Ranitomeya reticulata ( Boulenger, 1884 )

Klein, Benjamin, Regnet, Ruth Anastasia, Krings, Markus & Rödder, Dennis, 2020, Larval development and morphology of six Neotropical poison-dart frogs of the genus Ranitomeya (Anura: Dendrobatidae) based on captive-raised specimens, Bonn zoological Bulletin 69 (2), pp. 191-223 : 211-214

Ranitomeya reticulata ( Boulenger, 1884)

Breeding behavior in captivity. The breeding pair deposited the clutches, consisting of an egg, within the bromeliad phytotelm. Reproduction was occasionally.

Larval morphology. Description is based on three tadpoles at developmental stage 41 ( ZFMK 97359 ). Further voucher specimens are ZFMK 97360 , 97365 and 97378. According to McDiarmid & Altig (1999), the larvae belong to the exotrophic, lentic, benthic and arboreal larval type. All measurements that were used to calculate the following proportions and its comparison with the other species of this study, are be found in the Table 13 .

Dorsal view: The body is oval and elongated (MBW/ BL= 0.62). The snout is short and moderately pointed (RED/BL= 0.28, BWN/BWE = 0.65). The shape of the nares is not visible in dorsal view, nares are closer to the snout than to the eyes (RND/RED = 0.40). A skin fold, which originates at the nares, ends close to the anterior margin of the eyes; the two landmarks are not connected. The eyes are large (ED/BL = 0.09), positioned dorsally and orientated laterally. The internarial distance is small- er than the interorbital distance (IND/IOD = 0.53). The single, sinistral spiracle as well as parts of the oral apparatus are visible in dorsal view.

Lateral view: Body is slightly depressed (MBH/ MBW= 0.68), the snout is pointed. Nares are round, located and orientated dorsally. The spiracle is situated below the longitudinal axis, at the second half of the body (RSD/BL= 0.64), the inner wall is free from the body and the opening is round. The maximum body height is located posterior to the eye. The tail is long and moderately pointed (TAL/BL= 1.64, TAL/TL = 0.62). The “V”- shaped myosepta are visible along the whole length of the tail. The upper fin originates posterior to the lower fin and the tail-body junction, the margin of the lower fin is nearly parallel to the margin of the tail muscle. Ventral tube is strongly atrophied, emergence from abdomen sagittal. Hindlimbs are completely developed. Oral appa- ratus is visible in lateral view.

Oral apparatus: The oral disc is elliptical, emarginated, located anteroventrally and covers more than one third of the maximum body width (ODW/MBW= 0.40). Mar- ginal, pointed and pigmented papillae are present at the posterior labium and except the most lateral part, absent at the anterior labium. Submarginal papillae are absent. The anterior labium contains two tooth rows of an equal width (A1, A2), the second tooth row has a large medial gap (A2-GAP). The posterior labium contains three tooth rows (P1, P2, P3), with a moderate gap in the first row (P1-GAP). Tooth row P1 and P2 are of the same width, the width of the P3 was not discernible. Both jaw sheaths are black and serrated. The tooth row formula is 2(2)/3(1) ( Fig. 11D ).

Coloration of a living tadpole of R. reticulata (ZFMK 97359). The dorsum has an anthracite basic color, with three golden to orange stripes running on top or parallel to the longitudinal axis ( Fig. 11A 1 , A 2 ). The two dorsolateral stripes originate at one point posterior to the nares, bifurcate and run close to the eyes, with a moderate gap on eye level. The medial stripe runs in between the two others, situated on the symmetry line of the body. Depending on the specimen, the medial and the dorsolateral stripes are fused, originating from one point posterior to the nares and anterior to the eyes. The distance between the stripes decreased at the second half of the body. The hindlimbs and the tail are as anthracite as the dorsum, spotted with darker dots. Fins are transparent and spotted with grayish dots.

Coloration of a preserved tadpole of R. reticulata (ZFMK 97359). The dorsum has a beige basic color, with some darker areas at the outermost part of the forelimb pouches and one small line at the anterior margin of the dorsolateral stripes. The area in between the dorsolateral stripes, which extends to the tail-body junction, is of the same color as the dark areas mentioned beforehand. The dorsolateral and median stripes are clearly discernible on the head and the first half of the body, running on top or parallel to the longitudinal axis. The dorsolateral stripes originate and bifurcate at one point posterior to the nares and run next to the eyes, with a moderate gap on eye level. The whitish median stripe originates in between the eyes, not fusing with the origin of the dorsolateral stripes. Anterior to the eye, the dorsolateral stripes are beige, posterior they are whitish. The hindlimbs and the tail are as beige as the dorsum, spotted with some dark dots. Fins are transparent and spotted with dark dots. The ventral side is beige, spotted with gray dots. The hindlimbs’ ventral side is brighter than the dorsal side.

Larval staging. At stage 25, right after hatching, the tadpoles had a surface area of 0.23 ± 0.09 cm ². During the transition from stage 25 to 27, where the hindlimb buds were slightly visible, the surface area increased to 0.32 ± 0.11 cm ². After 29 to 41 days (median = 36 days), half of all larvae had developed a hindlimb bud that was equally in diameter and length and reached a surface area of 0.81 ± 0.01 cm ². Between the stages 28 to 40, the larvae had a surface area of 0.88 ± 0.06 cm ². During this development period, the hindlimbs grew, all toes became separat- ed and the typical dorsal color pattern was present. The forelimb pouches were discernible after a minimum of 42 and a maximum of 63 days, while half of all individuals reached that development stage after 54 to 58 days (median = 56 days). At this point, the tadpoles had a surface area of 1.02 ± 0.11 cm ². Not a single larva completed the full metamorphosis to a young froglet ( Fig. 6 , Table 9). A more detailed staging table based on stereomicroscopic determinations of five specimens from an external source between stages 25 to 37 can be found within the Table 10.

The development was observed under constant conditions with a temperature of 24 °C, while the annual mean temperature within the natural distribution area of R. reticulata is slightly higher (T Mean = 24.8 °C, T Max = 28.2 °C, T Min = 21.5 °C: Karger et al. 2017a,b; Fig. 7 ).

Figures

Fig. 11. Illustrations of the tadpole of Ranitomeya reticulata, satage 41 of Gosner (1960). A1. Dorsal view, photograph. A2. Dorsal view, drawing. B1. Ventral view, photograph.B2. Ventral view, drawing.C1. Lateral view, photograph.C2. Lateral view, drawing. D. Drawing of the oral disc. LTRF = 2(2)/3(1).

Fig. 1. Known distribution of Ranitomeya amazonica (green), R. benedicta (light blue), R. imitator (red), R. reticulata (yellow), R. sirensis (blue) and R. vanzolinii (orange). Darker shades of gray indicate higher elevations. The inset map displays the distribution of all six compared species, which are shown in the upper right corner of that figure with the corresponding color code.

Fig. 2. Landmarks andmeasurements of a tadpole body and definitions of the oral apparatus.A. Lateral view.B. Dorsal view.C. Oral apparatus. Abbreviations A–B: BL=body length; TAL=tail length; TL=total length; TMH =tail muscle height; MTH=maximum tail height; IND=internarial distance; IOD=interorbital distance; TMW=tail muscle width. The dotted line indicates the accurate progression of the measurement which represents the body length. Abbreviations C: A1=first anterior tooth row;A2=second ante- rior tooth row;A2-GAP=medial gap in second anterior tooth row; AL=anterior (upper) labium; LJ=lower jaw sheath; LP=lateral process of upper jaw sheath; M=mouth; MP=marginal papillae; OD=oral disc; PL=posterior (lower) labium; P1=first posterior tooth row; P2=second posterior tooth row; P3=third posterior tooth row; SM=submarginal papillae; UJ=upper jaw sheath.

Fig. 6. Developmental series of six Ranitomeya species during the transition from a hatchling to a froglet. The upper panel illustrates the increase of surface area over time, whereby the surface area [cm²] is highly correlated with the body mass. Warmer colors indicate a higher sample density; each circle represents one data point. Loess function represented by the red lines, whereby the outer lines display the 95% confidence interval. The lower panel illustrates the temporal occurrence of the following traits: 1=no limb bud discernible; 2=hindlimb bud discernible; 3=forelimb pouches discernible; 4=forelimbs emerged; 5=initiation of tail resorption.

Fig. 7. Climatic characteristics within the geographic ranges of six Ranitomeya species in terms of annual mean temperature, minimum and maximum temperature of the coldest / warmest month. Boxplots show the 95% range, lower and upper hinge enclosing 50% of the samples and the median based on a random sample per 10 km2.