Journal of Natural History

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Oviposition site preference and reproductive

ecology of Teratohyla midas (Anura: Centrolenidae)
in the Colombian Amazon

Juan C. Díaz-Ricaurte, Estefany Carolíne Guevara-Molina & Filipe Serrano

To cite this article: Juan C. Díaz-Ricaurte, Estefany Carolíne Guevara-Molina & Filipe Serrano
(2019) Oviposition site preference and reproductive ecology of Teratohyla�midas (Anura:
Centrolenidae) in the Colombian Amazon, Journal of Natural History, 53:29-30, 1811-1822, DOI:
10.1080/00222933.2019.1668490

To link to this article: https://doi.org/10.1080/00222933.2019.1668490

Published online: 01 Oct 2019.

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 JOURNAL OF NATURAL HISTORY
2019, VOL. 53, NOS. 29–30, 1811–1822
https://doi.org/10.1080/00222933.2019.1668490

Oviposition site preference and reproductive ecology of

Teratohyla midas (Anura: Centrolenidae) in the Colombian
Amazon
a,b c,d
Juan C. Díaz-Ricaurte , Estefany Carolíne Guevara-Molina
and Filipe Serrano a
a
Laboratório de Ecologia, Evolução e Conservação de Anfíbios e Répteis, Departamento de Ecologia,
Instituto de Biociências, Universidade de São Paulo, São Paulo, Brasil; bGrupo de Investigación en
Biodiversidad y Desarrollo Amazónico (BYDA), Programa de Biología, Facultad de Ciencias Básicas,
Universidad de la Amazonía, Florencia, Colombia; cLaboratório de Comportamento e Fisiologia Evolutiva,
Departamento de Fisiologia, Instituto de Biociências Universidade de São Paulo, São Paulo, Brasil; dGrupo
de Evolución, Ecología y Comportamiento (EECO), Programa de Biología, Universidad del Quindío,
Armenia, Colombia

ABSTRACT ARTICLE HISTORY

The family Centrolenidae (Glass frogs) includes 157 species of Received 28 May 2018
anurans with a Neotropical distribution. Although glass frogs Accepted 11 September 2019
have been the subject of several studies encompassing various KEYWORDS
aspects of their biology, natural history data on their reproductive Behaviour; glass frogs;
ecology is still scarce. One of the important aspects of reproduc- natural history;
tive ecology is the oviposition site since it can impact the repro- reproduction; substrate
ductive success of a species. Herein, we provide detailed preference
information on the reproductive ecology of a population of
Teratohyla midas from the Colombian Amazon foothills and test
whether this species shows a preference on substrate and height
of oviposition site. We monitored a population using capture-mark
-recapture of individuals identified by a photograph of their
unique pattern of dorsal yellow spots. Wild-ID Software was used
to corroborate if the dorsal pattern was different between indivi-
duals. Additionally, we monitored the presence of egg clutches,
amplexus and oviposition behaviour. We observed 110 males and
5 females of T. midas, seen at an average height of 3.1 m ± 2.9
(0–17.8 m) from the ground. Likewise, we recorded the amplexus
behaviour of two pairs for approximately 150 min. Once the
oviposition happened, the male retreated, and the female covered
the egg clutches for approximately 60 min. We observed 25 egg
clutches with 60% being deposited in leaves of Selaginella sp and
found at an average height of 2.9 ± 1.7 m (1.1–7.0 m). Thus, the
selection of oviposition site was not random but mostly specific to
one type of substrate. Furthermore, there was an overlap of the re-
sampled median height distributions of active individuals and
clutches, which suggests that oviposition does not occur at
a preferred height within the vertical distribution of individuals.
The information presented here is the first detailed record of
reproductive ecology for this species and we hope to provide
a basis to improve our knowledge on the biology of this species
and other glass frogs.

CONTACT Juan C. Díaz-Ricaurte juan.diaz@usp.br

© 2019 Informa UK Limited, trading as Taylor & Francis Group

Published online 01 Oct 2019

1812 J. C. DÍAZ-RICAURTE ET AL.

Introduction
The family Centrolenidae (Glass frogs) includes 157 species of anurans with a Neotropical
distribution (Frost 2019). They breed and deposit their eggs on the riparian vegetation along
streams (Toft and Duellman 1979). After a few days of embryonic development, tadpoles
hatch, fall into the water below, and complete their development (Cisneros-Heredia and
McDiarmid 2007; Guayasamin et al. 2009).
This group has been the focus of studies on reproductive biology (Greer and Wells 1980;
Vockenhuber et al. 2008; Delia et al. 2010; Hampton and Otto 2014; Vargas-Salinas et al. 2014),
phylogenetic relationships (Guayasamin et al. 2008, 2009; Castroviejo-Fischer et al. 2014),
territorial behaviour (Dautel et al. 2011; Rojas-Runjaic and Cabello 2011; Hütter et al. 2013),
parental care (Vockenhuber et al. 2009; Vargas-Salinas et al. 2014; Delia et al. 2017), and egg
attendance (Delia et al. 2013, 2017; Bravo-Valencia and Delia 2015).
Oviposition site is an important aspect of a species’ reproductive ecology since it can
influence the success of its offspring (Rudolf and Rödel 2005). In Centrolenidae, co-occurring
species vary on their oviposition height (Vockenhuber et al. 2008; Valencia-Aguilar et al.
2012) and one important factor might be the falling distance of tadpoles when hatching
(Valencia-Aguilar et al. 2012; Cabanzo-Olarte et al. 2013). Similarly, several studies have
shown preference on oviposition site but few have quantified this preference (Cardozo-
Urdaneta and Señaris 2012; Cabanzo-Olarte et al. 2013; Basto-Riascos et al. 2017). Despite
a broad availability of general information, there is a lack of detailed reproductive studies on
most species (e.g. reproductive behaviour, activity patterns). Documenting these aspects is
fundamental for studying species ecology and generating testable hypotheses regarding
their evolutionary biology (Delia et al. 2017). Likewise, this information will promote the
knowledge of species biology and inform management and conservation plans.
In Colombia, Teratohyla midas (Lynch and Duellman 1973) is distributed on the eastern
slope of Cordillera Oriental and in the Amazon basin in Amazonas and Caquetá depart-
ments, between 70 and 950 m above sea level (a.s.l.) (Lynch 2005; Osorno-Muñoz et al. 2011;
Malambo et al. 2013; Acosta-Galvis and Cuentas 2017). In Ecuador, Peru, Brazil and French
Guiana, the species is distributed in lowlands between 190 and 1050 m a.s.l. (Lynch and
Duellman 1973; Guayasamin et al. 2013). Individuals of this species are relatively small, with
body sizes ranging from 17.4 to 19.2 mm snout-vent-length (SVL) in males and from 20.6 to
25.6 mm SVL in females (Lynch and Duellman 1973). This species is usually found in
vegetation along streams (Lynch and Duellman 1973; Toft and Duellman 1979). Although
some details of its natural history (e.g. reproductive behaviour) have been recently docu-
mented (Díaz-Ricaurte et al. 2016), only a single event of amplexus has been reported.
Therefore, we aimed to evaluate if there is a preference for oviposition site in T. midas, as
well as to document additional information on several aspects of its reproductive ecology
(e.g. attendance of eggs by the female, clutch characteristics).

Materials and methods

The study area is located in the Reserva Natural y Comunitaria El Manantial, in the
district of El Caraño, to the north-east of the urban area of the municipality of Florencia,
department of Caquetá, at an altitude of 392 m a.s.l. (1°38ʹ N, 75°34ʹ W, WGS84; Figure 1).
The floristic composition of the study area corresponds to the tropical humid forest with
 JOURNAL OF NATURAL HISTORY 1813

Figure 1. (a) Study site in the department of Caquetá, Foothill Amazonian of Colombia. (b) Micro-watershed
study area of La Perdíz stream tributary of the Hacha River in the Reserva Natural y Comunitaria el Manantial,
municipality of Florencia, department of Caquetá, Colombia.

an average annual rainfall of 3793 mm3, average annual temperature of 25°C and
relative humidity of 85% (Pérez-Rico et al. 2011). The predominant vegetation in the
area includes the species Trichomanes elegans Rich 1972, Lycophyta sp Margulis and
Schwartz 1988, Selaginella cf. rosea Alston 1932, Vismia baccifera Triana and Planch 1862,
Adiantum tetraphyllum Humb and Bonpl 1810, Borreria latifolia Schumann 1888,
Graffenrieda gracilis Williams 1963 (Pérez-Rico et al. 2011).
Data collection was carried on eight field trips from February to April 2016, by free
and unrestricted search methodology (Heyer et al. 1994; Angulo et al. 2006), along
a linear transect of 500 m along the stream, between 19:00 and 02:00 h. Another species
of glass frog, genus Hyalinobatrachium Ruiz-Carranza and Lynch 1991a, is also found in
the area. However, Teratohyla midas is clearly distinguishable from all species of
Hyalinobatrachium by its lobed and transparent liver (Lynch and Duellman 1973)
whereas the liver of Hyalinobatrachium spp. is bulbous and covered by a white perito-
neum (Ruiz-Carranza and Lynch 1991b). When individuals of T. midas were located in the
vegetation they were hand-captured without gloves, and a photographed. As the dorsal
colour pattern is unique for each individual (Figure 2) (e.g. Basto-Riascos et al. 2017;
Ospina-L et al. 2017), this method represents a non-invasive marking technique, allowing
us to monitor the population in later sampling (Caorsi et al. 2012; Basto-Riascos et al.
2017). We measured body size (snout-to-vent length, SVL) with a digital calliper (accu-
rate to 0.01 mm) and sexed each individual using secondary sexual characteristics such
as the presence of a nuptial pad on the finger I and the presence of vocal sac, both only
present in males, or the presence of green eggs in the abdominal cavity for females
1814 J. C. DÍAZ-RICAURTE ET AL.

Figure 2. Dorsal colour patterns (yellow dots) between among individuals of Teratohyla midas. (a)
Individual 94 (Female; SVL: 19.94 mm); (b) Individual 95 (Female; SVL: 21.41 mm); (c) Individual 104
(Male; SVL: 21.51 mm); (d) Individual 97 (Male; SVL: 20.23 mm). Photographs: Juan C. Diaz-Ricaurte.

(Kubicki 2007). Additionally, we recorded the height above ground and the size of the
leaf (width and length) of the vegetation at which the individual was observed, taken
with a conventional measuring tape.
When amplexus was detected, we monitored until after the oviposition; then, we
captured both the male and the female and recorded their body sizes. In addition, clutch
dimension (width and length) was recorded, as well as clutch size (number of eggs), the
height of oviposition site and size of the leaf where oviposition took place. To test if
Teratohyla midas showed a preference for oviposition substrate, we used the methodology
proposed by Basto-Riascos et al. (2017). Photographs of the perches (substrates) were taken
from a distance of 3 m every 50 m along 500 m of linear transect parallel to the creek. Each
photograph was superimposed on a grid of 0.04 cm2 designed in the Microsoft Power Point
Vr. 14.0 (Microsoft Corporation 2013). The above allowed for the counting of the number of
 JOURNAL OF NATURAL HISTORY 1815

points (intersections) of the grid that were passed by a type of substrate observed in the
photograph. The delimited categories of substrates were: Selaginella sp. fern, Heliconia sp
Linnaeus, 1771, and other types of vegetation (leaves). Once this value was obtained, it was
compared with the observed proportion of substrates used by T. midas for oviposition.

Analysis of data
We use descriptive statistics for the data on body size, height and size of the substrate
where they were active, height and size of the oviposition site and dimension of the egg
clutches. For these parameters, we calculated the average, standard deviation, the
minimum value and the maximum value (range). To corroborate that the dorsal colour
pattern of points observed between individuals was not repeated, we used a computer-
assisted matching (CAM) using the software Wild-ID (Wildlife pattern recognition soft-
ware, Vr 1.0, Hannover, NH, USA; Bolger et al. 2011). This software allows to analyse
catch-mark patterns-recapture and is based on an algorithm of Scale Invariant Feature
Transform (SIFT; Lowe 2004), which extracts and combines the distinctive features in the
image, regardless of size and orientation. In order to do so, Wild ID processes the images
by comparing their geometric arrangement, generating a goodness-of-fit score for each
processed image (Bolger et al. 2011). In addition, with the proportion of substrates
available in the study area and the types of substrates where egg clutches were
observed, we applied a X2 test in the Software SPSS Vr. 22.0 (IBM). This test allowed us
to check if there was any preference of females to oviposit on some types of plants in
relation to the substrates available in the study area. To test for a preference of the
height of the oviposition site we compared its vertical distribution with the distribution
of heights at which individuals had been found in our study area, using the latter as
a null model. We randomised the median heights 5000 times for both distributions with
a bootstrap algorithm in R software (R Core Team 2015) and then compared the 95%
confidence intervals of the re-sampled median distributions.

Results
We observed 110 males with an average body size of 20.1 ± 1.5 mm (17.4–22.5 mm) and
five females with an average body size of 22.3 ± 1.5 mm (19.9–24.4 mm). All individuals
were found active (e.g. calling, movements, short journeys) on leaves at an average height
of 3.1 ± 2.9 m (0.3–17.8 m, n= 115). These plants presented an average size of 10.2 ±
5.9 cm in width (2.0–35.1 cm, n= 115) and 24.6 ± 20.7 cm in length (4.2–160.0 cm, n= 115).
The total dataset in the software included 119 images corresponding to 115 indivi-
duals, and 4 recaptures (the recapture images were used in order to ensure the accuracy
of software). The Choice-rank in CAM was high, with 100% of the correct matches ranked
and all the first choices, respectively. Two amplexus events were observed during the
study. This behaviour began with the axillary and nuchal position for approximately 150
min (Figure 3(a)). During this time, the females moved with the males on their backs
over several leaves or branches looking for potential places for oviposition. Once
oviposition started, the males made circular movements with their hind legs until the
females deposited all their oocytes. Then, the males left and the females lifted their belly
1816 J. C. DÍAZ-RICAURTE ET AL.

Figure 3. Axillary amplexus of Teratohyla midas. (a) At the end of the amplexus, the male retires, and
the female covers the clutch for 60 min (b). Images A and B (Male individual N° 50, SVL: 20.58 mm
and female individual N° 51, SVL: 21.70 mm) Photographs: Juan C. Diaz-Ricaurte.

twice, moving backwards, so that they covered the eggs, remaining in that position for
approximately 60 min (Figure 3(b)).
A total of 25 egg clutches were recorded at an average height of 2.9 m ± 1.7 (1.1–7.0 m).
All clutch substrates were leaves with an average size of 8.0 cm wide ± 12.1 (2.5–60.0 cm,
n= 21) and 20.0 cm long ± 25.8 (2.9–103.0 cm, n= 21). The size of the substrate of the four
remaining egg clutches could not be measured due to being laid above 3 m. The clutches
contained on average 21.6 eggs ± 6.0 (12–38 eggs, n= 21), and they averaged in size at
18.8 mm wide ± 19.0 (5.5–31.4 mm, n= 22) and 23.6 mm long ± 23.1 (8.2–46.9 mm, n= 22).
Fifteen of the 25 clutches were observed on leaves of Selaginella sp. (Figure 4), and
a smaller number on other substrates (e.g. fern leaves, leaves of Heliconia sp. and other
types of leaves) (X2: 87.7, df = 1, p < 0.001; Figure 5). In addition, we observed one egg mass
containing only one embryo. This may be attributed to predation on the remaining
embryos or early hatching. Therefore, this datum was not included in the averages of the
numbers of eggs recorded in each egg clutches. We found an overlap of the 95%
confidence intervals for both re-sampled median distributions, which demonstrated that
the clutch heights were not different from the population’s height distribution (individual
occurrence). However, the distribution of the re-sampled median heights of clutches was
larger than the distribution of the re-sampled median heights of the population.

Discussion
In our study, we observed males and females of Teratohyla midas performing stereotypical
centrolenid behaviours during the two events of amplexus and oviposition (see Díaz-Ricaurte
et al. 2016). After laying eggs, both females covered the egg clutch and stayed in that position
for approximately 60 min. As observed in many centrolenid species (Bravo-Valencia and Delia
2015), we hypothesise that the behaviour exhibited by females of T. midas is a type of maternal
assistance to the eggs (Delia et al. 2017), although it is unclear whether it enhances fertilisation
 JOURNAL OF NATURAL HISTORY 1817

Figure 4. Clutches of Teratohyla midas deposited on leaves; (a-d) leaves of the fern Selaginella sp. with
T. midas clutches; (e-f) substrates categorised as other types of leaves. Photographs: Juan C. Diaz-Ricaurte.

or increases egg hydration. A similar behaviour has been observed in other centrolenid
species, such as Espadarana prosoblepon (Jacobson 1985), Ikakogi tayrona Ruiz-Carranza and
Lynch 1991a (Marco Rada, personal communication quoted by Cisneros-Heredia and
McDiarmid 2007; Bravo-Valencia and Delia 2015) Nymphargus grandisonae Cochran and
Goin, 1970 (Guevara-Molina and Vargas-Salinas 2014), Teratohyla pulverata Peters, 1873 and
Cochranella granulosa Taylor, 1949 (Delia et al. 2017). However, only in I. tayrona, T. pulverata
and C. granulosa has it been experimentally demonstrated that maternal assistance influences
the survival of eggs by protecting them from desiccation and predators (Bravo-Valencia and
Delia 2015; Delia et al. 2017).
1818 J. C. DÍAZ-RICAURTE ET AL.

Figure 5. Preference as oviposition site of Teratohyla midas towards leaves of Selaginella sp. The
observed legend corresponds to the clutches recorded throughout the study area. The legend of
expected corresponds to the number of clutches that would be expected to find in relation to the
availability of the substrate in the entire study area. The category ‘others’ refers to other types of
leaves present in the area.

This study is the first to report oviposition site preference and reproductive ecology of
the genus Teratohyla. Our results confirm that Teratohyla midas displays a preference to
lay eggs on a specific plant genus, Selaginella sp. (Selaginellaceae), as has been reported
for other species of centrolenid, such as Espadarana andina on Hedychium coronarium
(Zingiberaceae) (Cabanzo-Olarte et al. 2013), Espadarana prosoblepon on Selaginella
geniculata (Selaginellaceae) (Basto-Riascos et al. 2017), and Hyalinobatrachium valerioi
and H. aureoguttatum both on Heliconia sp. (Heliconiaceae) (Vockenhuber et al. 2008;
Valencia-Aguilar et al. 2012). It is still unclear why T. midas prefers Selaginella sp. leaves as
their preferential oviposition site but we hypothesise that two factors might contribute to
this preference. First, studies have shown the antibacterial and antifungal properties of
Selaginella sp. (Lee et al. 2009; Irudayaraj et al. 2010) which may protect eggs from
pathogens such as the fungus Saprolegnia sp. (Guayara-Barragan et al. 2010). Second,
the rough leaf surface of Selaginella might offer beneficial adhesive qualities that prevent
rain or wind dislodgement. In our study of T. midas, height of oviposition site and height
of detected individuals did not significantly differ, despite no clutches being found above
7 m and individuals reaching up to almost 18 m. However, our observations suggest that
the height distribution of individuals is more restricted than the height distribution of
clutches. This might indicate that some reproducing individuals move further up or down
the vegetation to lay eggs outside of the regular height distribution. It is thus possible that
 JOURNAL OF NATURAL HISTORY 1819

this pattern reflects some density-dependent response or that it reflects a larger range of
height distribution for Selaginella sp. its preferred substrate.
We hope our observations provide important baseline data for further studies on the
reproductive ecology of centrolenid frogs and encourage fellow scientists to report data
on the natural history of poorly known taxa.

Acknowledgements
We thank Valentina Z. Caorsi and Taran Grant for their contributions in improving the manuscript.
We also thank Maria Camila Basto and Fernando Vargas Salinas for their contributions to the
methodology of this study. Thanks to Ana Maria Velasco for her valuable contributions to the
translation of the text. We thank Rolland D. Diaz Morales, Diego Ossa and Ricardo Rodriguez
Cardozo for their collaboration in field trips. Finally, yet important, we thank Marco A. Rada for his
comments that allowed us to improve the context of the manuscript.

Disclosure statement
No potential conflict of interest was reported by the authors.

ORCID
Juan C. Díaz-Ricaurte http://orcid.org/0000-0002-4659-0865
Estefany Carolíne Guevara-Molina http://orcid.org/0000-0003-4245-9058
Filipe Serrano http://orcid.org/0000-0002-8568-678X

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