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ALYTES

INTERNATIONAL JOURNAL OF BATRACHOLOGY

November 2009 Volume 27, N° 2

Alytes, 2009, 27 (2): 37-48.

Mating strategies and monogamy

in a territorial breeding anuran,

Rana dalmatina: a result of sexual conflict?

Thierry LODÉ

UMR CNRS 6552 ETHOS, Université de Rennes 1,

Campus de Beaulieu, 35042 Renne

<thierry.lode@univ-renne

In anurans, sexual conflict of interest between the sexes over the mating

system should be exacerbated by external fertilization and male-biased

sex-ratio. However, the agile frog Rana dalmatina exhibits numerous

monogamous characters despite a lack of parental care. Each caller was

found to defend a distinct territory but, upon the female arrival, the

frequency of calling males decreased. The number of observed amplexus

and the number of clutches were strictly equal to the number of females.

Examining sexual differences in the optimal mating system, sexual par:

ism (4.2 %), synchronous polyandry (5.2 % of the clutches) and successive

polygyny (4.2 %) were found as alternative strategies. Genetic polyandry

was evidenced in 18 % of the clutches. Satellite a ies are related to the

increase of competitive interactions and result in a strong female harass-

ment. Thus, sexual conflict influenced the development of alternative

strategies. These results suggest that female multiple amplexus may be

regarded as a forced mating strategy resulting in a coercive polyandry. In

contrast, resulting both from the male territorial behavior and from the

synchronous arrival of females, the prevalent monoandrous mating system

should reduce the sexual antagonism.

jothèque Centrale Muséum

INTRODUCTION

In most species, males can maximize their fitness by multiplying mates with numerous

partners, whereas females cannot increase their progeny by mating with many males (BATE-

MAN, 1948; ARNOLD & DUVvALL, 1994). This reasoning led to the hypothesis that most

monogamous or monoandrous breeding systems chiefly depend upon restricted access to

resources or on the need for parental care, and emphasized the role of female mate choice

CWITTENBERG & TiLsON, 1980; CLUTTON-BROCK, 1989; REYNOLDS, 1996). Thus, mating

system and pair cooperation are affected by resource dispersion in numerous socially mono-

gamous birds (DAVIES, 1989; KEMPENAERS, 1995). Interestingly, breeding systems have proven

more perplexing than previously imagined. Thus, the reasons why animals are monogamous

PARIS / Source : MNHN, Paris

38 ALYTES 27 (2)

are unclear when no resources are defended and no parental care occurs. Furthermore,

numerous recent studies have revealed a growing evidence for multiple mating in several

species formerly regarded as socially monoandrous. Polyandry is found practically ubiquitous

in insects (ARNQvIST & NILSSON, 2000), but it was also inferred in reptiles (MADSEN et al.,

1992), birds (BIRKHEAD & MOLLER, 1995; HASSELQUIST et al., 1996; DOUBLE & COCKBURN,

2000) and mammals (HOOGLAND, 1998; SCHENK & KovACs, 1995; WiLMER et al., 2000).

Because of their external fertilization mode and their generally weak or inconsistent

parental care, multiple mating and sperm competition should be common phenomena in

anuran amphibians (ROBERTS et al., 1999). The promiscuity of males chorusing in breeding

congregations (HALLIDAY & THJEDO, 1995; HAKANSSON & LOMAN, 2004) should facilitate

multiple paternities in egg masses by simple spermatic diffusion. Moreover, many anuran

species exhibit a noticeable sexual size dimorphism in favor of females and a male-biased

sex-ratio (GEISSELMANN et al., 1971; BLAB, 1986; READING et al., 1991; LoDé et al., 2005), since

males arrive precociously and usually stay for a longer time than females in the breeding site.

Such à male-biased sex-ratio could increase competitive interactions and may result in

multiple males amplecting with a single female (FUKUYAMA, 1991; JENNIONS et al., 1992;

Hazribay & THEDO, 1995). Surprisingly, only few studies referred to genetic polyandry

within a single clutch in the wild although multiple amplexus were commonly reported in

anurans. Polyandry as a result of multiple amplexus was revealed by DNA finger printing in

Agalychnys callidryas (D'ORGEIX & TURNER, 1995). Similarly, synchronous polyandry was

inferred from protein electrophoresis in Crinia georgiana (ROBERTS et al., 1999) and in Rana

dalmatina (LODÉ & LESBARRÈRES, 2004; Lopé et al., 2004). Moreover, multiple spawning was

observed in Leptodactylus (PRADO & HADDAD, 2003) and high multiple paternity was evi-

denced from egg masses in Rana temporaria (LAURILA & SEPPÀ, 1998). It may be alleged that

polyandry provides no real advantages for most anurans showing a lack of parental care

{see REYNOLDS, 1996), but the potential for multiple genetic paternity was not often investi-

gated.

By contrast, there are some anuran species in which multiple amplexus were rarely or

never observed, so that they could be regarded as socially monoandrous species. Here

monoandry refers to a female mating with a single male (but a male may have several

successive amplexus), whereas monogamy corresponds to a single male mating with a single

female. Thus, the agile frog Rana dalmatina could be thought as a typically monoandrous

species, as one female releases a single clutch during the breeding season and synchronous

multiple amplexus has never been reported (GEISSELMANN et al., 1971; BLAB, 1986; HETTYEY

et al., 2005). It is however difficult to hypothesize how monoandry could be favoured in the

absence of evolutionary advantages. Most of studies on sexual selection focused on female

mate choice but the evolutionary question rests in the asymmetry of interest between the

sexes, i.e., the sexual conflict (RICE, 2000). Resulting from the deviation of potential fitness of

males and females, sexual conflict is virtually omnipresent and stems from competition

zation of eggs (RICE, 2000). Genetic interest of male and female

do not only diverge but, in frogs, the sexual conflict should be exacerbated by the male-biased

sex ratio and the external fertilization. Agile frogs do not form choruses and, as most

precocious breeding anurans, do not forage during the breeding season, so that neither

resource dispersion nor the need for parental care do clearly influence their reproductive

behavior and monoandry. Competition within sexes mostly leads to alternative mating

between males for the fer

Source : MNHN, Paris

LODÉ 39

strategies (TABORSKY, 1994; Lucas & HowaRD, 1995), but the evolution of such tactics may

increase the variance in reproductive success (NErF, 2001) and therefore influence the conflict

between the sexes (GAVRILETS et al., 2001; JONES et al., 2001). Consequently, it could be

predicted that male and female should adopt different optimal mating strategies as a result of

sexual conflict (RICE, 2000; see also LODÉ, 2006). Actually, although there is a lack of

empirical studies, the sexual conflict is proved to raise an important issue in evolutionary

biology (GAVRILETS et al., 2001; CHAPMAN et al., 2003), but how monogamy may reduce the

sexual conflict is still hardly ever evoked.

Widely found throughout Europe, the agile frog Rana dalmatina is a nocturnal and

terrestrial anuran which gathers in small breeding congregations during approximately 20

days from February to March. Amplexus is axillary and frog amplecting pairs are distant

from each others.

By examining variations in the agile frog mating system, this paper aims at investigating

whether sexual differences in optimal mating result in alternative reproductive strategies.

Exploring the basis of sexual conflict, i.e., alternative strategies in male-biased frog popula-

tions, this work contributes to the understanding of the maintenance of monoandrous

strategy in animals.

MATERIAL AND METHODS

MATING STRATEGIES

Field study was conducted in four breeding ponds near Redon (47°34°N, 2°50°W),

western France, from 1998 to 2000. One month before the breeding period, every pond was

fenced by a plastic canvas associated to buckets covered with a transparent and semi-rigid

plastic. Males arrived some days earlier than females and spent more time in the pond.

Captures were surveyed twice daily in order to intercept all breeding individuals. Frogs were

marked (toe-clipping) and then released in the breeding pond. The breeding adult sex-ratio

(ASR) was calculated as total number of males captured / total number of females captured.

A quadrat with 2 m grid was set one month before in the four ponds surveyed by five observers

deployed around the ponds. Frogs were located at dusk using a night optic and male locations

were recorded on the quadrat map. The radius of the area of male breeding locations was

estimated by measuring the distances among 72 callers. The number of caller males was

estimated every night between 21 and 24 h by both auditory and visual localization by five

observers, and the number of satellite males (i.e., with no calling activity) was estimated by the

difference between number of callers and number of intercepted males. Samples of callers,

satellites and females were hand caught, measured and immediately released. Reproductive

events and aggressive behavior were monitored every night throughout the breeding season.

As soon as the amplecting frogs were spawning, some animals were hand caught and

measured. Every female was released after spawning. The objective of this procedure was to

minimize all perturbations. The stress of frogs was considered as minimal since animals were

rapidly hand caught, measured and immediately released. Every observed animal resumed

normal behaviors (calling, moving or amplecting) after release.

Source : MNHN, Paris

40 ALYTES 27 (2)

Table 1. Effective number of alleles (EN), observed heterozygosity (Ho) and non-biased expected

heterozygosity (Hxs) (average + standard deviation) in Rana dalmatina tadpoles collected in

four ponds.

| EN Ho Hxs n

| Pondi 33 04332 + 0.061 0.5876 + 0.056 132

Pond 2 3.33 0.3909 + 0.120 0.5773 + 0.072 165

Pond 3 | 3.33 0.4130 + 0.125 0.5760 + 0.065 143

Pond 4 3.33 A 0.4022 + 0.099 0.5934 + 0.083 210

Mean heterozygosity 0.4079 + 0.094 0.5863+ 0.069 650

PATERNITY ANALYSIS

Some eggs (less than 10 %) were randomly collected from 28 separated clutches to avoid

diffuse fertilization and hatching tadpoles (7 = 22-24 per clutch for a total of 650 tadpoles)

were reared during 20 days in constant environmental conditions. Regarding ethical consider-

ations, less than 10 % of eggs were collected to minimize the impact on frog populations as

our goal was only to demonstrate multipaternity and only 22-24 tadpoles from collected

clutches were instantaneously killed for genetic analysis using MS222. The others were

released on the site. Paternity was inferred from allozymic data following LAURILA & SEPPÀ

(1998) and RoBERTS et al. (1999). Polymorphic loci of offspring were analyzed by starch gel

electrophoresis using standard techniques. Samples were homogenized in equal volume of

distilled water and centrifuged at 10,000 g for 15 minutes at 4°C. Migration was performed

using two buffe s-citrate pH6 and Tris-EDTA-borate pH8. Slices were stained for

revealing five specific enzymes encoded by six polymorphic loci with 2 to 5 alleles (tab. 1).

From allozymic data, F-statisties were performed using Genetix software (BELKHIR et al.,

Genetix@crit.univ-montp2.fr) and Popgenes 32 (YEH et al., 1997). Allozyme phenotypes

were considered evidences for heritable genotypes, and multipaternity was estimated using

PAPA 1.0 (DUCHESNE et al., 2002). The purpose was to determine a minimal set of loci based

on the expected number of parents, the possibility of sexing parents and the level of

genotyping error. The parentage allocation method used in PAPA is based on the likelihood

that a parental pair produces multilocus genotypes found in the tested offspring. In calculat-

ing likelihood, mating is assumed to be random and all potential parents are supposed to have

equal reproductive capability. Some deviation from the latter conditions will not seriously

impair the efficiency of the allocation process. Since every female produces a single clutch

during the breeding season, the program PAPA simulates parental genotypes allowing

estimating the minimal number of genitors for each clutch. Monoandry refers to genetic

evidence of mating with a single male and polyandry with two males at least. Polygyny refers

to the observation of one male fertilizing successively several clutches with no genetic

evidence.

Source : MNHN, Paris

LODÉ 41

120

100

aFemales

mMales

Château Le cormier La Haye Vernon

Fig. 1. Male-biased sex-ratio in the four studied ponds as revealed by the total number of individuals

intercepted.

RESULTS

MATING STRAT S

The adult sex-ratio was male-biased in every pond, averaging 2 males per females (SD =

0.6, ASR range 1.48-2.82, n = 288 frogs; fig. 1) with no significant differences among ponds

(2=4.75, df. = 3, P = 0.19). No frogs were detected in the ponds before spring dispersal, and

therefore agile frogs did not hibernate under water in ponds. As soon as they arrived, most

males (78.3 %, n = 92) entered the ponds and exhibited a calling activity. Each caller defended

a distinct territory ranging 2.1 m in diameter (+ 0.9 m, » = 72), so that callers were widely

separated, and some other males arrived progressively (total males n = 192). Male intrusions

into another male calling place were followed by brief chases. Females arrived with a mean of

6.5 days later than first males, but the sex-ratio remained male-biased averaging 2.0 males for

a female (SD = 0.6, range 1.48-2.82, total females » = 96). With the female arrival, the

frequency of calling males decreased to reach only 52.6 % (7 = 192 males: fig. 2) and breeding

(amplexus) extended for 9 days until the last female departure. Numerous males (47.4 %)

moved around the pond side exhibiting a satellite behavior searching for mate opportunities.

The mean size of callers, averaging 47.7 mm (+ 5.6 mm, nr = 38), was significantly higher than

the size of satellites (44.1 mm + 4.4 mm, n = 32; 1 = 2.97, d.f. = 68, P < 0.02).

AMPLECTING PAIRS

The number of observed amplexus and the number of clutches were strictly equal to the

number of females (n = 96). Over 83.3 % of females entered water alone and went towards the

Source : MNHN, Paris

4 ALYTES 27 (2)

250

200

150

Dsatellites

Mn callers

100

at the beginning after female arrival

Fig. 2 - Respective number of caller and satellite males in the breeding pond at the beginning

of the breeding period and after the arrival of females.

callers. However, in 16 cases (16.7 %), when a female approached the water, some male

satellites tried amplecting dorso-laterally, ventrally or even over the legs of females. Hostility

between sexes was evidenced since females actively rejected them. Most observed male

satellites (68.8 %) gave up their amplexus attempts as soon as they intruded a caller territory

or were actively rejected by the caller. After amplecting male and female left the clutch, some

male satellites (4.2 %, n = 4 on 97) exhibited a sexual parasitism, by attempting to come above

the clutch. Only five multiple amplexus on 96 (5.2 % versus 94.8% in mono-amplexus, n = 96)

were observed for a very brief period so that the proportion of observed multiple amplexus

was significantly lower than the proportions of attempts by satellites (z = -2.544, P = 0.01).

Amplecting pairs were distant from each others and females released a single clutch and

then went back. The caller persisted to have a calling activity after this first amplexus during

a mean of 8 days. In only four cases (4.2 ), a second female was found to consent to an

amplexus with a caller which had already fertilized a clutch, realizing a successive polygyny

some days after the first amplexus (mean = 3 days, range 1-5). Numerous (45 %) caller males

switched for alternative behavior during the breeding period.

PATERNITY ANALYSIS

Five analyzed loci (u-gdh, Ldh-1, Ldh-2, Mpi and 6-Pgdh) exhibited a pattern with at least

three alleles, but enzyme Pgm showed a di-allelic pattern. The effective number of alleles per

locus was 3.33. Among the ponds, observed heterozygosity ranged from H, = 0.433 to H, =

Source : MNHN, Paris

LODÉ 43

Table 2. - Polyandry evidences and off$pring proportion resulting from a fertilization by a second

male in five multiple paternal clutches as inferred from PAPA software.

Proportion of Proportion of

offspring offspring

nanalysed nestimated fathers | correspondingto | corresponding to a

offspring (minimum) | the first male second male

Clutch 1 24 2 0.708 0.291

Clutch 2 24 2 0.792 0.208

Clutch 3 22 2 0.727 0.273

Clutch 4 22 2 0.818 0.182

Clutch 5 _22 2 0.773 0.227

Total 114 | Mean = 2 Mean = 0.763 Mean = 0.238

0.391 (tab. 2) and most loci showed significant deviation from Hardy-Weinberg equilibrium as

it could be expected in samples structured into sub-samples, here clutches.

In most clutches (82.1 %, » = 28), paternity could be assigned to a single male per clutch

using different simulations. However, for five clutches (17.9 %), a single male was unlikely to

have fathered the offspring, and at least two males had shared paternity, evidencing multipa-

ternity. In each multi-paternal clutch, a single male fertilized on average 76.2 % of the eggs

whereas only 23.8 % of the eggs could be attributed to a second male, with no significant

differences among clutches —1.207, P = 0.11, tab. 2). No evidence for a third male

fathering some tadpoles was found. Because clutches were sampled at distance from each

others on different male territories, the results could not be attributable to two females. The

proportion of clutches evidencing multiple paternity did not significantly differ from the

proportion of satellite amplexus attempts (z = 0.148, P = 0.441) but was significantly higher

than the proportion of observed multiple amplexus (z = 2.163, P = 0.01). Nonetheless,

because of male pond fidelity resulted in male relatedness, multiple paternity may be higher

than found. The frequency of putative successive polygyny (4.2 %) is significantly lower than

the frequency of polyandry (17.9 %, z = 2. 46, P < 0.007).

DISCUSSION

Sexual conflict of interest between the sexes is widely considered as an evolutionary force

driving mating strategies (CARO & BATESON, 1986; GROS, 1996; GAVRILETS, 2000: GAVRILETS

et al., 2001). Indeed, interactions between sexes are recognized to influence alternative

behaviors. The present study suggests that, although both synchronous polyandry and

successive polygyny occurred in Rana dalmatina, the mating system is basically dominated by

monogamous reproductive strategies, reducing sexual conflict.

Source : MNHN, Paris

44 ALYTES 27 (2)

ALTERNATIVE STRATEGIES

In the agile frog, whereas large males (callers) defend territories based on call advertise-

ment, other males (satellites) actively move searching for mate opportunities. Since the

discovery of sexual parasitism in the tree frog (PERRILL et al., 1978), callers and alternatively

satellites have often been identified in breeding anurans (HowaRD, 1984; ARak, 1988). Male

strategies can vary throughout the lifetime. Mature dominant frogs can use durable calling

activities, wWhereas young and subordinate animals should only adopt a search for mate

behavior (LOMAN & MADSEN, 1986; HOUSTON & MCMaMARA, 1987; LUCAS & HOWARD,

1995). Agile frogs do not hibernate under water in ponds before their breeding dispersal and

males have to control a call area in the spawning pond. Because the cost of defending a

territory depends upon the level of competition, mature males may switch for alternative

behaviors if the sex-ratio is strongly male-biased. Male-biased sex-ratio was often evidenced

in anuran populations (GEISSELMANN et al., 1971; READING et al., 1991; Lopé et al., 2005) but

was rarely documented in agile frogs (BLAB, 1986). In agile frogs, callers are significantly larger

than satellites but have to actively defend their exclusive breeding territory each time a satellite

intrudes. Although callers show a better mating success (LESBARRI et al., 2008), call

advertisement constitutes a strong attractive cue for females but the call activity remains

insufficient to exclude all satellites (LESBARRÈRES & LODÉ, 2002). Satellites move around the

pond searching for mate opportunity and try to catch any female approaching the water.

Nonetheless, most satellites do not keep the benefit of this effort and have to renounce or are

evicted by the caller as soon as the female arrives in a caller territory. In most cases, satellites

fail amplecting but they may marginally succeed if the caller is not vindictive enough. As it

was observed in other anuran species (ROBERTS et al., 1999), such amplexus are rarely dorsal

but lateral or even ventral and therefore can only lead to a partial fertilization. Thus the

satellite strategy allows certain males to partly fertilize a clutch realizing a genetic polyandry.

Satellite activities should be related to the increase of competitive interactions and mainly

result from mating rivalry in which males compete over access to females, some males

switching to alternative behavior as soon as the first females arrive. Therefore, multiple

amplexus may be regarded as a forced mating strategy resulting in a coercitive polyandry.

Moreover, such simultaneous polyandrous mating do not seem to allow a better fertilization

as BYRNE & ROBERTS (1999) demonstrated in Crinia georgiana. Nevertheless, polyandry may

be also thought of as a result of a secondary fertilization. Some satellite males show a sexual

parasitism trying to fertilize the clutch of another pair. JENNIONS & PASSEMORE (1993)

demonstrated the capability of sperm release by a second male in Chiromantis. Although in

Rana dalmatina male territorial behavior perseveres and leads to a guarding behavior, such a

secondary fertilization may explain the apparent discrepancy between the apparent number

of multiple amplexus and the frequency of multiple paternity. Actually, multiple paternity

should be underestimated in agile frogs both because allozymic variations are not the best

genetic marker for polyandry and because of the breeding site fidelity of most anurans (see

READING et al., 1991). Breeding site fidelity should result in increasing relatedness of breeding

adults.

Anyway, whether multiple mating results from forced mating or secondary fertilization,

the polyandry should restrict the evolutionary influence of female mate choice and reduce the

opportunity for sexual selection (see JONES et al., 2001). However, the females actively move

Source : MNHN, Paris

LoDé 45

towards a caller territory. Although females go to breeding territories where no female laid a

clutch, alternatively some females may have amplexus with a polygynous male. Such polygyny

consists in a successive polygyny since these females release their clutch in the same territory

where a male fertilized a first clutch a few days ago. The reason why those females appeared to

avoid mating with a previously mated male is not clear. In numerous fish species, females are

more attracted by a male which guarded a clutch (BisazZA & MARRCONATO, 1988; WARNER et

al., 1991). But, in the agile frog, polygyny occurs marginally and may be interpreted as a

prudent strategy performed by an inexperienced female by copying the behavior of an

experienced female (SIROT, 2001). Anyway, the relative synchrony of spawning events restricts

their opportunity to mate with a previously mated male. Moreover, the rareness of this

strategy suggests that it is little eMicient for improving the fitness. Females may restrain their

polygyny to avoid the competition risk unfavorable to the tadpoles of the second clutch.

Negative competitive interactions in tadpoles were widely reported (WiLBUR, 1982: TRAVIS.

1984; GRiIFFITHS, 1991; FARAGHER & JAEGER, 1998; BARNETT & RICHARDSON, 2002). More-

over, hatched after the first, these tadpoles may suffer cannibalism from tadpoles of the first

clutch (CRUMP, 1983).

THE RESULTING MATING SYSTEM

Although multiple paternity was found in at least four distinct anuran species (D'ORGEIX

& TURNER, 1995; LAURILA & SEPPÀ, 1998; ROBERTS et al., 1999; LoDÉ & LESBARRÈRES, 2004),

their mating behavior greatly differed. The territorial defense of an exclusive individual

breeding site promoted the prevalent monoandrous character of the agile frog. Indeed, both

polyandry and polygyny were found to be marginal strategies and agile frogs exhibited

numerous monogamous characters. As illustrated by numerous bird species (DAVIES, 1989:

SANDELL, 1998), it has been proposed that female competition was the key factor for the

evolution of monogamy (the female aggression hypothesis: WITTENBERG & TILSON, 1980).

Nonetheless, antagonistic interactions hardly ever occurred in monogamous females and

seemed unlikely to produce the frog monogamy. Mainly based on mammals, it has been also

argued that monogamy evolves due to the need for parental care (CLUTTON-BROCK, 1989).

Association between males and females may provide both a best feeding and safety to the

progeny. Nevertheless, that monogamy was promoted by parental care was rarely supported

by investigations on mating systems and was only found as special cases (KOMERS & BRo-

THERTON, 1997). The level of sociality of mammal females is the main parameter which

influenced the male capability to control them (EMLEN & ORING, 1977; BROTHERTON et al..

1997), and KOMERS & BROTHERTON (1997) proposed that monogamy in mammals is bi y

due to their solitary habits rather than the need for parental care. Relating monoandry to

female arrivals and dispersion of brecding males, our results suggest that monoandry in

anuran is chiefly associated with the territorial breeding behavior of males and with the

relative synchrony of females arrivals. Using small exclusive breeding territory, the male

behavior followed the prediction that sexual territory should be small enough to allow males

to defend them.

Actually, any deviation from monogamy results in an increase of sexual conflict, since in

à monogamous mating system any trait that enhances the fitness of one sex also improves the

fitness of the other. The main advantage of monogamy is that both male and female produce

Source : MNHN, Paris

46 ALYTES 27 (2)

most offspring whe: polygyny results in better success only in some males. Whereas sexual

differences in mating may result in alternative reproductive strategies, the optimal response of

agile frogs to the sexual conflict converges towards a monogamous breeding system achieving

a sexual equilibrium. Resulting both from the male territorial behavior and from the synchro-

nous arrival of females, the prevalent monogamous mating system reduces the sexual conflict.

The reason why frogs adopt a monogamous mating system may be related to the fact that

monogamy yields genetic benefits.

ACKNOWLEDGEMENTS

Lthank Prof. Jon Loman who provided helpful comments on the previous version, and

Hélène Birard, Hélène Blanchard, Romain Criou, Dominique Le Jacques, Stéphanie Mareau,

Marc Pondaven, Julie-Anne Rio, Yann Rigault and Sébastien Sellos for their field as

istance.

ARAK, A. 1988

ARNOLD, SJ. & DuvaLL. D. 1994, - Animal mating systems. à synthesis based on sel

Nat. 143: 317-348

ARNovist, G, & Nirsson., T., 2000, - The evolution of polyandry, multiple mating and female fitness in

insects. Anim. Behav., 60: 145-164.

Banner, K. H. & RicHapson, JS. 2002. - Predation risk and competition effects on the life-history

characteristics of larval Oregon spotted frog and larval red-legged lrog. Oecologia, 132: 436-444.

BATEMAN, A. J., 1948. - Intrasexual selection in Drosophila. Heredity, 2: 349-368

BirkneaD, T. R. & MoiLeR, A. P., 1995. - Extra pair copulation and extra pair paternity in birds. Anim.

Behur., 49: 843-848.

BisAZZA, À. & MARCONATO, À. 1988. - Female ma , male-male competition and parental care in

the river bullhead Cortus gobio. Anim. Bel 52-1360.

BLAB, 1. 1986. — Biologie, Okologie und Schut= von Amphibien. Bonn & Bad Godesberg, KildaVer

1-150.

BROTHERTON, P. N. M, PEMRERTON, J. M. KomiRs, P. E. & Mararky, G., 1997. - Genetic and

behavioural evidence of monogamy in a mammal, Kirk’s dik-dik (Madoqua kirkit). Proc. r Soc

Lond. (B), 264: 675-681.

BYRNE, P. G. & ROBERT D.. 1999. - Simultaneous mating with multiple males reduces fertilization

success in the myobatrachid lrog Crinia georgiana. Proc. r Soc. Lond.. (B), 266: 717-721.

Caro T, M. & BATESON, P., 1986. - Organization and ontogeny of alternative tacties. Anim. Behav. 34:

1483-1499.

Ciarman, T.. ARNovIST, G., BANGHAM, J. & ROWE, L., 2003. - Sexual conflict. Trends in Ecol. Evol., 18:

41-47.

Ciurrox-Brock, T. H., 1989, - Mammalia mating systems. Proc. r Soc. Lond. (B), 236: 339-372

Crumr, M. L. 1983. Opportunistie cannibalism by amphibian larvac in temporary aquatie environ-

ments, An. Nat. 121: 281-289.

D'ORGEX, CA. & TURNER, B. J., 1995

{Cope). Mol. Ecol., 4: 505-508.

Davis, N. B.. 1989, - Sexual conflict and the polygamy threshold. Anim. Behar., 38: 226-234.

ction theory. An

e choic:

ag:

Multiple paternity in the red-eyed treefrog Agalrchnis callidrvas

Source : MNHN, Paris

LoDÉ 47

DousLe, M. & CoCKkBURN, A., 2000. Pre-dawn infidelity, females control extra-pair mating in superb

fairy wrens. Proc. r. Lond., (B), 267: 465-470.

DUCHESNE, P., GobBoUT, M.-H. & BERNATCHEZ, L., 2002. - PAPA { Package for the Analy:

Allocation), a computer program for simulated and real parental allocation. Mol. E

191-194.

S. T. & ORING, L. W., 1977. - Ecology, sexual selection, and the evolution of mating systems.

Science, 197: 215-22:

FARAGHER, S. G. & JAEGER, R. G., 1998. - Tadpole bullies, examining mechanisms of competition in a

community of larval anurans. Can. J. Zool., 76: 144-153.

FUKUYAMA, K., 1991. — Spawning behaviour and male mating tactics of a foam-nesting treefrog,

Rhacophorus schlegelii. Anim. Behav., 42: 193-199,

GAVRILETS, S., 2000. - Rapid evolution of reproductive barriers driven by sexual conflict. Nature, 403:

886-889.

GAVRILETS, S., ARNQVIST, G. & FRIBERG, U., 2001. — The evolution of female mate choice by sexual

conflict. Proc. r Soc. Lond., (B), 268: 531-539.

MANN, B., FLINDT, R. & HEMMER, H., 1971. - Studien zur Biologie, Okologie und Merkmalsva-

riabilität der beiden Braunfroscharten Rana temporaria und Rana dalmatina. Zool. J. Syst., 98:

521-568.

GRirriTHs, R. A., 1991. - Competition between common frog, Rana temporaria, and natterjack toad,

Bufo calamita, tadpoles, the effect of competitor density and interaction level on tadpole develop-

ment. Oikos, 61: 187-196.

Gross, M. R., 1996. - Alternative strategies and tactics, diversity within the sexes. Trends in Ecol. Evol..

11: 92-98.

HAKANSSON, P. & LoMAN, J., 2004. - Communal spawning in the common frog Rana temporaria. Egg

temperature and predation consequences. Ethology, 110: 665-680.

HALLIDAY, T. R. & TEEDO, M., 1995. — Intrasexual selection and alternative mating behaviour. Zn: H

HEATWOLE & B. K. SULLIVAN (ed.), Amphibian biology, 2, Social behaviour, Sydney, Surrey Beatty:

419-468.

HASsELQUIST, D., BENSCH, S. & VON SCHANTZ, T., 1996. - Correlation between male song repertoire,

extra-pair paternity and offspring survival in the great reed warbler. Nature, 381:

Herrvey, À. Torok, J. & Hevrzi, G., 2005. - Male mate choice lacking in the agile frog, Rana dalmatina.

Copeia, 2005: 403-408.

HOOGLAND, J. 1998. — Why do female Gunnison's prairie dogs copulate with more than one male?

Anim, Behav., 55: 351-359.

Houston, A. I. & MCMamaRA, J. M., 1987. — Singing to attract a mate, a stocha

theor. Biol., 129: 57-68.

HowaRD, R. D., 1984. - Alternative mating behaviors of young male bullfrogs. 4m. Zool., 24: 397-406

JENNIONS, M. D. & PASSEMORE, N. L., 1993. — Sperm competition in frogs, testis size and a “sterile male”

experiment on Chiromantis xerampelina (Rhacophoridae). Biol. J. Linn. Soc., 50: 211-220.

JENNIONS, M. D., BLACKWELL, P. R. Y. & PASSEMORE, N. L., 1992. — Breeding behaviour of the African

frog, Chiromantis xerampelina, multiple spawning and polyandry. Anim. Behav., 44: 1091-1100

A. G., WaLkER, D., KVARNEMO, C., LINDSTRÔM, K. & AVISE, J. C., 2001. - How cuckoldry can

decrease the opportunity for sexual selection, data and theory from a genetic parentage analysis of

and goby. Proc. natn. Acad. Sci. USA, 98: 9151-9156.

KemPENAERS, B., 1995. — Polygyny in the blue tit, intra and intersexual conflict. Anim. Behav, 49:

1047-1064.

Kowers, P. E. & BROTHERTON, P. N. M. 1997. - Female space use is the best predictor of monogamy in

mammals. Proc. r. Soc. Lond., (B), 264: 1261-1270.

LAURILA, À. & SEprx, P., 1998. - Multiple paternity in the common frog (Rana temporaria), genetic

evidence from tadpole kin groups. Biol. J. Linn. Soc, 63

‘of Parental

ol. Notes, 2:

EMLE)

tic dynamic game. J

JONES,

LesnarRÈRes, D. & Loné, T., 2002. - Variations in male calls and res to unfamiliar advertisement

call in à territorial breeding anuran, Rana dalmatina: evidence for a dear enemy effect. Ethol. Ecol

Evol., 14: 287-295.

LesnaRRÈRES, D. MERILA J. & Loni, T., 2008. - Male breeding success is predicted by call frequency in

a territorial species, the agile frog (Rana dalmatina). Can. J. Zool., 86: 1273-1279.

Source : MNHN, Paris

48 ALYTES 27 (2)

LoDÉ, T., 2006. - La guerre des sexes chez les animaux, une histoire naturelle de la sexualité. Paris, Odile

Jacob: 1-368.

Lobé, T., HoLvEck, M. J. & LESBARRÈRES, D., 2005. - Asynchronous arrival pattern, operational sex

ratio and occurrence of multiple paternities in a territorial breeding anuran, Rana dalmatina. Biol.

J. Lin. Soc., 86: 191-200.

LODÉ, T., HOLVECK, M. J., LESBARRÈRES, D. & PAGANO, A., 2004. — Sex-biased predation by polecats

influent he mating system of frogs. Proc. r Soc. Lond., (B), 271: S399-S401.

Lobi, T. & LessarrÈRes, D., 2004. - Multiple paternity in Rana dalmatina, a monogamous territorial

breeding anuran. Naturwissenschaften, 91: 44-47.

LOMAN, J. & MADSEN, T., 1986. - Reproductive tactics of large and small male toads Bufo bufo. Oikos, 46:

57-61

LUCAS, J. R. & HowarD, R. D., 1995. - On alternative reproductive tactics in anurans, dynamic games

with density and frequency dependence. Am. Nat, 146: 365-397.

T.. SHINE, R., LOMAN, J. & HAKANSSON, T., 1992. - Why do female adders copulate so

frequently? Nature, 355: 440-441.

NërF, B. D., 2001. - Alternative reproductive tactics and sexual selection. Trends in Ecol. Evol., 16: 669.

Maps

Perkil, S. A. GErHarT, H. C. & DaniEL, R., 1978. - Sexual parasitism in the green trecfrog (Hyla

cinerea). Science, 200: 1179-1180.

Prabo, C. P. À. & HADDAD, C. F. B., 2003. - Testes size in leptodactylid frogs and occurrence of multiple

spawning in the genus Leprodactylus in Brazil. J. Herp., 37: 354-362.

READING, C. J., LOMAN, J. & MADSEN, T., 1991. - Brecding pond fidelity in the common toad, Bufo bufo.

J. Zool., London, 225: 201-211.

REvNOLDS, J. D. 1996. - Animal breeding systems. Trends in Ecol. Evol., M: 68-72.

Rice, W. R. 2000, - Dangerous liaisons. Proc. nan. Acad. Sci, USA, 97: 12953-12955.

D.. SranDis, R. J., BYrNr, P. G. & DouGnry, P., 1999. - Synchronous polyandry and

multiple paternity in the frog Crinia georgiana (Anura, Myobatrachidae). Anim. Behar., 57:

721-726.

Saveur, M. L, 1998. — Female aggression and the maintenance of monogamy: female behaviour

predicts male mating status in European starlings. Proc. r. Soc. Lond., (B), 265: 1307-1311.

Scnexk, À. & Kovacs, K. M. 1995. — Multiple mating between black bears revealed by DNA

fingerprinting. Anim. Behav., 50: 1483-1490

Siror, E. 2001. - Mate-choice copying by females, the advantages of a prudent strategy. J evol. Biol, 14:

418-423.

Tanorsk, M.. 1994. — Sneakers, satellites and helpers, parasitic and cooperative behavior in fish

reproduction. Ady. Stud. Behar., 21: 1-100.

Travis, J., 1984. — Anuran size at metamorphosis, experimental test of a model based on intraspecific

competition. Ecology, 65: 1155-1160.

WaRNER, R. R. WERNERUS, F., LEJEUNE, P. & VAN DEN BERGHE, E., 1991. - Dynamics of female choice

for parental care in a fish species where care is facultative. Behav. Ecol., 6: 73-81.

Wizeur, H. M., 1982. - Competition between tadpoles of Hyla femoralis and Hyla gratiosa in laboratory

experiments. Ecologr, 63: 278-282.

Wiimer, J. W., OVERALL, À. J., POMEROY, P. P., Twiss, S. D. & Amos, W., 2000. - Patterns of paternäl

relatedness in British grey seal coloni 9: 283-292,

3. F. & TiLsoN, R. L., 1980. - The evolution of monogamy, hypothesis and evidence. Ann

ol. Syst., 1: 197-232.

Ven, EC, YANG, R. €. BOYLE, T. BJ, Yr, Z. & XIYAN, J. M. 1997, - POP-GENE, the user-friendly

shareware for population genetic analysis. Edmonton, Canada, Molecular Biology and Biotechno-

logy Centre, University of Alberta: 1-28

Corresponding editor: Franco ANDREONE.

Source : MNHN, Paris

Alytes, 2009, 27 (2): 49-61. 49

A new species of the genus Quasipaa

(Anura, Ranidae, Dicroglossinae)

from northern Vietnam

Alain Dugois & Annemarie OHLER

Reptiles et Amphibiens, UMR 720$ OSEB,

matique et Evolution, Muséum national d'Histoire naturelle,

25 rue Cuvier, CP 30, 75005 Paris, France

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

Département de Sy

A new species of the genus Quasipaa from northern Vietnam is

described and compared with four related species from China: Quasipaa

spinosa, Q. jiulongensis, Q. exilispinosa and Q. courtoisi, the latter being

here confirmed, on morphometric grounds, as a distinct species. Q. cour-

toisi differs from the four other species by measurements concerning the

hands, feet and head. The new species is further distinguished from Q.

exilispinosa by its larger webbing. It is a sibling species of Q. spinosa from

which it differs by a higher number of nuptial spines on the prepollex and

finger I of breading males.

INTRODUCTION

During his travels of exploration of the Chinese Empire, the father Armand David

discovered a large frog living in torrents of the mountains in the surroundings of Jinjiang

(Jiangxi Sheng), the breeding males of which emit a strong and loud call and have the chest

and fingers covered with black horny spines. He described it as new on two occasions, first

(Davib, 1872: 76) as Rana latrans, a nomen which later proved invalid, being a junior primary

homonym, and later (Davib, 1875: 253) as Rana spinosa. This species is still known under the

latter specific nomen, but it is now referred to the genus Quasipaa Dubois, 1992 (Ranidae,

Dicroglossinae, Paini; see JIANG et al., 2005; OnLEr & Dugois, 2006; FRosr et al., 2006; CHE

et al., 2009).

Although many nomina have been proposed in the literature for species of the genus

Quasipaa, OniEr & Duois (2006) only recognized 11 valid species in this genus. Among

these, two informal groups can be distinguished by the aspect of their warts on the mid-dorsal

skin: a group of seven species with longitudinally elongate, regularly arranged warts, some of

which are quite wide and prominent: and a group of four species with smaller warts, not very

prominent, rounded or slightly elongate, or if elongate not wide and regularly arranged on

Source : MNHN, Paris

50 ALYTES 27 (2)

back. The latter group can be provisionally designated as “Quasipaa sensu stricto”, as it

includes Rana spinosa, the type-species of Quasipaa, whereas for the former group the generic

nomen Eripaa Dubois, 1992 (type-species Rana fasciculispina Inger, 1970) would be available

if it proved holophyletic and had to be recognized formally as a subgenus. The four species of

“Quasipaa sensu stricto” recognized by OuLEr & Dugois (2006) include three species recog-

nized by all recent authors (e.g., Fer, 1999; Fr et al., 2006; CHE et al., 2009), i.e., Quasipaa

exilispinosa (Liu & Hu, 1975), Quasipaa jiulongensis (Huang & Liu, 1985) and Quasipaa

spinosa (David, 1875), and a species, Quasipaa courtoisi (Angel, 1922), usually considered as

a synonym of the latter. Recent molecular data (CHE et al., 2009) suggest that additional

species probably require recognition in this group.

Most species of Quasipaa are endemic to China, but a few of them occur in the eastern

part of the Indochinese peninsula (Cambodia, Laos, Thailand and Vietnam). One of them

was reported under the nomen Rana spinosa spinosa by BOURRET (1937, 1942) on the basis of

14 adult specimens collected by him on the Mau Son (then spelt Mao-Son) in northern

Vietnam. Six of these specimens (5 males, 1 female) are still kept in the collections of the Paris

Museum under the numbers MNHN 1938.0001-0006. A seventh specimen from the same

series was transferred to the Edward H. Taylor collection and later to the Field Museum in

Chicago, where it is still kept under the number FMNH 123883 (Alan Resetar, personal

communication). Two additional specimens of the same species from Mau Son are known to

exist in collections. The first additional one was collected in 1903 by H. Frühstorfer between

915 and 1220 m (3000-4000 ft) in the Mau Son, along with several other frog species

(BOULENGER, 1903; BOURRET, 1942: 13). It was identified as Rana spinosa by BOULENGER

(920: 75). It is still kept in the Natural History Museum collection in London under the

number BMNH 1903.7.2.26. Finally, a second additional specimen was part of the collection

of herpetological specimens made by J. Delacour and W. P. Lowe in Tonkin and Annam in

1926 and 1927: this specimen, stated to be from Lang Son, is also probably from Mau Son

(BOURRET, 1942: 291). It was identified by H. W. Parker as Rana duboisreymondi and reported

under this nomen by ANGEL (1928). It is still present in the Paris Museum collection under the

number MNHN 1928.0025.

Although by their overall aspect these Mau Son specimens indeed resemble Chinese

specimens of Quasipaa spinosa, they differ from them in a few respects, as dis ed below. We

used morphometric data to compare them with numerous Chinese specimens referred to the

four species of “Quasipaa sensu stricto”. This analysis revealed constant and significant

differences between the Vietnamese specimens and all Chinese specimens, and we consider

that they demonstrate the existence of a distinct species in Vietnam, which is described and

named here.

MATERIAL AND METHODS

Appendix 1 provides a list of the specimens of “ Quasipaa sensu stricto” examined and

measured for this study, along with the abbreviations used to designate the collections where

they are kept. Specimens were sexed using their external characters (in the case of adult

breeding males) or through a slight lateral incision in order to see one of the gonad. AII

Source : MNHN, Paris

Dugois & OHLER 51

specimens examined in this study were adult, according to the criteria of DuBois (1976:

31-33).

Appendix 2 provides a list and descriptions of the measurements taken on these speci-

mens. Measurements were obtained with a slide calliper to the nearest 0.1 mm, or, for values

below 5 mm, with an ocular micrometer to the nearest 0.01 mm. For univariate comparisons

between samples, all measurements except snout-vent length (SVL) were transformed in ratio

to SVL, expressed in per thousands (%). Subgroups were composed according to two possible

criteria: taxonomic allocation and sex.

Univariate morphometric comparisons between samples were made using the non-

parametric Mann-Whitney U test (ZAR, 1984). Multivariate factor analyses were performed

using the Principal Component Analysis (PCA) with varimax rotation as implemented in the

software SPSS (ANONYMOUS, 1999: 426). According to the Kaiser criterion, eigenfactors

larger than 1 where retained (Norusis, 1992). Factors of PCA were plotted as scatterplots

indicating species allocation. To examine effects of species delimitation on the principal

component scores, factorial ANOVA were performed. Calculations and statistical analyses

were realised using SPSS statistical software (Norusis, 1992).

The holophoront (holotype) of the new species was described in detail using the same

format and methodology as in several of our previous works on Asian anurans, in particular

ranids (OHLER & DuBois, 1999; Dusois & OHLER, 2000, 2001, 2005; Dugois et al., 2001; VEITH

et al., 2001; OHLER et al., 2002). Some of the terms used below (holophoront, hypodigm,

onymotope) were defined elsewhere, and reasons were provided for using them (DuBois, 2000,

2005). The traditional terms of equivalent meaning are indicated below on first use between

parentheses.

TAXONOMY

Quasipaa acanthophora sp. nov.

fig. 1)

Etymology of specific nomen. — From the Greek æyavoe, “spine” and #00 , “I bear”. This

nomen is the Greek equivalent of spinosa in Latin.

Holophoront (holotype). - MNHN 1938.0001 (ex LZUH Z.108), adult male, SVL 101.7 mm.

Onymotope (type locality).- Mau Son (21°51°N, 106°58°E), Lang Son province, Vietnam.

Other specimens of the hypodigm (paratypes). - MNHN 1938.0002 (ex LZUH Z.107),

1938.0003 (ex LZUH Z.106), 1938.0004 (ex LZUH Z.115) and 1938.0006 (ex LZUH Z.109),

and FMNH 123883 (ex LZUH Z.112), 5 4, SVL 83.0-99.5 mm; and MNHN 1938.0005 (ex

LZUH Z.113), 1 ®, SVL 81.0 mm: all collected by René Bourret in the same locality as the

holophoront. MNHN 1928.0025, 1 4, SVL 79.0 mm, collected in 1926 or 1927 by Jean

Delacour and Willoughby Prescott Lowe in the same region. BMNH 1903.7.2.26, 1 young d,

SVL 61.3 mm, collected in 1903 by Hans Frühstorfer on the same mountain. Seven additional

Source : MNHN, Paris

52 ALYTES 27 (2)

Fig. 1. Quasipaa acanthophora sp. nov., holophoront MNHN 1938.0001, adult male, SVL 101.7 mm. (a)

Dorsal view: (b) ventral view: (c) right lateral view of head; (d) ventral view of right foot.

specimens (LZUH B.103-105, B.107,Z.110-111, Z.116) were reported by BOURRET (1942: 26)

from the ity and probably belonged in the same species. We have been unable until

now to locate any of them in current collections, but some might be rediscovered in the future.

However, because we have been unable to examine them, we refrain to formally designate

them as paratypes of the new species.

same loc:

Description of the holophoront. — (A) Size and general aspect. — (1) Specimen of large size

(SVL 101,7 mm), body rather stout.

(B) Head. — (2) Head rather large, wider (HW 41.0 mm) than long (HL 38.5 mm; MN

32.2 mm; MFE 25.1 mm; MBE 17.2 mm), flat above. (3) Snout rounded, slightly protruding,

Source : MNHN, Paris

Dusois & OHLER 53

its length (SL 14.4 mm) longer than horizontal diameter of eye (EL 11.2 mm). (4) Canthus

rostralis indistinct, loreal region concave, flared in cross section. (5) Interorbital space flat,

smaller (IUE 8.1 mm) than upper eyelid (UEW 9.0 mm) and internarial distance (IN 10.0 mm):

distance between front of eyes (IFE 15.3 mm) about three fifth of distance between back of

eyes (IBE 26.8 mm). (6) Nostrils oval, with flap of skin laterally, closer to eye (EN 6.8 mm)

than to tip of snout (NS 7.8 mm). (7) Pupil indistinct. (8) Tympanum indistinct. (9) Pineal

ocellus present, between anterior borders of eyes. (10) Vomerine ridges present, bearing

numerous small teeth (7 = 10), between choanae, with an angle of 60° relative to body axis, as

close to choanae as to each other, longer than distance between them. (11) Tongue large,

cordate, emarginated; median lingual process absent: tooth like projection on maxilla absent.

25.2 mm), distinctly enlarged. (13) Finger I rather long and strong; finger II rather short,

rather strong; finger II rather long and strong (TFL 12.8 mm); finger IV short, relatively thin.

(14) Relative length of fingers, shortest to longest: IT < 1 < IV < IE. (15) Tips of fingers

rounded, slightly enlarged, without discs. (16) Fingers IT and III with dermal fring ebbing

absent. (17) Subarticular tubercles prominent, rounded, single, all present. (18) Prepollex

oval, prominent; two oval, distinct palmar tube pernumerary tubercles absent.

(D) Hindlimbs. — (19) Shank three times longer (TL 53.5 mm) than wide (TW 18.8 mm),

about as long as thigh (FL 52.8 mm) and distance from base of internal metatarsal tubercle to

tip of toe IV (FOL 52.2 mm). (20) Toes rather short and thin: toe IV (FTL 28.9 mm) more

than one third of distance from base of tarsus to tip of toe IV (TFOL 72.1 mm). (21) Relative

length of toes, shortest to longest: 1 < II < V < III < IV. (22) Tips of toes rounded, distinctly

enlarged, without dises. (23) Webbingcomplete: 10-O110-OH10-01VO-OV(WTF 16.1 mm:

WFF 14,5 mm; WI 14.4 mm; WII 11.6 mm). (24) Dermal fringe along toe V well developed,

from tip of toe to basis of metatarsus. (25) Subarticular tubercles very prominent, oval, simple,

all present. (26) Inner metatarsal tubercle long, prominent: its length (IMT 8.3 mm) 1.7 times

in length of toe I (ITL 14.2 mm). (27) Tarsal ridge present, two thirds of distal parts of tarsus.

(28) Outer metatarsal tubercle, supernumerary tubercles and tarsal tubercle absent.

(E) Skin. — (29) Dorsal and lateral parts of head and dorsal part of back shagreened with

regularly disposed glandular warts on back: upper part of flanks shagreened with elongated

glandular warts; lower part of flanks with foldings. (30) Dorsolateral folds absent; lateral line

ervaryan line” absent: supratympanic fold prominent, from eye to above

arm; cephalic ridges absent: co skin absent. (31) Dorsal

shagreened: thigh shagreened with thin foldings; legs shagreened with thin foldin

spinules; tarsus smooth. (32) Ventral parts of head, chest and limbs smooth: belly with

transversal foldings. (33) No macroglands.

(F) Coloration in alcohol. - (34) Dorsal and lateral parts of head and body: dorsum

brown with dark brown spots around the warts: a dark brown band across upper eyelids and

head: upper part of snout clearer, light brown: upper part of flank like back: lower part of

flank brown with light marbling; loreal region light brown with dark brown bands: tympanic

region light brown with a dark brown band underlining tympanic fold: upper lip light brown

with three distinct vertical dark brown bars. (35) Dorsal parts of limbs: forelimbs, dorsal part

of thigh, leg and foot brown with indistinct darker bands: posterior part of thigh dark brown

Source : MNHN, Paris

54 ALYTES 27 (2)

Table 1. Maximum numbers of nuptial spines in brecding males of Quasipaa courtoisi, Q. exilispinosa, Q. jiulongensis. ©.

spinosa and Q. acanthophora. The table gives the total number of spines on breast and the maximum numbers of spines

observed on one arm (either left or right) in a given place (ppxmax, prepollex; imax, finger [; iimax, finger Il: iimax,

finger 111). Number of specimens observed is given in brackets. For Q. spinosa only males of size interval corresponding

to adult size in Q. acanthophora were included in the analysis. The Mann-Whitney U test compares the spine numbers of

Q. spinosa and Q. acanthophora. Significance level: ***, P< 0.001; **, P < 0.01

Spine number! Q.courtoisi Qexilispinosa Q jiulongensis Qspinosa ©. acanthophora Mann-Whitney Uuest

brest | 1533#372(7) #16:607(12) 1069:632(27) 1308+27.0(14) 139.54 145.9(6) u=3

“| is 0.198 0284 B#-171 0322 P-0s4lns.

xmax | ATHIOR(G) 94452012) 1134107027 18456014) 30.54 14.1 (6) u-7

set DRE 77 256 20 19.55 Poe

imax | 1590 28493(12) 3909421507 679+1S0(14) 1524238 (6) u-0

| 1342 22128 48-91 96-162 P= 0.000 ++

2764153($) O1463(12) 15928207 234+67(14) 35.84 15,6(6) U- 195

10-51 0-19 445 1-4 23-59 P-0062ns.

jüimax | 11341044) 17425012) 4+4607 7945704) 185415.6(6) U-325

M | 3-26 07 o-14 117 4-38 P-0444ns.

‘able 2. Snout-vent length and ratio of SVL to body measurements for adult males and female of Quasipaa acanthophora.

Ï " KE Males CAEN RER Males

Mesuvnens | Ms Meunnens| Mes Female [éme] Mi

Poon (OR go À | où |'ensn [07

F | 79-101.7 7 94-98 « 274-302

mwsu [AS us 'ensve | 6047 Go |'ammen, | 234

| 3824 3x : 1544.77 ; , +775

ms RU on ua [ST un | man 7 vu

320 1 8,76 a re 2524 17.66 . 162 à 5.93 V

CT TPE CO PE

| 263 + 1286 % 2384 10.4 143465

mes [21286 2 uns, [an 2e L'une | és a

16 à 10.6 Siam 181568

MBESVL | aus 170 TELSVL (De 127 WISVL Tour 182

Lissiros ET a | 17175

mesu LUE on nan JS ss umo [UNS im

svc Sr : 523 à 17.29

IBESVL | Us ou 257 FOLSVL | Vo3.sat 535

with light brown flecks. (36) Ventral parts: throat and chest brown with whitish marblings:

margin of throat whitish with brown spots; belly dirty whitish; thigh dirty white with brown

marbling on sides; webbing brown.

(G) Male secondary sex characters. - (37) Large-sized, black nuptial spines present on

prepollex and finger 1 (two separate pads), fingers IT and III and chest. Table 1 gives the

numbers of spines in these places on both hands. (38) Forearms enlarged. (39) Vocal sacs

indistinct on throat: pair, rounded openings posterior on mouth floor.

Variation. — The other members of the hypodigm are similar to the holophoront in most

respects. Variation concerning morphometrie measurements is summarized in table 2. The

dorsal colour of specimen MNHN 1938.0002 is different as this specimen is not more or less

uniformly dark brown with indistinct darker spots near warts, but lighter brown with distinct

dark brown patches including a band between the eyes. Six out of seven specimens show

elongate fine warts either on lateral part of back or all over back.

Source : MNHN, Paris

Dugois & OHLER 55

Table 3. - Principal component analysis using marivax rotation with Kaiser normalization of factor loadings for adult males of

Quasipaa courtoisi, Q. exilispinosa, Q. jiulongensis, Q. spinosa and Q. acanthophora

À. Total variance explained

" Initial cigenval | Rotation sums of squared loadings

Total % of variance Cumulative% | Toul Cumulative %

1 7.908 34.382 34382 | 5609 24.388

2 4262 18531 2913 | 5000 46.519

3 2.651 11.524 ar | 355 61.702

4 1713 7448 TLSKS | 2.063 70.760

5 1.041 4527 76412 | 1.300 76412

B. Rotated component matrix

Component | Compon

1 2 3 4 5 1 2 3 4 on

SvL |0676 “0151 024 0506 016 20676 “0151 0294 0506 0.163

RHW | 0063 0700 0077 -0289 0319 | RIN | 0428 0152 0271 0711 -0.058

RHL | 0404 0804 “0025 0236 0054 | REN |-0045 0362 0012 0057 0.754

RTL 0729 0233 0046 0215 0091 REL

RMN | 0300 0893 -0035 0193 0.106 | RTFL

0.507 0.569 -OIRS 0244 -0.184

0.747 0.177 0219 0117 -0.083

RMFE | 0.260 0891 0080 0.100 -0.040 | RFTL | O878 0.191 0.152 -0.006 -0.087

RMBE |-0137 0.906 -0.025 -0.11$ -0070 | RIMT |-0.105 -0296 0280 -0.100 0.648

RIFI 0227 0532 (0258 0037 -0095 | RITL | 0802 0040 0220 0030 0.116

RIBE 0498 0517 0078 O8 0087 | RWTF | 0142 O8 0876 0076 -0045

RELL | O143 “0122 0217 “0846 “0018 | RWFF | 021$ 0220 O60 “0007 0113

RHAL | 0765 0254 0055 “0095 0.052 RWI 0093 0068 0831 0297 -0.020

RFOL 0927 0050 0191 0010 0010 | RWII | 0103 0049 © OR6S 0028 0233

Comparisons with closely related species. — The new species displays the following characters

that are diagnostic of the genus Quasipaa (OnLEr & DuBois, 2006): first finger longer than

second: tarsal fold present: external fold along fifth toe extending to the base of the tarsus of

this toe; spines on chest of breeding male as a single group, not separated in two lateral

patches. Within this genus, the aspect of the dorsal warts in this species agrees with the

informal group “ Quasipaa sensu stricto”, as defined above. We provide multivariate analysis

and short pairwise comparisons with the four other species currently recognized in this group.

Principal component analysis including size-corrected measurements of Quasipaa cour-

toisi, Q. exilispinosa, Q. jiulongensis, Q. spinosa and Q. acanthophora results in 5 principal

components With a loading higher than 1 (tab. 3, fig. 2). They provide a rather good summary

of the data, accounting for 76.4 % of the total variance (tab. 3). The first principal component

shows a high loading for variables of limbs (HAL, TEL, TL, FOL, FTL, ITL); the second

principal component mainly describes head shape, having highest loadings from measure-

ments concerning head width (HW) and head length (HL, MN, MBE, MFE); the third

component is dominated by variables describing webbing (WTF, WFF, WI, WID); the fourth

component shows high loadings for forelimb length (FLL) and internarial distance (IN), and

the fifth for distance of nostril to eye (EN) and length of inner metatarsal tubercle (IMT).

Source : MNHN, Paris

56 ALYTES 27 (2)

sim sim

we] ww Gens

° K'enspinoss

longe

Gone

2004 É a 2004

. '

1004 OU AE. 100-

n LI e *-À

à o °» L

5 ÉPraI Peer £ à

Ë °°. Ë

ul op ‘o ts 000+

® 4e a

La + + +

100 5 OF CRU 1004

La *e

204 2004

—— — 5 — —

do de ce Dm 20 do 10 2w 1 où 10 2%

Factor 1 Factor 3

Fig. 2. - Resulis of multivariate morphometric analysis of adult males of Quasipau courtoisi, Q.

exilispinosa, Q. jiulongensis, Q. spinosa and Q. acanthophora. Left: plot of principal component

factor 1 against factor 2: right: plot of principal component factor 3 against factor 4.

ANOVA analysis shows that all these five principal components provide significant discrimi-

nation between the five species (tab. 4). Posthoc test shows pairwise significant differences for

some of these principal components for all groups studied. PCI allows significant di:

nation of Q. courtoisi from all other species and also to discriminate Q. spinosa from Q.

exilispinosa and Q,. jiulongensis. PC2 distinguishes Q. jiulongensis from Q. exilispinosa, Q.

spinosa and Q. acanthophora, Q. courtoisi from Q. spinosa and Q. acanthophora, and Q.

spinosa from Q. jiulongensis. PC3 separates Q. exilispinosa from all other taxa studied. PC4

shows significant differences between Q. courtoisi and Q. jiulongensis and Q. spinosa, and

between Q. exilispinosa and Q. jiulongensis. Thus all species can be discriminated from each

other by principal component analysis using morphometric characters, except for the pair

composed of Q. spinosa and Q. acanthophora.

rimi-

The results given above confirm the morphological distinction between Quasipaa cour-

toisi and the other species of Quasipaa briefly mentioned, but not documented, by OHLER &

Dumois (2006). PCT allows discriminating Q. courtoisi from the other species of this group by

lower values of the ratios to SVL of measurements which concern mainly the hands (HAL,

TFL), tibia (TL) and feet (FOL, FTL, ITL). PC2 distinguishes this species from Q. jiulongen-

sis, Q. spinosa and Q. acanthophora by ratios to SVL of measurements which concern the

head: width (HW) and length (HL, MN, MFE, MBE) are smaller in Q. courtoisi than in Q.

spinosa and Q. acanthophora. But Q. jiulongensis has larger values for HW and MBE than Q.

courtoisi, PC3 allows to distinguish Q. courtoisi from Q. exilispinosa by ratios concerning the

webbing (WTE, WFF, WI, WI) which are larger in Q. courtoisi than in Q. exilispinosa.

Source : MNHN, Paris

Dunois & OHLER O7:

# + Ospinosa

vs © acanthophor

1504

e. 1254

ë € x .

Ë 4 ë .

É É “3

Es 100- .

o ° o

204 o°

e CU o o

o° o

CE Les Q

104 o fe G] ss

o o

504 ®

750 mo #59 00 950 100 1050 750 800 850 900 950 1000 1050

sul si

Fig. 3.- Maximum numbers of nuptial spines present on prepollex (ppxmax) and finger 1 (imax), relative

to snout-vent length (SVL) in adult brecding males of Quasipaa spinosa and Q. acanthophora. The

value used for each specimen is the maximum number of spines displayed in each frog either on the

right or on the left hand.

PCI distinguishes the new species from Q. courtoisi by larger ratios of SVL of measure-

ments concerning the hand (HAL, TEL), tibia (TL) and feet (FOL. FTL, ITL). PC2 allows

distinction of these two species by ratios of SVL of measurements concerning the head (HW.

HL, MN, MFE, MBE) which are larger for Q. acanthophora than for Q. courtoisi. PC3

discriminates the new species from Q. exilispinosa by ratios of measurements which concern

the webbing(WTE, WFE, WI, WID), which is larger in Q. acanthophora than in Q. exilispinosa.

The new species must be considered a sibling species of Quusipaa spinosa (David, 1875)

as it does not differ in any of the morphometrical measurements or ratios. Nevertheless this

may be due to the heterogencity of the sample used in this study and considered to be Q.

spinosa. This sample includes specimens from various regions of China (see app. 1) that are

morphologically variable and which most probably consist of several spe Here we

recognize the Vietnamese population as a distinct species as these specime n be distin-

guished by sexual characters. In many Paini species, adult males show large black spines on

various parts of the forelimbs, chest and sometimes venter. Although within a species the

number of spines varies according to age and reproductive stage, in several cases very similar

species can be distinguished by the number of spines present in some locations (DuBois, 1976:

Duois & MATSUI, 1983). Figure 3 shows the numbers of nuptial spines on the prepollex and

finger 1 for specimens of Q. acanthophora and Q. spinosa of similar body sizes. These numbers

are significantly different and the numbers of spines on finger I does not even overlap between

the two groups: 14 males of Q. spinosa have 48-91 spines, whereas 6 males of Q. acanthophora

have 96-162 spines. (tab. 1).

Source : MNHN, Paris

58 ALYTES 27 (2)

Beside these differences in male nuptial spines, Q. acanthophora differs from Q. spinosa in

the aspect of warts on back, which are fine and elongate, whereas they are rounded in Q.

spinosa. The dorsal warts of Q. spinosa bear dark, keratinized spinules. These spinules are

absent or small and not keratinized in Q. acanthophora. Both species exhibit keratinized spines

on the dorsal surface of shanks.

Q. acanthophora can be distinguished from @. exilispinosa by adult size, the latter being

much smaller. In the sample of the latter species that we measured (see app. 1), SVL of 13 4

ranges from 40.0 to 69.0 (mean 55.9 + 8.40) and that of 11 © ranges from 48.5 to 64.9 (mean

55.6 + 4.66). Among our Q. acanthophora sample, SVL of 6 & ranges from 79.0 to 101.7

(mean 92.1 + 9.18) and that of our single © is 81.0 mm. If we consider that all the 14

specimens reported by BOURRET (1937) were indeed members of this species (which is quite

likely, as all samples of Bourret's amphibian collection in the Paris Museum prove to be

monospecific, even if they now bear a different nomen, which suggests that this excellent

naturalist had a good “feeling” for species identification), then the extreme values in the Viet-

namese species become 89-123 in and 84-104 in ©, which shows no overlap with Q. exilispi-

nosa. À single & specimen of our sample from Vietnam (BMNH 1903.7.2.26, SVL 61.3 mm)is

included in the range of adult males of Q. exilispinosa, but, although it shows some spines on

prepollex and fingers Land IL, itis not yet fully adult, as shown by absence of spines on finger III,

so we did not include it in our calculations of tab. 1. Beside size, these two species are also distin-

guished by webbing, which is less extended in Q. exilispinosa: significant differences between

them exist for all four webbing measurements used in this study. Q. exilispinosa can also be dis-

tinguished by its much lower number of nuptial spines on fingers and breast.

The new species can be distinguished from Q. jiulongensis by the shape of the head, which

is distinctly longer and larger in Q. acanthophora. Males of Q. jiulongensis also have signifi-

cantly smaller numbers of spines on prepollex and fingers I and II.

Finally, the new species differs from Q. courtoisi in head shape. The head is distinctly

longer in Q. acanthophora, which shows more distant nares and eyes. The tibia, foot, toes,

hand and fingers are longer in Q. acanthophora, and the webbing between toes III and IV is

less developed in Q. courtoisi.

ACKNOWLEDGEMENTS

We are grateful to all the curators who allowed us to examine specimens under their care: D. R. Frost

and C. W. Myers (AMNH), B. T. Clarke (BMNH), L. Fei and C. Ye (CIB), A. Resetar and H. Voris

(EMNH), J. Rosado (MCZ) and W. Bôhme (ZFMK). We would also like to thank R. Bour and J.

Marmayou (MNHN) for their help in the preparation respectively of the tables and figures for publica-

tion.

Source : MNHN, Paris

DuBois & OHLER 59

LITERATURE CITED

ANONYMOUS, 1999, — SPSS advanced models 9.0. Chicago: SPSS Ink

ANGEL, M. F., 1928. - Reptiles et Batraciens recueillis en Indo-Chine par la

Lowe. Bull. Mus. natn. Hist. nat., 34: 445-447.

BOULENGER, G. A., 1903. - Descriptions of three new batrachians from Tonkin. Ann. Mag. nat. Hist., (7)

12 (9): 186-188.

ee 1920. - A monograph of the South Asian, Papuan, Melanesian, and Australian frogs of the genus

Rana. Rec. indian Mus., 20: 1-226.

BourRET, R., 1937. - Notes herpétologiques sur l’Indochine française. XIV. Les Batraciens de la

collection du Laboratoire des Sciences Naturelles de l'Université. Descriptions de quinze espèces

ou variétés nouvelles. Annexe Bull. gén. Instr. publ., Décembre 1937, 4: 5-56.

1942, - Les Batraciens de l'Indochine. Hanoi, Institut océanographique de l’Indochine: i-x + 1-547, 4

pl.

CHE, J., Hu, J.S., ZHou, W. W., MURPHY, R. W., PAPENFUSS, T. J., CHEN, M. Y., R4O, D. Q., Li, P. P.

& ZHANG, Y. P. 2009. - Phylogeny of the Asian spiny frog tribe Paini (family Dicroglossidae) sensu

Dubois. Mol. Phyl. Evol., 50: 59-73.

Davib, A., 1872. - Rapport adi MM les Professeurs-Administrateurs du Muséum d'Histoire

Naturelle. Bull. nouv. Arch. Mus., “1871°,7: 75-100.

—— 1875. — Journal de mon troisième voyage d'exploration dans l'Empire Chinois. Tome 2. Paris, Hachette:

Lis] + 1348, 1 map.

Dugois, A., 1976. - Les Grenouilles du sous-genre Paa du Népal (famille Ranidae, genre Rana). Cahiers

népalais. Documents, Paris, CNRS, vi + 1-275.

LE 2000. - Synonymies and related lists in zoology: general proposals, with examples in herpetology.

Dumerilia, 4 (2): 33-98.

TE 200$. - Proposed Rules for the incorporation of nomina of higher-ranked zoological taxa in the

International Code of Zoological Nomenclature. 1. Some general questions, concepts and terms of

biological nomenclature. Zoosystema, 27 (2): 365-426.

Duois, A. & Marsut, M., 1983. — À new species of frog (genus Rana, subgenus Paa) from western Nepal

(Amphibia: Anura). Copeia, 1983: 895-901.

Dusois, A. & OuLER, A., 2000. - Systematics of Fejervarya limnocharis (Gravenhorst, 1829) (Amphibia,

Anura, Ranidae) and related species. 1. Nomenclatural status and type-specimens of the nominal

species Rana limnocharis Gravenhorst, 1829. A/ytes, 18 (1-2): 15-50.

EX 2001. — À new genus for an aquatic ranid (Amphibia, Anura) from Sri Lanka. A/ytes, 19 (2-4):

81-106.

— 2005. - Taxonomic notes on the Asian frogs of the tribe Paini (Ranidae, Dicroglossinae). 1

Morphology and synonymy of Chaparana aenea (Smith, 1922), with proposal of a new statistical

method for testing homogencity of small samples. Journal of natural History, 39 (20): 1759-1778.

Dusois, A., OHLER, A. & Buu, S. D., 2001. — A new genus and species of Ranidae (Amphibia, Anura)

from south-western India. Alytes, 19 (2-4): 53-79.

Fu, L. (ed.), 1999. — Arlas of amphibians of China. Zhengzhou (China), Henan Press of Science and

Technology: [i-ii] + 1-432. [In Chinese.]

Fer, L., YE, C., JIANG, J., XIE F. & HUANG, Y., 2006. — An illustrated key 10 Chinese amphibians. Sichuan

i-xv + 1-497.

on de MM. Delacour et

Publishing Group, Sichuan Publishing House of Science & Technology: 1-352. [In Chinese].

FRosT, D. R., GRANT, T., FAIVOVICH, J., BAIN, R. H., HAAS, A. HabDAD, C. FE B., S4, R. O. DE,

CHANNING, A. WILKINSON, M., DONNELLAN, S. C., RAXWORTHY, C. JL, CAMPBEI A., BLOTTO,

B. L., MOLER, P., DREWES, R. C., NUSSBAUM, R. A., LYNCH, I. D., GRi

2006. - The amphibian tree of life. Bull. Amer. Mus. nat. Hist., 297: |

JIANG, J., DUROIS, A., OHLER, A., TILLIER, A, CHEN, X., XIE, F. & STüci

relationships of the tribe Paini (Amphibi Ranidae) based Ke partial sequences of

mitochondrial 12S and 168 rRNA genes. Zoological Science, 22: 353-3

Norusis, M.J., 1992. - SPSS for Windows. Professional Statistics. Release 5. Hors SPSS Inc.: [i-xii] +

1-348.

, D. M. & WHrëLER, W. C..

370.

. 2005. — Phylogenetic

Source : MNHN, Paris

60 ALYTES 27 (2)

Our, A. & Dunots, A. 1999. - The identity of Elachyglossa gyldenstolpei Anderson, 1916 (Amphibia,

Ranidae), with comment on some aspects of statistical support to taxonomy. Zoologica scripta, 28

(3-4): 269-279.

= 2006. — Phylogenetic relationships and generic taxonomic of the tribe Paini (Amphibia, Anura,

Ranidae, Dicroglossinae), with diagnoses of two new genera. Zoosystema, 28 (3): 769-784.

OHLER, A., SWAN, S. R. & DaLTRy, J. C., 2002. - A recent survey of the amphibian fauna of the

Cardamom Mountains, southwest Cambodia with descriptions of three new species. Raffles Bull.

Zool., 50 (2): 465-481

Ver, M., KosuCH, JL, Our, A. & Dumois, A., 2001. - Systematics of Fejervarya limnocharis (Graven-

horst, 1829) (Amphibia, Anura, Ranidae) and related species. 2. Morphological and molecular

variation from the Great Sunda.Islands (Sumatra, Java, Borneo) with definition of two species.

Alytes, 19 (1): 5-28.

., 1984. - Biostatistical analysis. Second edition. Englewood Cliffs, Prentice-Hall International,

Corresponding editor: Stéphane GROSIFAN.

APPENDIX |

LIST OF SPECIMENS EXAMINED AND MEASURED

Beside the hypodigm of the new species described above, we examined and measured 133 specimens

of the four other species here referred 10 the “Quasipaa sensu stricto” group. They are currently or were

formerly kept in the following collections: American Museum of Natural History, New York, USA

(AMNH): Natural History Museum, London, United Kingdom (BMNH); Chengdu Institute of Bio-

logy, Chengdu, China (CIB); Field Museum of Natural History, Chicago, USA (FMNH); Laboratoire de

Zoologie de l'Université de Hanoï, Vietnam (LZUH); Museum of Comparative Zoology, Harvard, USA

(MCZ); Muséum National d'Histoire Naturelle, Paris, France (MNHN); Zoologisches Museum und

Forschungsinstitut Alexander Koenig, Bonn, Germany (ZFMK).

Quasipaa courtoisi (Angel, 1922). - CHINA. Anhui Province: Cheki: BMNH 1947.2.1.86, MCZ 17458,

MNHN 1922.0093, MNHN 1923.0014, MNHN 1923.0016, MNHN 1923.0018-0021, 9 &; MNHN

1923.0022-0025, 4 ©.

Quasipaa exilispinosa (Liu & Hu, 1975). Cina. (A) Fujian Province: (1) Chungan Xian: AMNH

29575-29576, BMNH 1956.1.9.78, 3 d: AMNH 28892, 1 9: (2) Daiyun Shan: CIB 920037, 1 d: CIB

920038, 19: (3) Kuatin: ZFMK 9723, 1 4: ZFMK 9726, 1 ©. (B) Hong Kong: The Peak: BMNH

1956.1.9.79-81, BMNH 1974.2122-2124, MNHN 1988.7892, MNHN 19944504, 9 d: BMNH

1956.1.9.82, BMNH 1974.2126-2128, MCZ 9423-9424, MNHN 1988.7801, MNHN 1988.7893, 8 ©

Quasipaa jiulongensis (Huang & Liu, 1985). - CHiNA. Figian Province: (1) Chungan Xian: AMNH

28804-28895, AMNH 28907, AMNH 28909, AMNH 28913, AMNH 28920, AMNH 28922-28026,

AMNH 29655-29656, AMNH 29659, AMNH 29661-29662, AMNH 29668, AMNH 29675, AMNH

29677, AMNH 29679-29681, AMNH 29684, AMNH 29745-29748, 27 €: AMNH 28008, AMNH

28910-28912, AMNH 28914-28016, AMNH 29485, AMNH 29660, AMNH 29663-29665, AMNH

29669-29671, AMNH 29673-29674, AMNH 29676, AMNH 29678, AMNH 29749-29750, CIB 64 1 1962,

22 9: (2) Wuyi Shan: CIB 920047, 1 ®

Quasipaa spinosa (David, 1875). - CHiNA. (A) Fujian Province: (1) no locality: AMNH 30824, 1 4: (2)

Amoy: AMNH 44396, 1 ©: (3) Chungan Xian: AMNH 05410, AMNH 05412, AMNH 28896, AMNH

29198-29199, AMNH 29480-29481, AMNH 29657, AMNH 29667, AMNH 29672, 10 4 : AMNH 28906,

AMNH 29479, AMNH 29482, AMNH 29658, 4 %; (4) Futsing Xian: AMNH 05414-05415, 2 ®:; (5)

Kuatin: BMNH 1899.4.24,68, ZFMK 9712, ZFMK 9728, 3 4: ZFMK 9724, 1 ?: (6) Pingho: BMNH

1907.10.30.3, 1 ©; (7) Yenping: AMNH 18457, AMNH 28173-28174, AMNH 28177, 4 d: AMNH

08082, AMNH 18450, AMNH 18453-18454, AMNH 28172, AMNH 28175-28176, 7 ©.(B) Guangdong

Source : MNHN, Paris

Dugois & OHLER 61

Province: (1) no locality: BMNH 1926.10.27.1, AMNH 24314,2 8; AMNH 24315, BMNH 1926.10.27.2,

2 9; (2) Lo Fau: MCZ 11756, 1 8; MCZ 11757, 1 ©. (C) Hunan Province: Yizhang: CIB 75.1.006, CIB

75.1.011,2 &. (D) Jiangxi Province: Pinghsiang: AMNH 00669, 1 4: ZFMK 9749, 1 ©. (E) Zhejiang

Province: Ningpo: BMNH 1854.2.10.39, 1 ©.

APPENDIX 2

LIST AND DESCRIPTION OF MEASUREMENTS TAKEN ON SPECIMENS STUDIED

Body. - SVL, snout vent length.

Head. - EL, eye length; EN, distance from anterior corner of eye to nostril: HL, head length (from

posterior corner of mandible to tip of snout); HW, head width, at the angle of jaws: IBE, distance

between posterior corners of eyes: IFE, distance between anterior corner of eyes; IN, internarial distance:

IUE, minimum distance between upper eyelids; MBE, distance from posterior corner of mandible to

posterior corner of eye; MFE, distance from posterior corner of mandible to anterior corner of eye; MN,

distance from posterior corner of mandible to nostril: NS, distance from nostril to tip of snout; SL,

distance from anterior corner of eye to tip of snout; TYD, maximum tympanum diameter; TYE, distance

between tympanum and posterior corner of eye; UEW, maximum width of upper eyelid.

Forelimb. — FLL, forelimb length (from elbow to base of outer palmar tubercle): HAL, hand length (from

base of outer palmar tubercle to tip of third finger): TFL, third finger length (from base of first

subarticular tubercle).

Hindlimb. — FL, femur length (from vent to knee); FOL, foot length (from base of inner metatarsal

tubercle to tip of fourth toe); FTL, fourth toe length (from base of first subarticular tubercle to tip of

fourth toe): IMT, length of inner metatarsal tubercle; ITL, inner toe length; TFOL, length of tarsus and

foot (from base of tarsus to tip of fourth toe); TL, tibia length; TW, maximum leg width.

Webbing. — FFTF, distance from maximum incurvation of web between fourth and fifth toe to tip of

fourth toe, toes being spread; MTTF, distance from distal edge of metatarsal tubercle to maximum

incurvation of web between third and fourth toe, toes being spread: MTFF, distance from distal edge of

metatarsal tubercle to maximum incurvation of web between fourth and fifth toe, toes being spread:

TFTF, distance from maximum incurvation of web between third and fourth toe to tip of fourth toe, toes

being spread.

Source : MNHN, Paris

Alytes, 2009, 27 (2): 62-66. Book review

Asexual and metasexual vertebrates

Alain DuBois

Reptiles et Amphibiens, UMR 7205 OSEB, Département de Systématique & Evolution,

séum national d'Histoire naturelle, CP 30, 25 rue Cuvier, 75005 Pari:

<adubois@mnhn.fr>

John C. Avisr, 2008. - Clonality. The genetics, ecology, and evolution of sexual abstinence in vertebrate

animals. New York, Oxford University Press: i-xi + 1237, ISBN 978-0-19-536967-0.

The focus recently attracted on “clones” by the sheep “Dolly” arose interest in the media for clonal

reproduction, à phenomenon that had long been known by biologists. First discovered by the Swis

Charles Bonnet in 1740 in plant lice (ROSTAND, 1966), the reproduction of virgin females was called

parthenogenesis by OWEN (1849). In the 19% and 20%" century, other unusual modes of reproduction were

described under the terms of gynogenesis, androgenesis, hybridogenesis, ete. Most of these phenomena

were first obtained artificially by embryologists in experimental conditions, often in amphibians, before

being discovered in nature. Initially thought to be very rare and to occur mostly in “invertebrates”, they

were found to exist in several groups of vertebrates (fishes, amphibians and reptiles). This book proposes

à review of some of these phenomena, called clonality by John C. Avise.

An original approach of this book is to consider clonality not only at the organismal, but also at the

cellular (mitotic cell divisions) and molecular (DNA replication) levels: “an individual can be viewed as à

huge symbiotic colony of asexually derived clonemate cells” (p. 13). This approach allows to realize that

clonality is a very general feature of all living organisms and explains many of their properties.

At the organismal level, clonality is presented as the “polar opposite” of sexuality (p. 30). The

evolutionary advantages of both systems are analysed and compared from a theoretical point of view.

Nevertheless, the fact that both systems do exist in nature shows that none of them is completely superior

to the other: according to the conditions, both systems can be efficient.

The book then proceeds to an overview of the characteristics of various unusual reproductive modes,

starting with parthenogenesis, gynogenesis, “hybridogenesis” and related systems, then exploring other

curiosities like polyembryony, hermaphroditic self-fertilization or human-sponsored clonality. AI these

strange phenomena are briefly described in a very clear language and pedagogic style. This lively text is

not only descriptive but also offers many interesting reflections on the evolutionary meaning of the

phenomena observed, often with original ideas, as can be expected from à brillant theoretician of

evolution as John C. Avise. Reading this book is both a pleasure and a very stimulating exercise, as it

provokes thought and sometimes suggests views alternative to those of the author.

A real problem with this book, which is not particular to it but has long been a common feature of

many “reviews” published by English-speaking authors (see e.g. in this respect the comments by MayR,

1978), is its being largely “US-centered”, as it displays a virtually complete ignorance of scientific

literature in languages other than English. This is particularly annoying in a research field like descriptive

and experimental embryology and related ones, where many of the publications, especially in the 19% and

early 20!" centuries, were published in German, French and sometimes other languages. The presentation

Source : MNHN, Paris

Dugois 63

both of the historical facts and of the theories in this book is therefore somewhat biased, although review

papers and books on these questions exist in French and German. Nice biographical notes are provided

about some United States researchers who significantly contributed to our knowledge of clonality in

vertebrates, but the same is lacking for European workers. Hopefully, in a revised edition of this book,

these lacks will be filled, perhaps through collaborations with European colleagues.

This book ignores a distinction that was introduced almost 20 years ago (Dumots, 1991) and that is

important when dealing with such particular “reproductive modes”. The latter formula is in fact

misleading, as it mixes two very different phenomena: the mode of formation of the gametes (gametoge-

nesis) and the mode of activation of the ovum to initiate the development of what then becomes the

embryo (germinogenesis or better kinetogenesis, from the Greck kineo, “I move”, to avoid a Latin-Greck

“hybrid” term). Gametogenesis can be either sexual (with “normal” meiosis involving reductional

divisions or eumeiosis), metasexual (with modified meiosis or metameiosis) or asexual (meiosis being

absent and replaced by simple equational divisions or mitoses, i.e.. ameiosis). Whercas phenomena like

parthenogenesis, gynogenesis and androgenesis are modes of kinetogenesis, the “reproductive mode”

often called “hybridogenesis” designates in fact a particular mode of gametogenesis. The embryonic

development of the animals that show such a mode of gamete formation usually starts through a fully

“normal” kinetogenesis, i.e., fertilization or =ygogenesis. Mixing both phenomena obscures the analysi

of these evolutionary situations, and suggests a misleading “parallelism” between parthenogencsis,

gynogenesis and androgenesis on one side, and “hybridogenesis” on the other. As for the complex

mechanisms recently described in salamanders of the genus Ambystoma under the general term of

kleptogenesis (BOGART et al., 2007), it covers in fact two different phenomena, abnormal gametogencsis

and mixed kinetogenesis processes, involving both zygogenesis and gynogenesis.

The term hyhridogenesis, improperly stated in the book (p. 81) to mean “she origin of hybrids”. has

long been used in botany and z0ology to designate the phenomenon of generation of an organism

through hybridization between two organisms belonging in different species. À homonymous term was

coined by ScHULTZ (1969) to designate the “reproductive mode” of some fishes. in which in fact it points

to a particular kind of kinetogenesis. This term therefore entails several kinds of confusion and should be

abandoned. In order to have more terminological clarity, Dunots (2008a) suggested to keep terms ending

in genesis form the categories of kinetogenesis, but to use differently formed terms, ending in -poiesis. for

the categories of gametogenesis, five of which at least can be distinguished (Dunois, 2008, 20094).

Elasopoiesis is the term that applies to the gametogenesis of so-called *’hybridogenctic” organisms sensu

ScauLrz (1969), whereas 1vchopoiesis applies to the gametogenesis of so-called “kleptogenetic” organ-

isms (BoGaRT et al., 2007). Elasopoiesis results in hemiclonal heredity, with one of the parental hemige-

nomes being transmitted complete and unmodified. or almost so, to all gametes, whereas tychopoiesis is a

more complex mechanism resulting in meroclonal heredity, as it produces various kinds of gametes

bearing one or several complete hemigenomes of variable origin. either maternal. paternal or both.

Adoption of these distinctions would have made clearer some parts of the discussion of Avise’s book.

For the same reason of inappropriate terminology, terms like parthenogen or parthenogenctic (as

adjective or substantive), grnogen or grmogenctie, androgen or androgenetie, ete., Should be avoided. Let

us consider the term hrbridogen. It is defined in the Glossarr of Avise's book (p. 184) as * An individual or

strain that reproduces by hvbridogenesis”. This definition is too broad and unclear. Individuals and strains

are two different things. An individual organism can reproduce, but à strain cannot. We need diflerent

Lerms to designate organisms and strains, just like we have the terms individuals and species 10 designate

organisms and the taxa in which they belong in the case of bisexual eumeiotie panmictie specions, The

terms Avbridogen or hvbridogenetie ave in fact particularly ambiguous as they may have ar least five

different meanings: (1) an individual produced bx a phenomenon of hybridization, Le. à first generation

hybrid (this is the original and traditional meaning of the term, still of widespread use in botany): (2) an

individual produced br a hybrid (second or subsequent generation): (3) an individual (of initial hybrid

origin, but possibly many generations ago) which produces gametes by clasopoiesis: (4) an individual

produced by gametes one of which at least resulted from an elasopoietie gametogenesis: (5) an individual

which possesses hosh these latter particularities. In front of sueh a terminological confusion, it appears

urgent 10 abandon completely this term, as well as the other ones ending in gen mentioned above, and 10

use à clearly defined and non-ambiguous terminology. In the case of the term androgen. an additional

confusion is due to its being identical to à well-known term designating à male sex hormone.

Source : MNHN, Paris

64 ALYTES 27 (2)

In fact, the use of such terms in this book points to an uncertainty in the way such special organisms

should be called. The book uses various formulae to designate them, including the terms discussed above

but also “parthenogenetic lineages”, “uniseXuals”, “hiotypes”, etc. It is not always clear what these terms

actually mean, if they apply to individuals, taxa or other non-taxonomic units. Apparently, they just

designate “kinds” of organisms, but do not refer them to formal taxonomic units or taxa. This point of

view is difficult to support, because it would imply that only some of the organisms in the world belong

10 taxa, whereas some others are “outside taxonomy”. In fact, this point is little tackled in the book,

which does not present à clear position regarding the “species problem”, except that in the Glossary (p.

189) the following definition is given for species (biological): * Groups of actually or potentially interbreed-

ing individuals that are reproductively isolated from other such groups”. The taxonomic problems posed by

the special organisms” considered in the book are just mentioned in passing by Avise (e.g.. p. 62), but not

really discussed. Possibly this means that in his mind only bisexual organisms with normal gametogenesis

and kinetogenesis, 1.e. corresponding to the “Biological Species Concept” or BSC in the traditional sense

(May & AsHLOCK, 1991), can or should be treated taxonomically. But this would not be consistent with

the basic requirement that, to be acceptable, taxonomic systems should be devised in such a way as 10

accommodate all organisms in the world, whatever their characteristies (DUBOIs, 1991: 70; 2005: 372). A

quite different approach from that of Avise (and of most North American authors as well) has been

proposed (Dunois & GÜNTHER, 1982; Durois, 1991, 2007, 2008a-h, 2009h). This is based first on a clear

distinction made between species as a nomenclatural rank and as a taxonomic category.

AS a nomenclatural rank, the term species applies to a level in the nomenclatural hierarchy

corresponding to the basic unit, the “brick”, used in all disciplines of biological research (sometimes far

away from evolutionary biology and systematics, like biochemistry, physiology, pathology, etc.), and also

in all other non-scientific domains where organisms have to be unambiguously designated, such as

environmental conservation, commerce, customs, laws, etc. This is the most widespread use of the term

species. In this context, all organisms alive must be uniformly referable to à taxonomic unit of species

level, designated by a Latin binomen, that may appear in faunistic lists, juridical texts, etc. For this

purpose, it is not appropriate to designate some taxa (“biological species”) by Latin binominals, and

others by letters or combinations of letters (such as Pocciliopsis Cx or Ambystoma LLJA) or compound

names (Such as Pocciliopsis monacha-lucida).

AS à taxonomic category, the term species may designate various kinds of units, according to the

biological properties of the organisms at stake. In order to distinguish this acceptation from the

nomenclatural one, these units may be known under the gencral term of specion (DUBOIs, 2007, 2008b),

and the different kinds of specions may be designated by terms ending in on, like taxon. The “common”

situation is that of the “biological species” or mayron (DUBots, 2007). a bisexual panmictic unit whose

gene pool is protected from those of other similar units by ecological, ethological, mechanic, biochemical,

chromosomal, genetic or other barriers. But other kinds of units can be recognized. These include taxa

that depend for their reproduction on other taxa which they so to speak “parasitize” sexually a each

gencration, cither through gynogenesis or through genuine fertilization, and for which the term klepton

was coined (Dusois & GÜNTHER, 1982), as well as unisexual female taxa that reproduce through

apomictic or automictic parthenogenesis, which can be known under the term of Ælonon (DuRoIs, 1991).

Several other subeategories can be recognized, and probably some have not yet been identified so far in

nature, The general term £yon has been proposed for all these categories of “strange species” reproducing

through clonality (Dusois, 20084, 2009).

In Europe, most authors use the category klepton (derived from the Greck term Æleptos. “thiel”, not

from the term kleptomania, as wrongly stated by Avise, p. 99) for ranid green frogs of the genus

Pelophylax, but this has not been adopted by most North American authors. The reluctance of the latter

to use special taxonomie units for these entities implies in some cases that they do not want to recognize

them as taxa. For example, FRosr & HizLis (1990) argued that these frogs with special gametogenesis

should be referred formally to the species with which they breed at cach generation, just like males are

members of the same species as the females with which they breed! This mode of reasoning by analogy is

wrong, as in bisexual species males and females are inter-dependent, which is not the case in systems like

that of European green frogs, where the klepton indeed depends from the associated mayron for its

reproduction, whercas the reverse is not true (see DuBois, 20084, 2009). Others apparently think that

these special organisms belong in distinet evolutionary units, which they call *biotypes” or “unisexuals”,

Source : MNHN, Paris

DuBois 65

but must be kept “outside taxonomy they are not “biological species”. But the à priori idea that all

organisms on earth should belong in a single taxonomic category, a “unified concept of species” (e.g., DE

QUEROZ, 1998), has no theoretical or empirical justification, and only seems to stem from a reductionist

scientific attitude. For any evolutionary biologist accustomed to the diversity and unpredictability of life,

itis no surprise to realize that different kinds of basic evolutionary units do exist in nature, that cannot be

unified except artificially. Be it as it may, it is clear that a discussion of the taxonomy of clonal, hemiclonal

or meroclonal organisms with asexual or metasexual gametogeneses is wanting in Avise’s book, as well as

à discussion of the different nomenclatural systems proposed for these taxa (see Duois & GÜNTH

1982; Dunois, 1991, 2008, 2009h). Hopefully this will appear in a subsequent edition of this exciting

book.

This book contains many other interesting discussions, some of which occupy only a few lines but

stimulate interesting thoughts. They cannot all be surveyed here, but let us just take one example, which

opens a reflection on the conflict that exists nowadays between evolutionary biology and taxonomy on

one side, as disciplines which aim at a better understanding of biodiversity on this planet, and conserva-

tion biology on the other, which sometimes acts as a break against this progress of knowledge (DuBois.

2003, 2006, 20094, c; Dusois & NEMÉS1O, 2007; NEMÉSIO, 2009): “{... ) the traditional kinds of data initially

suggestive of unisexuality (...) see to be gathered less often now because museum workers and systematists

generally tend to collect fewer vertebrate specimens. This restraint is due to ethical concerns about declining

biodiversity, as well as 10 stricter laws and protective regulations for vertebrate animals” (p. 51).

Pursing reflection on these questions leads to realize that, in order to be able to protect some of the

extraordinary organisms of multispecific origins that occur in some of these systems, like in the genus

Ambystoma (BOGART et al., 2007; Bret al., 2009), we need to recognize formally special taxa for them, and

to provide them with Latin nomina, as this is indispensable for placing them on official lists of protected

taxa (DuBois, 20064).

A last comment of general value here concerns these multihybrid organisms. Their mitochondrial

genome may in some cases originate from a mayron the nuclear genome of which is totally absent in their

genotype (BoGaRT et al., 2009), so that identifying them through “’barcode” would result in a completely

wrong taxonomic allocation. This suggests that great care should be taken in the use of barcode, as long

as so little is known about the gametogenesis and kinetogenesis of most living organisms.

Well, these “strange species” still have a lot to tell us and they no doubt reserve a lot of surprises to

biology. Rigid-minded people will perhaps be disturbed by these findings, but it is certainly more exciting

to learn from nature than only from our models and theories..

LITERATURE CITED

Bi, K. BoGarr J. P. & FU, J., 2009. - An examination of intergenomic exchanges in A. laterale-dependent

unisexual salamanders in the genus Ambystoma. Cytogeneties & Genome Research 124: 44-50.

BOGART, J. P., BARTOSZEK, J., NOBLE, D. W. A. & Bi, K.. 2009. - Sex in unisexual salamanders: disc

of à new sperm donor with ancient affinities. Heredity, in press,

BOGART, J. P,, Bt, K., FU,

isexual salamanders (genus

: 119-136.

and the proc

In: D. I. HOWARD &S.

species and speciation, New York, Oxford University Press:

De Queroz, K., 1998. - The general lineage concept of species,

speciation: a conceptual unification and terminological recommendations.

H. BERLOCHER (ed.), Endless form

57-75.

Dunois, A., 1991. Nomenclature of parthenogenetic, gynogenetic and “hybridogencti

taxons: new proposals. Alytes, 8 (3-4): 61-74.

2003. - The relationships between taxonomy and conservation biology in the century of extinctions.

Comptes rendus Biologies, 326 (suppl. 1): S9-S21.

vertebrate

Source : MNHN, Paris

66 ALYTES 27 (2)

200$. - Proposed Rules for the incorporation of nomina of higher-ranked zoological taxa in the

International Code of Zoological Nomenclature. 1. Some general questions, concepts and terms of

biological nomenclature, Zoosystema, 27 (2): 365-426.

— 20064. - New proposals for naming lower-ranked taxa within the frame of the /nternational Code of

Zoological Nomenclature. Comptes rendus Biologies, 329 (10): 823-840.

2006b. — Forum. Species introductions and reintroductions, faunistic and genetic pollution: some

provocative thoughts. A/ytes, 24 (1-4): 147-164.

2007. — Phylogeny, taxonomy and nomenclature: the problem of taxonomic categories and of

nomenclatural ranks. Zootaxa, 1519: 27-68.

2008a. - Drôles d'espèces. Hybridation, perturbations de la méiose et spéciation dans le règne

animal: quelques points délicats de terminologie, d'éidonomie et de nomenclature. /n: D. PRAT, A.

RAYNAL-ROQUES & A. ROGUENANT (ed.), Peut-on classer le vivant? Linné et la systématique

aujourd'hui, Paris, Belin: 169-202.

2008b.— Phylogenetic hypotheses, taxa and nomina in zoology. /n: A. MineLut, L. BONATO & G.

FUsCo (ed.), Updating the Linnaean heritage: names as tools for thinking about animals and plants,

Zootaxa, 1950: 51-86.

20094. — La notion de pollution biotique: pollutions faunistique, floristique, génétique et culturelle.

Bulletin de la Société zoologique de France, 133 (4): 357-382.

2009b. — Qu'est-ce qu'une espèce animale? /n: Aller à l'espèce: illusion ou néces

Société entomologique de France, 8: 9-48.

2009. - Endangered species and endangered knowledge. Zooraxa, 2201: 26-29.

Dunois, À. & GüNruER, R, 1982. Klepton and synklepton: two new evolutionary systematics

categories in zoology. Zool. Jb. Syst., 109: 290-305.

Dugois, A. & NEMÉsIO, A., 2007. — Does nomenclatural availability of nomina of new species or

subspecies require the deposition of vouchers in collections? Zootaxa, 1409: 1-22.

Frosr, D. R. & Hizis, D. M., 1990, - Species in concept and practice: herpetological applications.

Herpetologica, 46: 87-104.

May, E., 1978. [Book review]. Les problèmes de l'espèce dans le règne animal. Systematic Zoology, 21

(( 50-2:

May, E. & AsuLock, P. D.. 1991. — Principles of systematic zoology. Second edition. New York,

McGraw-Hill: i-xx + 1-475.

>, À. 2009. - Nomenclatural availability of nomina of new species should always require the

deposition of preserved specimens in collections: a rebuttal to Donegan (2008). Zootaxa, 2045:

1-14.

OWEN, T., 1849. - On parthenogenesis, or the successive production of procreating individuals from a single

ovum, London, John van Voorst: 1-76, pl. 1.

RosTAND, J., 1966. - Hommes d'autrefois et d'aujourd'hui. Paris, Gallimard: 1-235.

ScHuLrz R., 1969. Hybridization, unisexuality, and polyploidy in the teleost Pocciliopsis (Pocciliidae)

and other vertebrates. American Naturalist, 108: 605-619.

ité, Mémoires de la

NEMI

Corresponding editor: Annemarie OHLER.

CA 2009

Source : MNHN, Paris

Alytes, 2009, 27 (2): 67-68. 67

Premiers Tétrapodes

Alain DuBois

Reptiles et Amphibiens, UMR 7205 OSEB, Département de Systématique & Evolution.

Muséum national d'Histoire naturelle, CP 30, 25 rue Cuvier, 75005 Paris, France

<adubois@mnhn.fr>

Sébastien STEYER, 2009. — La terre avant les Dinosaures. Hlustré par Alain BÉN

ISBN 978-2-7011-4206-7. 25 €.

ÉTEAU. Paris, Belin: 1-205.

Voici un livre fort sympathique. Il se détache par son originalité au milieu de la profusion de livres sur

les fossiles célèbres ou les animaux spectaculaires, premiers humains ou Dinosaures, baleines, requins et

tigres

Le titre du livre est un peu trompeur, puisqu'il peut laisser penser qu'il traite de tous les animaux qui

vivaient sur les continents avant l’apparition des Dinosaures. En fait, il s’agit du premier livre en français

consacré aux premiers Tétrapodes, les premiers Amphibiens et les premiers Reptiles. Le livre frappe

d'abord par sa riche iconographie. Il comporte de nombreuses photos de fossiles, des schémas explicatifs

quelques photos de sites fossilifères et de fouilles, mais surtout de nombreuses reconstitutions en couleurs

de ces animaux dans leur milieu et “saisis” dans une de leurs activités, Ces “scènes” sont pour la plupart

d’une saisissante beauté. Les Amphibiens et les Reptiles sont des animaux difficiles à dessiner de telle

manière qu'ils paraissent vivants, et depuis les ouvrages magnifiquement illustrés par Z. Burian dans les

années 1960 je n'avais pas vu de reconstitutions aussi réuss

Une autre particularité de ce livre est sa démarche pédagogique appuyée, pour ne pas dire militante,

pour présenter aux lecteurs une interprétation darwinienne de l'évolution, débarrassée de toute idéologie

téléologique. L'évolution n'a obéi à aucun plan, aucun dessein préétabli, elle ne se dirigeait pas vers un

but, les Vertébrés homéothermes et l'homme ne constituent pas son but ultime et sa réussite absolue.

Chaque organisme qui a vécu sur cette planète a été, à un moment de l'histoire de cette dernière, une

réussite à sa manière, et aucun organisme n'est “supérieur” aux autres. Ces idées sont bien illustrées tout

le long de cet ouvrage, notamment à travers la critique qui y est présentée de deux formules célèbres,

connues de tous, mais fausses, celle de “sortie des eaux” et celle de “fossile vivant”, qui toutes deux

renvoient à une notion de “sens de l'évolution”.

Ce livre échappe à une tendance forte actuelle de beaucoup d'ouvrages contemporains, celle d’une

présentation “consensuelle” d’une seule théorie là où plusieurs théories sont actuellement en compétition

au sein de la communauté scientifique. Ce phénomène de désaccord entre spécialistes est très fréquent en

science, bien plus que ne l'imagine souvent le “grand public” à qui souvent l'on cache ces débats. À toute:

les étapes de l’histoire de la science, et dans tous les domaines de celle-ci, des théories se sont affrontées,

et ceci parfois pendant des décennies ou des s

même fortement, à une époque donnée, n'est en rien une garantie de sa *

est jalonnée de “révolutions conceptuelles”, à l'occasion desquelles telle conception hier majoritaire a pu

devenir minoritaire, ou même complètement et définitivement abandonnée, en un laps de temps parfois

très court, en raison de nouvelles découvertes, de nouveaux concepts ou de nouvelles synthèses. En

science, seul le long terme permet souvent de trancher définitivement entre deux théories contradictoires

contemporaines. Que l'on pense à cet égard quelques grandes “erreurs historiques” de la communauté

scientifique dans le passé, dont rien ne permet d'affirmer que la science est aujourd'hui prémunie (DUBOIS,

2009).

cles, Le fait qu'une théorie donnée soit majoritaire, parfois

justes l'histoire des sciences

Source : MNHN, Paris

68 ALYTES 27 (2)

Quelques petites erreurs de terminologie, parfois dues à une influence de la littérature anglo-saxonne,

devraient être corrigées dans une réédition de l' ouvrage. Par exemple, si en anglais il n'existe qu’un seul

terme (dentition) pour les deux concepts, en français, le terme de dentition désigne le pro:

croissance et mise en place des dents, tandis que le terme de denture doit être employé pour di

nombre et les types de dents et leur disposition dans la bouche. L'emploi du terme Li

désigner tous les Amphibiens actuels n'est pas non plus justifié (DUBOIs, 2004), puisque ce terme à

créé par HaëckEL (1866) pour un taxon comportant les seuls Anoures et Urodèles, mais excluant les

Gymnophiones, constituant donc un strict synonyme du terme Batraciens de BRONGNIART (1800): le

terme correct pour désigner les trois ordres d'Amphibiens actuels est Néobatraciens de SARASIN &

SARASIN (1890).

LITERATURE CITED

BRONGNIART, A., 1800. - Essai d’une classification naturelle des reptiles. I partie. Établissement des

ordres. Bulletin des Sciences, par la Société philomatique, 2 (33): 81-82.

Dunois, A., 2004, - The higher nomenclature of recent amphibians, Alyvres, 22 (1-2): 1-14.

2009. Un pionnier méconnu du darwinisme en France. A/yres, 27 (2): 69-71.

Haëckëz, E., 1866. — Gencrelle Morphologie der Organismen. Zweïter Band. Allgemeine Entwicke-

lunggsgeschichte der Organismen. Berlin, Georg Kramer: i-clx + 1-462, pl. 1-8.

SarasiN, P. & SarasiN, F. 1890. — Zur Entwicklungsgeschichte und Anatomie der ceylonesischen

Blindwühle Zchthyophis glutinosus, L. Vierter Theil. “gebnisse naturwissenschaflicher Fors-

chungen auf Ceylon, Zwveiter Band, Wiesbaden, Kreïdel: 151-263, pl. 15-24.

Corresponding editor: Annemarie OHLER.

Source : MNHN, Paris

Alytes, 2009, 27 (2): 69-71. 69

Un pionnier méconnu du darwinisme

en France

Alain DuBois

Reptiles et Amphibiens, UMR 7205 OSEB, Département de Systématique & Evolution,

Muséum national d'Histoire naturelle, CP 30, 25 rue Cuvier, 75005 Paris, France

<adubois@mnhn.fr>

Yves CARTON, 2008. — Henry de Varigny, darwinien convaincu, médecin, chercheur et journaliste (1855-

1934). Paris, Hermann: i-vii + 1-116, pl. 1-7. ISBN 978-2-7056-6822-8. 21,50 €.

Contrairement à une idée souvent répandue, la science avance rarement d’un pas régulier et

tranquille, dans un consensus parfait, les nouvelles idées, théories et découvertes étant acceptées par tous

et dans le monde entier dès lors que les données et les arguments ont été publiés. Ce n’est qu'à longue,

parfois très longue, échéance que les théories considérées “iconoclastes” ou “’hérétiques” lors de leur

publication peuvent devenir consensuelles — souvent avant d'être à leur tour remplacées ultérieurement

par d’autres. Certaines “erreurs historiques” de la communauté scientifique dans le passé font

aujourd'hui réfléchir et parfois frémir, Ce fut le cas, par exemple, en France, du rejet quasiment unanime

par la communauté universitaire de la théorie chromosomique de l'hérédité, alors même que les preuves

de cette théorie avaient été publiées de manière irréfutable aux Etats-Unis: pour briser ce tabou, il fallut

attendre la publication du livre Les chromosomes (ROSTAND, 1928) par un “amateur” ne faisant pas partie

de l‘*establishment scientifique”.

Ilen va de même du rejet tout aussi vif dans notre pays, pendant longtemps et encore aujourd'hui par

certains, de la théorie darwinienne de la sélection naturelle, une histoire bien retracée dans le petit livre

d'Yves Carton consacré à la vie et l'œuvre de Henry de Varigny. Celui-ci fut le premier véritable

“darwinien militant” français. Dès sa découverte de L'origine des espèces, ce médecin de formation,

anglophone, docteur ès sciences, ayant travaillé au Muséum national d'Histoire naturelle, se consacra à la

diffusion des idées de Darwin, aussi bien vis-à-vis de la communauté scientifique que du grand public. Il

publia plusieurs ouvrages sur Darwin et le darwinisme, traduisit en français les lettres de Darwin et

d'autres ouvrages sur le darwinisme. Préfigurant ceux de Jean Rostand quelques années plus tard, il

écrivit de nombreux articles sur ces questions pour des quotidiens à grand tirage, à une époque où la

“vulgarisation scientifique” était rare. Sa démarche est d'autant plus remarquable que la communauté

scientifique française se montrait très réticente vis-à-vis de la théorie de la sélection naturelle, dont on peut

dire sans exagération que la plupart des “grands savants” de l’époque ne la comprirent tout simplement

pas. Il n'est pas à l'honneur de la France que l'Académie des Sciences ait diseuté pendant huit ans (près

de 3000 jours) de l'élection de Darwin comme correspondant étranger, et encore dans sa section de

botanique! Les discussions qui précédèrent ce vote furent édifiantes

“perles” ressuscitées dans l'ouvrage de Yves Carton, comme celle-ci: Sc

de pigeons (...) prouveraient qu'il manque de véritable esprit scientifique

comme le montrent certaines

es longues recherches sur les races

(p.42).

Un tel manque de discernement de la part des “leaders” de la science est-il envisageable aujourd'hui?

Rien ne permet d'affirmer le contraire. Ce n'est pas ce qu'on entend actuellement sur la science et

son “contrôle” par la société qui peut nous rassurer à cet égard... Des termes jusque-là absents du

discours sur la recherche, comme “excellence” et “évaluation” y sont désormais d'emploi courant

L'‘évaluationnite” actuelle a de quoi inquiéter à plusieurs titres (MILLER & Mi. NER, 2004: LAWRENCE,

Source : MNHN, Paris

70 ALYTES 27 (2)

2007; MANIGLIER, 2007). Bien qu'il fût sensible à la contribution particulière de certains “hommes de

vérité” au progrès scientifique, mon maître Jean Rostand considérait la science comme une entreprise

collective, où chacun apporte sa “petite pierre” à un édifice que n'auraient pu construire seuls quelques

“génies”, Aujourd’hui, il semble parfois qu'il ne s'agisse plus de savoir si les chercheurs contribuent

efficacement à cette entreprise collective, mais de les “classer”. Les multiples commissions et instances

d’‘évaluation” et de classement de dossiers et de candidats auxquelles les chercheurs eux-mêmes sont

tous amenés, de gré ou de force, à participer, ressemblent à certains égards à des jurys de jeux télévisés, et

leurs classements à des palmarès sportifs, des hits parades, des prix littéraires ou des pages du Guinness

Book of Records. Les curricula vitae, rapports et dossiers de candidature sont de plus en plus truffés de

superlatifs. Sous peine de déchoir, un chercheur digne de ce nom, de nos jours, est tenu d'étudier ce qui

dans son domaine est “le plus gros”, “le plus ancien”, “le plus rare”, “le plus menacé”, ou pourquoi pa

“le plus jaune”: il est très instructif à cet égard d'être attentif dans ces dossiers à de telles affirmations

selon lesquelles un chercheur ou une équipe est “le premier” ou “la première”, “le seul” ou “la seule” à

avoir étudié, trouvé, résolu un problème, une question. Celui qui oserait écrire qu'il a simplement

contribué modestement à faire avancer la connaissance dans son domaine de recherche signerait son arrêt

de mort institutionnel. L'autre face de la médaille de l'évaluation à tout crin est la forte pression en faveur

du conformisme. Rien n'est plus risqué dans ce contexte pour un individu que de ne pas ressembler à

l'image du chercheur formaté dans ses choix de sujets de recherche, ses idées dominantes, sa manière

d'écrire les articles: les rédacteurs, “lecteurs”, “referees” et “reviewers” sont là pour veiller à ce que pas

une tête ne dépasse et que tous les membres de la grande famille des chercheurs partagent les mêmes

opinions, pratiques, conclusions...

Classer c'est hiérarchiser, humilier et exclure. La culture du classement est une culture du secret et de

l'exclusion, qui s'oppose à la culture de communication et de collaboration qui devrait prévaloir au sein

de la communauté scientifique. Il n'est pas très difficile de voir ce qui se joue derrière les formules

ampoulées sur l“excellence”: ce sont les réductions de postes, de crédits et de locaux, les économies

budgétaires et la précarisation des métiers de chercheur et d'enseignant-chercheur. La crise économique

et sociale de notre société mondialisée s'accroît d'année en année, de jour en jour. Dans toutes les

s s d'“évaluation” de la recherche qui se sont multipliées, il ne s agit plus seulement, comme dans

les décennies qui ont précédé, d'associer les chercheurs et les enseignants à la “gestion de la pénurie”, il

faut les associer à la destruction progressive de leur propre communauté professionnelle, pour en faire de

plus en plus, comme dans d'autres domaines de notre société, de dociles employés précaires et jetables

comme des kleenex. Ces objectifs sont ceux annoncés clairement par la Communauté Européenne dans

sa “Déclaration de Bologne” (ScHuLruEïS et al., 2008). Quant à la pertinence des “choix stratégiques” de

la recherche actuelle, elle est également douteuse, quand on constate que ceux-ci aboutissent à privilégier

la recherche de la vie dans d'autres planètes ou le séquençage du mammouth à l'inventaire et l'étude des

espèces en train de s'éteindre sous nos yeux sur toute la planète (DUBOIS, 2008a-b, 2009a-b). Non, il ne

semble pas que la communauté scientifique soit devenue plus sage, prévoyante et compétente dans ses

choix aujourd’hui qu'elle ne l'était il y a un siècle et demi

LITERATURE CITED

Dunois, A., 2008a. - Handicap taxinomique et crise de la biodiversité: un nouveau paradigme pour la

biologie au xxI° siècle. Zn: D. PRAT, A. RAYNAL-ROQUES & A. ROGUENANT (ed.), Peut-on classer le

vivant? Linné et la systématique aujourd'hui, Paris, Belin: 141-160.

2008b. - Un nouveau paradigme pour la biologie au xxr° siècle. /n: M. VEUILLE, J.-M. DROUIN, R.

DELEPORTE & J.-F. SILVAIN (ed.), Linnaeus - Systématique et biodiversité, Biosystema, 25: 127-142.

20094. - La notion de pollution biotique: pollutions faunistique, floristique, génétique et culturelle.

Bulletin de la Société zoologique de France, 133 (4): 357-382.

2009b. - Endangered species and endangered knowledge. Zooraxa, 2201: 26-29.

LAWRENCE, P. A., 2007. - The mismeasurement of science, Current Biology, 17: R5S83-R585.

MANIGLIER, P., 2007. - Vous avez dit ‘misère de la philosophie"? Le Monde des Livres, supplément au

journal Le Monde, 29 juin 2007, 63 (19417):

Source : MNHN, Paris

Dugois 71

Muzzer, J.-A. & MILNER, J.-C., 2004. — Voulez-vous être évalué? Entretiens sur une machine d'imposture.

Paris, Grasset: 1-81

RosTAND, J., 1928. — Les chromosomes, artisans de l'hérédité et du sexe. Paris, Hachett

ScHuLrHers, F., RoCA 1 EscopA, M. & Cousin, PF, 2008. - Le cauchemar de Humboldt. Les réformes de

l'enseignement supérieur européen. Paris, Raisons d'Agir: 1-234.

Corresponding editor: Annemarie OHLER.

Source : MNHN, Paris

‘4 DEC. 2008

Alytes, 2009, 27 (2): 72.

Erratum

In pages 44 and 59 of the article quoted below, an unfortunate mistake has resulted in an

inversion between two paragraphs giving the entexognoses of two tribes of the family

PLEURODELINAE. The authors are grateful to Jean-Michel Collet for pointing out this error. The

correct texts are given below.

Page 44:

Tribus Mozcivi Gray, 1950

Nucleogenus. - Molge Merrem, 1820: 166, by original specific monophory.

Entexognosis. — The most inclusive holophyletic taxon including the species Triturus cristatus

(Laurenti, 1768) and excluding the species Pleurodeles walt! (Michahelles, 1830).

Page 59:

Tribus PLrvropErINI Tschudi, 1838

Nucleogenus. - Pleurodeles Michahelles, 1830: 195, by implicit etymological designation.

Entexognosis

(Michahell

The most inclusive holophyletic taxon including the species Pleurodeles waltl

1830) and excluding the species Triturus cristatus (Laurenti, 1768).

LITERATURE CITED

Dunois, A. & RAFFAËLLI, JL, 2009. - À new ergotaxonomy of the family Salamandridae Goldfuss, 1820

(Amphibia, Urodela). Alrtes, 26 (1-4): 1-85.

O ISSCA 2009

Source : MNHN, Paris

AIVTES

International Journal of Batrachology

published by ISSCA.

EDITORIAL BOARD

Chief Editor: Stephane GrossraN (Reptiles et Amphibiens, UMR 7205 OSEB, Département de Systématique &

Evolution, Muséum national d'Histoire naturelle, CP 30, 25 rue Cuvier 75005 Paris, France;

<sgrosja@mnhn.fr>).

Deputy Editor: Franco ANDREONE (Museo Regionale di Scienze Naturali, Via G. Giolitti 36, 10123 Torino, ltaly:

<fandreone@libero.it>)

Alytes Editorial Board: Ariadne ANGULO (Toronto, Canada); David C. BLACKBURN (Kansas, USA): Lauren E.

Brown (Normal, USA); Angus I. CaRPeNTIER (Norwich, UK); Ignacio DE LA Riva (Madrid, Spain}:

Rafael O, be Sà (Richmond, USA); Alain Dunors (Paris, France): W. Ronald Heyex (Washington, USA):

(Madrid, Spain); Masafumi MaTsut (Kyoto, Japan): Annemarie OHLER (Paris, France):

EL (Berlin, Germany); Miguel VENCES (Braunschweig, Germany).

hibia Mundi Edigril Board: Alain Dunois, Chief Editor (Paris. France): Ronald 1. Cote (San

ancisco, USA): Stéphane GROSIEAN (Paris, France): W. Ronald Hrver (Washington, USA): JIANG

Jaune (Chengdu, China): Esteban O. LAVILLA (Tucumän, Argentina): Jean-Claude RAGE (Paris,

France); David B. Wake (Berkeley, USA)

Technical Edirorial Team (Paris, France): Alain Dusois (texts): Roger BoUR (tables): Annemarie Ouen (figures).

Book Review Editor: Annemarie OuEr (Paris, France)

SHORT GUIDE FOR AUTHORS

(for more detailed /nstructions to Authors, see Alytes, 1997, 14: 175-200)

Iytes publishes original papers in English, French i

r Spanish, in any discipline dealing with amphibians.

le articles and notes reporting results of original research, consideration is given for publication to synthetic

review articles, book reviews, comments and replies, and 10 pap: sed 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 addresses) 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 cm. The size of the lettering should ensure its legibility after reduction. The legends of figures and tables

should be assembled on à 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 follor

BOURRET, R., 1942. — Les batraciens de l'Indochine. Hanoï, Institut Océanographique de l'Indochine: i-x + 1-547,

1. 1

Graf. J.-D. & PoLLs PELAZ, M. 1989. - Evolutionary genetics of the Rand eseulenta complex. Ir: R. M. DAWLEY

& 1. P. BOGART (ed.), Evolution and ecology of unisexual vertebrates, Albany, The New York State Museum:

280-302

INGER, R. EF. 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.

Manuscrits should be submitted either as attached document by e-mail, or in paper form by mail but tien

in triplicate, either to Alain DUBoIs (address above) if dealing with amphibian morphology. anatomy, syst: na-

tics, biogeography, evolution, genetics, genetics, anomalies or developmental biology, or to Franco AND BONE

(address above) if dealing with amphibian population genetics, ecology, ethology, life history or conser_ ation

biology, including declining amphibian populations or pathology. Acceptance for publication will be decided by

the editors following review by at least two refe

After acceptance, a copy of the final manuscript should be sent to the Chief Editor, either as attachment by

e-mail, or by mail on a floppy disk (3 4 or 5 %). We welcome the following formats of text processing: (I)

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 2 high

density 1.44 Mo floppy disk only).

Page charges are requested only from authors having institutional support for this purpose. The publication

of colour photographs is charged. For each published paper, a free pdf or 25 free reprints are offered by ISSCA

to the author(s). Additional reprints may be purchased.

Published with the s

{Association des Amis du Laboratoire des Reptiles et Amphibiens

du Muséum National d'Histoire Naturelle, Paris, France).

Directeur de la Publication: Alain Durois

Numéro de Commission Paritaire: 64851.