Comparative morphology and evolution of the lungless caecilian Atretochoana eiselti (Taylor) (Amphibia: Gymnophiona: Typhlonectidae)

Abstract

Atretochoana iselti is a radically divergent aquatic caecilian until recently known from only a single specimen from South America. In addition to its status as the largest lungless tetrapod known, and the only known lungless caecilian, this species has a suite of highly unusual morphological features that sets it apart from all other tetrapods, including sealed choanae (internal nostrils), complete loss of pulmonary arteries and veins, novel cranial architecture, and a novel stapedial muscle. The external, buccal, skeletal, muscular and cardiovascular anatomies of Atretochoana eiselti are described and compared to these features in other caecilians, particularly representatives of all typhlonectid genera which are its closest relatives. The comparative morphological data are used as a basis for interpretations of the ecology and evolution of Atretochoana &elti. It is argued that lunglessness and the transition to cutaneous gas cxchange is correlated with life in cold, montane, fast-flowing streams. Here, high oxygn concentrations and reduced metabolic rate serve to relax the physiological limitations on body size imposed by a reliance upon cutaneous gas-exchange, and lungs can produce disadvantageous buoyancy. Cranial evolution has increased the gape of Atretochoana eiselti relative to other caecilians, and seems likely to be associated with a shift in prey size and possibly type. Several modifications of the cranium appear to be associated with enhanced cranial kinesis in which a distinct cheek unit is highly mobile. The novel stapedial musculature is interpreted as contributing to this cranial kinesis. Respiratory and cranial evolution are argued to be correlated, with the ventilatory function of the buccopharyngeal pump constraining the evolution of the skull. The evolution of lunglessness removed this constraint facilitating repatterning of the skull. 0 I997 'The Linnean Soriety or Iandon

A new lungless caecilian (Amphibia: Gymnophiona) from Guyana

“…Other caecilians, except for typhlonectids, have the left lung well developed, the right usually absent, and a few have a 'tracheal' respiratory component. Typhlonectids, in contrast and often suggested to be correlated with their aquatic lifestyle, have a well-developed left lung that may extend to the cloacal region (Typhlonectes natans: M. Wake, personal observations), and also have the right lung well developed and of varying lengths relative to the left among species (although respiratory function has not been determined for most, and the large right lung in Potamotyphlus lacks respiratory epithelium and is presumed to be a rheotactic organ (Wilkinson & Nussbaum 1997)). Lung development is more extensive in typhlonectids than that of nearly all other caecilians, rather than less.…”

Is solid always best? Cranial performance in solid and fenestrated caecilian skulls

“…Based on recently published caecilian phylogenies (Roelants et al, 2007;Zhang and Wake, 2009;Pyron and Wiens, 2011;Wilkinson et al, 2011) (Fig.2), the zygokrotaphic skull has evolved independently several times in caecilians, in the Scolecomorphidae, Typhlonectidae and Dermophiidae (Brand, 1956;Taylor, 1969;Nussbaum, 1977;Nussbaum, 1985;Wilkinson and Nussbaum, 1997;Müller et al, 2009). Zygokrotaphy in the Rhinatrematidae, however, has usually been considered to be the ancestral condition for the Gymnophiona (Nussbaum, 1977;Nussbaum, 1983;Wake, 2003;Müller, 2007), and the reduction of bone coverage in the temporal skull region was considered to be homologous among caecilians, frogs and salamanders.…”

“…The stegokrotaphic skull would, on casual inspection, appear better suited to burrowing than the zygokrotaphic skull with the large unroofed region and, for two caecilian groups with zygokrotaphic skulls, there might actually be an ecological link to poorer burrowing performance; rhinatrematids are considered to be poor burrowers that can be readily trapped during surface activity (Nussbaum, 1983;Gower et al, 2010); typhlonectids are mainly aquatic species and may therefore be relieved of the constraints of burrowing (Wilkinson and Nussbaum, 1997). However, the zygokrotaphic scolecomorphids are considered to be specialized burrowers (Nussbaum, 1977;Nussbaum, 1983); furthermore, the zygokrotaphic dermophiid caecilian Geotrypetes seraphini shows similar burrowing performance to other stegokrotaphic caecilians (Herrel and Measey, 2010).…”

Caecilita Wake & Donnelly, 2010 (Amphibia: Gymnophiona) is not lungless: implications for taxonomy and for understanding the evolution of lunglessness

“…Hoogmoed et al's (2011) discovery of living populations of the lungless aquatic caecilian Atretochoana eiselti (Taylor, 1968) within the Amazon basin provided the first concrete evidence of the environment of that species. Their discoveries falsify the speculation that this species inhabits cold, upland waters (Wilkinson & Nussbaum, 1997), but nonetheless supports the notion (Wilkinson & Nussbaum, 1997) that it inhabits fast-flowing waters where lungs could provide disadvantageous buoyancy.…”

“…Secondary lunglessness is a rare condition that is currently considered to have evolved independently five times within amphibians, twice in caecilians, twice in salamanders and once in frogs (Hutchison, 2008;Wake & Donnelly, 2010), but nowhere else within the tetrapods. Explanations of the evolution of this unusual condition have mostly suggested that lunglessness is or was an adaptation to life in fast-flowing waters where pulmonary buoyancy, and concomitant difficulty in maintaining position, could be positively disadvantageous (e.g., Wilder & Dunn, 1920;Wilkinson & Nussbaum, 1997;Bickford et al, 2008). This is a plausible, if controversial, explanation of lunglessness in amphibians (Hutchison, 2008) with the clear exception of lunglessness in the recently discovered monotypic caecilian genus Caecilita.…”