International Society for the Study

and Conservation of Amphibians

(International Society of Batrachology)

SEAT

Laboratoire des Reptiles et Amphibiens, Muséum national d'Histoire naturelle,

25 rue Cuvier, 75005 Paris, France

BOARD FOR 1991

President: Raymond F. LAURENT (Tucumän, Argentina).

General Secretary: Alain Duois (Paris, France).

Treasurer: Dominique PAYEN (Paris, France).

tant Secretary, Europe: Günter GOLLMANN (Wien, Austria).

tant Treasurer, Europe: Annemarie OHLER (Paris, France).

tant Secretary, outside Europe: David B. WAKE (Berkeley, U.S.A.).

istant Treasurer, outside Europe: Janalee P. CALDWELL (Norman, U.S.A).

Other members of the Board: Jean-Louis FISCHER (Paris, France); David M. GREEN (Montreal,

Roy W. McDiarmin (Washington, U.S.A.); James I. MENZIES (Boroko, Papua New

a), Richard WaAssERSUG (Halifax, Canada).

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Source : MNHN, Paris

AINTTES

INTERNATIONAL JOURNAL OF BATRACHOLOGY

September 1991 Volume 9, N° 3

Alytes, 1991, 9 (3): 61-69. 6l

Predator-prey relationship between

giant water bugs (Belostoma oxyurum)

and larval anurans (Bufo arenarum)

que Centrale Muséum

es ||

Buenos Aires, Argentina

The relationship between an invertebrate predator (Belostoma oxyurum,

Hemiptera, Belostomatidae) and its prey (Bufo arenarum, Anura, Bufonidae)

was analyzed experimentally. Both species were collected in a small semi-

permanent pond near Buenos Aires, Argentina. In replicated trials, tadpoles of

three developmental stages were held at five densities and offered to

individual predators of three developmental stages representing several

predator sizes. We analyzed the effect of prey stage and size, predator stage,

and prey density on the proportion of eaten tadpoles. Predation rate (indi-

viduals consumed / predator.time) was higher on smaller preys, except at the

highest prey density, independent of predator size and stage. At large prey size,

the predation rate was higher for adult water bugs than it was for immature

water bugs. The predation rate was low at the highest prey density tested (32

individuals), particularly when the smallest preys were offered to one adult

giant water bug.

Larval amphibian population structure has been regarded to be greatly influenced by

intraspecific competition, particularly where density-dependent differential growth rate

causes unequal competitive abilities among amphibian larvae (SMITH-GiLL & GiLL, 1978;

WiLBUR, 1980). However, predation can be more important than intraspecific competition

in regulating anuran populations and communities (CRuMP, 1984). Furthermore, tadpole

differential growth rates also affect predatory impact upon them, especially if predators

display size preferences among their preys (BRODIE & FORMANOWICZ, 1983; SEMLITSCH &

GiBBoNS, 1988).

It is frequently observed that anurans colonize ephemeral as well as semi-permanent

lentic environments, which usually lack efficient piscine predators on their larvae (e.g.,

GRUBB, 1972). However, improvement in survival associated with this behavior could be

counterbalanced by the mortality inflicted by the abundant predaceous insects commonly

detected in this kind of limnotope (BROCKELMAN, 1969; CALDWELL et al., 1980; CALEF,

1973; CRONIN & TRAVIS, 1986; CRUMP, 1984; FORMANOWICZ & BRODIE, 1982; HEYER et

al., 1975; KEHR & BASso, in press; SMITH, ,198, 4

F°

Source : MNHN, Paris

62 ALYTES 9 (3)

In contrast to piscine predation, the success of predatory insects is strongly limited by

the size of potential preys. Beyond a certain maximum size tadpoles may become

invulnerable to insect predation. Therefore, an increase in the prey growth rate can be a

selective advantage (TRAvIS, 1983; Travis et al., 1985). In particular, as tadpoles become

larger, they become invulnerable to predatory attacks by odonate naiads (BRODIE &

FORMANOWICZ, 1983; HEYER & MUEDEKING, 1976; HEYER et al., 1975; PRITCHARD, 1965)

and adult Belostoma sp. (BRODIE & FORMANOWICZ, 1983). A4eschna naiads, however, are

able to capture and kill all stages of Hyla pseudopuma offered (CRUMP, 1984).

The size limitation of insects that prey on larval amphibians has been a matter of

controversy during the last decade. CALDWELL et al. (1980), for example, suggested that

dragonfly naïads Anax junius are not size limited, since they can hold on to large struggling

prey of Hyla gratiosa. Conversely, BRODIE & FORMANOWICZ (1983) stated that Belostoma

sp. and À. junius of all tested sizes killed and consumed more small tadpoles than large

ones, whereas Lethocerus sp. exhibited no preference for prey size (30-38, GOsNER, 1960).

Small tadpoles may be able to avoid insect attacks by being unpalatable. Bufo

americanus, for example, has been regarded as unpalatable, not only to sucking (Belostoma

sp.) and chewing (A. junius) invertebrate predators, but also to vertebrate predators

(BRODIE & FORMANOWICZ, 1987). Previously, WASsERSUG (1973) postulated that

unpalatability was not an effective strategy for amphibians to reduce predation by

invertebrate predators which suck body fluids.

Another prey benefit can be attained by aggregation (BRODIE & FORMANOWICZ, 1987).

The several proposed mechanisms include the “confusion” of predator to select individual

prey from an aggregation (MiLiNski, 1979; TREHERNE & FOSTER, 1981).

Some of the above ideas were tested experimentally with a predator-prey system

composed of giant water bugs and larval anurans. Giant water bugs are conspicuous

insects that inhabit lentic environments where they are important predators upon anuran

populations. À predator (Belostoma oxyurum, Hemiptera, Belostomatidae) and a prey

(Bufo arenarum, Anura, Bufonidae) species were selected to evaluate the following

factors : (1) the influence of the size of the predator and prey on their interactions ; (2) the

effects of prey density on predation rate ; and (3) the existence or non-existence of a prey

size threshold for water bug predation.

METHODS

THE TEST SPECIES

Geographically, B. oxyurum is one of the more restricted species among the South

American belostomatids. It occurs in the southern portion of the “Mesopotamia” and

along most of the oriental border of the Pampasic Dominion (RINGUELET, 1961), in

Argentina.

In the area where the tested B. oxyurum specimens were captured, giant water bugs

are multivoltine. Only fifth instar nymphs and adults overwinter. First instar nymphs hatch

Source : MNHN, Paris

KEHR & SCHNACK 63

from overwintering incubant males by the beginning of spring, and they reach the adult

stage in about fifty days (Domizi et al., 1978). Females of Belostoma, as well as other

genera of the Belostomatinae, glue their eggs on the dorsum of males, who carry and care

for them until they hatch (MENKE, 1979).

AI five nymphal instars and adults of B. oxyurum, like other species of belostomatids,

are efficient predators. Their “sit-and-wait” predatory tactic (SCHOENER, 1969) is

non-selective, i.e. the predator usually lies in ambush for occasional prey. The ability of

giant water bugs to make successful attacks is due to their strength, tenacity, and the

paralyzing effect of the toxin injected by these sucking predators to subdue prey (PICADO,

1937; DE CARLO, 1959; MENKE, 1979).

Bufo arenarum is widespread in Argentina, occurring from northern Jujuy Province to

the Chubut river, near the Patagonian Coast, and in Southern Brazil, Uruguay and

Bolivia. Its reproduction is potentially continuous, since spawning and egg laying extend

through most of the year. From August to April, metallic-sounding choruses of this toad

can be heard in natural or artificial ponds or lagoons after occasional rainfalls. The small,

black-colored eggs are laid in large, gelatinous strings, placed at random on the bottom.

Average clutches of 4000-5000 eggs are usual for a seasonal spawning of a single mature

female. During the winter, B. arenarum is rarely found, since it is hidden in natural refuges

or underground (Cet, 1980).

Both tested species, B. oxyurum and B. arenarum, display synchronous sexual cycles

in the collecting site, where mating and egg laying take place from August to April.

STUDY SITE AND COLLECTING PROCEDURE

The predator and the prey were collected in a small semi-permanent pond located at

Los Talas, District of Berisso, Buenos Aires, Argentina. Only the fourth and fifth instar

and adult stages of the water bugs were used in this study. Each stage of development was

held separately in a plastic bag and starved after capture for 48 h prior to the start of a

trial. Anuran tadpoles were collected at the same time but kept separately in plastic

containers. Tadpoles not eaten or injured were either used again (only in three different

trials) or released.

EXPERIMENTAL DESIGN

Three groups of tadpoles in different stages were used : (1) stages 26-29 ; (2) stages

31-35 ; and (3) stages 38-40 (GosnER, 1960). Tadpoles of each stage of development, at

different densities (2, 4, 8, 16 and 32 individuals), were offered to one predator of each

stage of development tested (IV, V and adult stage) in 15 x 15 cm all-glass aquaria

containing 2 1 of previously dechlorinated water. Three replicates for each 24 h trial were

performed, for each of the nine trials (three for each tadpole stage and three for each

predator stage) by tadpole density tested (five densities). The various tadpole stages,

tadpole densities and predator stages were provided in separate trials. As each predator

was utilized only once, 27 predator individuals were needed for each tadpole density.

Source : MNHN, Paris

64 ALYTES 9 (3)

Hence, a total of 135 predator individuals were used for all experiments. Adult predators

of each sex were randomly assigned to each treatment (sex identification is only possible

for adult stages). The predators were weighed in advance to + 1 mg precision. Remaining

tadpoles were counted at the end of each experiment. Temperatures ranged from 20° to

24°C. A similar experimental design with two replicates for the smaller prey sizes tested

(stages 26-29) was performed with mature water bugs to evaluate effects of predator

incubating activity. To examine differences in predation due to the sex of adult water bugs,

individual male and female water bugs were offered small tadpoles at two densities (4 and

16 tadpoles) in separate trials (two replicates per each sex). All collections and experiments

in this study took place between August and December, 1987.

ANALYTICAL PROCEDURE

Data were recorded as number of tadpoles eaten for each treatment. Several statistical

tests were used to analyze the data. For tests on the proportions of tadpoles eaten (# eaten

1 # offered), arc-sine transformations were performed before analysis.

A Chi-square test with “Yates correction for continuity” was used to assess the effects

of predator, sex, and reproductive condition of males (encumbered vs. unencumbered) on

the number of tadpoles eaten by adult water bugs. The Kruskal-Wallis test was used to

determine differential predation rates, with respect to: (a) tadpole stage; (b) tadpole

density; and (c) predator stage. In addition, a non-parametric Tukey-type multiple

comparisons test (ZAR, 1984) was applied for each of these three relations. Since

comparisons were analyzed by “mean ranks” and not by “sum ranks”, the S.E. (standard

error) was obtained, as proposed by MILLER (1966). The significance level of both tests was

a = 0.05.

Preliminary tests were performed to analyze interactions between variables and to

examine the homogeneity of the group variances, for subsequent application of a

Multivariate Analysis of Variance (MANOVA) on the proportions of tadpoles eaten. All

treatments and interactions were included in the MANOVA. Some may object to the use of

this test, due to the non-normal distribution of data, particularly at the lower prey densities

(2 and 4 tadpoles). Therefore, we also performed the non-parametric tests described above.

The significance level for the MANOVA was arbitrarily selected as « = 0.001.

RESULTS

Table I summarizes the data for the mean number of tadpoles eaten per predator, for

each treatment shown (3 replicates / treatment). Although not statistically significant,

differences were observed for the numbers of tadpoles eaten by the two sexes and by

encumbered vs. unencumbered males. The following results were obtained for separate

Chi-square tests (in each, P > 0.05, d.f. = 1) : (1) for encumbered vs. unencumbered

males, at 2, 4, 8, 16 and 32 tadpole densities respectively, y? = 3.21, ÿ? = 0.01, y? = 0.81,

x = 0.59 and x? = 0.15 ; and (2) for male vs. female water bugs, 4? = 0.01 (4 tadpoles)

and x? = 0.88 (16 tadpoles).

Source : MNHN, Paris

KEHR & SCHNACK 65

Table I. — Prey size and density preferences of giant water bugs, nymph and adult

Belostoma oxyurum, for Bufo arenarum tadpoles.

Predators Tadpoles ! eaten / 24h

] Stage (Gosner, 1960)

26-29 31-35 38-40

predator ? x + SD. offered + SE. x + SE. X+SE.

0.019 + 0.002 | 0.088 + 0.002 |0.178 + 0.020

IV | 0034+0004 | 1 | 2 |200+0 0.00 + 0 0.00 + 0

1 4 |400+0 0.00 + 0 0.00 + 0

1 8 |760+037 | 0.00 +0 0.00 + 0

1 16 |300+160 | 300+0 0.00 + 0

_[1/] 32 |1330+#450 |133+047 | 100+0

V = 0.104+0.010 | 1 2 |200+0 0.00 + 0 1.00 + 0

1 4 |370+027 |000+0 1.00 + 0

1 8 |420+130 | 200+0 2.00 + 0.81

1 16 |800+212 |200+0 2.00 + 0.75

se 11 32 |410+1.50 |400+081 | 2.00 + 0.81

Adults | 0.152+0.034 | 1 2 |20+0 2.00 +0 2.00 + 0

unencum- 1 4 |300+0.73 | 400 +0 3.50 + 0.47

bered 1 8 |660+124 |330+1.80 | 3.00 + 0.80

1 16 |1033+047 |700+0.81 | 2.50 + 1.20

1| 32 |566+7250 |i000+3.0 | 3.00 + 0.82

1. Each trial lasted 24 h and was replicated three times.

2. Each predator was used for only one trial.

The proportions of preys eaten were significantly different for the three tadpole stages

tested (Kruskal-Wallis test: H = 30.83, P < 0.01) (Table II). The analysis performed to

determine the levels where differences occurred (non-parametric, Tukey-type multiple

comparisons test), reflected two homogeneous groups (1: tadpole stages 26-29; 2: tadpole

stages 31-35 and 38-40) (Table II). By examining Table I, it is evident that the group of

smaller tadpoles was more vulnerable to predation.

The influence of tadpole densities on predation was evident (Kruskal-Wallis test: H

= 11.26, P < 0.05) (Table II). However, pairwise significant differences were detected only

between the extreme densities tested (2 vs. 32 tadpoles), with proportionately more of the

tadpoles at lower densities being eaten. Compared to later predator stages, fourth instar

water bugs ate a larger proportion of the small tadpoles at high densities. At the highest

prey densities, adult water bugs ate proportionately more of the medium-sized prey (31-35)

(Table 1).

A significant heterogeneity was estimated in two of the groups (tadpole stage and

tadpole density). However, the MANOVA test (Table III) revealed trends that were similar

Source : MNHN, Paris

66 ALYTES 9 (3)

Table II. — Analysis of arc-sine transformation of proportion eaten (# tadpoles eaten /

# tadpoles offered), for two non-parametric tests for each of three levels tested:

tadpole stages; tadpole densities; and predator stages.

Level tested Sample size Meanrank Non-parametric!

multiple comparisons

(homogeneous groups)

Bufo stage

1 (26-29) 45 94.1444 bi

2 (31-35) 45 55.4889 #

3 (38-40) 45 54.3667 *

Kruskal-Wallis test : H = 30.8325; P < 0.01.

Bufo density

1 (2 tadpoles) 27 81.5556 *

2 (4 tadpoles) 27 77.6481 oi

3 (8 tadpoles) 27 69.3889 La

4 (16 tadpoles) 21 60.3704 var

5 (32 tadpoles) 27 51.0370 ie

_Kruskal-Wallis test: H = 112650; P < 0.05. a. . =”

Belostoma stage

3 (adults) 45 90.6444 L:

2 (stage V) 45 64.5556 $

1 (stage IV) 45 48.8000 x

Kruskal-Wa

st: H = 26.8459; P < 0.01.

1. Non-parametric, Tukey-type multiple comparisons test.

to those obtained with the non-parametric tests described above. The MANOVA analysis

showed highly significant differences for all treatments (predator stage, tadpole density and

tadpole stage), as well as for all interactions.

DISCUSSION

Smaller tadpoles were more vulnerable to predation than larger ones for all of the

tested stages of water bugs in these studies. Nevertheless, adult predatory rate declined as

the newly-hatched preys were offered at the highest experimental density (32 individuals).

We rejected the explanation that a large adult giant water bug is unable to subdue a much

smaller prey, because, at low experimental densities, predation rate on the smallest prey

was high, regardless of predator size. The lack of efficiency of adult giant water bugs to

predate on tiny tadpoles could be due to the “confusion” in selecting individual prey from

an aggregation (MiLiNski, 1979; TREHERNE & FOSTER, 1981; BRODIE & FORMANOWICZ,

1987; KEHR, in press a). A benefit to clumped tadpoles might be a reduction of individual

Source : MNHN, Paris

KEHR & SCHNACK 67

Table III. — Analysis of arc-sine transformation of proportion eaten (# tadpoles eaten /

# tadpoles offered), using a MANOVA test on the three levels tested: tadpole stages

(tadstage); tadpole densities (taddens) and predator stages (prestage).

D.F. MS. F Sign. of F

“Within cells 790 005

Constant 1 60.02 1144.76 0001

Tadstage 2 543 103.49 0001

Taddens 4 1.61 30.80 0001

Prestage 2 341 64.98 -0001

Tadstage by taddens 3.32 8 0.41 7.91 0001

Tadstage by prestage 4.74 4 1.19 22.61 0001

Prestage by taddens 3.08 8 039 7.35 0001

risk to predation. À member of the group, while hidden behind other individuals, has just

one chance in many of being caught by one predator (ALCOCK, 1979). Newly-hatched B.

arenarum usually aggregate in nature (KEHR, in press b).

The overall water bug predatory trend showed a positive preference for smaller prey,

particularly by fourth and fifth instar predators (Table I). Probably, immature water bugs

are more susceptible to danger of injury to the prey-capturing apparatus (BRODIE &

FORMANOWICZ, 1983), and they also may require longer handling times for subduing large

prey than adult giant water bugs. The stronger predatory structures of B. oxyurum adults

certainly make them less exposed to injury. Nevertheless, the highest predation rate of

adult predators was observed on tadpoles of stages 26-29 and 31-35, being lower on larger

individuals.

A reduction of predatory efficiency has been suggested for encumbered males of the

giant water bug Abedus herberti from Central Arizona (SmirH, 1976 a). This reduction is

partially attributed to the limitation imposed by the higher weight of the incubant males.

In addition, it has been pointed out that in several groups of giant water bugs a brooding

male spends many hours resting near the surface to aerate fertilized eggs. During this time

it is assumed that an encumbered male cannot feed efficiently (SmirH, 1976 b; ALCOCK,

1979). Data obtained during this study show that B. oxyurum can double its weight when

heavily encumbered by eggs. Although male water bug incubating activity could reduce

predatory efficiency, differences between encumbered and unencumbered B. oxyurum were

not significant. This observation is logical, because tadpole capture by ambush predators

could be facilitated more by the motion of the tadpole than by active chasing by the

predator (MENKE, 1979).

Unpalatability to vertebrate predators, as well as to both sucking (Belostoma sp.) and

chewing (Anax junius) insect predators, has been pointed out for newly-hatched Bufo

americanus tadpoles (BRODIE & FORMANOWICZ, 1987). Chemical cues to deter predation,

associated with schooling, are assumed to be competitively advantageous for B. americanus

tadpoles (WALDMAN, 1982; WALDMAN & ADLER, 1979; BRODIE & FORMANOWICZ, 1987).

Our experiments support the inference that newly-hatched B. arenarum tadpoles are

palatable to giant water bugs.

Source : MNHN, Paris

68 ALYTES 9 (3)

WASsERSUG (1973) and WALDMAN & ADLER (1979) postulated the evolution of

aggregations in the larvae of unpalatable amphibians. However, although unpalatability

may be a precursor of the evolution of aggregations, aggregations should not be viewed

as a precursor of the evolution of unpalability (BRODIE & FORMANOWICZ, 1987). Our

results are compatible with this hypothesis. Aggregation in B. arenarum could play a

similar role to unpalatability in B. americanus. This might mean that a behavioral

mechanism would substitute for a physiological one in order to lessen predatory impact

upon newly-hatched tadpoles.

ACKNOWLEDGEMENTS

We are grateful to Dr. Richard J. WASSERSUG and two anonymous reviewers for the critical

review of the manuscript.

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Evolutionary biology of the anurans, Columbia, Univ. Missouri Press: 273-297.

Wizur, H. M., 1980. — Complex life cycles. Ann. Rev. Ecol. Syst., 11: 67-93.

ZAR, J. H., 1984. — Biostatistical analysis. Englewood Cliffs, N.J., Prentice-Hall: 1-718.

in the competition equations: an experiment

Corresponding editor: Dianne B. SEALE.

Source : MNHN, Paris

70 ALYTES 9 (3)

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Alytes, 1991, 9 (3): 71-77. 71

Images d’Amphibiens camerounais.

IV. Les constructeurs de nids

Jean-Louis AMIET

Université de Yaoundé,

Faculté des Sciences, Laboratoire de Zoologie,

B.P. 812, Yaoundé, Cameroun

In Cameroon, the Anurans of three genera (Afrixalus, Opisthothylax and

Chiromantis) build “nests” above the water. In the three cases, both parents

cooperate in the construction of the nest. The latter is here particularly

described, and illustrated with photos, in Afrixalus and Opisthothylax. The

function of the nests seems to be different according to the genus.

La chambre de ponte des Hemisus, évoquée dans un précédent article (AMIET, 1991),

peut être considérée comme un nid. Le même terme pourrait s'appliquer aussi aux cavités

creusées par certains Leptopelis où Arthroleptis pour abriter leurs œufs.

Les nids montrés par les photos des figures 1 à 6 sont d’un type très différent. Ils sont

en effet construits au-dessus de l’eau grâce à une collaboration active des deux parents et

intègrent des éléments de la végétation environnante.

Ce mode de nidification est pratiqué au Cameroun par trois genres d’Anoures:

Afrixalus, Opisthothylax et Chiromantis.

LE NID DES AFRIXALUS

Le genre Afrixalus regroupe des petites rainettes d'aspect assez proche de celui des

Hyperolius. On y reconnaît environ 25 espèces. Quelques-unes sont sylvicoles mais la

plupart vivent dans les formations secondaires en zone forestière ou dans des savanes plus

ou moins sèches.

Il semble que les premières descriptions de nids d’Afrixalus aient été faites par WAGER

(1965), à qui l’on doit de fines observations sur les Anoures d'Afrique australe. Peu après,

ScHieTz (1967) a donné des informations sur la nidification de plusieurs espèces d'Afrique

de l'Ouest, dont 4. weidholzi, espèce existant aussi au Cameroun.

La photo de la figure 1 montre dans quelle position acrobatique un couple d’une

espèce camerounaise, À. paradorsalis, construit son nid. Celui-ci est toujours constitué par

l'extrémité d’une feuille (souvent de Zingibéracée ou de Marantacée) qui est repliée

longitudinalement, suivant la nervure principale. Mieux qu’une longue description, la photo

Source : MNHN, Paris

72 ALYTES 9 (3)

permet de comprendre comment ce résultat est obtenu par le mâle et la femelle en

amplexus. Les deux partenaires doivent faire preuve d’une remarquable coordination

gestuelle pour rapprocher les bords du limbe et les maintenir jusqu’au moment où la

substance visqueuse enrobant les œufs leur permettra de les faire adhérer l’un à l’autre.

Terminé, le nid passe totalement inaperçu dans la végétation. En général, il est placé de

1 à 2 m au-dessus de l'eau.

Tous les Afrixalus ne procèdent pas de la même façon. D'après ScHioTz (1967), une

petite espèce de savane, 4. weidholzi, utilise une feuille de Graminée qu'elle replie

transversalement (‘“transversally folded grass leaves”). Le nid d’A. nigeriensis, espèce

d'Afrique occidentale, peut comprendre “one or few leaves folded and glued round a

rather small mass of eggs”.

Un Afrixalus strictement sylvicole, 4. laevis, pose un problème évolutif intéressant car

il ne construit pas de nid: comme on peut le constater par la figure 3, les œufs, au nombre

d’une demie douzaine au maximum et de teinte vert pâle, sont déposés sur ou sous une

feuille sans aucune protection et parfois même bien en évidence. Les pontes surplombent

de petits cours d’eau, où se développent les têtards. 4. laevis représente-t-i x

primitive” qui aurait conservé le mode ancestral d’oviposition ou, au contraire, a-t-il

abandonné secondairement la méthode de nidification de ses congénères ? Je penche pour

la seconde hypothèse, étayée par le fait que le têtard d'A. laevis est allé plus loin que celui

des autres Afrixalus dans la réduction de la formule dentaire puisqu'il n’a plus du tout de

denticules cornés, alors qu'il en reste une rangée, sous le bec, chez les autres espèces. De

même, l'habitat du têtard en eau courante s’oppose à celui des autres A/frixalus, tous

inféodés aux eaux stagnantes, et peut être conçu comme une “percée évolutive” réalisée par

cette espèce!.

LE NID D'OPISTHOTHYLAX IMMACULATUS (BOULENGER, 1903)

Cette rainette sylvicole, dont l'aire de distribution ne dépasse guère les limites du

Cameroun, est aisément reconnaissable à sa pigmentation dorsale jaune, orange ou

brun-roux uniforme à l'exception de deux petites macules noires occipitales. Elle se

distingue de tous les autres Hyperoliidae par le fait que sa ponte est incluse dans une sorte

de mucus battu comme chez les Rhacophoridae.

La masse spumeuse, peu volumineuse, et les œufs (une dizaine au plus, de 4,6 mm de

diamètre) se trouvent à l’intérieur d’une feuille repliée transversalement. L'ensemble

constitue un nid très discret, placé au-dessus d’un petit cours d’eau (AMIET, 1974).

Postérieurement à la description du nid dans le travail cité, j'ai eu la chance de

pouvoir observer et photographier sinon toute son élaboration, du moins la phase finale,

illustrée par la figure 5.

La formule dentaire et l'habitat du tétard d'A. lacteus, une espèce orophile, sont semblables à ceux d'A.

Afritals ne plaide pas pour leur regroupement'ave les Las dans une même bu ou sous famille statut

proposé par LAURENT (1982, 1986) mais récusé par DREWES (1984).

Source : MNHN, Paris

AMIET 73

Les premières phases peuvent cependant être facilement reconstituées. Au terme d’une

“‘promenade nuptiale” du couple en amplexus (fig. 4), une feuille convenable est trouvée:

elle doit pendre plus ou moins verticalement au-dessus de l’eau. Les ovules sont émis et

fécondés sur le limbe, la face n’important pas (sauf, peut-être, si la face supérieure est trop

envahie d’épiphylles). La ponte est accompagnée d’un liquide visqueux apparemment

sécrété par la partie distale, très élargie, des oviductes (AMIET, 1974).

Le mâle, après avoir fécondé les œufs, passe de la position d’amplexus axillaire à la

position lombaire et, à l’aide de ses pieds, saisit l'extrémité de la feuille par l'autre face, la

replie et la glisse entre son ventre et la région postéro-dorsale de la femelle.

C'est cette dernière qui, seule, bat le mucus en agitant ses pattes dans le repli de la

feuille: la photo de la figure 5 est prise à ce stade d’élaboration du nid. Elle montre bien

la position assez extraordinaire des pieds du mâle pendant cette phase et permet de

constater qu’il y a une certaine opposabilité des deux orteils les plus internes, facilitant la

“mise en pli” de la feuille.

Quand le mucus battu a atteint une consistance suffisante pour que la pliure persiste,

le mâle s'éloigne après que la femelle se soit avancée un peu sur la feuille où, visiblement

fatiguée, elle s'accorde un moment de repos.

J'ai émis l’hypothèse (AMIET, 1974) que le comportement nidificateur d’Opisthothylax

pouvait être dérivé de celui des Afrixalus, mais il est possible aussi qu’il s'agisse d’une

simple convergence. Une analyse détaillée des séquences gestuelles lors de la construction

du nid chez les diverses espèces d’Afrixalus et chez Opisthothylax permettrait peut-être de

trancher entre ces deux hypothèses.

LE NID DE CHIROMANTIS RUFESCENS (GÜNTHER, 1868)

Les Rhacophoridae, nombreux en Asie et à Madagascar, ne sont représentés en

Afrique que par un seul genre, Chiromantis, comprenant deux espèces savanicoles en

Afrique orientale et australe et une espèce répandue dans la zone forestière mais plutôt

parasylvicole, C. rufescens.

Au Cameroun, cette espèce a été bien étudiée par MONAYONG AKO°0 (1978). Le nid,

comme chez les autres espèces du genre, est constitué par une volumineuse masse d’écume,

d’environ 12-15 cm de plus grande dimension, dont la surface durcit plus ou moins en lui

donnant l’aspect d’une meringue. Il contient une centaine d’œufs mesurant environ 2 mm

de diamètre.

Le mâle (ou les mâles, car il est fréquent que plusieurs s’accouplent avec la même

femelle) coopère à l'élaboration du nid: les partenaires, accouplés, battent de leurs pattes

postérieures une substance glaireuse produite par la femelle et la “montent en neige”. Le

nid peut ou non incorporer des feuilles de la plante servant de support et n’est d’ailleurs

pas forcément déposé sur un support végétal: un rocher surplombant l’eau, les parois des

profondes ornières creusées par les engins forestiers, sont souvent utilisés. De même, la

hauteur du nid au-dessus de l’eau est très variable, de quelques centimètres à 2 ou 3 m.

Source : MNHN, Paris

2 3

Fig. L. — Couple d'Afrixalus paradorsalis Perret, 1960 en train de pondre dans une feuille repliée

Kala, 10-11-76

Un nid d’Afrixalus paradorsalis ouvert, montrant les jeunes larves encore incolor

Ponte d'Afrixalus laevis (Al, 1930). Cette ponte n'est pas nécessairement pla

xtrémité d’une feuille comme sur la photo. Kala, 4-X1-74.

: MNHN, Paris

AMIET 75

Fig. 4. — Couple d'Opisthothylax immaculatus (Boulenger, 1903) en “promenade nuptiale”. Les gros

ovules sont visibles par transparence sous la peau du flanc droit de la femelle. Nkoladzap,

12-11-76.

Fig. 5. — Fin de la construction du nid chez Opisthothylax immaculatus. Pendant que le mâle tient

la feuille repliée, la femelle bat le mucus dans lequel sont inclus les œufs. Nkoladzap, 12-I11-76.

Fig. 6. — Nid d'écume de Chiromantis rufescens (Günther, 1868) adhérant à une feuille. Comme on

peut le constater, ce nid est très apparent. Yaoundé, XI-73

Source : MNHN, Paris

76 ALYTES 9 (3)

LE RÔLE DES NIDS

Tout comme pour la garde des œufs, on peut s'interroger sur le rôle des nids qui

viennent d’être décrits.

Deux fonctions possibles viennent à l'esprit : (1) dissimuler la ponte à d’éventuels

prédateurs; (2) la protéger contre la dessiccation et/ou l’action directe des rayons solaires.

Il est certain que les nids d’Afrixalus et d’Opisthothylax sont, dans la nature, très

difficiles à détecter (du moins pour l’homme, car il n’est pas sûr qu’ils puissent échapper

à la vue d’un oiseau!) et peuvent de ce fait assurer aux œufs une protection contre les

prédateurs. Encore faudrait-il que ceux-ci existent dans la faune camerounaise: comme je

l'ai déjà fait remarquer (AMIET, 1991), il n’a pas été possible jusqu'ici d’avoir la preuve

qu’un quelconque prédateur (à l’exception de celui dont il sera question ci-après) puisse

s'attaquer à des pontés d’Anoures dans le territoire étudié. Le fait qu’A. laevis ait

apparemment “renoncé” à la construction d’un nid et laisse ses œufs en évidence comme

nombre d’autres rainettes à ponte suspendue montre d’ailleurs que, au stade œuf, la

prédation ne doit pas constituer une contrainte évolutive efficace.

Le nid de Chiromantis rufescens, contrairement à celui des Afrixalus et Opisthothylax,

est très apparent en raison de sa grande taille et de sa teinte, caractères qui seraient

difficilement concevables si les œufs étaient en butte à l’action des prédateurs. Pourtant,

BROSSET (1976) a montré comment, au Gabon, les nids de C. rufescens sont souvent mis à sac

par un petit oiseau, Wigrita bicolor, qui mange les œufs ou les jeunes têtards. Au Cameroun,

j'ai pu observer de telles scènes de pillage mais elles m’ont paru tout à fait exceptionnelles (NW.

bicolor “signe” ses déprédations en projetant de tous côtés des éclaboussures d’écume). Il est

très possible que ce comportement corresponde à une habitude alimentaire acquise depuis

peu (à rapprocher du cas des mésanges ayant appris à décapsuler les bouteilles de lait) et qui

ne s’est pas encore généralisée. Si cela se produisait, l'avenir de C. rufescens dans les régions

peuplées par N. bicolor pourrait être sérieusement compromis.

Si le nid ne paraît pas destiné à protéger les œufs contre les prédateurs, qu’en est-il

d’une protection contre la dessiccation ou l’action du soleil?

Pour les espèces sylvicoles ou pour les espèces de brousse secondaire dense en zone fo-

restière, celle-ci ne paraît pas nécessaire, compte tenu de l’humidité atmosphérique presque

constamment élevée et de l’effet d’écran joué par la végétation. En revanche, pour les Anou-

res qui se reproduisent en milieu très ouvert, en particulier les savanes sèches, le nid doit

assurer une réelle protection contre la sécheresse et l’insolation. Le cas de C. rufescens, qui

peuple la zone forestière et produit un nid particulièrement volumineux, n’est contradictoire

qu’en apparence, d’abord parce que cette espèce n’est pas franchement sylvicole mais vit

plutôt dans des formations dégradées paraforestières, et ensuite parce qu’elle fait partie d’un

genre plutôt savanicole si l’on en juge par la distribution des autres espèces. Les Anoures de

savane ne déposent généralement pas leurs œufs au-dessus de l’eau, ou sinon à faible hau-

teur, et ilest probable que sans la protection apportée par la masse d’écume du nid, les pontes

aériennes des Chiromantis savanicoles seraient exposées à un prompt déssèchement 2.

2. Il faut rappeler aussi que dans la famille des Rhacophoridae, dont fait partie le genre Chiromantis, la

production de nids d'écume est pratiquée par la majorité des espèces.

Source : MNHN, Paris

AMIET 77

En ce qui concerne les Afrixalus savanicoles, l'argumentation précédente se trouve

cependant affaiblie par quelques espèces d'Afrique australe qui construisent leur nid sous

l’eau! Ce comportement a été observé par WAGER, qui en donne une photo (WAGER, 1965).

On peut imaginer que le nid, en changeant de milieu, change aussi de fonction et qu'il

assure alors une protection des œufs contre les prédateurs, probablement plus nombreux

en milieu aquatique qu’en milieu aérien.

Le cas du nid d’Opisthothylax me paraît devoir être dissocié des précédents. Chez cette

rainette en effet les œufs sont riches en vitellus (4,6 mm de diamètre!) et les larves ne sortent

du nid que 2 à 3 semaines après la ponte, déjà munies de bourgeons de pattes postérieures

(AMHET, 1974). Le jeune têtard est alors plus apte à affronter les risques de la vie libre, tels

que les prédateurs, mais aussi le courant puisque la suite du développement se fait dans

de petites rivières. En construisant son nid, le couple d'Opisthothylax travaille au moins

autant pour les têtards que pour les œufs.

RÉSUMÉ

Au Cameroun, les Anoures de trois genres (Afrixalus, Opisthothylax et Chiromantis)

construisent des “nids” situés au-dessus de l’eau. Dans les trois cas, les parents coopèrent

à l'élaboration du nid. Celle-ci est particulièrement décrite, et illustrée de photos, chez

Afrixalus et Opisthothylax. La fonction des nids paraît différer suivant les genres

considérés.

RÉFÉRENCES BIBLIOGRAPHIQUES

AMIE, J.-L. 1974. — La ponte et la larve d’Opisthothylax immaculatus (Boulenger) (Amphibien

Anoure). Ann. Fac. Sc. Cameroun, 17: 121-130.

= 1991. — Images d'Amphibiens camerounais. III. Le comportement de garde des œufs. Alytes, 9:

15-22.

BROSSET, A., 1967. — La vie dans la forêt équatoriale. Paris, Nathan: 1-126.

DREWES, R. C., 1984. — A phylogenetic analysis of the Hyperoliidae (Anura): treefrogs of Africa,

Madagascar and the Seychelles Islands. Occ. Pap. Calif. Acad. Sci., 139: i-x + 1-70.

LAURENT, R. F., 1982. — Le genre Afrixalus Laurent (Hyperoliidae) en Afrique centrale. Ann. Mus.

roy. Afr. centr., Sc. Zool., 235: 269-280.

= 1986. — The systematic position of the genus Afrixalus Laurent (Hyperolidae). Alytes, 5: 1-6.

MoNAYoNG AKko°o, M., 1978. — Développement embryonnaire et larvaire de Chiromantis rufescens

(Günther) (Amphibien Anoure). Ann. Fac. Sc. Yaoundé, 25: 159-188.

ScHieTz, A., 1967. —The trecfrogs (Rhacophoridae) of West Africa. Spolia zool. Mus. haun., 25:

1-346.

WAGER, V. A., 1965. — The frogs of South Africa. Cape Town & Johannesburg, Purnell & Sons: 1-242.

Corresponding editor: Alain DuBois.

Source : MNHN, Paris

Alytes, 1991, 9 (3): 78.

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Source : MNHN, Paris

Alytes, 1991, 9 (3): 79-88. 79

Variation in size and fecundity

between neïighbouring populations

in the common frog, Rana temporaria

Pierre JOLY

URA CNRS 1451 Ecologie des Eaux douces et des grands Fleuves,

Université Claude Bernard Lyon I,

69622 Villeurbanne Cédex, France

Differences in body size were detected among neighbouring populations

of common frogs (Rana temporaria) in Jurassian Bresse (Eastern France).

Variation in fecundity and egg size was positively correlated with body size.

Frogs using one wooded area were smaller than those elsewhere. Small body

size might result from a slower growth rate or from earlier sexual maturation.

Demographic parameters of these French populations differed from those of

other European populations, but no correlation between demographic para-

meters and latitude or altitude were detected.

INTRODUCTION

Variation in demographic parameters on a geographic scale (cline or isolated

populations) has been the subject of considerable attention in anurans (MARTOF &

HUMPHRIES, 1959; PETTUS & ANGLETON, 1965; KosLOWsKA, 1971; NEVO, 1972; KOSKELA &

PASANEN, 1975; BERVEN, 1982, 1988; READING, 1988, 1990), but variation on a smaller scale

has received little study. Isolation of populations may lead to genetic adaptation to local

environmental conditions (BERVEN, 1982, 1988); when genetic exchange between local

populations becomes frequent, variation reflects the influence of epigenic factors on

phenotypes. Among such mechanisms of plasticity, differences in growth rate can

determine variation in adult size, age at maturity, fecundity and egg size (BERVEN & GILL,

1983; STEARNS & KOELLA, 1986).

Estimating the level of isolation between neighbouring populations is difficult; site

fidelity can play a discrete isolating role (OLDHAM, 1963; HAAPANEN, 1970). I studied

neighbouring demes of Rana temporaria (the common frog) that had been subjected to

numerous transfers of tadpoles over a period of twenty years. In the Jurassian Bresse

Source : MNHN, Paris

80 ALYTES 9 (3)

region of France, common frogs are heavily harvested from certain ponds by professional

fish-farmers. This practice is authorized on condition that the frogs be allowed to spawn

before being killed; eggs or tadpoles are taken back to the ponds without taking into

account the original site of their parents. Such a mix has been occurring for 15 years, and

one may assume the local populations to be genetically homogeneous. This paper

demonstrates variation of body size among these demes and defines the relationship of

adult size with fecundity and egg size. Characteristics of Jurassian Bresse populations are

compared with those from other regions of Europe.

MATERIALS AND METHODS

The Jurassian Bresse region (north of Lons-le-Saulnier, Jura Department) varies

between 200 and 250 m in altitude. The main ecosystems are forests (Quercus, Fraxinus

and Carpinus), agrosystems alternating between pastures and crop, and shallow ponds

devoted to carp culture. These ponds vary in area from 2 to 20 ha and in depth to a

maximum 3 m at the draining point; average depth is approximately 0.7 m. Ponds are

drained every winter to fish the carp and are then filled with water from small brooks or

rain. Most ponds are surrounded by forest. The common frog is abundant, several

thousands individuals breed in certain ponds. In each pond, frogs gather in one or several

spawning sites, where their eggs are clumped. In 1986 and 1987, frogs were sampled in

ponds A (Servotte, 19.7 ha) and B (Thévenon, 3.5 ha) during the breeding season (fig. 1).

The distance between these ponds is about 9 km and their altitude is similar (220 m).

In 1987, populations of three other ponds were sampled (C: Roche, 2.5 ha; D: Char-

dennet, 6.6 ha; E: Neuf, 3 ha). All five ponds are situated along a 20 km North-South

transect.

Frogs were caught around spawning areas in traps installed by pisciculturists, weighed

using Pesola letter-scales (precision 0.1 g), and measured from snout to urostyle with

vernier calipers. Only gravid females were weighed. Females from ponds A and B were

dissected to obtain clutch weights and egg counts (site A: n — 27; site B: n — 22). Because

oocytes are coated with a sticky gelatinous envelope preventing their being counted easily,

it was not possible to estimate egg number, spawn mass, and oocyte mass from the same

individual. Dissolving mucins in the envelope involves the use of potassium cyanide (2

hours in a 20 % KCn solution) which may also damage oocyte proteins and modify their

mass. ['extracted eggs by dissection of the spawn immediately after laying, before egg mass

began to increase (it remains stable for 12 hours after spawning; CUMMINS, 1986). The

clutch obtained by dissecting a female provided the wet weight of both oocyte and jelly and

the egg extracted after spawning allowed for measurement of wet and dry mass.

Correlation and regression analyses of female body size and these different parameters

were performed. Clutch wet weights were combined for the two years under study, while

egg wet and dry mass data were collected in 1987 only. In 1987, males and females from

ponds A and B were paired (n = 22) and isolated in 40 x 40 x 10 cm tanks for spawning.

Within 12 hours after egg laying, 30 eggs were extracted from the gelatinous envelope by

Source : MNHN, Paris

JoLy 81

females

50 60 70 80

Le fl

ENGEA RE

Lin,

T RS FERRER

JUIN,

mile

Fig. L. — Distributions of frog lengths in five ponds along a 20 km long transect. Black patches:

ponds. Dotted area: forest. White area: cultures and pastures. On the graphs, the triangles

indicate mean values. A: Servotte; B: Thévenon; C: Roche; D: Chardennet; E: Etang Neuf.

Demes of small frogs were found at B, C and D; those ponds are grouped in the same forest area,

where density of ponds is higher than elsewhere.

Source : MNHN, Paris

82 ALYTES 9 (3)

dissection, clumped in groups of 10, weighed, and then dried for 48 h at 80°C. This

procedure gives a better estimation of egg size than measuring egg diameter, and allows

the estimation of reproductive investment (CUMMINS, 1986).

RESULTS

BODY SIZE

Size distributions of males and females were approximately normal. During 1986 and

1987, males and females from site B were, on average, 1 cm smaller and 10 g lighter than

those from site A (Table I). Variation from one year to the other was also significative. In

order to determine where small size occurred, three other ponds situated approximately

along a 20 km transect which includes ponds A and B at the North end (fig. 1) were

sampled during the breeding season of 1987. Ponds C and D (Roche and Chardennet) are

situated in the same forest as B, while pond E (Etang Neuf de Lombard) is close to another

forest area to the South. Length of frogs breeding in ponds B, C and D was significantly

smaller than length of frogs breeding in A and E (ANOVA, F test: P < 0.0001 for both

males and females). Frogs from B, C, and D were significantly smaller than those from A

and E in all pair-wise comparisons (Fisher PLSD). Snout-urostyle length did not vary

significantly between A and E and snout-urostyle length of frogs from B, C and D are not

different from each other. À smaller size was not a characteristic of frogs inhabiting pond

B, but was related to that group of demes (B, C, D) inhabiting the forest area (Bois de

Champrougier).

Table I. - Comparison of length (mm) and weight (g) of frogs from ponds A and B for

two years (t test). Frogs from A are always larger than those from B.

(Es Site À _ SiteB | P |

jp Ju n Li 5 | n & (Etes)

Males |1986 | length (mm) 87 | 66.1 | 64 | 79 | 564 <0.0001

Lust | [és [79] [ico| 53 |<oon

1987 | length (mm) 63 | 617 | 51] 79 | 546 <0.0001

weight (8) | 260 | 63 | |<0.0001

Females |1986 [length (mm) Eu 67.2 | 68 | 40 _<0.0001

weight (g) [ 30.1 94 <0.0001

1987 | length (mm) 70 | 638 | 7.5 | 48 <0:0001

weight (g) | 29.2 | 120 | 146 | 63 |<0.0001

Source : MNHN, Paris

JoLy 83

RELATIONSHIP OF REPRODUCTIVE PARAMETERS WITH BODY SIZE

Fecundity, expressed as the number of mature oocytes per female, and reproductive

investment, estimated by spawn mass, were both correlated with body size (fig. 2). The

relationship between body size and fecundity may be described as an exponential model:

for site A, N (oocytes) = 0.003L*'° and for site B, N = 0.0018L*'?. The two models are

not significantly different (covariance analysis after log-transformation: F = 3.64, df 1/47

[slope]; F = 5.54, df 1/48 [Y-intercept]). However, the coefficient of determination (r?)

shows higher variability at B (0.73 and 0.55 for 1986 and 1987, respectively) than at A

(0.83 and 0.87). Such a relationship indicates considerable variation relative to size: while

a 50 mm female laid 400 eggs, a 70 mm female laid 1600 eggs. Wet clutch mass was

strongly correlated with female body size (r? = 0.87 and 0.90 for sites À and B,

respectively). The relationship is also exponential: M (clutch mass) = 1.3 x 10"$L?-%

for site À and M = 4.8 x 107L#% for site B. The difference between slopes, however, is

not significant (F = 3.69, df 1/47). When the two populations are combined, the

relationship becomes: M = -14.9L%'$, The slope of the relationship between female length

and average mass of a single egg (oocyte + capsule) was not strong: wet mass of a single

egg = -0.33L°%; wet mass of the oocyte was related to female size (r? = 0.65). The linear

model (M = 0.13L!*) is acceptable for describing that last relationship (analysis of

residuals). Dry mass was also related to female body size: M = 0.02L°°2 (r? = 0.69).

COMPARISON WITH OTHER EUROPEAN POPULATIONS

Table II presents fecundity and clutch mass for a 70 mm female in 13 European

populations the adequate regression parameters of which were available in the literature.

Table III shows different reproductive investments in 4 populations, estimated by the

relationship of clutch mass to body mass. Fecundity of frogs varies among populations

with no apparent relationship to altitude, latitude or clutch mass. The 13 investigated

populations are distributed among three groups: 5 populations had very low fecundity

(fewer than 1300 eggs per 70 mm female), 6 had intermediate fecundity (1300 to 1600 eggs

per female) and 2 had high fecundity (more than 1900 eggs per female). Populations from

sites À and B in this study fall within the intermediate group. They are characterized by

higher clutch masses and higher relative reproductive investments than are found

elsewhere. Whether these parameters reflect a reaction to mortality induced by fishing or

the consequence of a climatic cline (the studied populations represent those from South)

is questionable. Data and measurements are needed from other populations, using

comparable methods. Comparisons with other unfished populations in neighbouring areas

might shed light on this problem. Figure 3 highlights the relationship between female

length and dry egg weight in 6 populations. Values are distributed linearly except for the

population from Spitchwick (Devon, England), in which eggs were larger relative to female

size when compared with all other populations.

Source : MNHN, Paris

84 ALYTES 9 (3)

3 Dé

Egg number (x10Ÿ)

(

Clutch weight (g)

501 0 C e

Ë Fu e °° 2° e° °

RS SCT e *

ne 970000.

É se ° o

& à] e

È o

2 4l

né o

2 —————— ————

18] D °e

S e

E 16 e e

Ê 14 : ®

5 | e

8 12 o e

o o o o

8 © o

4 a

°_o

40 7 45 7 30 55 60 65 70 75 80 85

Female body length (mm)

Fig. 2. - Relationship between female length and several demographic parameters. A: relationship with

fecundity. B: relationship with clutch mass (clutch mass/n eggs). C: relationship with a single egg

mass (before spawning). D: relationship with dry weight of an oocyte (each point is an average

value for 30 oocytes). Black dots: site À (Servotte pond); open dots: site B (Thévenon pond).

Source : MNHN, Paris

JoLy 85

Table II. - Fecundities of frogs from different European populations. Fecundity (N eggs)

and clutch mass (weighed before spawning) were estimated for a 70 mm female using

allometric models. Fecundity varies greatly from one site to another without clear

relationship to altitude or latitude. Frogs under study show intermediate fecundity.

Region Lat. Alt.(m) Neggs Mclutch(g) Authors

Berne (CH) 46° 600 — 1000 RYSER, 1988 b

Haapavesi (FL) 64°10 100 1067 12.8 KOskELA & PASANEN, 1975

Clare (IL) 53° 1140 128 GiBBons & MCCARTHY, 1985

Tatras W (PL) 50° 1000 1199 11.5 KozLowskA, 1971

Devon (GB) 50°31 100 1235 Cummixs, 1986

Thévenon (F) 46°55 215 1383 14.3 This study

Lincoinshire (GB) 53°26 ll 1533 Cummins, 1986

Beskid (PL) 50° 700 1538 14.5 KozLowska, 1971

High-Tatras (PL) 50° 1000 1538 12.1 KozLowska, 1971

Norfolk (GB) 52°42 60 1544 Cummins, 1986

Servotte (F) 46°58 200 1573 16.0 This study

Cracov (PL) 50° 200 1905 11.3 KozLowska, 1971

Cambridgeshire (GB) _52°26 10 1915 CuMMINs,_1986

Table III. - Comparison of reproductive investment of females from different populations.

Frogs in the present study show a greater investment than populations from which

data are available.

“Region Lat. Alt. (m) M clutch/M body (%) Authors k

Poland 50° 1000 17.2 Juszczvk, 1959

North Finland 64 100 203 KOSKELA & PASANEN, 1975

Thévenon 86 46° 210 39.38 This study

Thévenon 87 id. id. 26.48 id.

Servotte 86 id. id. 43.53 id.

Servotte 87 id id. 38.25 id.

DISCUSSION

Average size of the common frog varies greatly among neighbouring demes and size

variation is positively correlated to fecundity and egg size. Why are frogs smaller in the

“Bois de Champrougier”? Transfer among the studied ponds of eggs and tadpoles has

occurred several times during the last twenty years; genetic homogeneity is probable.

Source : MNHN, Paris

86 ALYTES 9 (3)

CCambridgeshire ALincolnshire Osite A

Devon ANorfolk Osite B

A 24 = E

2 o

& o

ä A

8 56 A

T A

ÿ 12] @ A

60 70 80

MEAN LENGTH OF FEMALE mm

Fig.

3. - Relationship between means of female length and dry egg mass. Repctition of a symbol

corresponds to data from several years. Data for English populations are from CUMMINs (1986);

the population from Devon seems to show unusually large eggs.

Differences in size may be expressions of phenotypic plasticity influenced by subtle

ecological variation. Any of three hypotheses may explain the smaller size of the Bois de

Champrougier frogs:

(1) Small frogs experienced slower growth than large frogs.

(2) Small frogs are younger than large ones.

(3) Frogs are small when fishing is locally more intensive.

The first hypothesis assumes that maturity depends on age rather than on size or rate

of growth. By contrast, the second hypothesis assumes that age at maturity depends on

growth rate, Both hypotheses are theoretically acceptable (STEARNS & KOELLA, 1986). Age

at maturity varies from one population to the other in the common frog, as well as within

the same population. At low altitude, the common frog may mature in two or three years

(GiBBons & MCCARTHY, 1984), suggesting the major role of growth on maturation

(RYSER, 1988 a). Variation of size from one year to the other may suggest the role of

environmental constraints on either growth or recruitment (juvenile survival). The third

hypothesis supposes that harvesting is, relatively to the population number, more intensive

at Thévenon than at Servotte, leading the breeding population to be composed of a greater

proportion of young animals. Such a hypothesis supposes that adult frogs reproduce more

Source : MNHN, Paris

JoLy 87

than once. In Switzerland, at an altitude of 600 m, frogs seem to spawn twice during their

life span (RYSsER, 1986), but age structures observed at low elevation in Ireland (GiBBONS

& MCCARTHY, 1984) and Spain (ESTEBAN RUIZ, 1990) indicate that adult mortality is so

high that most females breed only once. Al these hypotheses concern factors influencing

maturation and longevity; determination of the age structure of each population becomes

essential. The influence of harvesting will only be determined by comparing age structures

of the present populations with populations which are not harvested in the same region.

In Europe, the relationship between size and fecundity shows great variation from one

population to another and no clear correlation appears with altitude or latitude. Further

description of local and annual variation within populations is needed prior to

consideration of variation on a larger scale. The reproductive investment of Jurassian frogs

seems higher than that observed in more Northern populations. SAVAGE (1961: 82)

postulated (from data of BOULENGER and HÉRON-ROYER) that the higher fecundity of

Southern frogs was an adaptation to higher tadpole mortality due to heat death. This

hypothesis remains to be tested.

RÉSUMÉ

Des comparaisons de la taille corporelle de Grenouilles rousses entre des populations

voisines en Bresse jurassienne (est de la France) montrent d'importantes variations. Les

variations de taille sont corrélées à d'importantes variations de fécondité et de taille de

l'œuf. Le nanisme est limité à des étangs qui sont tous situés dans le même massif forestier.

Toutes les populations étudiées sont soumises à une pêche par des pisciculteurs

professionnels, mais il n’est pas possible d’estimer l'impact de cette acti sur chaque

population. La petite taille des Grenouilles pourrait résulter soit d’un ralentissement de

croissance, soit d’un abaissement de l’âge d'acquisition de la maturité sexuelle, dû à la forte

mortalité induite par la pêche. Les paramètres démographiques de ces populations

françaises sont comparés à ceux d’autres populations européennes.

ACKNOWLEDGEMENTS

am particularly indebted to MM MoresTin and BOURDY, aquaculturists, for their collaboration

in this work. I thank Dominique AUGERT, Stephen D. BUSACK, Louis CAILLÈRE, Alain DUBOIS.

GoLLMANN, Dominique PONTIER, Brian K. SULLIVAN and an anonymous referee for their cri

on first drafts of the manuscript. The correction of the English version is due to Louis LEFEBVRE and

Glyn THOIRON.

LITERATURE CITED

BERVEN, K. A., 1982. — The genetic basis of altitudinal variation in the wood frog Rana sylvatica.

L. An experimental analysis of life history traits. Evolution, 36: 962-983.

Source : MNHN, Paris

88 ALYTES 9 (3)

en 1988. — Factors affecting variation in reproductive traits within a population of wood frogs

(Rana sylvatica ). Copeia, 1988: 605-615.

BERVEN, K. A. & Giiz, D. E., 1983. — Interpreting geographic variation in life-history traits. Amer.

Zool., 23: 85-97.

Cummins, C. P., 1986. — Temporal and spatial variation in egg size and fecundity in Rana temporaria.

J. anim. Ecol., 55: 303-316.

ESTEBAN RuIz, M. L., 1990. — Evoluciôn del genero Rana en la peninsula iberica: estudio de la

variabilidad morfologica y genetica del complejo Rana temporaria L. Thesis, Madrid: 1-21, pl.

I-CXLVIIT.

GiBBons, M. M. & MCCARTHY, T. K., 1984. — Growth, maturation and survival of frogs Rana

temporaria L. Holarctic Ecology, 7: 419-427.

ES 1985. — The reproductive output of frogs Rana temporaria (L.) with particular reference to body

size and age. J. Zool., Lond., 209: 579-593.

HAAPANEN, A., 1970. — Site tenacity of the common frog (Rana temporaria L.) and the moor frog

(R. arvalis Nilss.). Ann. Zool. Fennici, 7: 61-66.

Juszczvk, W., 1959. — The development of the reproductive organs of the female common frog

(Rana temporaria L.) in the yearly cycle. Ann. UMCS, Lublin, 14: 169-231.

KoskELA, P. & PASANEN, S., 1975. — The reproductive biology of the female common frog, Rana

temporaria L. in Northern Finland. Aquilo, (Zool.), 16: 1-12.

KosLowskA, M., 1971. — Difference in the reproductive biology of mountain and lowland common

frogs, Rana temporaria L. Acta biol. Cracov., 16: 17-32.

MARTOF, B. S. & HUMPHRIES, R. L., 1959. — Geographic variation in the wood frog, Rana sylvatica.

Am. Mid. Nat., 61: 350-389.

NEvo, E., 1972. — Climatic adaptation in size of the green toad (Bufo viridis ). Israel J. Med. Sci.

8: 1010.

OLDHAM, R. S., 1963. — Homing behaviour in Rana temporaria L. Brit. J. Herpetol., 3: 116-127.

Perrus, D. & ANGLETON, G. M., 1967. — Comparative reproductive biology of montane and

piedmont chorus frog. Evolution, 21: 500-507.

READING, C. J., 1988. — Growth and age at sexual maturity in common toads (Bufo bufo) from two

sites in Southern England. Amphibia-Reptilia, 9: 277-288.

-- 1990. À comparison of size and body weights of common toads (Bufo bufo) from two sites in

Southern England. Amphibia-Reptilia, 1: 155-163.

RYSsER, J., 1986. — Altersstruktur, Geschlechterverhältnis und Dynamik einer Grasfrosch-Population

(Rana temporaria L.) aus der Schweitz. Zool. Anz., 217: 234-251.

= 1988 a. — Determination of growth and maturation in the common frog, Rana temporaria, by

skeletochronology. J. Zool., Lond., 216: 673-685.

== 1988 b. — Clutch parameters in a Swiss population of Rana temporaria. Herpetol. J., 1: 310-311.

SAVAGE, R. M. 1961. — The ecology and life history of the common frog (Rana temporaria

temporaria). London, Pitman & Sons: 1-221.

STARS, S. C. & KoëLA, J. C., 1986. — The evolution of phenotypic plasticity in life-history traits:

predictions of reaction norms for age and size at maturity. Evolution, 40: 893-913.

Corresponding editor: Stephen D. BUSACK.

Source : MNHN, Paris

AINTTES

International Journal of Batrachology

published by ISSCA

EDITORIAL BOARD FOR 1991

Chief Editor: Alain Dumois (Laboratoire des Reptiles et Amphibiens, Muséum national d'Histoire

naturelle, 25 rue Cuvier, 75005 Paris, France).

Deputy Editor: Günter GOLLMANN (Institut für Zoologie, Universität Wien, Althanstr. 14, 1090 Wien,

Austria

Other members of the Editorial Board: Jean-Louis AMIET (Yaoundé, Cameroun); Stephen D. BUSACK

(Ashland, U.S.A.); Tim HaLLiDay (Milton Keynes, United Kingdom): William R. HEYER

(Washington, U.S.A.); Walter HôbL (Wien, Austria): Pierre JOLY (Lyon, France); Milos

KALEZIÉ (Beograd, Yugoslavia); Raymond F. LAURENT (Tucumän, Argentina); Petr ROTH

(Libechov, Czechoslovakia); Borja SANCHIZ (Madrid, Spain); Dianne B. SEALE (Milwaukee,

U.S.A.); Ulrich SinscH (Bonn, Germany).

Index Editor: Annemarie OHLER (Paris, France).

GUIDE FOR AUTHORS

Alytes publishes original papers in English, French or Spanish, dealing with amphibians. Beside

papers reporting results of original research, consideration will be given for publication to review

articles, comments and replies, and to papers based upon original high quality color photos of

amphibians, showing beautiful or rare species, interesting behaviors, etc.

The title should be followed by the name(s) and addresses) of the author(s). The text should be

organized as follows: English abstract, introduction, method, results, discussion, conclusion, French

or Spanish abstract, acknowledgements, literature cited.

Figures and tables should be mentioned in the text as follows: fig. 4 or Table IV. Figures

should not exceed 16 X 24 cm. 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 (SOMEONE, 1989; EVERYBODY et al.,

1980; So & So, 1987). References in the literature cited section should be presented as follows:

— when in a periodical:

INGER, R. F., Vois, 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.

- when in a multi-authors book:

GRAF, J.-D. & PoLLs PELAZ, M., 1989. — Evolutionary genetics of the Rana esculenta complex. In:

R. M. DAWLEY & J. P. BOGART (eds.), Evolution and ecology of unisexual vertebrates, Albany, The

New York State Museum: 289-302.

— when a book:

BourRET, R., 1942. - Les Batraciens de l'Indochine. Hanoï, Institut Océanographique de l’Indochine:

i-x+1-547, pl. I-IV.

Manuscripts should be submitted in triplicate to Alain DuBois (address above) if dealing with

amphibian morphology, systematics, biogcography, evolution, genetics or developmental biology, or

to Günter GOLLMANN (address above) if dealing with amphibian population genetics, ecology,

ethology or life history.

Âcceptance for publication will be decided by the editors following review by at least two

referees.

No page charges are requested from author(s), but the publication of color photographs is

charged. For each published paper, 25 free reprints are offered by Alytes to the author(s). Additional

reprints may be purchased.

Published with the support of

the Muséum national d'Histoire naturelle (Paris, France).

Directeur de la Publication: Alain Dupois.

Numéro de Commission Paritaire: 64851.

Source : MNHN, Paris

Alytes, 1991, 9 (3): 61-88.

Contents

Arturo I. KEHR & Juan A. SCHNACK

Predator-prey relationship between giant water bugs (Belostoma oxyurum)

and larval anurans (Bufo arenarum) ...............,................... 61

HaCssUesOf A I)rEs AndiG rca tes ET LUN LR mere nee 70

Jean-Louis AMIET

Images d’Amphibiens camerounais.

IVe constructeurs ide nids REA Re ARR er ne 71

Application for membership of ISSCA

AN OFSUDSCTIPUONNO AIDES EURE dense nent Ne et 78

Pierre JOLY

Variation in size and fecundity between neighbouring populations in the

COMMON ATOS M RANA NL EMPONArIA I eee seen sel es De 79

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: 3" trimestre 1991.

Source : MNHN, Paris