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Early developmental biology of Platymantis vitiana including supportive evidence of structural specialization unique to the Ceratobatrachidae
Abstract
Direct embryonic development belongs to one of six unique developmental guilds within the endotrophic anurans. Few studies have been conducted on the embryonic development of direct developers. Herein, we present a unique form of embryonic development for direct developers from the genus Platymantis (Family Ceratobtrachidae). We incubated fertile eggs (n=2 egg clutches; 40 eggs per clutch) of the endangered Fijian ground frog Platymantis vitiana under controlled laboratory conditions (25 1C and 100% relative humidity). Embryonic development (fertilization to hatching) took on average 29 days. Several unique embryonic structures were recorded, including the presence of very large eggs [8.5mm diameter inclusive of egg-jelly and yolk, with the largest yolk diameter (6.0 mm) recorded for the genus Platymantis], the complete loss of the usual larval mouthparts, egg-tooth, gill buds and gills. Embryonic structural specialization included large abdominal sacs with blood capillaries which are likely the main medium of gas and waste exchange in P. vitiana. We provide a novel 10-stage staging system of embryonic development for P. vitiana which may also be useful for staging other members of the Platymantis genus. Our study contributes to existing knowledge on the developmental biology of the little studied direct developing endotrophic anurans. Yes Yes
... This, together with the limited amount of data available on other direct-developing species (e.g. Patil and Kanamadi 1997;Bahir et al. 2005;Anstis 2008;Anstis et al. 2007;Narayan et al. 2011), suggests that direct development is not as stereotypical as generally assumed. ...
... Some authors also employed modified stage definitions, which accounts for a lack of correspondence of the early stages between Townsend and Stewart (1985) and other staging tables (e.g. Bahir et al. 2005;Narayan et al. 2011). To compensate for the broad divisions of early development into stages, Moury and Hanken (1995) subdivided TS 3 into three substages defined by the degree of neural fold closure. ...
... In Philautus glandulosus, they appear as lamellae and are also only present for a short period (Krishnamurthy et al. 2002). External gills have further been reported in the ceratobatrachid Platymantis vitiana (Narayan et al. 2011). In Terrarana, external gills have been reported in some species but seem to be absent in others. ...
Direct development has evolved independently several times in anurans and direct-developing species are
characterized by large-scale developmental repatterning and a complete, or near complete, absence of most tadpole specific structures. Earlier studies stressed the similarities among different direct-developing species, but more recent studies have indicated differences in the reduction of tadpole-specific structures among different taxa. Here, we describe egg deposition, clutch characteristics and embryonic development of the direct-developing squeaker frogs of the genus Arthroleptis, providing the first detailed description of
direct development in Arthroleptidae. Embryonic development in Arthroleptis is characterized by the presence of an opercular fold that still encloses the developing forelimbs, the absence of external gills and an only moderately extended tail. A comparison with published information on other direct developing anurans reveals broad dissimilarities in the formation of an opercular fold and very different tail morphology among different taxa. An egg tooth, often considered characteristic of direct-developing anurans, seems to be restricted to
NewWorld Terrarana. The embryonic diversity seen in direct developing anuran taxa argues against simplistic assumptions about the evolution of direct development.
... Its natural range has been reduced to one location on the second largest island of Vanua Levu and to four small outer islands within the Fijian archipelago, including Viwa Island, Ovalau, Gau and Taveuni [17]. The Fijian ground frogs spend majority of their life on the ground and breed only within terrestrial dense leaf litter or rotting logs [24], and have an annual breeding pattern [20,22]. The Fijian tree frogs are much smaller of the two native frog species and are currently found in some parts of the two main islands, Viti Levu and Vanua Levu. ...
... Unlike the ground frogs, the tree frogs are arboreal species (live in trees) that have a close affinity to Pandanus trees (Pandanus tectoris) and they lay eggs in leaf axils of Pandanus trees (1-2 m above the ground) from November to April [28]. Like ground frogs, the tree frogs also undergo direct development (directly hatch as miniature frogs rather than tadpoles) [24]. Thus because of their close phylogenetic relationships like other Platymantis sp. ...
... Sexes were identified via distinct 'stress calls' of male and female frogs as described earlier [15]. Adult female frogs were identified as nonvitellogenic because of no developing underbelly oocytes as earlier described by [24]. The climatic pattern on Viwa is seasonal because it is a low-lying small island [18]. ...
Studies of baseline (unstressed) and short-term corticosterone stress responses in free-living amphibians can provide crucial information on the physiological responses of different populations to environmental change. In this study, we compared baseline and urinary corticosterone metabolite responses of free living adult males and females of two closely related Fijian frogs of the Platymantis genus (Family: Ceratobatrachidae). Fijian ground frogs (Platymantis vitiana) live on the ground while Fijian tree frogs (Platymantis vitiensis) are arboreal. We captured free-living frogs and applied our moderate stress protocol (5 min handling during urine sampling at hourly intervals), with urinary corticosterone metabolite concentrations measured by enzyme-immunoassay. Mean urinary corticosterone metabolite concentrations in male and female Fijian ground frogs increased from 0 to 2 h and continued to increase to peak concentrations 5–6 h after capture. Mean baseline corticosterone concentration was significantly different
between sexes (higher in males than females) only for Fijian ground frogs. There was no significant difference between sexes in the integrated corticosterone responses for both species. Mean baseline and urinary corticosterone metabolite responses of Fijian tree frogs were lower than those of Fijian ground frogs. Corticosterone levels increased for 4–5 h in both species and began to decrease again 7 h after initial capture. Corticosterone responses were consistently higher for Fijian ground frogs than Fijian tree frogs. Individuals in both species showed markedly variable corticosterone responses over the 8 h duration of the stressor, with some individuals showing low stress responses and others showing high stress responses. The magnitude of the corrected integrated response of the ground frogs was almost twice that of the tree frogs. These differences in baseline and short-term corticosterone stress responses between these two species could be a consequence of ecological differences including micro-habitat, predator
interactions and/or competitive interactions with the introduced cane toad (Rhinella marina). Comparisons of corticosterone responses between populations and species provide a valuable tool for measuring the physiological responses of the amphibians to environmental change.
... Its natural range has been reduced to one location on the second largest island of Vanua Levu and to four small outer islands within the Fijian archipelago, including Viwa Island, Ovalau, Gau and Taveuni [17]. The Fijian ground frogs spend majority of their life on the ground and breed only within terrestrial dense leaf litter or rotting logs [24], and have an annual breeding pattern [20,22]. The Fijian tree frogs are much smaller of the two native frog species and are currently found in some parts of the two main islands, Viti Levu and Vanua Levu. ...
... Unlike the ground frogs, the tree frogs are arboreal species (live in trees) that have a close affinity to Pandanus trees (Pandanus tectoris) and they lay eggs in leaf axils of Pandanus trees (1-2 m above the ground) from November to April [28]. Like ground frogs, the tree frogs also undergo direct development (directly hatch as miniature frogs rather than tadpoles) [24]. Thus because of their close phylogenetic relationships like other Platymantis sp. ...
... Sexes were identified via distinct 'stress calls' of male and female frogs as described earlier [15]. Adult female frogs were identified as nonvitellogenic because of no developing underbelly oocytes as earlier described by [24]. The climatic pattern on Viwa is seasonal because it is a low-lying small island [18]. ...
Studies of baseline (unstressed) and short-term corticosterone stress responses in free-living amphibians can provide crucial information on the physiological responses of different populations to environmental change. In this study, we compared baseline and urinary corticosterone metabolite responses of free-living adult males and females of two closely related Fijian frogs of the Platymantis genus (Family: Ceratobatrachidae). Fijian ground frogs (Platymantis vitiana) live on the ground while Fijian tree frogs (Platymantis vitiensis) are arboreal. We captured free-living frogs and applied our moderate stress protocol (5 min handling during urine sampling at hourly intervals), with urinary corticosterone metabolite concentrations measured by enzyme-immunoassay. Mean urinary corticosterone metabolite concentrations in male and female Fijian ground frogs increased from 0 to 2 h and continued to increase to peak concentrations 5-6 h after capture. Mean baseline corticosterone concentration was significantly different between sexes (higher in males than females) only for Fijian ground frogs. There was no significant difference between sexes in the integrated corticosterone responses for both species. Mean baseline and urinary corticosterone metabolite responses of Fijian tree frogs were lower than those of Fijian ground frogs. Corticosterone levels increased for 4-5 h in both species and began to decrease again 7 h after initial capture. Corticosterone responses were consistently higher for Fijian ground frogs than Fijian tree frogs. Individuals in both species showed markedly variable corticosterone responses over the 8h duration of the stressor, with some individuals showing low stress responses and others showing high stress responses. The magnitude of the corrected integrated response of the ground frogs was almost twice that of the tree frogs. These differences in baseline and short-term corticosterone stress responses between these two species could be a consequence of ecological differences including micro-habitat, predator interactions and/or competitive interactions with the introduced cane toad (Rhinella marina). Comparisons of corticosterone responses between populations and species provide a valuable tool for measuring the physiological responses of the amphibians to environmental change.
... Most studies of anuran embryogenesis involve the use of species that possess free-living larvae that metamorphose into terrestrial adults (Chipman et al., 2000;Mitgutsch et al., 2009;Romero-Carvajal et al., 2009;among others). In contrast, there have been relatively few published studies on the embryonic morphology of direct-developing taxa (e.g., Townsend and Stewart, 1985;Nokhbatolfoghahai et al., 2010;Anstis et al., 2011;Narayan et al., 2011;Goldberg et al., 2012). Causes of this scarcity of data come from the difficulty of finding recently laid eggs that allow the acquisition of complete embryonic series. ...
... In addition, Eleutherodactylus coqui has been extensively considered a model species for direct-developing frogs and therefore most studies have included this species (Townsend and Stewart, 1985;Elinson, 1990Elinson, , 2001Hanken et al., 1997a, b;Hanken, 1999;Callery et al., 2001;Kerney et al., 2010). As embryonic development in more species is studied, however, structural and temporal variations, including the evolution of novel traits, are described (Nokhbatolfoghahai et al., 2010;Narayan et al., 2011;Goldberg et al., 2012). ...
The New World direct-developing frogs (Brachycephaloidea = Terrarana) comprise nearly a thousand species that share direct development among other putative synapomorphies, yet embryonic development in this group has been thoroughly described in only about 20 species. Here we describe the early ontogeny of the craugastorid Haddadus binotatus, making special emphasis on tail structure and development, and its differences and similarities with that of other terraranans. The morphological changes during embryonic development of H. binotatus and those of other Neotropical direct-developing species are alike, with some variation including the absence of external gills, timing of limb differentiation, and tail configuration. The tail with a rotated core axis and lateral and asymmetric fins that cover the posterior half of the embryo represents an outstanding case of developmental repatterning. We present some interpretations of the evolution of the tail and its three major aspects, the rotation of the core axis, and the origin and extensions of the fins, and pinpoint that those mechanisms underlying fin development should be fairly plastic, allowing the ontogenetic and evolutionary variation within the Brachycephaloidea clade.
... Seymour & Bradford, 1995), and exceptional respiratory structures-such as overdeveloped gills, abdominal sacs or tail fins-are frequent (e.g. Nokhbatolfoghahai et al., 2010;Narayan et al., 2011;Salica et al., 2011;Goldberg et al., 2012). In this sense, the overall, likely plesiomorphic reduction of gills and ciliation in Batrachyla could be compensated by tail morphology, including high, very thin, puckered fins, and seemingly profuse vascularization. ...
The Patagonian rainforest has environmental conditions that may have been appropriate for the evolution of different reproductive strategies in anurans. Despite its low species richness, the endemic family Batrachylidae has a wide diversity of reproductive modes. All species have exotrophic tadpoles, but oviposition sites may vary from lakes/ponds to the forest floor and tree holes. Here we study the embryonic development of five species to explore the morphological diversity and heterochronic shifts related to aquatic vs. terrestrial development. The main differences concern the length of the intracapsular period, morphology at tailbud stage, and gut and hind-limb development. Terrestrial embryos of Batrachyla have some peculiar features also reported in species with endotrophic development, such as yolk-rich eggs, poorly developed gills, precocious development of hind limbs and delayed gut coiling. Furthermore, observations on embryos releasing from the jelly layers with the vitelline membrane intact plus the likely absence of hatching gland cells at hatching stages make it likely that differences can occur in the hatching mechanism. Our results highlight that batrachylids and other neoaustraranans offer an excellent opportunity to investigate the evolution and diversity of reproductive and developmental strategies divergent from aquatic/exotrophic development.
... Direct development evolved numerous times during amphibian phylogeny (e.g., Schweiger et al. 2017), and in this context, it is reasonable to expect different sets of clade-specific features. This is already reported in several character systems exhibiting high variation in the presence, morphology, and developmental timing across anuran groups, such as gasexchange structures (e.g., gills, opercules, tails, abdominal sacs), hatching structures (egg tooth, hatching cells), adhesive glands, vent tube, and limbs (e.g., Hanken et al. 1992;Bahir et al. 2005;Anstis et al. 2007;Narayan et al. 2011;Goldberg and Vera Candioti 2015;Schweiger et al. 2017). Skeletal ontogeny seems to follow the same pattern, with heterochronic shifts likely different among groups. ...
Direct development implies transformations with respect to the anuran biphasic life cycle, including changes in embryonic anatomy. In the clade Brachycephaloidea, skeletal ontogeny is known in Eleutherodactylus coqui of the basal family Eleutherodactylidae. In this work, we study it in four species representing the two other families in the group. We worked with developmental series of Oreobates barituensis, Haddadus binotatus, Ischnocnema henselii, and Brachycephalus ephippium. Specimens were prepared following protocols of clearing and staining and histology. In the cranium, results show an overall shared pattern that, as summarized for E. coqui, combines a partial recapitulation of aspects of the ancestral biphasic ontogeny with a profound remodeling that includes lost/novel structures and heterochronic shifts of developmental events. Among these transformations are the absence of suprarostrals and trabecular horns and the precocious ossification of jaw and suspensorium. In addition, each lineage shows particular features such that skull ontogeny varies interspecifically. In turn, the morphogenesis of the axial and appendicular skeleton is highly conserved, with main variations including the extent of ossification at hatching. Along with some external features such as the egg tooth and the enveloping tail with transversely arranged fins, an ossification sequence with extremely accelerated ossification of jaws and suspensorium could be distinctive of Brachycephaloidea.
... Continuous lines correspond to brachycephaloid species and dashed lines represent non-closely related taxa. Note the wide heterochronic variation in rate and offset of stage progression among species (Anstis 2008;Anstis et al. 2011;Bahir et al. 2005;Narayan et al. 2011). an incremental number of epidermal layers, development of glands, and differentiation of two dermal strata (Duellman & Trueb 1986;Yoshizato 1992;Tamakoshi et al. 1998;Brown & Cai 2007). ...
Due to the difficulty in finding newly fresh spawn in natural environments, few embryonic developmental studies have been carried out in anurans with direct development. Here we provide detailed data on the embryonic ontogeny of Ischnocnema henselii, and compare some morphological aspects related to its developmental mode within and outside of the brachycephaloid clade. Embryonic development in I. henselii is characterized by a unicuspid egg tooth (bicuspid in most other Brachycephaloidea), external gills present, open vent tube, and tail fins with dorsoventral orientation throughout the development. We also provide the first account of skin development in direct-developing frogs, revealing that the maturation of the integument has a typical dorsal to ventral sequence of changes as in most biphasic anurans. The early onset of thyroid development seems to be consistent with the hypothesis that the evolution of direct development in anuran amphibians involved precocious activation of the thyroid axis. A comparative analysis with the still few described embryonic ontogenies for direct-developing species reveals variation in the length of the embryonic period, rate of development, size at hatching and presence/absence of external morphological characters, which suggests heterochronic shifts in the rate of species-specific stage progression. All these details reinforce the idea of the high morphological variability among direct-developing frogs.
... Large, yolk-rich, kyphotic embryos are known in some anuran species in relation to oviposition in lotic environ-ments (e.g., species of several genera of stream-breeding hylids and mantellids ;Lang 1995;Faivovich et al. 2006;Scheld et al. 2013), oviposition outside of the water (e.g., some Batrachyla, Hyalinobatrachium, Leptodactylus fuscus Townsend and Stewart 1985;De Bavay 1993;Anstis et al. 2007;Nokhbatolfoghahai et al. 2010;Narayan et al. 2011;Goldberg and Vera Candioti 2015). In our study, a relationship with oviposition site is not always clear. ...
In recent decades, a renewed interest in comparative studies of embryonic ontogeny in anurans is taking place. Toad embryos are often employed as model organisms, and scarce attention has been put on interspecific variations. In this work we analyze the development of transient embryonic and larval structures in 21 species in five genera of Bufonidae. These species vary in their ovipositional mode and the type of environments where the embryos and tadpoles develop, including ponds, streams, and axils of leaves of terrestrial or epiphytic plants. Comparative anatomical studies and sequence heterochrony analyses show that primary morphological variations occur in the morphology at the tail-bud stage, the arrangement and development of the external gills, adhesive gland type and division timing, growth of the dorsal hatching gland on the head, configuration of the oral disc, emergence and development of the hind limbs, and presence of the abdominal sucker. Some of these transformations are best explained by phylogeny (e.g., early divergent taxa of bufonids have embryos with kyphotic body curvature, Type C adhesive glands, and a very small third pair of gills). Other traits might be correlated with reproductive modes (e.g., phytotelmata embryos hatch comparatively late and show an accelerated development of hind limbs). Because these actual variations are not well studied (e.g., less than the 10% of the known diversity of bufonids has been studied from this perspective), comprehensive analyses are required to interpret character evolution and the relationship with reproductive modes within the family.
... two genera in the Philippines (but not in Palawan) may date INTRODUCTION The frog family Ceratobatrachidae (currently Platymantis, Batrachylodes, Discodeles, Ceratobatrachus, Palmatorappia, and portions of the genus Ingerana) is a remarkable assemblage of amphibians distributed throughout the Philippines, Palau, eastern Indonesia, New Guinea, the Solomon−Bismarck−Admiralty archipelagos, and the islands of Fiji (Brown, 1952;Zweifel, 1960Zweifel, , 1969Brown & Tyler, 1968;Edgar & Lilley, 1993;Allison, 1996;Brown, 1997;Günther, 1999;Alcala & Brown, 1999;Inger, 1999;Tyler, 1999). Ceratobatrachids are noted for conspicuous characteristics of morphology (Boulenger, 1886(Boulenger, , 1887Brown, 1952;Norris, 2002), larval direct development (Alcala, 1962;Brown & Alcala, 1982), including unique structures and patterns of embryonic growth (Thibaudeau & Altig, 1999;Narayan et al., 2011), and the ability to colonize habitats that otherwise conspicuously lack ranoid frogs (small, arid islands, dry limestone habi-tats, and high-elevation mossy rain forests with no standing water; Menzies, 2006;Pikacha, Morrison & Richards, 2008). This ability to persist and reproduce in environments lacking standing fresh water has been hypothesized to represent a key innovation that has facilitated dispersal and colonization across the South-West Pacific, and in the literature this life-history trait is associated with the presence of Platymantis on distant oceanic islands such as Palau (Crombie & Pregill, 1999) and Fiji (Gorham, 1965, 1968Tyler, 1979;Ryan, 1984;Gibbons, 1985;Kuramoto, 1985Kuramoto, , 1997Ota & Matsui, 1995;Narayan, Christi & Morley, 2008;Zug, 2013). ...
We present a near comprehensive, densely sampled, multilocus phylogenetic estimate of species relationships within the anuran family Ceratobatrachidae, a morphologically and ecologically diverse group of frogs from the island archipelagos of Southeast Asia and the South-West Pacific. Ceratobatrachid frogs consist of three clades: a small clade of enigmatic, primarily high-elevation, semi-aquatic Sundaland species currently assigned to Ingerana (for which we erect a new genus), which is the sister taxon of two large, monophyletic radiations, each situated on islands on either side of Wallace's Line. One radiation is composed of Philippine species of Platymantis and the other contains all taxa from the eastern Indonesian, New Guinean, Solomon, Bismarck, and Fijian archipelagos. Several additional genera (Batrachylodes, Discodeles, Ceratobatrachus, and Palmatorappia) are nested within Platymantis, and of these Batrachylodes and Discodeles are nonmonophyletic. To address the widespread paraphyly of the genus Platymantis and several additional nomenclatural issues, we undertook a wholesale nomenclatural reorganization of the family. Given our partially unresolved phylogeny, and in order to impart a conservative, stable taxonomy, involving a minimal number of genus-species couplet changes, we propose a conservative classification representing a few compromises. These changes are designed to preserve maximally the presumed original intent of taxonomy (widely used group names associated with morphological and ecological diversity of particular species or groups of species) while implementing a hierarchical system that is consistent with the estimate of phylogeny based on new molecular data. © 2015 The Linnean Society of London
... Nevertheless, preliminary data on the early development of Platymantis dorsalis and Platymantis hazelae from Philippines (Alcala, 1962) cannot completely correspond to formal requirements for the nonstandard pattern of cleavage in these frogs. Note that a recent detailed morphological study (Narayan et al., 2011) has dealt only with organogenesis in the embryos of Platymantis vitiana from Fiji. There are, at last, works describing the direct development in Philautus (Rhacophorinae) and related genera from south Asia (Alcala and Brown, 1982;Bahir et al., 2005;Kerney et al., 2007). ...
Literature describing peculiarities of embryonic cleavage in various frog families is reviewed. In a number of representatives of Eleutherodactylidae, Hemiphractidae, Myobatrachidae, Rhacophorinae, and some other families (subfamilies), the synchrony of animal blastomere divisions is lost already at early stages of the cleavage in large, yolk-rich, and unpigmented or weakly pigmented eggs. The "standard" frog cleavage (usually exemplified in embryological textbooks by Xenopus laevis, Rana pipiens or Rana temporaria), which includes about 10–12 synchronous divisions of comparatively small pigmented eggs with moderate yolk content, is characteristic not of all anuran amphibians. The evolutionary relationships between two main types of anuran early embryogenesis and a putative link of reproductive mode and cleavage pattern are discussed. For the advanced frogs (Neobatrachia), the standard pattern of cleavage (usually occurring in lentic water) seems to be a more primitive condition and several derived reproductive modes may produce similar effects on the early cleavage pattern. Thus, the repeated evolutionary transitions to the "nonstandard" pattern of cleavage might have occurred in various neobatrachian frog families.
... Although we did not focus on a detailed study of gastrulation in Phyllomedusa, the resulting configuration of the embryos is almost identical to that described in Hyperolius. Large, yolk-rich eggs, and, when early development has been described, embryos twisted around the yolk mass are also seen in many other species, often in relation with oviposition in lotic environments (e.g., species of several genera of stream-breading hylids; Faivovich et al. 2006; Lang 1995), or oviposition outside the water and endotrophic development (e.g., Myobatrachus gouldii, Philoria sphagnicola, Platymantis vi tianus, and several Terrarana; Anstis et al. 2007, De Bavay 1993, Narayan et al. 2011, Nokhbatolfoghahai et al. 2010, Townsend & Stewart 1985). ...
We present a comparative study of the early development of Phyllomedusa azurea and P. sauvagii, in order to discuss morphological and ontogenetic variations of ecological and systematic interest. Similarities between the species in-clude the large, yolk-rich eggs, the curled embryos at tail bud stage, the large external gills, and the sequential development of mouthparts. The main difference lies in the morphology and development of adhesive glands. Most of these characters can be related to leaf nest spawning and a long intracapsular period. The plasticity in the time of hatching (as observed in the related genus Agalychnis), and its relation to embryonic and larval morphology and ecology remain open questions in this genus.
Anurans have served as models in evolutionary studies on reproduction and development. Several generalizations have emerged but it is unclear whether they represent the diversity of the entire group. We studied the development of two species of the Neotropical family Cycloramphidae. Frogs in this family have peculiar spawning sites and developmental biologies. Whereas some cycloramphid tadpoles are exotrophic, quasi-terrestrial and thrive in films of water that flow over rocky outcrops, others are endotrophic, terrestrial and complete their development outside the eggs laid on the forest floor, under logs or in crevices. Cycloramphid tadpoles have aspects of their morphology distinct from those of pond and stream dwellers; they hatch in more advanced stages of development and have typical tadpole structures, either in a modified form or absent. Herein we present a study of the tadpoles of C. lithomimeticus and T. miliaris, in order to document and discuss alterations in the ontogeny of several larval structures. These changes seem to be associated with adaptations to life in the peculiar habitats where the tadpoles thrive. We infer that the observations we present are explained by development being associated with aspects of terrestrialization and endotrophism.
The vocal repertoire of males of Cornufer vitianus from the lowland mangrove forests of Viwa Island, off the coast of Viti Levu, Fiji is described. All calls were placed into two categories: those with a high fundamental frequency, and those with a low fundamental frequency. Within each category, there is relatively high call variation. Individual males are capable of producing both the low- and high-frequency calls; some males produce predominantly the high-frequency call, others are low-frequency callers, and others alternate between the two forms. C. vitianus is among the most sexually size dimorphic amphibians known. Females were conspicuously and significantly larger than males, and we found the ratio of the mean female-to-male snout–vent lengths of 2.22. Extreme sexual size dimorphism (SSD) is a trait rare among anurans as a whole, yet is most often seen among species of the genera Cornufer and Platymantis of the western Pacific. A hypothesis is put forward relating call variability and SSD in C. vitianus.
Introduction:
Forest frogs that undergo direct development (no tadpole stage) rely heavily on moist microhabitats for their survival. Objective: To describe the abundance and microhabitat use and some aspects of the breeding behaviour of the threatened forest frog Platymantis hazelae at Twin Lakes Balinsasayao Natural Park, Negros Island, Philippines. Methods: From September 2016 to February 2017, we surveyed Platymantis hazelae using 27 (400 m²) plots in Twin Lakes Balinsasayao-Danao Natural Park in Negros Oriental, Philippines. Results: After a total of six months survey P. hazelae was found abundant in the montane zone with mean density ranging from 30.56±6.94 to 86.11±15.65 ind./ha. Fourteen environmental variables were measured and subjected to multivariate principal component analysis (PCA). PCA revealed that rainfall, altitude, relative humidity, and air temperature influenced the density of P. hazelae. Screwpines (Pandanus) leaf axils and leaves (51.56 %) and palm leaves (14 %) were the preferred microhabitats for the species. Details of physical characters of embryos and froglets are also described. Conclusions: P. hazelae was found abundant in higher elevations (sub-montane and montane zones) where ambient temperature was generally lower, higher rainfall and relative humidity and microhabitats (e.g. screwpines) remain intact and abundant.
We describe the abundance and microhabitat use and some aspects of the breeding behaviour of the threatened forest frog Platymantis hazelae at Twin Lakes Balinsasayao Natural Park, Negros Island, Philippines. Fourteen environmental variables were measured and subjected to multivariate principal component analysis (PCA). PCA revealed that rainfall, altitude, relative humidity, and air temperature influenced the density of P. hazelae. After a total of six months survey (September 2016-February 2017) using 27 (400m2) plots, P. hazelae was found abundant in the montane zone with mean density ranging from 30.56±6.94 to 86.11±15.65 ind./ha. Screwpines (Pandanus) leaf axils and leaves (51.56 %) and palm leaves (14%) were the preferred microhabitats for the species. We recorded male-guarding behaviour for the first time in this species. Details of physical characters of embryos and froglets are also described.
In the life of an organism (ontogeny), phenotypic changes happen throughout the time. This contribution is a review of: a) terms and definitions used in studies of the ontogeny, b) the importance to distinguish between shape variation (development) and size variation (growth); and c) the need to consider the real time (age) in which the ontogeny takes place. Based on available information about the ontogeny among tetrapods with emphasis in anurans and nonavian sauropsids, it is outlined the need to increase the information about the ontogeny for comparative studies. We denote the relevancy to get tables of development to identify ontogenetic variation, the study of three fundamental components of ontogenies (it forms- size-time), and the processes that the age organizes (development and growth) to contribute the paradigm of the Evolution of the Development.
Australia and New Zealand are home to a remarkable and unique assemblage of flora and fauna. Sadly though, by virtue of their long isolation, and a naïve and vulnerable biota, both countries have suffered substantial losses to biodiversity since European contact. Bringing together the contributions of leading conservation biologists, Austral Ark presents the special features and historical context of Austral biota, and explains what is being conserved and why. The threatening processes occurring worldwide are discussed, along with the unique conservation problems faced at regional level. At the same time, the book highlights many examples of conservation success resulting from the innovative solutions that have been developed to safeguard native species and habitats in both New Zealand and Australia. Austral Ark fills an important gap regarding wildlife gains and declines, and how best to take conservation forward to keep this extraordinary area of the world thriving.
Physiological stress assessment is important for in-situ conservation and captive management of threatened wildlife. Leukocyte (white blood cell) evaluation, especially the neutrophil : lymphocyte (N : L) ratio, provides a logical representation of experimentally elevated corticosterone (stress hormone) in amphibians. Urinary corticosterone enzyme-immunoassay (EIA) is a rapid non-invasive tool for assessing stress responses in amphibians. To our knowledge, no one has explored the relationship between N : L ratio and urinary corticosterone in wild amphibians in a non-experimental way. This study provides a comparative assessment of relative leukocyte numbers, N : L ratios and urinary corticosterone responses of the endangered Fijian ground frog (Platymantis vitiana) during transportation and captivity. Adult frogs (n = 40) were collected from Viwa, Fiji Island for captive breeding. Frogs showed significant changes in leukocyte proportions during transportation and captivity. N : L ratios were higher 6 h after transportation and over 5 and 15 days in captivity. Urinary corticosterone responses of the frogs were also higher 6 h after transportation and after 5 and 15 days in captivity. All leukocyte proportions, N : L ratios and urinary corticosterone concentrations of the frogs returned near baseline levels after the frogs were kept in an environmentally enriched outdoor enclosure for over 25 days. These results highlight the value of leukocyte evaluation and urinary corticosterone EIAs as physiological tools for evaluating stress in amphibians.
Annual cycles of reproductive steroid metabolites were measured in urine collected from free-living and captive tropical endangered Fijian ground frogs (Platymantis vitiana) a terrestrial breeding. Free-living frogs were sampled on Viwa Island, Fiji and captive frogs were maintained in an outdoor enclosure in Suva, Fiji. Urinary estrone, progesterone and testosterone metabolite concentrations increased in male and female frogs after hCG challenges, with clear peaks in steroid concentrations 2 or 3 days after the challenges. There were annual cycles of testosterone metabolites in wild and captive males, and of estrone and progesterone metabolites in wild and captive females. Peaks of steroid concentrations in the wet season corresponded with periods of mating and egg laying in females in December and January. Steroid concentrations declined in January and February when maximum egg sizes in females were also declining. Body weights of wild male and vitellogenic female frogs showed annual cycles. Body weights of non-vitellogenic female frogs varied significantly between months, although there was no clear pattern of annual changes. Body weights of the 3 captive male frogs and 4 captive female frogs were similar to those of the wild frogs. Estrone metabolites were 80% successful in identifying non-vitellogenic females from males. The results suggest that the Fijian ground frog is a seasonal breeder with an annual gonadal cycle, and this species is likely to be photoperiodic. Urinary steroid measurements can provide useful information on reproductive cycles in endangered amphibians.
Many frogs lay their eggs in water; the development of these frogs is well-known. However, many frogs reproduce on land; their eggs are large and have an altered early development. As examples, Gastrotheca riobambae broods its embryos in a pouch on the mother's back, and Eleutherodactylus coqui exhibits direct development with no tadpole stage. We provide practical information on obtaining eggs and embryos from these terrestrial-breeding species and on analyzing their development. Our aim is to make these species more accessible to researchers who are interested in the developmental and evolutionary consequences of terrestrial development.
We incubated Pseudophryne bibronii eggs at selected $T_{a}$ (7°, 12°, 17°, 22° C) and substrate waterpotentials (0 and -25 kPa) to determine their effects on rate of O₂, consumption ( $\dot{V}o_{2}$ ) of the embryos, incubation time, growth rate, and differentiation rate. Incubation to median hatching stage (stage 27) increased from 17 d at 22° C to about 140 d at 7° C, and $\dot{V}o_{2}$ , increased in proportion to age at all temperatures. At 0 kPa water potential, the total O₂ consumed until hatching stage decreased from about 1.2 mL at 7°C, to 0.81 mL at 12°C, to a low of 0.58 mL at 17° C, and increased slightly to 0. 67 mL at 22° C. However, gut-free dry mass of 12° C hatchlings was significantly higher then those at 17° and 22° C, so the energy cost of producing 1 mg of dry, gut-free embryo was similar (0. 47-0.55 mL/mg) between 12° and 22°C. Incubation at lower water potential (-25 kPa) reduced $\dot{V}o_{2}$ , by 19%-28% and retarded growth rate but did not affect differentiation rate or incubation time.
Many herpetofauna species in the Pacific region have undergone dramatic declines due to invasive species, primarily introduced predators. Fiji has two species of endemic frogs (Family Ranidae, Genus Platymantis) one of which, the Fiji Ground Frog, P. vitianus, has been extirpated from much of its original range due to the mongoose Herpestes javanicus. We conducted a short-term follow up survey to confirm an earlier report (September 2003) of the co-existence between mongoose and the ground frog on mainland Fiji (Vanua Levu). We used systematic nocturnal and diurnal surveys to census the frog fauna of Waisali Reserve and described microhabitat and threatening processes. A series of key management actions are outlined to facilitate the long-term conservation of this frog in the reserve.
SYNOPSIS. The primitive, or ancestral reproductive mode for Recent amphibians involves a complex, biphasic life history. Yet evolutionarily derived, alternate modes are seen in all three living orders and predominate in some clades. Analysis of the consequences and mechanistic bases of one such mode-direct development-can provide insights into the evolutionary opportunities and constraints conferred by the ancestral metamorphic ontogeny. Direct development in the anuran genus Eleutherodactylus involves fundamental alterations to many features of embryonic and posthatching development. At hatching, young emerge as fully formed, albeit tiny versions of the adult; most larval features are absent. Pervasive changes in ontogenetic timing, in particular the precocious (embryonic). formation of many adult structures, appear to be correlated with early development of the thyroid axis, although responsiveness to exogenous thyroid hormone is diminished or even lacking in at least some peripheral tissues. Changes in cranial patterning are likely mediated by the embryonic neural crest, although many gross features of crest biology are highly conserved. Laboratory-based analyses of direct development and other derived reproductive modes in amphibians, using contemporary methods developed for more standard, "model" organisms, may contribute important insights into life-history evolution that complement those derived from analyses of morphology, ecology and phylogeny.
Terrestrial oviposition with free-living aquatic larvae is a common reproductive mode used by amphibians within the central Amazonian rainforest. We investigated the factors presently associated with diversity of microhabitats (waterbodies) that may be maintaining the diversity of reproductive modes. In particular, desiccation, predation by fish, competition with other anurans and water quality were examined in 11 waterbodies as possible forces leading to the evolution of terrestrial oviposition. Predation experiments demonstrated that fish generally do not eat anuran eggs, and that predacious tadpoles and dytiscid beetle larvae are voracious predators of anuran eggs. The percentage of species with terrestrial oviposition was only weakly correlated with the occurrence of pond drying, pH and oxygen concentration, suggesting that anurans in this tropical community are able to use the range of water quality available for egg development. There was a tendency for terrestrial oviposition to be associated with the number of species of tadpoles using the waterbody, but we consider this to be spurious as there was no obvious competitive mechanism that could result in this relationship. The percentage of species with terrestrial oviposition was significantly positively related to our index of egg predation pressure, and negatively related to our index of fish biomass. Egg predation pressure was also negatively related to the index of fish biomass. These results allow us to discount as improbable the hypothesis that predation by fish on anuran eggs was an important selective pressure leading to terrestrial oviposition in this community. The strong positive relationship between terrestrial oviposition and our index of egg predation pressure indicates that these predators have exerted, and are exerting, a significant selective pressure for terrestrial oviposition. The strong negative relationship between the occurrence of fish and the egg predators suggests the surprising conclusion that the presence of fish actually protects aquatic anuran eggs from predation in this tropical system, and allows aquatic oviposition to dominate only in those waterbodies with moderate to high densities of fish. Our results suggest that terrestrial oviposition is a fixed predator avoidance trait.
This paper reports on the terrestrial nesting behaviour and biometrics of eggs and froglets of the Fijian ground frog, Platymantis vitianus observed on Viwa Island (900m east of the mainland Vitilevu, Fiji Islands), including daytime choices of micro-habitats and variations in capture rates in the sex-age classes of adults and metamorphs with respect to in-situ rainfall conditions. More adult males and gravid females were captured during the wet months of November until January. Metamorphs were more common subsequent to these months. Furthermore, egg masses of P. vitianus were discovered on Viwa Island for the first time, two nests were located underneath rotten logs during high rainfall month of December, 2007. It is highly probable that the reproductive cycle of P. vitianus is continuous while courtship and nesting events are influenced by the variable and higher rainfall months on Viwa Island.
The life-histories of 11 Philippine frogs (8 ranids, 2 rhacophorids, and 1 microhylid) occurring on Negros Island are discussed in relation to their ecology, evolution, and classification. The basis for the discussion is data obtained both in the field and in the laboratory during the period, 1954-1958. Amphibian life-history characters may be interpreted as (1) those due to adaptive radiation, and (2) those which are stable characters. The stable characters can be used as indicators of phylogenetic relationships of different species. Some reproductive and developmental adaptations of the Negros frogs studied include: the laying by some species of eggs with sticky capsules for attachment to objects in the streams, the rapid rate of development of those eggs laid in temporary water, and some structural modifications in the larvae enabling them to live in the different environments. These modifications include depressed bodies, strong tail muscles, and reduced body and tail fins by larvae characteristic of streams; subspherical bodies, weak tail muscles, and high body and tail fins by larvae of the pond type; and the lack of typical larval structures with the development of functionally equivalent organs (e.g., abdominal sacs instead of gills as respiratory organs in Cornufer) among species undergoing direct development. Small eggs and large clutch size are typical of species ovipositing in water, whereas large eggs and small clutch size are typical of those ovipositing out of the water. More than fifty per cent of the species studied lay eggs out of the water. The smallest eggs develop wholly in water through metamorphosis; the largest eggs develop within the egg capsules without passing through the aquatic larval stages; eggs of intermediate size pass the embryonic stages out of the water but pass through the larval stages in the water. These specializations are correlated with the trend toward direct development as discussed by other authors. Of the 11 species considered in this paper, 3 belonging to the genus Cornufer undergo a terrestrial, direct development, and 2 species of the genus Rhacophorus and 2 species of Rana lay eggs that undergo embryonic development out of the water. The remaining species pass through the embryonic and the larval development in water. The life-histories of the Philippine species studied in general confirm the taxonomic status given them by Inger.
The Puerto Rican frog Eleutherodactylus coqui has terrestrial reproduction and direct development, as is the case for all known species of this large, neotropical group. To facilitate field measurements of embryonic age in E. coqui, a staging table was developed based on changes in the external morphology of embryos. Pre-hatching development was divided into 15 stages. Principal diagnostic features include formation of external gills, progressive pigmentation of the eyes, growth and differentiation of the limbs, development of endolymphatic calcium deposits, expansion of a pigmented body wall, growth of a large, vascularized tail and changes in embryonic behavior. We have used the table to stage the eggs of E. antillensis and E. portoricensis, related Puerto Rican species. A literature review suggests that our table may be useful as a general staging scheme for the genus.
Many taxa have evolved complex life cycles featuring a dramatic shift in habitat or resource use at metamorphosis. Despite their prevalence and unique characteristics, we understand little about the adaptive properties and evolution of these life histories. I offer a conceptual framework that considers how size-specific growth and mortality rates in both habitats interact with size at metamorphosis to affect lifetime fitness. This model predicts the size at metamorphosis that maximizes fitness, and I use this framework to interpret the wide variation in the life history structure of the amphibians. In particular, I speculate on the adaptive significance of the tadpole stage of the anurans and on the cause of variation in the size at metamorphosis both between and within anuran families. Further, I predict the conditions under which direct development or paedomorphosis will be selected for, and I offer hypotheses on the selective factors that may contribute to the three-stage life history of the newts. Fin...
The first part of this synthesis summarizes the morphology of the jelly layers surrounding ail amphibian ovum. We propose a standard terminology and discuss the evolution of jelly layers. The second part reviews the morphological diversity and arrangement of deposited eggs-the ovipositional mode; we recognize 5 morphological classes including 14 modes. We discuss some of the oviductal, ovipositional, and postovipositional events that contribute to these morphologies. we have incorporated data from taxa from thronghout the world but recognize that other types will he discovered that may modify understanding of these modes. Finally, we discuss the evolutionary context of the diversity of clutch structure and present a first estimate of its evolution.
This paper reports on the terrestrial nesting behaviour and biometrics of eggs and froglets of the Fijian ground frog, Platymantis vitianus observed on Viwa Island (900m east of the mainland Vitilevu, Fiji Islands), including day-time choices of micro-habitats and variations in capture rates in the sex-age classes of adults and metamorphs with respect to in-situ rainfall conditions. More adult males and gravid females were captured during the wet months of November until January. Metamorphs were more common subsequent to these months. Furthermore, egg masses of P. vitianus were discovered on Viwa Island for the first time, two nests were located underneath rotten logs during high rainfall month of December, 2007. It is highly probable that the reproductive cycle of P. vitianus is continuous while courtship and nesting events are influenced by the variable and higher rainfall months on Viwa Island.
The direct developing frog, Eleutherodactylus coqui, serves as a model for a divergent, derived pattern of anuran development. Reproduction and development occur normally in captivity, although individual embryos and sometimes entire clutches exhibit edema. Edematous embryos have abnormal pronephroi, as judged by histology and by alkaline phosphatase staining. The pronephric defects would be sufficient to account for the edema. The first indicator of later edema is loss or reduced development of the forelimbs. The coupling of forelimb and pronephric abnormalities is likely due to insufficient retinoic acid. The same syndrome can be produced experimentally by treatment with citral, an inhibitor of retinoic acid synthesis. The involvement of retinoic acid in forelimb development, found previously in other vertebrates, can now be extended to anuran amphibians. Reduced forelimb development in embryos may be a useful way to detect insufficient dietary vitamin A in reproductive colonies of direct developing frogs and of other vertebrates.
A table of development (25 stages) for the period of incubation in the pouch was constructed for Gastrotheca riobambae; it can be used to stage embryos of other egg‐brooding hylids. Analysis of embryonic weights during incubation shows that the mother does not contribute nutrients, but gases and other factors are probably exchanged between mother and embryos.
According to species, incubation on the back of the mother is carried to the froglet or to the tadpole stages. Development in these hylids is characterized by specialized gills, the bell gills derived from the branchial arches. In some species, the bell gills derive from the first branchial arch and cover less than 50% of the embryo, while in others, the bell gills come from both branchial arches I and II and cover from less than 50% to 100% of the embryo. The most complex bell gills derive from the fusion of the two branchial arches.
The majority of egg‐brooding hylids live in tropical forests and carry development to the froglet stage. Tadpoles are produced by species of Flectonotus , Fritziana , and Gastrotheca . Tadpole‐producing species of Gastrotheca have the most complex reproductive adaptations among egg‐brooding hylids Acceleration and retardation in development seem to have played important roles in the evolution of these frogs. The evolutionary trend has been toward direct development, i.e., disappearance of the free‐living larval stages through maternal incubation, and later to a recovery of the free‐living tadpole stages in species of Gastrotheca with the most complex reproductive adaptations.
I studied the ecology of parental care behaviors displayed by two closely related sympatric species of microhylid frogs in Papua New Guinea that occupy different microhabitats. Adult removal experiments on the terrestrial frog Hylophorbus rufescens and the undescribed arboreal frog Oreophryne sp. A demonstrate a significant positive effect of parental attendance on offspring survivorship and differential causes of egg mortality between microhabitats. Desiccation was the primary cause of egg mortality for the arboreal frog, whereas predation was the main source of mortality for the terrestrial frog. These selection pressures (desiccation and predation) are comparable to two of Wilsons prime movers of the evolution of parental care (harsh environment and predation) and may have driven and/or are maintaining the evolution of parental care behaviors in these Papuan microhylid frogs. These results highlight microhabitat-specific selection pressures in the evolution and maintenance of parental care behaviors.
We present research and management implications for captive propagation of the endangered Fijian Ground Frog Platymantis vitiana to develop methods for supplementing populations in the wild. In 2004, a captive propagation program was instituted at Kula Ecopark, Sigatoka, Fiji. However, there was little success with only a single froglet reared after three years. In 2006, a more intensive programme was undertaken between the University of the South Pacific (USP), Kula Ecopark and the community on Viwa Island. The aim of this programme was to create an outdoor enclosure to mimic natural habitat conditions so the frogs could exhibit natural breeding behaviour. A total of 39 froglets was reared after one year of this programme. We provide information on the methods of captive management, reproductive biology, captive diet varieties, and on problems of rearing froglets in captivity. This research is useful baseline information in guiding captive propagation techniques in zoological parks like the Kula Ecopark and for organizations such as the National Trust of Fiji.
Annual cycles of reproductive steroid metabolites were measured in urine collected from free-living and captive tropical endangered Fijian ground frogs (Platymantis vitiana) a terrestrial breeding. Free-living frogs were sampled on Viwa Island, Fiji and captive frogs were maintained in an outdoor enclosure in Suva, Fiji. Urinary estrone, progesterone and testosterone metabolite concentrations increased in male and female frogs after hCG challenges, with clear peaks in steroid concentrations 2 or 3 days after the challenges. There were annual cycles of testosterone metabolites in wild and captive males, and of estrone and progesterone metabolites in wild and captive females. Peaks of steroid concentrations in the wet season corresponded with periods of mating and egg laying in females in December and January. Steroid concentrations declined in January and February when maximum egg sizes in females were also declining. Body weights of wild male and vitellogenic female frogs showed annual cycles. Body weights of non-vitellogenic female frogs varied significantly between months, although there was no clear pattern of annual changes. Body weights of the 3 captive male frogs and 4 captive female frogs were similar to those of the wild frogs. Estrone metabolites were 80% successful in identifying non-vitellogenic females from males. The results suggest that the Fijian ground frog is a seasonal breeder with an annual gonadal cycle, and this species is likely to be photoperiodic. Urinary steroid measurements can provide useful information on reproductive cycles in endangered amphibians.
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