Verschiedenartigkeit von Morphologie- und Ernährungseigenschaften in den Larven von madagassische mantelliden Frösche

The Mantellidae is the largest Madagascan frog family in terms of species richness and diversity in morphology, ecology, and reproductive modes. This is also verified in the larval stages. Eleven ecomorphological guilds of tadpoles were defined, one endotrophic, the nidicolous larvae, and ten exotrophics which are generalized, adherent, suctorial, carnivorous, reduced-mouthed femoralis-like, reduced-mouthed mocquardi-like, specialized form in which the upper sheath is transformed into three big thorn-shaped papillae-like structures, specialized form in which the sheaths are transformed into many spike-like structures, sand-eater, funnel-mouthed. The morphological tree which is based on tadpole characters shows that (1) tadpole morphological characters correctly recover several genera and subgenera of mantellids: most species of Boophis are grouped together, most species of Spinomantis are grouped together, the subgenus Chonomantis is supported, and the relationship between subgenera Ochthomantis and Chonomantis is supported; (2) secondly, tadpole morphological characters place some unrelated species together: an example is the placement of Boophis picturatus with Mantidactylus (Ochthomantis). Two kinds of convergence are also found in the larval stage of Mantellidae. The first one is the reduction of the oral disk components in Boophis picturatus and in many mantellines belonging to Mantidactylus (Ochthomantis) and Gephyromantis. The second convergence is the enlargement of the oral disk found in four groups of Boophis: Boophis luteus group, Boophis albipunctatus group, Boophis mandraka group, and Boophis majori group. Generally, tadpole morphology is correlated to their ecology and feeding traits. The life coloration - yellowish brown or beige - of Boophis picturatus tadpoles allows their camouflage in sandy microhabitat where most of them are found, and their commodious oral disk permits the ingestion sand grains that we discovered in the gut. The streamlined body form and the enlarged oral disk in the strongly rheophilous Boophis (B. schuboeae and B. marojezensis, for example) tadpoles represents an adaptation for living in fast moving section of the streams where many specimens were caught. The identification of high amount of diatoms in the gut of B. marojezensis vs. B. schuboeae proves the different feeding traits of the 2 species, and this confirms also their classification in two different ecomorphological guilds. The use of DNA barcoding in this study induced an accurate assignation of the tadpoles to its true species, and an identification of many candidate species which are only known from larval stages on the other hand.Die Mantellidae stellen die größte madagassische Frosch-Familie in Bezug auf Artenreichtum und Verschiedenartigkeit in Morphologie, Ökologie, und Reproduktionsmodi dar. Das wird auch in den Larvenstadien nachgeprüft. Elf ökomorphologische "Gilden" madagassischer Kaulquappen werden in dieser Arbeit definiert, eine endotrophische mit nest-lebenden Larven sowie zehn exotrophische: generalisiert, anhaftend, stark anhaftend, fleischfressend, mit reduziertem femoralis-artigem Mundfeld, mit mocquardi-artigem reduziertem Mundfeld , in dem der obere Hornkiefer in drei große dornförmige Papiellen umgestaltet wird, eine Spezialform, in der die Hornkiefer in eine reusenartige Struktur umgebildet wurde, sansfressend, und Larven mit einem trichterförmigen Mundfeld. Der phylogenetische Baum, der mittels Kaulquappemerkmalen erstellt wurde, zeigt, dass (1) diese Merkmale die meisten Gattungen und Artengruppen als monophyletisch rekonstruiert, (2) in einigen Fällen aber Arten aufgrund ihrer Ähnlichkeit in morphologischen Merkmalen zusammengestellt werden, obwohl sie nicht nahe miteinander verwandt sind, zum Beispiel Boophis picturatus mit Mantidactylus (Ochthomantis). Zwei Beispiele für konvergente Evolution von Kaulquappenmerkmalen wurden identifiziert: Dies ist zum einen die Reduktion von keratinisierten Bestandteilen des Mundfeldes bei Boophis picturatus einerseits und bei vielen Vertretern der Unterfamilie Mantellinae andererseits, zum Beispiel bei Mantidactylus (Ochthomantis) und Gephyromantis. Zum anderen betrifft konvergente Evolution die Vergrößerung des Mundfeldes als Anpassung an stark stömende Lebensräume, welche sich in mehreren Artengruppen von Boophis findet: Boophis luteus Gruppe, Boophis albipunctatus Gruppe, Boophis mandraka Gruppe, und Boophis majori Gruppe. Im allgemeinen scheint die Kaulquappenmorphologie in Zusammenhang mit dem Lebensraum und Lebensweise der Larven zu stehen. Die Lebendfärbung - gelblich braun oder beige - von Boophis picturatus Kaulquappen erlaubt ihre Tarnung in sandigem Mikrohabitat, wo die meisten von ihnen gefunden werden, und ihre spezialisiertes Mundfeld erlaubt die Aufnahme von Sandkörnern, die wir in dem Darm dieser Larven finden konnten. Die stromlinienförmige Körperform und das vergrößerte Mundfeld der stark rheophilen Boophis-Arten (z. B. B. schuboeae und B. marojezensis) kann als Anpassung an schnell fließendes Wasser gewertet werden. Allerdings unterschieden sich diese Kaulquappen stark in der Zusammensetzung ihres Darminhalts (mit einer sehr großen Proportion von Diatomeen bei B. marojezensis), was eventuell auf eine unterschiedliche Ernährung der beiden Arten hinweist und ihre Einordnung in unterschiedliche Gilden bestätigt. Die Anwendung von molekularen Identifizierungsmethoden (DNA barcoding) in dieser Studie erlaubte die zuverlässige Zuordnung von Larvalstadien zu den entsprechenden Adultstadien, und ermöglichte in vielen Fällen die Entdeckung von noch taxonomisch unbeschriebenen Kandidatenarten, welche bislang nur über ihre Kaulquappen bekannt sind

The world's richest tadpole communities show functional redundancy and low functional diversity: ecological data on Madagascar's stream-dwelling amphibian larvae

<p>Abstract</p> <p>Background</p> <p>Functional diversity illustrates the range of ecological functions in a community. It allows revealing the appearance of functional redundancy in communities and processes of community assembly. Functional redundancy illustrates the overlap in ecological functions of community members which may be an indicator of community resilience. We evaluated patterns of species richness, functional diversity and functional redundancy on tadpole communities in rainforest streams in Madagascar. This habitat harbours the world's most species-rich stream tadpole communities which are due to their occurrence in primary habitat of particular interest for functional diversity studies.</p> <p>Results</p> <p>Species richness of tadpole communities is largely determined by characteristics of the larval habitat (stream structure), not by adult habitat (forest structure). Species richness is positively correlated with a size-velocity gradient of the streams, i.e. communities follow a classical species-area relationship. While widely observed for other taxa, this is an unusual pattern for anuran larvae which usually is expected to be hump-shaped. Along the species richness gradient, we quantified functional diversity of all communities considering the similarity and dissimilarity of species in 18 traits related to habitat use and foraging. Especially species-rich communities were characterised by an overlap of species function, i.e. by functional redundancy. By comparing the functional diversity of the observed communities with functional diversity of random assemblages, we found no differences at low species richness level, whereas observed species-rich communities have lower functional diversity than respective random assemblages.</p> <p>Conclusions</p> <p>We found functional redundancy being a feature of communities also in primary habitat, what has not been shown before using such a continuous measure. The observed species richness dependent pattern of low functional diversity indicates that communities with low species richness accumulate functional traits randomly, whereas species in species-rich communities are more similar to each other than predicted by random assemblages and therefore exhibit an accumulation of stream-specific functional traits. Beyond a certain species richness level, therefore, stream-specific environmental filters exert influence whereas interspecific competition between species does not influence trait assemblage at any species richness level.</p

The unexpectedly dull tadpole of Madagascar’s largest frog, Mantidactylus guttulatus

The Madagascar-endemic mantellid genus Mantidactylus contains one subclade with two described frog species characterized by very large body sizes. This subclade is classified as the subgenus Mantidactylus and is widespread in eastern and northern Madagascar, but their reproductive biology and larval stages are still unknown. We here provide a detailed description of the larvae of one species in this subgenus, M. guttulatus, on the basis of genetic assignment (16S DNA barcoding). The tadpoles were collected in the dry season from shallow waters near a stream in the Mahajanga Province in northwestern Madagascar. Their body and tail shape is remarkably generalized as typical for stream-adapted tadpoles, and the oral disc and labial keratodont row formula (4(2-4)/3(1)) are similar to those of other lotic mantellid frog larvae with generalized mouthparts like those in the subgenus Brygoomantis. The well-separated positions of these subgenera in the mantellid phylogeny suggest extensive homoplasy in the evolution of larval mouthpart morphology within Mantidactylus

Transcriptomic and macroevolutionary evidence for phenotypic uncoupling between frog life history phases

Wollenberg Valero KC, Garcia-Porta J, Rodriguez A, et al. Transcriptomic and macroevolutionary evidence for phenotypic uncoupling between frog life history phases. Nature Communications. 2017;8(1): 15213.Anuran amphibians undergo major morphological transitions during development, but the contribution of their markedly different life-history phases to macroevolution has rarely been analysed. Here we generate testable predictions for coupling versus uncoupling of phenotypic evolution of tadpole and adult life-history phases, and for the underlying expression of genes related to morphological feature formation. We test these predictions by combining evidence from gene expression in two distantly related frogs, Xenopus laevis and Mantidactylus betsi-leanus, with patterns of morphological evolution in the entire radiation of Madagascan mantellid frogs. Genes linked to morphological structure formation are expressed in a highly phase-specific pattern, suggesting uncoupling of phenotypic evolution across life-history phases. This gene expression pattern agrees with uncoupled rates of trait evolution among life-history phases in the mantellids, which we show to have undergone an adaptive radiation. Our results validate a prevalence of uncoupling in the evolution of tadpole and adult phenotypes of frogs

Diversity of the strongly rheophilous tadpoles of Malagasy tree frogs, genus Boophis (Anura, Mantellidae), and identification of new candidate species via larval DNA sequence and morphology

This study provides detailed morphological descriptions of previously unknown tadpoles of the treefrog genus Boophis Tschudi and analyses of habitat preferences of several of these tadpoles in Ranomafana National Park. A total of twenty-two tadpoles determined via DNA barcoding are characterized morphologically herein, fourteen of them for the first time. Twelve of these tadpoles belong to taxonomically undescribed candidate species which in several cases are so far only known from their larval stages. Our data show that the larvae of some of these candidate species occur syntopically yet maintaining a clearly correlated genetic and morphological identity, suggesting that they indeed are true biological and evolutionary species. Tadpoles considered to belong to the “adherent” ecomorphological guild inhabit fast-running waters and their oral disc is commonly to continuously attached to the rocky substrate, supposedly to keep their position in the water current. Some of these species are characterized by the presence of a dorsal gap of papillae and the absence of an upper jaw sheath. This guild includes the tadpoles of the B. albipuncatus group (B. ankaratra, B. schuboeae, B. albipunctatus, B. sibilans, B. luciae), and of the B. mandraka group (B. sambirano and six candidate species related to this species and to B. mandraka). Tadpoles considered belonging to the “suctorial” guild inhabit fast-running waters where they use frequently their oral disc to attach to the substrate. They have an enlarged oral disc without any dorsal gap, including two nominal species (B. marojezensis, B. vittatus), and five candidate species related to B. marojezensis. An ecological analysis of the tadpoles of B. luciae, B. schuboeae and B. marojezensis [Ca51 JQ518198] from Ranomafana National Park did not provide evidence for a clear preference of these tadpoles to the fast flowing microhabitat sections of the stream, although the tadpoles discussed in this study are typically caught in this habitat

The unexpectedly dull tadpole of Madagascar’s largest frog, <em>Mantidactylus guttulatus</em>

The Madagascar-endemic mantellid genus Mantidactylus contains one subclade with two described frog species characterized by very large body sizes. This subclade is classified as the subgenus Mantidactylus and is widespread in eastern and northern Madagascar, but their reproductive biology and larval stages are still unknown. We here provide a detailed description of the larvae of one species in this subgenus, M. guttulatus, on the basis of genetic assignment (16S DNA barcoding). The tadpoles were collected in the dry season from shallow waters near a stream in the Mahajanga Province in northwestern Madagascar. Their body and tail shape is remarkably generalized as typical for stream-adapted tadpoles, and the oral disc and labial keratodont row formula (4(2-4)/3(1)) are similar to those of other lotic mantellid frog larvae with generalized mouthparts like those in the subgenus Brygoomantis. The well-separated positions of these subgenera in the mantellid phylogeny suggest extensive homoplasy in the evolution of larval mouthpart morphology within Mantidactylus

Nidicolous tadpoles rather than direct development in Malagasy frogs of the genus Gephyromantis

Frogs in the genus Gephyromantis from Madagascar were assumed to have a direct developmental mode, i.e. the complete embryonic and larval development within the egg, but recently free-swimming, exotrophic tadpoles of a few species have been found. Herein we provide detailed morphological descriptions of the tadpoles of five more species of this genus, indicating a developmental mode other than direct development in species of Gephyromantis. Tadpoles of Gephyromantis granulatus, G. sculpturatus, G. tschenki, and G. ventrimaculatus were found free-swimming in streams, and tadpoles of G. sp. aff. blanci were raised after hatching from clutches found in the leaf litter. All tadpoles were identified by DNA barcoding. The oral discs of all five species are characterized by the lack of many typical morphological traits of exotrophic tadpoles (such as oral papillae and keratodonts). This indicates that these tadpoles are either non-feeding (endotrophic) or only facultatively feeding tadpoles. We classify these tadpoles as nidicolous based on the observation that the larvae of G. sp. aff. blanci stayed after hatching in the jelly nest until metamorphosis. It remains unclarified whether all species have strictly nidicolous tadpoles, and the larvae of the four species found in the streams were just accidentally washed into these streams; alternatively, some of these tadpoles might be nidicolous at first but in some species need to live in free water at later stages. © 2011 Copyright Taylor and Francis Group, LLC

Opposing Patterns of Seasonal Change in Functional and Phylogenetic Diversity of Tadpole Assemblages

Assemblages that are exposed to recurring temporal environmental changes can show changes in their ecological properties. These can be expressed by differences in diversity and assembly rules. Both can be identified using two measures of diversity: functional (FD) and phylogenetic diversity (PD). Frog communities are understudied in this regard, especially during the tadpole life stage. We utilised tadpole assemblages from Madagascan rainforest streams to test predictions of seasonal changes on diversity and assemblage composition and on diversity measures. From the warm-wet to the cool-dry season, species richness (SR) of tadpole assemblages decreased. Also FD and PD decreased, but FD less and PD more than expected by chance. During the dry season, tadpole assemblages were characterised by functional redundancy (among assemblages-with increasing SR), high FD (compared to a null model), and low PD (phylogenetic clustering; compared to a null model). Although mutually contradictory at first glance, these results indicate competition as tadpole community assembly driving force. This is true during the limiting cool-dry season but not during the more suitable warm-wet season. We thereby show that assembly rules can strongly depend on season, that comparing FD and PD can reveal such forces, that FD and PD are not interchangeable, and that conclusions on assembly rules based on FD alone are critical

Boophis bottae

&lt;i&gt;Boophis bottae&lt;/i&gt; &lt;p&gt;(Figures 5 and 8)&lt;/p&gt; &lt;p&gt;The following description refers to one tadpole in developmental stage 36, ZSM 488/2008 (field number LR 247) (TL 30 mm, BL 11 mm) from Analamazaotra Special Reserve. The 16S rDNA sequence of this specimen differs in 2 substitutions over an alignment of 525 bp from a reference sequence of an adult specimen (accession AJ314817) from the same locality.&lt;/p&gt; &lt;p&gt;In dorsal view, body elongated ovoid, snout rounded. In lateral view, body depressed, BW 143% of BH, snout as an almost uniform curve. Eyes moderately large, ED 13% of BL, not visible in ventral view, not bulging, positioned more laterally than dorsolaterally but directed dorsolaterally. Pineal ocellus absent. Nares nearly oval, moderately-sized, rimmed, positioned dorsolaterally, directed dorsally, much closer to the eyes than to the snout. RN 136% of NP, NN 57% of PP. Spiracle sinistral, moderately small, slightly conical, inner wall free from body, spiracular opening oval and directed more posteriorly than posterodorsally, the aperture is situated much closer to vent tube than to tip of snout, SS 70% of BL, situated below the longitudinal axis of tail musculature. Vent tube short, dextral, opening at ventral edge of fin, medial vent tube with lateral displacement. Caudal musculature moderately strong, TMH 55% of BH and 56% of MTH, TMW 45% of BW, height of caudal musculature almost the half of total tail height at mid-length of tail, reaching almost tail tip. Caudal fins regular with straight edges, very shallow, MTH 98% of BH; dorsal fin originating at the dorsal tail body junction and slightly taller than ventral fin at mid-length of tail; ventral fin originating at the level of the ventral terminus of the body, following the caudal muscle; tail tip nearly pointed. Oral disk moderately large, ODW 25% of BL and 45% of BW, positioned anteroventrally and directed ventrally, emarginated. Oral disk surrounded by a single row of 66 (32 on the left side and 34 on the right side) marginal papillae interrupted by a large gap on the upper labium (DG 61% of ODW), and by a small medial gap on the lower labium. Five submarginal papillae positioned in the lateral and posterolateral parts of the lower labium. Papillae of moderate size, round or conical with rounded tips. LTRF 1:4+4/1+1:2 after Dubois (1995) and 5(2&ndash;5)/3(1) after Altig &amp; McDiarmid (1999). The number of keratodonts on A1 is about 70/mm (a total of 123). The length of interrupted anterior keratodont rows (A2, A3, A4 and A5) decreases gradually towards the center of the disk, P1 and P2 of about similar size, slightly longer than P3. Both jaw sheaths coarsely serrated; upper jaw completely black with a large medial serration surrounded by a smaller on each side forming a slight convexity; lower jaw partially pigmented, V- shaped.&lt;/p&gt; &lt;p&gt; &lt;b&gt;Coloration in preservative.&lt;/b&gt; Dorsally: body and tail musculature brownish, covered by scattered dark patches, almost uniform. Intestinal coils not visible dorsally.&lt;/p&gt; &lt;p&gt;Laterally: intestinal coils obscure but partially visible on the lower part of the body; dorsal fin sparsely pigmented; ventral fin clear. Ventrally: bronchial and cardial region not visible through ventral body wall. Intestinal coils dextral, well visible ventrally with regular spiral shape&lt;/p&gt;Published as part of &lt;i&gt;Randrianiaina, Roger-Daniel, Raharivololoniaina, Liliane, Preuss, Claudia, Glaw, Frank, Teschke, Meike, Glos, Julian, Raminosoa, Noromalala &amp; Vences, Miguel, 2009, Descriptions of the tadpoles of seven species of Malagasy treefrogs, genus Boophis, pp. 23-41 in Zootaxa 2021&lt;/i&gt; on pages 30-31, DOI: &lt;a href="http://zenodo.org/record/274725"&gt;10.5281/zenodo.274725&lt;/a&gt

Boophis guibei

Boophis guibei (Figure 7) The following description refers to one tadpole in developmental stage 36 (field number FG/MV 2003-2018, ZSM 1609 / 2004, TL 38 mm, BL 15 mm) from Ranomafana National Park. The 16 S rDNA sequence of one specimen from the same batch differed in 18 substitutions over an alignment of 512 bp from a reference sequence of an adult specimen that originated from another locality near Ranomafana (accession AY 848480). In dorsal view body ovoid. In lateral view body depressed, snout almost uniformly curved, BW 115 % of BH. Moderately large eyes, ED 12 % of BL, positioned dorsally, directed laterally, situated at the anterior 1 / 3 of the body. Nares elliptical, prominent with marginal rim, positioned dorsolaterally, oriented anterolaterally, much closer to snout than to eyes, RN 58 % of NP and NN 42 % of PP. Wide and short sinistral spiracle, inner wall free and formed such that the aperture opens laterally instead of posteriorly not visible from dorsal view. The ellipical opening is situated close to the origin of the lower part of the tail musculature and oriented posterodorsally, the aperture is closer to end of body than to snout, SS 57 % of BL. Dextral vent tube, the aperture is under a flap. Strong caudal musculature in the anterior half, TMH 54 % of BH and TMW 45 % of BW. Dorsal fin higher than ventral fin. At midlength of tail, caudal musculature represents about ¼ of total tail height. Dorsal fin origins before the tail body junction and ventral fin originnates at the ventral terminus of the body. Oral disk moderately large, ODW 24 % of BL and 36 % of BW, positioned ventrally and directed anteroventrally, emarginated. One row of marginal papillae that is interrupted along by a large gap on the upper labium (DG 69 % of ODW); a total of 102 marginal papillae, density 18 papillae/mm, 34 submarginal papillae positioned in the lateral parts of the anterior and posterior labium (19 on the left side and 17 on the right side. Papillae of moderate size, round or conical with rounded tips. LTRF 1: 5 + 5 / 1 + 1: 3 after Dubois (1995) and 6 (2–6)/ 3 (1) after Altig & McDiarmid (1999). A 2 has 58 keratodonts/mm (a total of 217 keratodonts), A 1 has a total of 238 keratodonts (88 keratodonts/mm). Jaw sheaths partially pigmented and coarsely serrated, serrations rounded. Upper jaw sheath M-shaped, lower jaw sheath V-shaped. Coloration in preservation. Dorsally: small brown patches between the nares and at the beginning of the caudal musculature. The patches are condensed around and between the eyes. In lateral view, half-moon shaped brown patches behind the eye. Intestinal coils visible in ventral and lateral view, regularly spiralshaped. Some brown dots on dorsal and ventral fin. Variation: TL and BL of five tadpoles at stages 25–42 are 19–38 mm and 10–15 mm, respectively. BW 113–122 % of BH; ED 9–22 % of BL; RN 83–181 % of NP; NN 39–50 % of PP; TMH 48–79 % of BH; TMW 35–83 % of BW; ODW 23–28 % of BL; ODW 33–41 % of BW; SS 40–61 % of BL; TMH 45–62 % of MTH; MTH 104–120 % of BH.Published as part of Randrianiaina, Roger-Daniel, Raharivololoniaina, Liliane, Preuss, Claudia, Glaw, Frank, Teschke, Meike, Glos, Julian, Raminosoa, Noromalala & Vences, Miguel, 2009, Descriptions of the tadpoles of seven species of Malagasy treefrogs, genus Boophis, pp. 23-41 in Zootaxa 2021 on pages 33-34, DOI: 10.5281/zenodo.27472