Reproductive strategies, free-swimming tadpoles, and natural history of the Santa Marta rocket frog “Colostethus” ruthveni Kaplan, 1997 (Anura: Dendrobatidae), with a review of the distribution of larval and reproductive characters in Dendrobatoidea

doi:10.21203/rs.3.rs-3134487/v1

Download PDF

Research Article

Reproductive strategies, free-swimming tadpoles, and natural history of the Santa Marta rocket frog “Colostethus” ruthveni Kaplan, 1997 (Anura: Dendrobatidae), with a review of the distribution of larval and reproductive characters in Dendrobatoidea

https://doi.org/10.21203/rs.3.rs-3134487/v1

This work is licensed under a CC BY 4.0 License

Version 1

posted

You are reading this latest preprint version

Herein, we research several aspects of biology of the Santa Marta rocket frog “Colostethus” ruthveni from the Sierra Nevada de Santa Marta, Colombian Caribbean. Quantification of relative abundance and habitat use was provided. Likewise, free-swimming tadpoles and reproductive strategies were described. In addition, the distribution of larval and reproductive characters across Dendrobatoidea were examined as an approach for their evolution and to identify whether these can complement the diagnosis of the “C.” ruthveni group. We recorded 853 specimens of “C.” ruthveni in six localities, resulting in a fairly high relative abundance at each site. Leaf-litter and rocks were the most used substrata, although their proportion of uses varying across the sites. The external morphology of free-swimming tadpoles of “C.” ruthveni resembles the former members of the Colostethus sensu lato. The courtship is a complex interaction of acoustic, visual, and tactile displays, which leads to the cephalic amplexus. "Colostethus" ruthveni showed wide variation in oviposition sites, including natural and artificial substrates at ground level, as well as creeping vegetation above the ground or water. Therefore, we consider that the species exhibits multiple reproductive modes, one of them previously unknown for anurans. Several larval and reproductive characters of “C.” ruthveni consist of a compendium of ancestral states. However, some characters are of special interest because these could be considered reversions to ancestral states or apomorphies, which could constitute synapomorphies of the “C.” ruthveni group if demonstrated to occur in the other undescribed members of the complex. In addition, we evidenced that "C." ruthveni is the only Dendrobatine with considerably narrow A2-gap. All this information on morphology and natural history provides insight into the evolutionary processes of poison frogs and provides basic information necessary for the management of this potentially endangered species.

character mapping

courtship

larval morphology

microhabitat uses

relative abundance

reproductive mode

Poison frogs of the superfamily Dendrobatoidea are one of the most representative groups of Neotropical amphibian fauna. These frogs have a series of highly diverse and particular characteristics: color patterns; the presence or absence of toxicity; elaborate displays of visual and acoustic signals; reproductive mode, (Wells 1980a,b,c; Weygoldt 1987; Juncá et al. 1994; Bourne et al. 2001; Caldwell and Lima 2003; Lima and Keller 2003; Hill et al. 2011; Summers and Tumulty 2014).Within this family is the genus Colostethus sensu lato, a non-monophyletic group in which multiple efforts have been made to order it in recent decades (Grant 1998; Grant et al. 2006; Santos et al. 2009; Grant et al. 2017; Marin et al. 2018), however the genus remains polyphyletic (Grant et al. 2017). The “Colostethus” ruthveni group Kaplan 1997 was found more closely related to the aposematic dendrobatids (subfamily Dendrobatinae) than to Colostethus sensu stricto (ss). Therefore, the “C.” ruthveni group constitutes an undescribed genus endemic to the Sierra Nevada de Santa Marta (SNSM) (Grant et al. 2017). Currently, the “C.” ruthveni group is constituted by the nominal species (“C.” ruthveni ss) and at least two undescribed species (Grant et al. 2017; Jiménez-Bolaño et al. 2019).

In the last decade, knowledge of the biology of the “C” ruthveni group has increased considerably, including data on its distribution, feeding ecology, phylogenetic relationships, and acoustic repertoire (González-Maya et al. 2011; Blanco-Torres et al. 2014; Granda-Rodríguez et al. 2014; Grant et al. 2017; Jiménez-Bolaño et al. 2019; Meza-Joya et al. 2019). However, multiple topics related to its reproductive mode are still unknown. Knowing the reproductive modes is of great interest, because natural and sexual selection favor reproductive mechanisms that maximize the probability of successful mating and the survival of offspring, directly affecting fitness and biological performance in response to different selective pressures (Carvajal-Castro et al. 2020). In this sense, the reproductive mode was defined as the combination of ecological, physiological, developmental, and behavioral traits such as the oviposition site, ovule morphology, clutch size and the presence or absence of different types of parental care (Duellman and Trueb 1994). In the Dendrobatoidea, the study of the reproductive mode is particularly interesting due to its great diversity (Vitt and Caldwell 2014; Carvajal-Castro et al. 2020). However, the only information available on this aspect for the group “C.” ruthveni was published more than a century ago by Ruthven and Gaige (1915), who briefly described the reproductive habitat and microhabitat and male transport of larvae.

Tadpoles of “C.” ruthveni present the typical morphology of Colostethus sensu lato larvae. The first description tadpole description was based on back-riding larvae removed from the male dorsum and free-swimming specimens (Ruthven and Gaige 1915). However, this description is too limited under current standards and describes free-swimming and back-riding tadpoles together. This is not recommended, as it makes comparisons difficult due to the ontogenetic variation between the different larval stages (Anganoy-Criollo 2013). Other more recent research has been limited to describing particular characters, with the aim of inferring phylogenetic relationships with larval morphology and the evolution of larval characters (Sánchez 2013; Anganoy-Criollo and Cepeda-Quilindo 2017). Such studies revealed that “C.” ruthveni apparently possesses multiple ancestral character states (e.g., the presence of a notch in the upper jaw sheath, the long gut sinistrally coiled, and the inner margin of the nasal rim projected), especially considering the phylogenetic relationships of the group sensu Grant et al. (2017). Given the limited knowledge of the external morphology of free-swimming tadpoles of “C.” ruthveni and the potential phylogenetic implications obtained from this line of evidence, a redescription of the tadpoles of the species is necessary, following the standards of current descriptions.

This species is currently categorized by the IUCN as Near Threatened ( NT- B1a;IUCN SSC Amphibian Specialist Group 2018) due to habitat loss because of agricultural activities (including pollution) and livestock, particularly in the southeastern sector of the SNSM (Granda-Rodríguez et al. 2020). Despite its relatively small range (EOO < 11,000 km²), populations appear to be stable and somewhat tolerant of disturbance. Although the IUCN categorization states that populations are stable and abundant, the statement is based on anecdotal observations that do not account for sampling effort. Consequently, acquiring information on the basic ecological dimensions of “C.” ruthveni, its relative abundance and habitat use will provide more appropriate tools to identify priority areas for the management and conservation of the species. Thus, according to the multiple knowledge gaps detected about the biology of the "C." ruthveni group, we developed this research with multiple objectives as follows: (1) quantifying the relative abundance and use of microhabitats; (2) redescription of the external morphology of free-swimming tadpoles; (3) documenting some aspects of the reproductive mode such as amplexus and laying site in a population of Colostethus ruthveni ss; and (4) to explore from a phylogenetic perspective the distribution of external larval and reproductive characters and how these can potentially facilitate the diagnosis of the group "C." ruthveni on the most recent available topology of Dendrobatoidea.

Study area

The study was carried out in 10 sites distributed in four pericontinental basins of the northwestern sector of the Sierra Nevada de Santa Marta (SNSM), district of Santa Marta, department of Magdalena, Colombian Caribbean (Fig. 1, Table 1). The sites occupy the altitudinal strip from the foothills to the low mountains, between 400 and 1521 m altitude, covering almost the entire altitudinal distribution known for "C." ruthveni (Granda-Rodríguez et al. 2014; Jiménez-Bolaño et al. 2019). This altitudinal strip includes in its lower sector the tropical dry biomes that succeed one another with the sub-Andean forest biome at approximately 700 m (Fundación Pro-Sierra Nevada 1998), with the exception of the Los Rodríguez stream basin, where the limit could be at around 550 m above sea level. The lower altitude is due to the fog, a product of the condensation of the humid coastal winds (Fundación Pro-Sierra Nevada 1998). The area's water regimes vary between unimodal and bimodal, with one or two annual rainfall peaks. Both climatic modes converge from the driest period, extending from December to March and the rainiest period extending from August to November. There may or may not be a drop in rainfall in July. Mountain lotic ecosystems show a rapid flow due to the steep slope of the mountain that have abundant boulders and sandy or pebble bottoms (Manjarrés-Garcia and Manjarrés-Pinzón 2004).

Relative abundance and microhabitat use

To estimate the relative abundance, 21 sampling events were carried out at six locations during the rainy and dry seasons between both 2005 and 2021 (Table 2). Two observers searched randomly, carefully inspecting the microhabitats in search of specimens of “C.” ruthveni using a visual encounter survey method (Crump and Scott 1994). The sampling effort varied between 2–6 hours (h) per event, for a total of 105 h (Table 3). With the total counts of individuals, a relative abundance index (RAI) was estimated, defined as the number of individuals (n) per capture effort (hours × observers), denoted as n/h/obs. To estimate the use of microhabitat, we followed the proposals of Inger (1994) and Vargas-Salinas and Castro (1999), where we recorded the substrate just below the specimen and calculated the observation frequency for each substrate. We performed a Chi square test of homogeneity (χ2) to refute the null hypothesis that there is no significant variation in the use of substrate (microhabitat). We calculated the same expected frequency for each microhabitat category detected in the field, since we assumed that the microhabitats had the same probability of being occupied.

Free-swimming tadpoles

This study followed the nomenclature of the Dendrobatoidea superfamily proposed by Grant et al. (2017) with the arrangements of Marin et al. (2018). The description of the tadpole was based on a batch of 57 tadpoles deposited in the amphibian collection at the Centro de Colecciones Científicas de la Universidad del Magdalena (CBUMAG:ANF:00662), collected by J. M. Renjifo at the La Victoria farm, Minca village, District of Santa Marta, department of Magdalena, Colombia (see Fig. 1). Additionally, some observations on the natural history were conducted in the localities of Las Tinajas, Bella Vista, Pozo Azul and Arimaca. Tadpoles were determined to the species level as “Colostethus” ruthveni sensu stricto by the following characteristics: (1) the presence of the golden band on the body of the tadpole described by by Ruthven and Gaige (1915); (2) the geographic distribution of the complex proposed by Jiménez-Bolaño et al. (2019); and (3) the presence of three metamorphics in the lot whose morphological characters correspond to those described by Kaplan (1997). A Leica M205A stereomicroscope with a Leica DFC450 camera was used for the examination and photography of the specimens. The morphometric characters (expressed in mm) were characterized with the Leica Application Suite software (Version 4.6.0), with a precision of ± 0.01.

For tadpole description, we examined the external morphology based on three tadpoles at stage 35 of Gosner (1960), since this stage represents the midpoint of larval development (Suarez-Mayorga and Lynch 2001). The other stages were used to describe the ontogenetic variation of the morphological and morphometric characters. The terminology proposed by Altig and McDiarmid (1999) and (Anganoy-Criollo 2013) for morphometric characterization was followed, evaluating the total length (TL), body length (BL), body width (BW), tail length (TAL), maximum tail height (MTH), tail muscle height (TMH), tail muscle width (TMW), internarial distance (IND), interorbital distance (IOD), oral disc width (ODW), anterior lip gap width (AL-gap), width of medial gap in second anterior tooth row (A-2 gap), nostril length (NL), nostril-snout distance (NSD), nostril-eye distance (NED) spiracle length (SL), spiracle height (SH), spiracle -snout distance (SSD), Eye diameter (ED) eye-snout distance (ESD), upper jaw sheat width (UJS-W), lower jaw sheat width (LJS-W). Additionally, we examined the arrangement of the rows of papillae in the anterior (PAL) and posterior (PPL) lips, following the terminology of Sánchez (2010). Likewise, the number of papillae on each lip was counted in the space of one millimeter (Anganoy-Criollo 2013). For metamorphic tadpoles, total length, tail length, and body width were measured.

Reproductive strategies

To identify egg-laying sites, we carried out seven monthly fieldtrips lasting two days in Las Tinajas from June to December 2015. We conduct three additional fieldtrips during August 2015 (two days), December 2016 (one day), and January 2021 (one day) in Bella Vista, Arimaca, and Sierra Minca, respectively. At each site, two observers explored the watercourses proceeding upstream and using the visual encounter survey method (Crump and Scott 1994). We began the searches starting from 06:00 to 18:00 for a total effort of 210 h. × 2 observers (168 h in Los Rodríguez ravine; 24 h in Bella Vista; 12 h in Marinca; and 6 h in Sierra Minca). At each egg laying site, the number of eggs, egg diameter, location, and distance from the water source were recorded. Information on courtship and type of amplexus was obtained through direct observations. Aspects of courtship such as color change, jumps, circle jumps, body elevation, et al., were described following the terminology of Hödl and Amézquita (2001). The reproductive mode was established from the proposal Nunes-De-Almeida et al. (2021, see S2), where 11 reproductive and larval characters were examined using a dichotomous key.

Distribution of larval and reproductive characters

We built a matrix coding 35 phenotypic characters (larval and reproductive morphology) for each genus of the Dendrobatoidea superfamily (22 genera). Thirty-two characters were extracted from Appendix 1 of Grant et al. (2017) (characters 94–126). The coding of these characters was extracted via an extensive literature review on free-swimming tadpoles morphology and reproductive strategies of Dendrobatoidea (Ruthven and Gaige 1915; Breder 1946; Savage 1968, 2002; Edwards 1971, 1974; Silverstone 1975; Lescure 1976; Wells 1980a, b; Lynch 1982; Myers et al. 1984; La Marca 1985, 1989, 1993, 1994; La Marca and Mijares-Urrutia 1988; Donnelly et al. 1990; Schulte 1990; Caldwell and Myers 1990; Mijares-Urrutia 1991; Ruiz-Carranza and Ramirez-Pinilla 1992; van Wijngaarden and Bolaños 1992; Rodriguez and Myers 1993; Mijares-Urrutia and La Marca 1997; Myers and Donnelly 1997, 2001; Lüddecke 1999; Caldwell et al. 2002; Duellman 2004; Barrio-Amorós et al. 2004; Castillo-Trenn 2004; Caldwell 2005; Grant et al. 2006, 2007, 2017; Kok et al. 2006a,b, 2010, 2013; Lehtinen and Halley 2008; Brown et al. 2008; Twomey and Brown 2008, 2009; Von May et al. 2008; Masche et al. 2010; Páez-Vacas et al. 2010; Perez-Peña et al. 2010; Poelman et al. 2010; Simões et al. 2010, 2013; Almendáriz C et al. 2012; Simões and Lima 2012; Anganoy-Criollo 2013; Sánchez 2013; Downie and Nokhbatolfoghahai 2014; Lima et al. 2014, 2015; Schulze et al. 2015; Anganoy-Criollo and Cepeda-Quilindo 2017; Menin et al. 2017; Serrano-Rojas et al. 2017; Dias et al. 2018a, b, 2021; Granda–Rodríguez et al. 2018; Fouquet et al. 2019; French et al. 2019; Moraes et al. 2019; Duarte-Marín et al. 2020; Klein et al. 2020; Rojas-Morales et al. 2021; Pezzuti et al. 2022). One of the characters from Grant et al. (2006, 2017) was reinterpreted as follows:

119. Oviposition site: aquatic = 0; terrestrial: at ground level = 1; terrestrial: phytoteltama = 2; terrestrial: in leaves above ground or water level = 3. Additive.

This character is additive for describing the degree of association with the ground level or the distance from the water Grant et al. (2006). State 1 includes all microhabitats at ground level such as leaf litter, bare soil, as well as on and under fallen objects such as rocks, logs, and even artificial objects. State 2 is restricted to cavities with liquid water in terrestrial plants. State 3 consists of species that lay their eggs on the upper or underside of the leaves, which had been considered as part of state 2 by (Grant et al. 2006, 2017). Additionally, two new characters were declared following the argument of Sereno (2007) that were enumerated following the consecutive number of character list of Grant et al. (2017):

189. Second keratodon row of anterior lip, medial gap (A2-gap): absent = 0; present = 1.

190. First keratodon row of posterior lip, medial gap (P1-gap): absent = 0; present = 1.

Subsequently, these 35 characters were mapped by hand on the topology that summarizes the generic relationships of Dendrobatoidea proposed by Grant et al. (2017, modified from Fig. 47), seeking to identify how the larval morphological plans and the reproductive modes are distributed throughout this hypothesis of the evolutionary relationships of the Dendrobatoidea. In addition, we explored the intra- and intergeneric variation of a continuous character: the ratio of the width of the medial gap of the second row of keratodon teeth of the anterior lip by the width of the oral disc (A2-gap/ODW %), since it has recently been proposed as potentially useful for diagnosing some taxa within Dendrobatoidea (Granda-Rodríguez et al. 2018).

Relative abundance and microhabitat use

We observed a total of 853 individuals of “C.” ruthveni ss in six study locations. We found that the species was very abundant in all samplings and locations (Table 1), since in all cases the RAI reached values greater than 1, between 1.7–6.3 n/h/obs, with an exceptional observation of 10 n/h/obs. This means that the species maintained an approximate encounter rate of two to six individuals per hour throughout the entire time window studied. Although the largest number of individuals was detected in Las Tinajas (n = 258) and La Victoria (n = 209), the highest RAI values were obtained in Sierra Minca (10 n/h/obs) and Central Córdoba (6.2 n/h/obs), since at these sites less sampling effort was required to record a considerable number of specimens. We obtained microhabitat use data from 213 specimens. We identified six categories of substrate used by the species: litter, rock, bare soil, leaves, fallen logs, and stream, where the most used substrates were rocks (77 individuals, 36.2%) and litter (57 individuals, 26.8%). We found a differential use of microhabitats at all sites, and the proportion of use of each microhabitat also varied between them, since at one site rocks were the most used substrate, and at the remaining three sites, litter was the most used (Table 2).

Redescription of free-swimming tadpoles

Table 3 presents the summary of the morphometric characters analyzed (individual data for each tadpole in Supplementary Table 1). Stage 35 tadpoles have the following characteristics: body ovoid in dorsal view and compressed in lateral view (BW/BL = 60–64%, BH/BW = 78–86%, Fig. 2), reaching just over a third of the total length ;(BL/TL = 34–36%); snout rounded in dorsal and lateral view; nostrils rounded in dorsal view, directed dorsolaterally, with gently projecting margins, equidistant between eyes and tip of snout, occupying almost one third of eye diameter (NL/ED = 21–31%); internarial distance is approximately two-thirds of the interorbital distance (IND/IOD = 62–67%); and the interorbital distance one-half the body width IOD/BW = 47–48%). Eyes located dorsally and directed dorsolaterally, whose diameter is less than half the interorbital distance (ED/IOD = 39%). Sinister spiracle, as long as high (SH/SL = 48–54%), visible in lateral, dorsal, and ventral view, directed posterior-dorsally, opening posterior to midpoint of body, exceeding half body length (SSD/TL = 61–66%).

Vent opening dexterous, tail musculature as long as the fin, fin tip rounded. The tail exceeds half the total length (TAL/TL = 64–66%) and its maximum height is 15–16% of the total length, but 82–93% of the body height. Caudal myotomes visible, tail axis straight. Robust caudal musculature in the front part of the body, tapering gradually towards the end of the tail. The caudal musculature is half as wide and about one third shorter than the body (TMW/BW = 51–58%, TMH/BH = 61–65%). The dorsal fin extends only as a slight ridge along the body at the body-tail junction and is narrower than the tail muscle. In the middle of the tail, the dorsal fin is slightly higher than the ventral fin. The ventral fin originates from the body and is narrower than the tail muscle. The point of origin of the hind legs is parallel to the cloacal tube.

The oral disc is emarginate, directed anteroventrally, surrounded by marginal papillae, (except in the middle of the anterior lip, AL-gap/ODW = 53–68%) occupying just under half the width of the body (ODW/BW = 43 − 48%). Papillae are abundant on both lips, where the right lateral margin of the anterior lip has 16–17 papillae/mm that are blunt and smaller than those of the posterior lip. On the posterior lip, the papillae in the central part are conical, elongated, and blunt (13–16 papillae/mm), while on the lateral margins they are conical and pointed. Dental formula 2(2)/3(1) with a very small A-2 gap (A-2 gap/ODW = 3–7%). The first row of teeth of the posterior lip (P-1) is briefly interrupted (P-1 gap), while P-2 and P-3 are continuous. Rows P-1 and P-2 are of equal length, while P-3 is slightly short. The teeth in P-3 are slightly smaller and less keratinized than those in the other rows. The upper jaw sheath is half the width of the oral disc (UJS/ODW = 48–52%) with thin, arch-shaped, medially notched (W-shaped) lateral processes. On the other hand, the lower jaw sheath is narrower (LJS/ODW = 37–39%), thinner, and broad V-shaped; both with small, blunt striae.

The general morphology of the free-swimming tadpoles did not present abrupt changes between the different stages analyzed (Fig. 3a), however, slight variations were observed in some characters of the configuration of the oral disc. In stages 25–38, only one row of papillae was observed on the anterior lip and the number of these varied in a range of 11–23 papillae/mm. On the posterior lip, a simple row, a biseriate row and two rows of papillae were observed, with 11–21 papillae/mm (Fig. 3b). Regarding the length of the rows of teeth on the posterior lip, they could all have the same length (P1 = P2 = P3) or two equal ones and one shorter (P1 = P2 > P3 or P2 > P1 = P3). Metamorphics of stage 42 (n = 1; TL = 18.2 mm, TAL = 12.5 mm, BW = 4.5 mm), 43 (n = 2, TL = 17.7 mm, TAL = 9.0 mm, BW = 4.0 mm) and 45 (n = 1, TL = 11.4 mm, BW = 4.2) showed a reduction in total length, maximum tail height and tail length. In addition, other structures such as the oral disc, keratinized ornamentation (UPJ, LJS and tooth rows), blowhole and cloacal tube disappear.

Tadpoles are generally uniformly dark-backed, although some specimens have minute golden spots towards the front of the body. Free-swimming tadpoles have a gold stripe towards the back of the eyes, which have tiny gold dots (Fig. 4ab). Between the eyes and the tip of the snout there are golden spots directed laterally, passing under the nostrils. The back of the body is dark brown with golden spots (in some cases evenly brown). The tail in lateral view presents dark brown spots and spots, encompassing the dorsal and ventral fins. The caudal musculature greenish-yellow. In ventral view it is whitish to greyish, slightly translucent. When preserved, the body is light brown in dorsal view (completely black in some cases). The golden stripe and spots disappear, being replaced by brown or black spots on the tail. In the distal region, the tail becomes translucent. Ventrally, the intestine is visible under the skin showing a dark brown coloration.

The free-swimming tadpoles of “C”. ruthveni ss generally inhabit pools in small mountain lotic systems generally located under the shade of large trees and surrounded by medium-sized vegetation. These present benthic and hidden habits. In pools with a lot of sun exposure individuals hide under rocks, marginal vegetation, the bottom leaf litter, or partially buried in the sand. The tadpoles had an apparently omnivorous diet, since some individuals were found feeding on leaves and flowers that fell into the ponds as well as earthworm remains and a dead conspecific (Fig. 4cd).

Courtship and reproductive mode

We observed four pairs involved in courtship with which we built a general scheme of courtship behavior unknown up to now (Fig. 5). It is worth mentioning that the courtship of "C". ruthveni ss exhibits some slight variations among the partial observations we made. All the events began with the issuance of the mating call by the male from different substrates (e.g., cavities between the boulders, on fallen logs on the edge of the ravine, on the broad leaves of grazing vegetation). The males darken in color during vocalization (color change). This results in positive phonotaxis by the females that approach the vocalization sites.

In most of the observations, during the first phase of the close encounter between the male and the female, the male began to “circle”, circling the female with small jumps while she issued the mating call. Later, the male exhibited “body raising”, a raised posture stretching all four legs, followed by a “throat display”, inflating the vocal sac. In other cases, there were tactile interactions that included the stealthy approach of the male to the female, who then rubbed his forelimbs on her back, like a "massage". This was followed by the emission of the courtship or advertisement call and cephalic amplexus. This always occurred in hidden spaces, such as between spaces in the middle of boulders or in cavities of fallen logs. On one of the occasions and for a few seconds, pseudo positions or variants ranging from axillary to cephalic grasping were observed, ending in the latter. Only in one pair during cephalic amplexus did we observe the male making "toe trembling" (see supplementary material 2: video material).

Regarding the postures, we observed nine egg masses, of which five were deposited at the base of the upper leaves (Fig. 6a) of low-growing plants hidden by the foliage. Four egg masses (spawn) were laid on leaves just above the water surface. The remaining spawn was on a plant 0.57 m horizontally from the water and 14 cm high. However, it is possible that this was originally on the surface of the water, but probably moved away from it due to a decrease in the volume of water in the creek. In three of these positions, parental care was detected by the males. In addition, we identified the use of artificial substrates (Fig. 4bc), as we found egg masses deposited in a pile of damp cardboard and plastic sheets surrounded by leaf litter, both about 50 meters from the nearest watercourse. In both sexes we found parental care. On the other hand, we detected two egg masses at ground level. One of them was deposited in a hole in a rock covered by leaf litter, approximately two horizontal meters from the watercourse. The other spawn was deposited directly on the wet leaf litter (Fig. 6d) about four meters from the ravine. In neither of the two cases was parental care observed, but males were vocalizing around the spawn. Finally, in Sierra Minca we found a spawn oviposit directly on the surface of a rock next of the creek flowAlthough it was not possible for us to photograph this record, there are photographs available on social networks taken by other researchers in the region that prove it (available here: https://www.instagram.com/p/BlBQrNqhLDl/?igshid=MzRlODBiNWFlZA%3D%3D&fbclid=IwAR1F3LUaS7Y9XIUhZOhQ6uqUbhK3cRYSkZ5FRjVNHbhncKp-m32OJ9n3y74). The spawn of “C.” ruthveni ss reported in this study, suggests that this species produces a small number of eggs (Table 3, range = 2–15 eggs; mean ± standard deviation = 9.2 ± 4.4 eggs) of small size (1.8–7.3 mm, 4.4 ± 1).

Distribution of larval and reproductive characters

From the 35 characters examined, we obtained new information for 12 of them: 10 reproductive characters and two larval ones. (Fig. 7, see Supplementary Tables 2 and 3, and Supplementary document). Under the hypothesis of the relationships of the Dendrobatoidea genera of Grant et al. (2017, appendix 1), 27 characters (17 larval, 10 reproductive) can be considered symplesiomorphic for the group “C.” ruthveni. The caudal coloration of the larvae is arranged in dispersed melanophores grouped in diffuse spots [93(0); it is a character number in appendix 1 of Grant et al. (state of character)], occurrence of reproductive amplexus [115(1)], and larval habitat in wells and streams [123(0)] can consist of reversions to ancestral states. Likewise, the presence of a lateral line stitches [106(1)] could be considered as an apomorphy (character examined by Grant et al. 2017). Two polymorphic characters were observed. In the case of the laying site, terrestrial clutches at ground level [118(1)] are a simplesiomorphic state, while terrestrial clutches above ground or water level [118(3)] are an apomorphy. On the diet of exotrophic tadpoles, predatory habits [125(1)] consist of a simplesiomorphy, while detritivorous habits [125(2)] consist of a reversal.

Regarding the continuous character A2-gap/ODW (%), the ranges were so wide among most of the genera that it was not possible to classify them in a single category (see Supplementary Table 4). Only group "C." ruthveni, Rheobates and Mannophryne showed a strictly narrow A2-gap. Likewise, the genera Anomalogluss, Aromobates, Colostethus, and Leucostethus had narrow to moderate A2-gaps (in all cases the A2-gap/ODW ≤ 16%). Something similar occurred with Hyloxalus, where most of the species with the presence of A2-gap (absent in eight species), showed gaps falling between narrow and moderate (A2-gap/ODW = 3–13%). The exception was H. sauli that had a considerably wider A2-gap (A2-gap/ODW = 25%). The genera Allobates, Amereega, Epipedobates, Phyllobates, Dendrobates, Adelphobates and Andinobates had a moderate to wide A2-gaps. Only the genera Excidobates and Ranitomeya had a strictly wide A2-gap. This indicated to us that, “C.” ruthveni is the only dendrobatid with a narrow A2-gap.

Relative abundance and microhabitat use

"Colostethus" ruthveni ss is an abundant species, at least during the periods and at the sites sampled. Although these data do not allow us to assume that the relative abundance is constantly high, they suggest that the populations can remain very conspicuous, despite the marked water deficit suffered by the lower range of the SNSM (< 1000 masl) during the dry season (Fundación Pro-Sierra Nevada 1998). The variation of the relative abundance in each sampling event, could be the product of multiple factors inherent to the biology of “C.” ruthveni ss like the occupancy and detection probabilities, as well as those related to the characteristics of the sampling such as the capture effort and the accessibility to the microhabitats for the observer (MacKenzie et al. 2002). Regarding the latter, the localities where the greatest abundance was recorded (Sierra Minca, Central Córdoba and Las Tinajas) have easily accessible ravines, gentler slopes and longer walkable stretches, where observers have less physical difficulties in detecting specimens.

It is possible that the apparently stable population status of “C.” ruthveni ss in the study area is related to the fact that the northwestern sector of the SNSM is one of the best preserved areas of the entire massif, since it has the least loss of natural vegetation cover in the past two decades (Granda-Rodríguez et al. 2020). The studies carried out so far of the other endemic amphibians of the SNSM of the genera Atelopus, Pristimantis, Geobatrachus, and Ikakogi (Martinez-Baños et al. 2011; Granda Rodriguez et al. 2012; Granda-Rodríguez et al. 2020; Roach et al. 2021) show high relative abundances, despite the presence of chytridiomycosis in the region (Flechas et al. 2017). This is in contrast to the general panorama of the conservation status of amphibians in the North-Andean region, where multiple population declines have been documented (Womack et al. 2022).

Despite the apparent stability in the relative abundance of amphibians in the northwestern SNSM, multiple potential threats must be addressed. With the recent "Peace Process" in Colombia and the dismantling of some of the insurgent armed groups, areas previously indirectly protected by the Colombian armed conflict are now available for use. Due to the increase in tourism and agricultural activity in the area, demographic growth in the distributional area of “C.” ruthveni has recently accelerated (Carvajalino-Slaghekke 2015; Guardiola 2019). This leads to an increase in infrastructure and water demand, as well as environmental noise that, together with poor wastewater management, can synergistically affect the population status of this and other amphibian species in the area. Therefore, the implementation of environmental management measures and territorial planning in this region should be encouraged. Although, currently "C." ruthveni is considered a Near Threatened species, the recent discovery of cryptic diversity within “C.” ruthveni (Grant et al. 2017; Jiménez-Bolaño et al. 2019) will generate substantial changes in the interpretation of the conservation status, because the area of distribution and threats will be fragmented according to the number of species that make up the group and how they are distributed throughout the SNSM.

The microhabitat use data obtained show that the greatest activity of “C.” ruthveni occurs in the lowest strata of the forest, below approximately 50 cm. Like other dendrobatoids from northern Colombia, “C.” ruthveni finds shelter and food in microhabitats on the forest floor such as rocks and leaf litter (Blanco-Torres et al. 2013, 2014; Posso-Peláez et al. 2017; Granda-Rodríguez et al. 2018). Added to this is the fact that all the processes involved in reproductive biology known up to now, such as singing, courtship, amplexus, laying site, among others, also occur at ground level or in the lowest strata of the forest.

Free-swimming tadpoles

The tadpoles of “C.” ruthveni have the typical morphology of the larvae that were part of the genus Colostethus sensu lato (Coloma 1995; Anganoy-Criollo 2013), currently included in various genera of the families Aromobatidae and Dendrobatidae (Colostethinae and Hyloxalinae). Several character states of external larval morphology such as the UJS notch, sinister gut, and projecting nostril rim are ancestral (Sánchez 2013), symplesiomorphically shared with Aromobatidae, Colostethinae, Hyloxalinae, and Phyllobates. On the other hand, the narrow A-2 gap and the moderately sized nostrils could constitute putative synapomorphies of the “C” group ruthveni, if it is verified that they are also present in group members that are not yet described (sensu Grant et al. 2017; Jiménez-Bolaño et al. 2019).

The external morphology of the free-swimming tadpoles of “C.” ruthveni from La Victoria agrees with the character states described by Anganoy-Criollo (2013), Sánchez (2013) and Anganoy-Criollo and Cepeda-Quilindo (2017). However, part of the material examined and determined by Sánchez (2013) does not correspond to "C." ruthveni ss. One batch of specimens (ICN 35773) comes from the southwestern sector of the SNSM, where “C.” sp ruthveni-like is distributed (Grant et al. 2017; Jiménez-Bolaño et al. 2019). As well as, the ICN 35779 batch of specimens comes from the Serranía del Perijá, a region part of the Andean mountain range that is not connected to SNSM (Granda-Rodríguez et al. 2014; Jiménez-Bolaño et al. 2019; Meza-Joya et al. 2019). These tadpoles may correspond to two aromobatids from the western foothills of the Serranía de Perijá, Rheobates palmatus Werner, 1899 or Allobates ignotus Anganoy-Criollo, 2012 (Moreno-Arias et al. 2009; Anganoy-Criollo 2012; Romero-Martinez and Lynch 2012; Granda-Rodríguez et al. 2018).

The states of some tadpole characters of "C." ruthveni determined by us showed strong variation with respect to what was reported by Ruthven and Gaige (1915). The illustrations provided by them of back-riding and free-swimming tadpoles show the A-2 gap to be very wide (back-riding tadpole: A–2 gap/ODW = 30%, free-swimming tadpole: A-2 gap/ODW = 25%, calculated qualitatively from Ruthven and Gaige (1915, Figs. 1 and 3). Furthermore, referring to the same free-swimming tadpole with 20 mm TL, they suggested that “the upper second row of teeth is not always is interrupted”. Although it was not possible to determine the larval stage (sensu of the tadpoles illustrated by them. Our larvae of similar size (Stage 26, n = 13, TL = 16.7–23.3 mm) have a much reduced A-2 gap on average (A-2 gap/ODW = 5.1%), but it is never absent. It is possible that the marked differences in the A-2 gap ratio of Ruthven and Gaige (1915) tadpoles with respect to recent literature (Anganoy-Criollo and Cepeda-Quilindo 2017) obey ontogenic variation; however, this variation would far exceed that detected from our material, since the tadpole with the highest A-2 gap/ODW ratio had < 8% at stage 26.

Another contrasting detail of the Ruthven and Gaige (1915) illustrations is that they suggest that the UJS notch is absent, a condition contrary to that reported by recent studies (UJS notch present, UJS “W-shaped”; Sánchez 2013; Anganoy-Criollo and Cepeda-Quilindo 2017). The presence of the UJS notch is a character with little variation and easily distinguishable in free-swimming tadpoles (from stage 25; Sánchez 2013; M A. Anganoy-Criollo, pers. comm.). The A-2 gap/ODW ratio and the absence of the UJS notch in the free-swimming tadpole (20 mm TL) illustrated by Ruthven and Gaige (1915) could be considered as atypical character states in light of recent evidence.

Courtship and reproductive mode

Courtship, like other reproductive behavior traits, is undoubtedly considered one of the most conspicuous and fascinating features of dendrobatoids (Wells 2007; Summers and Tumulty 2014). Thus, partial observations on courtship in "C." ruthveni are similar to those reported in other dendrobatoid species such as Mannophryne trinitatis Garman 1888, Mannophryne collaris Boulenger 1912, Anomaloglossus stepheni Martins 1989, Allobates marchesianus Melin 1941, Allobates femoralis Boulenger 1884, Allobates paleovarzensis Lima, Caldwell, Biavati, and Montanarin 2010, Allobates velocicantus Souza, Ferrão, Hanken, and Lima 2020 R. palmatus, Colostethus panamansis Dunn 1933, Hyloxalus toachi Coloma, 1995, Dendrobates auratus Girard 1855 and Dendrobates tinctorius Cuvier 1797, where behaviors such as color changes, body raising, circling, throat displays, and tactile interactions have been observed (Duellman 1966; Dole and Durant 1974; Lüddecke 1976; Wells 1978, 1980a, b; Juncá 1998; Hödl and Amézquita 2001; Juncá and Rodrigues 2006; Quiguango-Ubillús and Coloma 2008; Lima et al. 2010; Montanarin et al. 2011; Rocha et al. 2018; Rojas and Pašukonis 2019). The tactile interactions of “C.” ruthveni are similar to those described in A. stepheni, Allobates subfolionidifcans Lima, Sánchez, and Souza 2007 and D. tinctorius, where the male approaches the female and places his front legs on her back, perhaps a stimulant prior to oviposition (Juncá and Rodrigues 2006; Souza et al. 2017; Rojas and Pašukonis 2019).

Of all the possible courtship variation within the Dendrobatoidea clade, some behaviors contrast with our observations. For example, something very particular and that differs notably from the behavior of “C.” ruthveni ss is the upright posture on its hind legs observed during courtship only in M. collaris and which the authors call “toe-dance” (Dole and Durant 1974). Likewise, in aposematic species such as Ameerega braccata Steindachner 1864, Ameerega flavopicta Lutz 1925 and Oophaga sylvatica Funkhouser 1956, courtship is accompanied by the display of conspicuous coloration of hidden surfaces through visual cues by moving their limbs (Summers 1992; Costa et al. 2006; Forti et al. 2013). “Toe-trembling” is a very common visual signal in anurans (Sloggett and Zeilstra 2008), however this signal exhibited by “C.” ruthveni ss during amplexus differs from that reported in species such as Oophaga histrionica Berthold, 1845, D. auratus and D. tinctorius, where it has been observed during courtship, foraging, and agonistic interactions (Silverstone 1973; Wells 1978; Rojas and Pašukonis 2019).

Cephalic amplexus is one of the most striking characteristics within dendrobatoid courtship. It is present in at least 22 species and is strongly associated with terrestrial habits representing 6.5% of the known diversity of the clade (Carvajal-Castro et al. 2020; Frost 2023). This behavior is quite complex, and the establishment of its homology depends to a great extent on the reproductive context, where certain pre-ovipositional variants are not part of the cephalic grasp in a strict sense (Castillo-Trenn and Coloma 2008). In accordance with the above, "C." ruthveni ss exhibits various forms of grasping in the nuptial embrace, resulting in intermediate points between the axillary position and the final cephalic position. This is similar to what was observed in A. flavopicta, where the axillary amplexus was initially reported (Costa et al. 2006). But later observations determined intraspecific variation in the position of the embrace, with intermediate positions between the axillary and cephalic amplexus, the last the predominant variation (Magrini et al. 2010). However, this differs from what was reported in Hyloxalus azureiventris (Kneller and Henle 1985) and some cryptic species that were part of the extensive group Colostethus sensu lato such as Allobates caeruleodactylus Lima and Caldwell 2001 and A. subfolionidificans in which this type of amplexus has not been recorded (Lima et al. 2002; Quiguango-Ubillús and Coloma 2008; Souza et al. 2017).

Several authors have considered parental care and larval transport as a reproductive mode trait (Duellman and Trueb 1994; Haddad and Prado 2005; Wells 2007; Crump 2015). However, Nunes-De-Almeida et al. (2021) in their redefinition of the reproductive mode, excluded parental care as it is a difficult characteristic to identify, except for those cases where care involves feeding and incubation. This is interesting when compared with our observations, since considering the proposal of Haddad and Prado (2005), the annotations for the transport of larvae made by Ruthven and Gaige (1915) complemented with the masses of eggs at ground level found in “C.” ruthveni ss in localities of the SNSM coincide with Mode 20 (eggs that hatch in exotrophic tadpoles that are transported to the water by the adult), agreeing with that exhibited by C. panamansis and other dendrobatoids of the Ameerega, Silverstoneia, Epipedobates, Hyloxalus and Allobates genus (Wells 1980b; Lima et al. 2010; Summers and Tumulty 2014; Crump 2015).

Regarding the postures above ground level of “C.” ruthveni found in the Las Tinajas, these are similar to what was observed in Allobates brunneus (Cope, 1887), Ameerega bilinguis (Jungfer 1989), Ameerega hahneli (Boulenger 1884), Allobates carajas Simões, Rojas, and Lima, 2019, and Leucostethus fraterdanieli (Silverstone 1971), and A. subfolionidificans (Lima et al. 2009; Beirne and Whitworth 2011; Brown et al. 2019; Simões et al. 2019; Rojas-Morales et al. 2021), which latter is different from the others because it deposits its eggs on the underside of leaves (Lima et al. 2007; Souza et al. 2017). Unlike the species mentioned, in “C.” ruthveni, the transport of larvae in this area was not observed, so we elaborated two hypotheses to explain this event: a) the transport and deposition of larvae in the pond is done immediately after hatching and b) there is a mode without transport of larvae larvae, in which they hatch and fall directly into the water (Mode 24, Haddad and Prado 2005). The latter and the location of egg masses at and above ground level at “C.” ruthveni suggested some degree of phenotypic plasticity in reproductive mode, as has been shown in the species Dendropsophus ebraccatus Cope 1874 (Hylidae) that alternates between aquatic and terrestrial postures (Touchon and Warkentin 2008).

"Colostethus" ruthveni ss egg masses in vegetation above ground level, as well as those deposited at ground level correspond to modes 22 and 32 (Nunes-De-Almeida et al. 2021). Curiously, in the scheme of Nunes-De-Almeida et al. (2021) there is no reproductive mode that includes clutches deposited on rocky substrates that derive from tadpoles (indirect development) from exotrophic nutrition and lotic habitats. So far, only rocks have been documented as ovipositing substrates in salamanders that produce direct development offspring (Mode 35). Therefore, we propose an additional reproductive mode that continues the list of Nunes-De-Almeida et al. (2021): Mode “75”: Terrestrial non-froth eggs laid on rock. Offspring with indirect development, lecithotrophic nutrition, exotrophic, and without parental feeding. Known only for anurans. In passing, we want to note that the use of quotation marks in the number does not necessarily indicate the consecutive under the Nunes-De-Almeida et al. (2021) scheme. This variation in reproductive mode are probably the product of phenotypic plasticity of this species against environmental conditions. This must be tested experimentally both in situ and ex situ (Barboza 2014).

Distribution of larval and reproductive characters

The hypothesis about the phylogenetic relationships of the group “C.” ruthveni by Grant et al. (2017) could be considered a surprising result, since phylogenetic logistic models indicate that the probability of gaining the ability to sequester alkaloids or going from a cryptic to aposematic phenotype is considerably higher than that of a reversion (Santos et al. 2014). However, this hypothesis has the robustness conferred by the Goodman-Bremer values and the YBIRÁ procedure that tests the stability of the nodes through the removal of clades or "wildcard" terminals (Grant and Kluge 2008; Machado 2015). Although our objective is far from evaluating whether the phylogenetic relationships of group “C.” ruthveni proposed by Grant et al. (2017) are plausible or not, according to the new evidence, we believe that the sampling and refinement of certain characters could provide greater clarity about the relationships. First, whether group “C.” ruthveni shares the synapomorphic status of the Dendrobatinae subfamily [160(1); the ability to sequester lipophilic alkaloids present] should be examined. But we detected that at least 27 characters (Supplementary Table 5) were declared as a mixture of neomorphic and transformational characters. This character set includes the three synapomorphies of the clade group “C.” ruthveni + Dendrobatini (characters 71, 72 and 156). Although the declarations of these characters undoubtedly follow a logical sequence (Sereno 2007), examining the appearance/loss and the transformation of the states in the same character is inappropriate because it violates the precept of the independence of characters. Including these considerations and the additional characters presented here could at best reinforce the Grant et al. (2017) hypothesis or perhaps a different perspective of the relationships of the group “C.” ruthveni and even Dendrobatoidea.

Even considering these aspects of Grant et al. (2017) on the relationships of Dendrobatoidea, this is the most comprehensive and complete approach on the topic and on it we will base our hypotheses on the evolution of larval and reproductive characters. In general terms, the larval morphology of Dendrobatoidea is conservative, where there is a generalized ancestral morphological pattern symplesiomorphically shared by Aromobatidae, Colostethinae, Hyloxalinae, and some members of Dendrobatinae such as Phyllobates and the group “C” ruthveni (Sánchez 2013). Compiling the data obtained by (Sánchez 2013), Grant et al. (2017) and this study, this ancestral body plane can be characterized with the caudal coloration of the tadpole with scattered melanophores scattered melanophores clumped to form diffuse blotches [93(1)], the presence of a notch in the upper jaw sheath [103(0)], the anal tube in dextral position [104 (0)], the long gut concealing other organs [107 (0)], and the presence of a projection of the external sagittal edge of the nostril [108 (1)]. Although the larval characters of “C.” ruthveni mostly correspond to a compendium of symplesiomorphies, some provide an interesting perspective. The caudal coloration in “C.” ruthveni as clusters of melanophores forming diffuse spots [93(1)] corresponds to the loss of an acquired novelty in the Dendrobatinae subfamily clade [93(2)]. Both this reversal and the presence of lateral line stitches [106 (1)] could constitute a synapomorphy of the “C” ruthveni synapomorphies if they are shown to be present in the undescribed members of the complex. Likewise, the presence of lateral line stitches could constitute a synapomorphy of the clade group “C.” ruthveni + Dendrobatini, if the presence of this character state is demonstrated in Minyobates steyermarki (Rivero, 1971). The A2-gap/ODW ratio also proved to be valuable for the diagnosis of the genera, despite the strong intrageneric variation detected. Intergeneric variation in A2-gap width in the phylogenetic context of Grant et al. (2017) suggests that narrow to moderate gaps could be the ancestral condition and that moderate to wide gaps evolved independently in Allobates, Amereega, Epipedobates, a species of Hyloxalus and the subfamily Dendrobatinae. In that sense, the presence of a narrow A2-gap in “C.” ruthveni could be a reversal, and a synapomorphy if its presence is verified in the other members of the group.

Of the reproductive characters, the occurrence of amplexus [115(1)] and of cephalic grasping [116(1)] is quite informative. For decades, cephalic amplexus was considered to be a Dendrobatoid synapomorphy with multiple subsequent losses (Myers et al. 1991) (Myers et al. 1991). However, from total evidence-based phylogenies, Grant et al. (2006) noted that cephalic amplexus has arisen in three independent lineages within the clade (Anomaloglossus beebei Noble 1923, Colosthethinae, and M. steyermarki). Nevertheless, the occurrence of this character is known to be much more widely distributed throughout the Dendrobatoidea, being present in some Anomaloglossus, Allobates, Colostethinae, Paruwrobates, Hyloxalus and the group “C” ruthveni (Myers et al. 1978; Wells 1980c; Myers and Burrowes 1987; Jungfer 1989; Roithmair 1994; Grant and Castro 1998; Juncá 1998; Bourne et al. 2001; Quiguango-Ubillús and Coloma 2008; Castillo-Trenn and Coloma 2008; Lima et al. 2010; Magrini et al. 2010; Montanarin et al. 2011; Forti et al. 2013; Grant et al. 2017 [see Supplementary Material S4]; Rocha et al. 2018; Carvajal-Castro et al. 2020; Souza et al. 2020). So far, this is the only member of the Dendrobatinae subfamily that still retains some form of amplexus, as Myers (1987) observations on M. steyermarki may be related to aggressive behavior, i.e., possible male-fighting (López-López et al. 2016) and for this reason it must be verified (Castillo-Trenn and Coloma 2008). All the above suggests that the larval and reproductive characters are a good source of information to understand the relationship between the genera of Dendrobatoidea, and that also some characteristics such as free-swimming tadpoles with a lateral line and a narrow A-2 gap, as well as the occurrence of cephalic amplexus are useful to diagnose the group “C.” ruthveni.

Acknowledgements

We are grateful to Juan Manuel Renjifo, Sigmer Quiroga, Paula Sepúlveda, Adolfo Amézquita for their support during the development of this research. Special mentions to Marvin Anganoy Criollo for his comments on the early stages of document. Thanks to Elkin Hernández and the Parque Nacional Natural Taytona for link this research to their research portfolio. Thanks to Ángel Moreno, Rubén Moreno, Wilman Moreno, Yuli Castro, Efraín Rada, Orlando Linares, Erika Linares, and Cesar Linares for their support during the field trips. Many thanks to Roberto Guerrero (CBUMAG) and the Entomology Laboratory of the Universidad del Magdalena for providing us with the specimens and the necessary elements for their examination. We are grateful to Jhulyana López-Caro for her illustrations. Finally, thanks to Thomas Defler for translation and Orlando J. Ayos Oñate for his comments on the final document.

Funding. This research was financed by own resources of the authors.

Conflicts of interest. The authors declare no conflicts of interest.

Ethics approval. Since this study did not require the direct manipulation of live animals, it was not submitted to the ethics committee of the Universidad del Magdalena.

Consent to participate. Not applicable

Consent for publication. Not applicable

Availability of data and material. All relevant raw data are available in supplementary materials

Code availability. Not applicable

Authors' contributions. The description of the larval morphology and the reproductive strategies of this research were part of the undergraduate project of FPC and KLV to obtain their degree as biologists at the University of Magdalena, which was advised by LSA. ACMC, JDJB and HDGR were later added to the project. Field data were collected by all authors. Data from collection specimens were obtained by FPC and KLV. Processing of field data was performed by ACMC and HDGR. Literature review of larval and reproductive characters of Dendrobatoidea genera was conduct by FPC y ACMC. ACMC carried out all analyzes related to the mapping of larval and reproductive characters on the topology of the phylogenetic relationships of the Dendrobatoidea genera. The first version of the manuscript was written by FPC, ACMC, and HDGR. All authors participated in writing the final version. Figures were designed and assembled by ACMC and JDJB. Tables and supplementary material was performed by ACMC. FPC and ACMC edited the final version of the manuscript, which was approved by all the authors.

Almendáriz C A, Ron SR, Brito M J (2012) Una especie nueva de rana venenosa de altura del género Excidobates (Dendrobatoidea: Dendrobatidae) de la Cordillera del Cóndor. Pap Avulsos Zool 52:387–399.
Altig R, McDiarmid RW (1999) Body Plan. Development and Morphology. In: McDiarmid RW, Altig R (eds) Tadpoles. The Biology of Anuran Larvae. The University of Chicago Press, Chicago, USA, Chicago, USA, pp 24–51.
Anganoy-Criollo M (2012) A new species of Allobates (Anura, dendrobatidae) from the western Flank of the Serranía de Perijá, Colombia. Zootaxa 3308:49–62.
Anganoy-Criollo M (2013) Tadpoles of the High-Andean Hyloxalus subpunctatus (Anura:Dendrobatidae) with description of larval variation and species distinction by larval morphology. Pap Avulsos Zool 53:211–224.
Anganoy-Criollo M, Cepeda-Quilindo B (2017) Redescription of the tadpoles of Epipedobates narinensis and E. boulengeri (Anura: Dendrobatidae). Phyllomedusa 16:155–182.
Barboza FR (2014) Retomando el concepto de plasticidad fenotípica en el estudio de los modos reproductivos de anfibios anuros. Bol. Soc. Zool. Uruguay 23:1–14.
Beirne C, Whitworth A (2011) Frogs of the Yachana Reserve. Global Vision International, United Kingdom.
Blanco-Torres A, Navarro-Gutierrez K, Gutierrez-Moreno LC (2013) Colostethus inguinalis (Common Rocket Frog) diet. Herpetol Rev 44:493–494.
Blanco-Torres A, Ordónez-Pachón MP, Franco-Rozo MC (2014) Colostethus ruthveni (Santa Marta poison arrow frog) diet. Herpetol Rev 45:476.
Bourne GR, Collins AC, Holder AM, Mccarthy CL (2001) Vocal communication and reproductive behavior of the frog Colostethus beebei in Guyana. J Herpetol 35:272–281.
Breder CM (1946) Amphibians and Reptiles of the Rio Chucunaque drainage, Darien, Panama, with notes on their life histories and habitats. Bull Am Museum Nat Hist 86:375–346.
Brown JL, Morales V, Summers K (2008) Divergence in parental care, habitat selection and larval life history between two species of Peruvian poison frogs: An experimental analysis. J Evol Biol 21:1534–1543.
Brown JL, Siu-Ting K, von May R, et al (2019) Systematics of the Ameerega rubriventris complex (Anura: Dendrobatidae) with descriptions of two new cryptic species from the East-Andean versant of Peru. Zootaxa 4712:211–235.
Caldwell JP (2005) A new Amazonian species of Cryptophyllobates (Anura:Dendrobatidae). Herpetologica 61:449–461.
Caldwell JP, Myers CW (1990) A new poison frog from Amazonian Brazil, with further revision of the quinquevittatus group of Dendrobates. Am Museum Novit 2988:1–21.
Caldwell JP, Lima AP (2003) A new amazonian species of Colostethus (Anura: Dendrobatidae) with a nidicolous tadpole. Herpetologica 59:219–234.
Caldwell JP, Lima AP, Biavati GM (2002) Descriptions of tadpoles of Colostethus marchesianus and Colostethus caeruleodactylus (Anura: Dendrobatidae) from their type localities. Copeia 2002:166–172.
Carvajal-Castro JD, López-Aguirre Y, Ospina-L AM, et al (2020) Much more than a clasp: Evolutionary patterns of amplexus diversity in anurans. Biol J Linn Soc 129:652–663.
Carvajalino-Slaghekke A (2015) Territorio e identidad en la Sierra Nevada de Santa Marta (Colombia) Territory. Rev Lat Sociol 8:94–112.
Castillo-Trenn P (2004) Description of the tadpole of Colostethus kingsburyi (Anura: Dendrobatidae) from Ecuador. J Herpetol 38:600–606.
Castillo-Trenn P, Coloma LA (2008) Notes on behaviour and reproduction in captive Allobates kingsburyi (Anura: Dendrobatidae), with comments on evolution of reproductive amplexus. Int Zoo Yearb 42:58–70.
Coloma LA (1995) Ecuadorian frogs of the genus Colostethus (Anura:Dendrobatidae). Univ Kans Nat Hist Mus 87:1-82.
Costa RC, Facure KG, Giaretta AA (2006) Courtship, vocalization, and tadpole description of Epipedobates flavopictus (Anura: Dendrobatidae) in southern Goiás, Brazil. Biota Neotrop 6:1
Crump ML (2015) Anuran reproductive modes: Evolving perspectives. J Herpetol 49:1–16.
Crump ML, Scott NJJ (1994) Visual Encounter Survey. In: Heyer WR, Donelly MA, McDiarmid RW, et al. (eds) Measuring and Monitoring Biological Diversity. Standar Methods for Amphibians. Smithsonian Institution Press, Washington D.C, Washington D.C, pp 84–91
Dias PHDS, Anganoy-Criollo M, Guayasamin JM, Grant T (2018a) The tadpole of Epipedobates darwinwallacei Cisneros-Heredia and Yánez-Muñoz, 2011 (Dendrobatidae: Colostethinae), with new synapomorphies for Epipedobates. South Am J Herpetol 13:54–63.
Dias PHDS, Brandão AP, Grant T (2018b) The buccopharyngeal morphology of the tadpole of Ameerega flavopicta (Anura: Dendrobatidae: Colostethinae), with a redescription of its external morphology. Herpetologica 74:323–328.
Dias PH dos S, Anganoy-Criollo M, Rada M, Grant T (2021) The tadpoles of the funnel-mouthed dendrobatids (Anura: Dendrobatidae: Colostethinae: Silverstoneia): external morphology, musculoskeletal anatomy, buccopharyngeal cavity, and new synapomorphies. J Zool Syst Evol Res 59:691–717
Dole JW, Durant P (1974) Courtship Behavior in Colostethus collaris (Dendrobatidae). Copeia 1974:988–990
Donnelly MA, Guyer C, de Sá RO (1990) The tadpole of a dart-poison frog Phyllobates lugubris (Anura: Dendrobatidae). Proc Biol Soc Washingt 103:427–431
Duarte-Marín S, González-Acosta CC, Dias PHDS, et al (2020) Advertisement call, tadpole morphology, and other natural history aspects of the threatened poison frog Andinobates daleswansoni (Dendrobatidae). J Nat Hist 54:3005–3030.
Duellman WE (1966) Aggressive Behavior in Dendrobatid Frogs. Herpetologica 22:217–221.
Duellman WE (2004) Frogs of the genus Colostethus (Anura; Dendrobatidae) in the Andes of Northern Peru. Sci Pap - Nat Hist Museum, Univ Kansas 35:1–49.
Duellman WE, Trueb L (1994) Biology of Amphibians. Baltimore and London.
Edwards SR (1971) Taxonomic notes on South American Colostethus with descriptions of two new species (Amphibia, Dendrobatidae). Proc Biol Soc Washingt 84:147–162.
Edwards SR (1974) Taxonomic notes on South American dendrobatid frogs of the genus Colostethus. Occas Pap Museum Nat Hist Univ Kansas 30:1–14.
Flechas S V., Paz A, Crawford AJ, et al (2017) Current and predicted distribution of the pathogenic fungus Batrachochytrium dendrobatidis in Colombia, a hotspot of amphibian biodiversity. Biotropica 49:685–694.
Forti LR, Mott T, Strüssmann C (2013) Breeding biology of Ameerega braccata (Steindachner, 1864) (Anura: Dendrobatidae) in the Cerrado of Brazil. J Nat Hist 47:2363–2371.
Fouquet A, Vacher JP, Courtois EA, et al (2019) A new species of Anomaloglossus (Anura: Aromobatidae) of the stepheni group with the redescription of A. baeobatrachus (Boistel and de Massary, 1999), and an amended definition of A. leopardus Ouboter and Jairam, 2012. Zootaxa 4576:439–460.
French CM, Burkette C, Reichle S, Brown JL (2019) The tadpole of Ameerega boehmei in southeastern Bolivia. Zootaxa 4661:197–200.
Frost DR (2023) Amphibian Species of the World: an Online Reference. Version 6.2. In: Am. Museum Nat. Hist. New York, USA. Available: http://research.amnh.org/herpetology/amphibia/ index.html. (Accessed: 25 May 2023).
Fundación Pro-Sierra Nevada (1998) Evaluación Ecológica Rápida. Definición de áreas críticas para la conservación en la Sierra Nevada de Santa Marta. Santa Marta, Magdalena. Pp 1-134, Santa Marta, Magdalena.
González-Maya JF, González M, Zárrate-Charry D, et al (2011) A new population record and conservation assessment of the Santa Marta Poison Arrow Frog Colostethus ruthveni Kaplan, 1997 (Anura: Dendrobatidae) from Sierra Nevada de Santa Marta, Colombia. J Threat Taxa 3:1633–1636.
Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190.
Granda–Rodríguez HD, Montes-Correa AC, Jiménez-Bolaño JD, Anganoy-Criollo M (2018) Natural history and conservation of the Nurse Frog of the Serranía del Perijá Allobates ignotus (Dendrobatoidea: Aromobatidae) in northeastern Colombia. Acta Herpetol 13:51–64.
Granda-Rodríguez HD, Montes-Correa AC, Jiménez-Bolaño JD, et al (2020) Insights into the natural history of the endemic Harlequin Toad, Atelopus laetissimus Ruiz-Carranza, Ardila-Robayo and Hernández-Camacho, 1994 (Anura: Bufonidae), in the Sierra Nevada de Santa Marta, Colombia. Amphib Reptile Conserv 14:29–42.
Granda-Rodríguez HD, Montes-Correa AC, Jiménez-Bolaño JD, Anganoy-Criollo M (2018) Natural history and conservation of the Nurse Frog of the Serranía del Perijá Allobates ignotus (Dendrobatoidea: Aromobatidae) in northeastern Colombia. Acta Herpetol 13:51–64.
Granda-Rodríguez HD, Saboyá-Acosta LP, del Portillo-Mozo A, Renjifo JM (2014) Range extension of dendrobatid frog Colostethus ruthveni Kaplan, 1997 (Anura: Dendrobatidae) in the Sierra Nevada de Santa Marta, Colombia. Check List 10:674–676.
Granda-Rodriguez HD, Mozo A, Renjifo JM, Bolaños F (2012) ¿Están declinando todos los Atelopus de alta montaña? el caso de las ranas arlequín de la Sierra Nevada de Santa Marta, Colombia. Herpetotropicos 7:21–30.
Grant T (1998) Una nueva especie de Colostethus del grupo edwardisi de Colombia. Rev la Acad Colomb Ciencias Exactas, Fis y Nat 22:423–428.
Grant T, Castro F (1998) The cloud forest Colostethus (Anura, Dendrobatidae) of a region of the Cordillera Occidental of Colombia. J Herpetol 32:378–392.
Grant T, Frost DR, Caldwell JP, et al (2006) Phylogenetic systematics of dart-poison frogs and their relatives (Amphibia: Athesphatanura: Dendrobatidae). Bull Am Museum Nat Hist 299:1–262.
Grant T, Acosta A, Rada M (2007) A name for the species of Allobates (Anura: Dendrobatoidea: Aromobatidae) from the Magdalena Valley of Colombia. Copeia 2007:844–854.
Grant T, Kluge AG (2008) Clade support measures and their adequacy. Cladistics 24:1051–1064.
Grant T, Rada M, Anganoy-criollo M, et al (2017) Phylogenetic Systematics of Dart-Poison Frogs and Their Relatives Revisited (Anura: Dendrobatoidea). South Am J Herpetol 12:S1–S90.
Guardiola A del R (2019) Potencial turístico de Santa Marta (Colombia): Una revisión de su desarrollo, crecimiento y barreras. Espacios 40:22.
Haddad CFB, Prado CPA (2005) Reproductive modes in frogs and their unexpected diversity in the Atlantic forest of Brazil. Bioscience 55:207–217.
Hill RL, Kaylock JB, Gagliardo RW, et al (2011) Observations on the captive reproduction of Colostethus pratti (Boulenger, 1899). Herpetol Rev 42:365–367.
Hödl W, Amézquita A (2001) Visual signaling in anuran amphibians. In: Ryan MJ (ed) Anuran Communication. Smithsonian Institution Press, Washington D.C, Washington D.C, pp 121–141.
Inger RF (1994) Distribution of Microhabitat. In: Heyer RW, Donelly MA, Mcdiarmid RW, et al. (eds) Measuring and monitoring biological diversity standard methods for amphibians. Smithsonian Institution Press, Washington D.C, pp 60–66.
IUCN SSC Amphibian Specialist Group (2018) Colostethus ruthveni. https://www.iucnredlist.org/species/55144/85891000. (Accessed 7 Jun 2023).
Jiménez-Bolaño JD, Montes-Correa AC, Polo-Córdoba F, et al (2019) Acoustic repertory of the “Colostethus” ruthveni group (Anura: Dendrobatidae) and comments on the distribution in the sierra nevada de Santa Marta, Colombia. Salamandra 55:27–38.
Juncá FA (1998) Reproductive biology of Colostethus stepheni and Colostethus marchesianus (Dendrobatidae), with the description of a new anuran mating behavior. Herpetologica 54:377–387.
Junca FA, Altig R, Gascon C (1994) Breeding biology of Colostethus stepheni, a dendrobatid frog with a nontransported nidicolous tadpole. Copeia 1994:747–750.
Juncá FA, Rodrigues MT (2006) The reproductive sucess of Colostethus stepheni (Anura:Dendrobatidae). Stud Neotrop Fauna Environ 41:9–17.
Jungfer K (1989) Pfeilgiftfrösche der Gattung Epipedobates mit rot granuliertem Rücken aus dem Oriente von Ecuador und Peru. Salamandra 25:81–98.
Kaplan M (1997) A new species of Colostethus from the Sierra Nevada de Santa Marta (Colombia) with comments on intergeneric relationships within the Dendrobatidae. J Herpetol 31:369–375.
Klein B, Regnet RA, Krings M, Rödder D (2020) Larval development and morphology of six Neotropical poison-dart frogs of the genus Ranitomeya (Anura:Dendrobatidae) based on captive-raised specimens. Bonn Zool Bull 69:191–223.
Kok PJR, MacCulloch RD, Gaucher P, et al (2006a) A new species of Colostethus (Anura, Dendrobatidae) from French Guiana with a redescription of Colostethus beebei (Noble, 1923) from its type locality. Phyllomedusa 5:43–66
Kok PJR, Sambhu H, Roopsind I, et al (2006b) A new species of Colostethus (Anura: Dendrobatidae) with maternal care from Kaieteur National Park, Guyana. Zootaxa 1238:35–61.
Kok PJR, MacCulloch RD, Lathrop A, et al (2010) A new species of Anomaloglossus (Anura: Aromobatidae) from the Pakaraima Mountains of Guyana. Zootaxa 2660:18–32
Kok PJR, Willaert B, Means DB (2013) A new diagnosis and description of Anomaloglossus roraima (La Marca, 1998) (Anura: Aromobatidae: Anomaloglossinae), with description of its tadpole and call. South Am J Herpetol 8:29–45.
La Marca E (1985) A new species of Colostethus (Anura:Dendrobatidae) from the Cordillera de Merida, Northern Andes, South America. Occas Pap Museum Zool Univ Michigan 710:1–10.
La Marca E (1989) A new species of collared frog (Anura: Dendrobatidae: Colostethus) from Serrania de Portuguesa, Andes of Estado Lara, Venezuela. Amphibia-Reptilia 10:175–183.
La Marca E (1993) Phylogenetic relationships and taxonomy of Colostethus mandelorum (Anura:Dendrobatidae), with notes on coloration, natural history, and description of the tadpole. Bull Maryl Herpetol Soc 29:4–19.
La Marca E (1994) Taxonomy of the frogs of the genus Mannophryne (Amphibia; Anura; Dendrobatidae). Publicaciones la Asoc Amigos Doñana 4:1–75.
La Marca E, Mijares-Urrutia A (1988) Description of the tadpole of Colostethus mayorgai (Anura:Dendrobatidae) with preliminary data on reproductive biology of the species. Bull Maryl Herpetol Soc 24:47–57
Lehtinen RM, Halley A (2008) A description of the tadpole of Mannophryne olmonae (Anura:Aromobatidae). Caribb J Sci 44:260–264.
Lescure J (1976) Étude de deux Têtards de Phyllobates (Dendrobatidae): P. femoralis (Boulenger) et P. pictus (Bibron). Bull la Société Zool Fr 101:299–306
Lima AP, Keller C (2003) Reproductive characteristics of Colostethus marchesianus from its type locality in Amazonas, Brazil. J Herpetol 37:754–757.
Lima AP, Caldwell JP, Biavati GM (2002) Territorial and reproductive behavior of an Amazonian dendrobatid frog, Colostethus caeruleodactylus. Copeia 2002:44–51.
Lima AP, Sanchez DEA, Souza JRD (2007) A new amazonian species of the frog genus Colostethus (Dendrobatidae) that lays its eggs on undersides of leaves. Copeia 2007:114–122.
Lima AP, Caldwell JP, Strussmann C (2009) Redescription of Allobates brunneus (Cope) 1887 (Anura: Aromobatidae: Allobatinae), with a description of the tadpole, call, and reproductive behavior. Zootaxa 1988:1–16.
Lima AP, Caldwell JP, Biavati G, Montanarin A (2010) A new species of Allobates (Anura: Aromobatidae) from Paleovárzea Forest in Amazonas, Brazil. Zootaxa 2337:1–17.
Lima AP, Simões PI, Kaefer IL (2014) A new species of Allobates (Anura: Aromobatidae) from the Tapajós River basin, Pará State, Brazil. Zootaxa 3889:355–387.
Lima AP, Simões PI, Kaefer IL (2015) A new species of Allobates (Anura: Aromobatidae) from Parque Nacional da Amazônia, Pará State, Brazil. Zootaxa 3980:501–525.
López-López FJ, Rada M, Kahn TR (2016) La Planada Poison Frog Amereega andina (Myers and Burrowes 1987). In: Kahn TR, La Marca E, Lötters S, et al. (eds) Aposematic poison frogs (Dendrobatidae) of the Andean countries: Bolívia, Colombia, Perú, and Venezuela. Conservation International, Tropical Fields Guides Series., Arlington, USA., pp 116–120
Lüddecke H (1976) Einige Ergebnisse aus Feldbeobachtungen an Phyllobates palmatus (Amphibia, Ranidae) in Kolumbien. Mitteilungen Aus Dem Inst Colombo Alemán Investig Científicas 8:157–163.
Lüddecke H (1999) Behaviral aspects of the reproductive biology of the Andean frog Colostethus palmatus (Amphibia:Dendrobatidae). Rev Acad Colomb Cienc 23:303–316.
Lynch JD (1982) Two new species of Poison-Dart Frogs (Colostethus) from Colombia. Herpetologica 38:366–374.
Machado DJ (2015) YBYRÁ facilitates comparison of large phylogenetic trees. BMC Bioinformatics 16:2–5.
MacKenzie DI, Nichols JD, Lachman GB, et al (2002) Estimating site occupancy rates when detection probabilities are less than one. Ecology 83:2248–2255.
Magrini L, Facure KG, Giaretta AA, et al (2010) Geographic call variation and further notes on habitat of Ameerega flavopicta (Anura, Dendrobatidae). Stud Neotrop Fauna Environ 45:89–94.
Manjarrés-Garcia G, Manjarrés-Pinzón G (2004) Contribución al conocimiento hidrobiológico de la parte baja de los rios de la vertiente noroccidental de la Sierra Nevada de Santa Marta, Colombia. Rev Intropica 1:39–50.
Marin CM, Molina-Zuluaga C, Restrepo A, et al (2018) A new species of Leucostethus (Anura: Dendrobatidae) from the eastern versant of the Central Cordillera of Colombia and the phylogenetic status of Colostethus fraterdanieli. Zootaxa 4461:359–380.
Martinez-Baños V, Pacheco V, Ramírez-Pinilla MP (2011) Abundancia relativa y uso de microhábitat de la rana Geobatrachus walkeri (Anura: Strabomantidae) en dos hábitats en Sierra Nevada de Santa Marta, Colombia. Rev Biol Trop 59:907–920.
Masche S, Zimmermann H, Pröhl H (2010) Description and ecological observations of the tadpole of Ranitomeya variabilis (Anura: Dendrobatidae). South Am J Herpetol 5:207–211.
Menin M, Pinto RMC, Pegorini RJ, Silva MR Da (2017) Redescription of the tadpole of Ameerega hahneli (Boulenger, 1884) (Anura: Dendrobatidae) with notes on ontogenetic variations and development habitats. South Am J Herpetol 12:236–243.
Meza-Joya FL, Chinchilla-Lemus W, Ramos E, et al (2019) New and noteworthy locality records of anurans from northeastern Andes of Colombia. Herpetol Notes 12:61–69.
Mijares-Urrutia A (1991) Descripcion del renacuajo de Colostethus leopardalis Rivero con algunos comentarios sobre su historia natural. Amphibia-Reptilia 12:145–152
Mijares-Urrutia A, La Marca E (1997) Tadpoles of the genus Nephelobates La Marca 1994 (Amphibia Anura Dendrobatidae), from Venezuela. Trop Zool 10:133–142.
Montanarin A, Kaefer IL, Lima AP (2011) Courtship and mating behaviour of the brilliant-thighed frog Allobates femoralis from Central Amazonia: Implications for the study of a species complex. Ethol Ecol Evol 23:141–150.
Moraes LJC de L, Pavan D, Lima AP (2019) A new nurse frog of Allobates masniger-nidicola complex (Anura, Aromobatidae) from the east bank of Tapajós River, eastern Amazonia. Zootaxa 4648:401–434.
Moreno-Arias RA, Medina-Rangel GF, Carvajal-Cogollo JE, Castaño-Mora O V (2009) Herpetofauna De La Serranía De Perijá. In: Rangel-Ch JO (ed) Colombia Diversidad Biótica VIII: La alta montaña de la Serranía del Perijá, Colombia. Instituto de Ciencias Naturales-Universidad Nacional de Colombia - CORPOCESAR, Bogotá D.C, Colombia, pp 449–470.
Myers CW (1987) New generic names for some neotropical poison frogs (Dendrobatidae). Pap Avulsos Zool 36:301–306.
Myers CW, Burrowes PA (1987) A new poison frog (Dendrobates) from Andean Colombia, with notes on a lowland relative. Am Museum Novit 2899:1–17.
Myers CW, Donnelly MA (1997) A Tepui herpetofauna on a granitic mountain (Tamacuari) in the borderland between Venezuela and Brazil : Report from the Phipps Tapirapecó Expedition. Am Museum Novit 3213:1–71.
Myers CW, Donnelly MA (2001) Herpetofauna of the Yutajé-Corocoro massif, Venezuela: Second report from the Robert G. Goelet American Museum–Terramar Expedition to the Northwestern Tepuis. Bull Am Museum Nat Hist 261:1–85.
Myers CW, Daly JW, Malkin B (1978) A dangerously toxic new frog (Phyllobates) used by Emberá indians of western Colombia, with discussion of blowgun fabrication and dart poisoning. Bull Am Museum Nat Hist 161:307–366.
Myers CW, Daly JW, Martinez V (1984) An arboreal poison frog (Dendrobates) from Western Panama. Am Museum Novit 2783:1–20.
Myers CW, Paolillo O A, Daly JW (1991) Discovery of a defensively malodorous and nocturnal frog in the family Dendrobatidae: Phylogenetic significance of a new genus and species from the Venezuelan Andes. Am Museum Novit 3002:1–33.
Nunes-De-Almeida CHL, Haddad CFB, Toledo LF (2021) A revised classification of the amphibian reproductive modes. Salamandra 57:413–427.
Páez-Vacas MI, Coloma LA, Santos JC (2010) Systematics of the Hyloxalus bocagei complex (Anura: Dendrobatidae), description of two new cryptic species, and recognition of H. maculosus. Zootaxa 2711:1–75.
Perez-Peña PE, Chavez G, Twomey E, Brown JL (2010) Two nw species of Ranitomeya (Anura: Dendrobatidae) from eastern Amazonian Peru. Zootaxa 2439:1–23.
Pezzuti TL, Araújo RB, Sanches PR, et al (2022) The tadpole of the endemic poison frog Ameerega pulchripecta (Silverstone, 1976) with the description of its chondrocranium (Anura: Dendrobatidae: Colostethinae). Zootaxa 5115:295–300.
Poelman EH, Verkade JC, Van Wijngaarden RPA, Félix-Novoa C (2010) Descriptions of the tadpoles of two poison frogs, Ameerega parvula and Ameerega bilinguis (Anura: Dendrobatidae) from Ecuador. J Herpetol 44:409–417.
Posso-Peláez C, Blanco-Torres A, Gutierrez-Moreno LC (2017) Uso de microhábitats, actividad diaria y dieta de Dendrobates truncatus (Cope, 1861) (Anura: Dendrobatidae) en bosque seco tropical del norte de Colombia. Acta Zoológica Mex 33:490–502.
Quiguango-Ubillús A, Coloma LA (2008) Notes on behaviour, communication and reproduction in captive Hyloxalus toachi (Anura: Dendrobatidae), an endangered Ecuadorian frog. Int Zoo Yearb 42:78–89.
Roach NS, Acosta D, Lacher TE (2021) Shade coffee and amphibian conservation, a sustainable way forward? Understanding the perceptions and management strategies of coffee growers in colombia. Ecol Soc 26:33.
Rocha SMC, Lima AP, Kaefer IL (2018) Reproductive behavior of the Amazonian nurse-frog Allobates paleovarzensis (dendrobatoidea, aromobatidae). South Am J Herpetol 13:260–270.
Rodriguez L, Myers CW (1993) A new poison frog from Manu National Park, Southeastern Peru (Dendrobatidae, Epipedobates). Am Museum Novit 3068:1–16.
Roithmair ME (1994) Field studies of reproductive behaviour in two dart-poison frog species (Epipedobates femoralis, Epipedobates trivittatus) in Amazonian Peru. Herpetol J 4:77–85.
Rojas-Morales JA, La Marca E, Ramírez-Chaves HE (2021) Advertisement call of a population of the nurse frog Leucostethus fraterdanieli (Anura: Dendrobatidae), with notes on its natural history. Biota Colomb 22:122–132.
Rojas B, Pašukonis A (2019) From habitat use to social behavior: Natural history of a voiceless poison frog, Dendrobates tinctorius. PeerJ 7:1–30.
Romero-Martinez HJ, Lynch JD (2012) Anfibios de la Región Caribe. In: Rangel-Ch JO (ed) Colombia Diversidad Biótica XII. La Región Caribe de Colombia. Instituto de Ciencias Naturales-Universidad Nacional de Colombia, Bogotá D.C, Bogotá D.C, Colombia, pp 677–701.
Ruiz-Carranza P, Ramirez-Pinilla MP (1992) Una nueva especie de Minyobates (Anura:Dendrobatidae ) de Colombia. Lozania 61:1–16.
Ruthven AG, Gaige HT (1915) The breeding habitats of Prostherapis subpunctatus Cope. Occas Pap Museum Zool - Univ Michigan 11:1–7.
Sánchez DA (2010) Larval development and synapomorphies for species groups of Hyloscirtus Peters, 1882 (Anura: Hylidae: Cophomantini). Copeia 351–363.
Sánchez DA (2013) Larval morphology of Dart-Poison Frogs (Anura:Dendrobatoidea: Aromobatidae and Dendrobatidae). Zootaxa 3637:569–591
Santos JC, Baquero M, Barrio-Amorós C, et al (2014) Aposematism increases acoustic diversification and speciation in poison frogs. Proc R Soc B Biol Sci 281:.
Santos JC, Coloma LA, Summers K, et al (2009) Amazonian amphibian diversity is primarily derived from late Miocene Andean lineages. PLoS Biol 7:0448–0461.
Savage JM (1968) The Dendrobatid frogs of Central America. Copeia 1968:745–776.
Savage JM (2002) The Amphibians and Reptiles of Costa Rica: A Herpetofauna between two continents, between two seas. The University of Chicago Press, Ltd., Chicago and London.
Schulte R (1990) Redescubrimiento y redefinición de Dendrobates mysteriosus (Myers 1982) de la Cordillera del Cóndor. Bol Lima 70:57–68.
Schulze A, Jansen M, Köhler G (2015) Tadpole diversity of Bolivia’s lowland anuran communities: molecular identification, morphological characterisation, and ecological assignment. Zootaxa 4016:1–111.
Sereno PC (2007) Logical basis for morphological characters in phylogenetics. Cladistics 23:565–587.
Serrano-Rojas SJ, Whitworth A, Villacampa J, et al (2017) A new species of poison-dart frog (Anura: Dendrobatidae) from Manu Province, Amazon region of southeastern Peru, with notes on its natural history, bioacoustics, phylogenetics, and recommended conservation status. Zootaxa 4221:71–94.
Silverstone PA (1973) Observations on the Behavior and Ecology of a Colombian Poison-Arrow Frog, the Kokoe-Pa (Dendrobates histrionicus Berthold). Herpetologica 29:295–301.
Silverstone PA (1975) Two new species of Colostethus (Amphibia:Anura:Dendrobatidae) from Colombia. Nat Hist Museum Los Angeles Cty - Contrib Sci 268:1–10.
Simões PI, Lima AP (2012) The tadpole of Allobates sumtuosus (Morales, “2000” 2002) (Anura: Aromobatidae) from its type locality at Reserva Biológica do Rio Trombetas, Pará, Brazil. Zootaxa 3499:86–88.
Simões PI, Lima AP, Farias IP (2010) The description of a cryptic species related to the pan-Amazonian frog Allobates femoralis (Boulenger 1883) (Anura: Aromobatidae). Zootaxa 2406:1–28.
Simões PI, Sturaro MJ, Peloso PLV, Lima AP (2013) A new diminutive species of Allobates Zimmermann and Zimmermann, 1988 (Anura, Aromobatidae) from the northwestern Rio Madeira - Rio Tapajós interfluve, Amazonas, Brazil. Zootaxa 3609:251–273.
Simões PI, Rojas D, Lima AP (2019) A name for the nurse-frog (Allobates, Aromobatidae) of Floresta Nacional de Carajás, Eastern Brazilian Amazonia. Zootaxa 4550:71–100.
Sloggett JJ, Zeilstra I (2008) Waving or tapping? Vibrational stimuli and the general function of toe twitching in frogs and toads (Amphibia: Anura). Anim Behav 76:1–4.
Souza JRD, Ferrão M, Hanken J, Lima AP (2020) A new nurse frog (Anura: Allobates) from Brazilian Amazonia with a remarkably fast multi-noted advertisement call. PeerJ 8:1–31.
Souza JRD, Kaefer IL, Lima AP (2017) The peculiar breeding biology of the amazonian frog Allobates subfolionidificans (Aromobatidae). An Acad Bras Cienc 89:885–893.
Suarez-Mayorga AM, Lynch JD (2001) Redescripction of the Tadpole of Hyla vigilans (Anura:Hylidae) and notes about possible taxonomic relationships. Caribb J Sci 37:116–119.
Summers K (1992) Mating strategies in two species of dart-poison frogs: a comparative study. Anim Behav 43:907–919.
Summers K, Tumulty J (2014) Parental Care, Sexual Selection, and Mating Systems in Neotropical Poison Frogs. In: Macedo RH, Machado G (eds) Sexual Selection: Perspectives and Models from the Neotropics. Academic Press, Elsevier, Oxford, United Kingdom, Oxford, United Kingdom, pp 289–320.
Touchon JC, Warkentin KM (2008) Reproductive mode plasticity: Aquatic and terrestrial oviposition in a treefrog. Proc Natl Acad Sci U S A 105:7495–7499.
Twomey E, Brown JL (2008) Spotted poison frogs: Rediscovery of a lost species and a new genus (Anura: Dendrobatidae) from Northwestern Peru. Herpetologica 64:121–137.
Twomey E, Brown JL (2009) Another new species of Ranitomeya (Anura: Dendrobatidae) from Amazonian Colombia. Zootaxa 2302:48–60.
van Wijngaarden R, Bolaños F (1992) Parental Care in Dendrobates granuliferus (Anura:Dendrobatidae), with a description of the tadpole. J Herpetol 26:102–105.
Vargas-Salinas F, Castro F (1999) Distribución y preferencias de microhábitat en anuros (Amphibia) en bosque maduro y áreas perturbadas en Anchicayá, Pacífico Colombiano. Caldasia 21:95–109.
Vitt LJ, Caldwell JP (2014) Herpetology: An introductory biology of Amphibians and Reptiles, Fourth Edi. Academic Press & Elsevier Inc., London.
von May R, Medina-Müller M, Donnelly MA, Summers K (2008) The tadpole of the bamboo-breeding poison frog Ranitomeya biolat (Anura: Dendrobatidae). Zootaxa 1857:66–68.
Wells KD (1978) Courtship and parental behavior in a Panamanian Poison-Arrow Frog (Dendrobates auratus). Herpetologica 34:148–155.
Wells KD (1980a) Social behavior and communication of a Dendrobatid frog (Colostethus trinitatis). Herpetologica 36:189–199.
Wells KD (1980b) Evidence for growth of Tadpoles during parental transport in Colostethus inguinalis. J Herpetol 14:428–430.
Wells KD (1980c) Behavioral ecology and social organization of a Dendrobatid Frog (Colostethus inguinalis). Behav Ecol Sociobiol 6:199–209.
Wells KD (2007) The Ecology and Behavior of Amphibians. The University of Chicago Press, Chicago and London.
Weygoldt P (1987) Evolution of parental care in dart poison frogs (Amphibia:Anura:Dendrobatidae). Zeitschrift für Zool Syst und Evol 25:51–67.
Womack MC, Steigerwald E, Blackburn DC, et al (2022) State of the Amphibia 2020: A Review of Five Years of Amphibian Research and Existing Resources. Ichthyol Herpetol 110:638–661.

Tables 1 to 4 are available in the Supplementary Files section.

No competing interests reported.

Table1.xlsx
Table 1. List of localities where “Colostethus” ruthvenisensu stricto was recorded, with date of observation, sampling effort, total count per sampling event, and relative abundance (n/h/obs) per sampling event
Table2.xlsx
Table 2. Microhabitat uses of “Colostethus” ruthveni sensu stricto in four localities of the northwestern sector of the Sierra Nevada de Santa Marta. χ²=Chi square test, df=degrees of freedom.
Table3.xlsx
Table 3. Summary of morphometric characters of free-swimming tadpoles of “Colostethus” ruthveni sensu stricto thorough Gosner (1960) stages. Measurements expressed in mm, with range (average ± standard deviation). For abbreviation, see section of “free-swimming tadpoles” of materials and methods
Table4.xlsx
Table 4. Summary of features of nests of “Colostethus” ruthveni sensu stricto. Egg diameter expressed in range (average ± standard deviation).
supplementarymaterial1.xlsx
Supplementary material 1. Supplementary tables: ST1. Morphological data of all tadpoles of the batch CBUMAG:ANF:00662 ST2. List of larval and reproductive character states of “C.” ruthveni. ST3. List of larval and reproductive character states across genera of Dendrobatoidea ST4. Data of A2-gap and P1-gap from all available tadpole description of Dendrobatoidea. ST5. list of larval and reproductive characters from Grant et al. (2017) considered as not independent under the considerations of Sereno (2007)
supplementarymaterial2.mov
Supplementary material 2. Supplementary video: Never-before-seen images partially describe the courtship of “C.” ruthveni
Supplementarymaterial3.pdf
Supplementary material 3. Supplementary document: List of larval and reproductive characters mapped on the summary topology with the generic relationships of Dendrobatoidea from Grant et al. (2017).

Download PDF

Version 1

posted

You are reading this latest preprint version

Reproductive strategies, free-swimming tadpoles, and natural history of the Santa Marta rocket frog “Colostethus” ruthveni Kaplan, 1997 (Anura: Dendrobatidae), with a review of the distribution of larval and reproductive characters in Dendrobatoidea

Status:

Version 1

Abstract

Figures

Introduction

Materials and methods

Study area

Relative abundance and microhabitat use

Free-swimming tadpoles

Reproductive strategies

Distribution of larval and reproductive characters

Results

Relative abundance and microhabitat use

Redescription of free-swimming tadpoles

Courtship and reproductive mode

Distribution of larval and reproductive characters

Discussion

Relative abundance and microhabitat use

Free-swimming tadpoles

Courtship and reproductive mode

Distribution of larval and reproductive characters

Declarations

References

Tables

Additional Declarations

Supplementary Files

Status:

Version 1