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46

Reproductive behaviour of spadefoot toads

(Pelobates fuscus): daily sex ratios and males’
tactics, ages, and physical condition
Christophe Eggert and Robert Guyétant

Abstract: In anuran competition over mates, disadvantaged (i.e., less competitive) males are generally known to be the
smallest ones, but ages of those males have rarely been documented. In the context of a high level of male competition
for mates, disadvantaged males were expected to use alternative mating tactics. To test for alternative tactics in a terri-
torial toad (the spadefoot toad, Pelobates fuscus, Pelobatidae), daily breeding migration patterns were observed during
3 consecutive years. Relationships between migration pattern, operational sex ratio (OSR), and male’s age (inferred
from skeletochronological analysis), size, and mass were analysed. During 2 of the study years, OSRs were highly
male-biased at the beginning of the breeding season and then gradually decreased when male numbers increased. Males
with a low body condition index (CI) tend to arrive later and to lose relatively more mass than males with a higher CI.
There was a negative relationship between percent mass loss per day and CI as well as length of stay in the breeding
area, which suggests that a high energetic cost tactic was adopted by males with a higher CI. A negative relationship
between length of stay and age was also observed. We conclude that based on competition for mates, male P. fuscus
seem to adopt reproductive behaviour that differs according to body condition and age.
Résumé : Chez les anoures, dans la compétition qui oppose les mâles les uns aux autres pour des partenaires, il est
bien connu que les mâles les plus petits sont désavantagés (i.e., ils sont des compétiteurs moins efficaces), mais l’âge
de ces mâles a rarement été signalé. Au cours d’une compétition intense entre des mâles, on s’attendrait à ce que les
mâles désavantagés utilisent des stratégies d’accouplement différentes. Pour vérifier cette hypothèse, nous avons ob-
servé les patterns quotidiens de migration de reproduction chez un crapaud territorial, Pelobates fuscus (Pelobatidae),
durant 3 années consécutives. Nous avons analysé les relations entre ces patterns, le rapport des sexes opérationnel
(OSR), l’âge des mâles (déterminé par analyse squeletto-chronologique), leur taille et leur masse. Au cours de 2 des
années de l’étude, le rapport des sexes opérationnel avantageait fortement les mâles au début de la saison de la repro-
duction, mais diminuait graduellement par la suite à mesure que le nombre de mâles augmentait. Les mâles dont le
coefficient d’embonpoint (CI) est faible ont tendance à arriver plus tard et à perdre une plus grande partie de leur
masse que les mâles à coefficient d’embonpoint plus élevé. Il y a une relation négative entre, d’une part, le pourcen-
tage de masse perdu chaque jour et, d’autre part, le coefficient CI ainsi que la durée du séjour dans la région de la re-
production, ce qui reflète probablement l’utilisation de tactiques de coût énergétique élevé chez les mâles à coefficient
CI plus élevé. Nous avons également trouvé une relation négative entre la durée de séjour des mâles en territoire de re-
production et leur âge. Nous concluons que, selon l’intensité de la compétition pour des partenaires, les crapauds mâles
de cette espèce semblent adopter des comportements reproductifs distincts en fonction de leur âge et de leur coefficient
d’embonpoint.
[Traduit par la Rédaction] 51
Introduction ble competition occurs, and male mating success depends
Eggert and Guyétant
greatly on the ability to locate females and to stay paired
Anuran reproduction patterns range from explosive (short- with them until the eggs are laid (e.g., Davies and Halliday
duration) to prolonged breeding (Wells 1977a). We assume 1979). In prolonged breeders, males attract females with ad-
that in a particular species, the type of male–male competition vertisement calls (see Gerhardt 1994) and (or) may defend
for mates and females’ mating preferences depend greatly on oviposition sites (Wells 1977b; Howard 1978), therefore fe-
the temporal and spatial pattern of reproduction. Hence, in male choice (and males’ ability to attract females) is a deter-
explosive breeders, when male density is high, intense scram- minant of male mating success (Ryan 1980, 1983; Arak
1983a; Sullivan 1985; Roberston 1986; Marquez and Tejedo-
Received 30 April 2002. Accepted 19 November 2002. Madueno 1990). This leads to vocal competition or the de-
Published on the NRC Research Press Web site at fence of individual territories. Thus, for a given male, the
http://cjz.nrc.ca on 5 February 2003.
probability of obtaining a mate could depend on such factors as
C. Eggert1 and R. Guyétant. Laboratoire de Biologie des the patterns of arrival of other males and females in breed-
Populations d’Altitude, Unité Mixte de Recherche 5553, ing ponds, other males’ age, size, or density, the operational
Centre National de la Recherche Scientifique, Centre sex ratio (OSR, the ratio of potentially receptive females to
Interdisciplinaire Scientifique de la Montagne, Université de males) and also the time spent at the breeding site (reviewed
Savoie, F 73376 Le Bourget du Lac, France. in Halliday and Tejedo 1995; Sullivan et al. 1995).
1
Corresponding author (e-mail: eggert@univ-savoie.fr). It is expected that when mating competition is severe, dis-
Can. J. Zool. 81: 46–51 (2003) doi: 10.1139/Z02-224 © 2003 NRC Canada

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Eggert and Guyétant
advantaged males will use alternative mating tactics to en-
hance their mating probabilities (Perrill 1984; Andersson
1994; Lucas and Howard 1995). For example, one of the
best known alternative behaviours of chorusing anurans is
the “satellite tactic” (silent males surround callers), which
has been modelled as a dynamic game (Waltz 1982; Lucas
et al. 1996). Low energetic cost tactics are expected to be
adopted by disadvantaged, i.e., youngest or smallest, males
(Waltz 1982; Krupa 1989; Lucas and Howard 1995).
Skeletochronological techniques allow reliable individual
age estimation in amphibians (see Castanet and Smirina 1990),
but only a few studies of amphibians have dealt with mating
success in relation to age (e.g., Höglund and Säterberg 1989;
Cherry and Francillon-Vieillot 1992; Howard and Young 1998).
In many other amphibian studies, the extent to which the ob-
served competitive or mating advantages enjoyed by larger
males depended on size (or mass) or age is not known.
The spadefoot toad, Pelobates fuscus, is a nocturnal fossorial
species that lives in sandy ground during the daytime, and
reproduces in quite large ponds (up to 80 m2) (Eibl-Eibesfeldt
1956; Nöllert 1990). In most cases males were just deep
enough in the water to be not visible from the bank. Their
secretive breeding activity occurs from late March to late
May (Nöllert 1990). During this prolonged breeding period,
males defend territories and exhibit site attachment and in-
tolerance of intruders (Eibl-Eibesfeldt 1956; Müller 1984).
An average of 80-cm spacing is maintained between two males
using two types of territorial calls (Müller 1984). Moreover,
males emit an underwater mating call (or courtship call)
whose dominant frequency is inversely related to male body
size, providing the opportunity for female choice based on
body size (Müller 1984).
Because severe mating competition was observed in this
species (based on territoriality, courtship call, and male-biased
OSR), we tested for age-, size-, or mass-based differential
reproductive tactics by observing breeding migration pat-
terns in a wild population for 3 years. We predicted that
small and (or) young males would optimize their probability
of mating by adjusting their breeding phenology so as to
avoid strong competitors.
Material and methods
The study area was located in northeast France (described
in Eggert and Guyétant 1999, 2002; Eggert 2002). Four tem-
porary ponds situated close together were surrounded with
drift fences, with pitfall traps on both sides of each fence
(see Gibbons and Semlitsch 1982). The drift fences were
45–50 cm high and buried 10–15 cm in the ground. De-
pending on the water level, the fences were situated between
0 and 20 m from the water. Hence, an nonflooded area was
always present inside the enclosed area. Pelobates fuscus
were caught in traps during nocturnal breeding migrations
on 94 consecutive days in 1996, 67 in 1997, and 65 in 1998.
Passive integrated transponders were slipped under the
skin to allow identification of individuals. Snout–vent length
was measured with a caliper to the nearest 0.1 mm (with an
accuracy of ±5% between two successive measures) and mass
(empty bladder) with an electronic balance (accuracy 0.1 g).
After monitoring, animals were immediately released on the
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47
side of the fence opposite to that on which they were caught,
where they could bury themselves in the ground.
Skeletochronological analysis was conducted on the sec-
ond phalanx of the third toe on the right forelimb using the
methods described in Eggert and Guyétant (1999). Age esti-
mation was based on counting rest lines, or lines of arrested
growth (LAG), which correspond to hibernation periods (see
Castanet and Smirina 1990; Miaud et al. 1993). Age was es-
timated with a maximum of 1 LAG error, mainly because
the spacing between the outermost LAGs in the oldest indi-
viduals was small.
To analyse phenological patterns, we considered the first
recorded entry into the fenced area and the last recorded de-
parture for each individual. We do not consider that the only
male which stayed less than 2 nights inside the encircled
area was taking part in the reproductive process; it was evi-
dent that he fell into the closest trap after being released, and
did not reach the water. Since all captured toads entering or
leaving the ponds were measured and marked, we could de-
termine the number of individuals in the breeding area on a
given date. Some individuals were only caught leaving and
were presumed to have been inside the encircled area before
the fences were installed. Others were only caught entering
and were presumed to be still inside after the study had
ended.
As already observed in P. fuscus (Jehle and Hödl 1998)
and Scaphiopus holbrooki (Dodd 1991), we assumed that
some individuals may have dug under the fence at the end of
their nocturnal activity and come out at the other side of the
fence the following night. As the bottom of each fence was
buried in the ground and particular care was taken to avoid
rodent tunnels or cavities under or against it, we presumed
that the level of trespassing had been low and did not signifi-
cantly influence our results. However, an unknown portion
of the individuals that were assumed (by analysing individ-
ual captures) to have been inside the enclosed area before
the fences were installed simply entered by trespassing across
the fences. Nonetheless, because there is no reason to as-
sume that males trespassed across the fences at a higher rate
than females, the observed breeding sex ratio was probably
correct.
Length of stay and percent mass loss were log-transformed
to avoid violation of the assumption of normality. To analyse
relationships between individuals’ traits and migration pat-
terns, we transformed arrival and departure dates by sub-
tracting each from its respective annual median. To avoid
autocorrelations we eliminated data from individuals that
were observed for several years, and for these we kept only
the year having the most complete dataset. Following Jehle
and Hödl (1998), CI was calculated as (mass (g)/size3 (cm)) ×
100. In our analysis we did not consider males who gained
mass during the breeding period, as we cannot assume that
they participated in breeding activities.
Results
During the three seasons, 261 males were caught; we esti-
mated the year of birth of 211 of them. Because of recap-
tures between years, our samples represented 176 estimates
from 227 individuals. The total breeding sex ratio was
significantly male-biased in all 3 years (Table 1). The daily
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48
Fig. 1. Daily sex ratios (males/females) and numbers of male spadefoot toads (Pelobates fuscus) in the breeding area in 1996 (dotted
line), 1997 (thin solid line), and 1998 (thick solid line). Day zero is the annual median day of arrival.
Table 1. Breeding sex ratios in the population of
spadefoot toads (Pelobates fuscus) studied.
Year Sex ratio χ2 P Year
1996 3:1 29 <0.0001
1997 1.66:1 10.37 <0.002
1998 1.62:1 6.14 <0.02
sex ratio in the ponds varied greatly during the breeding peri-
ods (Fig. 1) and was always male-biased. In 2 (1996, 1998)
of the 3 years, the sex ratio in the breeding area was strongly
male-biased during the first weeks of observation and the
bias declined as the season progressed.
Toads whose dates of both first immigration and last emigra-
tion were known were used to compare interannual lengths
of stay (Table 2). There were no significant differences be-
tween the 3 years for length of stay (ANOVA, F[2,55] = 0.87,
P = 0.42), relative day of entering the ponds (F[2,55] = 0.39,
P = 0.68), or relative day of leaving the ponds (F[2,55] = 0.47,
P = 0.63). Therefore, we combined the 3 years for further
analysis.
Multiple regression analysis of the effects of age and CI
on migration pattern revealed that CI had a significant nega-
tive effect on mean day of arrival, relative mass loss, and
daily rate of mass loss over the season and a significant pos-
itive effect on absolute mass loss (Table 3). That is, for any
given age, males with a high CI tend to arrive earlier and to
lose a larger amount of energy at a slower rate than other
males. Nevertheless, they leave the ponds having lost less
mass relative to their mass at arrival than males with a low
CI do. Total mass loss was not related to length of stay or to
day of arrival or departure (all P > 0.1), but a significant
negative effect of length of stay on relative rate of daily
body mass loss (percent mass loss per day) was observed
(Fig. 2). Mass loss was also related to mass at arrival (R =
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Can. J. Zool. Vol. 81, 2003
Table 2. Lengths of stay in the breeding area by
male P. fuscus.
Mean SD Range
1996 18.1 (n = 21) 17.1 2–68
1997 18.7 (n = 23) 13.4 4–48
1998 17.3 (n = 14) 6.7 8–30
0.48, P < 0.0002). Length of stay was also correlated with
date of arrival (R = –0.45, P < 0.001) and date of departure
(R = 0.60, P < 0.001). That is, “short breeders” arrived later,
left earlier, and lost mass at a faster rate than “long breed-
ers”. Moreover, younger males tended to stay longer at the
breeding location (Table 3). No significant relationship was
found between age and CI (P = 0.67).
Discussion
Unlike American Pelobatidae, whose reproduction lasts a
few days (see Wells 1977a; Woodward 1982), P. fuscus is
not a typical explosive breeder, and because breeding activ-
ity could last more than a month, we categorized this species
as a prolonged breeder. We observe that, in at least 2 of the
3 study years, competition for mates due to a biased sex ra-
tio gradually decreased during the course of the breeding
season in P. fuscus, when numbers of males in the ponds in-
crease. Males with the lowest CI were observed to arrive
later. These males may optimize their breeding migration
phenologically in order to reduce intrasexual competition ac-
cording to the sex ratio. Nevertheless, the number of males
was higher at this period and territories may have been more
difficult to find. Whatever their CI, males that arrived during
this period spent less time but engaged in more vigorous tac-
tics, based on relative daily mass loss. By arriving earlier,
males with a higher CI encounter a more biased sex ratio
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Eggert and Guyétant 49

Table 3. Multiple regression summary of the effects of age, body-condition index (CI) on
the day of arrival, day of departure, length of stay in the breeding area, and mass loss in
P. fuscus.
Variable Effect R t P
Day of arrival (n = 98) Age 0.14 1.50 0.14
CI –0.30 –3.04 0.003
Day of departure (n = 47) Age –0.15 –1.02 0.31
CI –0.11 –0.73 0.47
Length of stay (n = 47) Age –0.33 –2.32 0.03
CI –0.16 –1.11 0.27
Mass loss (n = 47) Age 0.07 0.53 0.59
CI 0.35 2.53 0.02
Percent mass loss (n = 47) Age –0.19 –1.30 0.20
CI –0.34 –2.34 0.02
Percent mass loss per day (n = 47) Length of stay –0.65 –5.05 <0.001
Day of arrival 0.13 1.01 0.32
Age –0.14 –1.10 0.28
CI –0.26 –2.27 0.03
Note: Significant P values are in boldface type.

Fig. 2. Relationship between relative daily mass loss (RDML;
mass loss per day relative to initial mass) and breeding-site
attendance for male P. fuscus. RDML = 0.0353 – 0.009935
log(day of entry into pond); R = 0.731.
and expend more energy during the breeding period, but the
cost seems to be lower, based on relative mass loss. Also,
in some Bufonidae, larger males arrive at the pond earlier
(Gatz 1981; Loman and Madsen 1986), and this has even
been observed in P. fuscus (Hildenhagen 1986) and Pelobates
cultripes (Lizana et al. 1994). However, the fact that earlier
arrival of smaller males was also observed in Bufo bufo em-
phasizes the flexibility of mating systems (Gittins et al. 1980).
In theoretical studies (Lucas and Howard 1995; Lucas et
al. 1996), important predictions dealing with male age, en-
ergy stores, and mating tactics have been made. High ener-
getic cost mating tactics are expected to be used more often
by males with large energy stores. Males with small energy
stores will only engage in vigorous mating tactics later in
the season if they did not breed earlier. Furthermore, the
smallest males were expected to show less reduction in en-
ergy stores over the season than larger males. We observed
this last predicted relationship between mass or CI and sea-
sonal mass loss in P. fuscus, which suggests that large males
engage in vigorous mating tactics more often than smaller
ones do. Empirical studies have shown that in other amphib-
ian species, smaller males may be less competitive because
they are less attractive (e.g., Forester and Thompson 1998;
Howard and Young 1998) or because they cannot not allo-
cate enough energy to advertisement calls (e.g., Krupa 1989;
Tejedo 1992). Larger males invest more often than smaller
males in high-cost reproductive tactics such as fights (pref-
erentially against smaller paired males; Tejedo 1988) or call-
ing activity (see Sullivan and Sullivan 1985; Höglund and
Robertson 1988; Marquez and Tejedo-Madueno 1990).
In many amphibian species, length of stay in a breeding
pond is correlated with the probability of obtaining a female
by random mating (e.g., Reading and Clarke 1983; Semlitsch
et al. 1993) and is a major determinant of male mating suc-
cess (reviewed in Halliday 1987). Multiple mating by males
occurs in some species (e.g., Arak 1983b; Sullivan 1985;
Roithmair 1994), but is probably rare in P. fuscus because
males that have reproduced do not call anew, and sexual re-
gression starts right away and ends 10 days after mating
(Müller 1984). Wesenberg-Lund (1922) observed that males
as well as females left the pond immediately after egg lay-
ing. As a result we assume that a longer stay in the breeding
location probably does not result in multiple mating.
In our study, older (i.e., experienced) males tend to stay
fewer days in the breeding area, which suggests that they
succeed more quickly in finding a mate. Experience should
therefore be an advantage. Few studies have examined age
and reproduction patterns or reproductive success in amphib-
ians. The mating success of yearling male bullfrogs (Rana
catesbeiana) was lower when the number of old males was
high (Howard 1984). No differential age-based mating suc-
cess was observed in Bufo pardalis (Cherry and Francillon-
Vieillot 1992), and Forester and Thompson (1998) argued in
favour of age-linked alternative tactics (“gauntlet behaviour”)
in Bufo americanus, but they based their hypothesis on a
size-based analysis. In some species, young males may not
be sexually mature at the start of the breeding season, and

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50
arrive later (Howard 1981). The relationships between males’
mating tactics (territoriality, calling, fighting, satellite tactics)
in the breeding ponds and sex ratio, carrying capacity of the
pond, and male quality remain to be studied in P. fuscus. Our
study suggests that, according to the results of theoretical
studies, these relationships will evolve considerably over the
course of the breeding season. Age could be a weighty pa-
rameter that should be included in studies of amphibian be-
haviour, as not only mass and or size but also male
experience could influence individual behaviour, as was ob-
served in our study.
Acknowledgements
We thank S. Camaret and S. Blanc-Manel for statistical
discussions, C. LeBihan, P.H. Peyret, and J.N. Avrillier for
practical assistance, D. Allainé, C. Miaud, and G. Luikart
for reviewing an earlier version of the manuscript. Financial
support was provided by the Office National des Forêts and
Electricité de France. We had permission from the French
Ministère de l’Environnement to collect the toads (permit
No. 96/180).
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