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A Comparative Study of Divergent Embryonic and Larval Development in the Australian Frog Genus Geocrinia (Anura: Myobatrachidae)

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A Comparative Study of Divergent Embryonic and Larval Development in the Australian Frog Genus Geocrinia (Anura: Myobatrachidae) Records of the Western Australian Museum 25: 399–440 (2010). A comparative study of divergent embryonic and larval development in the Australian frog genus Geocrinia (Anura: Myobatrachidae) Marion Anstis School of Biological Sciences, Newcastle University, Callaghan, Newcastle, New South Wales 2308, Australia. E-mail: [email protected] Abstract - Embryonic and larval development of the seven Geocrinia species across Australia are described and compared. This Australian myobatrachid genus includes three species with terrestrial embryonic development followed by aquatic exotrophic larval development and four species with entirely terrestrial and endotrophic development. Comparisons are made among species within the terrestrial/exotrophic group and the endotrophic group, and between the two breeding modes of each different species-group. Morphological differences are noted between northern and southeast coastal Western Australian populations of G. leai tadpoles. The G. rosea group shares some similarities with the other Australian endotrophic species in the genus Philoria and Crinia nimbus. IntroductIon Australia (Main 1957, 1965), have terrestrial embryonic development and exotrophic (aquatic, About 38 species of anurans from 22 genera and feeding) larval development. The remaining four 7 families worldwide are known to have nidicolous allopatric species in southwestern Australia (G. alba, endotrophic larvae, and if endotrophy occurs in G. lutea, G. rosea and G. vitellina) belong to the G. a genus, usually all species in that genus are of rosea that developmental guild (Thibaudeau and Altig species-group (Wardell-Johnson and Roberts 1999). These authors listed some known exceptions, 1993; Roberts 1993) and have terrestrial endotrophic including Gastrotheca (one endotrophic and one (non-feeding) embryonic and larval development exotrophic guild), Mantidactylus (one endotrophic (Main 1957; Roberts et al. 1990; Roberts 1993). All and several exotrophic guilds) and Megophrys seven species of adult frogs are small, ranging (one endotrophic and one exotrophic guild). The from 19–33 mm snout-vent length (SVL) and are Australian myobatrachid genus Geocrinia also generally similar in morphology (Littlejohn and includes two developmental guilds as defined by Martin 1964; Driscoll 1997). Altig and Johnston (1989), with three terrestrial/ Read et al. (2001) presented a mitochondrial exotrophic species and four terrestrial/endotrophic gene tree for the myobatrachids as then defined species. with an emphasis on Crinia and Geocrinia. They The family Myobatrachidae in Australia has a included all species of Geocrinia except G. lutea, great variety of breeding modes representative and their data divided Geocrinia into two strongly of various guilds (Altig and Johnston 1989) from supported lineages: (a) G. leai, G. victoriana and G. the entirely aquatic (e.g. Uperoleia, Mixophyes, laevis (with G. leai somewhat divergent) and (b) G. Taudactylus, Notaden and most Crinia) to the rosea, G. alba and G. vitellina (G. lutea is presumed terrestrial/aquatic (e.g. Pseudophryne and Geocrinia to belong in this lineage based on other characters). laevis group), nidicolous (Philoria, Crinia nimbus, Edwards (2007) found that G. leai consists of three Geocrinia rosea group), the exoviviparous Assa, distinct lineages which show no morphological paraviviparous Rheobatrachus and the three closely- differences as adults and occur in: (i) the northern related direct developers Arenophryne, Myobatrachus Darling escarpment, (ii) the southeast coast and and Metacrinia (Roberts 1993; Anstis et al. 2007; (iii) the southern coastal regions of southwestern Anstis 2008). Australia. Comparisons of G. leai tadpoles from Across southern Australia and Tasmania, there populations (i) and (iii) are included here. To are seven species of frogs currently assigned to facilitate descriptions, G. leai, G. laevis and G. the myobatrachid genus Geocrinia. Three species, victoriana (i.e. lineage ‘a’ of Read et al. 2001) are including G. victoriana and G. laevis found in the referred to as the G. laevis group (terrestrial/ southeast (Littlejohn and Martin 1964; Watson exotrophic) and the other four species as the G. and Martin 1973) and G. leai from southwestern rosea group (terrestrial/endotrophic). 400 M. Anstis These two groups are also clearly separated by terrestrial/exotrophic species: Geocrinia laevis their breeding biology, call structure (Littlejohn group and Watson 1974; Roberts et al. 1990; Roberts and Wardell-Johnson 1995) and larval life history Geocrinia leai (Main 1957, 1965; Littlejohn and Martin 1964; This species occurs mainly in forest habitats of Roberts et al. 1990; Roberts 1993). Anstis (2008) southwestern Australia from the Darling Scarp included the G. rosea group in the nidicolous east of Perth along the southwest coastal region to endotrophic category of Altig and Johnston (1989) southern forests and Cape Leeuwin, and east to because the larvae of this group remain in a Albany (Main 1957). Dorsal colour is variable, but terrestrial nest, hatch from the eggs as free-moving most have a broad brown to black band (which tadpoles and metamorphose without feeding, may be divided) on a lighter background. Ventral unlike direct developers, which do not have a colour is dull, translucent greenish-yellow (Figure tadpole stage and differ significantly in other 1A,B). Males usually call from April to late October aspects of their physiological development (Altig (Main 1957) from hidden shady sites on land within and Johnston 1989; Thibaudeau and Altig 1999; or beside dry creek beds, above existing water in Callery et al. 2001). ponds or swamps, or in other areas that will be Various descriptions of the embryonic and larval flooded later. Frogs are mostly found in leaf litter, development of the two eastern exotrophic species beneath or within clumps of sedges or grass, or have been published (Littlejohn and Martin 1964; under logs in moist areas beside creeks, swamps, Martin 1967; Littlejohn et al. 1971; Watson and ponds or dry creek beds later to be flooded during Martin 1973; Martin and Littlejohn 1982; Gollmann the winter wet period. and Gollmann 1991a,b, 1992a,b, 1993, 1994, 1995, Eggs are laid on land from April to late October 1996a,b; Anstis 2002). For the southwestern species, (autumn to spring), usually prior to rain, and are there are studies including some developmental found in moist leaf litter, beneath matted reeds, descriptions of G. leai and G. rosea by Main (1957, under logs or attached to living vegetation. After 1965) and of G. vitellina by Mitchell (2001). the eggs have been laid, the male frog remains in This paper reviews the known breeding biology the vicinity and resumes calling. For this reason, of all Geocrinia species based on the published clutches of more than one female at different literature and original observations. It then developmental stages may be found in the nesting provides comprehensive descriptions of embryos territory of the same male. Eggs of a single clutch and larvae with a developmental staging system adhere together (Figure 3C). Several other clutches for the G. rosea group, and enables detailed contained 52–96 eggs (Main 1957). Hatching comparisons between individual species and begins from 15 days after the eggs are laid (Main between each group of the seven Geocrinia species 1957). Metamorphosis occurs in spring, usually during their embryonic and larval development. from October (Main 1957). The duration of larval It should enhance our comparative knowledge of development from eggs reared to metamorphosis in the developmental life history and morphology of the laboratory was 149–174 days (Main 1957). Geocrinia embryos and larvae and facilitate a better Geocrinia laevis understanding and interpretation of the evolution of these divergent cases of embryogenesis. This species occurs in Tasmania, southwestern A summary is provided of key differences in Victoria including the Grampians, and across to the early development of the G. laevis group and Mount Burr in southern coastal South Australia the G. rosea group as compared to Gosner (1960) (Woodruff and Tyler 1968). Adults have a brown dorsum, often with a darker bifurcated patch less stages 18–26, and shows the main characters of obvious in some, but dorsal pattern is variable limb, oral, optic and opercular development that (Littlejohn and Martin 1964). Ventral surface of are not reconcilable with the Gosner staging system males from Garvoc is white with dark flecks and a during early development (see Appendix 3). dull yellow throat and in females it is all white with Comparisons of the G. rosea group with tadpoles of darker flecks and patches (Figure 1C-E). the only other Australian nidicolous species, Crinia nimbus and the genus Philoria, are summarised in In Tasmania calling begins in autumn from the Discussion. late February to April (Littlejohn and Martin 1964) and mostly from about mid-March to mid- rEVIEW oF GEOCRINIA BrEEdInG BIoLoGY May in southwestern Victoria, depending on the weather (Littlejohn and Watson 1973; Harrison This section reviews the known literature on and Littlejohn 1985). In peak periods males call Geocrinia breeding biology (as cited), supplemented day and night while hidden beneath vegetation with original observations while in the field during in matted grasses, sedges or leaf litter and at the the study. base of tussocks within or beside low-lying areas A comparative study of Geocrinia development 401 Figure 1 Adults of the Geocrinia
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