Mantidactylus (Chonomantis)

Grosjean, Stéphane, STRAUss, Axel, Glos, Julian, Randrianiaina, Roger-Daniel, Ohler, Annemarie & Vences, Miguel, 2011, Morphological and ecological uniformity in the funnel-mouthed tadpoles of Malagasy litter frogs, subgenus Chonomantis, Zoological Journal of the Linnean Society 162 (1), pp. 149-183 : 179-180

CHONOMANTIS TADPOLES

It is striking that the tadpoles of all Chonomantis are very uniform morphologically. Indeed, only minor morphological variations were detected, especially in the proportion of certain ratios such as the interpupilar distance, the width of the umbelliform oral disc or the point where the upper fin begins on the caudal muscle, and possibly general body size. Oral morphology, which usually is very useful in discriminating tadpole species, often even in closely related species (e.g. Scott & Jennings, 1985; Schmidt et al., 2008) is very uniform in these species. Even if the number and the size of the papillae and ridges that occur on the inner side vary amongst species, they show the same pattern of distribution in all species.

Some morphometric ratios could be useful in discriminating some Chonomantis species, as specified in the ‘Morphometric comparison’ section of the Results. The height and width of the caudal muscle discriminate M. aerumnalis from M. opiparis , and M. aerumnalis from M. sp. 59 for the height only. However, this result should be taken with caution as these differences could be related to the preservation of M. aerumnalis in absolute alcohol, which dries out soft tissues. The width of the oral disc is the most discriminant character, involving 12 species pairs. The variability of this soft structure is weak within species but its relative size shows some relevant differences amongst species.

Mantidactylus opiparis shows great variation in morphometric values despite the developmental range of the sample being restricted to young stages (25–28). On the contrary, samples of the other species encompass a larger range of developmental stages, except for M. albofrenatus , for which only stages 26 are available. It is worth noting that in the young developmental stages the upper fin is less developed than in the older ones and begins further along on the caudal muscle, leading to great variation in the SU /BL ratios.

Mantidactylus opiparis and especially M. melanopleura are the most widespread and also locally the most common tadpoles. This is confirmed by our tadpole surveys, as these two species also occur in Ranomafana (and co-occur in many streams; Fig. 8 ). Despite their wide co-occurrence, there is no obvious morphological or ecological differentiation of their tadpoles ( Figs 6–8 ), except possibly some differences in body size ( M. opiparis tadpoles being larger at the same developmental stage; Table 2) and the presence of a thin vertebral line in many but not all specimens of M. opiparis (absent in our sample of M. melanopleura tadpoles). As well in the adult stage, these two species are very similar in morphology and (as far as known) ecology, and the only obvious differences are again in body size ( M. melanopleura reaching larger sizes) and in characters that certainly (advertisement calls) or probably (frenal stripe) are involved in premating reproductive isolation and species recognition.

The short divided row of keratodonts on the lower labium of M. sp. 59 is unique to this species and is the only character that allows the reliable discrimination of a species of Chonomantis from all others on the basis of larval morphology. Similarly, the coloration with distinct transversal patterns in M. aerumnalis allows the reliable recognition of most tadpoles of this species. The clear mediodorsal band on the back of M. opiparis is characteristic of this species but it is not present in all specimens examined. Mantidactylus brevipalmatus has longer lungs than any other tadpoles of this group. This feature could indicate that tadpoles of this species have a more aerial respiration mode, or that they live in quieter habitats where buoyancy caused by lungs filled with air is not disadvantageous. Further studies are necessary to ascertain if this character is an autapomorphy of M. brevipalmatus or might reflect phenotypic plasticity. Paradoxically, this species largely lives in montane habitats and tadpoles are typically found in fast streams with crystal-clear, highly oxygenated water, although they are restricted to shallow and slowmoving parts of these streams.

At present, there are few reliable phylogenetic data that would allow an evolutionary interpretation of the faint variation. Vieites et al. (2009) presented a tree of mantellid frogs, including all Chonomantis , based on analyses of sequences of the 16S rRNA gene. Unfortunately, most of the relationships in this subgenus could not be reliably resolved. Mantidactylus aerumnalis from An’Ala and the population from Ranomafana here also assigned to M. aerumnalis were placed in a clade with high support. Even if these two forms might in the future be recognized as two distinct species, it is relevant that their molecular relationships are mirrored by the conspicuous coloration of their tadpoles.

Mantidactylus delormei and M. brevipalmatus were recovered as closely related sister species, but this is not reflected by morphological similarity of their larvae: in fact, the tadpoles of M. delormei lack the enlarged lungs of M. brevipalmatus , and in the morphometric analysis the two species are placed far from each other.

Mantidactylus sp. 59 is not reliably placed in the phylogeny and an interpretation of its rudimentary keratodonts as either plesiomorphy or reversal is not possible at present.

In conclusion, on the one hand, the high morphological similarity amongst Chonomantis larvae strongly supports the monophyly of the subgenus. No other mantellid tadpoles have umbelliform oral discs, and these as well as the associated oral structures are thus clearly a synapomorphy of Chonomantis species. Molecular data place Chonomantis as a sister group to the subgenus Brygoomantis that have a generalized tadpole morphology (e.g. Glaw & Vences, 2006), but interestingly the molecular phylogenetic signal for monophyly of Chonomantis is not very strong, especially if short DNA sequences of only one marker are used (e.g. Vieites et al., 2009). In this case, thus, tadpole morphology gives an important and very convincing argument to support current classification and help in clarifying evolutionary relationships amongst mantellid frogs.

On the other hand, given the high degree of sympatric occurrence of Chonomantis (see Vences & Glaw, 2004), confirmed here also for their tadpoles, which occur in the same microhabitat in often the same streams, it remains mysterious as to why their morphological and ecological differentiation has not been driven further by selective pressures. Whether competition is a relevant factor in rainforest frogs has not been sufficiently assessed, but especially for their tadpoles that often occur in high densities in the Malagasy rainforest streams, competition might be an important factor. It needs to be assessed further whether the diet and activity rhythms of these tadpoles may be more different amongst species than is superficially apparent, and in general, how strong competition is as a force in shaping the community structure and morphological adaptation of rainforest frogs.

Figures

Figure 6. Results of multivariate morphometric analysis of tadpoles of Mantidactylus species in the subgenus Chonomantis (DNA voucher specimens only). A: plot of discriminant functions based on all 18 measurements; B: plot of principal component factor 1 against factor 2.

Figure 7. Histogram showing the mean preferences for microhabitat structures by tadpoles of six Mantidactylus species in the subgenus Chonomantis, sampled during a tadpole community study in Ranomafana National Park. Ivlev’s electivity index (E, Ivlev, 1961) is plotted for each species and each microhabitat. Positive values indicate that microhabitat was used more often than expected by chance, negative values represent an avoidance of microhabitat structure. Missing bars show that the respective microhabitat was not available to the specific species.

Figure 8. Principal component (PC) ordination biplots of habitat preferences of tadpoles of four common Mantidactylus species in the subgenus Chonomantis, sampled during a tadpole community study in Ranomafana National Park and identified by DNA barcoding. A: biplot of PC1 and PC2; B: biplot of PC3 and PC4; each data point represents a species sample. Data points close to each other represent similar microhabitat preferences. Frequently occurring colorations show very common/abundant species, colorations of only a few dots stand for scarce/patchy species.