Behavioral Ecology Vol. 13 No. 2: 175–181
Population differences in female resource
abundance, adult sex ratio, and male mating
success in Dendrobates pumilio
Heike Pröhl
Institut für Zoologie, Tierärztliche Hochschule Hannover, Bünteweg 17, 30559 Hannover, Germany
In this study I examined the relationship among abundance of reproductive resources, population density, and adult sex ratio
in the strawberry dart-poison frog, Dendrobates pumilio, and how these variables in turn influence the mating system, male
reproductive success, and sexual selection. I studied the mating behavior in two populations of D. pumilio living in a primary
and secondary rainforest on the Caribbean slope of Costa Rica. The abundance of tadpole-rearing sites (reproductive resources
for females) was approximately 10-fold higher in the secondary forest. Accordingly, the population density was higher and the
adult sex ratio was strongly female biased in the secondary forest, whereas the adult sex ratio was even in the primary forest.
The female-biased sex ratio was associated with a higher level of polygyny and higher male mating and reproductive success in
the secondary forest. In contrast, the level of polyandry did not differ between habitats. As expected, the opportunity for sexual
selection on male mating success was lower in the secondary forest, the habitat with high female density. In conclusion, my
results suggest that ecological variables such as resource availability have a great impact on the mating system and sexual selection
through their effect on population structure. Moreover, the results of this study give further evidence that the opportunity for
sexual selection is influenced by the adult sex ratio and hence by the operational sex ratio in a population. Key words: Dendrobates
pumilio, female reproductive resources, frogs, reproductive success, sex ratio, sexual selection. [Behav Ecol 13:175–181 (2002)]
T
he operational sex ratio (OSR), the ratio of males to females who are ready to mate in a population at a given
time (Emlen and Oring, 1977; Kvarnemo and Ahnesjö, 1996),
is an important determinant of the direction of mating competition and the intensity of sexual selection. Theory predicts
that a biased OSR will make the more abundant sex compete
for matings, and as a result the limited sex often has a greater
opportunity to mate selectively (Clutton-Brock and Parker,
1992; Emlen and Oring, 1977). Two factors that influence the
OSR are the potential reproductive rates (PRR) of the sexes
and the adult sex ratio (Clutton-Brock and Parker, 1992; Clutton-Brock and Vincent, 1991; Kvarnemo and Ahnesjö, 1996).
The PRR is inversely related to the relative parental investment expressed as time devoted to reproduction (CluttonBrock and Parker, 1992; Clutton-Brock and Vincent, 1991;
Parker and Simmons, 1996) and can be affected by certain
features of the social and physical environment, such as food
(Gwynne and Simmons, 1990; Kvarnemo, 1997; Kvarnemo
and Simmons, 1998; Simmons, 1992), temperature (Ahnesjö,
1995; Kruse, 1990; Kvarnemo, 1994) or nest site availability
(Almada et al., 1995).
The adult sex ratio also causes shifts in the OSR, as demonstrated in several animal groups (insects: Lawrence, 1986;
snakes: Madsen and Shine, 1993; birds: Colwell and Oring,
1988; fish: Balshine-Earn, 1996; Jirotkul, 1999; Kvarnemo et
al., 1995; Okuda, 1999). Interpopulation variation in the adult
sex ratio could therefore explain variation in the patterns of
intra- and intersexual behavior (Kvarnemo et al., 1995), direction of mating competition (Lawrence, 1986), degree of
polygyny and polyandry (Davies, 1992), variance in reproduc-
Address correspondence to H. Pröhl, who is now at the Section of
Integrative Biology C0930, University of Texas, Austin, TX 78746,
USA. E-mail: [email protected].
Received 21 October 1999; revised 12 March 2001; accepted 6 May
2001.
2002 International Society for Behavioral Ecology
tive success (Kodric-Brown, 1988), and intensity of sexual selection (Carroll and Salamon, 1995; Kodric-Brown, 1988).
Furthermore, spatial and temporal dispersal of resources
and other ecological conditions contribute to within-species
variation in mating patterns by directly affecting male–male
competition over nest sites (Forsgren et al., 1996), male spermatophore production (Gwynne, 1984; Gwynne and Simmons, 1990), and male reproductive success (Forsgren et al.
1996; Townsend, 1989). Resource abundance may also determine population density (Stewart and Pough, 1983), and it
influences the adult sex ratio and OSR (Almada et al., 1995;
Kvarnemo and Simmons, 1999; Simmons and Bailey, 1990).
In most species, female reproductive success is limited by access to resources necessary for reproduction, whereas male
reproductive success is limited by access to females (Trivers,
1972; Williams, 1966). Therefore, female density should be
higher where resources necessary for reproduction are more
abundant, and males should compete for places with high
female density (Davies, 1991, 1992; Emlen and Oring, 1977;
Ims, 1987). The impact of variation in available resources and
its consequences on OSR together with male mating success
have yet not been studied in anurans.
The aim of my field study was to show how the abundance
of a resource necessary for female reproduction could affect
sexual selection in the Neotropical frog Dendrobates pumilio.
I focus here on the relationship between the abundance of
tadpole rearing sites and the adult sex ratio and how these
variables in turn influence the mating system, male mating
success, and opportunity for sexual selection in two natural
populations.
The strawberry dart-poison frog, D. pumilio, is distributed
on the Caribbean slope from Nicaragua to Panama (Myers
and Daly, 1983). Populations are polymorphic in aposematic
color pattern (mostly orange to red), toxic skin alkaloid composition, density, body size, and vocalization (Myers and Daly,
1983). The frogs are diurnal and terrestrial, with most activity
occurring within 1 m from the forest ground. Males call from
exposed sites defending a territory for several months or years
Behavioral Ecology Vol. 13 No. 2
176
Table 1
Differences between primary and secondary forest in two study periods regarding vegetation structure
and availability of tadpole-rearing sites
Primary forest
Size of study area, m2
No. of 4-m2 quadrants
No. of observation days
No. of quadrants with
potential tadpole plants
Total no. of potential tadpole plants
Bromeliads
Dieffenbachia
Heliconia
Banana (Musa)
Maranthaceae
Tree holes
Sum
(Pröhl, 1997b). Eggs are laid after a complex and prolonged
courtship and moistened by males once a day (McVey et al.,
1981; Pröhl, 1997b). Females provide most parental investment by transporting the tadpoles to water-filled plant axils
(only one tadpole per axil) and subsequently feeding them
with unfertilized eggs (Weygoldt, 1980). During tadpole transportation females move short (⬃1 m) or longer distances (10–
15 m) to repeatedly used tadpole rearing sites that are located
within or outside the males’ territories (Pröhl, in press). The
mating system is polygamous, and male mating success is highly variable, being largely influenced by male calling activity
(Pröhl and Hödl, 1999). Reproductive systems of other dendrobatid frogs, especially the evolution and distribution of parental care between the sexes and the importance of this for
the direction of mating competition, have been intensely investigated (e.g., Summers, 1992; Summers and Earn, 1999).
The PRR of the sexes (‘‘time out’’ estimates, sensu Parker
and Simmons, 1996) have been used to explain the direction
of mating competition in one Costa Rican population of D.
pumilio (Pröhl and Hödl, 1999). These estimates suggested
that PRR of males are much higher than PRR of females. Female PRR is constrained by a high maternal investment that
includes tadpole transport and tadpole egg feeding that takes
several weeks during which females are not able to mate.
Thus, in a population with even adult sex ratio, females are
limiting as mates (i.e., the OSR is strongly biased toward
males), and males compete intensely for them (Pröhl and
Hödl, 1999). Use of a greater availability of tadpole rearing
sites (bromeliads) in another study led to an increase in the
density of adults of both sexes (Donnelly, 1989a). Donnelly
concluded that tadpole-rearing sites are a limiting resource
for D. pumilio. Population densities of D. pumilio vary greatly:
from the lowest densities found in primary forests with 2–3
adults per 100 m2 (Pröhl and Hödl, 1999) to the highest densities found in active cacao plantations with 13 adults per 100
m2 (Donnelly, 1989a,b). Likewise, the adult sex ratio varies
among studies from unbiased (Bunnell, 1973; Pröhl and
Hödl, 1999), to slightly biased (Donnelly, 1989a,b), to strongly
female biased (McVey et al., 1981).
I selected two study areas in a Costa Rican rainforest and
examined the population density and the adult sex ratio. I
found that the population density was low and the adult sex
ratio was unbiased in the first area, whereas the population
density was higher and female biased in the second area. Because the population structure of D. pumilio appears to be
influenced by the availability of tadpole-rearing sites and the
Secondary forest
1996
1997
884
221
88
884
221
91
16 (7.2%)
15 (6.8%)
10
4
1
—
—
2
17
9
6
1
—
—
1
17
1996
556
139
83
92 (66%)
—
2
⬎100
⬃60
3
—
⬎160
1997
556
139
95
89 (64%)
—
3
⬎100
⬃70
3
—
⬎170
adult sex ratio directly relates to the OSR, my hypotheses in
this study were (1) the higher population density and the
more female biased adult sex ratio are associated with a higher abundance of tadpole rearing sites; (2) the average male
mating and reproductive success increase in areas of higher
female density due to a higher level of polygyny; (3) the opportunity for sexual selection on males is higher in the area
with the unbiased adult sex ratio because it should result in
a more male-biased OSR (Emlen and Oring, 1977; Sullivan et
al., 1995); (4) the level of polyandry is unaffected by the adult
sex ratio because females cannot increase their reproductive
success by mating with a larger number of males due to their
low PRR (Pröhl and Hödl, 1999). To my knowledge, this is
the first report dealing with the relationship between the population structure and the mating system as well as male reproductive success in an anuran amphibian.
MATERIALS AND METHODS
Study area
The field research was conducted in a lowland rainforest at
Hitoy Cerere Biological Station on the Caribbean side of Costa Rica, between April and December 1996 and 1997. Two
study areas were selected, differing in their successional stage:
(1) an old secondary forest with transition to primary forest
and (2) an old banana plantation with transition to a young
secondary forest. Hereafter I refer to them as primary and
secondary forest, respectively (Table 1). Approximately 0.7 km
and a river separated the two study areas. The vegetation of
the primary forest principally consisted of large and smaller
trees, palms, lianas, and Dieffenbachia sp. (Araceae). The secondary forest was mainly composed of perennial plants such
as banana (Musa sp., Musaceae), Heliconia sp. (Heliconiaceae), Calathea sp. (Maranthaceae), and bamboo (Bambusa
sp., Poaceae). In the beginning of the observation period in
April 1996, a grid system was established in both study areas
by dividing the areas with nylon strings into 4-m2 quadrants.
The sizes of the study areas (Table 1) were chosen with regard
to the number of calling males, such that there were 12 males
in both areas in the beginning of the study.
Behavioral observations
During the first days of the study periods in 1996 and 1997 I
marked all frogs present in the study areas for permanent
Pröhl • Resources, sex ratio, and mating success in a dendrobatid frog
identification by toe-clipping in order to estimate population
density and mating success. Toe-clipping may impair frogs and
should be avoided whenever possible. Nevertheless, D. pumilio
is too small for the application of other markings, and because
toe-clipping did not seem to influence behavior or survivorship of D. pumilio, I used toe-clipping in this study after careful consideration of welfare implications. Frogs were observed
daily from 0700 to 1200 h, which is the time of the day when
calling and courtship activities are the highest (Pröhl, 1997a).
Observations alternated between the two study areas, one day
in the primary forest and the next day in the secondary forest.
However, on certain occasions, observations were made for 2
consecutive days in the same study area. In such cases, 2-day
observations were made in the other study area as well, so
that the total observed time in any given area was almost equal
(Table 1).
To determine population density, adult sex ratio, and male
mating success, I combined two observation methods: localization of all frogs in the study area and behavior sampling of
calling and courtship activities. In the first 20 min of every
day, I used the first method, scanning through the whole study
area to localize acoustically as well as visually as many frogs as
possible and to record their positions in the grid system. I
recognized individuals by natural marks such as black spots
on the back or head and their toe-clip pattern. I recorded if
the males called and if any animal was involved in courtship
activities. A male and female were considered a courting pair
when they were close together (⬍1 m), the male emitted
courtship or advertisement calls, and the female showed some
response to the male’s courtship (e.g., she moved toward him,
followed him through his territory, or was in body contact).
Unknown frogs were captured and toe-clipped. Subsequently,
I used the second method to observe courting pairs until oviposition or until one sex stopped the courtship. Often, more
than one courting pair was discovered but no more than one
could be observed at the same time. Therefore, in order to
avoid a bias in observations, I used a daily random ordering
of males to determine which courting male should be observed first. Because the calls of all males could be perceived
from any place in the study areas and every territory was
checked equally often, it was unlikely that specific males were
detected more frequently than others. When the observed
courtship was finished, I repeated the behavioral observations
in the same manner on different pairs until noon. On days
in which courting and mating activity were very high, I only
observed courting pairs throughout the observation day after
the initial localization of all frogs at 0700 h. Due to the higher
female density, courtship activity was also higher in the secondary forest, and on days with high activities several matings
could have remained undetected. Therefore, the average mating success of males in the secondary forest is probably underestimated, making the comparison between the sites conservative. Male mating and reproductive success are defined,
respectively, as the number of matings and the number of
tadpoles that hatched from eggs fertilized by that male.
Distribution of female resources
After a successful courtship, female D. pumilio laid a clutch of
several eggs in the leaf litter or in low vegetation. They then
transported their tadpoles to water-filled leaf axils of bromeliads or other plants. To assess the availability of tadpole-rearing sites, I counted all potential tadpole-rearing sites (i.e., all
plants similar to those observed to be used by frogs), which
were bromeliads (diam ⬎ 20 cm), bananas, Heliconia sp., Calathea sp., Dieffenbachia sp. (all ⬎ 1 m height), and little tree
or liana holes. I compared the study areas with regard to the
total number of potential tadpole-rearing sites as well as the
177
number of 4-m2 quadrants that contained potential tadpolerearing sites. The females in my study areas used tadpole-rearing sites close to the ground or in the low vegetation rather
than in the canopy (see Young, 1979). During 15 observed
tadpole transports in the primary forest, all tadpoles were deposited in tadpole-rearing sites below 3 m height. In the secondary forest (where no canopy existed at all) the highest
observed tadpole-rearing site was about 4 m in a banana leaf
axil. For that reason, I recorded only tadpole-rearing sites up
to 5 m height.
Data analysis
The population density within the study areas was determined
with the Peterson method (Krebs, 1989) comparing the observed individuals between two sample periods once each
month. One sample period combined the observations of 2
successive days (about the 10th of the month) and was separated from the second sample period (about the 20th) by at
least one week. Because the males of D. pumilio are territorial
and call (Pröhl, 1997b), they could be found almost all days
and their population size was exactly known. To calculate the
female population size, I subtracted the number of males
from the estimated population size for both sexes. After estimating the number of females and males, the adult sex ratio
was calculated as the percentage of males in the population:
number of males/(number of males ⫹ number of females)
(see Kvarnemo and Ahnesjö, 1996).
The Peterson method may give more reliable data for male
than for female population size and may violate some assumptions of the Peterson estimate such as equal catchability
of both sexes (see McVey, 1981) and a closed population
(Krebs, 1989). Therefore, I compared the Peterson estimates
with the number of daily observed individuals of both sexes
and populations and sex ratio estimates obtained by the JollySeber method (Krebs, 1989). Regarding the adult sex ratio,
the Peterson method resulted in values that were intermediate
between the values of the two other methods. The Jolly-Seber
method applies to open populations; nevertheless, it assumes
that any emigration is permanent. Because the majority of
females left the study area for shorter and longer times but
returned later, the Jolly-Seber method most likely resulted in
too-high values for female density. In contrast, the daily observed number of adults was probably male biased because
males behave more conspicuously than females. For these reasons, I consider the Peterson estimate as the most reliable
one, and only these data are presented here. In addition, the
estimates of population density and adult sex ratio should be
considered as relative rather than absolute values due to the
shortcomings in the assessment of the number males and females.
I used a chi-square test for comparisons of the number of
tadpole-rearing sites between habitats. A binominal test was
used to determine whether the numbers of males versus females deviated from a 1:1 ratio. A Fisher’s Exact test of independence was used to test whether the adult sex ratio differed between the habitats (Sokal and Rohlf, 1995). I compared male mating and reproductive success of territorial
males with a two-way ANOVA with area and year as independent factors. Because a Bartlett test revealed that variances
were not homogenous (Bartlett test, p ⬍ .05), data of male
mating and reproductive success were square-root transformed (Y⬘ ⫽ 兹Y ⫹ 0.5; Barlett test p ⬎ .3; Sokal and Rohlf,
1995) before conducting the ANOVA. Differences in levels of
polygyny and polyandry between areas were determined by
means of a Mann-Whitney U test (MWU).
To obtain an estimate of the overall potential for sexual
selection, I used the variation in male mating success. Al-
178
Behavioral Ecology Vol. 13 No. 2
though this is not a measure of selection intensity and says
nothing about the mechanism of selection (Koenig and Albano, 1986; Sutherland, 1985, 1987), it should give an estimate of the maximum opportunity for selection (Arnold and
Duvall, 1994; Arnold and Wade, 1984). I calculated the opportunity for sexual selection [Is ⫽ variance in male mating
success/(mean male mating success)2] and the coefficient of
variation (CV ⫽ SD ⫻ 100/mean) (following Arnold and Duvall, 1994; Arnold and Wade, 1984) for male mating success
at each site in each breeding season. Because the number of
observation days differed slightly between the study areas (Table 1), I also conducted all calculations adjusting the data of
mating and reproductive success to 80 observation days. The
results of these tests did not deviate essentially from the results
of the tests with original data, so only the latter are presented
here.
RESULTS
Availability of female reproductive resources
The secondary forest hosted significantly more suitable tadpole-rearing sites compared to the primary forest (Table 1).
The difference was significant comparing the number of
quadrants with potential tadpole plants (1996: ␹2 ⫽ 47.2, df
⫽ 1, p ⬍ .0001; 1997: ␹2 ⫽ 47.7, df ⫽ 1, p ⬍ .0001) as well
as comparing the total number of potential tadpole plants
found in both areas (1996: ␹2 ⫽ 115.5, df ⫽ 1, p ⬍ .0001;
1997: ␹2 ⫽ 125.2, df ⫽ 1, p ⬍ .0001).
Population density and adult sex ratio
In 1996, I found 26 females and 18 males (15 territorial) in
the primary forest area (Pröhl and Berke, 2001). In the same
year, I found 64 females and 14 males (13 territorial) in the
secondary forest. Only males that stayed and called inside the
study areas for at least 3 weeks were considered territorial.
Territorial males remained inside the study areas for longer
time periods, whereas the other frogs were probably more
mobile. Monthly estimates of the population density ranged
from 1.7 to 3.1 adults per 100 m2 in the primary forest (mean
⫾ SD ⫽ 2.3 ⫾ 0.53) and 6.1 to 8.5 adults (6.8 ⫾ 0.73) in the
secondary forest. In every month the secondary forest contained a greater density of adults than did the primary forest,
mainly due to the higher number of females (Figure 1).
During 1997, I found 20 females and 10 males (all territorial) in the primary and 64 females and 13 males (10 territorial) in the secondary forest. The population density was
always higher in the secondary forest, with densities ranging
from 1.5 to 2.2 adults per 100 m2 in the primary forest (mean
⫾ SD ⫽ 1.7 ⫾ 0.30) and from 5.3 to 8.2 adults per 100 m2 in
the secondary forest (7.2 ⫾ 0.96; Figure 1). In summary, the
population density in the secondary forest was approximately
three times the population density in the primary forest.
In the primary forest, the mean adult sex ratio was 0.54 ⫾
0.06 in 1996 (range ⫽ 0.50–0.69, n ⫽ 8 months) and 0.55 ⫾
0.08 in 1997 (range ⫽ 0.42–0.67). It did not deviate from a
1:1 ratio in any of the months (binominal test; 1996 and 1997:
p ⬎ .2 in all months). In contrast, in the secondary forest the
adult sex ratio was female biased, with a mean of 0.31 ⫾ 0.06
in 1996 (range ⫽ 0.22–0.39) and 0.24 ⫾ 0.04 in 1997 (range
⫽ 0.20–0.33) deviating from a 1:1 ratio in almost all months
(binominal test, all months p ⬍ .01, except May, July, August
1996 and November 1997: p ⬎ .05). The difference in the
adult sex ratio between sites was almost significant in 1996
(Fisher’s Exact test of independence, p ⫽ .08) and was significant in 1997 (p ⫽ .04). The differences in the adult sex ratio
between the areas were similar in both years and were not
Figure 1
Monthly estimated population size of male and female Dendrobates
pumilio in two study areas and during two study periods, (a) 1996
and (b) 1997. Black bars ⫽ primary forest, gray bars ⫽ secondary
forest: The first bar of every pair represents the number of males
(M), the second bar represents the number of females (F).
statistically distinguishable from one another (Fisher’s Exact
test of independence, p ⫽ .54).
Male mating and reproductive success, mating system, and
opportunity for sexual selection
A two-way ANOVA revealed differences in male mating success
between the study areas and the years (area: F1,44 ⫽ 12.5, p ⫽
.0009, year: F1,44 ⫽ 7.6, p ⫽ .008, interaction: F1,44 ⫽ 0.08, p
⫽ .78, after square root transformation); in other words, the
mating success was higher in the secondary forest and in the
second year (Figure 2). The number of tadpoles that survived
each year in a males’ territory was 0–7 and 0–5 in the first
area (mean ⫾ SD, 1996: 1.1 ⫾ 2.3, n ⫽ 15 males; 1997: 1.1
⫾ 1.6, n ⫽ 10 males) and 0–13 and 0–20 in the second area
(1996: 2.2 ⫾ 3.9, n ⫽ 13 males; 1997: 5.1 ⫾ 7.1, n ⫽ 10 males).
The difference in male reproductive success was significant
between areas (F1,44 ⫽ 4,18, p ⫽ .047) but not between years
(F1,44 ⫽ 1.81, p ⫽ .18, interaction: F1,44 ⫽ 1.35, p ⫽ .25, after
square-root transformation).
The level of polygyny (number of females mated per male)
was significantly higher in the secondary than in the primary
forest in both years (1996: U ⫽ 44, p ⫽ .013, n1 ⫽ 15, n2 ⫽
13, 1997: U ⫽ 13, p ⫽ .005, n1 ⫽ 10, n2 ⫽ 10; Figure 3). I did
not estimate female mating success because females were observed to follow courting males outside the study area, but
comparing the level of polyandry of females with high obser-
Pröhl • Resources, sex ratio, and mating success in a dendrobatid frog
Figure 2
Mating success of male Dendrobates pumilio (measured as number of
matings per male) in two study areas. PF ⫽ primary forest, SF ⫽
secondary forest.
vation frequency (n ⬎ 15 observations) inside both study areas, I found no difference between the habitats in either year.
The females in the primary forest mated with 0–3 males in
both years, and the females in the secondary forest mated with
0–5 (1996) or 0–4 males (1997) (MWU test, p ⬎ .7 in both
years).
In both years, estimates of the opportunity for sexual selection (Is) and the coefficient of variation of male mating success were higher in the primary than in the secondary forest
(t test for dependent samples: t ⫽ 14.8, p ⫽ .043, n ⫽ 2).
Thus, the opportunity for sexual selection was stronger in the
less female-biased population (Figure 4).
DISCUSSION
Together with other published work (Donnelly, 1989a), this
study suggests that the strawberry dart-poison frog, D. pumilio,
occupies habitats that vary in the availability of resources necessary for female reproduction. The data are also consistent
with the hypothesis (although they do not prove it) that resource availability has a strong impact on the mating system
and the degree of sexual selection through its influence on
population density and adult sex ratio in this species. Taking
into account the large difference in PRRs between the sexes
(Pröhl and Hödl, 1999), the OSR was strongly male biased in
the primary forest and, although the adult sex ratio is female
biased, the OSR remained male biased, only less, in the secondary forest. This difference in the OSR between the areas
should be ultimately responsible for the differences in the
mating system and the opportunity for sexual selection.
A higher density of female reproductive resources, namely
tadpole-rearing sites, was associated with a female biased adult
sex ratio and higher population density (prediction 1). The
great skew toward females in the secondary forest can be explained by female clumping in the vicinity of tadpole-rearing
sites (Pröhl and Berke, 2001). These results confirm those
from many other studies that documented that, as the abundance of reproductive resources (like nest sites) increases,
population density also increases (Donnelly, 1989a; Stewart
and Pough, 1983) or that the OSR shifts to the sex that depends on the reproductive resources (Almada et al., 1995;
Breitburg, 1987; Forsgren et al., 1996). In previous studies
(except Donnelly, 1989a) the impact of varying male reproductive resources was investigated, and an increase of these
resources was associated with a shift to a more male-biased
OSR corresponding to the demographic consequences of female resources in this study. In addition to resource availability, migration schedules, differences between the sexes in age
179
Figure 3
Degree of polygyny in Dendrobates pumilio measured as the number
of different (individual) mated females per male in two study areas.
Males in the primary forest mated with 0–4 females in 1996 and
with 0–5 females in 1997. In the secondary forest males mated with
0–10 females in both years. PF ⫽ primary forest, SF ⫽ secondary
forest.
at maturity, and mortality (Kvarnemo and Ahnesjö, 1996) or
sex change (Grafe and Linsenmair, 1989) may also affect the
adult sex ratio or OSR.
As a result of the more female-biased adult sex ratio in the
secondary forest, the average and maximum degree of polygyny was higher. Hence, because males obtained more mates,
the average male mating and reproductive success were also
higher (prediction 2).
Moreover, this study supports the hypothesis that an OSR
biased toward males should increase the intensity of selection
through a greater variance in male mating success (prediction
3; Emlen and Oring, 1977). However, my results do not support another prediction from Emlen and Oring (1977) that
the maximum degree of polygamy increases with the bias toward males in the OSR and is positively associated with the
intensity of sexual selection. Both the average and the maximum levels of polygyny were higher in the habitat with the
smaller bias in the OSR because more females were available
as mating partners. This fact demonstrates that the level of
polygyny (or polygamy) may not be positively correlated with
the intensity of sexual selection in animals with extended
Figure 4
Mean adult sex ratio (black bars) and opportunity for sexual
selection Is (striped bars) in terms of variation in male mating
success of Dendrobates pumilio measured in two different habitats
during two breeding seasons. Values of Is and coefficient of
variation (CV, in parentheses) are given above bars. PF ⫽ primary
forest, SF ⫽ secondary forest.
Behavioral Ecology Vol. 13 No. 2
180
breeding seasons. The same was found for anurans with short
breeding seasons (Sullivan et al., 1995).
So far, there have been few studies of how variation in OSR
might affect mating dynamics in amphibian breeding populations. In particular, the prediction that the degree of the
male bias will influence the variation in male mating success
has been rarely tested (Halliday and Tejedo, 1995; but see
Sullivan, 1989; Wagner and Sullivan, 1992). The present results are therefore important in supporting the hypothesis
that the intensity of selection will be higher when the OSR is
relatively more male biased and that environmental variables
have profound consequences for the action of sexual selection
(Emlen and Oring, 1977; Kvarnemo and Ahnesjö, 1996).
I found no differences in the level of polyandry between
the habitats (prediction 4). In accordance with an earlier
study (Pröhl and Hödl, 1999), females were observed to mate
with at most three (area 1) or five different males (area 2,
1997). I suspect that the distribution of tadpole-rearing sites
determines the size and shape of the females’ home ranges.
Females may then visit several males near their tadpole-rearing sites while assessing male quality (e.g., based on their calling activity; Pröhl and Hödl, 1999) and finally mate with them.
Because of the long time that females spent rearing tadpoles
(maximum four tadpoles at the same time; Pröhl, personal
observation), they may simply not have the time to increase
their reproductive success by assessing and mating with larger
numbers of males (see ‘‘time out’’ estimates in Pröhl and
Hödl, 1999).
Male mating and reproductive success not only varied between sites, but also between years. Nineteen ninety-seven was
an El Niño year with higher than average temperatures and
precipitation (Pröhl, personal observation). As I have previously demonstrated, high temperatures and precipitation
stimulate reproductive activity in D. pumilio (Pröhl, 1997b) as
well as in other frogs (Aichinger, 1987; Beebee, 1995; Duellman and Trueb, 1986). Due to more favorable climatic conditions in 1997, the mating activity and therefore male mating
and reproductive success were higher than in 1996. It seems
likely that climatic conditions influence the PPR in D. pumilio,
as has been found in the midwife toad Alytes muletensis (Bush,
1993) and some fish (Ahnesjö, 1995; Kvarnemo, 1994). For
instance, a higher female PRR might be responsible for the
lower Is in 1997 in the primary forest (Figure 4). The dependence of PRR and OSR on climatic factors was not the subject
of this study but should be considered for further investigation of D. pumilio’s reproductive behavior.
It has been emphasized that environmental factors can have
an intense influence on the distribution of the sexes (Emlen
and Oring, 1977) and might therefore be involved in the plasticity of anuran mating patterns. Sullivan (1989) described
how the spatial and temporal availability of water affects the
breeding system and opportunity of sexual selection in three
desert anurans. Climatic differences between northern and
southern Europe may account for different mating strategies
(i.e., scramble or lek) in common toads (Bufo bufo; Davies
and Halliday, 1977, 1978) and natterjack toads (Bufo calamita;
Arak, 1983; Denton and Beebee, 1993; Tejedo, 1988). Densityand OSR-dependent mating strategies have been documented
for Bufo calamita (Denton and Beebee, 1993; Tejedo, 1988),
Bufo valliceps (Sullivan et al., 1995; Wagner and Sullivan,
1992), Bufo bufo (Höglund and Robertson, 1988), Rana sylvatica (Woolbright, 1990), and Rana catesbeiana (Emlen,
1976; Howard, 1978). However, it remains unclear which
agents are responsible for differences in density and sex ratio
among years and populations. Reproductive resources (except
the breeding pond itself) may not play a role in any of the
mentioned species because they inhabit temperate zones and
provide no parental care. In contrast, many tropical anuran
exhibit (bi-)parental care and rely on reproductive resources.
To date the association between density and resource availability has only be successfully demonstrated for the tropical
species Eleutherodactylus coqui (Stewart and Pough, 1983) and
D. pumilio (Donnelly, 1989a,b). Hence, studies on mating system variation in tropical anuran are still lacking.
In conclusion, my results corroborate the prediction that
males and females disperse in response to ecological factors,
creating spatial differences in population parameters, mating
patterns, and the strength of sexual selection. However, due
to a lack of repeated observations in study areas with different
amounts of tadpole-rearing sites, this study shows only an association between ecological and behavioral variables. In future experiments, it will be necessary to track the relative importance of tadpole-rearing sites, adult sex ratio, and population density for the variability in mating success and the opportunity of sexual selection. Moreover, future work on the
ecology of mating systems should consider how resource availability influences male and female quality (i.e., fecundity),
PRR, and choosiness. Because all the mentioned variables interact in a complex way (e.g., Johnstone et al., 1996; Kvarnemo and Simmons, 1999), further analysis is needed to learn
how environmental factors affect these dynamic interactions
in mating systems.
Many thanks to the government of Costa Rica (Servicio de Parques
Nacionales) for providing the necessary permit to carry out the research, especially to Gustavo Induni for his support. For cooperation
and discussion in Costa Rica, I thank Jorge Cabrera and Carlos Drews
from the Universidad Nacional and Annely Haase for help in the
field. Comments of D. Johnson, G. Johnston, N. Kime, C. Kvarnemo,
C.M. Lessels, U. Radespiel, M. Ryan, I. Schlupp, E. Zimmermann, and
three anonymous referees greatly improved the manuscript. I am also
grateful to Olaf Berke for statistical advice and to Katja Heubel for
introducing me the Signal Plot Graphic Program. This work was supported by the German Academic Exchange Service, DAAD.
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