MICROHYLIDAE

Candioti, M. Florencia Vera, 2007, Anatomy of anuran tadpoles from lentic water bodies: systematic relevance and correlation with feeding habits, Zootaxa 1600, pp. 1-175 : 102-118

MICROHYLIDAE

Chiasmocleis panamensis . External and internal morphology of this species were described in Vera Candioti (2006b); the name “postnarial papilla” is replaced with the most accurate name “narial wall papilla”, and the lateral ridge papillae are considered absent, according to Wassersug (1980) and Chou and Lin (1997).

Chondrocranium and hyobranchial skeleton (N = 5, stages 35 and 36. Fig. 58). The chondrocranium of these larvae represents 58% of the body length. The maximum width is at the plane of the processus lateralis posterior of the palatoquadrate. The suprarostral cartilage has corpus and alae fused in a single structure with a curved anterior margin and a posterior margin bearing a medial projection. The suprarostral is fused to the anterior margin of trabecular horns, and only the lateral part of the horns remains free. The trabecular horns correspond approximately to 22% of the total length of the chondrocranium and are flat and distally wider. Posteriorly, on the trabecular plate, the olfactory foramina are clearly distinguishable. The cranial floor is completely cartilaginous, with thin cartilage in the central area. The carotid and craniopalatine foramina are visible, the latter elongate and larger than the former. In the posterior margin of the cranial floor, the notochordal canal extends 20% of the chondrocranium length. In the lateral walls of the chondrocranium, the orbital cartilages are formed only marginally, and the central region is occupied by a large foramen that joins the optic, oculomotor, trochlear and prootic foramina. The chondrocranium is open dorsally, and the frontoparietal fenestra is bordered by the taeniae tecti marginales. The otic capsules are quadrangular and occupy nearly 31% of the chondrocranium total length. The fenestra ovalis (37% of the capsule length) is located ventrolaterally on each otic capsule. The otic capsules are dorsally joined by the tectum synoticum. In the palatoquadrate, the articular process is short and wide. The muscular process is scarcely developed and bears a small ventrolateral process in its ventral surface. The subocular bar shows a uniform width, and in the most posterior part presents a long, rectangular, flat, posterolaterally directed processus lateralis posterior. In the ventral surface of this process, the subotic process is present, as a chondrified, subcylindrical, bifurcated structure. The palatoquadrate attaches to the braincase via three points: the quadratocranial commissure, bearing a small quadratoethmoid process, the ascending process, attached to the cranial floor, and the larval otic process. The lower jaw includes the Meckel’s and infrarostral cartilages. Meckel’s cartilages are bar-like, with dorsal and retroarticular process conspicuous. The infrarostral cartilages are fused forming a ring-like structure with a laminar projection arising from the medial, posterior margin. In the hyobranchial skeleton, the ceratohyals are elongate and have a small, rounded anterior process, a tall, pointed anterolateral process, and a thin, triangular posterior process, partially concealed by the ceratobranchial I; the lateral edge of the ceratohyal shows a wide laminar projection posteriorly directed; the articular condyle outlines in the posterodorsal margin of the ceratohyal. The basihyal is a very thin, cartilaginous bar. The pars reuniens is continuous with the ceratohyals and the basibranchial. The basibranchial is small, and bears a thin and long urobranchial process (1.7 times longer than the basibranchial). The basibranchial is posteriorly fused to the hypobranchial plates, which are in turn fused to each other. The ceratobranchials are fused to the hypobranchial plates and constitute a large, complexly reticulated branchial basket. Between the ceratobranchials II and III there is a closed branchial process. Dorsally, three large spicules are differentiated, and the most lateral, wider than the others, apparently represents the complete fusion of spicules I and II.

Musculature (N = 5, stages 35 and 36. Table 17 and Fig. 59). Thirty muscles appear in this species.

Muscle Insertions Comments

Levator mandibulae articularis dorsal surface of the muscular process – lateral it is a very short muscle

edge of Meckel’s cartilage

Suspensoriohyoideus posterior part of the ventral surface of the it is formed of a few fibers, loosely disposed processus lateralis posterior – dorsal surface of

the lateral process of the ceratohyal

Orbitohyoideus anterior, dorsal margin of the muscular process it is scarcely developed

– lateral edge of the ceratohyal

Suspensorioangularis ventral surface of the palatoquadrate – it is located laterally to the m.

retroarticular process of Meckel’s cartilage quadratoangularis, and it is almost

indistinguishable from it

Quadratoangularis ventral surface of the palatoquadrate –

retroarticular process of Meckel’s cartilage

Hyoangularis dorsal surface of the ceratohyal – retroarticular it is scarcely developed

process of Meckel’s cartilage

Interhyoideus ventral surface of the lateral process of the it is formed of parallel, fibers, transversally ceratohyal – median aponeurosis and obliquely disposed

Interhyoideus posterior it forms a continuous and extensive layer,

ventral to the peribranchial chamber

Geniohyoideus posterior, ventral surface of the infrarostral –

diffuse, near the thyroid gland

Levator arcuum branchialium I ventral surface of the processus lateralis

posterior, near its lateral margin – lateral surface

of the ceratobranchial I

Levator arcuum branchialium II ventral surface of the otic capsule and ventral

surface of the processus lateralis posterior, near

its lateral margin – ceratobranchials I and II

Levator arcuum branchialium two slips: anterior and anterolateral points on

III the ventral surface of the processus lateralis

posterior – terminal commissure II and III

Levator arcuum branchialium ventral surface of the otic capsule – medial

IV margin of the ceratobranchial IV

Dilatator laryngis posterolateral surface of the otic capsule –

arytenoid cartilage

Constrictor branchialis II branchial process – terminal commissure I

Constrictor branchialis III branchial process – terminal commissure II

Constrictor branchialis IV branchial process – terminal commissure III

Subarcualis rectus I three slips: lateral base of the posterior process the ventral 2 slip is very long and thin, and

of the ceratohyal – spicule I (dorsal slip), originates laterally to the base of the posterior

ceratobranchial I (ventral 1 slip), and branchial process, on a small process of the posterior

process (ventral 2 slip) margin of the ceratohyal; the insertion of the

ventral 1 slip on the ceratobranchial I is medial

regarding that of the dorsal slip

Subarcualis rectus II-IV ventromedial surface of the ceratobranchial IV

– branchial process

Subarcualis rectus II-IV distal part of the ceratobranchial IV – branchial

lateralis process

Subarcualis obliquus urobranchial process – branchial process

Diaphragmatobranchialis peritoneum – ceratobranchial III

Rectus cervicis peritoneum – branchial process

Rectus abdominis peritoneum, approximately at half the abdomen

level – pelvic griddle

Oral apparatus and buccopharyngeal cavity (N = 2, stage 36. Figs. 60 and 61). The mouth is terminal with a wide oral slit devoid of papillae and keratinized structures. Gape width reaches 28% of the body length. Two upper labial flaps hang covering the spatulate lower lip. The buccal roof is not pigmented. The prenarial arena shows a single bifid papilla. The choanae are large, subcircular and unperforated. From the posterior margin of each choana, a large, flat and multifid narial wall papilla arises. A bifid papilla projects medially from the choana lateral margin, accompanied by scarce smaller papillae. The median ridge is three times higher than wide, triangular, and with a pustulate margin. Lateral ridge papillae are absent. Posteriorly to the median ridge, the buccal roof arena is poorly defined; some pustules and short papillae distribute on the central and lateral regions. Secretory pits appear in a broad array on the posterior region of the buccal roof. The dorsal velum is comparatively long and smooth, without projections. In the buccal floor, the posterior surface of Meckel’s cartilage has small pustules. The tongue anlage is small and devoid of lingual papillae. The buccal pockets are well-developed and have two prepocket papillae projecting from the anterior margin. The glottis is far anteriorly placed, on the posterior margin of the buccal floor arena. On both sides, tall, conical papillae are arranged, approximately following a wide V-shape. Among them, small pustules are scattered. The ventral velum is very long and posteriorly expanded; the margin has wide undulations and a small median notch.

Gut content (N = 7, stages 34–36). In this species digestive tract, as in the other two microhylids examined, distinctive strings appear, coming from each side of the branchial basket, and then entering into the oesophagus forming a conspicuous double-helix ( Fig. 65). The digestive contents of the specimens analyzed appear full of a very fine material impossible to quantify. The specimens come from the same pond but from different collection dates, so it seems improbable that the tadpoles had not been feeding on both cases. It could be suggested that this species diet include very small items to be detected with a different methodology. For this reason, this species could not be included in the correspondence analysis of the gut contents, nor in the canonical correspondence analysis later applied to morphological and food variables.

Dermatonotus muelleri . Previous literature for this species includes papers by Lavilla (1992b), Echeverría and Lavilla (2000), and Ulloa Kreisel (2003). A revision on internal morphology appeared in Vera Candioti (2006b).

Chondrocranium and hyobranchial skeleton (N = 5, stages 34–36. Fig. 62). The chondrocranium of these larvae represents 43% of the body length. The maximum width is at the level of the processus lateralis posterior of the palatoquadrate. The suprarostral cartilage has corpus and alae fused in a single structure with a curved anterior margin and a posterior margin bearing a medial, triangular projection. The suprarostral is fused to the anterior margin of trabecular horns, and only the lateral part remains free. The trabecular horns correspond approximately to 21% of the total length of the chondrocranium and are flat and distally wider. The cranial floor is lightly chondrified in the central area. The carotid and craniopalatine foramina are visible, the latter elongate and larger than the former. In the posterior margin of the cranial floor, the notochordal canal extends 15% of the chondrocranium length. In the lateral walls of the chondrocranium, the orbital cartilages are formed only marginally, and the central region is occupied by a large foramen that joins the optic, oculomotor, trochlear and prootic foramina. The chondrocranium is open dorsally through the frontoparietal fenes- tra lined by the taeniae tecti marginales. The otic capsules are quadrangular and occupy nearly 27% of the chondrocranium total length. The crista parotica appears as a scarcely chondrified, lateral and posteriorly expanded plate that curves ventrally and overlaps to the lateral part of the branchial basket. The fenestra ovalis (35% of the capsule length) is located ventrolaterally on each otic capsule. The otic capsules are dorsally joined by the tectum synoticum. In the palatoquadrate, the articular process is short and wide, with three small anterior processes. The muscular process is scarcely developed. The subocular bar shows a uniform width, and in the most posterior part presents a long, rectangular, flat, and posterolaterally oriented processus lateralis posterior. In the ventral surface of this process, the subotic process is present. The palatoquadrate attaches to the braincase via three points: the quadratocranial commissure, bearing a small quadratoethmoid process, the ascending process, attached to the cranial floor, and the larval otic process, long and extended between the posterior third of the processus lateralis posterior and the anterior part of the crista parotica. The lower jaw includes the Meckel’s and the infrarostral cartilages. Meckel’s cartilages are bar-like, with dorsal and retroarticular processes. The infrarostral cartilages are fused forming a ring-like structure with a laminar projection arising from the medial, posterior margin. In the hyobranchial skeleton, the ceratohyals are elongate and have a low, rounded anterior process, a tall, thin, pointed and medially directed anterolateral process, and a tall, thin posterior process, partially concealed by the ceratobranchial I; the lateral edge of the ceratohyal has a wide laminar projection posteriorly directed; the articular condyle is outlined in the posterodorsal margin of the ceratohyal. The basihyal is a very thin, cartilaginous bar. The pars reuniens is continuous with the ceratohyals and the basibranchial. The basibranchial is small and bears a thin and long urobranchial process (1.4 times longer than the basibranchial). The basibranchial is posteriorly fused to the hypobranchial plates, which are in turn fused to each other. The ceratobranchials are fused to the hypobranchial plates and form a voluminous branchial basket. Between the ceratobranchials II and III there is a closed branchial process. Dorsally, three large spicules are differentiated, and the most lateral, wider than the others, apparently represents the complete fusion of spicules I and II.

Musculature (N = 5, stages 34–36. Table 18 and Fig. 63). Twenty-nine muscles are present in this species.

Muscle Insertions Comments

Suspensoriohyoideus posterior part of the ventral surface of the processus it is formed of a few fibers, loosely lateralis posterior – dorsal surface of the lateral process of disposed

the ceratohyal

Orbitohyoideus anterior, dorsal margin of the muscular process – lateral it is scarcely developed

edge of the ceratohyal

Suspensorioangularis ventral surface of the palatoquadrate – retroarticular it is located laterally to the m. process of Meckel’s cartilage quadratoangularis, and it is almost

indistinguishable from it

Quadratoangularis ventral surface of the palatoquadrate – retroarticular

process of Meckel’s cartilage

Hyoangularis dorsal surface of the ceratohyal – retroarticular process of it is scarcely developed

Meckel’s cartilage

Interhyoideus ventral surface of the lateral process of the ceratohyal – it is formed of parallel, fibers, median aponeurosis transversally and obliquely

disposed

Interhyoideus posterior it forms a continuous and extensive layer, ventral to the

peribranchial chamber

Geniohyoideus posterior, ventral surface of the infrarostral – diffuse, near it is very thin, formed of a few thyroid gland fibers

Levator arcuum branchialium I ventral surface of the processus lateralis posterior, near its

lateral margin – lateral surface of the ceratobranchial I

Levator arcuum branchialium II lateroventral surface of the otic capsule – ceratobranchials

I and II

Levator arcuum branchialium two slips: anterior and anterolateral points on the ventral

III surface of the processus lateralis posterior – terminal

commissure II and III

Levator arcuum branchialium ventral surface of the otic capsule – medial margin of the

IV ceratobranchial IV

Dilatator laryngis posterolateral surface of the otic capsule – arytenoid

cartilage

Constrictor branchialis II branchial process – terminal commissure I

Constrictor branchialis III branchial process – terminal commissure II

Constrictor branchialis IV branchial process – terminal commissure III

Subarcualis rectus I two slips: lateral base of the posterior process of the

ceratohyal – spicule I (dorsal slip), and ceratobranchial I

(ventral slip)

Subarcualis rectus II-IV ventromedial surface of the ceratobranchial IV –

branchial process

Subarcualis rectus II-IV distal part of the ceratobranchial IV – branchial process

lateralis

Subarcualis obliquus urobranchial process – branchial process

Diaphragmatobranchialis peritoneum – ceratobranchial III

Rectus cervicis peritoneum – branchial process

Rectus abdominis peritoneum, approximately at half the abdomen level –

pelvic griddle

Oral apparatus and buccopharyngeal cavity (N = 2, stages 34 and 35. Fig. 64). The mouth is terminal with a wide oral slit devoid of papillae and keratinized structures. Gape width reaches 26% of the body length. Two upper labial flaps hang covering the spatulate lower lip. In the buccal roof, the prenarial arena shows a single small papilla and some pustules. The choanae are large, subcircular and unperforated. From the posterior margin of each choana, a large, flat and multifid narial wall papilla arises. Four tall, conical papillae project medially from the choana lateral margin, accompanied by scarce smaller papillae and pustules. The median ridge is nearly four times higher than wide, triangular, and with pustulate margin. Lateral ridge papillae are absent. The buccal roof arena is not defined, and numerous pustules distribute on the central zone and posterior edge of the roof. Secretory pits appear in a broad array on the posterior margin of the buccal roof. The dorsal velum is comparatively long and smooth. In the buccal floor, the posterior surface of Meckel’s cartilage shows 2–3 small pustules. The tongue anlage is small and devoid of lingual papillae. The buccal pockets are well-developed and have one bifid prepocket papilla projecting from the anterior margin, accompanied by small pustules. The glottis is far anteriorly placed, on the posterior margin of the buccal floor arena. On both sides, 9–11 tall, conical papillae are arranged approximately following a wide V-shape. Among them, small pustules are scattered. The ventral velum is well-developed and posteriorly expanded; it has three marginal projections on the filter plates, and a small median notch.

Gut content (N = 7, stages 34–36. Tables 21 and 22). The digestive content was almost completely composed of small Volvocales (99.23%) with sizes below 1% of the tadpole body length. Figure 65 shows the distinctive food-strings obtained from the oesophagus and the most anterior part of the intestine.

Elachistocleis bicolor . Previous literature for this species includes papers by Lavilla and Langone (1995), Lajmanovich (1998), Echeverría and Lavilla (2000), Haas (2001; 2003), and Ulloa Kreisel (2003). A revision on internal morphology appeared in Vera Candioti (2006b).

Chondrocranium and hyobranchial skeleton (N = 5, stages 34 and 35. Fig. 66). The chondrocranium of these larvae represents 31% of the body length. The maximum width is at the level of the processus lateralis posterior of the palatoquadrate. The suprarostral cartilage has corpus and alae fused in a single structure with a curved anterior margin and a posterior margin bearing a medial, slightly outlined projection. The suprarostral is fused to the anterior margin of trabecular horns, and only the lateral part remains free. The trabecular horns correspond approximately to 21% of the total length of the chondrocranium and are flat and distally wider. The cranial floor is lightly chondrified in the central area. The carotid and craniopalatine foramina are visible, the latter elongate and larger than the former. In the posterior margin of the cranial floor, the notochordal canal extends 13% of the chondrocranium length. In the lateral walls of the chondrocranium, the orbital cartilages are formed only marginally and the central region is occupied by a large foramen that joins the optic, oculomotor, trochlear and prootic foramina. The chondrocranium is open dorsally, and the frontoparietal fenestra is lined by the taeniae tecti marginales. The otic capsules are quadrangular and occupy nearly 31% of the chondrocranium total length. The fenestra ovalis (26% of the capsule length) is located ventrolaterally on each otic capsule. The otic capsules are dorsally joined by the tectum synoticum. In the palatoquadrate, the articular process is short, wide, and has three small anterior processes. The muscular process is scarcely developed and has a long ventrolateral process with a length similar to that of the subocular bar. The subocular bar is uniformly wide and in the most posterior part presents a long, rectangular, flat processus lateralis posterior that bears a ventral, bifid subotic process. The palatoquadrate attaches to the braincase via three points: the quadratocranial commissure, the ascending process, attached to the cranial floor, and the larval otic process. The lower jaw includes the Meckel’s and the infrarostral cartilages. Meckel’s cartilages are bar-like with dorsal and retroarticular processes. The infrarostral cartilages are fused forming a ring-like structure with a laminar projection arising from the medial, posterior margin. In the hyobranchial skeleton, the ceratohyals are elongate and have a wide, rounded anterior process, a tall, thin, medially directed anterolateral process, and a tall and thin posterior process, partially concealed by the ceratobranchial I; the lateral edge of the ceratohyal has a wide laminar projection posteriorly directed; the articular condyle is outlined in the posterodorsal margin of the ceratohyal. The basihyal is a very thin, cartilaginous bar. The pars reuniens is contin- uous with the ceratohyals and the basibranchial. The basibranchial is small and bears a thin and very long urobranchial process (about 2 times longer than the basibranchial). The basibranchial is posteriorly fused to the hypobranchial plates, which are in turn fused to each other. The ceratobranchials are fused to the hypobranchial plates and constitute a large branchial basket. Between the ceratobranchials II and III there is a closed branchial process. Dorsally, three large spicules are differentiated, and the most lateral, wider than the others, apparently represents the complete fusion of spicules I and II.

Musculature (N = 5, stages 34 and 35. Table 19 and Fig. 67). Thirty muscles are present in this species.

Oral apparatus and buccopharyngeal cavity (N = 2, stage 35. Fig. 68). The mouth is terminal with a wide oral slit devoid of papillae and keratinized structures. Gape width reaches 29% of the body length. Two upper labial flaps hang covering the spatulate lower lip. In the buccal roof, the prenarial arena shows a single small papilla. The choanae are large, subcircular and unperforated. From the posterior margin of each choana, a large, flat and multifid narial wall papilla arises. A single, flat, pustulate papilla projects medially from the choana lateral margin, accompanied by scarce pustules. The median ridge is two times higher than wide, triangular, and with a pustulate margin. Lateral ridge papillae are absent. Posteriorly to the median ridge, the buccal roof arena is not defined; numerous pustules and small conical papillae distribute irregularly on the central region of the roof. Secretory pits appear in a broad array on the posterior region of the buccal roof. The dorsal velum is long and smooth. In the buccal floor, the posterior surface of Meckel’s cartilage shows small pustules. The tongue anlage is small and devoid of lingual papillae. The buccal pockets are well-developed and have a large, wide, flat and multifid prepocket papilla projecting from the anterior margin. The glottis is far anteriorly placed, on the posterior margin of the buccal floor arena. On both sides, 6 tall, bifid papillae are arranged approximately following a wide V-shape. Among them, small pustules are scattered. The ventral velum is well-developed and posteriorly expanded; it shows an undulate margin, and a small median notch.

Gut content (N =10, stages 34 and 35. Tables 21 and 22). The gut contents were mainly composed of euglenoids and diatoms with sizes ranging from <1–1% of the tadpole body length. Like in the other microhylids, the food is organized in strings that coil when entering into the oesophagus ( Fig. 65).