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Direct Development in the Australian Myobatrachid Frog Metacrinia Nichollsi from Western Australia

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Direct Development in the Australian Myobatrachid Frog Metacrinia Nichollsi from Western Australia DOI: 10.18195/issn.0312-3162.24(2).2008.133-150 Records of the Western Australian Museum 24: 133-150 (2008). Direct development in the Australian myobatrachid frog Metacrinia nichollsi from Western Australia Marion Anstis 26 Wideview Rd, Berowra Heights, New South Wales 2082, Australia. Email: frogpolecditpg.com.au Abstract - The development of the myobatrachid frog Metacrinia nichol/si from southwestern Australia is described. Metacrinia nichollsi and the related myobatrachid direct developing species Myobatrachus gouldii and Arenophryne rotunda all differ from Eleutherodactylus coqui in that their forelimbs develop internally and emerge later, and they do not have a keratinised egg tooth. Eggs of M. nichol/si were found deposited beneath leaf litter on dry sand not associated with water and embryonic development is completed entirely within the jelly capsule over a period of more than two months. Observations on a predatory nematode worm are noted. Keywords: Australia, frog, embryo, endotrophic, predatory nematode INTRODUCTION our knowledge of the taxa with this developmental Endotrophic anurans derive all their mode typically is lacking in detail. Much of the developmental energy from vitellogenic yolk or available information is based on three genera with other parentally produced material (Thibaudeau a specific concentration on the South American frog and Altig 1999), unlike typical exotrophic anuran Eleutherodactylus coqui (Thibaudeau and Altig larvae that need to feed to gain energy post 1999; Altig and Crother 2006). Anstis et al. (2007; hatching. In taxa with direct development, all Myobatrachus gouldii and Arenophryne rotunda) embryonic development takes place within the jelly is the only study involving Australian taxa, but layers of the egg until a froglet hatches; there is no provides little information on living specimens. hatched free-living embryo or tadpole. In broad Metacrinia nichollsi is a small myobatrachid frog reviews of Australian anuran life-histories, Tyler restricted to forests in southwestern Australia, (1985) and Roberts (1993) included the Australian including a population in the Stirling ranges (Tyler endotrophic genera Assa, Kyarranus, Phi/oria, et al. 2000). Originally described by Harrison (1927) Rheobatrachus and the Geocrinia rosea group as Pseudophryne nichollsi, it was identified as a as direct developers. These genera, however, have possible variant of P. bibronii by Parker (Barbour mostly been classified in three different endotrophic and Loveridge 1929). The monotypic genus guilds by Altig and Johnston (1989), but some Metacrinia was later erected for this frog by Parker genera are added here to the nidicolous guild as (1940), but Blake (1973) proposed the species be follows: nidicolous - Phi/oria, plus Bryobatrachus referred to Pseudophryne and that the genus and Geocrinia rosea group; exoviviparous - Assa; Metacrinia be suppressed. More recently Maxson paraviviparous - Rheobatrach us. None of these are and Roberts (1985) found that Metacrinia and in the specific category of direct developers like the Pseudophryne are most closely related to the microhylids Cophixalus and Austrochaperina and lineage giving rise to Myobatrachus and the myobatrachids Arenophryne and Myobatr- Arenophryne, and retained the genus Metacrinia as aclws. Direct development has arisen in at least distinct from Pseudophryne. Further work by Read nine anuran families around the world, showing its et al. (2001) places Metacrinia as the sister clade to propensity for occurrence in distantly related Myobatrachus and Arenophryne, while Frost et al. groups and similarly, the nidicolous guild of (2006) place Metacrinia and Arenophryne in the endotrophs occurs in at least seven families same clade, with 1'v1yobatrachus being more (McDiarmid and Altig 1999). In this paper, the distantly related. Australian myobatrachid Metacrinia (closely related Little is known of the breeding biology of to Myobatrachus and Arenophryne) is also i\.1etacrinia, as observations of embryonic material confirmed as an additional direct developer. have been very limited. They live in areas of the Direct developing embryos differ in many ways highest rainfall in southwestern Australia and frogs from both exotrophic tadpoles and from other are found mainly among leaf litter or under rotting guilds of endotrophs (Altig and Johnston 1989), and logs in Karri (Eucalyptus diversicola) and Jarrah (E. 134 M. Anstis marginata) eucalypt forests away from water. They with water. Initially the clutch was not separated, can occur in association with nests of the bull ant but after two days, three embryos at the bottom of Myrmecia regularis (Barbour and Loveridge 1929; the clutch were found dead and were removed in Glauert 1945). Driscoll (1998) observed males their capsules with fine scissors. The rest of the eggs calling perched in bushes up to 50 cm above were laid out in a single layer (and some separately) ground, and they also are known to call from on moistened filter paper in a partly covered petri secluded sites (such as beneath leaf litter) on the dish kept in a darkened area during the day. As the ground, as well as from burrows made by other eggs were not found in association with water in frog species. Driscoll even reports a female calling the field, they were only moistened twice a day (with a different type of call) from a shallow with a drop of rainwater over each. burrow. Apart from one clutch found with two To avoid distortion caused by the jelly capsule in adults beneath a log near Pemberton on 17 March photographs, it was necessary to immerse embryos 1929 by W. S. Brooks (Barbour and Loveridge 1929) in water for a few minutes to see them more clearly and another by B. Knight who found a frog with a through the jelly. This was done once a day for the clutch at Springfield near Pemberton on 18 March first four weeks but reduced to once every two or 1943 (Glauert 1945), no other embryonic material three days for a shorter time during later has been previously reported. In his early field development after two embryos appeared to observations (March 1927), Brooks noted that the develop <Edema. Apart from the first two days clutch contained "a pile of 25-30 eggs each about before the clutch was separated, measurements of 3/ 16 inch [4.8 mm] in diameter". This would have live and preserved embryos were taken with an been the diameter of the external jelly capsule, as ocular micrometer attached to a Wild M5 the developing embryos were not studied with a stereoscopic microscope while embryos were microscope. Brooks states that embryos were active immersed in water (Appendix 1 and 2). Individual with obvious eyes and the capsules appeared to specimens at various stages were first anaesthetised have been "rolled in dust to retard evaporation." in 1% chlorbutol solution and then preserved in He kept them alive for more than six weeks before Tyler's fixative (1962) diluted by one third. Material they died (within their capsules), without reporting was catalogued in the Western Australian Museum further observations on their development (Barbour (WAM R133194). and Loveridge 1929). The single clutch of 12 eggs collected at Based on these limited early observations, Glauert Springfield, near Pemberton by B. Knight in 1943 (1945) stated that "eggs are laid in a hollow under a (WAM R8543/44) was examined and comparisons log or stone, where they are guarded by the parent" with the present clutch were made. Photographs of and "the eggs develop directly without any tadpole live specimens (Figures 2-5) were taken with a stage." Direct development in Metacrinia has been Nikon 070 and 60 mm macro lens. To present considered probable as calling males are not found images more clearly, waste yolk material circulating near or associated with water, and the species is inside the vitelline membrane from stage 5 that closely related to the direct developing A. rotunda obscured parts of the embryo was edited out in all and M. gauldii (Tyler 1976; Maxson and Roberts photographs except Figure 4E and F, and also 1985). Although some juvenile froglets of Figure 2H, in which the yolk released as a direct Metacrinia have been found under leaf litter in result of the worm attack was also retained. forest not near water (D. Edwards, pers. comm.), no Drawings of some stages of preserved specimens other early material was available for study. were made with a camera lucida attached to the The recent collection of a single clutch has microscope (Figure 1). Preserved specimens were enabled a detailed description of the live stained in a very weak solution of crystal violet development of this species (Table 1; Figures 1-5). before drawing. Comparisons are made between the development The staging system of Townsend and Stewart of Metacrinia and A. rotunda and M. gauldii from (1985) for E. caqui was used, as this is the only Anstis et a1. (2007), and with the well-known South direct developing species for which an appropriate American E. caqui. Observations of an attack on one staging table exists. As this system was devised embryo by a predatory nematode warm are given. purely for use in the field without a microscope, it only stages embryos based on a combination of more obvious morphological, behavioural and MATERIALS AND METHODS pigmentation features visible macroscopically such A single, freshly laid clutch of 15 eggs was as cleavage furrows (stage 1), blastopore formation collected by M. Dziminski at Coalmine Beach to neural folds (stage 2), neural tube (stage 3), first Caravan Park, 4 km west of Walpole on the limb bud development (stage 4) etc., but numerous southern coast of Western Australia on 26 March other features are combined in the classification of 2006. Sand and soil were removed from the egg each of the fifteen stages. To provide more jellies with forceps and a fine sable brush moistened information, and to set a basis for future Direct development of Metacrinia nichollsii 135 A B c ".
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