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Journal of Natural History
ISSN: 0022-2933 (Print) 1464-5262 (Online) Journal homepage: http://www.tandfonline.com/loi/tnah20
Not every drought is bad: quantifying reproductive
effort in the harlequin frog Atelopus laetissimus
(Anura: Bufonidae)
Andres A. Rocha Usuga, Fernando Vargas-Salinas & Luis Alberto Rueda
Solano
To cite this article: Andres A. Rocha Usuga, Fernando Vargas-Salinas & Luis Alberto
Rueda Solano (2017): Not every drought is bad: quantifying reproductive effort in the
harlequin frog Atelopus laetissimus (Anura: Bufonidae), Journal of Natural History, DOI:
10.1080/00222933.2017.1355075
To link to this article: http://dx.doi.org/10.1080/00222933.2017.1355075
Published online: 15 Aug 2017.
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Not every drought is bad: quantifying reproductive effort in
the harlequin frog Atelopus laetissimus (Anura: Bufonidae)
Andres A. Rocha Usuga
a
, Fernando Vargas-Salinas
b
and Luis Alberto Rueda Solano
a,c
a
Grupo de Investigación en Biodiversidad y Ecología Aplicada (GIBEA), Universidad del Magdalena, Santa
Marta D.T.C.H, Colombia;
b
Grupo de Investigación en Evolución, Ecología y Conservación EECO,
Universidad del Quindío, Armenia, Colombia;
c
Grupo Biomics, Universidad de los Andes, Bogotá, Colombia
ABSTRACT
Atelopus laetissimus is an endemic and threatened harlequin frog
from the high mountain forests of Sierra Nevada de Santa Marta,
Colombia. Knowledge of its reproductive biology is essential for
understanding the intraspecific interactions that can help the
conservation of Atelopus species. We quantified the energy, mea-
sured in body weight, invested by males and females of A. laetis-
simus for reproduction, and how this energetic investment is
related to the survival of individuals and rainfall conditions in
habitats during two years (2014 and 2015). Our results show
plasticity in terms of reproductive phenology linked to rainfall
with short- and long-duration breeding strategies. The first year
of this study, 2014, had a precipitation level in accordance with
the annual averages at the area. During this time frogs exhibit a
short breeding period. Contrary to 2014, 2015 was a year with little
precipitation, below the annual averages, which probably facili-
tated the females’quick spawning in the creeks and a consequent
reduction in the duration of amplexus and low breeding efforts by
males. This, in turn, was related to a long breeding period that
favors the survival and reproduction of males during the entire
year. In 2014 we found a decrease of 25% to 30% body weight of
potentially reproductive males, which may be attributed to a
prolonged duration of amplectant events.
ARTICLE HISTORY
Received 3 August 2016
Accepted 19 June 2017
Online 15 August 2017
KEYWORDS
Reproductive strategy;
phenology; survival; Sierra
Nevada de Santa Marta
Introduction
Reproductive effort is defined as the total specific and biologically significant energy
invested by an individual in breeding during a defined time interval (Stearns 1976).
Reproductive effort depends on the food resources in the habitat, and the activities
that the individual carries out before and during the breeding process (Lemckert &
Shine 1993). The current reproductive effort invested by an individual directly
impacts its survival and breeding probabilities in the future (Stearns 1992;Nilsson
& Svensson 1996;Roff2002). Predictions about reproductive efforthavebeensup-
ported by empirical evidence in plants (Reekie & Bazzaz 1987), invertebrates (e.g.
Ward et al. 2009) and all vertebrate groups (e.g. fishes: Jones & Reynolds 1999;birds:
CONTACT Luis Alberto Rueda Solano biologoluisrueda@gmail.com
JOURNAL OF NATURAL HISTORY, 2017
https://doi.org/10.1080/00222933.2017.1355075
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Visser & Lessells 2001; reptiles: Miles et al. 2000). Amphibians typically have high
reproductive efforts compared to reptiles (Vitt & Caldwell 2013). In anurans, apart
from any form of post-fertilization parental behaviour that enhances offspring survi-
val or growth at some expense to the parent (parental care) (Clutton-Brock 1991),
reproductive effort can manifest in many forms. In females, for instance, reproductive
effort is reflected by the number and size of eggs laid in each oviposition (Lemckert &
Shine 1993) while in males it is reflected by periods of sustained calling (Humphries
1979;Ryser1989). Additionally, total body mass in males could decrease during
reproductive behaviours associated with finding and courting females (Vitt &
Caldwell 2013).
While multiple studies have been conducted regarding the reproductive behaviour of
Neotropical anurans, environmental factors and intraspecific interactions that influence
such species’behaviour are largely unknown (Wells 2007). There are a number of inter-
actions that rule the reproductive behaviour of Neotropical anurans (Hödl 1990; Haddad &
Prado 2005;Lipinskietal.2012), including courtship (Pröhl 1997; Rojas-Morales & Escobar-
Lasso 2011; Vargas-Salinas et al. 2014;Sandovaletal.2015), agonistic interactions between
males for gaining access to females (Savage 2002; Delia et al. 2010;Cardozo-Urdaneta&
Celsa Señaris 2012), the duration of amplexus (Sexton 1958; Wells 1977;Lynch1986;
Gawor et al. 2012) and, in general, the efforts that the individuals put into breeding
with the costs associated in terms of survival (Lemckert & Shine 1993;Nilsson&Svensson
1996;Sanabriaetal.2007; Camargo et al. 2008; Quiroga & Sanabria 2012).
Mating ball of Atelopus laetissimus from San Pedro de la Sierra population, observed in June 2016.
Photo: José Luis Pérez González.
2A. A. ROCHA USUGA ET AL.
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Harlequin frogs (Atelopus: Bufonidae) include 100 species that occur in 11 countries in
the Neotropics. Most species have restricted geographic distributions (Lötters 1996;
Frost 2016). Many of those species are possibly extinct, or in risk of extinction (Rueda-
Almonacid et al. 2004; Young et al. 2004; La Marca et al. 2005; IUCN 2016) due to
chytridiomycosis, climate change or habitat loss (Lips et al. 2003; La Marca et al. 2005;
Pounds et al. 2006; Lötters 2007; Tarvin et al. 2014). The reproductive behaviour in
Atelopus tends to be similar between species and consists of prolonged amplexus
known as ‘female-guarding’(Wells 1977). The majority of species lay eggs under rocks
in small- or medium-sized streams (Karraker et al. 2006; Lötters 2007; Crump 2009;
Crump 2010). Nevertheless, some reproductive behaviour differences occur between
species. For example, the females of Atelopus zeteki (Dunn 1933) are found in the interior
of forests during the rainy season, and come back to the creeks during the dry season to
breed with males that were defending territories in the riparian forest throughout the
year (Poole 2006). Oviposition by female A.zeteki occurs in creeks with low depth and
flow (Karraker et al. 2006). Another example of reproductive strategies exhibited by male
Atelopus varius is to attract females and pair during the rainy season, since the popula-
tion sex ratio is biased towards males (Crump 1988), and initiate amplexus before the
breeding season and wait until the dry season when oviposition succeeds (Pounds &
Crump 1987). In Atelopus senex breeding usually begins at the end of the dry season,
with a large number of amplexed individuals occurring during the height of the rainy
season (Savage 2002). Males of Atelopus flavescens wait along streams all year, while
females remain distant until the breeding season in rainy periods (Lötters et al. 2011).
These differences in reproductive behaviours imply different breeding strategies that
could directly impact the survival of individuals, and hence the conservation of this
highly threatened clade.
Atelopus laetissimus (Ruíz-Carranza et al. 1994) is an endemic Harlequin frog of the Sierra
Nevada de Santa Marta, Northern Colombia, which inhabits well-preserved forests, though it
can be tolerant to modifications in its habitat (Granda-Rodríguez et al. 2008; Rueda-Solano
pers. obs.). The individuals of this species are usually found in closed canopy forests near
small streams (Carvajalino-Fernández et al. 2008; Rueda-Solano pers. obs.), and exhibit
reproductive activity between the months of May and August, right before the beginning
of the rainy season (Carvajalino-Fernández et al. 2008; Granda-Rodríguez et al. 2008). Like
other species in the genus, clutches consist of chains of eggs laid in water, where tadpoles
develop adhering with suctorial oral discs to rocks in the bottom of the streams and move
around while feeding (Lötters 1996). Although there is descriptive data and generalizations
concerning the reproduction of A. laetissimus, its reproductive biology and how it associates
with environmental factors is not known in detail. Additionally, the individual reproductive
effort and relation to survival probabilities has not been quantified.
The objective of this study was to quantify the reproductive effort (measured as weight
loss and nutritional state) in males and females of A. laetissimus and examine if such effort
influences the survival probability of the individuals. Moreover, we describe the phenol-
ogy and reproductive behaviour of this species, in relation to environmental factors. It is
expected that individuals of A.laetissimus present a high-energy investment during the
reproductive season, which will be reflected in weight loss, which could affect their
survival chances. Quantifying these aspects provides important information to determine
the times of the year when the individuals in natural populations of A. laetissimus can be
JOURNAL OF NATURAL HISTORY 3
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more susceptible to mortality and, hence, eventual in situ management plans could be
more effective in terms of maintaining or increasing population sizes.
Methodology
Study area
This research was conducted at the Estación Experimental de San Lorenzo (EESL) (11° 06′
54.96″N, 74° 03′03.46″W) located at approximately 2200 m asl in the Serranía de San
Lorenzo, north-western slope of the Sierra Nevada de Santa Marta (SNSM), department
of Magdalena, northern Colombia (Figure 1a). The SNSM is one of the countries’high
endemism centres and one of the most important protected areas in the world (Lynch
et al. 1997; Le Saout et al. 2013).
Vegetation in this region includes mature and secondary mid-mountain Andean
forest subjected to two rainy seasons (April–June and August–November; Figure 1b)
that alternate with two seasons of low precipitation or drought (December–March and
June–August; Figure 1c). The average annual temperature at EESL is 13°C (ranging from
8–19°C), the average annual precipitation is around 3000 mm and the relative humidity
ranges between 73–98% (Tamaris-Turizo et al. 2007).
Field sampling
In April, June and November of 2014, and from April until November of 2015, 11 two-day
field trips were conducted in San Lorenzo creek (11° 6′56.199″N 74° 3′1.0008″W).
During each field trip sampling for Atelopus was conducted inside a 50 m long and 5 m
wide transect. Since A.laetissimus has its activity peak at night (Rueda-Solano et al. 2016)
transects were sampled from 18:00–00:00 hours.
We recorded the weight and body size (snout–vent length, SVL) of the individuals in
periods prior to reproduction (April 2014 and 2015), during the reproductive peak (June
2014 and May–June 2015) and after reproduction (November 2014 and 2015). Weight
and body size were recorded with a digital scale (PPS200, d= 0.01 g; © PESOLA AG,
Switzerland) and callipers (Bull Tools rm814, d= 0.01 mm; Black Bull Tools, Guatemala).
The monitoring of males and females was done using the capture–mark–recapture
technique for the samplings of 2015. Photo identification (PhotoID) (Maldonado 2010;
Himmel 2013) was used to identify individuals based on the spot patterns displayed on
the ventral surface.
Data analysis
Reproductive effort of Atelopus laetissimus
The reproductive effort in males was quantified using only individuals potentially cap-
able of breeding, by using the minimum size found in amplexed males as a reference.
We conducted a factorial analyses of variance to compare the average weight of males
between the sampled years and between each of the monthly samplings. Student’s
t-tests were applied for paired samples to determine whether there had been significant
changes in weight during and after the breeding period of the recaptured individuals
4A. A. ROCHA USUGA ET AL.
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Figure 1. (a) Map of the Serranía de San Lorenzo, Sierra Nevada de Santa Marta, Colombia. The circle
signals the location of Estación Experimental San Lorenzo at 2200 msnm; (b) San Lorenzo creek,
SNSM, during the rainy season; (c) during the dry season.
JOURNAL OF NATURAL HISTORY 5
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that bred (i.e. registered in amplexus). Additionally, the relative nutritional status of
individuals was examined using the relationship between weight and the cube of SVL;
individuals under the central tendency are underfed (Stevenson & Woods 2006). We
observed few females and therefore the reproductive effort of females was calculated
with all observed adult individuals. The application of inferential statistical tests for
female Atelopus was not possible. All analyses were conducted using IBM SPSS
Statistics Version 22 (IBM Corp 2013) statistical software.
Because reproduction in tropical anurans is mainly related to rainfall (Duellman &
Trueb 1994), this factor was considered as the most important environmental variable to
understand the reproductive phenology of A. laetissimus. We obtained precipitation
levels from the virtual platform of the Institute of Hydrology, Meteorology and
Environmental Studies of Colombia (http://institucional.ideam.gov.co/jsp/index.jsf).
Probabilities of survival of Atelopus laetissimus
We used the Cormack–Jolly–Seber (CJS) method to determine the survival probabilities
(Phi) for males of A. laetissimus in 2015 (White & Burnham 1999). For this analysis four
models were implemented for open populations: (1) survival probability and recapture
probability vary in time: {Phi(t)p(t)}; (2) constant survival probability and recapture
probability varies in time: {Phi(.)p(t)}; (3) survival probability and constant recapture
probability varies in time {Phi(t)p(.)}; and (4) constant survival probability and constant
recapture probability: {Phi(.)p(.)}. We used the Akaike information criterion (AICc) to
select the best model, which would be the model that better adjusts to the capture
and recapture data.
The population models that were used require four main assumptions: (1) the mark-
ings on individuals are not lost; (2) all captured animals are released immediately; (3) all
marked and non-marked individuals have the same capture probability; and (4) there is
homogeneity of survival (Amstrup et al. 2005). The first two assumptions were fulfilled
during the samplings. To determine if the latter two assumptions were fulfilled we
conducted a goodness-of-fit test (test 2 and test 3, respectively) using MARK software
version 6.2 (Choquet et al. 2002). Test 2 suggests that the marked and non-marked
individuals (males) presented the same capture probability (χ
2
= 6.6457; GL =5;
P= 0.2484); test 3 showed that the homogeneity of survival assumption was fulfilled
(χ
2
= 28.553; GL =6;P= 0.0001).
Results
We captured 218 individuals of A.laetissimus (29 females, 189 males), among which
there were 23 pairs in amplexus. In 2014, seven females, 57 males, and three in
amplexus were documented. In 2015, 22 females, 132 males and 20 pair in amplexus
were registered.
Precipitation varied between 2014 and 2015; 2014 was considered a normal rainy
year with 2465 mm rainfall (in accordance to the annual averages), while 2015 was a
mostly dry year with average rainfall below the annual averages (185 mm) (Figure 2a).
Reproductive phenology of A. laetissimus was related to the annual differences in
precipitation. In 2014, there was a short reproductive period. In 2015 the reproductive
6A. A. ROCHA USUGA ET AL.
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Figure 2. Reproductive phenology/strategy of Atelopus laetissimus in San Lorenzo creek. (a)
Precipitation; (b) number of amplexus; (c) males’weight). *Highly significant differences.
JOURNAL OF NATURAL HISTORY 7
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period was prolonged and individuals bred throughout almost the entire year, having a
peak in the number of amplexus in June (Figure 2b).
The average weight of potentially reproductive males was 4.28 g (SD ± 0.57; n= 189)
with an average SVL of 39.87 mm (SD ± 1.46; n= 189). This weight was lower in 2014 than
in 2015 (n= 189; F= 13.024; GL =10;P< 0.05). Males in June 2014 weighed approximately
30% less than in June 2015 (
X= 2.99 g; SD ± 0.67; n=12and
X= 4.31 g; SD ± 0.47; n=91,
respectively) and for this same month in 2014 weight loss was between 25%–30% in
relation to the average body weights of the other months sampled (n=189;F=13.024;
GL =10;P<0.01;Figure 2c). In contrast, the weights of males registered in October 2015
(
X= 4.63 g; SD = 0.48; n= 52) showed a weight increase between 6%–13% in comparison
to the averages of 2014 and 2015. We found no differences (n=5;T= 0.78; P= 0.117)
comparing the weight of the males registered during (
X=4.08g)andafter(
X=4.21g)
amplectant events. As expected, the nutritional state was variable among individuals.
However, for the rainy year (2014) there was a group of individuals particularly underfed
(i.e. undernourished) (Figure 3a). An image of an undernourished male in June 2014 and a
well-fed male in June 2015 is depicted in Figure 3b, c), respectively. With 132 captures and
403 recaptures of male in 2015 (Table 1), the survival probability of the potentially
reproductive male individuals was high and constant (Phi = 0.8281657;
IC95% = 0.7632776–0.8781077) in 2015 (population model = Phi(.)p(t); Table 2).
Females exhibited an average weight of 13.72 g (SD ± 2.55; n= 36) and a SVL average
of 57.43 mm (SD ± 2.80; n= 36). We obtained the weight of a female just before
(14.88 g) and after (9.68 g) spawning (35% in body weight loss). Individual effort was
estimated as the number of eggs that a female produces (̴386) assuming that the
average individual egg weight is 0.0131 g (± SD 0.0032; n=10).
In general, the breeding behaviour of A. laetissimus occurred in dry periods, where the
highest number of females are often sighted in the vegetation adjacent to the creek
(Figure 4a). The males actively chase the females inside their home ranges without forming
territories, and often sporadically form mating balls around a female (Figure 4b, c).
Generally, the winner is the one who firmly maintains axillary amplexus position for a longer
length of time, female-guarding until the female decides to leave (Figure 4d). During the
mating balls, low-intensity vocalizations were emitted by males and females. However, in
this study no advertisement calls from males in their home range were observed. Once the
male obtains a female, it remains amplexed to the female without feeding (Figure 4d, e).
During this period, the female can feed and move freely from the ground to the canopy.
These amplexus can last a long time, based on captures and recaptures. It was measured
that an amplexus can last for at least 22 days, although we do not reject that A.laetissimus
has a prolonged amplexus duration of several months in rainy years. Once the female
decides to spawn, it returns to the creek from the canopy or the forest floor and lays a large
number of eggs in cryptic places inside the water, for example, under rocks where small
flows are formed (Figure 4f). The eggs are laid in chains and usually form masses due to the
water stream that drags some broods to lentic areas in the creek.
Discussion
The behaviour and reproductive effort of A.laetissimus varied in duration and energy
invested by males in reproduction and appears related to precipitation levels.
8A. A. ROCHA USUGA ET AL.
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Figure 3. (a) Body condition in males of Atelopus laetissimus in a rainy year (2014) and a dry year
(2015); the circle highlight undernourished males at June 2014. (b) Image of an undernourished
male at June 2014 and (c) well-fed male at June 2015. (d) The same male with different body
condition recorded reproductive season at June 2015, (e) May 2016 (rainy year). This figure was
made with capture and recapture data.
JOURNAL OF NATURAL HISTORY 9
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Specifically, in months of low rainfall, breeding occurs with less effort and the survival of
individuals (at least males) is high (Figure 2). This pattern in the reproductive phenology
of A. laetissimus has been reported for other species of the genus (Savage 1972; Lötters
1996), and might be more associated with Atelopus of high mountains (Gawor et al.
2012). Likewise, in species such as A. zeteki and A. varius, inter-population variation was
observed in the duration of reproductive seasons that are explosive/short or long
(McCaffery et al. 2015), in other words, each population has its own dynamics of
reproductive phenology. In contrast to what was reported in these species, the variation
in A. laetissimus was observed at the intra-population level. Variations in reproductive
phenology are commonly observed in anurans that inhabit temperate zones. Exposure
to large local climatic variations of environmental temperature and rainfall cause those
anurans to breed discontinuously (Crump 1974; Tsiora & Kyriakopoulou-Sklavounou
2001; Martori et al. 2005; Wells 2007). In some cases those species have genetic varia-
tions that are produced in response to environmental conditions and often alter their
reproductive strategies (Martori et al. 2005), but this has not been documented in A.
laetissimus.
In 2014, the population had a short reproductive period (Figure 2), ending before the
beginning of heavy rains and the corresponding increase in streams’water flow. These
conditions make spawning difficult and raise the risk of egg entrainment (Karraker et al.
2006), delaying oviposition and lengthening the duration of amplexus (female-guarding
by males). Careful selection of oviposition sites by female Atelopus has been suggested
in A. zeteki (Karraker et al. 2006) and A. flavescens (Gawor et al. 2012). Although there is
no certainty that the period of famine reflected in male body weights in June 2014 is
attributed to reproduction, prolonged amplexus suggests a large reproductive effort
that could produce the low weight in males after breeding (Figure 3a). We find support
for the above hypotheses in the observation of a male with an average nutritional state
Table 1. Summary of capture effort at the eight sampling events during 2015 for male individuals of
Atelopus laetissimus in San Lorenzo creek, Serranía de San Lorenzo, Sierra Nevada de Santa Marta.
Sampling events Total
April May June July August September October November
Events 2015 1 2 3 4 5 6 7 8 8
Individuals registered 31 32 57 17 26 32 51 17 263
Newly captured 31 21 30 4 7 17 14 8 132
Recaptured 0 11 27 13 19 15 37 9 403
Total captured 31 52 82 86 93 110 124 132
Table 2. MARK models used to estimate survival probabilities and recapture rates for individual
males of Atelopus laetissimus in San Lorenzo creek, Serranía de San Lorenzo, SNSM.
Model AICc Delta AICc Weight AICc Model likelihood No. parameters Deviance
Phi(.)p(t)* 543.3736 0.0000 0.88590 1.0000 8 167.6677
Phi(t)p(t) 547.5004 4.1269 0.11252 0.1270 13 160.8290
Phi(t)p(.) 556.0330 12.6595 0.00158 0.0018 8 180.3272
Phi(.)p(.) 580.5505 37.1770 0.00000 0.0000 2 217.4052
Phi(t), estimated survival probability varied in time; Phi(.), estimated survival probability constant in time; p(t), estimated
capture probabilities varied in time; p(.), estimated capture probabilities constant in time. *Selected model.
10 A. A. ROCHA USUGA ET AL.
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in 2015, a dry year (Figure 3d), but undernourished in 2016, a rainy year, when observed
in amplexus (Figure 3e). In other Bufonidae (e.g. Anaxyrus terrestres, Rhinella arenarum)
similar results have been reported: males of such species exhibit weight loss from 17%–
18% and 36%, respectively (Brattstrom 1979; Quiroga & Sanabria 2012). This high energy
investment in breeding can increase the mortality of parental individuals due to the high
physiological effort, and may also increase their chances of being preyed upon (Ryan
et al. 1983; Guayara-Barragán & Bernal 2012).
The reproductive period of A. laetissimus for 2014 was much shorter than that of
2015, which can be attributed to the low rainfall of the latter year. The low precipitation
Figure 4. Atelopus laetissimus individuals. (a) Female; (b) male; (c) mating ball consisting of several
males and one female; (d) prolonged axillary amplexus position/female guarding; (e) amplexus
perched in the riparian vegetation; (f) amplexus submerged in the stream possibly searching for
spawning sites. Photographs: L.A. Rueda Solano (a, b, d, e, f) and A.A. Rocha Usuga (c).
JOURNAL OF NATURAL HISTORY 11
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of 2015 kept stream and flow rate levels low, thus probably increasing the availability of
spawning sites for females. This is a characteristic of the reproduction strategies of the
Atelopus species (Savage 1972; Lötters 1996), in which females spawn during the dry
season when streams have a low flow rate (Savage 1972; Crump 1988,2009; Savage
2002; Karraker et al. 2006). Although field sampling was different between 2014 and
2015, the main comparisons took place in periods prior, during and after the reproduc-
tion of A. laetissimus (April, June and November of both years). Otherwise, in 2015,
amplectant events lasting more than 22 days were observed; long amplexus duration is
a generalized pattern in species of the genus Atelopus (Wells 1977; Lynch 1986). In the
genus, Atelopus carbonerensis presents the longest amplexus duration of 125 days (A.
oxyrhynchus in Dole & Durant 1974), followed by A. lozanoi, (60 days, estimation based
on a pair that was already amplexed in the field and then kept in captivity; C. Navas pers.
comm), A. flavescens (35 days, Gawor et al. 2012) and A. cruciger (19 days, Sexton 1958).
These long amplectant events will directly impact the male reproductive effort.
The estimated reproductive effort of an A. laetissimus female, measured as the
number of eggs laid, is similar to that reported in A. zeteki (202–623 eggs; Karraker
et al. 2006); A. flavescens (250 eggs; Boistel et al. 2005); A. chiriquiensis (364 eggs;
Lindquist & Swihart 1997), but different from that reported in other species such as A.
varius (910 eggs; McDiarmid 1971)orA. muisca (up to 69 eggs; Rueda-Almonacid &
Hoyos 1991). Altogether, this indicates high interspecies variation in relation to the
number of eggs per oviposition and, therefore, female reproductive effort.
ThesurvivalofmaleindividualsofA. laetissimus was high during the extended
reproductive period in the dry year (2015), possibly favoured by relatively small
body weight loss in reproduction (Figure 2). In populations of A. varius in Panama
(McCaffery et al. 2015)andA. cruciger in Venezuela (Lampo et al. 2012), a high
probability of survival and recapture has also been reported. However, a population
of A. zeteki in Panama had a high survival rate, but varied in time and with the
probability of constant recaptures (McCaffery et al. 2015). According to McCaffery
et al. (2015) survival probabilities can vary due to changes in environmental con-
ditions, which can generate some sort of behavioural change. Taking this into
account, the reproductive behaviour and effort in individuals of A. laetissimus
probably varies between rainy years and those of extreme droughts, which would
also affect its survival.
In summary, the population of A.laetissimus in San Lorenzo creek, SNSM, could
exhibit plasticity in terms of strategy and reproductive effort, tied to local rainfall and
flow rate of the stream where the individuals spawn. This leads to variations in its
reproductive phenology with short and long breeding periods. The predominantly dry
year promoted breeding in this population and was related to a high survival of males.
In terms of energetic expenditures invested in reproduction, both males and females
may have similar reproductive effort in rainy years. However, dry periods favour a lower
energy investment in males, probably because females advance their decision of when
to lay eggs, reducing the time in female guarding by males. The comparison with other
A. laetissimus populations or other Atelopus species is necessary to establish if the
reproductive patterns vary depending on the physical factors of each locality or if they
are specific for each species. In the future, we recommend sampling additional sites
12 A. A. ROCHA USUGA ET AL.
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across multiple years to build a more robust dataset and further our understanding of
Atelopus reproductive behaviour.
Acknowledgements
This research was a result of project Atelopus: Monitoring Harlequin Frogs in Sierra Nevada,
Colombia, funded by the Conservation Leadership Programme (CLP) and Magdalena University
(Project ID: 02177014). Thanks to Corporación Autónoma Regional del Magdalena for manip-
ulation permits (resolution number 0425). Thanks to Parques Nacionales Naturales de
Colombia (Caribe territorial) and Parque Sierra Nevada de Santa Marta for all logistic support
during our field trips. Thanks to Alice Reifeld, Nicolette Roach, Johannes Reiter, Stefan Lötters
and Jeffrey W. Streicher for their help in manuscript review. Our gratitude extends to the
students of the Herpetology Group (froglets) of Magdalena University: J.L. Pérez, L. Mejía, J.
Eguis and L. Jiménez, who gave us their valuable assistance in the fieldwork. This study was A.
Rocha Usuga’s undergraduate thesis directed by LARS (Beto Rueda).
Disclosure statement
No potential conflict of interest was reported by the authors.
Funding
This work was supported by the Conservation Leadership Programme (Project ID: 02177014).
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