Southern Gastric Brooding Frog

Rheobatrachus silus was a medium-sized frog with a snout-vent-length of 33-41 mm for males, and snout-vent-length of 44-54 mm for females. The skin was finely granular dorsally and smooth ventrally. The snout was round and blunt, and nostrils were directed upwards. The eyes, also directed upwards, were large and projected outwards. The eyes were close together and were located to the front of the head. The tympanum was hidden. The toes were fully webbed to the tip, but the fingers did not have webbing. All of the digits had small discs. The tadpoles were bulbous, pale, low-finned, and did not have keratinized mouthparts (CITES 2013). Rheobatrachus silus could be differentiated from its sister taxa by its distribution, color pattern, and mottled webbing. It was also smaller than R. vitellinus (CITES 2013).The dorsal coloration ranged from olive to almost black and it had small light and dark patches scattered throughout. There was a dark streak that ran from the eye to the base of the forelimb. The limbs had dark crossbars and the digits and webbings had a variety of pale and dark patches. The white or cream ventral surface had yellow markings on the limbs. Tadpoles brooded in the stomach and initially lacked any pigmentation on their skin (Tyler and Davies 1983).Species Authority: The species authority is Liem 1973.Phylogenetic Relationships: Rheobatrachus silus was one of two gastric-brooding frogs, the other being its sister species R. vitellinus. R. vitellinus is also thought to be extinct; the last wild sighting was in 1985 (CITES 2013).Etymology: The common name of this species refers to its eccentric reproductive behavior (see “Life History”). This frog has been part of the Lazarus Project at the University of New South Wales whose goal is to bring the frog back to life. The Lazarus Project team has recovered cell nuclei from tissues from the 1970s and kept frozen for 40 years. Their goal is to clone the frog by implanting these cell nuclei into fresh eggs from another frog species. The researchers used a technique called somatic cell nuclear transfer to do this. They took the fresh eggs of the barred frog and destroyed the nucleus manually or with UV radiation. They replaced the egg nuclei with a dead nuclei from R. silus. Some of the eggs began to divide and grow to early embryo stage. As of March 2013, none of the embryos survived more than a few days, but researchers confirmed that the dividing cells contained genetic material from R. silus (Yong 2013).

Rheobatrachus silus was first discovered in 1972, although there was a possible sighting in 1914 in the Blackall Ranges of southeast Queensland in Australia. The species was restricted to an elevation of 350 - 800m above sea level and its geographic range was limited to 1,400 km2. The species was endemic to southeast Queensland and found in the Blackall and Cononale Ranges between Coonoon Gibber Creek and Kilcoy Creek. Found in Kondalilla and Conondale National Parks, Sunday Creek State Forest, State Forest 311, Kenilworth State Forest, and from private land not in these areas, it primarily inhabited the streams of Mary, Stanley, and Mooloolah Rivers (Hines et al. 1999). It inhabited rainforests, wet sclerophyll forests, and tall open forests that had a closed understory. The forests were closely associated with rocky mountain streams, rock pools, and soaks (Czechura 1991). The rock pools had to be deep enough that the frog could sit in the water with its head out and be able to submerge safely in it. The frog only sat fully exposed on the rocks if there was light rain (Ingram 1983). Although it was considered both a terrestrial and aquatic species, it preferred to live in mostly permanent water that only dried up in years of low rainfall and was never observed to be more than four meters from water. In spring and summer, the frogs were located in or at the edge of rock pools among the leaf litter, under or between stone, or in the crevices around the edge. Its winter habitat was unknown, but there is speculation that individuals hibernated in deep crevices in terrestrial or underwater rocks (Ingram 1983).

The species underwent a rapid decline in 1979 and was last sighted in the wild in September 1981 in Blackall Range. This occurred at the same time as a sympatric species, Taudactylus diurnus, commonly known as the southern day frog, went extinct (Czechura and Ingram 1990). The last specimen of R. silus in captivity died in November 1983 (Tyler and Davies 1985). In 1995, an intensive “frog search” occurred in Conondale Range, and over 50 surveys have been conducted in an attempt to find the species, but no frogs have been sighted. Since then, the species is believed to be extinct. The reason for the extinction of R. silus is unknown. There were stream catchments due to logging between 1972 and 1979 while R. silus inhabited the area (Hines et al. 1999). No studies have been done on the effects of logging on the populations, but the populations continued to persist through it (CITES 2013). There is a possibility that the chytrid fungus caused the decline in R. silus. This infectious disease, caused by the fungal pathogen Batrachochytrium dendrobatidis, has been the cause of the decline and extinction of at least 13 other rainforest frog species in Queensland, Australia that inhabited high elevations. Feral pigs, weed invasion (especially the mistflower Ageratina riparia), and altered stream flows threaten its potential habitat (CITES 2013; Hines et al. 1999).

As the common name of Southern Gastric Brooding frog suggests, female R. silus brooded young within the stomach and gave birth through the mouth. The eggs averaged 5.1 mm in diameter and had large yolk sacs that nourished the embryos as they developed. Fertilized eggs or early stage larvae were presumably swallowed by the female and completed their development in the stomach (Tyler and Carter 1982). The production of hydrochloric acid in the stomach of the female ceased during brooding, which was caused by hormones produced by the young that altered the structure and physiology of the mother (Tyler et al. 1983). The number of eggs in gravid females (approximately 40) exceeded the number of juveniles found to occur in the stomach (21-26). It is not known whether the female ingested the excess eggs or if they were simply not swallowed (Tyler 1989). After 6-7 weeks, the females gave birth to up to 25 young (Tyler and Davies 1983a). In the brooding stage, the mother would cease eating until her juveniles were released after 36-43 days as fully formed metamorphs. They would exit the mother through her mouth (Ingram 1983). After the juveniles exit the mother, the digestive tract returned to normal and her feeding habits would return within four days of the young’s release (Tyler et al. 1983). The female probably would not have bred more than once per breeding season due to the duration of brooding (Ingram 1983).Tadpoles developed in a manner similar to the aquatic tadpoles of other species, but lacked labial teeth, and formed the intestines at a later stage of development (Tyler 1989). Rheobatrachus silus has been observed to forage and take insects from both land and water (Ingram 1983). In an aquarium situation, Lepidoptera, Diptera and Neuroptera were eaten (Liem 1973). It was preyed upon by birds, fish, and other aquatic fauna (CITES 2013). Males, females and juveniles appeared to have limited home ranges, although juveniles and gravid females were particularly immobile (females carrying young tend to be sedentary). Adult males primarily inhabited deeper pools; the females and juveniles inhabited pools that were newly created after the rain, but only if the pools contained stones or leaf litter. Only two juveniles out of ten were found to have moved more than 3 m between observations. Juveniles were mobile in the sense that they would move to newly created pools, but once stationed there they usually remained in that area. During a breeding season, the home range of females and males was estimated to be 0-3.4 m (n=4) and 0-6.2 m (n=10) respectively (Ingram 1983). Ingram (1983) also reported the distance traveled along a stream by seven individuals between seasons. Four females moved 1.8-46 m, and the males moved 0.9-53 m. Only three individuals moved more than 5.5 m (46, 46, and 53 m respectively) and it would appear that they remained within the same pool or group of pools throughout the breeding season, only moving away during periods of high flow or flooding. Non-breeding winter habitat is unknown (Ingram 1983). Breeding activity occurred between October and December, during the warmer months, and the breeding season appeared to be dependent on the summer rains. Males called from rock crevices above pools (Ingram 1983). The call had an upward inflection that lasted for about half a second and repeated every 6-7 seconds for 30-34 pulses up to 260-290 ms. The dominant frequency was 1000 Hz, but there were also calls at the frequencies of 500, 700, 1200, and 1400 Hz. The calls can be differentiated from the Northern Gastric-brooding frog, which has a shorter call with a deeper pitch and fewer repeats (CITES 2013; Tyler and Davies 1983).

If the frog had not disappeared so quickly, the medical community was interested in studying how the frog was able to stop making acid in its stomach to brood its young. These studies could have led to new treatments for stomach ulcers or faster healing treatments for people who underwent stomach surgery (Yong 2013).

The diet of R. silus consists mainly of small live insects. Once the prey is captured, the frog manipulates it further into the mouth with its forelimbs. Soft-bodied insects are eaten at the water surface, while stronger prey are taken underwater for consumption. Rheobatrachus silus has been observed catching insects on land as well as in water (Tyler, 1983).

Animal Foods: insects

Primary Diet: carnivore (Insectivore )

The two major predators of R. silus, white-faced herons and eels, inhabit the same streams as the frogs. The leaves from eucalyptus trees and stones along the stream banks aid in hiding this species from predators. When grasped, as an escape mechanism, they excrete a coat of mucus that enables them to slip away.

Known Predators:

• white-faced herons (Egretta novaehollandiae)
• eels (Anguillidae)

The length of the oval-shaped R. silus ranges in females from 45 to 54 mm, and 33 to 41 mm in males. Extremely large eyes dorsally protrude from its small, flattened head (Tyler, 1983). The skin color on its back ranges from dull gray to slate, with obscure dark and light patches. When the background is pale, a broad brown and posteriorly curved, superocular bar is detectable (Barker, 1995). Its belly is marked with large creamy patches on a white surface. The feet of this frog are extensively webbed to suit its aquatic lifestyle.

Range length: 33 to 54 mm.

Other Physical Features: ectothermic ; heterothermic ; bilateral symmetry

Sexual Dimorphism: female larger

In captivity, individual R. silus have lived up to 3 years.

Range lifespan
Status: captivity: 3 (high) years.

This frog is mostly aquatic and is found in rocky creek beds, adjacent pools, and rock pools in the Australian rainforest. It also lives along the rocky streams of the moist eucalyptus forest.

Habitat Regions: tropical ; freshwater

Terrestrial Biomes: forest ; rainforest

Aquatic Biomes: lakes and ponds; rivers and streams; temporary pools

Wetlands: marsh ; swamp

This species of frog is only found in the Blackall and Conondale Ranges in Southeastern Queensland, Australia (Barker, 1995).

Biogeographic Regions: australian (Native )

The ability to shut down the secretion of powerful digestive acids could have an important bearing in the medical treatment of humans who suffer from gastric ulcers.

Gastric brooding frog tadpoles develop in their mother's stomach for 6 to 7 weeks. The tadpoles do not feed during this time, as they lack tooth rows. The young develop at different rates and are birthed when they are ready; expelling all of the juvenile frogs may take several days.

Development - Life Cycle: metamorphosis

The gastric brooding frog has limited distributions, which has been detrimental to its existence. It is listed as endangered in the Appendix of the Convention on International Trade in Endangered Species of Wild Fauna and Flora. In 1973, when this species was discovered, they were extremely abundant, and believed common. Astonishingly, less than a decade after their discovery, they seemingly disappeared without a trace. There are several speculated causes for the population crash: drought, over-collection by herpetologists, habitat pollution by the logging industry and by the damming of the creeks for the gold-panning industry (Tyler, 1985). This species' permeable skin makes them especially susceptible to the pollution in their aquatic environment.

This species is currently listed as Extinct by the International Union for the Conservation of Nature. No individuals have been observed in the wild since 1981, despite extensive searches.

US Federal List: no special status

CITES: appendix ii

IUCN Red List of Threatened Species: extinct

The advertisement call of the southern gastric brooding frog is a pulse with a slight upward inflection lasting for 0.5 seconds, repeated every 6 seconds.

Communication Channels: visual ; tactile ; acoustic ; chemical

Other Communication Modes: choruses

Perception Channels: visual ; tactile ; acoustic ; chemical

Gastric brooding frogs cannot be tamed and always struggle when handled.

The reproductive habits of the gastric brooding frog set it apart from other species. The breeding age for this frog is about two years. The process of egg deposition and amplexus has never been observed; it is only known that the eggs are ingested through the mouth (Barker, 1995). The female swallows between 18 and 25 fertilized cream-colored eggs, which develop in her stomach. During this 6 to 7 week period, the colorless tadpoles lack tooth rows and do not feed. The female also stops feeding entirely because of the egg jelly and chemicals secreted by the tadpoles which switch off the production of hydrochloric acid in the stomach wall (A.N.C.A., 1996). The entire digestive system shuts down, which prevents the digestion of the young. Birth is accomplished by the female widely opening her mouth and dilating her esophagus. The offspring are propelled from the stomach to the mouth, and then hop away.

The breeding season occurs during the spring and summer months. Though the warm temperatures of these months aren't essential for reproduction, rain and moisture are necessary (Tyler, 1983).

Range age at sexual or reproductive maturity (female): 2 (low) years.

Range age at sexual or reproductive maturity (male): 2 (low) years.

Key Reproductive Features: seasonal breeding ; gonochoric/gonochoristic/dioecious (sexes separate); sexual ; fertilization (External ); oviparous

Each female gastric brooding frog contributes yolk to her eggs, and then after they are fertilized, she swallows them and carries them in her stomach for 6 to 7 weeks. During this time, her digestive system shuts down and she cannot eat. Once the young are fully developed and expelled from her mouth, she has no further contact with them. Male gastric brooding frogs contribute nothing to the next generation except their sperm.

Parental Investment: pre-fertilization (Provisioning); pre-hatching/birth (Protecting: Female)

The common name of this species refers to the extraordinary method of parental care. Mating occurred in the spring and the female then swallowed the eggs (4). Thus the larvae developed in her stomach; safe from digestion as the digestive system shut down completely (5). For the entire six to seven weeks of egg development the female did not eat, and when the young had metamorphosed into tiny frogs, they were expelled into the mouth and then crawled out and hopped away (4). Feeding occurred both on land and in the water; small insects (2) were caught with the tongue, and the forelimbs were then used to manoeuvre the item into the mouth (2). The gastric-brooding frog was a strong swimmer, but it was not very active and often stayed still for hours, drifting or floating in the water (2).

The southern gastric-brooding frog has been listed as Extinct by the Environment Protection and Biodiversity Conservation Act (EPBC) (2), and as Endangered in Queensland (4). Sadly, it seems likely that the secrets of this frog's amazing ability to 'switch off' the secretion of digestive acids have been lost forever.

Only recently discovered, this Australian frog is now believed to be extinct. The body was grey on the back with variable darker and lighter patches, whilst the underparts were white with large creamy markings. There was a dark streak running from the eye to the forelimbs. The small, flattened head featured large, protruding eyes and the toes were fully webbed (2) (4).

This species was aquatic; it inhabited rainforest creeks, pools and streams (2).

Endemic to Australia, the southern gastric-brooding frog was first discovered in 1973, and occurred only in the Conondale and Blackall Ranges of southeastern Queensland at an altitude between 400 and 800 metres (2). No wild specimens have been recorded since 1981, and the last captive individual died in 1983 (4).

Classified as Extinct (EX) by the IUCN Red List 2007 (1), and listed on Appendix II of CITES (3).

The southern gastric-brooding frog was first discovered in 1973, but it had vanished from the wild less than a decade later in 1981 (4). A number of explanations have been proposed to explain this startling decline, including drought, climate change and increased ultra-violet radiation (7). Since the end of the 1970s, a total of 14 frog species endemic to Australia have undergone dramatic and sudden declines, reflecting the global decline in amphibian populations. Recent analysis has indicated that the simultaneous declines of these species may be the result of a fungal infection (6).