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Home , Centrolene, Centrolene savagei, Glass frog, Hyalinobatrachium

Herpetology Notes, volume 11: 293-299 (2018) (published online on 17 April 2018)

Parental attendance and site selection of savagei (Ruiz-Carranza and Lynch 1991) in the western and central of

María Lucia Prado-Sañudo1, Alan Giraldo1.* and Wilmar Bolívar-García1

Abstract. (Centrolenidae) is part of the group of glassfrogs and is an endemic to Colombia. It is characterized by a small size, a green dorsum with dark green and white dots, lack of humeral spine and rounded snout. The males of this particular species perform parental care of the clutches by sitting on them. In to describe parental attendance strategies exhibited by males of this species, we monitored eight localities in the Western and Central Andes of Colombia, where the species has been reported. For each individual and clutch identified we recorded height, distance to the edge, nearest edge, and leaf area. We also recorded number of eggs, canopy cover, and presence or absence of parental care of each clutch. We established that male attendance is less common during daylight hours, and it is not related with climatic or local environment conditions, but may be associated with other factors such as the presence of potential predators. Centrolene savagei presents a significant preference for laying its clutches on sites with heights between 0.1–2.0 m above water level; however, the number of eggs is not related with factors such as height, leaf area, distance to the edge or nearest edge.

Keywords: , Centrolenidae, oviposition site, male attendance

Introduction Castro-Herrera and Vargas-Salinas, 2008; Guayasamin et al., 2008; 2009; Luna-Mora, 2011; Rojas-Morales et Centrolene savagei (Ruiz-Carranza and Lynch, al., 2011; Escobar-Lasso and Rojas-Morales 2012; Diaz- 1991) is an endemic glassfrog of Colombia that is Gutiérrez et al., 2013). This species lays egg clutches characterized by a small body size, green dorsum with in the upper side of the leaves and the males exhibit dark green and white dots, rounded snout when viewed parental attendance placing themselves near to or over dorsally, and lack of humeral spine (Fig. 1). Since the clutch (Vargas-Salinas et al., 2007; Quintero-Angel 2004, Centrolene savagei has been listed by IUCN as a vulnerable species (Castro-Herrera and Bolivar-García, 2010; AmphibiaWeb, 2009), being mainly affected by the clearing of forests for agriculture and environmental pollution (Blaustein and Kiesecker, 2002). Currently, Centrolene savagei has been registered in the Central and Western Andes of Colombia (Cordilleras Occidental and Central of Colombia) in the departments of Quindío, Antioquia, Risaralda, Caldas, Tolima and Valle del Cauca (Ruiz-Carranza-Carranza and Lynch, 1991; Cadavid et al., 2005; Vargas-Salinas et al., 2007;

1 Universidad del Valle, Facultad de Ciencias Naturales y Exactas, Departamento de Biología, Grupo de Investigación en Ecología . Calle 13 # 100-00, Cali, Colombia. * Corresponding Author. E-mail: alan.giraldo@correounivalle. Figure 1. Male of Centrolene savagei Ruiz-Carranza and edu.co Lynch 1991. 294 María Lucia Prado-Sañudo et al.

Table 1. Localities.1 LAT: latitude, LON: Longitude, E: Elevation (m above sea level), P: mean precipitation (mm/year), T: mean 2 Table 1. Localities. LAT: latitude, LON: Longitude, E: Elevation (m above sea level), P: temperature (°C) 3 mean precipitation (mm/year), T: mean temperature (°C) 4 LOCALITY MUNICIPALITY LAT LON E P T Alto Bonito Manizales 05°06’42.9’’N 75°30’33.4’’W 1780 2600 18 Florencia Samaná 05°31’41.3’’N 75°02’52.0’’W 1520 1460 20 La Pastora Pereira 04°42’07.0”N 75°32’04.9”W 2100 2220 12 Santa Rosa Santa Rosa de 04°53’23.5’’N 75°37’10.3’’W 1650 2573 19 de Cabal Cabal Finlandia Finlandia 04°40’57.6’’N 75°38’21.2’’W 1830 2515 17 Boquía Salento 04°38’05.8’’N 75°35’28.2’’W 1720 1820 15 Alto el Otoño Santiago de Cali 03°22’21.4”N 76°36’08.1”W 1650 2000 18 Chicoral La Cumbre 03°33’44.5’N 76°35’35.1’’W 1790 1200 19 5 6 7 8 9 10 et al., 2008; Ruiz-Carranza11 and Lynch, 1991; Vargas- of parental attendance and to evaluate the tendency of Salinas et al., 2014).12 staying and ovipositting at higher levels. 13 Recently, absence14 of male attendance during the daylight hours15 was Table observed 2. Number at Alto of individuals el Otoño, and Cali, clutches of Centrolene savagei registered at 6 localities 16 of study. Materials and Methods department of17 Valle del Cauca (Pers. Obs. Prado- Sañudo). According LOCALITYwith Delia etAlto al. (2014),Santa Rosa the Finlandialack TheBoquía data was Alto collected del Chicoral in 8 field trips Total between October of parental care in glassfrogs mayBonito cause de Cabal embryos to 2012 and JuneOtoño 2013; each field trip lasted 3 days, and Males 7 7 2 2 20 8 46 hatch faster. Additionally, other behavioural changes was performed in one of the eight localities established Females 0 2 0 0 1 0 3 were observed, such as the tendency of males to stay according to previous registers of the species (Table 1, Juveniles 0 0 0 1 6 2 9 and sing on leaves 3m above the ground (Pers. Obs. Figure 2). Visual encounter survey was conducted along Amplexus 0 1 0 0 1 0 2 Prado-Sañudo). Clutches 2 5 0 one creek 1 over 8 an established 3 transect 19 of 500 meters Here, we examined18 eight populations of Centrolene per locality. All individuals and egg clutches were savagei in the departments19 of Caldas, Risaralda, Quindío registered and a consecutive number was assigned. 20 and Valle del Cauca,21 in order to describe the changes Adult individuals were marked by toe clipping; and 22 23 24 25 26 27 28 29 30 31

1

Figure 2. Sampled localities. 1 2 Table 1. Localities. LAT: latitude, LON: Longitude, E: Elevation (m above sea level), P: 3 mean precipitation (mm/year), T: mean temperature (°C) 4 LOCALITY MUNICIPALITY LAT LON E P T Alto Bonito Manizales 05°06’42.9’’N 75°30’33.4’’W 1780 2600 18 Florencia Samaná 05°31’41.3’’N 75°02’52.0’’W 1520 1460 20 La Pastora Pereira 04°42’07.0”N 75°32’04.9”W 2100 2220 12 Santa Rosa Santa Rosa de 04°53’23.5’’N 75°37’10.3’’W 1650 2573 19 de Cabal Cabal Finlandia Finlandia 04°40’57.6’’N 75°38’21.2’’W 1830 2515 17 Boquía Salento 04°38’05.8’’N 75°35’28.2’’W 1720 1820 15 Alto el Otoño Santiago de Cali 03°22’21.4”N 76°36’08.1”W 1650 2000 18 Chicoral La Cumbre 03°33’44.5’N 76°35’35.1’’W 1790 1200 19 5 6 7 8 9 10 11 Parental attendance12 and site selection of Centrolene savagei in Colombia 13 295 14 Table 2. Number15 of Tableindividuals 2. Number and clutches of individuals of Centrolene and clutches savagei of Centroleneregistered at savagei 6 localities registered of study. at 6 localities 16 of study. 17 LOCALITY Alto Santa Rosa Finlandia Boquía Alto del Chicoral Total Bonito de Cabal Otoño Males 7 7 2 2 20 8 46 Females 0 2 0 0 1 0 3 Juveniles 0 0 0 1 6 2 9 Amplexus 0 1 0 0 1 0 2 Clutches 2 5 0 1 8 3 19 18 19 20 21 22 Table 3. Hours23 of male attendance over clutches of Centrolene savagei. 3224 Table 3. Hours of male attendance over clutches of Centrolene savagei. 3325 26 OBSERVATION TIME 27 MALE PRESENT MALE ABSENT 28 29 LOCALITY CLUTCH DURING DURING DURING DURING 30 DAY NIGHT DAY NIGHT 31 1 - 21:35 12:01 - Alto Bonito 2 - 21:50 12:01 - 1 20:45 1 11:54 11:27 - 20:59

- 11:22 2 21:15 20:16 Santa Rosa - 11:20 de Cabal 11:22 3 - 21:20 20:16 11:20 20:16 4 11:22 - 11:20 21:22 5* - - 11:55 - 11:43 20:39 Boquía 1 - 21:36 12:39 20:17

1 - 20:30 13:56 21:11

14:01 22:57 2 - 21:30 11:52 22:36 12:25 14:03 23:09 3 22:10 12:14 - Alto del 11:41 Otoño 21:33 11:37 4 - 21:50 - 12:07 11:48 5 - 22:38 - 12:18 6 - 20:55 12:27 - 7 - 21:50 12:33 - 8 - 22:15 12:38 - 1 - - 10:53 19:45 Chicoral 2 - 21:25 11:00 - 3 11:00 - 11:00 21:30 34 *Fully hatched clutch 35 36 37 38 additionally, height above the ground, distance to the For clutches, the number of eggs,2 canopy cover, and edge of the creek, nearest edge and leaf area were presence or absence (overnight and daylight hours) of registered for each individual and each clutch detected. male surveillance were registered as well. 296 María Lucia Prado-Sañudo et al.

Figure 3. Types of parental attendance exhibited by males of Centrolene savagei. a) male over the clutch, b) male next to the clutch, and c) male in a leaf near the clutch.

In order to search for individuals and clutches at is a relationship between the number of eggs per clutch heights above 3m, 4 ascent stations were set up along and variables such as height, nearest edge, distance to the transect, and ascent equipment was used to reach the edge of the creek, and leaf area, Spearman tests was heights up to 6m above the ground. During the sampling used. effort, a data logger to register temperature and humidity was installed in each transect. Every sampling event Results occurred between 7pm and 1am, and between 11am and 2pm, by two persons, for a total sampling effort of 54 During the sample period, a total of 49 adult individuals hours per locality. (46♂ and 3♀), 9 juveniles, 19 egg clutches and 2 In order to determine if the encounters of male amplexus were registered; however, registers were only attendance of Centrolene savagei were consistent with found in 6 of the 8 localities (absent in Ucumarí and the expected, according to literature (male attendance Florencia, Table 2). Male attendance was observed in 17 over day and night hours) a Chi-square test was carried of the clutches in different ways: male over the clutch, out and a Hotelling’s T2 was performed for evaluating if male next to the clutch, and male in a leaf near the clutch the presence or absence of parental care was associated (Figure 3); parental attendance was also observed at with biotic or abiotic variables. To determine if there different hours of the day (Table 3). was a tendency of oviposition at higher altitudes Chi- Although it was expected to find the male at different square test was carried out and in order to know if there day times, from 59 observations made to the clutches, Parental attendance and site selection of Centrolene savagei in Colombia 297

Table 4. Types of male attendance registered. 39 Table 4. Types of male attendance registered. 40 PARENTAL CARE

LOCALITY CLUTCH ABSENT OVER THE NEXT TO LEAF CLUTCH THE NEAR THE CLUTCH CLUTCH 1 X Alto Bonito 2 X 1 X X

2 X

Santa Rosa de 3 X Cabal 4 X

5*1 X Boquía 1 X 1 X

2 X

3 X X X

4 X Alto del Otoño 5 X

6 X

7 X

8 X Chicoral 1 X*2

2 X

3 X X 41 *1Fully hatched clutch 42 *2 No recapture of the “possible” father. 43

males were present only in 23 (18 overnight hours, upper side of the leaf, with a mean area of 639.32cm2± 5 over daylight hours). Only 4 of the 19 clutches 970.74, a mean distance to the edge of 31.63cm ± (21.05%) had parental care during daylight hours, while 34.16, and a mean height of 178.1cm ± 97.6. One of the the 73.68% of them had care during the night (Table clutches was fully hatched, so the number of eggs could 3). Parental care was absent in two of the clutches; one not be determined, the other 18 had an average size of of them was a fully hatched clutch and, for the other, a 20 eggs± 4.14. male was observed in a leaf near it, but no recapture was According to selection of oviposition sites, it was registered, so it was not possible to determine if the male established that Centrolene savagei prefer to locate was the father of the clutch. However, the most common their clutches at heights between 0.1-2.0 meters above type of parental care was male over the clutch (84.21%), 2 ground level (X 2=9.57, p<0.008), over3 running water. while the male next to the clutch or in a leaf near the However, no significant relationship between the size clutch was only registered in 3 clutches respectively of the clutches and height (rs=0.39, p>0.05), the area of (15.78%). Furthermore, two clutches exhibited two the leaves (rs=0.14, p>0.05), distance to edge (rs=0.04, types of parental care and only one exhibited the three p>0.05), and nearest edge (rs=0.10, p>0.05) was types of parental care registered (Table 4). detected. According to these results, males of Centrolene savagei are not always attending their clutches (X2=21.96, p<0.001), however, this behavior is more often during night hours than daylight hours. It was also It is known that 10% of species exhibit established that male presence or absence is not related parental care; male glassfrogs tend to attend their with the nearest edge, distance to edge, height, leaf eggs, especially within the Centrolene and area, temperature, humidity or canopy cover (T2=6.73, (McDiarmid, 1975; Crump, 1996; p<0.542). All the registered clutches were located at the Deutel et al. 2011; Vargas-Salinas et al. 2014). Even 298 María Lucia Prado-Sañudo et al. though anurans may present several types of parental main causes for the varying size of the clutch. Likewise, care (egg transport, egg attendance, attendance, Villa (1984) presented evidence suggesting that the size tadpole transport or tadpole feeding), it has been of the clutch in Centrolene group is highly variable established that the most common type of parental due to the variation in energy investment required by care in this group is egg attendance, since it is the most the heterogeneity of the conditions for oviposition vulnerable life stage, which may cause high mortality sites. According to the results, there is no relationship rates (Crump, 1996; Vockenhubert et al., 2009; Lehtinen between the number of eggs per clutch and factors like: and Georgidis, 2012). height, area of the leaf, distance to the edge or nearest Three main reasons have been suggested to explain edge. This suggests that this variation may depend on the parental care in amphibians: increase reproductive other aspects that are not related to oviposition sites. success when fertility is low, decrease developmental We conclude that parental attendance in Centrolene abnormalities caused by yolk stratification or lack savagei is not displayed during all daylight and night of oxygen, and provide a more suitable microhabitat hours, being less frequent during the day. This behavior for the development of the offspring (Crump,1996; is not related to climatic and environmental conditions Vockenhuber et al., 2008). According to Hayes of the locality, but may be associated with other factors (1991), one of the main functions of parental care in such as the presence of potential predators. Males are is to keep hydration of the embryos to ensure the ones that select and defend territories, including their development. However, this behavior seems to oviposition sites, having preference for those located be closely related to the climate, being more intense at heights between 0.1-2.0m. When higher places are during dry seasons or hot afternoons (Delia et al., 2010; selected, clutches tend to have a bigger number of eggs, 2013). Therefore, a variable parental care may generate probably to counteract the risk of death of . environmental instability during the egg stage, altering the optimal time to hatch (Vockenhuber et al., 2009; Acknowledgments. We thank Ximena García, Carlos Burbano, Delia et al., 2014). Luz Angela Florez, Laura Tabares, Victor Gonzalez, Laura Vanesa Posso, Luz Marina Sañudo, Edder Alemson Escobar, As shown, the absence of male attendance during Ana Maria Soria, Natalia Rivera, and Juan Pablo Capera for daylight and night hours is not related to climatic their help in fieldwork. This research was partially founding by conditions of the localities, or specific characteristics COLCIENCIAS (program: Jóvenes Investigadores e Innovadores of the oviposition site, however, it could be associated “Virginia Gutiérrez de Pineda”), Universidad del Valle (postgrado with the need of protection against potential predators en Ciencias Biología), Karen´s Pizza y Carlos Eduardo Valencia. (Escobar-Lasso and Rojas-Morales, 2012). The male Special thanks to UMATA, Carton Colombia, and all property owners for their authorization to do the study inside their farms. presence or absence in each clutch could be related to the risk for each one of them, of remaining in the clutch, References due to the presence of predators, or the low incidence of clutches predators in the area. Confirming this would AmphibiaWeb. (2009): Centrolene savage. Available at: http:// require an extensive monitoring strategy in order to test amphibiaweb.org/species/1794. University of California, Berkeley, CA, USA. Accessed on 2 September 2017. this hypothesis. Blaustein, A.R., Kiesecker, J.M. (2002): Complexity in It is widely accepted that males of Centrolenidae conservation: lessons from the global decline of amphibian are not only territorial but also are the ones populations. Ecology Letters 5: 597–608. that apparently select sites where the conditions may Cabanzo-Olarte, L. C., Ramírez-Pinilla, M. P., Serrano-Cardozo, V. increase the survival of the embryos (Rueda-Almonacid, H. (2013): Oviposition, Site preference, and evaluation of male 1994; Valencia-Aguilar et al., 2012; Cabanzo-Olarte et clutch attendance in andina (Anura: Centrolenidae). Journal of Herpetology 47(2): 314–320. al., 2013; Dias et al., 2014). In this context, the results Cadavid, J.G., Roman-Valencia, C., Gómez, A. (2005): Composición suggest that males of Centrolene savagei preferred y estructura de anfibios anuros en un transecto altitudinal de los leaves located at heights between 0.1-2.0m; this could be Andes Centrales de Colombia. Revista del Museo Argentino de in order to prevent a potential threat to their reproductive Ciencias Naturales 7(2): 103–118. success, like the impact produced to tadpoles that fall Castro-Herrera, F., Bolívar-García, W. (2010): Libro rojo de los anfibios del Valle del Cauca. Cali, Colombia, Feriva Impresores from higher places. SA. The size of the egg clutches in frogs may vary due to Castro-Herrera, F., Vargas-Salinas, F. (2008): Anfibios y reptiles external factors. However, Duellman and Trueb (1986) en el departamento del Valle del Cauca, Colombia. Biota identified the age, size, and health of the female as the Colombiana 9(2): 251–277. Parental attendance and site selection of Centrolene savagei in Colombia 299

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Accepted by Anamarija Zagar