| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Behavioral Ecology Vol. 13 No. 2: 175-181
© 2002 International Society for Behavioral Ecology
Population differences in female resource abundance, adult sex ratio, and male mating success in Dendrobates pumilio
Institut für Zoologie, Tierärztliche Hochschule Hannover, Bünteweg 17, 30559 Hannover, Germany
Address correspondence to H. Pröhl, who is now at the Section of Integrative Biology C0930, University of Texas, Austin, TX 78746, USA. E-mail: hproehl{at}hotmail.com .
Received 21 October 1999; revised 12 March 2001; accepted 6 May 2001.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
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.
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
The 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
(Clutton-Brock 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
reproductive 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 (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 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 |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
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 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 ovi-position 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 number of 4-m2 quadrants that contained potential
tadpole-rearing 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
Jolly-Seber 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
(
; 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. Although 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 x 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 |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
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 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 observation 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 |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
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 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
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). Density- and 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.
|
ACKNOWLEDGEMENTS |
|---|
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.
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Ahnesjö I, 1995. Temperature affects male and female potential reproductive rates differently in the sex-role reversed pipefish Syngnathus typhle. Behav Ecol 6: 229-233.
Aichinger M, 1987. Annual activity patterns of anurans in a seasonal neotropical environment. Oecologia 71: 583-592.[Web of Science]
Almada VC, Goncalves EJ, Oliviera RF, Santos AJ, 1995. Courting females: ecological constraints affect sex roles in a natural population of the blenniid fish Salaria pavo. Anim Behav 49: 1125-1127.
Arak A, 1983. Male-male competition and mate choice in anuran amphibians. In: Mate choice (Bateson P, ed) Cambridge: Cambridge University Press; 181-210.
Arnold SJ, Duvall D, 1994. Animal mating systems: a synthesis based on selection theory. Am Nat 143: 317-348.[Web of Science]
Arnold SJ, Wade MJ, 1984. On the measurement of natural and sexual selection: theory. Evolution 38: 709-719.[Web of Science]
Balshine-Earn S, 1996. Reproductive rates, operational sex ratios and mate choice in St Peter's fish. Behav Ecol Sociobiol 39: 107-116.[Web of Science]
Beebee TJC, 1995. Amphibian breeding and climate. Nature 374: 219-220.[Web of Science]
Breitburg DL, 1987. Interspecific competition and the abundance of nest sites: factors affecting sexual selection. Ecology 68: 1844-1855.[Web of Science]
Bunnell P, 1973. Vocalizations in the territorial behavior of the frog Dendrobates pumilio. Copeia 1973: 277-285.
Bush S, 1993. Courtship and male parental care in the Majorcan midwife toad, Alytes muletensis (PhD dissertation). East Anglia: University of East Anglia.
Carroll S, Salamon MH, 1995. Variation in sexual selection on male body size within and between populations of the soapberry bug. Anim Behav 50: 1463-1474.
Clutton-Brock TH, Parker GA, 1992. Potential reproductive rates and the operation of sexual selection. Q Rev Biol 67: 437-456.
Clutton-Brock TH, Vincent ACJ, 1991. Sexual selection and the potential reproductive rates of males and females. Nature 351: 58-60.[Medline]
Colwell MA, Oring LW, 1988. Sex ratios and intrasexual competition for mates in a sex-role reversed shorebird, Wilson's phalarope (Phalaropus tricolor). Behav Ecol Sociobiol 22: 165-173.[Web of Science]
Davies NB, 1991. Mating systems. In: Behavioral ecology: an evolutionary approach (Krebs JR, Davies NB, eds). Oxford: Blackwell Scientific; 263-294.
Davies NB, 1992. Dunnock behaviour and social evolution. Oxford: Oxford University Press.
Davies NB, Halliday TR, 1977. Optimal mate selection in the toad Bufo bufo. Nature 269: 56-58.
Davies NB, Halliday TR, 1978. Deep croaks and fighting assessment in toads Bufo bufo. Nature 274: 683-685.
Denton JS, Beebee TJC, 1993. Reproductive strategies in a female biased population of natterjack toads, Bufo calamita. Anim Behav 46: 1169-1175.
Donnelly MA, 1989a. Effects of reproductive resource supplementation on space-use patterns in Dendrobates pumilio. Oecologia 81: 212-218.[Web of Science]
Donnelly MA, 1989b. Reproductive phenology and age structure of Dendrobates pumilio in Northeastern Costa Rica. J Herpetol 23: 362-367.
Duellman WE, Trueb L, 1986. Biology of amphibians. New York: McGraw-Hill.
Emlen ST, 1976. Lek organization and mating strategies in the bull-frog. Behav Ecol Sociobiol 1: 283-313.[Web of Science]
Emlen ST, Oring LW, 1977. Ecology, sexual selection,
and the evolution of mating systems. Science
197: 215-223.
Forsgren E, Kvarnemo C, Lindström K, 1996. Mode of sexual selection determined by resource abundance in two sand goby populations. Evolution 50: 646-654.[Web of Science]
Grafe TU, Linsenmair KE, 1989. Protogynus sex change in the reed frog Hyperolius viridiflavus. Copeia 1989: 1024-1029.
Gwynne DT, 1984. Sexual selection and sexual differences in mormon crickets (Orthoptera: Tettigoniidae, Anabrus simplex). Evolution 38: 1011-1022.[Web of Science]
Gwynne DT, Simmons LW, 1990. Experimental reversal of courtship roles in an insect. Nature 346: 172-174.
Halliday T, Tejedo M, 1995. Intrasexual selection and alternative mating behavior. In: Amphibian biology, social behavior, vol 2 (Heathole H, Sullivan BK, eds). Chipping Norton, UK: Surrey Beatty & Sons; 419-468.
Höglund J, Robertson JGM, 1988. Chorusing behaviour, a density dependent alternative mating strategy in male common toads Bufo bufo. Ethology 79: 324-332.[Web of Science]
Howard RD, 1978. The evolution of mating strategies in bullfrogs, Rana catesbeiana. Evolution 32: 850-871.[Web of Science]
Ims RA, 1987. Responses in spatial organization and behaviour to manipulations of the food resource in the vole Clethrionomys rufocanus. J Anim Ecol 56: 585-596.
Jirotkul M, 1999. Operational sex ratio influences female preference and male-male competition in guppies. Anim Behav 58: 287-294.[Web of Science][Medline]
Johnstone RA, Reynolds JD, Deutsch JC, 1996. Mutual mate choice and sex differences in choosiness. Evolution 50: 1382-1391.[Web of Science]
Kodric-Brown A, 1988. Effects of sex-ratio manipulation on territoriality and spawning success of the male pupfish, Cyprinodon pecosensis. Anim Behav 36: 1136-1144.
Koenig WD, Albano SS, 1986. On the measurement of sexual selection. Am Nat 127: 403-409.[Web of Science]
Krebs CJ, 1989. Ecological methodology. New York: Harper & Row.
Kruse KC, 1990. Male backspace availability in the giant waterbug (Belostoma flumineum). Behav Ecol Sociobiol 26: 281-289.[Web of Science]
Kvarnemo C, 1994. Temperature differentially affects
male and female reproductive rates in the sand goby: consequences for OSR.
Proc R Soc Lond B 256:
151-156.
Kvarnemo C, 1997. Food affects the potential
reproductive rates of sand goby females but not of males. Behav
Ecol 8:
605-611.
Kvarnemo C, Ahnesjö I, 1996. The dynamics of operational sex ratio and competition for mates. Trends Ecol Evol 11: 404-408.
Kvarnemo C, Forsgren E, Magnhagen C, 1995. Effects of sex ratio on intra- and inter-sexual behaviour in sand gobies. Anim Behav 50: 1455-1461.
Kvarnemo C, Simmons LW, 1998. Male potential reproductive rate influences mate choice in a bushcricket. Anim Behav 55: 1499-1506.[Web of Science][Medline]
Kvarnemo C, Simmons LW, 1999. Variance in female quality, operational sex ratio and male mate choice in a bushcricket. Behav Ecol Sociobiol 45: 245-252.[Web of Science]
Lawrence WS, 1986. Male choice and competition in Tetraopes tetraophthalmus: effects of local sex ratio variation. Behav Ecol Sociobiol 18: 289-296.[Web of Science]
Madsen T, Shine R, 1993. Temporal variability in sexual selection acting on reproductive tactics and body size in males snakes. Am Nat 141: 167-171.[Web of Science]
McVey ME, Zahary RG, Perry D, MacDougal J, 1981. Territoriality and homing behavior in the poison-dart frog (Dendrobates pumilio). Copeia 1981: 1-8.
Myers CW, Daly JW, 1983. Dart-poison frogs. Sci Am 248: 120-133.[Web of Science][Medline]
Okuda N, 1999. Sex roles are not always reversed when the potential reproductive rate is higher in females. Am Nat 153: 540-548.[Web of Science]
Parker GA, Simmons LW, 1996. Parental investment and
the control of sexual selection: predicting the direction of sexual
competition. Proc R Soc Lond B 263:
315-321.
Pröhl H, 1997a. Patrón reproductivo en Dendrobates pumilio (Anura: Dendrobatidae). Rev Biol Trop 45: 1671-1676.
Pröhl H, 1997b. Territorial behavior of the strawberry poison-dart frog, Dendrobates pumilio. Amphib-Reptil 18: 437-442.
Pröhl H, Berke O, 2001. Spatial distribution of male and female strawberry poison frogs and their relation to female reproductive resources. Oecologia 129: 534-542.[Web of Science]
Pröhl H, Hödl W, 1999. Parental investment, potential reproductive rates and mating system in the strawberry poison-dart frog Dendrobates pumilio. Behav Ecol Sociobiol 46: 215-220.[Web of Science]
Simmons LW, 1992. Quantification of the role reversal in a relative parental investment in a bushcricket. Nature 358: 61-63.
Simmons LW, Bailey WJ, 1990. Resource influenced sex roles of zaprochiline tettigonids (Orthoptera: Tettigoniidae). Evolution 44: 1853-1868.[Web of Science]
Sokal RR, Rohlf FJ, 1995. Biometry. New York: Freeman.
Stewart MM, Pough FH, 1983. Population density of
tropical forest frogs: relation to retreat sites. Science
221: 570-572.
Sullivan BK, 1989. Mating system variation in woodhouse's toad (Bufo woodhousii). Ethology 83: 60-68.[Web of Science]
Sullivan BK, Ryan MJ, Verrell PA, 1995. Female choice and mating system structure. In: Amphibian biology, social behavior, vol 2 (Heathole H, Sullivan BK, eds). Chipping Norton, UK: Surrey Beatty & Sons; 469-517.
Summers K, 1992. Mating strategies in two species of dart-poison frogs: a comparative study. Anim Behav 43: 907-919.
Summers K, Earn DJD, 1999. The cost of polygyny and the evolution of female care in poison frogs. Biol J Linn Soc 66: 515-538.
Sutherland WJ, 1985. Chance can produce a sex difference in variance in mating success and account for Bateman's data. Anim Behav 33: 1349-1352.
Sutherland WJ, 1987. Random and deterministic components. In: Sexual selection: testing the alternatives (Bradbury JW, Andersson MB, eds). Chichester, UK: Wiley & Sons; 209-219.
Tejedo M, 1988. Fighting for females in the toad Bufo calamita is affected by the operational sex ratio. Anim Behav 36: 1765-1769.
Trivers RL, 1972. Parental investment and sexual selection. In: Sexual selection and the descent of man (Campbell BG, ed). Chicago: Aldine; 136-179.
Townsend DS, 1989. The consequences of microhabitat choice for male reproductive success in a tropical frog (Eleutherodactylus coqui). Herpetologica 45: 451-458.[Web of Science]
Wagner EW, Sullivan BK, 1992. Chorus organization in the Gulf Coast toad (Bufo valliceps): male and female behavior and the opportunity for sexual selection. Copeia 1992: 647-658.
Weygoldt P, 1980. Complex brood care and reproductive behavior in captive poison arrow frogs, Dendrobates pumilio O. Schmidt. Behav Ecol Sociobiol 7: 329-332.[Web of Science]
Williams GC, 1966. Adaption and natural selection. Princeton, New Jersey: Princeton University Press.
Woolbright LL, Greene EJ, Rapp G, 1990. Density-dependent mate searching strategies of male woodfrogs. Anim Behav 40: 135-142.
Young AM, 1979. Arboreal movement and tadpole-carrying of Dendrobates pumilio Schmidt (Dendrobatidae) in Northeastern Costa Rica. Biotropica 11: 238-239.[Web of Science]
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  H. Kokko and D. J Rankin Lonely hearts or sex in the city? Density-dependent effects in mating systems Phil Trans R Soc B, February 28, 2006; 361(1466): 319 - 334. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. G. Byrne and J. D. Roberts Intrasexual selection and group spawning in quacking frogs (Crinia georgiana) Behav. Ecol., September 1, 2004; 15(5): 872 - 882. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||