Ó Springer-Verlag 1999
Behav Ecol Sociobiol (1999) 46: 215±220
ORIGINAL ARTICLE
Heike ProÈhl á Walter HoÈdl
Parental investment, potential reproductive rates, and mating system
in the strawberry dart-poison frog, Dendrobates pumilio
Received: 9 June 1998 / Received in revised form: 27 March 1999 / Accepted: 3 April 1999
Abstract We studied the e€ect of relative parental investment on potential reproductive rates (PRRs) to explain sex di€erences in selectivity and competition in the
dart-poison frog Dendrobates pumilio. We recorded the
reproductive behavior of this species in a Costa Rican
lowland rainforest for almost 6 months. Females spent
more time on parental care than males, and `time out'
estimates suggest that PRRs of males are much higher
than than those of females, rendering females the
limiting sex in the mating process. Males defended
territories that provide suitable calling sites, space for
courtship and oviposition, and prevent interference by
competitors. Male mating success was highly variable,
from 0 to 12 matings, and was signi®cantly correlated
with calling activity and average perch height, but was
independent of body size and weight. Estimates of
opportunity for sexual selection and variation in
male mating success are given. The mating system is
polygamous: males and females mated several times with
di€erent mates. Females were more selective than
males and may sample males between matings. The
discrepancy in PRRs between the sexes due to di€erences in parental investment and the prolonged breeding
season is sucient to explain the observed mating
pattern i.e., selective females, high variance in male
mating success, and the considerable opportunity for
sexual selection.
H. ProÈhl (&)
Institut fuÈr Zoologie, TieraÈrztliche Hochschule Hannover
BuÈnteweg 17, D-30559 Hannover, Germany
e-mail: [email protected], Fax: +49-511-9538586
W. HoÈdl
Institut fuÈr Zoologie, UniversitaÈt Wien, Althanstraûe 14
A-1090 Wien, Austria
Supplementary material Appendix 1 containing visiting sequences
and intersexual interactions of 12 females is available in electronic
form on Springer Verlag's server at http://link.springer.de/
journals/bes/index.htm
Key words Potential reproductive rates á
Parental investment á Territoriality á
Sexual selection á Dendrobates pumilio
Introduction
The concept of parental investment has been used to
explain sex di€erences in mating competition found in
many animal reproductive systems (Trivers 1972). Emlen
and Oring (1977) synthesized the evolution of animal
mating systems, parental investment, sexual selection,
resource defense, and environmental factors into a uni®ed theory. They argued that when one sex becomes a
limiting factor (e.g., due to high parental investment), the
result is increased intrasexual competition among members of the opposite sex. A more recent approach introduced the concept of potential reproductive rates (PRRs,
measured as the maximum number of independent o€spring that parents can produce per unit time) in relation
to the direction of mating competition (Clutton-Brock
and Vincent 1991; Clutton-Brock and Parker 1992). The
PRR is inversely (but not exclusively) related to parental
investment. Recently, it has been suggested that the costs
of reproduction can be measured empirically as the
parent's `time out', a principal component of PRR,
which in turn relates directly to the operational sex ratio
(OSR, the ratio of males to females ready to mate;
Kvarnemo and AhnesjoÈ 1996). In this model, `time out' is
the processing time for a given reproductive event and
`time in' is the time spent on mate acquisition (Parker and
Simmons 1996). The ratios of `time out' are sucient to
predict the direction of mating competition: the sex with
the lower `time out' or the higher PRR competes more
intensely for mates, whereas the sex with the higher `time
out' can a€ord to be selective and choose high-quality
mates without loosing mating opportunities (Kvarnemo
and AhnesjoÈ 1996; Parker and Simmons 1996).
Selective females and competing less selective males
have been reported in several studies investigating the
216
behavior of neotropical poison frogs (Dendrobatidae)
(Summers 1989; Roithmair 1992, 1994). The inequality
of relative parental investment and variance in male
quality have been identi®ed as factors causing sexual
selection in this group (Summers 1992a,b). Two studies
suggest that female mate choice is the reason for variance in male mating success and that male territoriality
is associated with competition for females (Roithmair
1992, 1994). The direction of mating competition has
not yet been analyzed in terms of PRR or OSR in these
frogs. This study analyzes the mating system of
Dendrobates pumilio within the framework of the
above-mentioned concepts. The social behavior of
D. pumilio seems particularly interesting, because males
are territorial and their parental care is minimal,
whereas females perform most duties associated with the
care of o€spring (Weygoldt 1980; McVey et al. 1981).
We test the following hypotheses about the mating
system of D. pumilio. First, due to di€erences in parental
investment, `time out' of female D. pumilio will be
greater than male `time out' and, therefore, females are
the sex with the lower PRR and are limited as mates.
Second, because of their lower PRR, females are more
selective about mates than males, and female choice may
lead to variance in male mating success and polygyny in
successful males. Finally, male territorial behavior is
related to competition for access to females.
Methods
The study organism
The strawberry dart-poison frog D. pumilio is a member of the
neotropical family Dendrobatidae. Its distribution ranges from
Nicaragua to Panama on the Atlantic coast (Myers and Daly 1983)
where it inhabits lowland forests and fruit plantations (McVey et al.
1981; Donnelly 1989b). Populations vary in color, color pattern,
density, body size, and calls (Myers and Daly 1983). Populations in
Costa Rica are colored orange to red with red, black, or blue hind
limbs. The aposematic coloration indicates the defensive function
of toxic skin alkaloids in D. pumilio (Myers and Daly 1983).
The courtship of D. pumilio is complex, prolonged, and involves
tactile, visual, and acoustic stimuli (Limerick 1980; Zimmermann
and Zimmermann 1988). Oviposition is terrestrial (Limerick 1980)
and fertilized eggs are hydrated by the male. After hatching, tadpoles are transported to water-®lled axils of bromeliads (only one
tadpole per axil) by the female frogs and are subsequently fed with
unfertilized eggs (Limerick 1980; Weygoldt 1980, 1987).
Males are territorial and females are not (Bunnell 1973; McVey
et al. 1981). Males' advertisement calls are used for mate attraction
and spacing and are characterized by a high sound intensity.
Courtship calls consume less energy and are used in short-range
and tactile interactions between the sexes (Zimmermann 1990).
Adult D. pumilio are sexually monomorphic in color (except
throat), have a mean snout-vent length (SVL) of 2.14 cm and a
mean weight of 0.93 g (ProÈhl 1997a).
In Hitoy Cerere, D. pumilio is very common and reaches
higher population densities than other sympatric dendrobatid
species (personal observation). The high population density,
territoriality, continuous breeding (Donnelly 1989a,b), diurnal
activity (ProÈhl 1997a) and longevity (Weygoldt 1987) make
D. pumilio an ideal subject for ecological, behavioral, and
demographic ®eld studies.
Field studies
The study was carried out during the wet season between 2 July and
21 December 1993, at Hitoy Cerere biological station on the
Atlantic side of Costa Rica (9°40¢ N, 83°05¢ E). The study area was
located at 200 m above sea level in a primary forest rich in vines,
palms, and climbing plants. The area measured 748 m2 (22 ´ 34 m)
and was divided into 1 ´ 1 m quadrants using a system of overhead-running nylon strips.
All adult frogs captured in the study area were toe-clipped (one
or two toes on di€erent feet) for individual identi®cation. Toeclipping did not seem to in¯uence behavior because males continued to call after their release. The sexes were distinguished by
throat color: females have a red throat and males have a gray or
black throat. All adult frogs captured in the study area were
measured to the nearest 0.01 mm SVL and weighed to the nearest
0.01 g using a spring balance (Pesola). Measurements were repeated for males at least three times within the study period and
average values were used for statistics.
Because calling and mating activity of the frogs were highest
between 8:00 a.m. and 11:00 a.m. (ProÈhl 1997a), their reproductive
behavior was studied daily from 7:00 a.m. to 12:00 a.m. The study
covered a total of 143 days. Males and females were located every
hour and their position in the study area (quadrant number) was
recorded. In addition, type of calling site (e.g., litter, vines, or
buttresses) and perch height were recorded for calling males.
Interactions between any two individuals were recorded ad
libitum. A courtship was de®ned as an interaction where a female
approaches and follows a calling male at least a short distance. A
mating is a courtship that results in oviposition and a single clutch.
After mating had been observed, egg development until hatching of
tadpoles was monitored. The number of times a male was observed
to mate is considered as his mating success and the number of
hatched tadpoles as his reproductive success.
Data analyses
The density of both sexes within the study area was determined
from population estimates using the Peterson method (Krebs 1989)
comparing the observed individuals between two sample periods
once each month from July to November. One sample period
combined the observations of 2 successive days and was separated
from the second sample period by at least 1 week. In December, the
activity was very low so that the majority of the frogs could not be
found (ProÈhl 1997a). To determine if the sex ratio di€ered from a
1:1 ratio, we used the chi-square test.
The total calling activity of each male was calculated by adding
up all hours when a male called at least once. A territory is de®ned
as the calling area of one male, used exclusively and defended from
male intruders. The territory size was calculated using the modi®ed
minimum-area method (Harvey and Barbour 1965) which eliminates large areas without records. The centers of all quadrants in
which a male called were connected to obtain the limits of his
territory.
The data were analyzed using the software package Statistica
5.0. The distribution of data was assessed from visual analysis of
box-and-whisker plots. For some variables (e.g., mating success)
the box-and-whisker plots revealed a skewed distribution and
outliers. For this reason, nonparametric descriptive statistics were
generally used. A correlation analysis (Pearson product-moment)
and a multiple-regression model (stepwise forward-selection procedure) were used to explain the e€ects of male traits on male
mating success.
The reproductive cycle of an individual is divided between being
ready to mate (`time in') and not being ready to mate (`time out').
`Time out' is the time devoted to gamete production, mating, and
parental care. It was calculated for both sexes of D. pumilio using
the technique proposed by Parker and Simmons (1996). The technique considers a series of special cases according to the degree of
male parental investment and number of males and females involved in one reproductive event. Since the production of one
217
clutch in our species involves just one male and one female and
male parental care is low, we used a slightly modi®ed approach
from `case 1' including male parental care and egg mortality. Thus,
we added the means of the duration of the observed reproductive
activities not compatible with mate searching. These are mating
and egg attendance for the males and production of clutches,
mating, and tadpole transport for the females.
The calculation of the opportunity for sexual selection on male
reproductive success followed the modi®cation by Kluge (1981) of
the models developed by Wade and Arnold (1980). According to
these models the index of the opportunity for sexual selection IS is
the variance of male mating success S2S divided by the square mean
of male mating success X2S . This index and the coecient of variation on male mating success are given for comparisons with other
species (Table 2).
Results
Population density and territoriality
The calculation of population density indicates that 9±
12 males (mean=11, n=5) and 6±12 (mean=9, n=5)
females resided in the study area. The sex ratio did not
di€er signi®cantly from 1:1 (chi-square test: P > 0.4 for
each month). Because several animals stayed only some
days in the area, however, a total of 29 females and 20
males were recorded within the study period.
Six males either did not call or called for less than
3 days and left the study area after a short time. These
males were not considered as territorial. They did not
di€er from territorial males regarding color, SVL
(t=0.30, P=0.77), or weight (t=0.74, P=0.47). The
remaining 14 males defended territories using them as
calling site, courtship area, and oviposition site (Fig. 1)
from 13 days to the entire study period (172 days,
mean=128 days, n=14 males). Territories were defended against conspeci®c calling intruders with calls
(n=13) and ®ghts (n=4) which were always won by the
residents. Territory centers, where males were predomi-
nantly found, contained vegetation structures (e.g.,
vines, stilt roots, and buttresses) which males used as
calling sites: 70% of calling activity occurred from elevated calling perches. Tadpole-rearing sites (bromeliads)
were located outside the territories and were not defended by males. Female home ranges exceeded the
limits of the study area (ProÈhl 1997b).
Di€erences in male traits, mating,
and reproductive success
Individual males di€ered considerable in their territorial
and mating behavior. Thus, we found great variation in
calling activity among territorial males ranging from 5 to
291 h [median=145.5, interquartile range (Iqr)=169,
n=14 males]. The median individual perch height varied
from 5 to 79 cm (median=26, Iqr=27, n=14 males)
and territory size from 1 to 24.5 m2 (median=11,
Iqr=10, n=14).
Mating frequency and reproductive success of males
were also highly variable. Only territorial males were
observed mating. The two most successful males mated
12 times, the other males mated between 0 and 5 times
(median=1.5, Iqr=5, n=14 males) (Fig. 1). Male
calling activity and average perch were highly correlated
with mating success and explained 86% of the variation
in male mating success in a multiple-regression model
(Table 1). Territory size and number of days present
showed lower correlations, and SVL and weight did not
correlate nor did they enter the regression model
(Table 1). Moreover, reproductive success, de®ned as
the number of hatched tadpoles (Median=0, Iqr=3,
n=14 males) was highly correlated with mating success
(r=0.81, P < 0.001). The 22 hatched tadpoles were
from ten clutches which belonged to four males.
Females visited males with higher mating success
more frequently than less successful ones. The number
of females found in a territory and the visiting frequency
(Fig. 1) were both signi®cantly correlated with mating
success (r=0.66, P=0.010, n=14; r=0.84, P < 0.001,
n=14, respectively). Estimates of the opportunity for
sexual selection based on variance in male mating success are presented in Table 2.
Courtship behavior and mating system
Fig. 1 Territorial boundaries of male Dendrobates pumilio. Male 17
settled after male 1 disappeared from the study area (n©/n$/
n=number of matings a male achieved/number of di€erent females
that visited the territory/total number of female visits to the territory)
All courtships and ovipositions took place during the
morning in the territory of the resident male. The mean
duration of a mating was 1.5 h (mean=89 min,
SD=37 min, n=33) and mean clutch size was 4.6 eggs
(range: 3±7 eggs, SD=1.06, n=37) (ProÈhl 1997a,b).
A total of 9 males and 14 females mated. Females visited
up to four territories before and between matings
(Appendix 1). In 36 of 42 matings (42 observed
matings + 2 clutches found=evidence for 44 successful
matings) it was possible to identify the mating female. In
11 unsuccessful courtships, the females rejected the male
218
Table 1 Summary of correlation and multiple-regression analysis
for male mating success and variables (male traits) potentially affecting the mating success. Because of a skewed distribution, the
Dependent
variable
Explanatory
variable
Male mating
success
Calling activity
Average perch
height
Territory size
Number of days
present
Snout-vent length
Weight
dependent variable was square root transformed for the regression
model. Minimum F to enter the model was 4.0. Variables with a
nonsigni®cant e€ect (P>0.05) were omitted from the model
Simple correlation
Multiple regression model
Correlation coecient P-value
Partial correlation coecient P-value R2 model P-value model
0.79
0.83
0.0008
0.0002
0.75
0.57
0.52
0.47
0.057
0.092
0.18
0.06
0.54
0.85
Table 2 Calculation of the opportunity for sexual selection in male
Dendrobates pumilio (according to Wade and Arnold 1980; Kluge
1981)
Mean of male mating success
Variance of male mating success
Intensity of sexual selection
Coecient of variation of male mating
success
XS = 3.14
S2S = 17.36
IS = S2S /X2S = 1.76
CV = 132.6
and left the territory. On only two occasions did the
male stop calling during the courtship, although females
seemed to be willing to court. The di€erence between 11
female to 2 male courtship stops is signi®cant
(chi-square=6.2, df =1, P=0.01). Prior to the matings,
females had been courted by the same (n=5) or another
male (n=4), they had mated with the same (n=15) or
another male (n=3), or they had neither mated nor
courted (n=9). Female-female aggression was never
observed even in the presence of a calling male (n=8).
One of the most successful males (M2, Fig. 1) mated
with at least ®ve di€erent females, while females mated
with one to three males (Appendix 1). However, females
also mated with males outside the study area. Eight females returned to the same male and mated with him
repeatedly, e.g., F19 and M8 mated six times until tadpole transport (Appendix 1). The two most successful
males were observed to mate once with two (M8) and
once with three females (M2) in succession. In contrast,
the average observed interval between two matings of a
female was 4.4 days (range=3±7 days, n=8).
0.0027 0.86
0.400
<0.001
Since males moistened their clutches once a day,
which on average took 10 min (0.17 h, n=8), males
`time out' to rear one o€spring, Gm, is 2 ´ 1.5 h (two
matings) + 12 ´ 0.17 h (to moisten one clutch during
12 days)=5 h.
Because the average clutch size was 4.6 eggs and the
average interval between two successive matings of a
female was 4.4 days we conclude that the production of
one egg takes approximately 1 day. Furthermore, the
mean duration of tadpole transport to water®lled
bromeliads was 3 h (range 2.0±4.5 h, n=4 completely
observed tadpole transports). Development until metamorphosis of two tadpoles lasted 43 and 46 days, respectively. Because the mothers of these tadpoles had a
second tadpole at the same time, tadpole rearing of only
one tadpole may cost 22±23 days. This is consistent with
the observation that the females provided each tadpole
with unfertilized eggs ®ve times (5 ´ 4.6 eggs=23 eggs
corresponding to approximately 23 days of egg production).
Hence, female `time out', Gf, is: 8 days (egg production) + 2 ´ 1.5 h (matings) + 3 h (tadpole transport) + 22 days (tadpole rearing)=30 days + 6 h.
It follows that the ratio female `time out' to male
`time out', Gf/Gm, is 366/5 h=73.2.
It is evident that mating, egg attendance, and tadpole
transport are negligible compared to egg production for
clutches and tadpole rearing. This calculation did not
consider the time for sperm replenishment because it is
not known. But even if we assume that sperm replenishment takes 1 or more days, male `time out' should be
much smaller than female `time out' or, in other words,
male PRR is much greater than that of the female.
Parental investment and calculation of `time out'
While both sexes provide parental care, females spend
more time raising the o€spring. To demonstrate this, we
calculated `time out' for both sexes of our species. For
these calculations, we took into account that only 12% of
the eggs survived and if so, lasted on average 12 days
until tadpole hatching. Because of high egg mortality and
small clutch size, a female must produce eight eggs and a
pair must mate twice to obtain one hatched tadpole.
Discussion
In this study `time out' of females was higher than `time
out' of males providing evidence that male PRR is
greater than female PRR (Clutton-Brock and Vincent
1991; Parker and Simmons 1996). Behavioral observations support empirical measures of the PRR: male
219
D. pumilio can mate in succession on di€erent days or
even on the same day with di€erent females and guard
several clutches at the same time (personal observation),
whereas females can only mate every few days and do
not mate during tadpole rearing (n=4 tadpole-rearing
females). This intensive maternal investment clearly
illustrates the increase in an o€spring's chance of
survival at the cost of the parent's ability to invest in
other o€spring (sensu Trivers 1972).
As the adult sex ratio did not seem to deviate from
unity, the unequal PRR of the sexes generates a malebiased OSR, the main determinant of mating competition (Kvarnemo and AhnesjoÈ 1996). In the case reported
here, the sex with the smaller parental investment is the
predominant competitor because the discrepancy in
parental investment strongly determines the inequality
in PRR. Other factors than parental investment that
may a€ect PRR and OSR are temperature, food, and
nest site availability (Bush 1993; Kvarnemo and AhnesjoÈ
1996) but were not analyzed in our study.
It has been argued that variance in mating success
alone is not necessarily evidence for the operation of
sexual selection (Koenig and Albano 1986; Sutherland
1987). Nevertheless, it should give an estimate of the
maximum opportunity for sexual selection and has been
applied for comparisons of mating systems between and
within amphibian species (Ryan 1985; Sullivan et al.
1995). Measures of the opportunity for sexual selection
IS on male reproduction and the coecient of variation
of male mating success in D. pumilio (Table 2) fall within
the range calculated by Kluge (1981) for a number of
species with a prolonged breeding season (IS : range 0.5±
3.0 (outlier 13.6), median=1.7; CV: range 72.9±286.6,
median=134). In anurans, a male-biased OSR is often
associated with a prolonged breeding season and leads
to high values of IS and sometimes high levels of polygyny (Sullivan et al. 1995) and our results are consistent
with these ®ndings.
Furthermore, three criteria for identifying sexual
selection (Koenig and Albano 1986) seem to apply to
D. pumilio. (1) Both intrasexual competition and mate
choice are given. As in many frog species, territoriality
represents a form of intrasexual competition and has
evolved toward defense of calling sites for mate attraction, and areas involved in courtship and mating rather
than defense of feeding areas (Mathis et al. 1995; ProÈhl
1997b). In turn, females seem to sample males before
and between mating and may interrupt courtships. This
behavior suggests female selectivity. (2) There is variance
in some ®tness measurements such as mating and reproductive success. (3) Mate choice acts on speci®c
characters that might provide reproductive advantages
over other individuals of the same sex. Energetically
expensive calls in frogs seem to be such a character, e.g.,
louder calls, longer calls, and higher calling activity are
attractive to females in many amphibians and other
groups (Ryan 1985; Roithmair 1992; review in Halliday
and Tejedo 1995).
The mating system of D. pumilio is best described as
sequential polygamy (Davies 1991) comprising sequential and simultaneous polygyny and sequential polyandry, with male and female parental care. This mating
system is associated with a prolonged breeding season
due to a tropical environment where the constant
availability of water and food allows females to produce
clutches continuously. The same mating system was
found in D. histrionicus (Silverstone 1973) and may be
true for all dendrobatids of the histrionicus group sharing the same parental-care pattern (Myers et al. 1984;
Zimmermann and Zimmermann 1988; review in Sullivan
et al. 1995). In general, dendrobatids show great variability in mating patterns ranging from species with
exclusively male or female parental care, through biparental care, to temporal pair bonding (Weygoldt 1987;
Summers 1992b; Caldwell 1997). In some species with
territorial males and male parental care (D. auratus and
D. leucomelas), both sexes are competitive with respect
to access to mates, although females are more selective
(Summers 1989, 1992a). Those studies showed that apart
from relative parental investment, variation in mate
quality a€ects the direction of mating competition and
that choice and competition, in contrast to the situation
in D. pumilio, need not necessarily be opposite sex roles
(Owen and Thompson 1994). The mating system variability in dendrobatids may re¯ect adaptations to different environments but may also be the result of sexual
con¯ict ending up in deception and reproductive parasitism (Caldwell 1997; Summers and Amos 1997).
This study was conducted during only 6 months. We
observed three males 3 years later still defending their
territory on the study area (H. ProÈhl, unpublished data)
and assume that the observed mating success represented between 20 and 50% of lifetime mating success.
Long-term research would be an essential complement
to this study, because lifetime reproductive success is a
more accurate indicator of ®tness, to estimate di€erences
between individuals and the signi®cance of sexual selection as an evolutionary force (Sullivan et al. 1995).
The theoretical predictions outlined in the introduction concerning di€erences in PRR between the sexes,
competition for mates, selectivity for mates, variance in
male mating success, and the function of territoriality
were con®rmed. A new, unpredicted component of the
mating system is polyandry, which can be attributed to
short intervals between clutch production and female
mate choice.
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 J.D. Alfaro for his
support. For critiques and suggestions on our work we thank T.
Halliday, C. Drews, O. Seehausen, E. Zimmermann, U. Radespiel,
V. Groû, M.E. Roithmair, K. Summers, S. Schmidt, and three
anonymous reviewers. We are indebted to G.C. Carrojal and A.L.
RamõÂ rez for help during the ®eld and computer work. The German
Academic Exchange Service DAAD, M. and J. ProÈhl and ± exclusively during the publication phase ± the Austrian Science
Foundation (P 11565 Bio) provided ®nancial support to H. ProÈhl.
220
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Communicated by L.W. Simmons