upper labium is flexed to cover the lower labium. When the disc is closed the

medial ends of labial tooth rows A-1 overlap.

The body is widest posteriorly in dorsal view. The dorsal fin is very reduced, as high as it

is wide. The ventral fin is absent. In an earlier stage 23 tadpole (fig. 9) both fins are better

developed. At this stage the external gills are still present. In specialised tadpoles like these

that live on wet rocks, the timing of the loss of external gills and the development of hind legs

Fig. 9. - A stage 23 tadpole of Arthroleptides vakusini from Kihansi, Udzungwa Mountains, Tanzania,

AC 2453, to show the dorsal and ventral fin development

Source : MNHN, Paris

24 ALYTES 20 (1-2)

for locomotion are not comparable to more typical tadpoles and it is not possible to compare

stages directly. The eyes protrude dorsally. The spiracle opening is a small vertical slit 0.1 high.

The vent tube is rounded, extending 0.5 beyond the hind legs, the opening not attached to the

tail muscle. Femoral glands are present extending from near the knee, for 1.3 along the back

of the thigh. The toes are separate with distinct discs. The bifid dorsal disc scutes are not yet

developed.

The dorsal surface is dark with darker markings and pale spots. The dorsal half of the

tail is much darker than the lower half. Nine light dorsal patches on the tail extend on to the

sides. These are saddle-like in living specimens. Ventrally the belly has some mid-belly

speckling with fine spots. AII other ventral surfaces are white. Five gut spirals are just visible

through the belly muscles.

Tadpoles hatch from the eggs and remain on the wet rock faces. They may occur at high

densities on rock faces in a film of water, with 22 counted in one square meter below the

Uluguru North Forest Reserve, grazing on algae. They complete development in the film of

water, taking 8 to 10 weeks. Tadpoles were found during the day under stones in a road-side

ditch at Morningside, Uluguru Mts (1 May 1980). After the tail is resorbed, juveniles leave the

nursery rock and can be found feeding in vegetation along streams and in leaf litter in forest.

Etymology. - The species name yakusini is an adjective, derived from the Swahili ya kusini,

meaning “of the south”. It refers to the distribution of this species in the mountains to the

south of the range of A. martiensseni, With which it has long been confused.

DISTRIBUTION AND HABITAT OF THE THREE SPECIES

The three species of Arthroleptides are allopatric as far as is known, but further fieldwork

is needed to determine their detailed distributions. Arthroleptides dutoiti is known from rocky

streams that drain Mt. Elgon, an extinct volcano on the common border of Kenya and

Uganda. Much of the forest habitat on the lower slopes has been cleared and it has been

suggested that this species is extinct (DREWES et al., 1989). However, these seasonally common

frogs should be looked for at the start of the rains. They are found in cracks and under large

rocks on the side of steep slopes, a habitat requiring a lot of search-effort. Their eggs are large

(3 mm) and pigmented, but the tadpoles are unknown.

Arthroleptides martiensseni is found in the East and West Usambaras, and Nguru

mountains. It occurs both in forest leaf litter far from water, and along rocky streams.

Juveniles have been found in quiet pools and seepages. The adults shelter under large boulders

along fast flowing streams, emerging after nightfall to feed. The wide jaws suggest that this

species and 4. yakusini are important predators on smaller frogs like Arthroleptis stenodacty-

lus Pfeffer, 1893 that are common in the forest leaf litter. The eggs are unknown, but the

tadpoles of 4. martiensseni with very characteristie mouthparts have been described (DREWES

et al., 1989).

Arthroleptides yakusini is known from the Uluguru and Udzungwa mountains from 300

m up to 2800 m. After the tadpoles metamorphose, the juveniles leave the nursery rock and

move into vegetation and leaf litter to feed. They have been found in small pools along

Source : MNHN, Paris

CHANNING, MOYER & HOWELL 25

Streams, or climbing on leaves on the top of vegetation. Small, non-adult individuals of 4.

yakusini are also found in cracks and fissures of vertical rock and soil faces along small

streams and drying stream beds. They peer out at observers and immediately try to go deeper

in if disturbed. The adults, especially the larger animals, move deep into cracks under large

rocks during the day, emerging onto wet rock faces after dark to feed. Adults have been found

on the forest floor some distance from water, under a rotting log on a stream bank, and

occupying a crack in tree bark. Sometimes an individual will emerge and sit out on rocks just

covered with shallow, fast flowing water, where it can easily escape downstream with the

current. Adults are capable of large leaps.

IDENTIFICATION

The characters used by LOVERIDGE (1935) to distinguish between A. dutoiti and A.

martiensseni (eyes visible from below, and dark belly with white spots) are of limited use. The

jaws are relatively wider in larger animals, and the eyes may be visible from below in smaller

specimens of À. martiensseni and À. yakusini. AI three species have individuals with purple

bellies and white spots. The following key will help identifying species of Arthroleptides:

la. Base of glandular supratympanic ridge thickened, animals never over 35 mm SVL ...….

. Arthroleptides dutoiti

Ib. Base of sobraiane ridge never thickened, mature RS cicecline 50 mm SVL

a )

2b. Web notch never reaching proximal subarticular tubercle of fourth toe.

ACKNOWLEDGEMENTS

The National Geographic Society is thanked for providing grant 6475 to AC. The Wildlife Conser-

vation Society of New York provided support through Michael W. Klemens who also provided illustra-

tive material, Jenny Channing, Alison Channing, Billy Munisi, Elia Mulungu and Rafael de

thanked for assistance in the field. The Tanzanian Commission for Science and Technology COSTECH

issued a research permit 99-55-NA-99-40 to AC for which they are thanked. Jenny Channing prepared fig.

2,7 and 9. The National Research Foundation of South Africa assisted financially, and much of the work

was undertaken during a sabbatical granted to AC by the University of the Western Cape.

The following kindly loaned comparative material in their care: Dr L. Ford (AMNH), Jens

Rasmussen and Dr R. C. Drewes (CAS), José Rosado and Dr J. Hanken (MCZ), M. Menegon (MTSN).

We acknowledge Frontier Tanzania, a joint cooperative ‘ch programme between the Society for the

Exploration of the Environment, UK and the Faculty of Science, University of Dar es Salaam who

collected some of the material.

Dr J. C. Poynton offered valuable advice on an earlier draft.

Source : MNHN, Paris

26 ALYTES 20 (1-2)

LITERATURE CITED

ALTIG, R. & McDiarMip, R., 1999. - Body plan. Development and morphology. /n: R. MCDiARMID & R.

ALTIG (ed.), Tudpoles - The biology of anuran larvae, Chicago, Chicago University Press: 24-51.

DREWES, R. C., ALTIG, R. & HOWELL, K. M. 1989. - Tadpoles of three frog species endemic to the forests

of the Eastern Arc Mountains, Tanzania. Amphibia- Reptilia, 10: 435-443.

FuELpsA, J. & LOVETT, J. C., 1997. - Biodiversity and environmental stability. Biodiversity & Conservation,

6: 315-323.

GrirriTHs, C. J., 1993. - The geological evolution of East Africa. /n: J. LoverT & S. WassER, (ed.),

Biogeography and ecology of the rain forests of Eastern Africa, Cambridge, Cambridge University

Press: 9-21.

KLEMENS, M. W., 1998. - The male nuptial characteristics of Arthroleptides martiensseni Nieden, an

endemic torrent frog from Tanzania’s Eastern Arc mountains. Herp. J., 8: 35-40.

KiNGDoN, J., 1989. — Jsland Africa. Princeton, Princeton University Press: 287.

LOVERIDGE, A. 1935. - Scientific results of an expedition to rain forest regions in Eastern Africa. L. New

reptiles and amphibians from East Africa. Bull. Mus. comp. Zool., 79: 3-19.

Loverr, J. C. 1990., - Classification and status of the moist forests of Tanzania. Mitt. Inst. allgem. Bot.

(Hamburg), 23a: 287-300.

— 1993. - Climatic history and forest distribution in eastern Africa. Jn: J. LOVErT & S. WassER (ed.),

Biogeography and ecology of the rain forests of Eastern Africa. Cambridge, Cambridge University

Press: 23-29.

NaRiNs, P. M., LEWIS, E. R., PURGUE, A. P., Bishop, P. J., MINTER, L. R. & LAWsON, D. P., 2001. -

Functional consequences of a novel middle ear adaptation in the central African frog Petropedetes

parkeri (Ranidae). J exp. Biol., 204: 1223-1232

NtŒDEN, F., 1911. - Verzeichnis der bei Amani in Deutschostafrika vorkommenden Reptilien und

Amphibien. Sber. Ges. Naturf. Freunde Berlin, 1910: 441-452.

SAVAGE, J. M. & HEYER, W. R., 1997. - Digital webbing formulae for anurans: a refinement. Herp. Rev., 28:

131.

APPENDIX 1

LIST OF SPECIMENS EXAMINED

The following abbreviations are used:

AC. - Field numbers of À. Channing, Material is to be deposited in the American Museum of Natural

History.

AMNH. - American Museum of Natural History, New York.

CAS. - California Academy of Sciences, San Francisco.

ES. - Field numbers of E. Scott. Material will be deposited in the California Academy of Sciences.

KMH. - Field numbers of K. M. Howell, specimens in the collection of the Zoology & Marine Biology

department, University of Dar es Salaam.

MCZ. - Museum of Comparative Zoology, Harvard.

MTSN. - The Museo Tridentino di Scienze Naturali (Trento, Italy)

RdS. - Field numbers of R. de Sà. Specimens will be deposited in the National Museum, Washington,

UDSM. - The University of Dar es Salaam, collection of the Zoology and Marine Biology department.

Arihroleptides dutoiti

Five specimens from Mount Elgon, Kenya. - AMNH A.68670, A.68673, A.68675, À.68677-68678.

Source : MNHN, Paris

CHANNING, MOYER & HOWELL 27

Arihroleptides martiensseni

Altogether 19 frogs and two batches of tadpoles.

East Usambara Mountains, Tanzania. - Females: USDM 1107; CAS 168625, 168633, 168684; AC

2234; ES 705; ES 723. Males: CAS 168627, 168631. Juveniles: AC 1905, 2045.

Segoma Forest Reserve, East Usambara Mountains, Tanzania. - Male: KMH 17503. Juvenile:

KMH 17549.

Amani, East Usambara Mountains, Tanzania. - Females: MCZ A.12823. Males: MCZ A.12824.

Mt Lutind, East Usambara Mountains, Tanzania. - Female: MCZ A.12825.

Magrotto Mountain, East Usambara Mountains, Tanzani Males: MCZ A.25380-81. Juvenile:

MCZ A.25382.

Zigi river, East Usambara Mountains, Tanzania. - Tadpoles: CAS 168615, 168617.

Arthroletides yakusini

A total of 48 frogs and two batches of tadpoles.

Njokomoni River, Udzungwa Mountains National Park, Tanzania. - Males: AMNH A.151342

(holotype), A.151343 (paratype). Females: AMNH A.151341, A.151344 (paratypes).

Kihansi Gorge, Udzungwa Mountains, Tanzania. — Juvenile: UDSM 1038. Tadpoles: AC.

Udzungwa Mountains, Tanzania. - Males: UDSM 1116, 1138-39. Juveniles: AC 1930, UDSM 1038

(9 specimens).

Kihansi Gorge, Udzungwa Mountains, Tanzani

Kitolomero, Udzungwa Mountains, Tanzania. : MTSN unnumbered (20 specimens).

Kihanga, Udzungwa Mountains, Tanzania. — Females: MTSN unnumbered (2 specimens).

Tegetero, Uluguru Mountains, Tanzania. — Male: RdS 862. Juveniles: RdS 849, 866.

Morningside, Uluguru Mountains, Tanzania. - Tadpoles: CAS 159944.

Bagilo, Uluguru Mountains, Tanzania. - Males: AMNH A.37281, MCZ A.12817, A.12820.

Vituri, Uluguru Mountains, Tanzania. - Female: MCZ A.12822.

Corresponding editor: Alain DuRoïs.

Source : MNHN, Paris

Alytes, 2002, 20 (1-2)

A new species of Adenomera

(Anura, Leptodactulidae)

from the Araucaria forest

of Rio Grande do Sul (Brazil),

with comments on the systematic status

of southern populations of the genus

Axel KWET * & Ariadne ANGULO **

* Staatliches Museum für Naturkunde, Zoologie,

Rosenstein 1, 70191 Stutigart, Germany

<axel.kwet@uni-tuebingen.de>

Zoologisches Institut, Universität Tübingen,

Auf der Morgenstelle 28, 72076 Tübingen, G

** Departement of Zoology, Erindale College, University of Toronto,

Mississauga, ON, LSL 1C6, Canada

ariadne@z00.utoronto.ca>

many

Departamento. de Herpetologia, Museo de Historia Natural de San Marcos,

Apartado 140434, Lima 14, Peru

We describe a new species of Adenomera from Rio Grande do Sul,

southern Brazil. This new species inhabits the spiny understory of southern

Araucaria forests, and can be most easily distinguished from other Adeno-

mera by its small body size, unexpanded toe tips and distinctive advertise-

ment call. Calls are analyzed, described, and compared to advertisement

calls of other Adenomera of southern Brazil, and the systematic status of

these populations is discussed.

INTRODUCTION

Extensive morphological variation both within and among populations of species of the

leptodactylid genus Adenomera have traditionally rendered this a taxonomically difficult

group. The potential use of advertisement call data as a means of resolving this group’s

systematics had already been suggested by HeyEr (1984) and is being effectively used in

resolving species identity in member species distributed throughout the Amazon Basin

(ANGULO & ICOCHEA, in press; ANGULO et al., in press). Two species, Adenomera marmorata

Steindachner, 1867 and A. hokermanni (Heyer, 1973), have been reported to occur in sympatry

in southeastern Brazil (HevEr, 1973). Although these two nominal species have long been

Source : MNHN, Paris

KWET & ANGULO 29

suspected to be composites of two or more species (HEYER, 1977, 1984), it has not been until

recently that enough acoustic data from different localities were collected to determine species

identities within the group.

Kwer (1998) reported the southernmost record for the genus in the Brazilian state of Rio

Grande do Sul. This population, which was termed Adenomera cf. marmorata, has distinct

advertisement calls compared with those from populations in the states of Säo Paulo, Rio de

Janeiro and Santa Catarina. Comparison of specimens from Rio Grande do Sul with

specimens from other localities in southeastern Brazil, including type material of the nominal

species and their synonyms, revealed that there are also morphological differences associated

to this different call. Based on this evidence, we conclude that the Rio Grande do Sul

population comprises a new species of Adenomera and proceed to describe it herein.

MATERIALS AND METHODS

Individuals of the new species were collected in Rio Grande do Sul, at Serra Geral

between 600 and 1000 m altitude, and later deposited in the Museu de Ciências e Tecnologia

da PUCRS (MCP, Porto Alegre, Brazil). Specimens examined for comparisons are deposited

in the Museu de Ciências e Tecnologia da PUCRS (MCP, Porto Alegre, Brazil), Naturhistoris-

ches Museum Wien (NHW, Wien, Austria), Staatliches Museum für Naturkunde Stuttgart

(SMNS, Stuttgart, Germany), National Museum of Natural History (USNM, Washington,

D.C., USA), Museum für Naturkunde Berlin (ZMB, Berlin, Germany), Zoologisches

Museum Hamburg (ZMH, Hamburg, Germany) and Zoologische Staatssammlung München

(ZSM, München, Germany). Our specimens were fixed in 6 % formalin and preserved in

70% ethyl alcohol. AÏl measurements were made with digital calipers. The following

measurements were made to the nearest 0.1 mm: snout-vent length (SVL); head length, defined

as the diagonal distance from the tip of the snout to the right angle of the jaw (HL); head width,

defined as the distance between the angles of the jaw (HW); horizontal eye diameter (ED);

horizontaltympanum diameter (TD); eye-nostril distance (END); interorbital distance (10D);

internarial distance (IND); thigh length (THL); tibia length (TL); foot length (FL).

Field work took place from 1995 to 1999 (in each year from about October to March), at

the Centro de Pesquisas e Conservaçäo da Natureza Pré-Mata (CPCN) (29°30'S, 50°10°W),

municipality of Säo Francisco de Paula, state of Rio Grande do Sul, Brazil. Acoustic signals

were recorded using a Sony WM-D6C tape recorder, a Sennheiser microphone system K6

with ME66 module, and metal tapes Sony Metal XR-90. Advertisement calls of four males of

the new species were recorded at CPCN Pré-Mata: (a) on 8 November 1995, 23.30 h, 19°C air

temperature; (b) on 20 December 1995, 14.00 h, 26°C air temperature; (c, d) on 1 November

1996, 3.00 h, 16°C air temperature. These calls are unvouchered. Acoustic analysis was

performed using a Macintosh-based digital signal analysis software, Signalyze 3.12 (KELLER,

1994), at a sampling rate of 44.1 kHz and 16 bit precision. Temporal and spectral si

figures were produced using a combination of Signalyze 3.12, DADISP, a PC-based s

analysis software, and Corel Draw. Measurements of six acoustic parameters were taken: call

length, call rise time (time from beginning of call to peak amplitude), dominant

frequency, other frequencies with perceptible energy and frequency modulation (measured as

Source : MNHN, Paris

30 ALYTES 20 (1-2)

the difference between final frequency and initial frequency). Temporal parameters were

measured in milliseconds (ms) and spectral parameters in Hertz (Hz). Dominant frequency

measurements were taken at the peak amplitude of each call.

RESULTS

Adenomera araucaria sp. nov.

(fig. 1-2)

Holotype.- MCP 2421, adult male, collected at the Centro de Pesquisas e Conservaçäo da

Natureza Pré-Mata (CPCN) (about 950 m a.s.l.), 29°30'S, 50°10°W, municipality of Säo

Francisco de Paula, Rio Grande do Sul, Brazil, on 20 December 1996, by Axel Kwet and

Marcos Di-Bernardo.

Paratypes. — Nine specimens collected at the type locality by Axel Kwet and Marcos

Di-Bernardo (MCP 1794, female, 19 December 1995; MCP 1849, subadult, 9 February 1996;

MCP 3208, male, 19 March 1997; MCP 3209, subadult, 23 November 1997; MCP 3463, male,

20 December 1996; MCP 3672-73, males, 24 November 1998; MCP 3676, male, 11 January

1999; MCP 3677, female, 4 January 1999); two specimens collected near Encruzilhada das

Antas, municipality of Bom Jesus, Rio Grande do Sul, by Axel Kwet and Marcos

Di-Bernardo (MCP 3345-46, males, 4 January 1998).

Diagnosis. — À small sized Adenomera (maximum SVL 18.8 mm in males, 19.9 mm in females;

tab. 1) with toe tips rounded or slightly swollen, not disked (stage B after HEYER, 1973).

Adenomera araucaria differs from all other known species in the genus by its advertisement

call. Morphologically, it is most similar to Adenomera marmorata, being distinguished from

this species by: (1) toe tips not flattened; (2) white tubercles on tarsus and on sole of foot less

developed; (3) shorter limbs; (4) snout more acuminate in dorsal and lateral view; and (5)

ventral surface of thigh smooth, whitish, only sparsely dotted with gray (partly granular and

dark mottled, often forming a net-like pattern in À. marmorata). Whereas the new species

differs from northern populations of 4. marmorata also by a smaller size (maximum SVL near

the type locality about 24 mm in males and 25 mm in females; HEYER, 1973), specimens from

southern populations of À. marmorata (which may be a distinct species) are equally sized

(maximum SVL of 4. marmorata at the type locality of Leptodactylus nanus Müller, 1922:

19.3 mm in males, 20 mm in females; tab. 1). Leptodactylus trivittatus Lutz, 1926, is considered

synonymous with 4. marmorata, having toe tips distinctly expanded.

Adenomera araucaria differs from Adenomera bokermanni (following the description of

Hever, 1973, but see discussion) by: (1) its smaller size (maximum SVL of 4. bokermanni: 25.1

mm in males, 27.6 mm in females); (2) absence of perceptible white tubercles on ti and (3)

distinct dorsal pattern, usually with longitudinal arranged dark marks and light dorsolateral

and mid-dorsal stripes (dorsum commonly uniform or with indistinct marks in 4. boker-

manni). The new species is distinguished from all other known species of the genus, i.e.,

Adenomera andreae (Müller, 1923), Adenomera diptyx (Boettger, 1885), Adenomera hylaedac-

tyla (Cope, 1868), Adenomera lutzi Heyer, 1975 and Adenomera martinezi (Bokermann, 1956)

by its smaller body size. Further, it differs from nominal 4. andreae and A. lutzi by non

expanded toe tips, from A. diptyx and A. hylaedactyla by less rugose skin texture and from 4.

Source : MNHN, Paris

KWET & ANGULO 31

Fig. 1. Adenomera araucaria sp. nov., holotype, male, MCP 2421. (a) Lateral and (b) dorsal views of

head; ventral views of (c) right hand and (d) right foot. Scale bar: Imm

Source : MNHN, Paris

32 ALYTES 20 (1-2)

Fig. 2. — Adenomera araucaria, type specimens in life showing intraspecific variation. (a) MCP 2421,

holotype, male; (b) MCP 1794, paratype,

paratype, male: (e) MCP 3676, paratype, male: (f

MCP 3463, paratype, male.

Source : MNHN, Paris

Table 1.- Morphometric characters for Adenomera araucaria from Serra Geral, Rio Grande do Sul, Adenomera cf. araucaria from Morro do Baü, Santa

Catarina, and Adenomera cf. marmorata from Corupé, Santa Catarina (type locality of Leptodactylus nanus). n, sample size; s, standard deviation.

Adenomera araucaria Adenomera cf. araucaria Adenomera cf. marmorata

Serra Geral, RS Morro do Baë, Ilhota, SC Coupé, SC

Males Females Male Females Males Females

(n=8) (n=3) @=1) (n=S) (a=S) (m=7)

Snout-vent length 171-188 | 184 | 0.59 |193199 | 196 | 031 | 179 [186200 | 192 | 0.52 [171193] 184 | 092 | 173200 | 18.8 | 090 Ël

Head length 596.5 | 62 | 020 | 57-69 | 62 | o61 | 57 | 58.68 | 64 | 044 59 | 026 60 | ou æ

Head width 5.5-6.7 6.0 037 5.9-6.0 6.0 0.06 5.6 5.6-6.5 6.0 041 54 0.28 6.1 0.28 Ë

Eye diameter 17419 | 18 | 007 | 2020 | 20 | o | 19 | 1921 | 20 | 008 19 | 005 19 | 010 ê

Tympanum diameter LI13 12 0.07 13-13 13 0 11 11-13 ie 0.08 10 0.08 [AI 0.17 5

Eye-nostril distance 14-17 16 0.09 14-17 1.6 0.15 16 15-19 17 0.18 14 0411 17 0.08

Interorbital distance 34-39 36 0.20 35 0.17 34 33-37 3.5 0.16 32 0.23 3.5 0.23

Internarial distance 20 |o14 19 | 006 | 20 | 1920 | 20 | 00s 20 | 013 20 | 013

Femur length 78 | 035 80 |o15 | 84 | 8289 | 85 | 026 75 | 050 87 |ost

FTibia length 79 | 027 84 | 040 | 87 | 8591 | 88 | 025 76 | 048 89 | 053

Foot length 94 0.33 10.0 0.15 94 9.6-10.5 10.1 0.37 88 0.47 9.8 035

Source : MNHN, Paris

34 ALYTES 20 (1-2)

martinezi by dorsal pattern not consisting of four symmetrically arranged rows of longitudi-

nal spots. Adenomera araucaria is currently known only from the southernmost extent of the

Atlantic Forest Domain in southeastern Brazil.

Description of holotype.- Body small, robust, with short limbs (tab. 1). Head as long as broad;

dorsal outline of snout subelliptical, slightly acuminate (fig. la); snout profile subacuminate

(fig. 1b). Nostrils directed dorsolaterally, closer to tip of snout than to eye; internarial

distance about one third of head width. Tympanum distinct, its diameter two thirds of eye

diameter; supratympanic fold poorly developed, highlighted with black. Canthus rostralis

indistinct, rounded. No cranial crests. Angle of jaw with white oval gland. Vocal sac single,

internal. Paired, elongate vocal slits in males. Vomerine teeth in short transverse series,

posterior to choanae and separated from each other by about the length of one tooth row.

Arms and fingers relatively short. Finger lengths II > I = II > IV; finger tips rounded, not

expanded:; fingers without webbing or fringes (fig. 1c). Two large, ovoid metacarpal tubercles:

size of outer metacarpal tubercle about two times inner metacarpal tubercle; prominent,

rounded subarticular tubercles on fingers. Nuptial asperities absent. Hindlegs short, tibia a

little longer than femur. Toe lengths IV > II > V > I > I: toe tips slightly swollen but not

noticeably expanded nor flattened; toes without webbing or fringes (fig. Id). Distinct, ovoid

metatarsal tubercles and rounded subarticular tubercles; inner metatarsal tubercle slightly

larger than outer metatarsal tubercle. Distinct inner tarsal fold. Sole of foot and lower surface

of tarsus with small, but relatively distinct tubercles. Upper shank surface smooth, without

perceptible white tubercles. Dorsal texture smooth, except some tubercles around vent (on

posterior region of thighs and on sacral region) and, dorsolaterally, two longitudinal glandu-

lar folds. A distinct lateral fold partly separated into small glandular segments extending from

eye, over tympanum and shoulder, to inguinal region. Above this fold a second, less distinct

dorsal fold from shoulder to sacral region. Ventral surface smooth.

Color in life. - Dorsal coloration orange-brown, with a symmetrical pattern of dark marks

(fig. 2a). A black, pentagonal interorbital spot followed by a larger rectangular blotch between

shoulders (fig. la) and another spot on anterior part of dorsum. A black stripe on each dorsal

glandular fold joined on middorsum by a black bar, and a light stripe on each lateral fold. On

posterior half of body, a light mid-dorsal stripe. A black line from nostril to anterior margin

of eye; another line from posterior margin of eye, over tympanum and a white gland on angle

of jaw, to insertion of arm. Black, irregular cross-bars on hindlimbs and partly on arms. Belly

white, immaculate; skin on throat and ventral surface of thigh very sparsely dotted with small

melanophores.

Color in preservative. — In 70 % alcohol, dorsum brownish with the dorsal pattern of dark

marks described above. Venter white, immaculate.

Measurements of holotype (in mm).-SVL 18.1; HL 5.9; HW 5.9; ED 1.8; TD 1.2; END 1.6;

IOD 3.5; IND 1.9; THL 7.3; TL 7.6; FL 9.3.

Variation. - Females slightly larger than males (tab. 1). Dorsal outline of snout subelliptical or

nearly acuminate in males but more rounded in females. In all specimens, inner metacarpal

tubercle smaller than outer metacarpal tubercle, in size varying between one half and two

thirds. Dorsal coloration very variable, consisting of various shades of light or dark brown,

orange-brown, tan or gray, with a usually inconspicuous pattern of longitudinally arranged,

irregular, dark marks (fig. 2, see color photos in KwET & Di-BERNARDO, 1999). Variable,

Source : MNHN, Paris

KWET & ANGULO 35

black, triangular or hourglass-shaped interorbital spot from between upper eyelids to region

between shoulders. Light middorsal stripe usually extending from above vent to middle of

body not reaching head; this stripe very weak in one of the 12 type specimens (MCP 3676).

Dorsolaterally, most specimens with two black longitudinal lines and below with two finer,

light stripes, but in two specimens (MCP 3208, 3346), these stripes expanded into broad, white

lateral lines. Two specimens (MCP 3673, 3677) with dark dorsal coloration and pattern hardly

visible. Ventral surface of body usually white, finely dotted with gray on throat and posterior

part of thighs, but one specimen (MCP 3209) very dark ventrally, with a lot of melanophores

on lower thighs, throat and belly.

Advertisement call. — Acoustic parameter measurements of four specimens are listed in tab. 2;

fig. 3 depicts oscillogram, spectrum, and sonogram images of the call. The call length of the

new species ranges from 85.5 to 139.5 ms in duration and call rate is relatively slow (26.2 to

44.8 calls/min). Call onset is gradual and call rise time varies from 35.1 to 81.0 ms, constituting

approximately 26.8 to 66.6 % of the total call duration. The call does not possess perceptible

pulses, although it does show some amplitude modulation that can take the form of 5-11

severe amplitude modulations on the amplitude envelope. The call is a frequency-modulated

signal, with an upward frequency sweep where the end of each call has a higher frequency

than the respective beginning of the call. This frequency sweep is audible to the human ear

and varies from 775.3 to 1808.8 Hz. The fundamental frequency or first harmonic lies between

1722 and 3359 Hz and the main carrier frequency oscillates between 4625 and 5403 Hz,

comprising the second harmonic band. Other frequency components which have some energy

lie approximately at 5943-8613 Hz and 8354-10938 Hz. À much higher harmonic band also

presents perceptible energy, greater than all other aforementioned frequencies, except for the

carrier, between 13716 and 15231 Hz. However, the energy peaks of any of these frequencies

are substantially lower than the main carrier, making the call almost a pure tone (see spectrum

on fig. 3: other frequencies are not depicted as their energy levels fall below the cutoff point of

30 dB). The number of frequencies detected at any one time in calls varies from three to six,

although this may vary with recording conditions.

Natural history. — The new species inhabits subtropical rainforest of northeastern Rio Grande

do Sul and southern Santa Catarina, from about 300 to 1100 m altitude. It was very abundant

in secondary forests and Araucaria stands on the eastern Planalto of Rio Grande do Sul.

Most specimens were found near trunks of the Paranä pine, Araucaria angustifolia, where

they may find protection against potential predators by hiding among the spiny leaves of this

conifer. Adenomera araucaria is a predominantly diurnal species. During the breeding time

from October to late January, males usually called from early afternoon to midnight. No

specimens were heard at late night or at dawn. Calling activity increased after showers. Males

were calling on the ground, mostly hidden between roots, stones and fallen branches. Neither

eggs nor tadpoles were found but terrestrial reproduction in foam nests with non-feeding

larvae is assumed (mode 22 after DUELLMAN & TRUEB, 1985), as described for most other

members of the group (e.g., HEYER et al., 1990), because Adenomera araucaria was never

observed near streams or standing water. At Pré-Mata, the new species was found living in

sympatry with Eleutherodactylus cf. guentheri.

Distribution, — Adenomera araucaria occurs in the southern region of the Serra Geral,

southern Brazil. At present, it is known from several municipalities in northeastern Rio

Source : MNHN, Paris

36 ALYTES 20 (1-2)

Grande do Sul, i.e., Bom Jesus, Cambarä do Sul, Canela, Gramado, Säo Francisco de Paula

and Säo José dos Ausentes. The municipality of Säo Francisco de Paula marks the southern-

most distribution limit of new species, the genus and the Atlantic Rainforest Domain. Calling

specimens were also heard in southern Santa Catarina, municipality of Timbé do Sul (on 4

January 1998). It is not known where the northern and western distribution limits of 4.

araucaria lie, but the species may be restricted to a small area of the southern Serra Geral.

Populations from northern Santa Catarina are slightly different and probably belong to

another species (see discussion). Specimens from Misiones, Argentina, have different calls

(Diego Baldo, personal communication) and presumably represent the recently revalidated

Adenomera diptyx (Boettger, 1885) (DE LA Riva, 1996).

Etymology. — The new species is named after the Paranä pine, Araucaria angustifolia, in

allusion to the preferred microhabitat at CPCN Pr6-Mata and the difficulty of finding

specimens in the spiny understory of the Araucaria forest. The name is used as an invariable

noun in apposition.

DISCUSSION

Differences in morphological features have traditionally been considered good evidence

for allocation of specific status. With the advent of technology, the acoustic realm has

undergone a boost, as it is now possible to visualize and analyze signals digitally. Advertise-

ment calls have become as important as morphology in species determination in anurans, at

times being the major discriminator between one or another population (e.g., HEYER et al.,

1996). Because advertisement calls are important in species recognition, work as premating

isolating barriers among sympatric species (DUELLMAN & PYLES, 1983) and tend to be rather

stereotyped, workers use them for species identification in the field.

HEYER (1974) studied the relationships of the marmoratus species group within the family

Leptodactylidae and revalidated the genus Adenomera. HEYER (1977) also suggested that

Adenomera marmorata may be a composite species, although the evidence was not as clear as

for Adenomera bokermanni. He found a broad overlap in morphological characters between

different populations from southeastern Brazil and stated that advertisement call data are

needed for resolving the systematics of this group (HEYER, 1984). Our comparison of calls of

Adenomera from Rio Grande do Sul (tab. 2, fig. 3) with those from other localities in

southeastern Brazil demonstrate noticeable differences. BARR10 (1965) described the call of 4.

marmorata from Paranapiacaba, state of Säo Paulo. At a temperature of 20°C, he described

a call length of 100 ms, issued at a call repetition rate of 75 calls/min, a fundamental frequency

Of 2200-3200 Hz and a dominant frequency of 5200-6000 Hz. STRAUGHAN & HEYER (1976)

described the call of 4. marmorata from Tijuca, state of Rio de Janeiro (figured in HEYER,

1973). At 22°C, they reported call length to be of 100 ms and a call repetition rate of 94

calls/min, while the dominant frequency oscillated between 4500-5600 Hz, and an apparent

broad fundamental below 1000 Hz, amplitude modulation apparent throughout call. HEYER

et al. (1990) also reported the call of À. marmorata from Boracéia, Säo Paulo. At a tempera-

ture of 18°C, call lengths were found to vary between 40 and 70 ms in duration, issued at a rate

of 0.8 to 1.4 calls/s (approximately 48-84 calls/min), with a main carrier frequency (which is

also the fundamental frequency) of 4500 to 5400 Hz. Call onset was abrupt and intensity was

Source : MNHN, Paris

Table 2. — Acoustic parameters for four males (a-d) of Adenomera araucaria. Numbers of first line are means + standard deviations, numbers in

brackets are ranges.

Frequency modulation (Hz)

(775.3-1292.0)

(1033.6-1808.8)

(861.3-947.5)

Recording (a) 8 Nov. 1995 (b) 20 Dec. 1995 €) 1 Nov. 1996 (@) 1 Nov. 1996

Number of calls 4 20 11 8

Temperature (°C) 19 26 16 16

90.0 + 4.3 127.6 + 3.1 129.3 + 3.4 1343 42.7

Call length :

ILlength (us) (85.5-95.7) (123.5-137.3) (125.6-136.6) (130.6-139.5)

Call rate (calls/min) 346 448 262 274

Call rise time (ms) 56.3 +6.0 57.5 + 16.2 46.9+ 11.1 39.1+4.7

(47.3-60.2) (41.2-81.0) (5.1-64.8) (35.6-50.4)

: 5318+68 5000 + 94 4672 + 43 4650 + 37

D: t fr H:

prinentequeny (He) (5263-5403) (885-5144) (4625-4745) (4625-4705)

à x _ 14847 + 247 13875 13819 + 86

Other f th bl H

er frequencies with perceptible energy (Hz) Ce an Less

1076.7 + 258.4 1438.4 + 218.4 822.2 + 20.0 818.3 + 46.0

(775.2-861.3)

OINONY P LIN

Source : MNHN, Paris

38 ALYTES 20 (1-2)

Het

0.0 2.0 40 60 80 100 120 140 Kk

1° x C]

400ms

Fig. 3. — Oscillogram of six calls, waveform at higher resolution, power spectrum and audiospectrogram

of the advertisement call of Adenomera araucaria from Pré-Mata, Rio Grande do Sul: recorded on

20 December 1995; 14.00 h; air temperature 26°C: no voucher specimen.

Source : MNHN, Paris

KWET & ANGULO 39

maintained for most of the beginning of the call, declining towards end. There was upward

frequency modulation within the call, and no harmonics were reported.

In addition to these reported calls, W. R. Heyer kindly made available to us recordings of

Adenomera from an area geographically close to Rio Grande do Sul, Pirabeiraba, in Santa

Catarina, and Serra da Bocaina, Säo Paulo (see tab. 3). We have identified two distinct

advertisement calls from Pirabeiraba and have analyzed recordings from two calling males (7

= 2) for each of the two call types (there is one voucher specimen for call type II and two for

call type I but calls from one of the Pirabeiraba I call type vouchers were not used in analysis

due to the very poor signal to noise ratio). For the population of Serra da Bocaina, we have

analyzed recordings from three calling males (n = 3). For comparative purposes, calls from

Serra da Bocaina have been tentatively assigned to Adenomera bokermanni because: (1) the

frogs were heard calling and were collected in an open formation environment, which is

understood to be the preferred habitat of 4. bokermanni (HEYER, 1984); and (2) the single

voucher has slender, unexpanded toe tips (characteristic of 4. bokermanni; HEYER, 1984) and

besides a discontinuous mid-dorsal dark brown stripe running from shoulder to groin, the

dorsal pattern is mostly uniform. However, nominal 4. bokermanni has long been suspected to

be a composite of more than one species (HEYER, 1977, 1984), and given that its taxonomy still

remains unresolved we are conservative about allocating this population to 4. bokermanni in

a definitive way. On the other hand, the single vouchers for the two distinct call types from

Pirabeiraba differ from each other as one has expanded toe tips (call type IT) and a nearly

rounded to rounded snout, whereas the other has slender, unexpanded toe tips (call type I)

and a subelliptical to pointed snout, so we believe that there are at least three different taxa

considering both localities. Unfortunately, because the number of call vouchers is limited, it is

difficult to properly allocate identities to these populations, but it is important to compare the

new species’ call to those in geographic proximity and to note that there are more advertise-

ment calls than available names.

With regards to reported calls, there is overlap in values of main carrier frequency for all

three reported calls and the new species. There are, however, clear differences with each

reported call. The new species has a much lower call rate than any of those reported in the

literature, presenting no overlap with any of them, save the closeness of the Boracéia calls

calling rate. There is overlap in call length with calls from Paranapiacaba and Tijuca, but calls

from Boracéia are shorter than those of the new species. The Boracéia calls do not have severe

amplitude modulations, which calls of the new species possess. The call from Rio de Janeiro

has apparent intensity (amplitude) modulation (STRAUGHAN & HEYER, 1976), but it is difficult

to tell in the case of the Paranapiacaba call as spectrogram information does not allow

observation of amplitude patterns in detail. Additionally, although the number of harmonies

detected will be a function of the closeness of the recording equipment to the animal and of

the recording equipment per se, the new species consistently shows higher harmonics, extend-

ing to about 15 kHz.

In contrast with both call types from Pirabeiraba, calls of the new species are consistently

longer. Call rate is also notably lower in the new species than that of Pirabeiraba call type I,

although there is some overlap with Pirabeiraba call type IT. Call rise time is generally longer

in the new species than in the Pirabeiraba calls, although this parameter is subject to

considerable variability. Main carrier frequency differs by about 1600-2000 Hz with Pirabei-

Source : MNHN, Paris

Table 3. - Acoustic parameters for two distinct call types of Adenomera from Pirabeiraba, Santa Catarina (a-d; Adenomera cf. marmorata, call type 1

and I) and for Adenomera from Serra da Bocaina, Säo Paulo (e-g; Adenomera cf. bokermanni). Numbers of first line are means + standard

deviations, numbers in brackets are ranges. Question marks (?) indicate that frequency values observed may be a product of masking

background noise rather than the acoustic signal being measured. Adenomera cf. bokermanni shows negative values or none at all for frequency

modulation (Hz) as this modulation may be inverse (falling frequency with time rather than rising) or nonexistent.

(ua

(T-D) 07 SALATV

Adenomera, Adenomera, Adenomera, Adenomera, re DT or

Identification calltypel, call type L, call type H, call type I, cts Bones || Stseu Bou || Suede tre

Pirabeiraba Pirabeiraba Pirabeiraba Pirabeiraba

Number of calls 10 10 10 3 10 10 10

Temperature (°C) 245 245 215 = - 19-20 19-20

Cal length (ms) 716437 882466 759435 7594122 584423 526417 484442

(67.7-79.1) (80.1-98.0) (70.1-80.8) (61.9-83.9) (543-615) (512-55.9) (45.4-59.7)

Call rate (calls/min) 932 n31 371 317 308.7 238.6 288.9

Call rise time (ms) 29436 732132 2814254 119411 140422 163414 118429

(04-92) (0.9-43.9) (6.6-68.2) (G0.6-12.7) (8:5-16.1) (3:5-18.6) (.6-15.9)

Dominant frequency (Hz) 30384 17 3034413 5343477 52854 30 2284413 221340 2327419

{3030-3070) (030-3070) (5212-5443) (251-5311) (2248-2288) (2213-2213) (2288-2367)

- - 30114 1897 7963 4 185? 43964 155 4296 + 691 -

Other frequencies with - - (4177-4694) (808-4785)

perceptible energy (Hz) 10779 + 189 10529 + 61 63984 87

(10486-10965) | (10462-10582) (6273-6531)

Frequency modulation (Hz) | 32544 1347 62024 792 - 601.640 (859-1719) (861-2004) (0-257.8)

(86.1-516.8) (5168-7752) (601.6-601.6)

Source : MNHN, Paris

KWET & ANGULO 41

raba call type I and there is some overlap with call type IT. Calls of the new species are audibly

frequency-modulated, and although there is almost no overlap with Pirabeiraba call type I in

frequency modulation, this is not obvious in the case of Pirabeiraba call type IL. To the ear,

Pirabeiraba call type II seems to be less frequency modulated than the new species’ call,

although measuring this modulation was not possible due to the excessive background noise

and poor signal to noise ratio. In addition, the one voucher for Pirabeiraba call type IL is rather

small (SVL 17.1 mm), has rounded, expanded toe tips, and a nearly rounded to rounded

snout, which could fit the new species. With regards to Adenomera cf. bokermanni calls from

Serra da Bocaina, these are much shorter in length than those of the new species, and call rate

is several orders of magnitude higher in A. cf. bokermanni than what it is in the new species.

Call rise time is also much longer in the new species’ call than in A. cf. bokermanni. The main

carrier frequency differs by about 2500-3000 Hz between these taxa, and frequency modula-

tion in À. cf. bokermanni is either nonexistent, negative or minimal, whereas the new species

possesses considerable frequency modulation. Overall, and with the exception of Pirabeiraba

call type IL, the differences in call rate, call length, main carrier, amplitude modulation and

higher harmonies support that this is a distinct call distinguished from any other reported in

the literature for the southeastern Brazil region.

Although the morphological characteristics of Adenomera araucaria revealed intraspe-

cific variation, especially in dorsal coloration, which could make discrimination from other

species of the genus difficult, the combination of several features should in most cases allow

identification, i.e., small body with short arms and hindlimbs, non-expanded toe tips, whitish

ventral surface of thigh without granules, inconspicuous dorsal pattern of longitudinally

arranged, dark marks and development of tubercles on tarsus and sole of foot. The new

species is most similar to Adenomera marmorata, but our examination of the holotype (NHM

16453, fig. 4a), presumably from Rio de Janeiro (BOKERMANN, 1966), revealed notable

differences, e.g., larger body proportions (SVL 21.6 mm, HL 7.7 mm, HW 7.4 mm, THL 9.2

mm, TL 9.6 mm) and intensively granulated lower parts of thigh.

On the other hand, only small morphological differences were found comparing the new

species with small-sized Adenomera from populations in northern Santa Catarina that, at

present, are allocated to À. marmorata. Specimens from Corupä and Pirabeiraba, both

localities near the border of Paranä about 50 km from each other, differ from 4. araucaria

only in subtle characteristics. Besides the toe tips being a little more expanded and the ventral

surface of thighs more granular and dark mottled, the dorsal pattern is more accentuated.

Our comparison with the type material of Leptodactylus nanus (ZSM 661/1920/1-3, fig. 4b)

described from Corupä (MÜüLLER, 1922) confirmed that this is a species different from

Adenomera araucaria. However, material collected at Morro do Baü, Ihota, about 50-100 km

st from Corupä, differ morphologically very slightly and only gradually from 4.

araucaria and, therefore, could be conspecifi with this species. The most noticeable difference

is the dorsal pattern, which consists of conspicuous blotches producing a symmetrical, dark

brown marbling in five of eight s s examined. Morro do Baü lies in the crystalline

tal range of the Serra do Mar in northeastern Santa Catarina, about 200-300 km distance

from the Serra Geral in Rio Grande do Sul, where the new species occurs. Both mountain

ranges are geologically different and separated by the southeastern Catarinean depression.

Pending further studies, including analysis of advertisement calls from Morro do Bat, this

population is identified as Adenomera €. araucaria.

Source : MNHN, Paris

42 ALYTES 20 (1-2)

Fig. 4. — (a) Adenomera marmorata, holotype, NHM 16453; (b) Leptodactylus nanus, lectotype,

ZSM 661.1920.3.

Based on combined evidence from bioacoustical and morphological data, the differences

between the populations of Adenomera in Rio Grande do Sul and other populations in

southeastern Brazil (with the exception of possible conspecific specimens from Morro do Baü

and call type II from Pirabeiraba) justify the allocation of specific status to the southernmost

contingent of the genus in Brazil.

ACKNOWLEDGEMENTS

We thank Marcos Di-Bernardo, Wolf Engels and Andreas Schlüter for their assistance and for

providing the opportunity for the ficldwork of AK. For critical comments on the manuscript we

acknowledge W. Ronald Heyer and Marcos Di-Bernardo. We are also grateful to Tatiana Miranda who

kindly made the drawings and to Jochen Ketterl who collected two specimens and provided one photo.

For access to material under their care we thank Marcos Di-Bernardo (MCP), Franz Tiedemann

(NMW), Andreas Schlüter (SMNS), W. Ronald Heyer (USNM), Rainer Günther (ZMB), Jakob Hal-

lermann (ZMH) and Frank Glaw (ZSM). We also thank Diego Baldo and Paulo C. A. Garcia for

additional information. Field work of AK was supported by grants of the LGFG, DAAD and SHIFT

(Germany). Financial support for AA was provided by operating NSERC grant #4946 to G. K. Morris.

LITERATURE CITED

ANGULO, À. COCROFT, R. B. & REICHLE, $., in press. - Species identity in the genus Adenomera (Anura:

Leptodactylidae) in southeastern Peru. Herperologica.

ANGULO, À. & ICOCHEA, J., in press. — Adenomera cf. andreae (NON). Vocalization. Herp. Rev.

BARRIO, A.. 1965. — Afinidades del canto nupcial de las especies cavicolas del género Leprodactylus

(Anura-Leptodactylidae). Physis, 28 (70): 401-410

BOKERMANN, W. C. A., 1966. - Lista anorada das localidades tipo de anfibios brasileiros. Säo Paulo, Serv

Docum., RUSP: 1-183.

DE LA Riva, LL, 1996. - The specific name of Adenomera (Anura: Leptodactylidae) in the Paraguay river

basin. J Herp., 30 (4): 556-558

Source : MNHN, Paris

KWET & ANGULO 43

DuëLLMAN, W, E. & PYLES, R. A., 1983. — Acoustic resource partitioning in acoustic communities.

Copeia, 1983 (3): 639-649.

DuELLMAN, WE. & TRUE, L., 1985. - Biology of amphibians. New York, MeGraw-Hill, 1986”: i-xix +

1-670.

Hever, W. R., 1973. - Systematics of the marmoratus group of the frog genus Lepodactylus (Amphibia,

Leptodactylidae). Contr. Sci. nat. Hist. Mus. Los Angeles County, 251: 1-50.

= 1974. — Relationships of the marmoratus species group (Amphibia, Leptodactylidae) within the

subfamily Leptodactylinae. Contr. Sci. nat, Hist. Mus. Los Angeles County, 253: 1-46.

= 1977. — À discriminant function analysis of the frogs of the genus Adenomera (Amphibia: Lepto-

dactylidae). Proc. biol. Soc. Washington, 89 (51): 581-592.

ee 1984. — The systematic status of Adenomera griseigularis Henle, with comments on systematic

problems in the genus Adenomera (Amphibia: Leptodactylidac). Amphibia-Reptilia, 5: 97-100.

Hever, W., R., Garcia-Lorez, J. M. & CaRDOso, A. J., 1996. — Advertisement call variation in the

Leptodactylus mystaceus species complex (Amphibia: Leptodactylidae) with a description of a

new sibling species. Amphibia-Reptilia, 17: 7-31.

Hever, W. R., RAND, A. $,, Cruz, C. A. G., PrIXOTO, O. L. & NELSON, C. E., 1990. — Frogs of Boracéia.

Arg. Zool., 31 (4): 230-410.

KELLER, E., 1994. — Signalyze!” version 3.12. Infosignal Inc., Lausanne, Switzerland.

KweT, A., 1998. — Adenomera cf. marmorata. Geographic Distribution. Herp. Rer., 29 (1): 48.

Kwer, A. & DI-BERNARDO, M., 1999. — Prô-Mata — Anfibios. Amphibien. Amphibians. Porto Alegre,

Brazil, Edipucrs: 1-107.

MüLLer, L., 1922. - Über eine Sammlung Froschlurche von Sta. Catharina nebst Beschreibung zweier

neuer Arten. Bl. Aquar. Terrarkde., 33: 167-171.

STRAUGHAN, L. R. & HEVER, W.R., 1976. - À functional analysis of the mating calls of the neotropical

frog genera of the Leptodactylus complex (Amphibia, Leptodactylidac). Papeis Avulsos Zool., 29

(23): 221-245.

APPENDKX |

ADDITIONAL SPECIMENS EXAMINED

Adenomera andreae (Müller, 1923). - BRAZIL: AMAZONAS, ltacoatiara: SMNS 8718.1-7; Paré,

Peixeboi: lectotype ZSM 145.1911.4; paralectotypes ZSM 145.1911.1-3. PERU: Rio Yuyapichis, Pan-

guana: SMNS 7131.

Adenomera araucaria sp. nov. - BRAZIL: Rio GRANDE Do SuL, Säo Francisco de Paula, CPCN

Prô-Mata: SMNS 9023.

Adenomera cf. araucaria. - BRAZIL: SANTA CATARINA, Ilhota, Moro do Baü: MCP 1345-52.

Adenomera bokermanni (Heyer, 1973). - BRAZIL: RIO DE JANEIRO, Niteroi: ZSM 34.1947. BRA-

ZIL: Bamia, lhéus, Centro de Pesquisas do Cacau: USNM 336245-48.

Adenomera diptyx (Boettger, 1885). - PARAGUAY: paralectotype ZMB 10595.

Adenomera hylaedactyla (Cope, 1868). - BOLIVIA: BEN: SMNS 9087. ECUADOR: MORON4-

SanrtaGo: SMNS 7751; Napo: SMNS 7762. PERU: Rio Yuyapichis, Panguana: SMNS 6384, 7132, 8853.

SURINAM: Caboeri creek: SMNS 8222.1-3.

Adenomera marmorata Steindachner, 1867. - BRAZIL: R10 DE JANEIRO: holotype NMW 16453; SA0

PauLo, Salesépolis, Boracéia: USNM 209116-20; Säo Sebastiäo island: ZSM 19.1952.1-3.

Adenomera cf. marmorata 1 (Leptodactylus nanus Müller, 1922). - BRAZIL: SANTA CATARINA,

Pirabeiraba: USNM 243737-39, 243741-42; Rio Novo, Colonia Hansa: ZMH A.01737-44, A.01746-50,

lectotype ZSM 661.1920.3, paralectotypes ZSM 661.1920.1-2.

Adenomera cf. marmorata 1. — BRAZIL: SaNTA CaTaRINA, Florianépolis island: MCP 1340.

Corresponding editor: W. Ronald HEvER

Source : MNHN, Paris

Alytes, 2002, 20 (1-2): 44-54.

Régimes alimentaires

de deux espèces de Bufonidae

(Bufo bufo spinosus et Bufo mauritanicus)

au lac Aguelmam Azegza (Maroc)

L. CHiLLASsE*, M. DAKKI** & M. THÉVENOT***

* Faculté des Sciences, Département de Biologie, B.P. 4010, Meknès, Maroc

** Institut Scientifique, Département de Zoologie, Ecologie Animale, B.P.703, Rabat, Maroc

**# École Pratique des Hautes Etudes, Montpellier, France

This study deals with the diets of two toad species (Bufo bufo spinosus

and Bufo mauritanicus) through examination of the stomach contents of

specimens collected in the area of the Aguelmam Azegza lake in the

Moroccan Middle Atlas. The expression of results in terms of presence

frequency and relative abundance suggests a similarity of the two species

diets, which were both high in Coleoptera, Hymenoptera Formicidae and

Dermaptera. Measures of the amplitudes and overlaps of trophic niches as

well as the prey sizes exclude the existence of any kind of food competition

between the two species. The diversity of the two Bufonidae diets increases

during low prey availability, and decreases with prey abundance. The main

preys are not significantly different between the two sexes of the same

species. À comparison of several Bufonidae species around the world leads

to the conclusion that their diets are primarily composed of Formicidae and

Coleoptera.

INTRODUCTION

La connaissance de l’alimentation des Anoures dans leur milieu naturel

indispensable à la compréhension de leur biologie et de leur écologie; elle peut contribuer à

expliquer comment s'effectue le partage des ressources du milieu entre les espèces, à quantifier

l'importance des phénomènes de compétition et à déterminer la place des Amphibiens dans

chant que ces animaux sont souvent en populations

st une étape

les réseaux trophiques de la biocénose, s

denses.

Par l'analyse quantitative des contenus stomacaux de 43 Bufo bufo spinosus et 48 Bufo

es sites marocains où les deux espèces cohabitent, à savoir le lac

: (1) d'étudier, pour la première fois, la composition

mauritanicus, dans l’un des ra

Aguelmam Azegza, nous nous proposor

quantitative des régimes alimentaires de ces deux espèces de Bufonidae, demeurée méconnue

en dehors des données qualitatives fournies par PASTEUR et BONS (1959); (2) de comparer

Source : MNHN, Paris

, DAKKI & THÉVENOT 45

Vers Arhbal

Si Cherif

juelmam

egza

PLATEAU

D'AGDIR

x Lieux de coptures

it km

Fig. 1. Carte de situation du lac Aguelmam Azegza dans le Moyen Atlas central (Maroc).

globalement les régimes alimentaires de ces deux espèces, par le biais de l'indice H' de

Shannon en tant que mesure l'amplitude de la niche trophique (BARBAULT, 1974) et de l'indice

R de recouvrement des niches trophiques (PIANKA, 1973); (3) d'analyser le spectre de tailles et

la composition spécifique des proies consommées pour vérifier la présence ou l'absence d’une

compétition alimentaire entre ces deux espèces. Soulevant le problème de la place des

Amphibiens dans la chaîne trophique, la présente étude s'inscrit dans le cadre d’un travail plus

général consacré à l'étude de la place des Amphibiens dans les réseaux trophiques des

écosystèmes lacustres du Moyen Atlas.

UDE ET MÉTHODES

TERRAIN D

Le Moyen-Atlas central, massif bien arrosé aux terrains calcaires et dolomitiques

parsemés de dolines karstiques, offre une quinzaine de lacs naturels permanents (fig. 1). Le lac

Aguelmam Azegza, situé à une altitude de 1470 m avec une latitude de 32°58°50"-32°58"15"N

et une longitude de 05°26°15"-05°2730"W, occupe une profonde dépression entourée de

reliefs calcaires couverts par une belle forêt de chêne vert et de cèdre. Sa superficie est

d'environ 50 ha et sa profondeur maximale est de 26 m. Le bioclimat de la région est du type

sub-humide à humide, Les précipitations moyennes sont de 1150 mm/an, en grande partie

Source : MNHN, Paris

46 ALYTES 20 (1-2)

sous forme de neige qui peut parfois persister sur les hauts versants jusqu'au mois de mars. La

température mensuelle moyenne varie entre -2°C et 31°C. Durant les mois de décembre à

février, elle n’excède pas les 9°C, alors qu’en automne elle se situe entre 2 et 22°C. Le lac

Aguelmam Azegza est fréquenté par la plupart des Anoures de la région pendant leurs

périodes de reproduction, les espèces les plus abondantes étant Rana saharica, Hyla meridio-

nalis, Bufo bufo spinosus et Bufo mauritanicus. La présence de Discoglossus pictus est égale-

ment notée. L'activité des deux Bufonidés commence après une longue période d’hibernation

entre novembre et février, et s'étend sur la période mars-octobre.

L'analyse porte sur 91 Crapauds adultes (43 Bufo bufo spinosus et 48 Bufo mauritanicus)

récoltés de nuit entre 20 h et 1 h, de février 1988 jusqu’en mars 1990, avec des échantillonnages

mensuels. La plupart des spécimens ont été récoltés dans un rayon de 6 km autour du lac. Ils

appartiennent au même peuplement, tous les individus des deux espèces fréquentant le lac

pendant leur période de reproduction. Aussitôt prélevés, tous les Crapauds ont été fixés, cavité

viscérale ouverte, dans l'alcool à 70° mélangé au formol à 4 %, afin d'arrêter rapidement la

digestion post-mortem (GRANVAL, 1987). Les contenus stomacaux ont été extraits dans une

solution d’alcool, puis examinés sous une loupe binoculaire équipée d’un micromètre permet-

tant la mesure de la taille des proies. Le statut taxinomique des proies a été déterminé jusqu’à

la famille. La détermination du genre, voire de l'espèce, dépendait du stade de digestion des

proies. Une identification préliminaire a été faite grâce aux différentes clés qui existent à

l’Institut Scientifique de Rabat; elle a souvent été suivie par une vérification à l’aide des

collections de ce même institut.

Les résultats ont été exprimés de différentes façons complémentaires, afin de mieux

assurer leur interprétation:

(1) L’abondance relative des catégories de proies, calculée à l’aide de la formule Pi =

(4iln) X 100, où Ai est le nombre d'individus de la catégorie de proies considérée et n est le

nombre total d'animaux dénombrés dans le tube digestif. Cette estimation attribue la même

importance à des proies de valeur énergétique et de taille plus ou moins inégales (LESCURE,

1973).

(2) Le degré de présence, défini par la formule Ci = (Si/S) x 100, où Si est le nombre

d’estomacs contenant la catégorie de proie i et S est le nombre total d’estomacs examinés. Ce

paramètre constitue, du point de vue éthologique, une mesure de la préférence du Batracien

étudié pour un type de proie { (LESCURE, 1971).

(3) L’amplitude de la niche trophique, mesurée par l'indice de Shannon (BARBAULT,

1974) H°= - Pi log, Pi, où Pi est l'abondance relative de la catégorie de proie 5.

(4) Le coefficient de vacuité E)xX100 où Er est le nombre total d’estomacs vides

et E est le nombre d’estomacs examint

(5) L'indice de recouvrement des niches trophiques R (PIANKA, 1973; FORGE & BAR-

BAULT, 1978):

Z Pi x pik

RS )

VE PP x Pie

Source : MNHN, Paris

CHILLASSE, DAKKI & THÉVENOT 47

où Pij et Pik représentent l'abondance relative d’une catégorie de proie i dans le régime

alimentaire de deux espèces prédatrices jet k. Cet indice de similitude permet de comparer des

spectres d’utilisation de ressources alimentaires, sans qu'il soit un véritable indice de compé-

tition (BARBAULT, 1981).

Le test de Chi-deux (4?) sur les abondances relatives des proies a été employé afin d'établir

s’il existe une différence significative entre le régime alimentaire des mâles et des femelles

(SoLANO, 1983).

RÉSULTATS ET DISCUSSION

L'ALIMENTATION DE BUFO BUFO SPINOSUS

Il est important de signaler que cette espèce ne cherche pas sa nourriture durant la

période de reproduction où le coefficient de vacuité West de 100 %. Plusieurs observations

dans ce sens ont été publiées (LESCURE, 1965; CHRISTIAN, 1982). Cette constatation ne

corrobore pas les prévisions théoriques des régimes optimaux qui envisagent un apport

énergétique élevé durant la période de reproduction (MAC ARTHUR & PIANKA, 1966). Le

comportement agonistique, comme les autres activités associées à la reproduction, impliquent

des dépenses d'énergie élevées (SCHONER, 1971). Bufo bufo spinosus, à l'issue d’une longue

période d’hibernation à jeun, semble investir presque tout son temps dans des activités

reproductrices. Il possède la plus courte et précoce période de reproduction connue chez les

Anoures de la région d'étude (mi-février — fin mars; CHiLLASSE, 1990).

L'alimentation de Bufo bufo spinosus est composée de 13 catégories de proies, représen-

tées dans des proportions très différentes, les Coléoptères, les Dermaptères et les Formicidae

représentant 90 % de l'effectif total (tab. 1: fig. 2). Parmi les Coléoptères, les Curculionidae,

actifs la nuit, l'emportent de loin sur les autres 15 %; Ci = 58 ); les genres les

plus représentés sont Oriorhynchus, Temnorhinus et Thylacites. Les Tenebrionidae et les

Pterostichidae viennent en seconde position, suivis par les Scarabaeidae et les Harpalidae. Les

autres familles sont peu représentées dans l'alimentation de cette espèce. Elles sont, pour la

plupart, diurnes ou crépusculaires et vivent dans des endroits peu accessibles aux Crapauds.

Les Dermaptères sont représentés par deux espèces, Forficula auricularia (Forficulidae) et

Labiduria riparia (Labiduridae), avec une abondance relative Pi de 35 % et un degré de

présence Ci de 46 %. Les Hyménoptères (Formicidae) se trouvent dans presque 40 % des

contenus stomacaux examil avec une abondance relative de 22 . Les Arachnides, les

Myriapodes et les larves d’Insectes sont moyennement représentés. Notons la présence d’une

petite Couleuvre (Natrix maura) dans l'estomac d’un Crapaud commun. Des observations

similaires ont été rapportées par LOVERIDGE (1936).

L'étude comparative de la composition des contenus stomacaux des deux sexes de Bufo

bufo spinosus montre que ceux-ci utilisent les mêmes ressources alimentaires durant toute leur

période d'activité: il n'y a pas de différence significative entre les profils d’abondance des

proies chez les deux sexes (4°, df = 12, P > 0.05).

Source : MNHN, Paris

48 ALYTES 20 (1-2)

Tableau 1. — Abondance relative ct degré de présence des différentes catégories de proies dans les

contenus stomacaux de Bufo bufo spinosus et Bufo mauritanicus dans la région du lac

Aguclmam Azegza (Maroc).

ARE Abondance relative (79 Degré de présence (CD

crie EE Fo spirosus | Emaurianes | Ebdospnons | E-maurartes 1

T1) Coléopières (Co) EL 55 ë 5

Curculionidse 15 17 58 si

Tenebrionidae 5 5 4 @

Prerostichidae 5 6 50 44

Scarabeidae 4 8 4 25

Harpalidae 1 2 14 60

Staphylinidae 03 1 6 mn

Chtysomidae 03 005 2 2

Helophoridae o1 ° 2 0

Elateridae 01 00s 2 2

Cerambycidue 005 0 2 °

Histeridae o 02 0 7

Lebiidae 0 01 o 4

Meloidac 0 005 0 2

Melyridae 0 005 o 2

Dipières (Dip) 03 15 & 16

Tipulidse 02 1 6 u

Muscidae û 01 ° 4

L: Tachinidae 0.05 0 2 Q

CD Hymenoptères (Hyn) 3 15 3 &

Formicidae 2 16 35 e

Myrucidae 1 2 6 23

Ichneumonidae °1 02 4 2

Pompilidae 0 01 o 2

TO Heteropières (Het) T 15 4 El

Pentatomidae 03 1 8 nl

Caspidae 005 005 2 2

Lygacidae 005 004 2 2

Nabidae 005 005 2 2

O5 Dermaptères (Der) 3 El 46 46

Forficulidae 28 19 4 39

Labiduridae 7 2 2 4

T Orihoptères (Ont) LO] 23 Z E]

Grylidae 005 0 2 0

Acridilidae o 03 o 9

TM) Lépidoptères (LEP) 7.2 T 6 25

Nos UN TE é 3

TO Lives d'insectes (Lan) 7 Z 2 37

L. Coléoptères 1 ï 21 3

L. Lépidoptères 07 1 21 mn

L. Diptères o1 005 4 2

L. Hétéroptères 0 00 0 2

L. Odonates 005 o 2 0

D) Arschnides (Are) 4 7 4 37

Thomisidae os 02 4 9

Agelenidae 04 Q 1 °

Dysderidae 03 005 8 2

Lycosidae 03 1 10 9

Linypiidae 02 0 2 0

Gnaphozidae 01 01 2 n

Sparassidae 005 0 2 o

Phalgnidae 1 1 3 2

Buthidae o os 0 2

110) Ropodes (150) 3 3 4 ST

Armadillididae 2 1! 31 16

Porcellionidae 2 > 29 3

TT) Mriapodes (Myr) 03 ï 17 16

Lithobiidae 01 02 5 4

Scolopendridae 005 os 2 2

lulidae 02 1 6 14

T9) Gistéropodes (Cas) 51 (] 7 TT

Physidae o1 0 2 o

[TS Reptiles (Rep) 005 © Zz ©

Colubridae 005 0 2 o

Source : MNHN, Paris

CHILLASSE, DAKKI & THÉVENOT 49

% 80

40 |

LE!

1 2 3 4 5 6 7 8 9 10 11 12 13

Catégories de proies.

Fig. 2. - Composition des contenus stomacaux de Bufo bufo spinosus.

L'ALIMENTATION DE BUFO MAURITANICUS

Pendant la période de reproduction de cette espèce (début mars — fin mai), le coefficient

de vacuité s’est révélé très faible (V = 7%), sans être nul comme chez l'espèce précédente.

Le spectre alimentaire est formé de 11 catégories de proies avec toujours une dominance

des Coléoptères, des Hyménoptères (Formicidae) et des Dermaptères qui totalisent respecti-

vement des abondances relatives de 50 %, 21 % et 18 % (tab. 1, fig. 3). Parmi les Coléoptères,

les Curculionidae (Oriorhyncus, Brachyderes et Othylacites) et les Harpalidae (Harpalus,

Acinopus et Ditomus) lemportent de loin sur toutes les autres familles. Mis à part les

Lépidoptères nocturnes (Noctuidae) activement chassés, les Insectes volants (Diptères,

Hyménoptères autres que les Formicidae, Hétéroptères, Orthoptères) sont négligeables dans

l'alimentation de l'espèce, leurs abondances relatives ne dépassant pas le seuil de 1 %.

La comparaison entre les régimes des mâles et des femelles montre, pour les trois groupes

les plus consommés, des proportions similaires chez les deux sexes. Les autres groupes, dont la

contribution dans l'alimentation de ce Crapaud est très faible, présentent de légères différen-

ces d’abondance: les Isopodes plus consommés par les mâles, alors que les femelles ingèrent

plus d'Hétéroptères. Il n’y a pas de différence significative entre mâles et femelles si l’on

considère la totalité des proies (72, df= 10, P > 0.05).

MESURE DE L'AMPLITUDE DES NICHES TROPHIQUES

En dehors de la période de reproduction de Bufo bufo spinosus, marquée par un

coefficient de vacuité très élevé, les spectres alimentaires des deux espèces sont très diversifiés.

Etant donnée la ressemblance très marquée entre les régimes alimentaires des deux espèces,

à plusieurs tests statistiques pour confirmer ou rejeter l'hypothèse d’une

nous avons eu recou:

compétition alimentaire.

Source : MNHN, Paris

50 ALYTES 20 (1-2)

% 100

60 F

aPi

20 :

1 2 3 4 5 6 T 8 9 10 11

Catégories de proies

Fig. 3. - Composition des contenus stomacaux de Bufo mauritanicus.

L'indice de Shannon H', utilisé comme mesure de l'amplitude de la niche trophique pour

chaque récolte mensuelle (fig. 4), montre chez Bufo bufo spinosus des valeurs relativement

faibles durant les mois de mai; juin et juillet, période pendant laquelle les ressources alimen-

taires sont très abondantes, mais constituées essentiellement de Coléoptères et de Dermaptè-

res. Chez Bufo mauritanicus, cet indice enregistre de faibles variations durant toute sa période

d’activité, les Coléoptères, les Dermaptères et les Formicidae étant toujours dominants.

La contraction estivale, période de pleine abondance, des régimes alimentaires des deux

espèces semble, a priori, vérifier une des prévisions de la théorie des régimes optimaux (MAC

ARTHUR & PIANKA, 1966) qui envisage que, lorsque la densité des proies est élevée, le

prédateur se concentre sur celles qui présentent la meilleure valeur énergétique, mais qu’au fur

et à mesure que les proies se font rares, la diversité du régime augmente. Selon SCHLUTER

(1981), les prévisions de la théorie des régimes optimaux ne sont pas valables pour prédire le

comportement des prédateurs dans un écosystème ou les réserves et la disponibilité de la

nourriture sont diversifiées et abondantes. Plusieurs facteurs entrent en jeu dans le choix des

proies (disponibilité, comportement de prédation, etc.). L'hypothèse du choix d’un aliment

selon sa seule valeur énergétique est peu réaliste et s’applique mal à des communautés

naturelles.

RECOUVREMENT LL

NICHES TROPHIQUES

Le recouvrement des niches trophiques des deux espèces est assez modéré (R = 0,126)

durant la période de faible abondance des proies (février, mars et avril), mais il devient élevé (R

= 0,36) pendant la période des pics d’abondance des proies (mai, juin et juillet). Les valeurs

faibles de R enregistrées, au moment le plus critique dans la recherche de la nourriture,

prouvent que la compétition entre les deux espèces est très faible. Les chevauchements des

niches trophiques, pendant la période de pleine abondance des proies, sont plutôt déterminés

par la grande disponibilité de la nourriture que par une compétition. Rappelons, à ce propos,

Source : MNHN, Paris

CHILLASSE, DAKKI & THÉVENOT 51

È 4 —+—B bio

$ 8-8 rrouitarious

ë 3

; .

0 | Mis

PF MD PAL LMI JA GDUS NEO N

Fig. 4. — Variation de l'amplitude de la niche trophique de Bufo bufo spinosus et Bufo mauritanicus.

que cet indice de similitude permet de comparer des spectres d'utilisation de ressources

alimentaires, sans qu’il soit un véritable indice de compétition (BARBAULT, 1981).

COMPOSITION SPÉCIFIQUE DES RÉGIMES ALIMENTAIRES

Le chevauchement des niches trophiques des deux Bufonidae étudiés, durant certaines

périodes de leur activité, n'implique pas l'identité parfaite de leurs régimes alimentaires. En

effet, une différence a été notée au niveau des genres de Coléoptères consommés. C’est ainsi

que parmi les Curculionidae, entre autres, on a trouvé chez B. bufo spinosus surtout les genres

Otiorhynchus, Temnorhius et Thylacites, et chez B. mauritanicus les genres Otiorhynchus,

Brachyderes et Othylacites. La même constatation s'applique aux genres d'Harpalidae: Z. bufo

spinosus consomme surtout des Acinopus et des Stenolophus, tandis que B. mauritanicus se

nourrit de Ditomus; toutefois, le genre Harpalus, très abondant, se trouve dans les contenus

stomacaux des deux Bufonidae. La dominance des Coléoptères et des Formicidae dans le

régime de ces deux Crapauds concorde, en grande partie, avec les conclusions de nombreux

auteurs qui ont travaillé sur le régime alimentaire des Bufonidae.

En effet, une comparaison des régimes alimentaires des Bufonidae étudiés dans diverses

régions du monde, en particulier au niveau des catégories de proies les plus consommées et

dominantes (Coléoptères et Formicidae), permet de conclure que les Coléoptères et les

Formicidae dominent nettement et représentent toujours plus de la moitié des proies ingérées

(tab. 2). L'originalité de nos résultats réside dans la dominance des Dermaptères en plus de ces

deux groupes d’Insectes (CHiLLASsE, 1990). Chez les Crapauds d'Afrique équatoriale et de

Malaisie, les Formicidae prédominent dans la nourriture. Ceci a été vérifié particulièrement

chez Bufo funereus (INGER & Marx, 1961) et Bufo regularis. (PAULLIAN & VILARDEBO, 1946;

CHAPMAN & CHAPMAN, 1958; INGER & MaRX, 1961: LESCURE, 1971; BARBAULT, 1974). Dans

les régions tempérées européennes, les Formicidae et les Coléoptères sont d’égale importance

Source : MNHN, Paris

52 ALYTES 20 (1-2)

Tableau 2. - Abondance relative et degré de présence des Coléoptères et des Fourmis dans les

régimes alimentaires de différentes espèces de Bufonidae.

Espèces Pays, régions Fous Cosoptères Références

ñ69 | co | m6 T ac

Fufo asper BERRY, 1970

3 100 05 36

- Cavemes 54 65 3 e

Bufo melanostictus | Malaisie: BERRY & BULLOCK,1962

- Savane et forêts 45 91 3 44

- Champs 19 57 8 40 |

Fifo regularis Basse Côte d'Ivoire | 87 100 17 73 [PAULLIAN & VILARDENO, 1946

Tanzanie à 42 s 76 | CHarman & CHarMaN, 1958

Sénégal 55 88 12 71 |LescuRr, 1971

Côte-d'Ivoire 93 91 2 46 |BARBAULT, 1974

Congo : 87 . 68 __| INGER & Marx, 1961

ue finereus Congo = 30 É TT ÎINGER & MARX 1961

Bufo melanopleura | Congo à 100 3 98 [INGER & MaRX, 1961

Bufo usberanus | Congo : ES Pme INGER & MARX, 1961

Bufo pentont Sahel Sénégalais ES] E] 2 89 [FORGE & BARBAULT, 1978

Bufo woodhouser — [ USA. 35 50 49 95 [Bus & MENHNR, 1962

Bufo calamita Espagne 25 oran PRE = LiZANA etal., 1986

Bufo bufo Espagne 553 = 65 TT [EzaN« etal,, 1986

France G 84 143 96 | LescURr, 1965

France 56 : 23 = [Duronr, 1962

Angleterre 416 : 16 = [com, 1932

Bufo bufo spinosus _ | Maroc 2 55 37 30 __|Cmtass, 1990

Bufo maurtanieus [Maroc 16 e 50 93 [CHiLrASSE, 1990

dans la nourriture des Bufonidae (DUPONT, 1962; LESCURE, 1965; LiZANA et al., 1986). En

revanche, les Coléoptères supplantent les Formicidae chez les Crapauds du Maroc

(CHiLLASSE, 1990) et ceux d'Amérique (BusH & MENHINK, 1962).

CONCLUSION

Les deux espèces étudiées sont qualifiées de polyphages. Bien qu’en des proportions

différentes, elles puisent leur nourriture parmi une faune d’Arthropodes abondante dans le

milieu d'étude. En termes de fréquence d’occurrence et d'abondance relative, les Coléoptères.

les Formicidae et les Dermaptères dominent nettement leur alimentation. Au contraire, les

Arachnides, les Isopodes, les Myriapodes et les Gastéropodes comptent peu dans l’alimenta-

tion.

Les deux sexes, pour chaque espèce, pa ent avoir des régimes similaire:

ségrégation sexuelle pour la collecte de la nourriture n'a été signalée.

aucune

trophiques diffèrent entre les deux espèces au regard de plusieurs facteurs:

Ÿ s inféodé au milieu

forestier que Bufo mauritanicus qui préfère les milieux dégagés, clairières et prairies humides:

(2) la composition spécifique des proies consommées difière. Ces facteurs assurent une

Source : MNHN, Paris

CHILLASSE, DAKKI & THÉVENOT 53

séparation écologique et une cohabitation de ces deux prédateurs. Par ailleurs, la grande

quantité et la variété des proies qu'ils consomment soulignent l'importance de ces Bufonidae

dans les réseaux trophiques de cet écosystème péri-lacustre.

RÉSUMÉ

L'étude concerne le régime alimentaire de deux espèces d’Amphibiens Anoures de la

famille des Bufonidae (Bufo bufo spinosus et Bufo mauritanicus) dans la région du lac

Aguelmam Azegza situé dans le Moyen Atlas Marocain. L'expression des résultats en termes

de fréquence d’occurrence des proies (degré de présence) et d’abondance relative suggère une

ressemblance des régimes alimentaires des deux espèces, avec une dominance des Coléoptères,

des Hyménoptères Formicidae et des Dermaptères. Les mesures de l'amplitude et des chevau-

chements des niches trophiques ainsi que la taille des proies excluent la présence de toute

forme de compétition alimentaire entre ces deux espèces. La diversité des régimes alimentaires

des deux Bufonidae s'accroît en période de faible disponibilité pour devenir très faible en

période des pics d’abondance des proies. Les deux sexes de la même espèce présentent des

régimes similaires: aucune différence significative n’a été enregistrée au niveau des proies

essentielles. Une comparaison des régimes de plusieurs Bufonidae étudiés dans diverses

régions du monde permet de conclure que les Coléoptères et les Formicidae dominent leurs

alimentations.

RÉ

2RENCES BIBLIOGRAPHIQUES

BARBAULT, R., 1974. - Le régime alimentaire des Amphibiens dans la savane de Lamto (Côte d'ivoire).

Bull. LE A.N., (A), 36 (4): 852-972.

eu 1981. — Ecologie des populations et des peuplements. Paris, Masson: 1-200.

Berry, P. V. 1970. - The food of the giant toad Bufo asper. Zool. J. Linn. Soc., 49: 61-68.

Berry. PV. & BULLOCK, J. A., 1962. — The food of the common Malayan toad Bufo melanostictus

Schneider. Copeia, 1962 (4): 736-741

Busn, FM. & MENHINR. E. E, 1962. - The food of Bufo woodhousei fowleri. Herpetologica, 18: 110-115

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(Schneider). Ann. Mus. Hist. nat. Nice, 1: 91-100.

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Corresponding editor: Thierry LoDÉ.

Source : MNHN, Paris

Alytes, 2002, 20 (1-2): 55-66. 55

Results of the first batrachian survey

in Europe using road call counts

Brandon P. ANTHONY

Environmental Sciences & Policy Department, Central European University,

Nädor u. 9, Budapest 1051, Hungary

<brandona@ceu.hu>

Within the last 20 years, there have been extensive efforts to monitor

populations of calling amphibians, especially in North America. One such

initiative involves use of volunteers in conducting road call counts. To date,

no attempt has been made to test the efficacy of this technique in Europe.

This paper summarizes research involving road call counts in the Biharugra

Landscape Protected Area, Kërôs-Maros National Park, Hungary. Seven of

Hungary's 12 anuran species were identified in the study area using this

method and an additional 3 species were detected by complementary visual

encounter surveys. Limitations, including variations in species calling radüi,

extraneous noise and program resource requirements should be considered

when designing similar volunteer-based road call count protocols for other

regions. However, this method should be of value in many areas in Hungary

and Central Europe, due to its low cost, accessibility of volunteers, and

value in accurately detecting most anuran species (including Bombina

bombina and Hyla arborea - both IUCN Red Data Book species).

INTRODUCTION

Widespread declines of amphibian populations, often without an apparent proximate

cause (BLAUSTEIN & WAKE, 1990; PricLiPs, 1990; Wake et al., 1991; GRIFFITHS & BEEBEE,

1992), have initiated a critical global review of the status of amphibian species (VIAL &

SAYLOR, 1993). Complicating the understanding of this decline are the naturally high fluc-

tuations of many amphibian populations (PECHMANN & WILBUR, 1994). Amphibians may

also display metapopulation dynamics, with decreases in some local populations coinciding

with increases in others (SIÜGRI 1991). Moreove mphibians have been recognized as

potential indicators of environmental change (Virr et al., 1990; SreBBiNs & COHEN, 1995;

BoweRs et al., 1998), an additional factor driving inventory and monitoring efforts. To as:

the status of amphibian populations, distribution patterns and population characteristics

need to be examined. However, assessments are difficult because few comparable data sets and

long-term studies exist (BLAUSTEIN, 1994; REED & BLAUSTEIN, 1995). The need to establish

long-term inventories and monitoring has been emphasized, both in Hungary and elsewhere

(PECHMANN & WiLBUR, 1994; Korsôs, 1997).

Source : MNHN, Paris

56 ALYTES 20 (1-2)

A number of species-specific considerations may affect detection of amphibians and

effective use of various survey methods. Breeding season and diurnal patterns may vary with

species and site (PÉCHY & HARASZTHY, 1997; BRIDGES & DoRCAS, 2000). Some populations,

species, or life history stages may be easily observed, while others, being more rare, cryptic or

fossorial, may require refined experience or trapping techniques. In addition, many biologists

believe that a few successful populations can contribute most of the reproductive output for

all populations in a local area (SOULÉ, 1987; PuLLiam, 1988; SIÔGREN, 1991). In these

situations, surveys based on distinctive courtship vocalizations may prove to be the best

possible method for detecting anuran species.

The Declining Amphibian Populations Task Force (DAPTF), now affiliated to IUCN,

was established to develop programs in participating countries (WAKE et al., 1991; ViaL, 1991;

HazciDaY & HEYER, 1997). The road call count (RCC) method has been a frequently

chosen monitoring technique in North America because of its relative ease for volunteers, and

many Canadian provinces and USA states have used similar monitoring methods (see

LaNNOO, 1998). However, Hungarian data are less comprehensive, and although monitoring

programs do exist in Europe (Gasc et al., 1997), the RCC methodology has never been tested

here.

Of the 74 amphibian species in Europe, 17 occur in Hungary, including 12 anurans

(NGLLERT & NÔLLERT, 1992). Hungary was one of the first European nations to enact

legislation protecting its wildlife, with its herpetofauna protected as early as 1947 (CORBETT,

1989). However, like the rest of Europe, amphibians in Hungary have not received a pro-

portionate degree of conservation action or resource allocation compared to animal

groups such as birds and mammals (BAK6 et al., 1992; Puy, 2000). The IUCN (ANONYMOUS,

1993) recognizes that this lack of knowledge is a threat to the wetland diversity of the

region.

Urban and agricultural development have had profound impacts on amphibian habitats

in Hungary, including the loss and alteration of lentic habitats and their historical hydrolog-

ical regimes. Vigorous programs of wetland drainage and channelization of the Tisza and

Kôrës rivers (in the study region) in the mid-1800s, primarily for conversion to arable land,

resulted in loss of many ox-bow lakes (Marosi & SZILARD, 1969). Lentic habitats provided by

river side channels, wooded flood plain areas and off-channel sloughs and swales have been

largely eliminated. For those temporary ponds which have remained or have been artificially

excavated in the Tisza River basin, eutrophication is a major problem since the traditional

yearly inundations have ceased (DENISOv et al., 1997). Thus, it is clear that without protective

intervention, the risk of threats to amphibian populations due to, inter alia, habitat loss and

deterioration, will likely increase. Although there have been some attempts to describe

amphibian species and distributions in the region (MARIAN, 1963; GUBANYI, 1992), there has

been little effort to develop a comprehensive list of amphibian species in the Kürôs-Maros

National Park (KMNP).

Currently, amphibian monitoring is a new focus of attention in Hungary, particularly

with its obligations in planned accession to the European Union. Until this study, no wide

scale, long term investigations have been conducted, yet there is a growing realization that

especially with limited resources, monitoring populations must employ a number of tech-

niques, including those that involve volunteers (KORsÔs, 1997). The goal of this study was to

Source : MNHN, Paris

ANTHONY 57

help standardize methods of amphibian monitoring in Hungary and to conduct an investi-

gation on the applicability of volunteer-based RCCSs in Europe, given their widespread use in

North America.

STUDY AREA

The 52 000 ha KMNP in east Hungary is a mosaic of large and small habitats. It lies

within the Great Hungarian Plain in one of the warmest (10-10.5°C annual mean tempera-

ture) and driest (550-600 mm annual precipitation) regions of Hungary (ANONYMOUS, 1993).

Protecting the rare flora and fauna in this region is of national importance and deserves

special attention (Bir6, 1996). The study area, located in the 9645 ha Biharugra Landscape

Protected Area, includes over 1900 ha of fishponds (fig. 1), Hungary’s second largest artificial

lake complex. Surrounded by vast reed beds, the ponds provide critical breeding habitats for

a large number of protected bird species and for mammals, fish, reptiles and amphibians

(ANONYMOUS, 1997). Owing to its rich, diverse habitat and landscape features, the ponds and

surrounding marshes gained international importance and were declared a Ramsar Conven-

tion on Wetlands of International Importance Especially as Waterfowl Habitat site in 1997.

CANTON { LA à fe"

{23 Landseape Protection Area

200 km

Fig. 1. Location of the study area in Biharugra Landscape Protected Area of Kôrôs-Maros National

Park, Hungary

Source : MNHN, Paris

58 ALYTES 20 (1-2)

MATERIALS AND METHODS

A RCC route between Biharugra and Zsadäny was selected for monitoring because of

the area’s unique diversity of amphibian habitats including vernal pools, drainage canals, fish

ponds, wooded swamps and marshes. These habitats exist among agricultural land that

focuses on wheat production and livestock grazing. Ten RCC stations were established

running in a south and westerly direction from Biharugra (fig.

The methodology in this research was based on the protocol developed by DAPTF

Canada for Ontario, i.e., of the North American Amphibian Monitoring Program (NAAMP)

specified in GARTSHORE et al. (1997). In Ontario, the route is chosen by the volunteer (thus,

non-random) and ideally consists of a straight, quiet road with 10 stations 0.8 km apart,

regardless of proximity to wetlands. Volunteers are requested to conduct three surveys over

the anuran breeding season, corresponding with optimum weather conditions and calling

periods for local species. Surveys are conducted between 30 min after sunset and midnight,

with participants listening at each station for a period of 3 min, recording all anuran species

heard according to the Wisconsin Index: (0) none heard; (1) individuals can be counted, no

overlapping calls; (2) calls overlapping, but distinguishable; (3) full chorus, calls continuous

and overlapping. Supplementary information including time, air and water temperatures,

wind speed, and land use are also recorded.

In this study, I carried out RCCSs between 6 March and 29 April 1998, using the Ontario

methodology with the following modifications: (1) European species were identified accord-

ing to the audio reproductions of anuran calls by ORSZAGH (1982) and ALSCHER et al. (1998);

(2) RCCSs were conducted on 19 evenings instead of the suggested three to attempt to detect

calling intensities of each species over the breeding season; (3) if present, extraneous noise was

described for each location; (4) a 60 s, instead of 30 s, waiting period was used after alighting

from the vehicle or following traffic noise before beginning or resuming the survey; (5) air

temperatures were taken at the start and finish of each survey, with the mean value presented

(fig. 3). As Mossman et al. (1998) noted, measuring water temperature was time-consuming

for volunteers. In this study, it was taken once per survey at station 6 to serve as a general

indicator only.

To determine how well the RCC detects species presence, visual encounter surveys (VES)

were conducted on two evenings (15 and 25 April) at four shallow ponds (fig. 2) located near

the RCC stations (pond A, 450 m from station 2, 0.25 ha; pond B, 100 m from station 10, 0.56

ha; pond C, 60 m from station 10, 0.001 ha; pond D, 1100 m from station 10; 0.8 ha). These

ponds were selected due to their easy access and because anurans were calling from these

locations during the RCCSs. During these evenings, RCCSs were conducted, recording species

heard directly from ponds A (station 2), B, € and D (station 10). Immediately following these

RCCS, thorough VES were conducted around the perimeter of the ponds as recommended by

THoms et al. (1997). A survey was first conducted around the shoreline examining the pond

littoral zone, followed by a second walk about 1.5 m from the shoreline, encompassing a 3m

wide sweep of the riparian zone. During these walks, stops were made every 2-3 m to

ahead for any anurans. This method also allowed detection of species calling underwater or

among thick vegetation. Only adults were recorded.

Source : MNHN, Paris

ANTHONY 59;

Biharugra

05 1

ui km

Fish Ponds

S = station

p = ponds

To Komädi

Open Water Fish Ponds

Zsadäny

Fig. 2. — Road call count route, including stations and study pond locations. Geographical coordinates of

Stations and study ponds (ANONYMOUS, 199$a-b): (S1) 21°35°32"E, 46°57"45°N; (S2) 21°3522°E,

46°5720"N; (S3) 21°35"02E, 46°5702°N; ($4) 21°34'30°E, 46256 48"N; (S5) 21°3354"E,

46°56"36"N; (S6) 21°3319"E, 46°56727"N; (S7) 21°3242"E, 46°5619°N: (S8) 21°32°05°"

46°5612"N; (S9) 21°31°32"E, 46°5612"N; (S10) 21°30'55"E, 46°5603"N; (pA) 21°35°1

46°5731"N; (pB) 21°3100"E, 46°5603"N; (pC) 21°30'50"E, 46°56"04"N; (pD) 21°29'4:

4655 3L°N.

enjea SAG

16-Apr js

5-Apr Ja

Be pes EME AUEUR ÉRERÉRÉSEES

She ANT ns + ENT IS LT ue

US IF nes RAR RAR ER À

10-Apr al

13-Apr eee

Fig. 3. - Beaufort Wind Scale values (shaded bars) and mean air (darkened squares) and water

temperatures (open circles) during RCC.

Source : MNHN, Paris

60 ALYTES 20 (1-2)

RESULTS

ROAD CALL COUNTS

Seven of Hungary’s 12 anuran species were detected at RCC stations along the Biharugra

route. Bombina bombina, Bufo viridis, Hyla arborea and Rana esculenta were each recorded at

all 10 stations (tab. 1). These four species were also heard on more evenings than any other

species. Number of species recorded at each station ranged from 4 to 7.

ENVIRONMENTAL PARAMETERS

Maximum Beaufort Wind Scale (BWS) values, and mean air and water temperatures for

each RCC are shown in fig. 3. BWS values ranged from 0 to 5 (mean 1.4). Although air

temperature ranged from 7.0 to 17.0°C and water temperature from 6.5 to 19.0°C at station 6

during the surveys, the onset of anuran calling was characterized when air and water

temperatures first reached 10.5 and 12.5°C, respectively. However, anurans continued calling

even when temperatures dropped below these values during the research period (e.g., 13-14

April).

DURATION OF RCC

Mean time taken to conduct an individual RCC, including the observation period at each

of the 10 stations, allowing time for driving and additional waiting periods in lieu of traffic

noise, etc., was 75 min (s 18.8; range 50-110).

VISUAL ENCOUNTER SURVEYS

Adults of 10 of Hungary’ 12 anuran species were detected during the VES (tab. 2). In

some cases, due to calling underwater or among thick vegetation, individuals were heard

during the VES but not seen (i.e., Pelobates fuscus at ponds A and C, Bufo bufo and R.

esculenta at pond B).

DISCUSSION

My road call counts revealed that anuran species richness in the Biharugra Landscape

Protected Area is almost two-fold greater than the KMNP Management Plan indicated. This

richness includes Hyla arborea and Bombina bombina — both IUCN International Red Data

Book species (BAILLIE & GROOMBRIDGE, 1996). In itself, this would be a suficient reason to

encourage the use of RCCS in other areas of the KMNP, as well as other national parks.

Minimally, the use of RCCSs in Hungary might be used to locate breeding amphibian

populations to target for more intensive survey strategies, thereby limiting the number of sites

that need to be surveyed. Indeed, the Zsadäny pond (pond D) was located in this fashion (i.e.,

anurans Calling in this pond, including the two IUCN listed species above, were heard from

RCC station 10 — over one kilometre away).

Source : MNHN, Paris

ANTHONY

Table 1. Percentage of evenings anuran species heard at RCC stations during research period. t

IUCN Red Data Book (BAILLIE & GROOMBRIDGE, 1996). * Bern Convention Appendix IT

(ANONYMOUS, 1994). ? Diminishing over European Range.

Species Ses ñ

1f2lslalsle 8 [o li

Hyla arborea + * 88 77 71 71 59 | 47 | 47 71 65 71 10

Rana esculenta 35 29 | 41 47 | 41 59 | 47 | 71 59 | 29 10

Bombina bombina + * + | 41 | 47 | 53 | 41 | 41 | 47 | 12 | 41 | 47 | 47 | 10

Bufo viridis * n|s 12/6182 li8ln|s|7| 10

Bufo bufo ololololx|»|6l6elolols:s

Rana ridibunda 0 0 0 0 12 is 3 0 29 12 0

Rana lessonae ololslololololslolo

Total species /station | 4 [4 | 514al6l6)s|7|sl|a

Table 2. - Comparison of species observed during visual encounter surveys (V) and road call counts

(R). * Species heard only, not seen during visual encounter surveys.

Ponds

Species A B c D

15 April{25 April|15 April|25 April|[15 April|25 April|15 April|25 April

Bombina bombina v |] vr | vr | vr | vR | vr | vr | v

Pelobates fascus vs | vs v v* v

Bufo bufo v v!

Bufo viridis vR | vR VR v v

Hyla arborea vr | vr | vr | vr VR | VR

Rana arvalis v

Rana dalmatina v v v v v v

Rana ridibunda v v

Rana lessonae v

Rana esculenta vr | v+ | vr v | vR

Total species / survey | 5 7 4 8 2 2 5

Source : MNHN, Paris

62 ALYTES 20 (1-2)

A prime issue to consider is the discrepancies observed between species reported by the

two survey methods. The VES confirmed all seven species observed with the RCC method, but

also detected three additional species not heard in any of the RCCSs along the route: P fuscus,

Rana dalmatina and Rana arvalis wolterstorffi. These species were probably not heard during

the RCCS because they call underwater, severely restricting detection distance (ORSZÂGH,

1982; personal observation), and the RCC stations were all more than 50 m from the ponds

surveyed by VES. For European anuran species, inter-station distance, call phenology and

detection radii should be further investigated in varying habitats (including different assem-

blages and species natural histories) to determine the likely maximum distance required

between RCC stations. A protocol of this nature should also account for frogs with relatively

large inter-individual calling distances (e.g., Æ. arborea) to maintain independence of data

and avoid double-counting. Furthermore, because human participants generally choose their

own routes in volunteer-based RCCSs, the sampling design is non-random, resulting in an

obvious bias to choose routes where known anuran populations are currently calling, and

neglecting inactive sites that potentially could develop future breeding populations. This

might produce false estimates of declines by ignoring increasing populations. Conversely,

although extensive (random or random-stratified) RCCs may give more accurate indications

of breeding population trends, more observers are needed and the latter are more reluctant to

conduct randomly selected routes due to the large number of “zeros” likely to be encountered

— an admittedly important limitation with random route selection (Mossman et al., 1998;

& MossMan, in press). As in the North American Amphibian Monitoring Program,

striking a balance between hearing the most species during a RCC given the variation in

calling distances, and the willingness of volunteers to spend time monitoring anurans is of

utmost importance.

In the case of R. dalmatina and R. arvalis wolterstorffi, the field season may have begun

too late, as these are relatively early breeders (PÉCHY & HARASZTHY, 1997) suggesting that the

first survey should be conducted in late February or early March. Corresponding with air and

water temperatures and life histories of the species present (PÉCHY & HARASZTHY, 1997),

three periods are suggested to carry out future RCCS in the study area: early March (R.

dalmatina, R. arvalis), mid-April (B. bombina, B. bufo, B. viridis, P fuscus, H. arborea) and

mid-May (R. esculenta, R. ridibunda, R. lessonae). More data may be needed to refine this

seasonal surveying regime.

An additional limitation with this technique is associated with extraneous noise at RCC

stations where birds were calling in large numbers, where frequent traffic noise was experi-

enced, or when wind speed exceeded 20 km/h (BWS > 3). These surveys took longer to

conduct and were more frustrating, indicating that volunteers should also be encouraged to

choose routes which have minimum extraneous noise from wind, barking dogs, birds, etc. A

second factor relating to extraneous noise involves calls of other animal species that sound

similar to local anurans. ALSCHER et al. (1998) demonstrated that both the European nightjar

(Caprimulgus europaeus) and the horse cricket (Gryllotalpa gryllotalpa) emit sounds similar to

the territorial call of the green toad (B. viridis). The distributions of both of these non-anuran

species extends throughout Hungary (BAKONYI et al., 1995), and during the VES conducted at

pond D the green toad and the horse cricket were heard calling simultaneously. Therefore,

improvements to this protocol should include descriptions of other calling species on instruc-

tional materials, and techniques to differentiate these calls. Given the limitations, calling

Source : MNHN, Paris

ANTHONY 63

surveys are unreliable for detecting relatively quiet species or explosive breeders, such as À.

temporaria and R. arvalis, when calling is limited to a short time period (ZIMMERMAN, 1994;

Pécay & HARASZTHY, 1997; BOWERS et al., 1998).

For many species, however, calls are useful to locate breeding populations, and can be

used to detect species presence or estimate the relative abundance of breeding males. On a

number of occasions, due to calling underwater or among thick vegetation, P fuscus, B. bufo

and R. esculenta were only detected by sound during VES and not seen, suggesting that in

cases where stations are located relatively close to calling individuals, RCCs may be advanta-

geous in detecting species that are cryptic, low in number, or call underwater. This may also

hold true for species such as F. arborea which have relatively long inter-individual calling

distances but migrate during the day from breeding ponds to surrounding vegetation where

they can be difficult to see (ORSZAGH, 1982; personal observation). RCCS can be an effective

monitoring tool, especially at sites where visual surveys conducted by walking are logistically

difficult, such as: (1) large wetlands: (2) montane lakes with inaccessible shorelines; (3) lakes

and wetlands with either soft-bottomed substrates, coarse substrates or extensive woody

debris; (4) inaccessible privately owned land. Moreover, when set up as permanent sample

sites, RCC routes can yield valuable data not only on local amphibian populations, but also on

concurrent changes in habitat components if habitat types are recorded along with data on

the species being investigated (COOPERRIDER et al., 1986). These surveys can be conducted by

volunteers, and training tapes and manuals make it possible to involve even inexperienced

observers (SHIROSE et al., 1997). Conversely, other more comprehensive surveys, including

VES, require more expertise, are intrusive in nature, and demand greater levels of time and

resources.

Validation of amphibian monitoring programs has been hotly debated at various levels

(SHIROSE et al. 1997; Dumois, 1998; HEMESATH, 1998). Canadian amphibian monitoring

programs have evaluated the accuracy of audio surveys (BERRILL et al., 1992; BisHop et al.,

1997; SHIROSE et al., 1997). Most significantly, these have shown that although calling

intensity cannot be considered a true constant-proportion index of abundance, they can be a

useful index for populations below a certain size, and to identify trends over extended periods

of time. Hence, their potential use in Europe should include analysing species

presence/absence at each station, or grouped stations to record trends, with multi-year data

sets. HEYER et al. (1994) recommended this technique should complement other alternative

monitoring methods such as egg or larval counts, or mark-recapture studies, but BEEBEE

(1983) pointed out that such methodologies have their own sets of problems. Nonetheless,

parallel trends among several techniques can increase the credibility of conclusions drawn

from monitoring efforts. MossmaN et al. (1998) accurately indicated that when planning such

volunteer-based monitoring programs, competent long term co-ordination must be main-

tained, dealing with issues including program promotion (e.g., volunteer encouragement),

creation of concise and easy-to-understand instructional materials, data compilation and

verification, quality control, report generation, and responding to volunteers’ enquiries.

This crucial component is imperative during the planning phase of any prospective RCC

program.

Source : MNHN, Paris

64 ALYTES 20 (1-2)

CONCLUSION

The extent of amphibian distributions in Hungary is poorly documented (Gasc et al.,

1997). Previous to this study, the KMNP Management Plan recognized only four amphibian

species in the Biharugra Landscape Protected Area. However, my RCCSs revealed almost

two-fold greater anuran species richness including Hyla arborea and Bombina bombina — both

IUCN International Red Data Book species. À national volunteer-based monitoring pro-

gram employing RCCS, recognizing both their limitations and benefits, would not only be an

appropriate complementary approach to monitor taxa indicative of habitats (FARAGO &

NEMES, 1997), but would also encourage the public at large to conserve and enhance biodi-

versity to a greater extent across all areas, not just restricted biotopes in protected areas.

ACKNOWLEDGMENTS

I thank: Central European University for financial assistance; Miklôs Puky and KMNP personnel

including Tamäs Zalai and Béla Kalivoda for guidance; Alan Watt and Dan Cogalniléeanu for insightful

comments on the text, Larisa Grujic for technical assistance, and Lauren E. Brown, Mike Mossman and

the other anonymous referees for their helpful comments on the manuscript.

LITERATURE CITED

ANoxYMous [World Conservation Union (IUCN)]. 1993. - The werlands of central and eastern Europe.

Environ. Gland, Switzerland & Cambridge, UK, IUCN, Res. Ser., 7: [i-xi] + 1-83.

ANONYMOUS [Bern Convention], 1994. - Convention on the conservation of European wildlife and natural

habitats. Appendices to the Convention. Strasbourg, Council of Europe T-PVS(94)2: 1-21.

ANONYMOUS [Magyar Honvédség Kartogräfia Üzem (MKHÜ)], 1995a. — Biharugra. Map N° L-34-44-

Map N° L-34-43-B-b (1:25000).

ANONYMOUS [Magyar Madärtani és Természetvédelmi Egyesület (MMTE)], 1997. - Biharugra. Szarvas,

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Source : MNHN, Paris

Alytes, 2002, 20 (1-2): 67-76. 67

Triturus vulgaris (Linnaeus, 1758)

at its southern limit: distribution

on the Peloponnese, Greece,

with range extensions from the Central

and South Peloponnese

Roger BouR* , Henrik BRINGSOE** & Maurice VANDERHAEGE***

* Laboratoire des Reptiles et Amphibiens, Muséum national d'Histoire naturelle,

25 rue Cuvier, 75005 P:

<bour@mnhn.fr>

** Irisvej 8, 4600 Koge, Danemark

voridonline.dk>

**# 22 rue de la Horgne, 57245 Peltre, France

This note presents a historical account of the discovery of the Greek

smooth newt, Triturus vulgaris graecus (Wolterstorff, 1905) in the Pelo-

ponnese. Recent observations of populations in the vicinity of Tripoli

(Arcadia) and Gvthion (Laconia), allow to extend its hitherto known range to

the Central and Southeastern parts of the peninsula. This range extension

includes the southernmost locality known for that species. The wide Pelo-

ponnesian range shown on a map in the Atlas of Amphibians and Reptiles

in Europe (Gasc et al., 1997) is rejected due to lack of documentation.

HISTORICAL RECORD

The first published observation of the smooth newt Triturus vulgaris (Linnaeus, 1758) in

the Peloponnese appeared very early: the Expédition en Morée of 1829-1831 mentioned and

depicted it under the name of “7riton abdominalis (Latreille, 1800)” (BiRON & BORY DE

SAINT-VINCENT, 1833: 76: pl. 15, fig. 4-5): “Cette espèce se trouve en Morée [= Peloponnese],

et notamment aux environs de Modon [= Modhon, Modoni, presently Methoni]””. BEDRIAGA

(1881: 287) published this mention, identifying the species as “Triton palustris (Linnaeus,

1758)”. The second observation, that of a female by Dr. Marän in April 1936 in Kalavryta,

was published by SrÉpaNEK (1944: 123), who identified the newt as Triturus vulgaris graccus

(Wolterstorff, 1905) (type locality: Corfu = Kerkyra). In recent annotated lists of amphibians

of the Peloponnese (BRINGSOE, 1986; KEYMAR, 19864), or in that for the genus Triturus in

Gree: >TIROPOULOS et al., 1995), the range of Triturus vulgaris on that peninsula appeared

to be scattered and limited to the northerly regions with one exception, that of Methoni.

BRINGSOE (1986: 282, 311) gave the following localities, with the references: Kalavrita [=

Kalavryta] (STÉPANER, 1944), “approx. 8 km N of Didyma”, from eggs, but with reservation

Source : MNHN, Paris

68 ALYTES 20 (1-2)

for their identity (ADEMA & IN DEN BosCH, 1980) and “Kalogria Wood” (personal communi-

cation to the author by Chondropoulos from 1985). Besides, Bringsoe called attention to the

old record at Methoni. Later, in 1994, the same author (H. B.) visited, together with

Jorgensen, the forest of Kalogria (more accurately Strofilia) where they observed many larvae

(BRINGSOE, unpublished; JORGENSEN, 1995). KEYMAR (19864: 5) mentioned only Kalavrita,

Methoni and Didyma, without further details, and the distribution map published by

NÔLLERT & NÔLLERT (1992: 203) included these same three localities, showing simultaneously

a question mark for the remaining part of the Peloponnese. In our opinion, some doubt could

also apply to Methoni, unconfirmed locality for 170 years. However, on the present basis we

are unable to judge whether 7: vulgaris still occurs around Methoni as we are not aware to

what extent the area has been investigated; so far we have not seen any reports describing

sufficiently detailed surveys which have been carried out at the right time of the year (as to the

proper season; see also further down this text).

In a second article, KEYMAR (1986b: 14, 19, 35) stated: “Die subspezies graecus kommt

auf den vier groBen Ionischen Inseln”, i.e. Kerkira [= Corfu], Lefkas, Kephalonia [= Kefal-

linia] and Zakinthos, whereas on the joined map this last island was indicated only with a

question mark. On the other hand, the same map seems to show a new point in the

northwestern part of the peninsula, to the north of Pyrgos, in the nomos (municipality) of

Ilias [= Ileia]. We think that actually Keymar wanted only to indicate the presence of this newt

on the nearby Peloponnese in a quite superficial way. CLARK (1989: 9), in a check-list of the

herpetofauna of the Argo-Saronic Gulf region, repeated the Didyma record as published by

Bringsoe, without adding any new data. Finally, one of us (BRINGSOE, 1994: 354-358)

presented a new locality for Triturus vulgaris graecus, “5-6 km east of Kertezi, east of Mt.

Erymanthos … altitude 745 m° [that is, approx. 10 km southwest of Kalavryta], where this

Triturus taxon is sympatric with Triturus alpestris (Laurenti, 1768).

SOTIROPOULOS et al. (1995) compiled an exhaustive study of the geographic distribution

of the genus 7riturus Rafinesque, 1815 in Greece, based on a large bibliography (primary or

secondary sources), quoting even. Aristotle! Thus, these authors listed the localities of

Didyma (BRINGSOE, 1986), Ileia [Ilias] without any details (KEyYMAR, 1986; we gave our

interpretation of this “locality” above), Kalavryta (STÉPANEK, 1944), Kalogria (BRINGSOE,

1986), Kertezi (BRINGSOE, 1994) and Modon (BIBRON & BORY DE SAINT-VINCENT, 1832).

Further, they added Patras, with reference to BURESCH & ZONKOV (1941: 223). This last

reference originates back from WERNER (1898); however, this author had in fact written (see

WERNER, 1899: 16): “Kryoneri, Arkananien, gegenüber Patras”. In doing so he clarified the

location of Kryoneri (a common toponym in Greece). Thus, only Kryoneri (nomos of

Arkanania) is a valid locality in this connection, and Patras has obviously been included by

mistake. The localities of Kalavryta, Kalogria and Kertezi are situated in the north-northwest

of the Peloponnese, in the nomos of Achai: Akhaia]. Didyma (northeast: in Argolis) has

a degree of uncertainty as the record is entirely based on eggs which were impossible to

identify properly. Likewise Methoni (southwest: in Messenia) has not been confirmed since its

original mention (see above).

1. About Triturus alpestris in Greece, see BREUIL & PARENT (1988a-b) and BRINGSOE (1994).

Source : MNHN, Paris

BouR, BRINGSOE & VANDERHAEGE 69

As for the Atlas of Amphibians and Reptiles in Europe (GaAsc et al., 1997: 88), on one hand

it depicts the Peloponnese almost completely covered with dots of recent presence (observa-

tions after 1970; one dot corresponds to a grid of 50 x 50 km), and absence being only

conspicuous for the eastern “finger”” (the Monemvassia area); on the other hand, the islands

of Kefallinia and Zakinthos are also covered, unlike Lefkas (fig. 1). However, the sources for

such a comforting distribution have not been published. Patrick Haffner, who participated in

the elaboration of this Ar/as, and especially in the collecting of data, has clarified to us

Fig. 1. - Southern Greece including the Peloponnese. Localities in the peninsula mentioned in the text

where the presence of Zriturus vulgaris is or was established, in chronological order: (1) Methoni

(1829-1831); (2) Kalavryta (1936); (3) Didyma (1980): (4) Kalogria (1985); (5) Kapsia (1987): (6)

Kertezi (1994); (7) Gythion (2001). The stars mark the new localities; dots indicate other localities

which have previously been published. The map in the inset shows the range of Triturus vulgaris

(large dots) according to GAsc et al. (1997: 88). Two previously published loc: mall diamonds)

were omitted in this map: the island of Lefkas (Lefkada), although the presence of the newt was

mentioned since 1938 (see SoriRoPouLoset al., 1995: 26), and the old locality of Methoni (Modhon).

We reject this distribution map (see text).

Source : MNHN, Paris

70 ALYTES 20 (1-2)

(personal communication, 15.X.2001) that the set of these “filled grids”” was supplied by

Sofianidou, but that the original data are retained with her. It is highly regrettable that no

document (publications, pictures or voucher specimens for example) authenticates such

findings, and we are unaware of the precise basis for selecting these Peloponnesian “localities”?

for T. vulgaris, which, in our opinion, makes the Atlas unreliable (on this subject read the

detailed criticism by Dugois, 1998). Therefore, nothing allows us to accept this new distribu-

tion of the smooth newt on the Peloponnese, and we reject it, awaiting possible clarification

and documentation. Heinz Grillitsch (personal communication, 16.X.2001) pointed out that

the same questions can be also asked, and for the same reasons, about the distribution of

Pelobates syriacus Boettger, 1889 on this peninsula.

RECENT OBSERVATIONS

Since 1978, one of us (H. B.) has made regular field excursions on the Peloponnese, with

the aim to clarifying eco-ethology and chorology in terms of herpetology. On April 23, 1987,

he discovered a population of Triturus vulgaris graecus (two males and three females ob-

served; fig. 2b) in the vicinity of Tripoli [= Tripolis, Arcadia], more exactly 4 km southeast of

Kapsia [= Kapses, Kapsas, Kapsias; i.e. approx. 10 km north of Tripoli; altitude approx. 680

m)], but this discovery has so far not been published. The environment consisted of some big

ponds, situated in pastures, olive groves and other kinds of arable fields (fig. 2a). Among

syntopic species, he noticed Rana cf. ridibunda Pallas, 1771*, Hyla arborea (Linnaeus, 1758),

Pelobates syriacus balcanicus Karaman, 1928 (a large tadpole) and Emys orbicularis hellenica

(Valenciennes, 1832). In the very nearby terrestrial habitat, Testudo hermanni boettgeri

Moijsisovics, 1889, Podarcis taurica ionica (Lehrs, 1902) and Malpolon monspessulanus à

gnitus (Geoffroy, 1829) were recorded as well. The same observer returned to this locality on

April 25-26, 1994, but his attempts to find 7: vulgaris by sweeping a net in the water were in

vain. However, a third visit (April 18, 2001) proved successful: after considerable searching

one male and two females were found. It is possible that the low number of specimens found

in the water was due to the relatively late time of spring regarding each of the three years. This

is the first mention of the presence of the smooth newt on the Central Peloponnese. The new

locality is situated roughly halfway between Kalavryta and Didyma.

During fifteen trips of one to three weeks duration to the southern Peloponnese, spread

over ten years, and dedicated primarily to the study of populations of Testudo weissingeri

Bour, 1995, the two other authors (R. B. & M. V.) carried out herpetological investigations in

a variety of habitats in the northern part of the area called Mani, especially inside a triangle

joining Kalamata, Areopoli and Gythion [= Yithio]. During these investigations, more than

2. Sofianidou published in the same period à *’check-list” of the tetrapods of Greece (SOFIANIDOU,

1996), where this sp is only briefly mentioned in the text; maps have only been arranged for two other

Greek ies of the genus Triturus, T alpestris (Laurenti, 1768) and T. karelinii (Strauch, 1870), whereas

T. carnifex (Laurenti, 1768) has been entirely omitted from the publication. We can add that in this work,

the Peloponnesian distribution map of Lacerta gracca Bedriaga, 1886 is also 100 wide and that of

Chalcides ocellatus (Forsskäl, 1775) is by far 100 exten:

3. The taxon is probably Rana kurimuelleri Gayda, 1940, older subjective synonym of Rana balcanica

Schneider & Sinsch, 1992 (see Dumois & OHLER, 1995: 175).

Source : MNHN, Paris

BOUR, BRINGSGE & VANDERHAEGE 71

Fig. 2a. - Habitat of Triturus vulgaris graccus, 4 km southeast of Kapsia (north of Tripoli), altitude about

680 m. Taken on 18 April 2001 (photo Henrik Bringsoe).

Fig. 2b. - Male Triturus vulgaris graecus recorded 4 km southeast of Kapsia (north of Tripoli), 23 April

1987, Notice the tail filament and the unspotted lower margin of the tail fin (photo Henrik Bringsoe).

Source : MNHN, Paris

72 ALYTES 20 (1-2)

Fig. 3a. — View of the habitat where the young newts were discovered, 5 km west-southwest of Gythion,

the southernmost known locality for L vulgaris. The bed of the Zminos (invisible) stretches on the

left, the pond on the right: both are dried out. Taken on 1° October 2001 (photo Roger Bour).

Fig. 3b-c. - Young Zriturus vulgaris graecus found $ km west-southwest of Gythion, 1” October 2001

{photo Roger Bour).

Source : MNHN, Paris

BOUR, BRINGSOE & VANDERHAEGE 73

950 individuals of Testudo weissingeri were measured and marked, and isolated micropopu-

lations of “dwarf” Testudo hermanni Gmelin, 1789 were discovered. Additionally, the sand

boa Eryx jaculus (Linnaeus, 1758) proved to be much less rare than was previously thought

(see BRINGSOE, 1986), due to the observation, under favourable atmospheric conditions (warm

and wet weather), of more than fifty specimens (young and adults) within about 20 hectares

of light but stony soil, on two olive groves. Encountering tailed amphibians was on the other

hand exceptional. The fire salamander Salamandra salamandra (Linnaeus, 1758) was ob-

served in or close to mountain streams (torrents) of the Mt. Taygetos range. The southern-

most localities are the monastery of Agios Samouil (36°53°N, 22°17°E:; altitude approx. 750 m

and above; larvae and one adult), and the eastern slope of the Mavrovounia, in Agios

Pandeleimonas (36°54°N, 22°21'E; altitude approx. 1500 m; larvae).

However, during the latest field trip (September 20-October 10, 2001), a second urodele

species was found (on October 1), more precisely, four young of Triturus vulgaris (Linnaeus,

1758) in their terrestrial phase (total length approx. 35 mm; fig. 3b-c), most probably

belonging to the subspecies graecus (Wolterstorff, 1905). These newts were gathered, hidden

under a slab of about 30 X 50 cm in size, on the sloppy and wooded bank of a dried pond. No

more newts were found under other objects like rocks, tree stumps and various garbage. The

pond, about 20 X 40 m, extends along the small river named Zminos, flowing like an oued,

which runs down from the south of the Taygetos, and which feeds it with water by infiltration.

In spring, the water level reaches 100 to 150 em. This place is partly covered with hydrophilous

vegetation and trees, but it is used mainly as a rubbish dump, with many piles of garbage half

submerged during the wet season (fig. 3a). Crops extend into the surroundings. The herpeto-

fauna of this semi-aquatic habitat has so far been observed to also consist of Rana cf.

ridibunda Pallas, 1771 (see note above), Hyla arborea (Linnaeus, 1758), Emys orbicularis

hellenica (Valenciennes, 1832), Mauremys rivulata (Valenciennes, 1833) and Natrix natrix

persa (Pallas, 1814). In the surrounding terrestrial habitat, Eryx jaculus turcicus (Olivier, 1801)

and Testudo hermanni subsp. were also registered. The exact place of these observations is

situated between Nea Marathea and Agios Vasilios (36°45°N, 22°3l’E; altitude approx. 10 m),

roughly 5 km west-southwest of Gythion (Laconia). Unfortunately we have to add that this

place, as many others, is used as a dump for garbage, and that pumps feeding irrigation

networks are more and more wide-spread along the banks of the Zminos: the future of this

habitat and its fauna is therefore very questionable*.

DISCUSSION AND CONCLUSION

With these new records, in total seven localities inhabited by 7° vulgaris are known from

the Peloponnese (fig. 1): (1) Methoni (Messenia); (2) Kalavryti (Achaia); (3) Didyma (Argo-

lis); (4) Kalogria (Achaia); (5) Kapsia (Arca ; (6) Kertezi (Achaia); and (7) Gythion

(Laconia). Five of them were discovered during the last twenty years. Results are encourag-

4. More generally, the problem of water supply is going to arise more and more in the Peloponnese,

mostly in connection with the increasing development of these irrigation networks and catchments made

into rivers, mostly temporary, or straight into Springs.

Source : MNHN, Paris

74 ALYTES 20 (1-2)

ing, because it is a priori surprising to notice southern range extensions of an animal species

which depends on aquatic environments, in a region where aridity seems to progress at an

alarming rate, simply due to major destructions of the environment throughout Greece.

Several explanations, in part complementary, may be put forward to explain these

discoveries. It is likely that researchers as well as the searches are today more numerous and

more accurate. It should be kept in mind that 7: vulgaris leaves its breeding pond relatively

quickly, after egg-laying, to adopt a fully terrestrial life. The metamorphosed young return to

the water only after several years: in spite of the drying of ponds, puddles or ditches during

summer, this species still manages to survive such hostile environments. We may also postulate

that on the Peloponnese - i.e. the very south of its range — T: vulgaris most probably breeds

earlier in the year and thus leaves the water earlier than in the north, but that will need to be

properly documented. The phenology of 7! vulgaris in another southern range, the Izmir

region of West Turkey, has already been established: adults are aquatic from around Decem-

ber through April (SCHMIDTLER & SCHMIDTLER, 1967; contrary to ÔzErt, 1964, who extends

the aquatic phase up to June). We think it probable that the South Greek populations of T:

vulgaris exhibit a similar tempo of activity. That may explain why it was so difficult to record

the species in the water of the Kapsia locality at the end of April. More surprising is the fact

that T. vulgaris and T. alpestris were found to be abundant in the ditches at the Kertezi locality

on 17-18 May (BRINGSOE, 1994). For comparison, in Central Europe adult T vulgaris usually

leave the water in about late June to early July (NÔLLERT & NÔLLERT, 1992). Another possible

explanation for this apparent sporadic range involves a positive human action, i.e. a wilful

introduction, or as stowaway. For instance, the last found locality is not far from a sports

ground and is used as a garbage: this place is frequently visited. Finally, nocturnal activity of

the newts on the ground does not favour observation of individuals in their terrestrial phases.

Early April and earlier may be best to register T vulgaris.

Although 7! vulgaris may be more common on the Peloponnese than what is usually

believed, we expect that it exists in rather sparse and isolated populations. Generally, the

Peloponnese is very dry and seems to have relatively few and scattered suitable freshwater

habitats. For 7! vulgaris the landscapes of the Peloponnese will appear fragmented and it may

be difficult to colonise and re-colonise new habitats. Other amphibians like Hyla arborea,

Bufo bufo (Linnaeus, 1758), B. viridis Laurenti, 1768 and Rana ridibunda s. 1. are known to be

able to migrate over longer distances and are more mobile on land than T! vulgaris (see for

instance the individual species accounts in GÜNTHER, 1996). These four anuran species are

common and widely distributed on the Peloponnese and often breed in man-made habitats of

standing freshwater (BRINGSOE, 1986).

RÉSUMÉ

Les découvertes successives du Triton ponctué grec, Triturus vulgaris graecus (Wolter-

storff, 1905), dans le Péloponnèse, sont rappelées dans leur chronologie. Cette note précise

la répartition actuellement connue du Triton ponctué pour l’ensemble de la presqu'île et

révèle la présence de cette espèce dans le centre (environs de Tripoli, Arcadie) et le sud-

est (environs de Gythion, Laconie, localité la plus méridionale connue). La distribution

Source : MNHN, Paris

BoUR, BRINGSOE & VANDERHAEGE 75

présentée dans l’Atlas of Amphibians and Reptiles in Europe (GAsc et al., 1997), couvrant la

majeure partie de la péninsule, est rejetée car elle n’est pas étayée par des spécimens ou des

données précises.

ACKNOWLEDGMENTS

We warmly thank all the following people or institutions. In Greece, Kostas et Gioula Georgouleas,

from Kardamili, for their welcome and their help, especially during hard times, and George I. Handrinos,

from Athens, for his confidence and his support. In Austria, Heinz Grillitsch, from Vienna, and in France,

Patrick Haffner, from Paris, for their valuable information and suggestions in connection with the Atlas.

The field work was undertaken with permits (2001: permit # 103866/4506) delivered by the Ministry of

Agriculture (General Secretariat of Forests and Natural Environment) in Athens. The manuscript was

improved thanks to the thorough revisions by Michel Breuil and Alain Dubois (Muséum national

d'Histoire naturelle, Paris), by Jarmo Perälä (University of Bristol) and to the comments of the referees.

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Corresponding editor: Alain Dunots.

SCA 2002

Source : MNHN, Paris

Alytes, 2002, 20 (1-2): 77-90. 77

Origin and development of the vent tube

in two species of the genus Bufo

Dinorah D. ECHEVERRIA

Laboratorio de Vertebrados,

Departamento de Ciencias Biolôgicas,

Facultad de Ciencias Exactas y Natural

Universidad de Buenos Aires (1428),

Buenos Aires, Argentina

<echeverria@bg.fcen.uba.ar>

The vent tube of Bufo arenarum (medial configuration) and Bufo

fernandezae (dextral configuration) tadpoles is derived from the ectoder-

mal portion of the embryonic intestine exit. Ciliated epithelial cells provided

by the epidermal surface (skin) stay as proctodeal mark inside of the cloaca

during the larval development. The distal region of the embryo’s procto-

deum and larval epidermis contribute to form the definitive vent tube. The

presumptive intestinal exit is present at Gosner stage 19, the anatomical

cloaca is fully formed at stage 20 or early 21 (urodaeum and procto-

daeum). After the common features are completed in B. fernandezae, the

final configuration of the dextral vent tube becomes evident at stage 23 by

the formation of a fold on the right side of the ventral fin. At stage 25, each

type of vent tube takes its definitive shape and becomes functional. In both

cases, a similar tissue organization of the cloaca and vent tube was found.

For comparative purposes, the vent tubes of different types of larvae (1, 2

and 3 sensu OrroN, 1953) in stages 25-26, and with medial configuration,

were examined at least, by one of the techniques indicated. They showed

similar structural organization, among them and with the bufonids exam-

ined in this study; however, two layers of epithelial tissue separated by

mesenchyme were always present.

INTRODUCTION

Tadpoles’ vent tubes may have various configurations and may or not be associated with

the anterior portion of the ventral fin. This tube usually projects from the medial part of the

ventral body wall on the sagittal plane (ALTIG & JOHNSTON, 1989, MCDiARMID & ALTIG ,

1999). Modifications of the distal parts of the ventral and/or right wall eventually produce

tube that opens either parallel with (medial) or to the right (dextral) of the plane of the ventral

fin (AzriG & McDiarMib, 1999). The presence of such an extension for fecal transport is

unique to anuran tadpoles. This larval feature develops during late embryonic stages, it has no

adult derivates, and it atrophies at about the same time when the front legs emerge through the

operculum (TAYLOR & KoLLROS, 1946: DEL CONTE & SIRLIN, 1951; GALLIEN & HOUILLON,

1951; Van Dur, 1959; ECHEVERRIA, 1998).

Source : MNHN, Paris

78 ALYTES 20 (1-2)

HUETTNER (1948) described the cloaca of Rana as continuous with the rectum, and as

formed partly by endodermic and ectodermic (proctodaeum, sensu Gapow, 1887, fide VAN

Vux, 1959) tissues. Among bufonids, the formation of the proctodeal pit has been reported by

several authors (MARCHETTI, 1919; RONDININI, 1928; KAGAWA,1932; SCHECHTMAN, 1939, for

B. bufo, fide VAN Duk,1959) without comments about its relationship with vent tube

development.

In an attempt to supply the comparative morphological information required to evaluate

the assumption that the presence of two vent tube configurations for the same function does

not necessary mean different anatomical and/or histological features, I report on the ontogeny

of the vent tube and the tissues that give rise to the vent tube.

MATERIAL AND METHODS

A total of 100 embryos and tadpoles of Bufo arenarum and 20 of Bufo fernandezae were

used to study the internal and external development of the vent tube between GOsNER (1960)

stages 17 and 25. Embryos were preserved in buffered 10 % formalin; B. arenarum embryos

and larvae were fixed every 60 min. The specimens were examined with incident lighting and

with a scanning electron microscope (SEM), after critical-point drying and gold-palladium

coating. B. fernandezae specimens were reared in the laboratory for taking photographs in

vivo of the main changes of the vent tube development.

For light microscopic examination, tadpoles and embryos were dehydrated intact in an

alcohol series, embedded in parafin (56-58°C), sectioned in transverse, sagittal and frontal

sections of 4 or 6 ym, and stained with hematoxilin-eosin or Massons trichrome (MARTOJA &

MARTOJA-PIERSON, 1970). Histological terminology follows WELsH & STORCH (1976).

Pertinent drawings of the development were drawn with a camera lucida. For SEM observa-

tion, three tadpoles of B. arenarum (stages 27, 31 and 32) and four specimens of B. fernande-

zae (stages 23, 24, 25 and 26) were dissected to study the inner walls of the cloaca and vent

tube.

The description of B. fernandezae vent tube development will be done in short form to

explain differences from B. arenarum. For comparative purposes, I examined the vent tubes of

tadpoles of different types (ORTON, 1953) of larvae, in Gosner stages 25-26, of Xenopus laevis

(Orton type 1), Gastrophryne carolinensis (Orton type 2), Ascaphus truei (Orton type 3), at

least by one of the techniques described.

The term inner cloaca is used to indicate that region of the cloaca which is situated in the

pleuroperitoneal cavity.

Source : MNHN, Paris

ECHEVERRIA 79

RESULTS

THE MEDIAL VENT TUBE OF BUFO ARENARUM

The first external evidence of the formation of the exit part of the gut appears at stage 16

as an indistinct pit on the posteroventral margin of the body. This pit is the incipient

proctodeum. Ciliated epidermal cells occur in the wall of this depression (fig. la). Sagittal

sections show an ectodermic invagination on the posterior part of the embryo. There is no

lumen in the hind-gut region (fig. 1b).

At stage 18, there is a definite depression although the proctodeum remains closed. AI

cells have yolk platelets, and cellular limits are not clear because of these platelets. In addition

this epithelial cells have black pigment in the peripheral cytoplasm of their distal edges.

Proctodeal cells appear more darkly pigmented, and these cells have long cilia that project into

the lumen (fig. 1c). The cloaca sensu stricto is not yet formed. Opistonephric kidneys buds and

pronephric ducts are not evident posteriorly, although the pronephric ducts have begun

differentiation anteriorly.

By stage 19, this proctodeal pit is located slightly anterior to the beginning of the ventral

fin anlage (fig. 1d). During stage 19, the cloacal membrane persists, that separates the intestine

per se from the outside. Below the epidermis there are a few dispersed mesodermal cells. The

proctodeum is separated from the endoderm by a layer of tissues hardy defined that constitute

the “cloacal membrane” (ectoderm, endoderm, and poorly evident to absent mesenchyme)

(fig. le). The proctodeum cavity is funnel-like, without connection to the inside of the gut, it

is held by the dorsal part of the ventral fin anlage (fig. 1f). Cells still have many yolk platelets

that makes the delineation of individual cells difficult. Black pigment remains in these cells.

Atstage 20, the pronephric ducts finally connect to the distal part of the hind gut, and the

functional larval cloaca is formed. A constriction in the cloaca marks the point of union

between ectoderm and endoderm, and presence/absence of ciliated cells of the epidermis

mark the limit between both tissue sources (fig. 2a-b). The proctodeal epithelium is stratified,

composed of two layers of cuboidal to polyhedral cells that rest on a basal layer.

At stage 21, an incipient peritoneum is forming in the pleuroperitoneal cavity. Cellular

surface specializations of the intestine are absent. A ventral constriction develops, that marks

the posterior part of the ventral zone of the body (fig. 2c). As the constriction grows inward,

the vent cylindrical mass is more evident on the ventral side and separates from the body. The

inner part of the larval cloaca has been composed by the wrodaeum and part of the

proctodaeum, before the ventral fin began to grow, and the tadpole’s intestine became

functional.

By stage 22, the body and tail arc upwards slightly, and the vent opening occurs where the

ventral fin contacts the body. Mesenchymal cells grow between the tail muscles and the dorsal

wall of the proctodeum. The ventral fin grows at the expenses of the mesenchyme placed

below the tail muscles, and in continuity with the posterior margin of the external orifice of

the intestine (fig. 2d).

Source : MNHN, Paris

Fig, 1. (a) Scanning electron photomicrograph of the proctodeum pit, from a Gosner stage 17 embryo

of Bufo arenarum. Left lateral side view. Scale line: 100 ym. — (b) Sagittal section through the

proctodeum invagination of a stage 16 embryo of B. arenarum. ED, endoderm; P, proctodeum

Stained with haematoxilin-eosin. Scale line: 100 um. - (ce) Sagittal section through a stage 18 embryo

of B. arenarum. Cilia (SC) in the lumen of the proctodeum (P). Stained with haematoxilin-cosin.

Scale line: 100 um. - (d) Scanning electron photomicrograph of the proctodeum pit (P), from a stage

19 embryo of & arenarum. Left lateral side view. F, ventral fin anlage; SC, cilia, Scale line: 100 m.

(e) Sagittal section of the cloacal membrane in à stage 19 embryo of 8. arenarum. CM, cloacal

membrane; M, tail muscles, Stained with haematoxilin-cosin, Scale line: 100 um. - (D Cross section

of the proctodeal region in a stage 19 embryo of &. arenarum. Cilia in the lumen of the proctodeum

(P). FE, ventral fin; M, tail muscles. Stained with haematoxilin-cosin. Scale line: 100 um

Source : MNHN, Paris

ÉCHEVERRIA 81

of the embryonic cloaca; CC, ciliated cells: P, proctodeum. Stained with Ma

line: 100 um. — (b) Cross section of the proctodeal region of à stage 20 embryo of B. arenarum. CD,

endodermal cavity of the embryonic cloaca: E, epidermis; N, mesenchyme: P, proctodeum. Stained

with Massons trichrome. Scale line: 100 um. — (c) Sagittal section of the posterior intestine and

clouca of à stage 21 embryo of &. arenarum. €, clonca; HI, posterior intestine; LT, ventral

U, peritoneum trac ù sons trichromic. le line: 100 um. — (d)

nlage (V) of embryo of &. arenarum.

: ained with haematoxilin-

F, ventral fin: LT, ventral constriction: M, tail mu

eosin. Scale line: 100 ym.

s of the

Atstage 23, the only external evidence of the vent tube anlage is a cylindrical ma:

epidermis that includes the presumptive hind limb buds (fig. 3a). Viewed externally, this mass

is continuous with the skin of the body, and limb buds begin to separate from the vent

structure at early stage 23. The aperture of the vent tube is slightly opened. At the end of this

stage the limit between the body and the vent tube anlage is evident (fig. 3a). Ciliate cells are

Source : MNHN, Paris

Fig. 3. (a) Scanning electron photomicrograph of the vent tube (V) and leg (L) buds in early stage 23 of

B. arenarum. T, vent tube exit. Scale line: 100 wm. — (b) Scanning electron photomicrograph of the

vent tube (V) and the leg bud (L) in lateral view from stage 24 of B. arenarum. T, vent tube exit. Scale

line: 100 um. — (c) Scanning electron photomicrograph of the vent tube (V) from a stage 25 of B.

arenarum. B, body; F, ventral fin; L, leg bud: T, vent tube exit. Scale line: 100 4m. —(d) Cross section

of a stage 25 tadpole of B. arenarum. À, rectus abdominis muscle; B, body wa

posterior intestine. Stained with Massons trichrome. Scale line: 100 um. — (e) Sagittal s

distal part of the eloaca (C) and vent tube (V) of a stage 26 tadpole of B. arenarum. B, body wall; F,

ventral fin; H String: K, kidney: P, proctodeum zone: U, peritoneum. Stained with Massons

trichrome. ge 26 tadpole of B. arenarum. FW, fin wall:

ed a Messone tretiroie Sc le, line:

ittal s section of the el all of the dit p part of the rectum (RE) next to the clou ie of a

stage 26 B. arenarum. J, ciliated surface; W, nephric duct orifice. Stained with Massons trichrome.

Scale line: 50um

Source : MNHN, Paris

ECHEVERRIA 83

still present on the skin, the tail increases in length, and the ventral fin is well formed and

attached to the posterior margin of the exit orifice (fig. 3a). The vent tube anlage grows in

distal direction, forming its external tube, in expenses of the epithelial and mesenchymal cells

around it.

Atstage 24, the vent tube and limb buds are evident. The tube is conical, and the terminal

aperture, which may be oval or circular, is open. The vent tube is still blocked inside (fig. 3b).

At stage 25, the vent tube is fully developed and becomes functional. The aperture is cireular

and faces ventrally. The anterior edge of the ventral fin is connected to the posterior side of

the vent tube (fig. 3c). Transversal section of the posterior region of the tadpole’s body shows

that the cloaca arises between the rectus abdominis muscles (fig. 3d). They are attached to the

posterior wall of the tadpole’s body, and they are the only muscles next to the inner cloaca.

After its final organization in stage 25, the vent tube grows continuously. It grows during

the later stages in expenses of the epidermis and dermis (fig. 3e). Epithelial and mesenchymal

tissues of varying thickness are surrounding the vent tube cavity and form the ventral fin too

(g. 3). The epidermis has definitively lost the cilia at stages after 25, but the surface of the

proctodeum epithelia region has not (fig. 3g).

Several features in B. arenarum are important to be commented. The microvilli of the

intestine appear at stage 24, in the anterior gut and midgut. The epithelium of the rectum is

formed by a single layer of prismatic to cuboid cells with a low brushborder. Ciliated cells are

only found behind the place where the nephric ducts enter the cloaca (fig. 3h). The procto-

daeum tissues do not make structural changes, at least during stages that have been covered in

this study (17 to 32).

THE DEXTRAL VENT TUBE OF BUFO FERNANDEZAE

Atstages 19 to 21, the embryo develops the cloacal exit presumptive zone and the dorsal

and ventral fin buds (fig. 4a). At stage 22, in the posterior and ventral zone of the body, the

vent tube anlage is evident (fig. 4b). At stage 23, on the right side of the ventral fin next to the

body appears a fold, which holds the incipient vent tube (fig. 4c). At stages 24-25, the median

and distal part of the vent tube is formed. The tube takes it definitive shape and is functional

at stage 25. The configuration is dextral and marginal to the ventral fin (fig. 4d).

Histological preparations of the vent tubes of B. arenarum and B. fernandezae showed

that the last part of the alimentary tract (rectum and proximal part of the cloaca) runs on the

left side of the pleuroperitoneal cavity, arising with medial configuration between the rectus

abdominis muscles (fig. 34, 5a). In both medial and dextral tubes, the proximal part of the vent

tube is placed between both walls of the ventral fin (fig. 3f, 5b-c); medial and distal parts of the

vent tube of B. fernandezae are placed on the right wall of the fin, and are attached to its

ventral edge (fig. 5d-f).

The definitive vent tube in B. arenarum and B. fernandezae is composed of an inner layer

of cuboidal epithelial tissue, surrounded by an outer wall (epidermis on most lateral and

ventral sides) separated by mesenchyme of different thickness (fig. 3e-f, 5). This inner

epithelium contains secretory cells, and is partially covered by ciliated cells on it proximal

part, next to the inner clo:

Source : MNHN, Paris

84 ALYTES 20 (1-2)

External morphology of the vent tube (V) of Bufo férnandezae. Photographs taken in vivo. - (a)

e 21. Scale line = Imm. - (b) Stage 23. Scale line = Imm. - (c) Scanning electron microscope

graph of the vent tube anlage (arrow). Stage 24. Scale line: 100 um. — (d) Stage cale

line = Imm. - D, dorsal fin: F, ventral fin; V, vent tube.

Source : MNHN, Paris

ECHEVERRIA 85

Fig. 5.— Cross section of the posterior part of the body and tail of a tadpole of B. fernandezae. Stage 4.

(a) Cloaca in the interior se the peus critoneal cavity (G).—(b-d) Median region of the vent tube.

le line: 300 m. À, rectus abdominis mu B, body wall: CI,

HI, posterior intestine; L, posterior leg buds: M, tail muscl

ons trichrome, Scale line: 300 um

Source : MNHN, Paris

86 ALYTES 20 (1-2)

Cloacas of B. arenarum and B. fernandezae tadpoles dissected after the critical point

procedure and observed by SEM confirmed that the ciliated cells are present in the distal

portion of the inner cloaca and in the proximal part of the vent tube. Ciliated cells are absent

on the distal wall of the vent tube after stage 26 (fig. 6a-c). In stage 25, microvilli of the surface

of the intestines next to the cloaca are low and continuous (fig. 6c). In intestines full with food,

the brushborder is more evident and dense than in the rectum and in the proximal part of the

inner cloaca.

pe microphotograph of a dissected stage 32 tadpole of B.

arenarum. EC, region of plane epithelium in the inner cloaca; GC, region with ciliated epithelium of

the proctodeum:; K, kidney; RE, hind intestine or rectum: $, skin; V, vent tube; W, nephric duct

orifice; Z, parietal peritoneum. White scale line: 1 mm. — (b) Detail of the distal margin of the

internal wall of vent tube with smooth sur! in a stage 32 tadpole of B. arenarum. White scale line:

0,1 mm. - (c) Detail of the surface of the cloacal epithelium. EC, region of plane epithelium in the

inner cloaca: FA, artifact: GC, region with ciliated epithelium of the proctodeum. White scale line:

10 um.

Fig. 6. — (a) Scanning electron micro

Source : MNHN, Paris

ÉCHEVERRIA 87

The larval cloaca of these tadpoles, could be “divided” in two anatomical parts,

urodaeum and proctodaeum. Urinary bladders are not formed earlier than at stage 32. The

region of the larval cloaca into which the nephric ducts open (wrodaeum) is endodermal. The

following region of the cloaca is ectodermal (proctodaeum) (fig. 3h).

Concerning the vent tube organization in the larvae of Xenopus laevis (type 1), Gas-

trophryne carolinensis (type 2) and Ascaphus truei (type 3), two layers of epithelial tissue

separated by mesenchyme were always present. The external layer corresponds to the skin of

the ventral fin (stratified epithelium), the internal layer to the inner wall of the vent tube

(simple cuboidal epithelium). The vent tube grows in centrifugal direction from the body wall

backwards, and develops its definitive configuration.

DISCUSSION

From the results of this study, the term vent tube deserves to be analysed. The posterior

opening of the gut in anuran larvae was given several names, such as anus (HUETTNER, 1948),

anal tube (INGER, 1985; CAMPBELL & CLARKE, 1998), anal opening (Cet, 1980), cloacal tube

(ECHEVERRIA & FioriTO DE Lopez, 1981), vent tube (ALTIG & JOHNSTON, 1986) or proctodeal

tube (LAvVILLA & LANGONE, 1991). The external tube is a structure formed from the epidermis

as the larva grows. It is connected to the cloaca, and it could be considered a part of the cloaca

of the embryo, specifically of the embryo proctodeum, an ectodermic structure. Vent tube can

be interpreted, in two ways: (1) as a prolongation of the proctodeum at the expense of the

ventral body skin, forming a tube from early stage 23 to the final 25, and (2) as an external tube

formed just from the posterior edge of the body wall, specifically from the ventral and lateral

epidermis that forms the ventral fin too. This second view is based on the tissues from which

the vent tube has started its development.

However, the external tube involves two kinds of epidermal tissues in the definite vent

tube: original proctodeal material (parts of the inner wall) and epithelial tissues grown a

posteriori (in inner and outer walls). MCDiARMID & ALTIG (1999) assumed the vent tube to be

a prolongation of the abdominal skin. This could be a wider interpretation enclosed in the

second case. The inner wall of the vent tube rises from the epithelial tissue attached to the

margin of the distal cloacal area. It is surrounded by the skin (epidermis and dermis) that

forms the outer wall. The connective tissue grows in width, and becomes more evident

between both epithelia (fig. 7). On the basis of natomy, perhaps better names for the tube

projected from the body wall for excreting feces could be at first sight proctodeal tube, cloacal

tube or vent tube. Proctodeal tube is restrictive only to a part of the cloaca, and it should not

be considered as a prolongation of the original proctodeum because it has a different tissue

composition. The term cloacal tube makes references to the functions and could be used in

opposition to the functional connotation that anal tube has. The term vent tube is probably

the best, it is a general term with no developmental connotation, unique to tadpoles, that

could be better used by English speakers.

The vent tube is functional by stage 25. Its inner wall is partially covered by ciliated and

secretory cells, that may probably contribute to the joining of feces into a string of intestinal

Source : MNHN, Paris

88 ALYTES 20 (1-2)

hematic representation of a dissected cloaca (C) and vent tube (V) of a tadpole. À, rectus

abdominis muscle: C, cloaca; D, dorsal fin; E, epidermis; F, ventral fin; M, tail muscles: N, loose

connective (mesenchyme); ND, nephric duct: P, proctodeum: RE, hind intestine or rectum: T, vent

tube exit; U, peritoneum; UO, urodaeum; V, vent tube; W, nephrie duct orifice.

particles before they are excreted. No traces of muscles are found around the wall of the vent

tube. The rectus abdominis muscle that is attached to the posterior wall of the body, next to the

inner cloaca, has been studied by Carr & ALTIG (1992) in several tadpoles. These authors

assume that this muscle could stabilize the abdomen and spiracular wall in suctorial tadpoles.

Furthermore, contraction of this muscle could indirectly reduce the inner cloaca lumen, by

compression. The compression over the lateral walls of the inner cloaca could help to remove

part of the fecal string when it reaches the exterior.

Different cell specializations (brushborder and microvilli), formed after stage 24, are

detected only in the intestines and are absent in the larval anatomical cloaca. Ciliated cells of

the cloaca have their long cilia oriented to the posterior end of the body. They probably help

to produce a current which conveys mucus and fecal particles through the cloaca, or they

contribute to organize the fecal string before it leaves the vent tube.

No structural differences were found in the vent tube of bufonid tadpoles studied in this

work. Intentionally, several tadpoles representing different anatomical and ecomorphological

types, sensu ALTIG & JOHNSTON (1989) (suctorial tadpole, Ascaphus truei, and suspension

feeders, Xenopus laevis, Gastrophryne carolinensis and Elachistocleis bicolor), carrying medial

Source : MNHN, Paris

ECHEVERRIA 89

vent tubes, were examined. They showed similar structural organization based on epidermis

and dermis. Probably this result suggests that vent tube configuration could have a taxonomic

rather than ecomorphological significance.

RESUMEN

El tubo cloacal de las larvas de Bufo arenarum y Bufo fernandezae deriva de la porciôn

ectodérmica de la abertura intestinal embrionaria. Células epiteliales perduran como indica-

doras del origen ectodérmico del proctodeo, permaneciendo en el interior de la cloaca

durante todo el desarrollo larval. La regiôn distal del proctodeo y de la epidermis larval

contribuyen a formar el tubo cloacal definitivo. En el estadio 19 slo estä presente la abertura

presuntiva del intestino; la cloaca larval se conforma en el estadio 20 o al inicio del 21. En el

estadio 25, el tubo cloacal es funcional. Se examinaron con menor detalle espcimenes de

larvas con tubo cloacal medial de varios tipos (larvas tipo 1, 2 y 3) mostrando una organiza-

ciôn tisular similar a los resultados obtenidos de la cloaca y del tubo cloacal de los bufénidos

estudiados.

ACKNOWLEDGMENTS

Lam most grateful to the mentor of this research, Dr. Ronald Altig (Mississippi State University); to

Ronald Heyer and Roy McDiarmid (Smithsonian Institution), who provided the specimens of Ascaphus

trueï: to Dr. Graciela Guerrero (Embryology Laboratory, Buenos Aires University), for comment:

10 Mr. Dante Jimenez (SEM Service of Centro de Investigaciones Técnicas de las Fuerzas Armadas), for

technical assistance. Special thanks to the University of Buenos Aires Board that gave me financial

support to make the trip to Mississippi State University (Expte. N° 931/1996), the place where I started

this research.

LITERATURE CITED

ALTIG, R. G. & JounstoN, G. F., 1986. - Major characteristics of free-living anuran tadpoles. Smithso-

nian herp. Inf. Serv., 67: 1-75.

— 1989. — Guilds of anuran larvae:

habitats. Herp. Mon., 3: 81-109.

CamPeLz, 3 À & CLARKE, B. T., 1998. - A review of frogs of the genus Orophryne (Microhylidae) with

the description of a new species. Herperologica, 54

Carr. K. M. & ALTIG, R., 1992. - Configurations of the rectus abdominis of anuran tadpoles. / Morph.,

214: 351-356.

Cüt, J. M. 1980. — Amphibians of Argentina. Monit. cool. ital., Mon, 2: i-xi + 1-609

& SiRLIN, JL L.. 1951. - Serie tipo de los primeros estadios embrionarios en Bufo arenarum

vol. Lilloana, 12: 495-500.

relationships among developmental modes, morphologies and

rrollo larval de Melanophrynis-

à del érgano de

Bidder. A/vres, 15 (4 170.

Source : MNHN, Paris

90 ALYTES 20 (1-2)

EcHeverkia, D. D. & FioriTo DE Lôpez, L. E., 1981. - Estadios de la metamorfosis en Bufo arenarum

(Anura). Physis, (B), 40 (98): 15-23.

GaboW, H., 1887. - Remarks on the cloaca and copulatory organs of Amniota. Philos. Trans., 178: 5-37.

GALLIEN, L. & HOUILLON, C., 1951. -Table chronologique du développement chez Discoglossus pictus.

Bull. Biol., 85 (4): 373-378.

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

identification. Herpetologica, 16: 183-190.

HUETTNER, A. F, 1948. — Fundamentals of comparative embryology of the vertebrates. New York,

Macmillan Company: i-xiv + 1-414.

INGER, R. F,, 1985. - Tadpoles of the forested regions of Borneo. Fieldiana: Zool., 26: 1-89.

KaAGAWA, T., 1932. - Über die Ausbildung des Afters und des Canalis neurentericus bei Bufo vulgaris

japonicus. Okayama Igk., 44: 2405-2418.

LaviLLa, E. O. & LANGONI A., 1991. - Ontogenetic changes in the spiracular and proctodeal tube

orientation in Elachistocleis bicolor (Anura: Microhylidae). J Herp., 25: 119-121.

MARCHETTI, L., 1919. — Sul destino del blastoporo durante la formazione del Canalis neurentericus e del

Proctodaeum nel Bufo vulgaris. Arch. ital. Anat. Embriol., 17: 216-238.

MARTOIA, R. & MARTOJA-PIERSON, M., 1970. — Técnicas de histologia animal. Barcelona, Torray-Masson:

1-350.

McDiakMID, R.W. & ALTIG, R., 1999. — Tudpoles. The biology of anuran larvae. Chicago, Univ. Chicago

Press. i-xiv + 1-444.

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

RONDININI, R., 1928. — Particolarità formative in alcuni organi primitivi e sviluppo della coda nelle larve

di Bufo vulgaris. Arch. ital. Anar. Embriol., 25: 98-130.

ScHscHrMan, À. M., 1939. - Experiments on anus formation in a frogegg. Proc. Soc. exp. Biol., 41: 48-49.

TayLoRr, A. C. & KOLLROS, J., 1946. — Stages in the normal development of Rana pipiens larvae. Anat.

VAN Duk, D. E., 1959. - On the cloacal region of Anura, in particular of larval Ascaphus. Ann Univ

Stellenbosch, 35: 169-249.

WELsH, U. & SrorCH, V., 1976. - Comparative animal cytology & histology. London, Sidgwick & Jackson:

i-xiv + 1-343.

Corresponding editor: Heinz GRILLITSCH.

Source : MNHN, Paris

Alytes, 2002, 20 (1-2): 91-92. Book review

Honduran amphibians

Jean-Christophe DE MASSARY

Muséum national d'Histoire naturelle,

Laboratoire de Conservation des Espèces animales,

57 rue Cuvier, 75005 Paris, France

<massary@mnhn.fr>

James R. MCCRANIE & Larry D. WiLsON. — The amphibians of Honduras. Ithaca, New York, USA,

SSAR Contribution to Herpetology 19, 2002: i-x + 1-625, 20 plates with 154 colour photos, 67 b&w

figures, 33 tables and 58 maps. US $ 60.00. Hardbound. ISBN 0-916984-57-5.

The book of James R. MCCRANIE and Larry D. WILSON deals with the Amphibians of Honduras.

This is the nineteenth item of the great series Contribution to Herperology published by the Society for the

Study of Amphibians and Reptiles (SSAR). The authors transmit us very methodically the result of more

than 30 years of field work spent in one of the less known countries of Middle America.

After a brief introduction where are given the intention and the architecture of the book, a detailed

material and methods part is given.

The first chapter of the book allows us to get a very good insight of the Honduran environment

through fourteen pages (p. 13-26). Data are provided on geography (main regions, rivers, relief, etc.),

climates and vegetation. The following chapter provides a brief history of amphibian studies in Hondu-

ras: the authors relate how our knowledge on the Honduran herpetofauna grew little by little thanks to

the scientific trips that occurred from the nineteenth century.

The following chapter (p. 35-87) consists of dichotomous keys: keys for orders, genera and species

were elaborated; they are illustrated by many figures and are provided both in English and Spanish. These

Keys allow to identify not only adult specimens but also tadpoles, alive or preserved.

The next chapter, titled Sysremaric accounts, is the most voluminous part of the book (p. 89-499). A

presentation of the nine families of amphibians occurring in Honduras is given. Systematic references,

range, content and etymology are presented for each genus name. An important amount of data is

provided for each species through diflerent sections: list of synonyms, range, diagnosis, description of

adults and tadpoles, illustrations, remarks (mostly in systematics), ecological distribution and natural

history comments, etymology, specimens examined, and other records. Let us note that there is no section

devoted to the call descriptions. In fact, the authors explained (p. 10) that they have few data in this

so that they just gathered the existing data of the literature and included them in the natural

history comments. Many distribution maps are given, where the localities are accurately indicated by

dots.

Twenty colour plates with good photographs come just after the systematic accounts. Both the

habitats (24 photographs) and the amphibians (130 photographs) are presented.

The three following pages (p. 501-503) deal with the possible or doubtful occurrence of several

amphibians species in Honduras. With regards to the amphibian species oceurring in the vicinities of

Hondu the authors indeed think that seven further species should occeur in that country. Conv

the occurrence of one frog species (Hyla crepitans Wied-Neuwied, 1824) is questioned.

Source : MNHN, Paris

92 ALYTES 20 (1-2)

Through the two following short chapters, the authors analyse the reproductive modes and guild

structures. The guild structures are taken into account for both adults and tadpoles.

Then, two chapters are devoted to environment and amphibian conservation in Honduras. In the

first one, the authors recall the major causes of extinction and insist on the fact that three of them are due

to human overpopulation. Given a high birth rate in Honduras, like in many other countries of Middle

America, the authors consider different scenarios of the environmental impact of human population for

the future. In the second one, they estimate by an interesting “environmental vulnerability scores” (EVS)

which amphibian species are prone to extinction. On the basis of the EVS they obtained for each

amphibian species, they discuss the efficiency of the existing system of Honduran biotic reserves in

protecting the amphibian fauna. A new plan of action to restrain environmental damage to these animals

is proposed.

After a two pages Spanish summary, a glossary, where 176 unfamiliar words are defined, is available,

which will be very useful to all amphibian non-specialists.

The next part is a gazetteer (p. 553-578): details are given for 699 localities (including misspellings

and various spellings of localities found in previous works). À map (p. 554) with 80 selected localities

indicated by dots is also provided.

The gazetteer is followed by a list of 658 references (p. 579-610), including as well ancient books or

papers of the previous centuries, as the most recent papers dealing with molecular phylogeny.

Finally, two indices are provided, one to the scientific names (p. 611-619), and another one to the

authors’ names (p. 619-625).

This book is well done and contains the largest quantity of data ever gathered on Honduran

amphibians so far. It is not only a simple updated systematic list of animals with a key and some

well-referenced details about their biology and biogeography, it is also an important tool of investigation

for the amphibian conservation in Honduras. Such a work is a model of what should be done, among

other things, to tackle the animal conservation problems on a sound foundation. I strongly recommend it

without any reserve to all people interested in the Middle-America herpetofauna and in animal conser-

vation.

Source : MNHN, Paris

AIN7TTES

International Journal of batrachology

published by ISSCA

EDITORIAL BOARD

Chief Editor: Alain Dupois (Laboratoire des Reptiles et Amphibiens, Muséum national d'Histoire naturelle,

25 rue Cuvier, 75005 Paris, France; <dubois@mnhn.fr>).

Deputy Editor: Thierry LODÉ (Laboratoire d'Ecologie animale, Université d'Angers, 2 boulevard Lavoisier,

49045 Angers Cedex, France; <thierry-lode@univ-angers.fr>).

Conservation Editor: Stephen J. RicHaRps (Vertebrates Department, South Australian Museum, North Terrace,

Adelaide, S.A. 5000, Australia; <Richards.Steve@saugov.sa.govau>).

Editorial Board: Franco ANDREONE (Torino, Italy); Lauren E. BROWN (Normal, USA); Janalee P. CALDWELL

(Norman, USA); Ulisses CARAMASCHI (Rio de Janeiro, Brazil); Günter GOLLMANN (Wien, Austria); Heinz

GLLrrsCH (Wien, Austria); Tim HALLIDAY (Milton Keynes, United Kingdom); W. Ronald HEYER

(Washington, USA); Esteban O. LAVILLA (Tucumän, Argentina); Karen R. Lips (Canton, USA); Masafumi

Marsur (Kyoto, Japan); Donald F. MCALPINE (Saint John, Canada); Alain PAGANO (Angers, France); John

C. PoynToN (London, England); Miguel VEeNcEs (Konstanz, Germany).

Technical Editorial Team (Paris, France): Alain Durois (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,

acknowledgements, literature cited, appendix.

Figures and tables should be mentioned in the text as follows: fig. 4 or tab 4. Figures should not exceed 16 x

24 em. The size of the lettering should ensure its legibility after reduction. The legends of figures and tables

should be assembled on a separate sheet. Each figure should be numbered using a pencil.

References in the text are to be written in capital letters (BOURRET, 1942; 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. Hanoi, Institut Océanographique de l’Indochine: i-x + 1-547,

pl. L4.

Graf, L-D. & PoLLs PeLAZ, M., 1989. - Evolutionary genetics of the Rana esculenta complex. In: R.. M. DAWLEY

& 1. P. BoGarr (ed.), Evolution and ecology of unisexual vertebrates, Albany, The New York State Museum:

289-302.

INGER, R. E, Voris, H. K. & Voris, H. H., 1974. - Genetic variation and population ecology of some Southeast

Asian frogs of the genera Bufo and Rana. Biochem. Genet. 12: 121-145.

Manuscripts should be submitted in triplicate cither to Alain DuBois (address above) if dealing with

amphibian morphology, anatomy, systematics, biogcography, evolution, genetics, anomalies or developmental

biology, or to Thierry LODÉ (address above) if dealing with amphibian population genetics, ecology, ethology or

life history, or to Stephen J. RICHARDS (address above) if dealing with conservation biology, including declining

amphibian populations or pathology. Acceptance 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 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 10 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% 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, 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 Publication: Alain DUBois.

Numéro de Commission Paritaire: 64851.

PRE Source : MNHN, Paris:

Alytes, 2002, 20 (1-2): 1-92.

Contents

Mark-Oliver RÔDEL, Daniel KRÂTZ & Raffael ERNST

The tadpole of Prychadena aequiplicata (Werner, 1898)

with the description of a new reproductive mode for the genus

tämphibia, Anura, Ranidae) Pen. Meter an cr 1-12

Alan CHANNING, David C. MoyEr & Kim M. HOWELL

Description of a new torrent frog in the genus Arthroleptides

from Tanzania (Amphibia, Anura, Ranidae) ........................... 13-27

Axel KWETr & Ariadne ANGULO

A new species of Adenomera (Anura, Leptodactylidae)

from the Araucaria forest of Rio Grande do Sul (Brazil),

with comments on the systematic status

ORSOUHÉIPOPUAUONS ONLINE BEBUS 2. he. 2 en 28-43

L. CHiLLASSE, M. Dakki & M. THÉVENOT

Régimes alimentaires de deux espèces de Bufonidae

(Bufo bufo spinosus et Bufo mauritanicus)

abac A Dtelmant A esZz4 (Maroc) sf. Rene eee 44-54

Brandon P. ANTHONY

Results of the first batrachian survey in Europe using road call counts .. 55-66

Roger Bour, Henrik BRINGS6E & Maurice VANDERHAEGE

Triturus vulgaris (Linnaeus, 1758) at its southern limit:

distribution on the Peloponnese, Greece, with range extensions

from the Central and South Peloponnese ............................. 67-76

Dinorah D. ECHEVERRIA

Origin and development of the vent tube in two species of the genus Bufo . 77-90

BOOK REVIEW

Jean-Christophe DE MASSARY

HODOUFANAMPhIDIANS Me eee ee tee 91-92

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: 4 trimestre 2002.

Source : MNHN, Paris: